Short Clinical Reviews

Brief Introduction to the SGM Communities

The sexual and gender minority (SGM) communities (see Table 1), also termed “LGBTQIA+ community” (lesbian, gay, bisexual, transgender, queer, intersex, asexual, plus — including two spirit) are historically minoritized with unique risks for inequities in gastrointestinal health outcomes.¹ These potential disparities remain largely uninvestigated because of continued systemic discrimination and inadequate collection of sexual orientation and gender identity (SOGI) data,² with the National Institutes of Health Sexual & Gender Minority Research Office (SGMRO) having been instructed to address these failures. There is increased SGM self-identification (7.1% of all people in the United States and 20.8% of generation Z).³ Given the high worldwide prevalence of disorders of gut-brain interaction (DGBIs)and the influence of biopsychosocial determinants of health in DGBI incidence,⁴ it becomes increasingly likely that research in DGBI-related factors in SGM people will be fruitful.

Disorders of Gut-Brain Interaction and the Potential Minority Stress Link in SGM People

DGBIs are gastrointestinal conditions that occur because of brain-gut axis dysregulation. There is evidence that chronic stress and trauma negatively influence brain-gut interaction, which likely results in minority communities who face increased levels of trauma, stress, discrimination, and social injustice being at higher risk of DGBI development.^5-7 Given increased rates of trauma in the SGM community, practicing trauma-informed care is essential to increase patient comfort and decrease the chance of retraumatization in medical settings.⁸ Trauma-informed care focuses on how trauma influences a patient’s life and response to medical care. To practice trauma-informed care, screening for trauma when appropriate, actively creating a supportive environment with active listening and communication, with informing the patient of planned actions prior to doing them, like physical exams, is key.

Trauma-Informed Care: Examples of Verbiage

Asking about Identity

• Begin by introducing yourself with your pronouns to create a safe environment for patient disclosure. Example: “Hello, I am Dr. Kara Jencks, and my pronouns are she/her. I am one of the gastroenterologists here at XYZ Clinic. How would you prefer to be addressed?”
• You can also wear a pronoun lapel pin or a pronoun button on your ID badge to indicate you are someone who your patient can be themselves around.
• The easiest way to obtain sexual orientation and gender identity is through intake forms. Below are examples of how to ask these questions on intake forms. It is important to offer the option to select more than one option when applicable and to opt out of answering if the patient is not comfortable answering these questions.

Sample Questions for Intake Forms

1. What is your sex assigned at birth? (Select one)

• Female
• Male
• Intersex
• Do not know
• Prefer not to disclose

2. What is your gender identity? (Select all that apply)

• Nonbinary
• Gender queer
• Woman
• Man
• Transwoman
• Transman
• Gender fluid
• Two-spirit
• Agender
• Intersex
• Other: type in response
• Prefer not to disclose

3. What are your pronouns? (Select all that apply)

• They/them/theirs
• She/her/hers
• He/him/his
• Zie/zir/zirs
• Other: type in response
• Prefer not to disclose

4. What is your sexual orientation? (Select all that apply)

• Bisexual
• Pansexual
• Queer
• Lesbian
• Gay
• Asexual
• Demisexual
• Heterosexual or straight
• Other: type in response
• Prefer not to disclose

Screening for Trauma

While there are questionnaires that exist to ask about trauma history, if time allows, it can be helpful to screen verbally with the patient. See reference number 8, for additional prompts and actions to practice trauma-informed care.

• Example: “Many patients with gastrointestinal symptoms and disorders have experienced trauma in the past. We do our best to ensure we are keeping you as comfortable as possible while caring for you. Are you comfortable sharing this information? [if yes->] Do you have a history of trauma, including physical, emotional, or sexual abuse? ... Have these experiences impacted the way in which you navigate your healthcare? ... Is there anything we can do to make you more comfortable today?”

General Physical Examination

Provide details for what you are going to do before you do it. Ask for permission for the examination. Here are two examples:

• “I would like to perform a physical exam to help better understand your symptoms. Is that okay with you?”
• “I would like to examine your abdomen with my stethoscope and my hands. Here is a sheet that we can use to help with your privacy. Please let me know if and when you feel any tenderness or pain.”

Rectal Physical Examination

Let the patient know why it would be helpful to perform a rectal exam, what the rectal exam will entail, and the benefits and risks to doing a rectal exam. An example follows:

• “Based on the symptoms you are describing, I think it would be helpful to perform a rectal exam to make sure you don’t have any fissures or hemorrhoids on the outside around the anus, any blockages or major issues inside the rectum, and to assess the strength and ability of your nerves and muscles or the pelvic floor to coordinate bowel movements. There are no risks aside from discomfort. If it is painful, and you would like me to stop, you tell me to stop, and I will stop right away. What questions do you have? Are we okay to proceed with the rectal exam?”
• “Please pull down your undergarments and your pants to either midthigh, your ankles, or all the way off, whatever your preference is, lie down on the left side on the exam table, and cover yourself with this sheet. In the meantime, I will be getting a chaperone to keep us safe and serve as a patient advocate during the procedure.”
• Upon returning to the exam room: “Here is Sara, who will be chaperoning today. Let myself or Sara know if you are uncomfortable or having pain during this exam. I will be lifting up the sheet to get a good look around the anus. [lifts up sheet] You will feel my hand helping to spread apart the buttocks. I am looking around the anus, and I do not see any fissures, hemorrhoids, or anything else concerning. Please squeeze in like you are trying to hold in gas. Please bear down like you are trying to have a bowel movement or let out gas. Okay, now you may feel some cold gel around the anus, and you will feel my finger go inside. Take a deep breath in. Do you feel any pain as I palpate? Please squeeze in like you are trying to hold in gas. Please bear down like you are trying to have a bowel movement or let out gas. I will be stopping the exam now.”
• You would then wash your hands and allow the patient to get dressed, and then disclose the exam findings and the rest of your visit.

Ilan H. Meyer coined the minority stress model when discussing mental health disorders in SGM patients in the early 2000s.⁹ With it being well known that DGBIs can overlap with (but are not necessarily caused by) mental health disorders, this model can easily apply to unify multiple individual and societal factors that can combine to result in disorders of brain-gut interaction (see Figure 1) in SGM communities. Let us keep this framework in mind when evaluating the following cases. 

 

Case Presentations

Case 1

A 56-year-old man (pronouns: he/him) assigned male sex at birth, who identifies as gay, presents to your gastroenterology clinic for treatment-refractory constipation-predominant irritable bowel syndrome. It has impacted his sexual function. Outside hospital records report a normal colonoscopy 1 year ago and an unremarkable abdominal computerized tomography 4 months ago, aside from increased stool burden in the entire colon. He has tried to use enemas prior to sex, though these do not always help. Fiber-rich diet and fermentable food avoidance has not been successful. He is currently taking two capfuls of polyethylene glycol 3350 twice per day, as well as senna at night and continues to have a bowel movement every 2-3 days that is Bristol stool form scale type 1-2 unless he uses enemas. How do you counsel this patient about his IBS-C and rectal discomfort?

After assessing for sexual violence or other potential trauma-related factors, your digital rectal examination suggests that an anorectal defecatory disorder is less likely with normal relaxation and perineal movement. You recommend linaclotide. He notices improvement within 1 week, with improved comfort during anoreceptive sex. 

 

Case 2

A 30-year-old woman (pronouns: she/her) assigned male sex at birth who has sex with men underwent vaginoplasty 2 years ago and is referred to the gastroenterology clinic for fecal incontinence and diarrhea. On review of her anatomic inventory, her vaginoplasty was a penile inversion vaginoplasty (no intestinal tissue was used for creation), and her prostate was left intact. The vaginal vault was created in between the urethra and rectum, similar to the pelvic floor anatomy of a woman assigned female sex at birth. Blood, imaging, and endoscopic workup has been negative. She is also not taking any medications associated with diarrhea, only taking estrogen and spironolactone. The diarrhea is not daily, but when present, about once per week, can be up to 10 episodes per day, and she has a sense of incomplete evacuation regularly. She notes having a rectal exam in the past but is not sure if her pelvic floor muscles have ever been assessed. How do you manage this patient?

To complete her evaluation in the office, you perform a trauma-informed rectal exam which reveals a decreased resting anal sphincter tone and paradoxical defecatory maneuvers without tenderness to the puborectalis muscle. Augmentation of the squeeze is also weak. Given her pelvic floor related surgical history, her symptoms, and her rectal exam, you recommend anorectal manometry which is abnormal and send her for anorectal biofeedback pelvic floor physical therapy, which improves her symptoms significantly. 

Case 3

A 36-year-old woman (pronouns: she/her) assigned female sex at birth, who identifies as a lesbian, has a history of posttraumatic stress disorder and chronic nausea and vomiting that has begun to affect her quality of life. She notes the nausea and vomiting used to be managed well with evening cannabis gummies, though in the past 3 months, the nausea and vomiting has worsened, and she has lost 20 pounds as a result. As symptom predated cannabis usage, cannabis hyperemesis syndrome (CHS) was less likely (an important point as she has been stigmatized during prior encounters for her cannabis usage). Her primary care physician recommended a gastroscopy which was normal, aside from some residual solid food material in the stomach. Her bowel movements are normal, and she doesn’t have other gastrointestinal symptoms. She and her wife are considering having a third child, so she is worried about medications that may affect pregnancy or breast-feeding. How do you manage her nausea and vomiting?

After validating her concerns and performing a trauma-informed physical exam and encounter, you recommend a 4-hour gastric emptying test with a standard radiolabeled egg meal. Her gastric emptying does reveal significantly delayed gastric emptying at 2 and 4 hours. You discuss the risks and benefits of lifestyle modification (smaller frequent meals), initiating medications (erythromycin and metoclopramide) or cessation of cannabis (despite low likelihood of CHS). Desiring to avoid starting medications around initiation of pregnancy, she opts for the dietary approach and cessation of cannabis. You see her at a follow-up visit in 6 months, and her nausea is now only once a month, and she is excited to begin planning for a pregnancy using assisted reproductive technology. 

 

Case 4

A 20-year-old nonbinary intersex individual (pronouns: he/they) (incorrectly assigned female at birth — is intersex with congenital adrenal hyperplasia) presents to the gastroenterology clinic with 8 years of heartburn, acid reflux, postprandial bloating, alternating diarrhea and constipation, nausea, and vomiting, complicated by avoidant restrictive food intake disorder. They have a history of bipolar II disorder with prior suicidal ideation. He has not yet had diagnostic workup as he previously had a bad encounter with a gastroenterologist where the gastroenterologist blamed his symptoms on his gender-affirming therapy, misgendered the patient, and told the patient their symptoms were “all in her [sic] head.”

You recognize that affirming their gender and using proper pronouns is the best first way to start rapport and help break the cycle of medicalized trauma. You then recommend a holistic work up with interdisciplinary management because of the complexity of his symptoms. For testing, you recommend a colonoscopy, upper endoscopy, a gastric emptying test with a 48-hour transit scintigraphy test, anorectal manometry, a dietitian referral, and a gastrointestinal psychology referral. Their anorectal manometry is consistent with an evacuation disorder. The rest of the work up is unremarkable. You diagnose them with anorectal pelvic floor dysfunction and functional dyspepsia, recommending biofeedback pelvic floor physical therapy, a proton-pump inhibitor, and neuromodulation in coordination with psychiatry and psychology to start with a plan for follow-up. The patient appreciates you for helping them and listening to their symptoms. 

 

Discussion

When approaching DGBIs in the SGM community, it is vital to validate their concerns and be inclusive with diagnostic and treatment modalities. The diagnostic tools and treatments for DGBI are not different for patients in the SGM community. Like with other patients, trauma-informed care should be utilized, particularly given higher rates of trauma and discrimination in this community. Importantly, their DGBI is not a result of their sexual orientation or gender identity, and hormone therapy is not the cause of their DGBI. Recommending cessation of gender-affirming care or recommending lifestyle measures against their identity is generally not appropriate or necessary. With increased scrutiny being a reality of SGM people’s existence in recent years, cultural humility is needed to establish the rapport necessary to treat DGBIs among members of the SGM communities.

Dr. Jencks (@karajencks) is based in the division of gastroenterology and hepatology, Mayo Clinic, Rochester, Minnesota. Dr. Vélez (@Chris_Velez_MD) is based in the division of gastroenterology, Massachusetts General Hospital and Harvard Medical School, both in Boston. Both authors do not have any conflicts of interest for this article.

References

1. Duong N et al. 2023 Apr. doi: 10.1016/S2468-1253(23)00005-5.

2. Vélez C et al. Am J Gastroenterol. 2022 Jun. doi: 10.14309/ajg.0000000000001804.

3. Jones JM. Gallup. LGBTQ+ identification in U.S. now at 7.6%. 2024 Mar 13. https://news.gallup.com/poll/611864/lgbtq-identification.aspx

4. Sperber AD et al. Gastroenterology. 2021 Jan. doi: 10.1053/j.gastro.2020.04.014.

5. Wiley JW et al. Neurogastroenterol Motil. 2016 Jan. doi: 10.1111/nmo.12706.

6. Labanski A et al. Psychoneuroendocrinology. 2020 Jan. doi: 10.1016/j.psyneuen.2019.104501.

7. Khlevner J et al. Gastroenterol Clin North Am. 2018 Dec. doi: 10.1016/j.gtc.2018.07.002.

8. Jagielski CH and Harer KN. Gastroenterol Clin North Am. 2022 Dec. doi: 10.1016/j.gtc.2022.07.012.

9. Meyer IH. Psychol Bull. 2003 Sep. doi: 10.1037/0033-2909.129.5.674.

10. Mahurkar-Joshi S and Chang L. Front Psychiatry. 2020 Aug. doi: 10.3389/fpsyt.2020.00805.

Brief Introduction to the SGM Communities

The sexual and gender minority (SGM) communities (see Table 1), also termed “LGBTQIA+ community” (lesbian, gay, bisexual, transgender, queer, intersex, asexual, plus — including two spirit) are historically minoritized with unique risks for inequities in gastrointestinal health outcomes.¹ These potential disparities remain largely uninvestigated because of continued systemic discrimination and inadequate collection of sexual orientation and gender identity (SOGI) data,² with the National Institutes of Health Sexual & Gender Minority Research Office (SGMRO) having been instructed to address these failures. There is increased SGM self-identification (7.1% of all people in the United States and 20.8% of generation Z).³ Given the high worldwide prevalence of disorders of gut-brain interaction (DGBIs)and the influence of biopsychosocial determinants of health in DGBI incidence,⁴ it becomes increasingly likely that research in DGBI-related factors in SGM people will be fruitful.

Disorders of Gut-Brain Interaction and the Potential Minority Stress Link in SGM People

DGBIs are gastrointestinal conditions that occur because of brain-gut axis dysregulation. There is evidence that chronic stress and trauma negatively influence brain-gut interaction, which likely results in minority communities who face increased levels of trauma, stress, discrimination, and social injustice being at higher risk of DGBI development.^5-7 Given increased rates of trauma in the SGM community, practicing trauma-informed care is essential to increase patient comfort and decrease the chance of retraumatization in medical settings.⁸ Trauma-informed care focuses on how trauma influences a patient’s life and response to medical care. To practice trauma-informed care, screening for trauma when appropriate, actively creating a supportive environment with active listening and communication, with informing the patient of planned actions prior to doing them, like physical exams, is key.

Trauma-Informed Care: Examples of Verbiage

Asking about Identity

• Begin by introducing yourself with your pronouns to create a safe environment for patient disclosure. Example: “Hello, I am Dr. Kara Jencks, and my pronouns are she/her. I am one of the gastroenterologists here at XYZ Clinic. How would you prefer to be addressed?”
• You can also wear a pronoun lapel pin or a pronoun button on your ID badge to indicate you are someone who your patient can be themselves around.
• The easiest way to obtain sexual orientation and gender identity is through intake forms. Below are examples of how to ask these questions on intake forms. It is important to offer the option to select more than one option when applicable and to opt out of answering if the patient is not comfortable answering these questions.

Sample Questions for Intake Forms

1. What is your sex assigned at birth? (Select one)

• Female
• Male
• Intersex
• Do not know
• Prefer not to disclose

2. What is your gender identity? (Select all that apply)

• Nonbinary
• Gender queer
• Woman
• Man
• Transwoman
• Transman
• Gender fluid
• Two-spirit
• Agender
• Intersex
• Other: type in response
• Prefer not to disclose

3. What are your pronouns? (Select all that apply)

• They/them/theirs
• She/her/hers
• He/him/his
• Zie/zir/zirs
• Other: type in response
• Prefer not to disclose

4. What is your sexual orientation? (Select all that apply)

• Bisexual
• Pansexual
• Queer
• Lesbian
• Gay
• Asexual
• Demisexual
• Heterosexual or straight
• Other: type in response
• Prefer not to disclose

Screening for Trauma

While there are questionnaires that exist to ask about trauma history, if time allows, it can be helpful to screen verbally with the patient. See reference number 8, for additional prompts and actions to practice trauma-informed care.

• Example: “Many patients with gastrointestinal symptoms and disorders have experienced trauma in the past. We do our best to ensure we are keeping you as comfortable as possible while caring for you. Are you comfortable sharing this information? [if yes->] Do you have a history of trauma, including physical, emotional, or sexual abuse? ... Have these experiences impacted the way in which you navigate your healthcare? ... Is there anything we can do to make you more comfortable today?”

General Physical Examination

Provide details for what you are going to do before you do it. Ask for permission for the examination. Here are two examples:

• “I would like to perform a physical exam to help better understand your symptoms. Is that okay with you?”
• “I would like to examine your abdomen with my stethoscope and my hands. Here is a sheet that we can use to help with your privacy. Please let me know if and when you feel any tenderness or pain.”

Rectal Physical Examination

Let the patient know why it would be helpful to perform a rectal exam, what the rectal exam will entail, and the benefits and risks to doing a rectal exam. An example follows:

• “Based on the symptoms you are describing, I think it would be helpful to perform a rectal exam to make sure you don’t have any fissures or hemorrhoids on the outside around the anus, any blockages or major issues inside the rectum, and to assess the strength and ability of your nerves and muscles or the pelvic floor to coordinate bowel movements. There are no risks aside from discomfort. If it is painful, and you would like me to stop, you tell me to stop, and I will stop right away. What questions do you have? Are we okay to proceed with the rectal exam?”
• “Please pull down your undergarments and your pants to either midthigh, your ankles, or all the way off, whatever your preference is, lie down on the left side on the exam table, and cover yourself with this sheet. In the meantime, I will be getting a chaperone to keep us safe and serve as a patient advocate during the procedure.”
• Upon returning to the exam room: “Here is Sara, who will be chaperoning today. Let myself or Sara know if you are uncomfortable or having pain during this exam. I will be lifting up the sheet to get a good look around the anus. [lifts up sheet] You will feel my hand helping to spread apart the buttocks. I am looking around the anus, and I do not see any fissures, hemorrhoids, or anything else concerning. Please squeeze in like you are trying to hold in gas. Please bear down like you are trying to have a bowel movement or let out gas. Okay, now you may feel some cold gel around the anus, and you will feel my finger go inside. Take a deep breath in. Do you feel any pain as I palpate? Please squeeze in like you are trying to hold in gas. Please bear down like you are trying to have a bowel movement or let out gas. I will be stopping the exam now.”
• You would then wash your hands and allow the patient to get dressed, and then disclose the exam findings and the rest of your visit.

Ilan H. Meyer coined the minority stress model when discussing mental health disorders in SGM patients in the early 2000s.⁹ With it being well known that DGBIs can overlap with (but are not necessarily caused by) mental health disorders, this model can easily apply to unify multiple individual and societal factors that can combine to result in disorders of brain-gut interaction (see Figure 1) in SGM communities. Let us keep this framework in mind when evaluating the following cases. 

 

Case Presentations

Case 1

A 56-year-old man (pronouns: he/him) assigned male sex at birth, who identifies as gay, presents to your gastroenterology clinic for treatment-refractory constipation-predominant irritable bowel syndrome. It has impacted his sexual function. Outside hospital records report a normal colonoscopy 1 year ago and an unremarkable abdominal computerized tomography 4 months ago, aside from increased stool burden in the entire colon. He has tried to use enemas prior to sex, though these do not always help. Fiber-rich diet and fermentable food avoidance has not been successful. He is currently taking two capfuls of polyethylene glycol 3350 twice per day, as well as senna at night and continues to have a bowel movement every 2-3 days that is Bristol stool form scale type 1-2 unless he uses enemas. How do you counsel this patient about his IBS-C and rectal discomfort?

After assessing for sexual violence or other potential trauma-related factors, your digital rectal examination suggests that an anorectal defecatory disorder is less likely with normal relaxation and perineal movement. You recommend linaclotide. He notices improvement within 1 week, with improved comfort during anoreceptive sex. 

 

Case 2

A 30-year-old woman (pronouns: she/her) assigned male sex at birth who has sex with men underwent vaginoplasty 2 years ago and is referred to the gastroenterology clinic for fecal incontinence and diarrhea. On review of her anatomic inventory, her vaginoplasty was a penile inversion vaginoplasty (no intestinal tissue was used for creation), and her prostate was left intact. The vaginal vault was created in between the urethra and rectum, similar to the pelvic floor anatomy of a woman assigned female sex at birth. Blood, imaging, and endoscopic workup has been negative. She is also not taking any medications associated with diarrhea, only taking estrogen and spironolactone. The diarrhea is not daily, but when present, about once per week, can be up to 10 episodes per day, and she has a sense of incomplete evacuation regularly. She notes having a rectal exam in the past but is not sure if her pelvic floor muscles have ever been assessed. How do you manage this patient?

To complete her evaluation in the office, you perform a trauma-informed rectal exam which reveals a decreased resting anal sphincter tone and paradoxical defecatory maneuvers without tenderness to the puborectalis muscle. Augmentation of the squeeze is also weak. Given her pelvic floor related surgical history, her symptoms, and her rectal exam, you recommend anorectal manometry which is abnormal and send her for anorectal biofeedback pelvic floor physical therapy, which improves her symptoms significantly. 

Case 3

A 36-year-old woman (pronouns: she/her) assigned female sex at birth, who identifies as a lesbian, has a history of posttraumatic stress disorder and chronic nausea and vomiting that has begun to affect her quality of life. She notes the nausea and vomiting used to be managed well with evening cannabis gummies, though in the past 3 months, the nausea and vomiting has worsened, and she has lost 20 pounds as a result. As symptom predated cannabis usage, cannabis hyperemesis syndrome (CHS) was less likely (an important point as she has been stigmatized during prior encounters for her cannabis usage). Her primary care physician recommended a gastroscopy which was normal, aside from some residual solid food material in the stomach. Her bowel movements are normal, and she doesn’t have other gastrointestinal symptoms. She and her wife are considering having a third child, so she is worried about medications that may affect pregnancy or breast-feeding. How do you manage her nausea and vomiting?

After validating her concerns and performing a trauma-informed physical exam and encounter, you recommend a 4-hour gastric emptying test with a standard radiolabeled egg meal. Her gastric emptying does reveal significantly delayed gastric emptying at 2 and 4 hours. You discuss the risks and benefits of lifestyle modification (smaller frequent meals), initiating medications (erythromycin and metoclopramide) or cessation of cannabis (despite low likelihood of CHS). Desiring to avoid starting medications around initiation of pregnancy, she opts for the dietary approach and cessation of cannabis. You see her at a follow-up visit in 6 months, and her nausea is now only once a month, and she is excited to begin planning for a pregnancy using assisted reproductive technology. 

 

Case 4

A 20-year-old nonbinary intersex individual (pronouns: he/they) (incorrectly assigned female at birth — is intersex with congenital adrenal hyperplasia) presents to the gastroenterology clinic with 8 years of heartburn, acid reflux, postprandial bloating, alternating diarrhea and constipation, nausea, and vomiting, complicated by avoidant restrictive food intake disorder. They have a history of bipolar II disorder with prior suicidal ideation. He has not yet had diagnostic workup as he previously had a bad encounter with a gastroenterologist where the gastroenterologist blamed his symptoms on his gender-affirming therapy, misgendered the patient, and told the patient their symptoms were “all in her [sic] head.”

You recognize that affirming their gender and using proper pronouns is the best first way to start rapport and help break the cycle of medicalized trauma. You then recommend a holistic work up with interdisciplinary management because of the complexity of his symptoms. For testing, you recommend a colonoscopy, upper endoscopy, a gastric emptying test with a 48-hour transit scintigraphy test, anorectal manometry, a dietitian referral, and a gastrointestinal psychology referral. Their anorectal manometry is consistent with an evacuation disorder. The rest of the work up is unremarkable. You diagnose them with anorectal pelvic floor dysfunction and functional dyspepsia, recommending biofeedback pelvic floor physical therapy, a proton-pump inhibitor, and neuromodulation in coordination with psychiatry and psychology to start with a plan for follow-up. The patient appreciates you for helping them and listening to their symptoms. 

 

Discussion

When approaching DGBIs in the SGM community, it is vital to validate their concerns and be inclusive with diagnostic and treatment modalities. The diagnostic tools and treatments for DGBI are not different for patients in the SGM community. Like with other patients, trauma-informed care should be utilized, particularly given higher rates of trauma and discrimination in this community. Importantly, their DGBI is not a result of their sexual orientation or gender identity, and hormone therapy is not the cause of their DGBI. Recommending cessation of gender-affirming care or recommending lifestyle measures against their identity is generally not appropriate or necessary. With increased scrutiny being a reality of SGM people’s existence in recent years, cultural humility is needed to establish the rapport necessary to treat DGBIs among members of the SGM communities.

Dr. Jencks (@karajencks) is based in the division of gastroenterology and hepatology, Mayo Clinic, Rochester, Minnesota. Dr. Vélez (@Chris_Velez_MD) is based in the division of gastroenterology, Massachusetts General Hospital and Harvard Medical School, both in Boston. Both authors do not have any conflicts of interest for this article.

References

1. Duong N et al. 2023 Apr. doi: 10.1016/S2468-1253(23)00005-5.

2. Vélez C et al. Am J Gastroenterol. 2022 Jun. doi: 10.14309/ajg.0000000000001804.

3. Jones JM. Gallup. LGBTQ+ identification in U.S. now at 7.6%. 2024 Mar 13. https://news.gallup.com/poll/611864/lgbtq-identification.aspx

4. Sperber AD et al. Gastroenterology. 2021 Jan. doi: 10.1053/j.gastro.2020.04.014.

5. Wiley JW et al. Neurogastroenterol Motil. 2016 Jan. doi: 10.1111/nmo.12706.

6. Labanski A et al. Psychoneuroendocrinology. 2020 Jan. doi: 10.1016/j.psyneuen.2019.104501.

7. Khlevner J et al. Gastroenterol Clin North Am. 2018 Dec. doi: 10.1016/j.gtc.2018.07.002.

8. Jagielski CH and Harer KN. Gastroenterol Clin North Am. 2022 Dec. doi: 10.1016/j.gtc.2022.07.012.

9. Meyer IH. Psychol Bull. 2003 Sep. doi: 10.1037/0033-2909.129.5.674.

10. Mahurkar-Joshi S and Chang L. Front Psychiatry. 2020 Aug. doi: 10.3389/fpsyt.2020.00805.

Brief Introduction to the SGM Communities

The sexual and gender minority (SGM) communities (see Table 1), also termed “LGBTQIA+ community” (lesbian, gay, bisexual, transgender, queer, intersex, asexual, plus — including two spirit) are historically minoritized with unique risks for inequities in gastrointestinal health outcomes.¹ These potential disparities remain largely uninvestigated because of continued systemic discrimination and inadequate collection of sexual orientation and gender identity (SOGI) data,² with the National Institutes of Health Sexual & Gender Minority Research Office (SGMRO) having been instructed to address these failures. There is increased SGM self-identification (7.1% of all people in the United States and 20.8% of generation Z).³ Given the high worldwide prevalence of disorders of gut-brain interaction (DGBIs)and the influence of biopsychosocial determinants of health in DGBI incidence,⁴ it becomes increasingly likely that research in DGBI-related factors in SGM people will be fruitful.

Disorders of Gut-Brain Interaction and the Potential Minority Stress Link in SGM People

DGBIs are gastrointestinal conditions that occur because of brain-gut axis dysregulation. There is evidence that chronic stress and trauma negatively influence brain-gut interaction, which likely results in minority communities who face increased levels of trauma, stress, discrimination, and social injustice being at higher risk of DGBI development.^5-7 Given increased rates of trauma in the SGM community, practicing trauma-informed care is essential to increase patient comfort and decrease the chance of retraumatization in medical settings.⁸ Trauma-informed care focuses on how trauma influences a patient’s life and response to medical care. To practice trauma-informed care, screening for trauma when appropriate, actively creating a supportive environment with active listening and communication, with informing the patient of planned actions prior to doing them, like physical exams, is key.

Trauma-Informed Care: Examples of Verbiage

Asking about Identity

• Begin by introducing yourself with your pronouns to create a safe environment for patient disclosure. Example: “Hello, I am Dr. Kara Jencks, and my pronouns are she/her. I am one of the gastroenterologists here at XYZ Clinic. How would you prefer to be addressed?”
• You can also wear a pronoun lapel pin or a pronoun button on your ID badge to indicate you are someone who your patient can be themselves around.
• The easiest way to obtain sexual orientation and gender identity is through intake forms. Below are examples of how to ask these questions on intake forms. It is important to offer the option to select more than one option when applicable and to opt out of answering if the patient is not comfortable answering these questions.

Sample Questions for Intake Forms

1. What is your sex assigned at birth? (Select one)

• Female
• Male
• Intersex
• Do not know
• Prefer not to disclose

2. What is your gender identity? (Select all that apply)

• Nonbinary
• Gender queer
• Woman
• Man
• Transwoman
• Transman
• Gender fluid
• Two-spirit
• Agender
• Intersex
• Other: type in response
• Prefer not to disclose

3. What are your pronouns? (Select all that apply)

• They/them/theirs
• She/her/hers
• He/him/his
• Zie/zir/zirs
• Other: type in response
• Prefer not to disclose

4. What is your sexual orientation? (Select all that apply)

• Bisexual
• Pansexual
• Queer
• Lesbian
• Gay
• Asexual
• Demisexual
• Heterosexual or straight
• Other: type in response
• Prefer not to disclose

Screening for Trauma

While there are questionnaires that exist to ask about trauma history, if time allows, it can be helpful to screen verbally with the patient. See reference number 8, for additional prompts and actions to practice trauma-informed care.

• Example: “Many patients with gastrointestinal symptoms and disorders have experienced trauma in the past. We do our best to ensure we are keeping you as comfortable as possible while caring for you. Are you comfortable sharing this information? [if yes->] Do you have a history of trauma, including physical, emotional, or sexual abuse? ... Have these experiences impacted the way in which you navigate your healthcare? ... Is there anything we can do to make you more comfortable today?”

General Physical Examination

Provide details for what you are going to do before you do it. Ask for permission for the examination. Here are two examples:

• “I would like to perform a physical exam to help better understand your symptoms. Is that okay with you?”
• “I would like to examine your abdomen with my stethoscope and my hands. Here is a sheet that we can use to help with your privacy. Please let me know if and when you feel any tenderness or pain.”

Rectal Physical Examination

Let the patient know why it would be helpful to perform a rectal exam, what the rectal exam will entail, and the benefits and risks to doing a rectal exam. An example follows:

• “Based on the symptoms you are describing, I think it would be helpful to perform a rectal exam to make sure you don’t have any fissures or hemorrhoids on the outside around the anus, any blockages or major issues inside the rectum, and to assess the strength and ability of your nerves and muscles or the pelvic floor to coordinate bowel movements. There are no risks aside from discomfort. If it is painful, and you would like me to stop, you tell me to stop, and I will stop right away. What questions do you have? Are we okay to proceed with the rectal exam?”
• “Please pull down your undergarments and your pants to either midthigh, your ankles, or all the way off, whatever your preference is, lie down on the left side on the exam table, and cover yourself with this sheet. In the meantime, I will be getting a chaperone to keep us safe and serve as a patient advocate during the procedure.”
• Upon returning to the exam room: “Here is Sara, who will be chaperoning today. Let myself or Sara know if you are uncomfortable or having pain during this exam. I will be lifting up the sheet to get a good look around the anus. [lifts up sheet] You will feel my hand helping to spread apart the buttocks. I am looking around the anus, and I do not see any fissures, hemorrhoids, or anything else concerning. Please squeeze in like you are trying to hold in gas. Please bear down like you are trying to have a bowel movement or let out gas. Okay, now you may feel some cold gel around the anus, and you will feel my finger go inside. Take a deep breath in. Do you feel any pain as I palpate? Please squeeze in like you are trying to hold in gas. Please bear down like you are trying to have a bowel movement or let out gas. I will be stopping the exam now.”
• You would then wash your hands and allow the patient to get dressed, and then disclose the exam findings and the rest of your visit.

Ilan H. Meyer coined the minority stress model when discussing mental health disorders in SGM patients in the early 2000s.⁹ With it being well known that DGBIs can overlap with (but are not necessarily caused by) mental health disorders, this model can easily apply to unify multiple individual and societal factors that can combine to result in disorders of brain-gut interaction (see Figure 1) in SGM communities. Let us keep this framework in mind when evaluating the following cases. 

 

Case Presentations

Case 1

A 56-year-old man (pronouns: he/him) assigned male sex at birth, who identifies as gay, presents to your gastroenterology clinic for treatment-refractory constipation-predominant irritable bowel syndrome. It has impacted his sexual function. Outside hospital records report a normal colonoscopy 1 year ago and an unremarkable abdominal computerized tomography 4 months ago, aside from increased stool burden in the entire colon. He has tried to use enemas prior to sex, though these do not always help. Fiber-rich diet and fermentable food avoidance has not been successful. He is currently taking two capfuls of polyethylene glycol 3350 twice per day, as well as senna at night and continues to have a bowel movement every 2-3 days that is Bristol stool form scale type 1-2 unless he uses enemas. How do you counsel this patient about his IBS-C and rectal discomfort?

After assessing for sexual violence or other potential trauma-related factors, your digital rectal examination suggests that an anorectal defecatory disorder is less likely with normal relaxation and perineal movement. You recommend linaclotide. He notices improvement within 1 week, with improved comfort during anoreceptive sex. 

 

Case 2

A 30-year-old woman (pronouns: she/her) assigned male sex at birth who has sex with men underwent vaginoplasty 2 years ago and is referred to the gastroenterology clinic for fecal incontinence and diarrhea. On review of her anatomic inventory, her vaginoplasty was a penile inversion vaginoplasty (no intestinal tissue was used for creation), and her prostate was left intact. The vaginal vault was created in between the urethra and rectum, similar to the pelvic floor anatomy of a woman assigned female sex at birth. Blood, imaging, and endoscopic workup has been negative. She is also not taking any medications associated with diarrhea, only taking estrogen and spironolactone. The diarrhea is not daily, but when present, about once per week, can be up to 10 episodes per day, and she has a sense of incomplete evacuation regularly. She notes having a rectal exam in the past but is not sure if her pelvic floor muscles have ever been assessed. How do you manage this patient?

To complete her evaluation in the office, you perform a trauma-informed rectal exam which reveals a decreased resting anal sphincter tone and paradoxical defecatory maneuvers without tenderness to the puborectalis muscle. Augmentation of the squeeze is also weak. Given her pelvic floor related surgical history, her symptoms, and her rectal exam, you recommend anorectal manometry which is abnormal and send her for anorectal biofeedback pelvic floor physical therapy, which improves her symptoms significantly. 

Case 3

A 36-year-old woman (pronouns: she/her) assigned female sex at birth, who identifies as a lesbian, has a history of posttraumatic stress disorder and chronic nausea and vomiting that has begun to affect her quality of life. She notes the nausea and vomiting used to be managed well with evening cannabis gummies, though in the past 3 months, the nausea and vomiting has worsened, and she has lost 20 pounds as a result. As symptom predated cannabis usage, cannabis hyperemesis syndrome (CHS) was less likely (an important point as she has been stigmatized during prior encounters for her cannabis usage). Her primary care physician recommended a gastroscopy which was normal, aside from some residual solid food material in the stomach. Her bowel movements are normal, and she doesn’t have other gastrointestinal symptoms. She and her wife are considering having a third child, so she is worried about medications that may affect pregnancy or breast-feeding. How do you manage her nausea and vomiting?

After validating her concerns and performing a trauma-informed physical exam and encounter, you recommend a 4-hour gastric emptying test with a standard radiolabeled egg meal. Her gastric emptying does reveal significantly delayed gastric emptying at 2 and 4 hours. You discuss the risks and benefits of lifestyle modification (smaller frequent meals), initiating medications (erythromycin and metoclopramide) or cessation of cannabis (despite low likelihood of CHS). Desiring to avoid starting medications around initiation of pregnancy, she opts for the dietary approach and cessation of cannabis. You see her at a follow-up visit in 6 months, and her nausea is now only once a month, and she is excited to begin planning for a pregnancy using assisted reproductive technology. 

 

Case 4

A 20-year-old nonbinary intersex individual (pronouns: he/they) (incorrectly assigned female at birth — is intersex with congenital adrenal hyperplasia) presents to the gastroenterology clinic with 8 years of heartburn, acid reflux, postprandial bloating, alternating diarrhea and constipation, nausea, and vomiting, complicated by avoidant restrictive food intake disorder. They have a history of bipolar II disorder with prior suicidal ideation. He has not yet had diagnostic workup as he previously had a bad encounter with a gastroenterologist where the gastroenterologist blamed his symptoms on his gender-affirming therapy, misgendered the patient, and told the patient their symptoms were “all in her [sic] head.”

You recognize that affirming their gender and using proper pronouns is the best first way to start rapport and help break the cycle of medicalized trauma. You then recommend a holistic work up with interdisciplinary management because of the complexity of his symptoms. For testing, you recommend a colonoscopy, upper endoscopy, a gastric emptying test with a 48-hour transit scintigraphy test, anorectal manometry, a dietitian referral, and a gastrointestinal psychology referral. Their anorectal manometry is consistent with an evacuation disorder. The rest of the work up is unremarkable. You diagnose them with anorectal pelvic floor dysfunction and functional dyspepsia, recommending biofeedback pelvic floor physical therapy, a proton-pump inhibitor, and neuromodulation in coordination with psychiatry and psychology to start with a plan for follow-up. The patient appreciates you for helping them and listening to their symptoms. 

 

Discussion

When approaching DGBIs in the SGM community, it is vital to validate their concerns and be inclusive with diagnostic and treatment modalities. The diagnostic tools and treatments for DGBI are not different for patients in the SGM community. Like with other patients, trauma-informed care should be utilized, particularly given higher rates of trauma and discrimination in this community. Importantly, their DGBI is not a result of their sexual orientation or gender identity, and hormone therapy is not the cause of their DGBI. Recommending cessation of gender-affirming care or recommending lifestyle measures against their identity is generally not appropriate or necessary. With increased scrutiny being a reality of SGM people’s existence in recent years, cultural humility is needed to establish the rapport necessary to treat DGBIs among members of the SGM communities.

Dr. Jencks (@karajencks) is based in the division of gastroenterology and hepatology, Mayo Clinic, Rochester, Minnesota. Dr. Vélez (@Chris_Velez_MD) is based in the division of gastroenterology, Massachusetts General Hospital and Harvard Medical School, both in Boston. Both authors do not have any conflicts of interest for this article.

References

1. Duong N et al. 2023 Apr. doi: 10.1016/S2468-1253(23)00005-5.

2. Vélez C et al. Am J Gastroenterol. 2022 Jun. doi: 10.14309/ajg.0000000000001804.

3. Jones JM. Gallup. LGBTQ+ identification in U.S. now at 7.6%. 2024 Mar 13. https://news.gallup.com/poll/611864/lgbtq-identification.aspx

4. Sperber AD et al. Gastroenterology. 2021 Jan. doi: 10.1053/j.gastro.2020.04.014.

5. Wiley JW et al. Neurogastroenterol Motil. 2016 Jan. doi: 10.1111/nmo.12706.

6. Labanski A et al. Psychoneuroendocrinology. 2020 Jan. doi: 10.1016/j.psyneuen.2019.104501.

7. Khlevner J et al. Gastroenterol Clin North Am. 2018 Dec. doi: 10.1016/j.gtc.2018.07.002.

8. Jagielski CH and Harer KN. Gastroenterol Clin North Am. 2022 Dec. doi: 10.1016/j.gtc.2022.07.012.

9. Meyer IH. Psychol Bull. 2003 Sep. doi: 10.1037/0033-2909.129.5.674.

10. Mahurkar-Joshi S and Chang L. Front Psychiatry. 2020 Aug. doi: 10.3389/fpsyt.2020.00805.

Endoscopists are often faced with unique challenges in the management and resection of various gastrointestinal tract lesions. These challenges could be lesion-related, endoscopist-related, or practice-related (see Table 1). As our knowledge, tools and resources, and training significantly evolved in the modern era, there has been a remarkable rise in advanced endoscopic techniques for advanced tissue resection (ATR). Not only does this organ-sparing approach offer a less invasive alternative to surgery, but it has also proved to have outcomes comparable to those of surgical standard of practice in specific scenarios.

When Do You Refer to an Advanced Endoscopist?

One of the most critical steps in caring for patients with complex lesions is the ability to accurately determine whether a referral to an advanced endoscopist is warranted. The initial assessment of a lesion should always involve a careful assessment that risk stratifies the lesion depending on the location, size, neoplastic potential, and the feasibility of standard endoscopic resection compared to the need for surgical input.

A practical example in the case of colonic polyps is highlighted by the American Gastroenterology Association (AGA) guidelines recommending the referral of patients with polyps’ size ≥ 20 mm, challenging polypectomy location, or recurrent polyp at a prior polypectomy site to an endoscopic referral center.¹ In the case of subepithelial lesions without endoscopic characteristics of benign etiology (i.e., lipomas, pancreatic rests, etc.), the threshold for referral to advanced endoscopists for further diagnostic testing by means of endoscopic ultrasonography or for therapeutic ATR should be lower.

Endoscopic tissue resection follows a spectrum, which often involves deeper layers of the gastrointestinal tract (GIT) as we progress along this spectrum (see Figure 1).

Dr. Madi; Dr. Rengarajan, and Dr. Bazarbashi

ATR, a term encompassing a variety of endoscopic techniques ranging from endoscopic mucosal resection to full thickness resection, has gained traction over the last years given the ability to effectively remove various lesions in a precise time and cost-effective manner while maintaining the integrity of the GIT and avoiding major surgery. The indications for ATR vary depending on the technique, but generally include the presence of large or poorly positioned lesions, particularly in high-risk areas of the GIT such as the esophagus and small intestine, lesions extending beyond the mucosal layer or originating from deeper layers, and when en bloc resection of select lesions is necessary.

Saint Louis University School of Medicine

Endoscopic Mucosal Resection (EMR)

EMR is currently utilized for curative treatment of a wide array of GIT lesions limited to the mucosal layer, whether metaplastic, dysplastic, or even in cases with early mucosal cancer, where the risk of submucosal and lymphatic invasion is minimal.⁴ This makes EMR a versatile and proven therapy, often serving as the first-line treatment for many GIT lesions.

Washington University

EMR has various techniques that could be categorized into suction or non-suction (lift and cut) techniques. In the suction technique, devices like multiband mucosectomy (MBM) are commonly used, especially in nodular Barrett’s dysplasia, forming a pseudopolyp for subsequent resection. The procedure is characterized by its safety, efficacy, and cost-effectiveness, contributing to its widespread adoption in clinical practice. In the lift and cut approach, a submucosal injection is utilized to separate the muscularis propria from the lesion, thereby reducing the risk of perforation. Different solutions, such as normal saline, hypertonic saline, 50% dextrose, or proprietary submucosal injection solutions, are employed for submucosal injection.⁵

The non-suction technique using a snare to resect polyps after injection is more often used in colonic and small intestinal EMR. Resection can be done via thermal energy in the form of cut or coagulation; however, there is rising data on the use of piecemeal cold snare resection for select flat polyps of the colon.⁶ There is also promising data on the role of underwater EMR, a common technique employed for colonic lesions, particularly if the lesion does not lift well with submucosal injection.⁷

Adverse events associated with EMR include bleeding (7%-8%) and perforation (0.9%-2%).^8-9 Adequate submucosal fluid injection is crucial to prevent perforations. However, the main limitation of EMR is the piecemeal nature of resections for lesions larger than 20 mm, leading to compromised histopathologic evaluation for complete excision, especially in cases with superficial submucosal invasion (SMI). This can result in residual or recurrent tissue, reportedly 8% to 20%.¹⁰ Despite this limitation, EMR remains a reliable strategy, and recurrent lesions are generally manageable through repeat sessions. The importance of EMR as a therapeutic modality lies in its role in addressing lesions with favorable characteristics, where the risk of SMI is low.

Washington University

Endoscopic Submucosal Dissection (ESD)

ESD is an evolving technique that can be utilized for submucosal lesions of the GIT, lesions not amenable to EMR due to submucosal fibrosis, when en bloc removal of a lesion is needed for accurate histopathological diagnosis, and when other techniques fail.^11-12

ESD was only recently adopted in the United States, requires specialized training, and usually is a lengthier procedure than EMR.¹³ Compared to EMR, it has higher en bloc resection rates and lower recurrence rates, making it curative for lesions with superficial SMI and favorable histologic features.^4,14 The safety profile of ESD appears favorable, with most of the adverse events managed successfully by endoscopic methods. Major complications include intraoperative and delayed perforation, intraoperative and delayed bleeding, aspiration pneumonia, thromboembolism, and stricture formation in the case of circumferential lesions.¹⁵

Despite being technically challenging, ESD may provide a cost-effective long-term solution by avoiding surgery, reducing the need for additional interventions by minimizing recurrence rates. Given the technical complexity of ESD, particularly the submucosal dissection portion, techniques such as hybrid ESD developed. Hybrid ESD combines snaring with circumferential mucosal incision and partial submucosal dissection. Although it promises shorter procedure times, reduced complication rates like perforation, and similar recurrence rates compared to traditional ESD, studies have shown lower success rates in en bloc resection.^16-17

Both EMR and ESD are considered complementary strategies, and the choice between them should be dictated by lesion characteristics, patient preferences, and local expertise.
 

Submucosal Tunneling Endoscopic Resection (STER)

STER has emerged as a well-established technique for the endoscopic resection of GI subepithelial tumors (SETs) originating from the muscularis propria layer. The standard STER procedure involves a series of steps including submucosal elevation proximal to the SET, mucosotomy, creation of a submucosal tunnel, dissection of the SET within the tunnel, enucleation from the deep muscle layer, and subsequent specimen retrieval followed by mucosal closure.

This technique is typically recommended for SETs smaller than 3.5 cm, particularly those located in the mid or distal esophagus, cardia, or along the greater curvature of the gastric body.¹⁸ However, STER may pose technical challenges for larger SETs or lesions in anatomically difficult locations, where surgical resection is recommended instead.¹⁹ Notably, recent large-scale meta-analyses have showcased the favorable complete resection and en bloc resection rates of STER in treating GI SETs.²⁰

Endoscopic Full Thickness Resection (EFTR)

EFTR has emerged as a valuable technique in the endoscopic management of gastrointestinal lesions, particularly SETs and lesions not amenable to EMR or ESD due to fibrosis. EFTR involves the resection of all layers of the GIT from mucosa to serosa, and therefore is well-suited for SETs arising from the muscularis propria (MP).²⁰

EFTR entails two main concepts: tissue resection and complete defect closure. Conventional EFTR consists of several steps, which include mucosal and submucosal pre-cutting, circumferential incision, and dissection through the MP or serosa. This results in a full thickness defect, for which closure of the wall defect is achieved using standard endoscopic clips or a combination of clips and endoloops or endoscopic suturing.²¹ For lesions less than 2 cm, EFTR can be performed in a single step using a cap-mounted full thickness resection device (FTRD). This results in deployment of over-the-scope clip over the target lesion followed by snaring the lesions above the clip.²¹

Location of the SET generally dictates the specific modality of ATR. For example, esophageal SETs may be more amenable to STER given that the lesion typically runs parallel with the lumen of the tubular esophagus, which allows for easier dissection without the need of full or partial retroflexion. While gastric SETs can be resected with STER, it may be challenging and more effectively addressed with EFTR, particularly when the entire lesion can be grasped into the full-thickness resection device.²² Limited data exists for duodenal EFTR, and colorectal SETs closure is particularly challenging.
 

Conclusion

It is key to emphasize that ATR cannot be safely established in practice without the incorporation of a multidisciplinary team (surgeons, radiologists, etc.), specialized tools, and trained personnel. This requires dedicated endoscopic rooms, careful patient selection, and a comprehensive approach to patient care before, during, and after these procedures.

Moreover, it is important to note that some patients may require post-procedure hospitalization for observation to ensure no early complications are encountered. Optimal surveillance strategies after ATR rely heavily on the potential for residual or recurrent disease, underlying pathology, and the expertise of the advanced endoscopist. As the field continues to evolve, ongoing research and technological advances of devices will further enhance the efficacy and safety of ATR in gastroenterology.

Dr. Madi (@MahMadi90) is based in the Division of Gastroenterology and Hepatology, Saint Louis University School of Medicine, Saint Louis, Missouri. Dr. Rengarajan (@ArvindRenga) and Dr. Bazarbashi (@AhmadBazarbashi) are based in the Division of Gastroenterology, Washington University in St. Louis. The authors have no conflicts of interest to disclose, and no funding was required for this project.
 

References

1. Copland AP, et al. AGA Clinical Practice Update on appropriate and tailored polypectomy: Expert review. Clin Gastroenterol Hepatol. 2024 Mar. doi: 10.1016/j.cgh.2023.10.012.

2. Lee SP, et al. Effect of preceding biopsy on the results of endoscopic submucosal dissection for colorectal laterally spreading tumor. Dig Dis Sci. 2019 Oct. doi: 10.1007/s10620-019-05625-3.

3. Medina-Prado L, et al. When and how to use endoscopic tattooing in the colon: An international Delphi agreement. Clin Gastroenterol Hepatol. 2021 May. doi: 10.1016/j.cgh.2021.01.024.

4. Rashid MU, et al. EMR and ESD: Indications, techniques and results. Surg Oncol. 2022 Aug. doi: 10.1016/j.suronc.2022.101742.

5. Castro R, et al. Solutions for submucosal injection: What to choose and how to do it. World J Gastroenterol. 2019 Feb. doi: 10.3748/wjg.v25.i7.777.

6. Rex DK. Best practices for resection of diminutive and small polyps in the colorectum. Gastrointest Endosc Clin N Am. 2019 Oct. doi: 10.1016/j.giec.2019.06.004.

7. Lv XH, et al. Underwater EMR for nonpedunculated colorectal lesions. Gastrointest Endosc. 2023 Apr. doi: 10.1016/j.gie.2022.10.044.

8. Fujiya M, et al. Efficacy and adverse events of EMR and endoscopic submucosal dissection for the treatment of colon neoplasms: a meta-analysis of studies comparing EMR and endoscopic submucosal dissection. Gastrointest Endosc. 2015 Mar. doi: 10.1016/j.gie.2014.07.034.

9. Kandel P, Wallace MB. Colorectal endoscopic mucosal resection (EMR). Best Pract Res Clin Gastroenterol. 2017 Aug. doi: 10.1016/j.bpg.2017.05.006.

10. Kemper G, et al; ENDOCARE Study Group. Endoscopic techniques to reduce recurrence rates after colorectal EMR: systematic review and meta-analysis. Surg Endosc. 2021 Oct. doi: 10.1007/s00464-021-08574-z.

11. Goto O, et al. Expanding indications for ESD: submucosal disease (SMT/carcinoid tumors). Gastrointest Endosc Clin N Am. 2014 Apr. doi: 10.1016/j.giec.2013.11.006.

12. Wang K, et al. Endoscopic full-thickness resection, indication, methods and perspectives. Dig Endosc. 2023 Jan. doi: 10.1111/den.14474.

13. Herreros de Tejada A. ESD training: A challenging path to excellence. World J Gastrointest Endosc. 2014 Apr 16. doi: 10.4253/wjge.v6.i4.112.

14. Chiba H, et al. Safety and efficacy of simultaneous colorectal ESD for large synchronous colorectal lesions. Endosc Int Open. 2017 Jul. doi: 10.1055/s-0043-110567.

15. Mannath J, Ragunath K. Endoscopic mucosal resection: who and how? Therap Adv Gastroenterol. 2011 Sep. doi: 10.1177/1756283X10388683.

16. Wang XY, et al. Hybrid endoscopic submucosal dissection: An alternative resection modality for large laterally spreading tumors in the cecum? BMC Gastroenterol. 2021 May. doi: 10.1186/s12876-021-01766-w.

17. McCarty TR, et al. Hybrid endoscopic submucosal dissection (ESD) compared with conventional ESD for colorectal lesions: a systematic review and meta-analysis. Endoscopy. 2021 Oct. doi: 10.1055/a-1266-1855.

18. Jain D, et al. Submucosal tunneling endoscopic resection of upper gastrointestinal tract tumors arising from muscularis propria. Ann Gastroenterol. 2017 Feb. doi: 10.20524/aog.2017.0128.

19. Lv XH, et al. Efficacy and safety of submucosal tunneling endoscopic resection for upper gastrointestinal submucosal tumors: a systematic review and meta-analysis. Surg Endosc. 2017 Jan. doi: 10.1007/s00464-016-4978-7.

20. Cao B, et al. Efficacy and safety of submucosal tunneling endoscopic resection for gastric submucosal tumors: a systematic review and meta-analysis. Rev Esp Enferm Dig. 2021 Jan. doi: 10.17235/reed.2020.6989/2020.

21. Cai M, et al. Endoscopic full-thickness resection (EFTR) for gastrointestinal subepithelial tumors. Gastrointest Endosc Clin N Am. 2016 Apr. doi: 10.1016/j.giec.2015.12.013.

22. Brigic A, et al. A systematic review regarding the feasibility and safety of endoscopic full thickness resection (EFTR) for colonic lesions. Surg Endosc. 2013 Oct. doi: 10.1007/s00464-013-2946-z.

Endoscopists are often faced with unique challenges in the management and resection of various gastrointestinal tract lesions. These challenges could be lesion-related, endoscopist-related, or practice-related (see Table 1). As our knowledge, tools and resources, and training significantly evolved in the modern era, there has been a remarkable rise in advanced endoscopic techniques for advanced tissue resection (ATR). Not only does this organ-sparing approach offer a less invasive alternative to surgery, but it has also proved to have outcomes comparable to those of surgical standard of practice in specific scenarios.

When Do You Refer to an Advanced Endoscopist?

One of the most critical steps in caring for patients with complex lesions is the ability to accurately determine whether a referral to an advanced endoscopist is warranted. The initial assessment of a lesion should always involve a careful assessment that risk stratifies the lesion depending on the location, size, neoplastic potential, and the feasibility of standard endoscopic resection compared to the need for surgical input.

A practical example in the case of colonic polyps is highlighted by the American Gastroenterology Association (AGA) guidelines recommending the referral of patients with polyps’ size ≥ 20 mm, challenging polypectomy location, or recurrent polyp at a prior polypectomy site to an endoscopic referral center.¹ In the case of subepithelial lesions without endoscopic characteristics of benign etiology (i.e., lipomas, pancreatic rests, etc.), the threshold for referral to advanced endoscopists for further diagnostic testing by means of endoscopic ultrasonography or for therapeutic ATR should be lower.

Endoscopic tissue resection follows a spectrum, which often involves deeper layers of the gastrointestinal tract (GIT) as we progress along this spectrum (see Figure 1).

Dr. Madi; Dr. Rengarajan, and Dr. Bazarbashi

ATR, a term encompassing a variety of endoscopic techniques ranging from endoscopic mucosal resection to full thickness resection, has gained traction over the last years given the ability to effectively remove various lesions in a precise time and cost-effective manner while maintaining the integrity of the GIT and avoiding major surgery. The indications for ATR vary depending on the technique, but generally include the presence of large or poorly positioned lesions, particularly in high-risk areas of the GIT such as the esophagus and small intestine, lesions extending beyond the mucosal layer or originating from deeper layers, and when en bloc resection of select lesions is necessary.

Saint Louis University School of Medicine

Endoscopic Mucosal Resection (EMR)

EMR is currently utilized for curative treatment of a wide array of GIT lesions limited to the mucosal layer, whether metaplastic, dysplastic, or even in cases with early mucosal cancer, where the risk of submucosal and lymphatic invasion is minimal.⁴ This makes EMR a versatile and proven therapy, often serving as the first-line treatment for many GIT lesions.

Washington University

EMR has various techniques that could be categorized into suction or non-suction (lift and cut) techniques. In the suction technique, devices like multiband mucosectomy (MBM) are commonly used, especially in nodular Barrett’s dysplasia, forming a pseudopolyp for subsequent resection. The procedure is characterized by its safety, efficacy, and cost-effectiveness, contributing to its widespread adoption in clinical practice. In the lift and cut approach, a submucosal injection is utilized to separate the muscularis propria from the lesion, thereby reducing the risk of perforation. Different solutions, such as normal saline, hypertonic saline, 50% dextrose, or proprietary submucosal injection solutions, are employed for submucosal injection.⁵

The non-suction technique using a snare to resect polyps after injection is more often used in colonic and small intestinal EMR. Resection can be done via thermal energy in the form of cut or coagulation; however, there is rising data on the use of piecemeal cold snare resection for select flat polyps of the colon.⁶ There is also promising data on the role of underwater EMR, a common technique employed for colonic lesions, particularly if the lesion does not lift well with submucosal injection.⁷

Adverse events associated with EMR include bleeding (7%-8%) and perforation (0.9%-2%).^8-9 Adequate submucosal fluid injection is crucial to prevent perforations. However, the main limitation of EMR is the piecemeal nature of resections for lesions larger than 20 mm, leading to compromised histopathologic evaluation for complete excision, especially in cases with superficial submucosal invasion (SMI). This can result in residual or recurrent tissue, reportedly 8% to 20%.¹⁰ Despite this limitation, EMR remains a reliable strategy, and recurrent lesions are generally manageable through repeat sessions. The importance of EMR as a therapeutic modality lies in its role in addressing lesions with favorable characteristics, where the risk of SMI is low.

Washington University

Endoscopic Submucosal Dissection (ESD)

ESD is an evolving technique that can be utilized for submucosal lesions of the GIT, lesions not amenable to EMR due to submucosal fibrosis, when en bloc removal of a lesion is needed for accurate histopathological diagnosis, and when other techniques fail.^11-12

ESD was only recently adopted in the United States, requires specialized training, and usually is a lengthier procedure than EMR.¹³ Compared to EMR, it has higher en bloc resection rates and lower recurrence rates, making it curative for lesions with superficial SMI and favorable histologic features.^4,14 The safety profile of ESD appears favorable, with most of the adverse events managed successfully by endoscopic methods. Major complications include intraoperative and delayed perforation, intraoperative and delayed bleeding, aspiration pneumonia, thromboembolism, and stricture formation in the case of circumferential lesions.¹⁵

Despite being technically challenging, ESD may provide a cost-effective long-term solution by avoiding surgery, reducing the need for additional interventions by minimizing recurrence rates. Given the technical complexity of ESD, particularly the submucosal dissection portion, techniques such as hybrid ESD developed. Hybrid ESD combines snaring with circumferential mucosal incision and partial submucosal dissection. Although it promises shorter procedure times, reduced complication rates like perforation, and similar recurrence rates compared to traditional ESD, studies have shown lower success rates in en bloc resection.^16-17

Both EMR and ESD are considered complementary strategies, and the choice between them should be dictated by lesion characteristics, patient preferences, and local expertise.
 

Submucosal Tunneling Endoscopic Resection (STER)

STER has emerged as a well-established technique for the endoscopic resection of GI subepithelial tumors (SETs) originating from the muscularis propria layer. The standard STER procedure involves a series of steps including submucosal elevation proximal to the SET, mucosotomy, creation of a submucosal tunnel, dissection of the SET within the tunnel, enucleation from the deep muscle layer, and subsequent specimen retrieval followed by mucosal closure.

This technique is typically recommended for SETs smaller than 3.5 cm, particularly those located in the mid or distal esophagus, cardia, or along the greater curvature of the gastric body.¹⁸ However, STER may pose technical challenges for larger SETs or lesions in anatomically difficult locations, where surgical resection is recommended instead.¹⁹ Notably, recent large-scale meta-analyses have showcased the favorable complete resection and en bloc resection rates of STER in treating GI SETs.²⁰

Endoscopic Full Thickness Resection (EFTR)

EFTR has emerged as a valuable technique in the endoscopic management of gastrointestinal lesions, particularly SETs and lesions not amenable to EMR or ESD due to fibrosis. EFTR involves the resection of all layers of the GIT from mucosa to serosa, and therefore is well-suited for SETs arising from the muscularis propria (MP).²⁰

EFTR entails two main concepts: tissue resection and complete defect closure. Conventional EFTR consists of several steps, which include mucosal and submucosal pre-cutting, circumferential incision, and dissection through the MP or serosa. This results in a full thickness defect, for which closure of the wall defect is achieved using standard endoscopic clips or a combination of clips and endoloops or endoscopic suturing.²¹ For lesions less than 2 cm, EFTR can be performed in a single step using a cap-mounted full thickness resection device (FTRD). This results in deployment of over-the-scope clip over the target lesion followed by snaring the lesions above the clip.²¹

Location of the SET generally dictates the specific modality of ATR. For example, esophageal SETs may be more amenable to STER given that the lesion typically runs parallel with the lumen of the tubular esophagus, which allows for easier dissection without the need of full or partial retroflexion. While gastric SETs can be resected with STER, it may be challenging and more effectively addressed with EFTR, particularly when the entire lesion can be grasped into the full-thickness resection device.²² Limited data exists for duodenal EFTR, and colorectal SETs closure is particularly challenging.
 

Conclusion

It is key to emphasize that ATR cannot be safely established in practice without the incorporation of a multidisciplinary team (surgeons, radiologists, etc.), specialized tools, and trained personnel. This requires dedicated endoscopic rooms, careful patient selection, and a comprehensive approach to patient care before, during, and after these procedures.

Moreover, it is important to note that some patients may require post-procedure hospitalization for observation to ensure no early complications are encountered. Optimal surveillance strategies after ATR rely heavily on the potential for residual or recurrent disease, underlying pathology, and the expertise of the advanced endoscopist. As the field continues to evolve, ongoing research and technological advances of devices will further enhance the efficacy and safety of ATR in gastroenterology.

Dr. Madi (@MahMadi90) is based in the Division of Gastroenterology and Hepatology, Saint Louis University School of Medicine, Saint Louis, Missouri. Dr. Rengarajan (@ArvindRenga) and Dr. Bazarbashi (@AhmadBazarbashi) are based in the Division of Gastroenterology, Washington University in St. Louis. The authors have no conflicts of interest to disclose, and no funding was required for this project.
 

References

1. Copland AP, et al. AGA Clinical Practice Update on appropriate and tailored polypectomy: Expert review. Clin Gastroenterol Hepatol. 2024 Mar. doi: 10.1016/j.cgh.2023.10.012.

2. Lee SP, et al. Effect of preceding biopsy on the results of endoscopic submucosal dissection for colorectal laterally spreading tumor. Dig Dis Sci. 2019 Oct. doi: 10.1007/s10620-019-05625-3.

3. Medina-Prado L, et al. When and how to use endoscopic tattooing in the colon: An international Delphi agreement. Clin Gastroenterol Hepatol. 2021 May. doi: 10.1016/j.cgh.2021.01.024.

4. Rashid MU, et al. EMR and ESD: Indications, techniques and results. Surg Oncol. 2022 Aug. doi: 10.1016/j.suronc.2022.101742.

5. Castro R, et al. Solutions for submucosal injection: What to choose and how to do it. World J Gastroenterol. 2019 Feb. doi: 10.3748/wjg.v25.i7.777.

6. Rex DK. Best practices for resection of diminutive and small polyps in the colorectum. Gastrointest Endosc Clin N Am. 2019 Oct. doi: 10.1016/j.giec.2019.06.004.

7. Lv XH, et al. Underwater EMR for nonpedunculated colorectal lesions. Gastrointest Endosc. 2023 Apr. doi: 10.1016/j.gie.2022.10.044.

8. Fujiya M, et al. Efficacy and adverse events of EMR and endoscopic submucosal dissection for the treatment of colon neoplasms: a meta-analysis of studies comparing EMR and endoscopic submucosal dissection. Gastrointest Endosc. 2015 Mar. doi: 10.1016/j.gie.2014.07.034.

9. Kandel P, Wallace MB. Colorectal endoscopic mucosal resection (EMR). Best Pract Res Clin Gastroenterol. 2017 Aug. doi: 10.1016/j.bpg.2017.05.006.

10. Kemper G, et al; ENDOCARE Study Group. Endoscopic techniques to reduce recurrence rates after colorectal EMR: systematic review and meta-analysis. Surg Endosc. 2021 Oct. doi: 10.1007/s00464-021-08574-z.

11. Goto O, et al. Expanding indications for ESD: submucosal disease (SMT/carcinoid tumors). Gastrointest Endosc Clin N Am. 2014 Apr. doi: 10.1016/j.giec.2013.11.006.

12. Wang K, et al. Endoscopic full-thickness resection, indication, methods and perspectives. Dig Endosc. 2023 Jan. doi: 10.1111/den.14474.

13. Herreros de Tejada A. ESD training: A challenging path to excellence. World J Gastrointest Endosc. 2014 Apr 16. doi: 10.4253/wjge.v6.i4.112.

14. Chiba H, et al. Safety and efficacy of simultaneous colorectal ESD for large synchronous colorectal lesions. Endosc Int Open. 2017 Jul. doi: 10.1055/s-0043-110567.

15. Mannath J, Ragunath K. Endoscopic mucosal resection: who and how? Therap Adv Gastroenterol. 2011 Sep. doi: 10.1177/1756283X10388683.

16. Wang XY, et al. Hybrid endoscopic submucosal dissection: An alternative resection modality for large laterally spreading tumors in the cecum? BMC Gastroenterol. 2021 May. doi: 10.1186/s12876-021-01766-w.

17. McCarty TR, et al. Hybrid endoscopic submucosal dissection (ESD) compared with conventional ESD for colorectal lesions: a systematic review and meta-analysis. Endoscopy. 2021 Oct. doi: 10.1055/a-1266-1855.

18. Jain D, et al. Submucosal tunneling endoscopic resection of upper gastrointestinal tract tumors arising from muscularis propria. Ann Gastroenterol. 2017 Feb. doi: 10.20524/aog.2017.0128.

19. Lv XH, et al. Efficacy and safety of submucosal tunneling endoscopic resection for upper gastrointestinal submucosal tumors: a systematic review and meta-analysis. Surg Endosc. 2017 Jan. doi: 10.1007/s00464-016-4978-7.

20. Cao B, et al. Efficacy and safety of submucosal tunneling endoscopic resection for gastric submucosal tumors: a systematic review and meta-analysis. Rev Esp Enferm Dig. 2021 Jan. doi: 10.17235/reed.2020.6989/2020.

21. Cai M, et al. Endoscopic full-thickness resection (EFTR) for gastrointestinal subepithelial tumors. Gastrointest Endosc Clin N Am. 2016 Apr. doi: 10.1016/j.giec.2015.12.013.

22. Brigic A, et al. A systematic review regarding the feasibility and safety of endoscopic full thickness resection (EFTR) for colonic lesions. Surg Endosc. 2013 Oct. doi: 10.1007/s00464-013-2946-z.

Endoscopists are often faced with unique challenges in the management and resection of various gastrointestinal tract lesions. These challenges could be lesion-related, endoscopist-related, or practice-related (see Table 1). As our knowledge, tools and resources, and training significantly evolved in the modern era, there has been a remarkable rise in advanced endoscopic techniques for advanced tissue resection (ATR). Not only does this organ-sparing approach offer a less invasive alternative to surgery, but it has also proved to have outcomes comparable to those of surgical standard of practice in specific scenarios.

When Do You Refer to an Advanced Endoscopist?

One of the most critical steps in caring for patients with complex lesions is the ability to accurately determine whether a referral to an advanced endoscopist is warranted. The initial assessment of a lesion should always involve a careful assessment that risk stratifies the lesion depending on the location, size, neoplastic potential, and the feasibility of standard endoscopic resection compared to the need for surgical input.

A practical example in the case of colonic polyps is highlighted by the American Gastroenterology Association (AGA) guidelines recommending the referral of patients with polyps’ size ≥ 20 mm, challenging polypectomy location, or recurrent polyp at a prior polypectomy site to an endoscopic referral center.¹ In the case of subepithelial lesions without endoscopic characteristics of benign etiology (i.e., lipomas, pancreatic rests, etc.), the threshold for referral to advanced endoscopists for further diagnostic testing by means of endoscopic ultrasonography or for therapeutic ATR should be lower.

Endoscopic tissue resection follows a spectrum, which often involves deeper layers of the gastrointestinal tract (GIT) as we progress along this spectrum (see Figure 1).

Dr. Madi; Dr. Rengarajan, and Dr. Bazarbashi

ATR, a term encompassing a variety of endoscopic techniques ranging from endoscopic mucosal resection to full thickness resection, has gained traction over the last years given the ability to effectively remove various lesions in a precise time and cost-effective manner while maintaining the integrity of the GIT and avoiding major surgery. The indications for ATR vary depending on the technique, but generally include the presence of large or poorly positioned lesions, particularly in high-risk areas of the GIT such as the esophagus and small intestine, lesions extending beyond the mucosal layer or originating from deeper layers, and when en bloc resection of select lesions is necessary.

Saint Louis University School of Medicine

Endoscopic Mucosal Resection (EMR)

EMR is currently utilized for curative treatment of a wide array of GIT lesions limited to the mucosal layer, whether metaplastic, dysplastic, or even in cases with early mucosal cancer, where the risk of submucosal and lymphatic invasion is minimal.⁴ This makes EMR a versatile and proven therapy, often serving as the first-line treatment for many GIT lesions.

Washington University

EMR has various techniques that could be categorized into suction or non-suction (lift and cut) techniques. In the suction technique, devices like multiband mucosectomy (MBM) are commonly used, especially in nodular Barrett’s dysplasia, forming a pseudopolyp for subsequent resection. The procedure is characterized by its safety, efficacy, and cost-effectiveness, contributing to its widespread adoption in clinical practice. In the lift and cut approach, a submucosal injection is utilized to separate the muscularis propria from the lesion, thereby reducing the risk of perforation. Different solutions, such as normal saline, hypertonic saline, 50% dextrose, or proprietary submucosal injection solutions, are employed for submucosal injection.⁵

The non-suction technique using a snare to resect polyps after injection is more often used in colonic and small intestinal EMR. Resection can be done via thermal energy in the form of cut or coagulation; however, there is rising data on the use of piecemeal cold snare resection for select flat polyps of the colon.⁶ There is also promising data on the role of underwater EMR, a common technique employed for colonic lesions, particularly if the lesion does not lift well with submucosal injection.⁷

Adverse events associated with EMR include bleeding (7%-8%) and perforation (0.9%-2%).^8-9 Adequate submucosal fluid injection is crucial to prevent perforations. However, the main limitation of EMR is the piecemeal nature of resections for lesions larger than 20 mm, leading to compromised histopathologic evaluation for complete excision, especially in cases with superficial submucosal invasion (SMI). This can result in residual or recurrent tissue, reportedly 8% to 20%.¹⁰ Despite this limitation, EMR remains a reliable strategy, and recurrent lesions are generally manageable through repeat sessions. The importance of EMR as a therapeutic modality lies in its role in addressing lesions with favorable characteristics, where the risk of SMI is low.

Washington University

Endoscopic Submucosal Dissection (ESD)

ESD is an evolving technique that can be utilized for submucosal lesions of the GIT, lesions not amenable to EMR due to submucosal fibrosis, when en bloc removal of a lesion is needed for accurate histopathological diagnosis, and when other techniques fail.^11-12

ESD was only recently adopted in the United States, requires specialized training, and usually is a lengthier procedure than EMR.¹³ Compared to EMR, it has higher en bloc resection rates and lower recurrence rates, making it curative for lesions with superficial SMI and favorable histologic features.^4,14 The safety profile of ESD appears favorable, with most of the adverse events managed successfully by endoscopic methods. Major complications include intraoperative and delayed perforation, intraoperative and delayed bleeding, aspiration pneumonia, thromboembolism, and stricture formation in the case of circumferential lesions.¹⁵

Despite being technically challenging, ESD may provide a cost-effective long-term solution by avoiding surgery, reducing the need for additional interventions by minimizing recurrence rates. Given the technical complexity of ESD, particularly the submucosal dissection portion, techniques such as hybrid ESD developed. Hybrid ESD combines snaring with circumferential mucosal incision and partial submucosal dissection. Although it promises shorter procedure times, reduced complication rates like perforation, and similar recurrence rates compared to traditional ESD, studies have shown lower success rates in en bloc resection.^16-17

Both EMR and ESD are considered complementary strategies, and the choice between them should be dictated by lesion characteristics, patient preferences, and local expertise.
 

Submucosal Tunneling Endoscopic Resection (STER)

STER has emerged as a well-established technique for the endoscopic resection of GI subepithelial tumors (SETs) originating from the muscularis propria layer. The standard STER procedure involves a series of steps including submucosal elevation proximal to the SET, mucosotomy, creation of a submucosal tunnel, dissection of the SET within the tunnel, enucleation from the deep muscle layer, and subsequent specimen retrieval followed by mucosal closure.

This technique is typically recommended for SETs smaller than 3.5 cm, particularly those located in the mid or distal esophagus, cardia, or along the greater curvature of the gastric body.¹⁸ However, STER may pose technical challenges for larger SETs or lesions in anatomically difficult locations, where surgical resection is recommended instead.¹⁹ Notably, recent large-scale meta-analyses have showcased the favorable complete resection and en bloc resection rates of STER in treating GI SETs.²⁰

Endoscopic Full Thickness Resection (EFTR)

EFTR has emerged as a valuable technique in the endoscopic management of gastrointestinal lesions, particularly SETs and lesions not amenable to EMR or ESD due to fibrosis. EFTR involves the resection of all layers of the GIT from mucosa to serosa, and therefore is well-suited for SETs arising from the muscularis propria (MP).²⁰

EFTR entails two main concepts: tissue resection and complete defect closure. Conventional EFTR consists of several steps, which include mucosal and submucosal pre-cutting, circumferential incision, and dissection through the MP or serosa. This results in a full thickness defect, for which closure of the wall defect is achieved using standard endoscopic clips or a combination of clips and endoloops or endoscopic suturing.²¹ For lesions less than 2 cm, EFTR can be performed in a single step using a cap-mounted full thickness resection device (FTRD). This results in deployment of over-the-scope clip over the target lesion followed by snaring the lesions above the clip.²¹

Location of the SET generally dictates the specific modality of ATR. For example, esophageal SETs may be more amenable to STER given that the lesion typically runs parallel with the lumen of the tubular esophagus, which allows for easier dissection without the need of full or partial retroflexion. While gastric SETs can be resected with STER, it may be challenging and more effectively addressed with EFTR, particularly when the entire lesion can be grasped into the full-thickness resection device.²² Limited data exists for duodenal EFTR, and colorectal SETs closure is particularly challenging.
 

Conclusion

It is key to emphasize that ATR cannot be safely established in practice without the incorporation of a multidisciplinary team (surgeons, radiologists, etc.), specialized tools, and trained personnel. This requires dedicated endoscopic rooms, careful patient selection, and a comprehensive approach to patient care before, during, and after these procedures.

Moreover, it is important to note that some patients may require post-procedure hospitalization for observation to ensure no early complications are encountered. Optimal surveillance strategies after ATR rely heavily on the potential for residual or recurrent disease, underlying pathology, and the expertise of the advanced endoscopist. As the field continues to evolve, ongoing research and technological advances of devices will further enhance the efficacy and safety of ATR in gastroenterology.

Dr. Madi (@MahMadi90) is based in the Division of Gastroenterology and Hepatology, Saint Louis University School of Medicine, Saint Louis, Missouri. Dr. Rengarajan (@ArvindRenga) and Dr. Bazarbashi (@AhmadBazarbashi) are based in the Division of Gastroenterology, Washington University in St. Louis. The authors have no conflicts of interest to disclose, and no funding was required for this project.
 

References

1. Copland AP, et al. AGA Clinical Practice Update on appropriate and tailored polypectomy: Expert review. Clin Gastroenterol Hepatol. 2024 Mar. doi: 10.1016/j.cgh.2023.10.012.

2. Lee SP, et al. Effect of preceding biopsy on the results of endoscopic submucosal dissection for colorectal laterally spreading tumor. Dig Dis Sci. 2019 Oct. doi: 10.1007/s10620-019-05625-3.

3. Medina-Prado L, et al. When and how to use endoscopic tattooing in the colon: An international Delphi agreement. Clin Gastroenterol Hepatol. 2021 May. doi: 10.1016/j.cgh.2021.01.024.

4. Rashid MU, et al. EMR and ESD: Indications, techniques and results. Surg Oncol. 2022 Aug. doi: 10.1016/j.suronc.2022.101742.

5. Castro R, et al. Solutions for submucosal injection: What to choose and how to do it. World J Gastroenterol. 2019 Feb. doi: 10.3748/wjg.v25.i7.777.

6. Rex DK. Best practices for resection of diminutive and small polyps in the colorectum. Gastrointest Endosc Clin N Am. 2019 Oct. doi: 10.1016/j.giec.2019.06.004.

7. Lv XH, et al. Underwater EMR for nonpedunculated colorectal lesions. Gastrointest Endosc. 2023 Apr. doi: 10.1016/j.gie.2022.10.044.

8. Fujiya M, et al. Efficacy and adverse events of EMR and endoscopic submucosal dissection for the treatment of colon neoplasms: a meta-analysis of studies comparing EMR and endoscopic submucosal dissection. Gastrointest Endosc. 2015 Mar. doi: 10.1016/j.gie.2014.07.034.

9. Kandel P, Wallace MB. Colorectal endoscopic mucosal resection (EMR). Best Pract Res Clin Gastroenterol. 2017 Aug. doi: 10.1016/j.bpg.2017.05.006.

10. Kemper G, et al; ENDOCARE Study Group. Endoscopic techniques to reduce recurrence rates after colorectal EMR: systematic review and meta-analysis. Surg Endosc. 2021 Oct. doi: 10.1007/s00464-021-08574-z.

11. Goto O, et al. Expanding indications for ESD: submucosal disease (SMT/carcinoid tumors). Gastrointest Endosc Clin N Am. 2014 Apr. doi: 10.1016/j.giec.2013.11.006.

12. Wang K, et al. Endoscopic full-thickness resection, indication, methods and perspectives. Dig Endosc. 2023 Jan. doi: 10.1111/den.14474.

13. Herreros de Tejada A. ESD training: A challenging path to excellence. World J Gastrointest Endosc. 2014 Apr 16. doi: 10.4253/wjge.v6.i4.112.

14. Chiba H, et al. Safety and efficacy of simultaneous colorectal ESD for large synchronous colorectal lesions. Endosc Int Open. 2017 Jul. doi: 10.1055/s-0043-110567.

15. Mannath J, Ragunath K. Endoscopic mucosal resection: who and how? Therap Adv Gastroenterol. 2011 Sep. doi: 10.1177/1756283X10388683.

16. Wang XY, et al. Hybrid endoscopic submucosal dissection: An alternative resection modality for large laterally spreading tumors in the cecum? BMC Gastroenterol. 2021 May. doi: 10.1186/s12876-021-01766-w.

17. McCarty TR, et al. Hybrid endoscopic submucosal dissection (ESD) compared with conventional ESD for colorectal lesions: a systematic review and meta-analysis. Endoscopy. 2021 Oct. doi: 10.1055/a-1266-1855.

18. Jain D, et al. Submucosal tunneling endoscopic resection of upper gastrointestinal tract tumors arising from muscularis propria. Ann Gastroenterol. 2017 Feb. doi: 10.20524/aog.2017.0128.

19. Lv XH, et al. Efficacy and safety of submucosal tunneling endoscopic resection for upper gastrointestinal submucosal tumors: a systematic review and meta-analysis. Surg Endosc. 2017 Jan. doi: 10.1007/s00464-016-4978-7.

20. Cao B, et al. Efficacy and safety of submucosal tunneling endoscopic resection for gastric submucosal tumors: a systematic review and meta-analysis. Rev Esp Enferm Dig. 2021 Jan. doi: 10.17235/reed.2020.6989/2020.

21. Cai M, et al. Endoscopic full-thickness resection (EFTR) for gastrointestinal subepithelial tumors. Gastrointest Endosc Clin N Am. 2016 Apr. doi: 10.1016/j.giec.2015.12.013.

22. Brigic A, et al. A systematic review regarding the feasibility and safety of endoscopic full thickness resection (EFTR) for colonic lesions. Surg Endosc. 2013 Oct. doi: 10.1007/s00464-013-2946-z.

Pelvic floor dysfunction (PFD) represents a spectrum of symptoms involving sensory and emptying abnormalities of the bowel and bladder and pelvic organ prolapse. The pelvic floor refers to a group of muscles that spans the pelvic outlet, providing support to the pelvic organs and coordinating constrictor mechanisms to control urination and defecation. Symptoms reported by patients experiencing PFD include involuntary loss of stool or urine, incomplete emptying of the bowel and bladder, a sensation of fullness, bulging in the vagina, and sexual dysfunction.¹

As such, symptoms related to PFD are very common concerns raised by patients to their gastroenterologists. Data from the National Health and Nutrition Examination Survey show that 23.7% of women over the age of 20 had at least one symptom of PFD.² Unfortunately, patients experiencing pelvic floor dysfunction often are hesitant to seek care because of embarrassment or perception that limited treatment options exist for their symptoms.
 

Pelvic Floor Anatomy

Regions of the pelvis are often referred to by anatomic compartment: anterior (bladder and urethra), middle (vagina and uterus or prostate), and posterior (colon, rectum, and anal canal). Supporting these compartments is the levator ani, a muscle group that is used synonymously with the term “pelvic diaphragm.”

University of Texas Medical Branch

Continence of stool is provided by the anal sphincter muscles and the puborectalis muscle, which wraps around the posterior aspect of the anorectal canal. Damage to the musculature or sensory perception to this area may result in fecal incontinence. Defecation is a coordinated process during which the abdominal and rectal muscles contract, while the anal sphincter muscles and puborectalis simultaneously relax. A disturbance in neuromuscular coordination (dyssynergic defecation) or structural pathology such as pelvic organ prolapse may lead to obstructed defecation.

PFD is thought to be a result of one or more insults to the pelvic floor such as chronic straining, childbirth, iatrogenic injury, or systemic disease such as diabetes.³
 

Evaluation of PFD Symptoms

Patients presenting with suspected PFD necessitate a comprehensive interdisciplinary assessment. In addition to obtaining a medical, surgical, and obstetric history, details about symptoms and lifestyle should include toileting habits, diet, and physical activity. The Pelvic Floor Distress Inventory (PFDI-20) is a commonly used tool that can be employed in the clinical setting.⁴

A pelvic exam can reveal pelvic organ prolapse and other mucosal pathology. The Pelvic Organ Prolapse Quantification System (POP-Q) is a widely used classification system for describing pelvic organ prolapse.⁵ Protrusion of the rectal wall into the vagina is referred to as a rectocele, while prolapse of small bowel into the upper posterior wall of the vagina is called an enterocele. While the finding of a rectocele on exam is common in parous women and may not cause any symptoms, a larger rectocele may cause a sensation of incomplete evacuation of stool.

University of Texas Medical Branch

Initial Management

A stepwise approach to the management of PFD can allow many patients to be effectively treated without the need for surgical intervention. For patients reporting liquid stool consistency, the evaluation should pivot toward the workup and management of diarrhea, which can easily overwhelm continence mechanisms and cause fecal incontinence. Fiber supplementation to normalize stool consistency is considered first-line therapy for patients presenting with both fecal incontinence and obstructed defecation. Other tools for fecal incontinence include avoiding foods that trigger diarrhea and use of loperamide.⁶ For patients with obstructed defecation, a trial of laxatives can be followed by a prescription agent if needed, such as a secretagogue or prokinetic.⁷

Vaginal splinting is a technique that can be used in patients with rectocele, whereby a finger is inserted into the vagina and pressure is applied on the posterior vaginal wall toward the rectum. Reducing the rectocele can facilitate emptying stool from the rectum and prevent leakage of retained stool.⁸ Similarly, use of rectal irrigation enemas can also help clear retained stool.

Pelvic floor physical therapists examine the strength, coordination, and tone of the pelvic floor muscles. When hypertonic musculature is present, manual interventions may be performed including trigger point release, myofascial release, and dry needling.⁹ When hypotonic musculature or dyssynergia is present, strengthening and neuromuscular re-education are recommended. Biofeedback can be administered via surface electromyography and/or balloon training to improve rectal sensitivity. Proper defecation techniques, including positioning, breathing, and behavioral modifications, improve clinical outcomes.

University of Texas Medical Branch

Diagnostic Testing

For patients who do not improve with conservative management, further testing is recommended to characterize the underlying pathology. Typically, anorectal manometry (ARM) is performed in conjunction with the balloon expulsion test and imaging. Each modality has its strengths and limitations (see Table 1).

ARM allows for the assessment of rectal sensation and recto-anal pressures and coordination.¹⁰

Dynamic imaging, by barium defecography under fluoroscopy or MRI, captures anatomy at rest and with simulated defecation to identify pelvic organ prolapse, compartmental defects, and organ mobility.¹¹ Endoanal ultrasonography is considered in patients experiencing fecal incontinence to evaluate the integrity of the anal sphincter muscles.
 

Minimally Invasive Procedures and Surgical Options for PFD

Functional abnormalities such as dyssynergia often coexist with structural abnormalities. Because structural abnormalities are commonly found in asymptomatic patients, noninvasive functional therapy, such as pelvic floor physical therapy and anorectal biofeedback, are preferred prior to surgical repair of a structural finding. For patients with fecal incontinence, sacral nerve stimulation (SNS) has emerged as a preferred therapy due to demonstrated efficacy in symptom improvement.¹² Sphincteroplasty is reserved for those with acute sphincter injury or failure of SNS.

University of Texas Medical Branch

In patients with findings of intussusception, prolapse, or rectocele that have not responded to conservative therapy, referral for surgical repair may be considered. While the specific surgical approach will depend on many factors, the goal is typically excision and/or suspension of rectal tissue and reinforcement of the rectovaginal septum.

Pelvic floor disorders and related gastrointestinal complaints are very common, and likely to increase with increasing longevity and an aging population. It is critical that we are equipped with the available knowledge and tools to provide these patients with optimal care.

Dr. Khan, Dr. Menon, Dr. Allen, and Dr. Corning are based at the University of Texas Medical Branch in Galveston, Texas. They report no conflicts of interest.

References

1. Grimes WR and Stratton M. Pelvic floor dysfunction. 2023 Jun 26. In: StatPearls [Internet]. Treasure Island (Fla.): StatPearls Publishing; 2024 Jan. PMID: 32644672.

2. Nygaard I et al. Prevalence of symptomatic pelvic floor disorders in US women. JAMA. 2008 Sep 17. doi: 10.1001/jama.300.11.1311.

3. Lawrence JM et al. Pelvic floor disorders, diabetes, and obesity in women: Findings from the Kaiser Permanente Continence Associated Risk Epidemiology Study. Diabetes Care. 2007 Oct. doi: 10.2337/dc07-0262.

4. Barber MD et al. Short forms of two condition-specific quality-of-life questionnaires for women with pelvic floor disorders (PFDI-20 and PFIQ-7). Am J Obstet Gynecol. 2005 Jul. doi: 10.1016/j.ajog.2004.12.025.

5. Persu C et al. Pelvic Organ Prolapse Quantification System (POP-Q) — A new era in pelvic prolapse staging. J Med Life. 2011 Jan-Mar. PMID: 21505577.

6. Wald A et al. ACG Clinical Guidelines: Management of benign anorectal disorders. Am J Gastroenterol. 2021 Oct 1. doi: 10.14309/ajg.0000000000001507.

7. Bharucha AE and Lacy BE. Mechanisms, evaluation, and management of chronic constipation. Gastroenterology. 2020 Apr. doi: 10.1053/j.gastro.2019.12.034.

8. Menees S and Chey WD. Fecal incontinence: Pathogenesis, diagnosis, and updated treatment strategies. Gastroenterol Clin North Am. 2022 Mar. doi: 10.1016/j.gtc.2021.10.005.

9. Wallace SL et al. Pelvic floor physical therapy in the treatment of pelvic floor dysfunction in women. Curr Opin Obstet Gynecol. 2019 Dec. doi: 10.1097/GCO.0000000000000584.

10. Carrington EV et al. The international anorectal physiology working group (IAPWG) recommendations: Standardized testing protocol and the London classification for disorders of anorectal function. Neurogastroenterol Motil. 2020 Jan. doi: 10.1111/nmo.13679.

11. El Sayed RF et al. Magnetic resonance imaging of pelvic floor dysfunction — Joint recommendations of the ESUR and ESGAR Pelvic Floor Working Group. Eur Radiol. 2017 May. doi: 10.1007/s00330-016-4471-7.

12. Thaha MA et al. Sacral nerve stimulation for faecal incontinence and constipation in adults. Cochrane Database Syst Rev. 2015 Aug 24. doi: 10.1002/14651858.CD004464.pub3.

13. Chiarioni G et al. Biofeedback benefits only patients with outlet dysfunction, not patients with isolated slow transit constipation. Gastroenterology. 2005 Jul. doi: 10.1053/j.gastro.2005.05.015.

14. Grossi U et al. Diagnostic accuracy study of anorectal manometry for diagnosis of dyssynergic defecation. Gut. 2016 Mar. doi: 10.1136/gutjnl-2014-308835.

15. Albuquerque A. Endoanal ultrasonography in fecal incontinence: Current and future perspectives. World J Gastrointest Endosc. 2015 Jun 10. doi: 10.4253/wjge.v7.i6.575.

Pelvic floor dysfunction (PFD) represents a spectrum of symptoms involving sensory and emptying abnormalities of the bowel and bladder and pelvic organ prolapse. The pelvic floor refers to a group of muscles that spans the pelvic outlet, providing support to the pelvic organs and coordinating constrictor mechanisms to control urination and defecation. Symptoms reported by patients experiencing PFD include involuntary loss of stool or urine, incomplete emptying of the bowel and bladder, a sensation of fullness, bulging in the vagina, and sexual dysfunction.¹

As such, symptoms related to PFD are very common concerns raised by patients to their gastroenterologists. Data from the National Health and Nutrition Examination Survey show that 23.7% of women over the age of 20 had at least one symptom of PFD.² Unfortunately, patients experiencing pelvic floor dysfunction often are hesitant to seek care because of embarrassment or perception that limited treatment options exist for their symptoms.
 

Pelvic Floor Anatomy

Regions of the pelvis are often referred to by anatomic compartment: anterior (bladder and urethra), middle (vagina and uterus or prostate), and posterior (colon, rectum, and anal canal). Supporting these compartments is the levator ani, a muscle group that is used synonymously with the term “pelvic diaphragm.”

University of Texas Medical Branch

Continence of stool is provided by the anal sphincter muscles and the puborectalis muscle, which wraps around the posterior aspect of the anorectal canal. Damage to the musculature or sensory perception to this area may result in fecal incontinence. Defecation is a coordinated process during which the abdominal and rectal muscles contract, while the anal sphincter muscles and puborectalis simultaneously relax. A disturbance in neuromuscular coordination (dyssynergic defecation) or structural pathology such as pelvic organ prolapse may lead to obstructed defecation.

PFD is thought to be a result of one or more insults to the pelvic floor such as chronic straining, childbirth, iatrogenic injury, or systemic disease such as diabetes.³
 

Evaluation of PFD Symptoms

Patients presenting with suspected PFD necessitate a comprehensive interdisciplinary assessment. In addition to obtaining a medical, surgical, and obstetric history, details about symptoms and lifestyle should include toileting habits, diet, and physical activity. The Pelvic Floor Distress Inventory (PFDI-20) is a commonly used tool that can be employed in the clinical setting.⁴

A pelvic exam can reveal pelvic organ prolapse and other mucosal pathology. The Pelvic Organ Prolapse Quantification System (POP-Q) is a widely used classification system for describing pelvic organ prolapse.⁵ Protrusion of the rectal wall into the vagina is referred to as a rectocele, while prolapse of small bowel into the upper posterior wall of the vagina is called an enterocele. While the finding of a rectocele on exam is common in parous women and may not cause any symptoms, a larger rectocele may cause a sensation of incomplete evacuation of stool.

University of Texas Medical Branch

Initial Management

A stepwise approach to the management of PFD can allow many patients to be effectively treated without the need for surgical intervention. For patients reporting liquid stool consistency, the evaluation should pivot toward the workup and management of diarrhea, which can easily overwhelm continence mechanisms and cause fecal incontinence. Fiber supplementation to normalize stool consistency is considered first-line therapy for patients presenting with both fecal incontinence and obstructed defecation. Other tools for fecal incontinence include avoiding foods that trigger diarrhea and use of loperamide.⁶ For patients with obstructed defecation, a trial of laxatives can be followed by a prescription agent if needed, such as a secretagogue or prokinetic.⁷

Vaginal splinting is a technique that can be used in patients with rectocele, whereby a finger is inserted into the vagina and pressure is applied on the posterior vaginal wall toward the rectum. Reducing the rectocele can facilitate emptying stool from the rectum and prevent leakage of retained stool.⁸ Similarly, use of rectal irrigation enemas can also help clear retained stool.

Pelvic floor physical therapists examine the strength, coordination, and tone of the pelvic floor muscles. When hypertonic musculature is present, manual interventions may be performed including trigger point release, myofascial release, and dry needling.⁹ When hypotonic musculature or dyssynergia is present, strengthening and neuromuscular re-education are recommended. Biofeedback can be administered via surface electromyography and/or balloon training to improve rectal sensitivity. Proper defecation techniques, including positioning, breathing, and behavioral modifications, improve clinical outcomes.

University of Texas Medical Branch

Diagnostic Testing

For patients who do not improve with conservative management, further testing is recommended to characterize the underlying pathology. Typically, anorectal manometry (ARM) is performed in conjunction with the balloon expulsion test and imaging. Each modality has its strengths and limitations (see Table 1).

ARM allows for the assessment of rectal sensation and recto-anal pressures and coordination.¹⁰

Dynamic imaging, by barium defecography under fluoroscopy or MRI, captures anatomy at rest and with simulated defecation to identify pelvic organ prolapse, compartmental defects, and organ mobility.¹¹ Endoanal ultrasonography is considered in patients experiencing fecal incontinence to evaluate the integrity of the anal sphincter muscles.
 

Minimally Invasive Procedures and Surgical Options for PFD

Functional abnormalities such as dyssynergia often coexist with structural abnormalities. Because structural abnormalities are commonly found in asymptomatic patients, noninvasive functional therapy, such as pelvic floor physical therapy and anorectal biofeedback, are preferred prior to surgical repair of a structural finding. For patients with fecal incontinence, sacral nerve stimulation (SNS) has emerged as a preferred therapy due to demonstrated efficacy in symptom improvement.¹² Sphincteroplasty is reserved for those with acute sphincter injury or failure of SNS.

University of Texas Medical Branch

In patients with findings of intussusception, prolapse, or rectocele that have not responded to conservative therapy, referral for surgical repair may be considered. While the specific surgical approach will depend on many factors, the goal is typically excision and/or suspension of rectal tissue and reinforcement of the rectovaginal septum.

Pelvic floor disorders and related gastrointestinal complaints are very common, and likely to increase with increasing longevity and an aging population. It is critical that we are equipped with the available knowledge and tools to provide these patients with optimal care.

Dr. Khan, Dr. Menon, Dr. Allen, and Dr. Corning are based at the University of Texas Medical Branch in Galveston, Texas. They report no conflicts of interest.

References

1. Grimes WR and Stratton M. Pelvic floor dysfunction. 2023 Jun 26. In: StatPearls [Internet]. Treasure Island (Fla.): StatPearls Publishing; 2024 Jan. PMID: 32644672.

2. Nygaard I et al. Prevalence of symptomatic pelvic floor disorders in US women. JAMA. 2008 Sep 17. doi: 10.1001/jama.300.11.1311.

3. Lawrence JM et al. Pelvic floor disorders, diabetes, and obesity in women: Findings from the Kaiser Permanente Continence Associated Risk Epidemiology Study. Diabetes Care. 2007 Oct. doi: 10.2337/dc07-0262.

4. Barber MD et al. Short forms of two condition-specific quality-of-life questionnaires for women with pelvic floor disorders (PFDI-20 and PFIQ-7). Am J Obstet Gynecol. 2005 Jul. doi: 10.1016/j.ajog.2004.12.025.

5. Persu C et al. Pelvic Organ Prolapse Quantification System (POP-Q) — A new era in pelvic prolapse staging. J Med Life. 2011 Jan-Mar. PMID: 21505577.

6. Wald A et al. ACG Clinical Guidelines: Management of benign anorectal disorders. Am J Gastroenterol. 2021 Oct 1. doi: 10.14309/ajg.0000000000001507.

7. Bharucha AE and Lacy BE. Mechanisms, evaluation, and management of chronic constipation. Gastroenterology. 2020 Apr. doi: 10.1053/j.gastro.2019.12.034.

8. Menees S and Chey WD. Fecal incontinence: Pathogenesis, diagnosis, and updated treatment strategies. Gastroenterol Clin North Am. 2022 Mar. doi: 10.1016/j.gtc.2021.10.005.

9. Wallace SL et al. Pelvic floor physical therapy in the treatment of pelvic floor dysfunction in women. Curr Opin Obstet Gynecol. 2019 Dec. doi: 10.1097/GCO.0000000000000584.

10. Carrington EV et al. The international anorectal physiology working group (IAPWG) recommendations: Standardized testing protocol and the London classification for disorders of anorectal function. Neurogastroenterol Motil. 2020 Jan. doi: 10.1111/nmo.13679.

11. El Sayed RF et al. Magnetic resonance imaging of pelvic floor dysfunction — Joint recommendations of the ESUR and ESGAR Pelvic Floor Working Group. Eur Radiol. 2017 May. doi: 10.1007/s00330-016-4471-7.

12. Thaha MA et al. Sacral nerve stimulation for faecal incontinence and constipation in adults. Cochrane Database Syst Rev. 2015 Aug 24. doi: 10.1002/14651858.CD004464.pub3.

13. Chiarioni G et al. Biofeedback benefits only patients with outlet dysfunction, not patients with isolated slow transit constipation. Gastroenterology. 2005 Jul. doi: 10.1053/j.gastro.2005.05.015.

14. Grossi U et al. Diagnostic accuracy study of anorectal manometry for diagnosis of dyssynergic defecation. Gut. 2016 Mar. doi: 10.1136/gutjnl-2014-308835.

15. Albuquerque A. Endoanal ultrasonography in fecal incontinence: Current and future perspectives. World J Gastrointest Endosc. 2015 Jun 10. doi: 10.4253/wjge.v7.i6.575.

Pelvic floor dysfunction (PFD) represents a spectrum of symptoms involving sensory and emptying abnormalities of the bowel and bladder and pelvic organ prolapse. The pelvic floor refers to a group of muscles that spans the pelvic outlet, providing support to the pelvic organs and coordinating constrictor mechanisms to control urination and defecation. Symptoms reported by patients experiencing PFD include involuntary loss of stool or urine, incomplete emptying of the bowel and bladder, a sensation of fullness, bulging in the vagina, and sexual dysfunction.¹

As such, symptoms related to PFD are very common concerns raised by patients to their gastroenterologists. Data from the National Health and Nutrition Examination Survey show that 23.7% of women over the age of 20 had at least one symptom of PFD.² Unfortunately, patients experiencing pelvic floor dysfunction often are hesitant to seek care because of embarrassment or perception that limited treatment options exist for their symptoms.
 

Pelvic Floor Anatomy

Regions of the pelvis are often referred to by anatomic compartment: anterior (bladder and urethra), middle (vagina and uterus or prostate), and posterior (colon, rectum, and anal canal). Supporting these compartments is the levator ani, a muscle group that is used synonymously with the term “pelvic diaphragm.”

University of Texas Medical Branch

Continence of stool is provided by the anal sphincter muscles and the puborectalis muscle, which wraps around the posterior aspect of the anorectal canal. Damage to the musculature or sensory perception to this area may result in fecal incontinence. Defecation is a coordinated process during which the abdominal and rectal muscles contract, while the anal sphincter muscles and puborectalis simultaneously relax. A disturbance in neuromuscular coordination (dyssynergic defecation) or structural pathology such as pelvic organ prolapse may lead to obstructed defecation.

PFD is thought to be a result of one or more insults to the pelvic floor such as chronic straining, childbirth, iatrogenic injury, or systemic disease such as diabetes.³
 

Evaluation of PFD Symptoms

Patients presenting with suspected PFD necessitate a comprehensive interdisciplinary assessment. In addition to obtaining a medical, surgical, and obstetric history, details about symptoms and lifestyle should include toileting habits, diet, and physical activity. The Pelvic Floor Distress Inventory (PFDI-20) is a commonly used tool that can be employed in the clinical setting.⁴

A pelvic exam can reveal pelvic organ prolapse and other mucosal pathology. The Pelvic Organ Prolapse Quantification System (POP-Q) is a widely used classification system for describing pelvic organ prolapse.⁵ Protrusion of the rectal wall into the vagina is referred to as a rectocele, while prolapse of small bowel into the upper posterior wall of the vagina is called an enterocele. While the finding of a rectocele on exam is common in parous women and may not cause any symptoms, a larger rectocele may cause a sensation of incomplete evacuation of stool.

University of Texas Medical Branch

Initial Management

A stepwise approach to the management of PFD can allow many patients to be effectively treated without the need for surgical intervention. For patients reporting liquid stool consistency, the evaluation should pivot toward the workup and management of diarrhea, which can easily overwhelm continence mechanisms and cause fecal incontinence. Fiber supplementation to normalize stool consistency is considered first-line therapy for patients presenting with both fecal incontinence and obstructed defecation. Other tools for fecal incontinence include avoiding foods that trigger diarrhea and use of loperamide.⁶ For patients with obstructed defecation, a trial of laxatives can be followed by a prescription agent if needed, such as a secretagogue or prokinetic.⁷

Vaginal splinting is a technique that can be used in patients with rectocele, whereby a finger is inserted into the vagina and pressure is applied on the posterior vaginal wall toward the rectum. Reducing the rectocele can facilitate emptying stool from the rectum and prevent leakage of retained stool.⁸ Similarly, use of rectal irrigation enemas can also help clear retained stool.

Pelvic floor physical therapists examine the strength, coordination, and tone of the pelvic floor muscles. When hypertonic musculature is present, manual interventions may be performed including trigger point release, myofascial release, and dry needling.⁹ When hypotonic musculature or dyssynergia is present, strengthening and neuromuscular re-education are recommended. Biofeedback can be administered via surface electromyography and/or balloon training to improve rectal sensitivity. Proper defecation techniques, including positioning, breathing, and behavioral modifications, improve clinical outcomes.

University of Texas Medical Branch

Diagnostic Testing

For patients who do not improve with conservative management, further testing is recommended to characterize the underlying pathology. Typically, anorectal manometry (ARM) is performed in conjunction with the balloon expulsion test and imaging. Each modality has its strengths and limitations (see Table 1).

ARM allows for the assessment of rectal sensation and recto-anal pressures and coordination.¹⁰

Dynamic imaging, by barium defecography under fluoroscopy or MRI, captures anatomy at rest and with simulated defecation to identify pelvic organ prolapse, compartmental defects, and organ mobility.¹¹ Endoanal ultrasonography is considered in patients experiencing fecal incontinence to evaluate the integrity of the anal sphincter muscles.
 

Minimally Invasive Procedures and Surgical Options for PFD

Functional abnormalities such as dyssynergia often coexist with structural abnormalities. Because structural abnormalities are commonly found in asymptomatic patients, noninvasive functional therapy, such as pelvic floor physical therapy and anorectal biofeedback, are preferred prior to surgical repair of a structural finding. For patients with fecal incontinence, sacral nerve stimulation (SNS) has emerged as a preferred therapy due to demonstrated efficacy in symptom improvement.¹² Sphincteroplasty is reserved for those with acute sphincter injury or failure of SNS.

University of Texas Medical Branch

In patients with findings of intussusception, prolapse, or rectocele that have not responded to conservative therapy, referral for surgical repair may be considered. While the specific surgical approach will depend on many factors, the goal is typically excision and/or suspension of rectal tissue and reinforcement of the rectovaginal septum.

Pelvic floor disorders and related gastrointestinal complaints are very common, and likely to increase with increasing longevity and an aging population. It is critical that we are equipped with the available knowledge and tools to provide these patients with optimal care.

Dr. Khan, Dr. Menon, Dr. Allen, and Dr. Corning are based at the University of Texas Medical Branch in Galveston, Texas. They report no conflicts of interest.

References

1. Grimes WR and Stratton M. Pelvic floor dysfunction. 2023 Jun 26. In: StatPearls [Internet]. Treasure Island (Fla.): StatPearls Publishing; 2024 Jan. PMID: 32644672.

2. Nygaard I et al. Prevalence of symptomatic pelvic floor disorders in US women. JAMA. 2008 Sep 17. doi: 10.1001/jama.300.11.1311.

3. Lawrence JM et al. Pelvic floor disorders, diabetes, and obesity in women: Findings from the Kaiser Permanente Continence Associated Risk Epidemiology Study. Diabetes Care. 2007 Oct. doi: 10.2337/dc07-0262.

4. Barber MD et al. Short forms of two condition-specific quality-of-life questionnaires for women with pelvic floor disorders (PFDI-20 and PFIQ-7). Am J Obstet Gynecol. 2005 Jul. doi: 10.1016/j.ajog.2004.12.025.

5. Persu C et al. Pelvic Organ Prolapse Quantification System (POP-Q) — A new era in pelvic prolapse staging. J Med Life. 2011 Jan-Mar. PMID: 21505577.

6. Wald A et al. ACG Clinical Guidelines: Management of benign anorectal disorders. Am J Gastroenterol. 2021 Oct 1. doi: 10.14309/ajg.0000000000001507.

7. Bharucha AE and Lacy BE. Mechanisms, evaluation, and management of chronic constipation. Gastroenterology. 2020 Apr. doi: 10.1053/j.gastro.2019.12.034.

8. Menees S and Chey WD. Fecal incontinence: Pathogenesis, diagnosis, and updated treatment strategies. Gastroenterol Clin North Am. 2022 Mar. doi: 10.1016/j.gtc.2021.10.005.

9. Wallace SL et al. Pelvic floor physical therapy in the treatment of pelvic floor dysfunction in women. Curr Opin Obstet Gynecol. 2019 Dec. doi: 10.1097/GCO.0000000000000584.

10. Carrington EV et al. The international anorectal physiology working group (IAPWG) recommendations: Standardized testing protocol and the London classification for disorders of anorectal function. Neurogastroenterol Motil. 2020 Jan. doi: 10.1111/nmo.13679.

11. El Sayed RF et al. Magnetic resonance imaging of pelvic floor dysfunction — Joint recommendations of the ESUR and ESGAR Pelvic Floor Working Group. Eur Radiol. 2017 May. doi: 10.1007/s00330-016-4471-7.

12. Thaha MA et al. Sacral nerve stimulation for faecal incontinence and constipation in adults. Cochrane Database Syst Rev. 2015 Aug 24. doi: 10.1002/14651858.CD004464.pub3.

13. Chiarioni G et al. Biofeedback benefits only patients with outlet dysfunction, not patients with isolated slow transit constipation. Gastroenterology. 2005 Jul. doi: 10.1053/j.gastro.2005.05.015.

14. Grossi U et al. Diagnostic accuracy study of anorectal manometry for diagnosis of dyssynergic defecation. Gut. 2016 Mar. doi: 10.1136/gutjnl-2014-308835.

15. Albuquerque A. Endoanal ultrasonography in fecal incontinence: Current and future perspectives. World J Gastrointest Endosc. 2015 Jun 10. doi: 10.4253/wjge.v7.i6.575.

Cases

Patient 1: 55-year-old cis-male, who identifies as gay, has ulcerative colitis that has been refractory to multiple biologic therapies. His provider recommends a total proctocolectomy with ileal pouch anal anastomosis (TPC with IPAA), but the patient has questions regarding sexual function following surgery. Specifically, he is wondering when, or if, he can resume receptive anal intercourse. How would you counsel him?

Patient 2: 25-year-old, trans-female, status-post vaginoplasty with use of sigmoid colon and with well-controlled ulcerative colitis, presents with vaginal discharge, weight loss, and rectal bleeding. How do you explain what has happened to her? During your discussion, she also asks you why her chart continues to use her “dead name.” How do you respond?

Patient 3: 32-year-old, cis-female, G2P2, who identifies as a lesbian, has active ulcerative colitis. She wants to discuss medical or surgical therapy and future pregnancies. How would you counsel her?

Many gastroenterologists would likely know how to address patient 3’s concerns, but the concerns of patients 1 and 2 often go unaddressed or dismissed. There is a paucity of literature to help guide the care of LGBTQ+ individuals with IBD. Numerous studies and surveys have been conducted on patients with inflammatory bowel disease (IBD), but the focus of these studies has always been through a heteronormative cisgender lens. The focus of many studies is on fertility or sexual health and function in cisgender, heteronormative individuals.^1-3 In the last few years, however, there has been increasing awareness of the health disparities, stigma, and discrimination that sexual and gender minorities (SGM) experience.^4-6 For the purposes of this discussion, individuals within the lesbian, gay, bisexual, transgender, queer/questioning, intersex, and asexual (LGBTQIA+) community will be referred to as SGM. We recognize that even this exhaustive listing above does not acknowledge the full spectrum of diversity within the SGM community.

Clinical Care/Competency for SGM with IBD is Lacking

Almost 10% of the US population identifies as some form of SGM, and that number can be higher within the younger generations.⁴ SGM patients tend to delay or avoid seeking health care due to concern for provider mistreatment or lack of regard for their individual concerns. Additionally, there are several gaps in clinical knowledge about caring for SGM individuals. Little is known regarding the incidence or prevalence of IBD in SGM populations, but it is perceived to be similar to cisgender heterosexual individuals. Furthermore, as Newman et al. highlighted in their systematic review published in May 2023, there is a lack of guidance regarding sexual activity in the setting of IBD in SGM individuals.⁵ There is also a significant lack of knowledge on the impact of gender-affirming care on the natural history and treatments of IBD in transgender and gender non-conforming (TGNC) individuals. This can impact providers’ comfort and competence in caring for TGNC individuals.

Mayo Clinic

Another important point to make is that the SGM community still faces discrimination due to sexual orientation or gender identity to this day, which impacts the quality and delivery of their care.⁷ Culturally-competent care should include care that is free from stigma, implicit and explicit biases, and discrimination. In 2011, an Institute of Medicine report documented, among other issues, provider discomfort in delivering care to SGM patients.⁸ While SGM individuals prefer a provider who acknowledges their sexual orientation and gender identity and treats them with the dignity and respect they deserve, many SGM individuals share valid concerns regarding their safety, which impact their desire to disclose their identity to health care providers.⁹ This certainly can have an impact on the quality of care they receive, including important health maintenance milestones and cancer screenings.¹⁰

An internal survey at our institution of providers (nurses, physician assistants, surgeons, and physicians) found that among 85 responders, 70% have cared for SGM who have undergone TPC with ileal pouch anal anastomosis (IPAA). Of these, 75% did not ask about sexual orientation or practices before pouch formation (though almost all of them agreed it would be important to ask). A total of 55% were comfortable in discussing SGM-related concerns; 53% did not feel comfortable discussing sexual orientation or practices; and in particular when it came to anoreceptive intercourse (ARI), 73% did not feel confident discussing recommendations.¹¹

All of these issues highlight the importance of developing curricula that focus on reducing implicit and explicit biases towards SGM individuals and increasing the competence of providers to take care of SGM individuals in a safe space.

Mayo Clinic

Additionally, it further justifies the need for ethical research that focuses on the needs of SGM individuals to guide evidence-based approaches to care. Given the implicit and explicit heterosexism and transphobia in society and many health care systems, Rainbows in Gastro was formed as an advocacy group for SGM patients, trainees, and staff in gastroenterology and hepatology.⁴

Research in SGM and IBD is lacking

There are additional needs for research in IBD and how it pertains to the needs of SGM individuals. Figure 1 highlights the lack of PubMed results for the search terms “IBD + LGBT,” “IBD + LGBTQ,” or “IBD + queer.” In contrast, the search terms “IBD + fertility” and “IBD + sexual dysfunction” generate many results. Even a systemic review conducted by Newman et al. of multiple databases in 2022 found only seven articles that demonstrated appropriately performed studies on SGM patients with IBD.⁵ This highlights the significant dearth of research in the realm of SGM health in IBD.

Newman and colleagues have recently published research considerations for SGM individuals. They highlighted the need to include understanding the “unique combination of psychosocial, biomedical, and legal experiences” that results in different needs and outcomes. There were several areas identified, including minority stress, which comes from existence of being SGM, especially as transgender individuals face increasing legal challenges in a variety of settings, not just healthcare.⁶ In a retrospective chart review investigating social determinants of health in SGM-IBD populations,¹² 36% of patients reported some level of social isolation, and almost 50% reported some level of stress. A total of 40% of them self-reported some perceived level of risk with respect to employment, and 17% reported depression. Given that this was a chart review and not a strict questionnaire, this study was certainly limited, and we would hypothesize that these numbers are therefore underestimating the true proportion of SGM-IBD patients who deal with employment concerns, social isolation, or psychological distress.

What Next? Back to the Patients

Circling back to our patients from the introduction, how would you counsel each of them? In patient 1’s case, we would inform him that pelvic surgery can increase the risk for sexual dysfunction, such as erectile dysfunction. He additionally would be advised during a staged TPC with IPAA, he may experience issues with body image. However, should he desire to participate in receptive anal intercourse after completion of his surgeries, the general recommendation would be to wait at least 6 months and with proven remission. It should further be noted that these are not formalized recommendations, only highlighting the need for more research and consensus on standards of care for SGM patients. He should finally be told that because he has ulcerative colitis, removal of the colon does not remove the risk for future intestinal involvement such as possible pouchitis.

In patient 2’s case, she is likely experiencing diversion vaginitis related to use of her colon for her neo-vagina. She should undergo colonoscopy and vaginoscopy in addition to standard work-up for her known ulcerative colitis.¹³ Management should be done in a multidisciplinary approach between the IBD provider, gynecologist, and gender-affirming provider. The electronic medical record should be updated to reflect the patient’s preferred name, pronouns, and gender identity, and her medical records, including automated clinical reports, should be updated accordingly.

As for patient 3, she would be counseled according to well-documented guidelines on pregnancy and IBD, including risks of medications (such as Jak inhibitors or methotrexate) versus the risk of uncontrolled IBD during pregnancy.¹

Regardless of a patient’s gender identity or sexual orientation, patient-centered, culturally competent, and sensitive care should be provided. At Mayo Clinic in Rochester, we started one of the first Pride in IBD Clinics, which focuses on the care of SGM individuals with IBD. Our focus is to address the needs of patients who belong to the SGM community in a wholistic approach within a safe space (https://www.youtube.com/watch?v=pYa_zYaCA6M; https://www.mayoclinic.org/departments-centers/inflammatory-bowel-disease-clinic/overview/ovc-20357763). Our process of developing the clinic included training all staff on proper communication and cultural sensitivity for the SGM community.

Dr. Chiang and Dr. Chedid are both in the Division of Gastroenterology and Hepatology, Mayo Clinic, Rochester, Minnesota. Dr. Chedid is also with the Robert D. and Patricia E. Kern Center for the Science of Health Care Delivery, Mayo Clinic. Neither of the authors have any relevant conflicts of interest. They are on X, formerly Twitter: @dr_davidchiang , @VictorChedidMD .

CITATIONS

1. Mahadevan U et al. Inflammatory bowel disease in pregnancy clinical care pathway: A report from the American Gastroenterological Association IBD Parenthood Project Working Group. Gastroenterology. 2019;156:1508-24.

2. Pires F et al. A survey on the impact of IBD in sexual health: Into intimacy. Medicine (Baltimore). 2022;101:e32279.

3. Mules TC et al. The impact of disease activity on sexual and erectile dysfunction in patients with inflammatory bowel disease. Inflamm Bowel Dis. 2023;29:1244-54.

4. Duong N et al. Overcoming disparities for sexual and gender minority patients and providers in gastroenterology and hepatology: Introduction to Rainbows in Gastro. Lancet Gastroenterol Hepatol. 2023;8:299-301.

5. Newman KL et al. A systematic review of inflammatory bowel disease epidemiology and health outcomes in sexual and gender minority individuals. Gastroenterology. 2023;164:866-71.

6. Newman KL et al. Research considerations in Digestive and liver disease in transgender and gender-diverse populations. Gastroenterology. 2023;165:523-28 e1.

7. Velez C et al. Digestive health in sexual and gender minority populations. Am J Gastroenterol. 2022;117:865-75.

8. Medicine Io. Washington (DC): The National Academies Press, 2011.

9. Austin EL. Sexual orientation disclosure to health care providers among urban and non-urban southern lesbians. Women Health. 2013;53:41-55.

10. Oladeru OT et al. Breast and cervical cancer screening disparities in transgender people. Am J Clin Oncol. 2022;45:116-21.

11. Vinsard DG et al. Healthcare providers’ perspectives on anoreceptive intercourse in sexual and gender minorities with ileal pouch anal anastomosis. Digestive Disease Week (DDW). Chicago, IL, 2023.

12. Ghusn W et al. Social determinants of health in LGBTQIA+ patients with inflammatory bowel disease. American College of Gastroenterology (ACG). Charlotte, NC, 2022.

13. Grasman ME et al. Neovaginal sparing in a transgender woman with ulcerative colitis. Clin Gastroenterol Hepatol. 2016;14:e73-4.

14. Prevention CfDCa. Lesbian, Gay, Bisexual, and Transgender Health — https://www.cdc.gov/lgbthealth/index.htm.

15. Institute TF. National LGBTQIA+ Health Education Center — https://www.lgbtqiahealtheducation.org/.

16. Services UDoHaH. LGBTQI+ Resources — https://www.hhs.gov/programs/topic-sites/lgbtqi/resources/index.html.

Cases

Patient 1: 55-year-old cis-male, who identifies as gay, has ulcerative colitis that has been refractory to multiple biologic therapies. His provider recommends a total proctocolectomy with ileal pouch anal anastomosis (TPC with IPAA), but the patient has questions regarding sexual function following surgery. Specifically, he is wondering when, or if, he can resume receptive anal intercourse. How would you counsel him?

Patient 2: 25-year-old, trans-female, status-post vaginoplasty with use of sigmoid colon and with well-controlled ulcerative colitis, presents with vaginal discharge, weight loss, and rectal bleeding. How do you explain what has happened to her? During your discussion, she also asks you why her chart continues to use her “dead name.” How do you respond?

Patient 3: 32-year-old, cis-female, G2P2, who identifies as a lesbian, has active ulcerative colitis. She wants to discuss medical or surgical therapy and future pregnancies. How would you counsel her?

Many gastroenterologists would likely know how to address patient 3’s concerns, but the concerns of patients 1 and 2 often go unaddressed or dismissed. There is a paucity of literature to help guide the care of LGBTQ+ individuals with IBD. Numerous studies and surveys have been conducted on patients with inflammatory bowel disease (IBD), but the focus of these studies has always been through a heteronormative cisgender lens. The focus of many studies is on fertility or sexual health and function in cisgender, heteronormative individuals.^1-3 In the last few years, however, there has been increasing awareness of the health disparities, stigma, and discrimination that sexual and gender minorities (SGM) experience.^4-6 For the purposes of this discussion, individuals within the lesbian, gay, bisexual, transgender, queer/questioning, intersex, and asexual (LGBTQIA+) community will be referred to as SGM. We recognize that even this exhaustive listing above does not acknowledge the full spectrum of diversity within the SGM community.

Clinical Care/Competency for SGM with IBD is Lacking

Almost 10% of the US population identifies as some form of SGM, and that number can be higher within the younger generations.⁴ SGM patients tend to delay or avoid seeking health care due to concern for provider mistreatment or lack of regard for their individual concerns. Additionally, there are several gaps in clinical knowledge about caring for SGM individuals. Little is known regarding the incidence or prevalence of IBD in SGM populations, but it is perceived to be similar to cisgender heterosexual individuals. Furthermore, as Newman et al. highlighted in their systematic review published in May 2023, there is a lack of guidance regarding sexual activity in the setting of IBD in SGM individuals.⁵ There is also a significant lack of knowledge on the impact of gender-affirming care on the natural history and treatments of IBD in transgender and gender non-conforming (TGNC) individuals. This can impact providers’ comfort and competence in caring for TGNC individuals.

Mayo Clinic

Another important point to make is that the SGM community still faces discrimination due to sexual orientation or gender identity to this day, which impacts the quality and delivery of their care.⁷ Culturally-competent care should include care that is free from stigma, implicit and explicit biases, and discrimination. In 2011, an Institute of Medicine report documented, among other issues, provider discomfort in delivering care to SGM patients.⁸ While SGM individuals prefer a provider who acknowledges their sexual orientation and gender identity and treats them with the dignity and respect they deserve, many SGM individuals share valid concerns regarding their safety, which impact their desire to disclose their identity to health care providers.⁹ This certainly can have an impact on the quality of care they receive, including important health maintenance milestones and cancer screenings.¹⁰

An internal survey at our institution of providers (nurses, physician assistants, surgeons, and physicians) found that among 85 responders, 70% have cared for SGM who have undergone TPC with ileal pouch anal anastomosis (IPAA). Of these, 75% did not ask about sexual orientation or practices before pouch formation (though almost all of them agreed it would be important to ask). A total of 55% were comfortable in discussing SGM-related concerns; 53% did not feel comfortable discussing sexual orientation or practices; and in particular when it came to anoreceptive intercourse (ARI), 73% did not feel confident discussing recommendations.¹¹

All of these issues highlight the importance of developing curricula that focus on reducing implicit and explicit biases towards SGM individuals and increasing the competence of providers to take care of SGM individuals in a safe space.

Mayo Clinic

Additionally, it further justifies the need for ethical research that focuses on the needs of SGM individuals to guide evidence-based approaches to care. Given the implicit and explicit heterosexism and transphobia in society and many health care systems, Rainbows in Gastro was formed as an advocacy group for SGM patients, trainees, and staff in gastroenterology and hepatology.⁴

Research in SGM and IBD is lacking

There are additional needs for research in IBD and how it pertains to the needs of SGM individuals. Figure 1 highlights the lack of PubMed results for the search terms “IBD + LGBT,” “IBD + LGBTQ,” or “IBD + queer.” In contrast, the search terms “IBD + fertility” and “IBD + sexual dysfunction” generate many results. Even a systemic review conducted by Newman et al. of multiple databases in 2022 found only seven articles that demonstrated appropriately performed studies on SGM patients with IBD.⁵ This highlights the significant dearth of research in the realm of SGM health in IBD.

Newman and colleagues have recently published research considerations for SGM individuals. They highlighted the need to include understanding the “unique combination of psychosocial, biomedical, and legal experiences” that results in different needs and outcomes. There were several areas identified, including minority stress, which comes from existence of being SGM, especially as transgender individuals face increasing legal challenges in a variety of settings, not just healthcare.⁶ In a retrospective chart review investigating social determinants of health in SGM-IBD populations,¹² 36% of patients reported some level of social isolation, and almost 50% reported some level of stress. A total of 40% of them self-reported some perceived level of risk with respect to employment, and 17% reported depression. Given that this was a chart review and not a strict questionnaire, this study was certainly limited, and we would hypothesize that these numbers are therefore underestimating the true proportion of SGM-IBD patients who deal with employment concerns, social isolation, or psychological distress.

What Next? Back to the Patients

Circling back to our patients from the introduction, how would you counsel each of them? In patient 1’s case, we would inform him that pelvic surgery can increase the risk for sexual dysfunction, such as erectile dysfunction. He additionally would be advised during a staged TPC with IPAA, he may experience issues with body image. However, should he desire to participate in receptive anal intercourse after completion of his surgeries, the general recommendation would be to wait at least 6 months and with proven remission. It should further be noted that these are not formalized recommendations, only highlighting the need for more research and consensus on standards of care for SGM patients. He should finally be told that because he has ulcerative colitis, removal of the colon does not remove the risk for future intestinal involvement such as possible pouchitis.

In patient 2’s case, she is likely experiencing diversion vaginitis related to use of her colon for her neo-vagina. She should undergo colonoscopy and vaginoscopy in addition to standard work-up for her known ulcerative colitis.¹³ Management should be done in a multidisciplinary approach between the IBD provider, gynecologist, and gender-affirming provider. The electronic medical record should be updated to reflect the patient’s preferred name, pronouns, and gender identity, and her medical records, including automated clinical reports, should be updated accordingly.

As for patient 3, she would be counseled according to well-documented guidelines on pregnancy and IBD, including risks of medications (such as Jak inhibitors or methotrexate) versus the risk of uncontrolled IBD during pregnancy.¹

Regardless of a patient’s gender identity or sexual orientation, patient-centered, culturally competent, and sensitive care should be provided. At Mayo Clinic in Rochester, we started one of the first Pride in IBD Clinics, which focuses on the care of SGM individuals with IBD. Our focus is to address the needs of patients who belong to the SGM community in a wholistic approach within a safe space (https://www.youtube.com/watch?v=pYa_zYaCA6M; https://www.mayoclinic.org/departments-centers/inflammatory-bowel-disease-clinic/overview/ovc-20357763). Our process of developing the clinic included training all staff on proper communication and cultural sensitivity for the SGM community.

Dr. Chiang and Dr. Chedid are both in the Division of Gastroenterology and Hepatology, Mayo Clinic, Rochester, Minnesota. Dr. Chedid is also with the Robert D. and Patricia E. Kern Center for the Science of Health Care Delivery, Mayo Clinic. Neither of the authors have any relevant conflicts of interest. They are on X, formerly Twitter: @dr_davidchiang , @VictorChedidMD .

CITATIONS

1. Mahadevan U et al. Inflammatory bowel disease in pregnancy clinical care pathway: A report from the American Gastroenterological Association IBD Parenthood Project Working Group. Gastroenterology. 2019;156:1508-24.

2. Pires F et al. A survey on the impact of IBD in sexual health: Into intimacy. Medicine (Baltimore). 2022;101:e32279.

3. Mules TC et al. The impact of disease activity on sexual and erectile dysfunction in patients with inflammatory bowel disease. Inflamm Bowel Dis. 2023;29:1244-54.

4. Duong N et al. Overcoming disparities for sexual and gender minority patients and providers in gastroenterology and hepatology: Introduction to Rainbows in Gastro. Lancet Gastroenterol Hepatol. 2023;8:299-301.

5. Newman KL et al. A systematic review of inflammatory bowel disease epidemiology and health outcomes in sexual and gender minority individuals. Gastroenterology. 2023;164:866-71.

6. Newman KL et al. Research considerations in Digestive and liver disease in transgender and gender-diverse populations. Gastroenterology. 2023;165:523-28 e1.

7. Velez C et al. Digestive health in sexual and gender minority populations. Am J Gastroenterol. 2022;117:865-75.

8. Medicine Io. Washington (DC): The National Academies Press, 2011.

9. Austin EL. Sexual orientation disclosure to health care providers among urban and non-urban southern lesbians. Women Health. 2013;53:41-55.

10. Oladeru OT et al. Breast and cervical cancer screening disparities in transgender people. Am J Clin Oncol. 2022;45:116-21.

11. Vinsard DG et al. Healthcare providers’ perspectives on anoreceptive intercourse in sexual and gender minorities with ileal pouch anal anastomosis. Digestive Disease Week (DDW). Chicago, IL, 2023.

12. Ghusn W et al. Social determinants of health in LGBTQIA+ patients with inflammatory bowel disease. American College of Gastroenterology (ACG). Charlotte, NC, 2022.

13. Grasman ME et al. Neovaginal sparing in a transgender woman with ulcerative colitis. Clin Gastroenterol Hepatol. 2016;14:e73-4.

14. Prevention CfDCa. Lesbian, Gay, Bisexual, and Transgender Health — https://www.cdc.gov/lgbthealth/index.htm.

15. Institute TF. National LGBTQIA+ Health Education Center — https://www.lgbtqiahealtheducation.org/.

16. Services UDoHaH. LGBTQI+ Resources — https://www.hhs.gov/programs/topic-sites/lgbtqi/resources/index.html.

Cases

Patient 1: 55-year-old cis-male, who identifies as gay, has ulcerative colitis that has been refractory to multiple biologic therapies. His provider recommends a total proctocolectomy with ileal pouch anal anastomosis (TPC with IPAA), but the patient has questions regarding sexual function following surgery. Specifically, he is wondering when, or if, he can resume receptive anal intercourse. How would you counsel him?

Patient 2: 25-year-old, trans-female, status-post vaginoplasty with use of sigmoid colon and with well-controlled ulcerative colitis, presents with vaginal discharge, weight loss, and rectal bleeding. How do you explain what has happened to her? During your discussion, she also asks you why her chart continues to use her “dead name.” How do you respond?

Patient 3: 32-year-old, cis-female, G2P2, who identifies as a lesbian, has active ulcerative colitis. She wants to discuss medical or surgical therapy and future pregnancies. How would you counsel her?

Many gastroenterologists would likely know how to address patient 3’s concerns, but the concerns of patients 1 and 2 often go unaddressed or dismissed. There is a paucity of literature to help guide the care of LGBTQ+ individuals with IBD. Numerous studies and surveys have been conducted on patients with inflammatory bowel disease (IBD), but the focus of these studies has always been through a heteronormative cisgender lens. The focus of many studies is on fertility or sexual health and function in cisgender, heteronormative individuals.^1-3 In the last few years, however, there has been increasing awareness of the health disparities, stigma, and discrimination that sexual and gender minorities (SGM) experience.^4-6 For the purposes of this discussion, individuals within the lesbian, gay, bisexual, transgender, queer/questioning, intersex, and asexual (LGBTQIA+) community will be referred to as SGM. We recognize that even this exhaustive listing above does not acknowledge the full spectrum of diversity within the SGM community.

Clinical Care/Competency for SGM with IBD is Lacking

Almost 10% of the US population identifies as some form of SGM, and that number can be higher within the younger generations.⁴ SGM patients tend to delay or avoid seeking health care due to concern for provider mistreatment or lack of regard for their individual concerns. Additionally, there are several gaps in clinical knowledge about caring for SGM individuals. Little is known regarding the incidence or prevalence of IBD in SGM populations, but it is perceived to be similar to cisgender heterosexual individuals. Furthermore, as Newman et al. highlighted in their systematic review published in May 2023, there is a lack of guidance regarding sexual activity in the setting of IBD in SGM individuals.⁵ There is also a significant lack of knowledge on the impact of gender-affirming care on the natural history and treatments of IBD in transgender and gender non-conforming (TGNC) individuals. This can impact providers’ comfort and competence in caring for TGNC individuals.

Mayo Clinic

Another important point to make is that the SGM community still faces discrimination due to sexual orientation or gender identity to this day, which impacts the quality and delivery of their care.⁷ Culturally-competent care should include care that is free from stigma, implicit and explicit biases, and discrimination. In 2011, an Institute of Medicine report documented, among other issues, provider discomfort in delivering care to SGM patients.⁸ While SGM individuals prefer a provider who acknowledges their sexual orientation and gender identity and treats them with the dignity and respect they deserve, many SGM individuals share valid concerns regarding their safety, which impact their desire to disclose their identity to health care providers.⁹ This certainly can have an impact on the quality of care they receive, including important health maintenance milestones and cancer screenings.¹⁰

An internal survey at our institution of providers (nurses, physician assistants, surgeons, and physicians) found that among 85 responders, 70% have cared for SGM who have undergone TPC with ileal pouch anal anastomosis (IPAA). Of these, 75% did not ask about sexual orientation or practices before pouch formation (though almost all of them agreed it would be important to ask). A total of 55% were comfortable in discussing SGM-related concerns; 53% did not feel comfortable discussing sexual orientation or practices; and in particular when it came to anoreceptive intercourse (ARI), 73% did not feel confident discussing recommendations.¹¹

All of these issues highlight the importance of developing curricula that focus on reducing implicit and explicit biases towards SGM individuals and increasing the competence of providers to take care of SGM individuals in a safe space.

Mayo Clinic

Additionally, it further justifies the need for ethical research that focuses on the needs of SGM individuals to guide evidence-based approaches to care. Given the implicit and explicit heterosexism and transphobia in society and many health care systems, Rainbows in Gastro was formed as an advocacy group for SGM patients, trainees, and staff in gastroenterology and hepatology.⁴

Research in SGM and IBD is lacking

There are additional needs for research in IBD and how it pertains to the needs of SGM individuals. Figure 1 highlights the lack of PubMed results for the search terms “IBD + LGBT,” “IBD + LGBTQ,” or “IBD + queer.” In contrast, the search terms “IBD + fertility” and “IBD + sexual dysfunction” generate many results. Even a systemic review conducted by Newman et al. of multiple databases in 2022 found only seven articles that demonstrated appropriately performed studies on SGM patients with IBD.⁵ This highlights the significant dearth of research in the realm of SGM health in IBD.

Newman and colleagues have recently published research considerations for SGM individuals. They highlighted the need to include understanding the “unique combination of psychosocial, biomedical, and legal experiences” that results in different needs and outcomes. There were several areas identified, including minority stress, which comes from existence of being SGM, especially as transgender individuals face increasing legal challenges in a variety of settings, not just healthcare.⁶ In a retrospective chart review investigating social determinants of health in SGM-IBD populations,¹² 36% of patients reported some level of social isolation, and almost 50% reported some level of stress. A total of 40% of them self-reported some perceived level of risk with respect to employment, and 17% reported depression. Given that this was a chart review and not a strict questionnaire, this study was certainly limited, and we would hypothesize that these numbers are therefore underestimating the true proportion of SGM-IBD patients who deal with employment concerns, social isolation, or psychological distress.

What Next? Back to the Patients

Circling back to our patients from the introduction, how would you counsel each of them? In patient 1’s case, we would inform him that pelvic surgery can increase the risk for sexual dysfunction, such as erectile dysfunction. He additionally would be advised during a staged TPC with IPAA, he may experience issues with body image. However, should he desire to participate in receptive anal intercourse after completion of his surgeries, the general recommendation would be to wait at least 6 months and with proven remission. It should further be noted that these are not formalized recommendations, only highlighting the need for more research and consensus on standards of care for SGM patients. He should finally be told that because he has ulcerative colitis, removal of the colon does not remove the risk for future intestinal involvement such as possible pouchitis.

In patient 2’s case, she is likely experiencing diversion vaginitis related to use of her colon for her neo-vagina. She should undergo colonoscopy and vaginoscopy in addition to standard work-up for her known ulcerative colitis.¹³ Management should be done in a multidisciplinary approach between the IBD provider, gynecologist, and gender-affirming provider. The electronic medical record should be updated to reflect the patient’s preferred name, pronouns, and gender identity, and her medical records, including automated clinical reports, should be updated accordingly.

As for patient 3, she would be counseled according to well-documented guidelines on pregnancy and IBD, including risks of medications (such as Jak inhibitors or methotrexate) versus the risk of uncontrolled IBD during pregnancy.¹

Regardless of a patient’s gender identity or sexual orientation, patient-centered, culturally competent, and sensitive care should be provided. At Mayo Clinic in Rochester, we started one of the first Pride in IBD Clinics, which focuses on the care of SGM individuals with IBD. Our focus is to address the needs of patients who belong to the SGM community in a wholistic approach within a safe space (https://www.youtube.com/watch?v=pYa_zYaCA6M; https://www.mayoclinic.org/departments-centers/inflammatory-bowel-disease-clinic/overview/ovc-20357763). Our process of developing the clinic included training all staff on proper communication and cultural sensitivity for the SGM community.

Dr. Chiang and Dr. Chedid are both in the Division of Gastroenterology and Hepatology, Mayo Clinic, Rochester, Minnesota. Dr. Chedid is also with the Robert D. and Patricia E. Kern Center for the Science of Health Care Delivery, Mayo Clinic. Neither of the authors have any relevant conflicts of interest. They are on X, formerly Twitter: @dr_davidchiang , @VictorChedidMD .

CITATIONS

1. Mahadevan U et al. Inflammatory bowel disease in pregnancy clinical care pathway: A report from the American Gastroenterological Association IBD Parenthood Project Working Group. Gastroenterology. 2019;156:1508-24.

2. Pires F et al. A survey on the impact of IBD in sexual health: Into intimacy. Medicine (Baltimore). 2022;101:e32279.

3. Mules TC et al. The impact of disease activity on sexual and erectile dysfunction in patients with inflammatory bowel disease. Inflamm Bowel Dis. 2023;29:1244-54.

4. Duong N et al. Overcoming disparities for sexual and gender minority patients and providers in gastroenterology and hepatology: Introduction to Rainbows in Gastro. Lancet Gastroenterol Hepatol. 2023;8:299-301.

5. Newman KL et al. A systematic review of inflammatory bowel disease epidemiology and health outcomes in sexual and gender minority individuals. Gastroenterology. 2023;164:866-71.

6. Newman KL et al. Research considerations in Digestive and liver disease in transgender and gender-diverse populations. Gastroenterology. 2023;165:523-28 e1.

7. Velez C et al. Digestive health in sexual and gender minority populations. Am J Gastroenterol. 2022;117:865-75.

8. Medicine Io. Washington (DC): The National Academies Press, 2011.

9. Austin EL. Sexual orientation disclosure to health care providers among urban and non-urban southern lesbians. Women Health. 2013;53:41-55.

10. Oladeru OT et al. Breast and cervical cancer screening disparities in transgender people. Am J Clin Oncol. 2022;45:116-21.

11. Vinsard DG et al. Healthcare providers’ perspectives on anoreceptive intercourse in sexual and gender minorities with ileal pouch anal anastomosis. Digestive Disease Week (DDW). Chicago, IL, 2023.

12. Ghusn W et al. Social determinants of health in LGBTQIA+ patients with inflammatory bowel disease. American College of Gastroenterology (ACG). Charlotte, NC, 2022.

13. Grasman ME et al. Neovaginal sparing in a transgender woman with ulcerative colitis. Clin Gastroenterol Hepatol. 2016;14:e73-4.

14. Prevention CfDCa. Lesbian, Gay, Bisexual, and Transgender Health — https://www.cdc.gov/lgbthealth/index.htm.

15. Institute TF. National LGBTQIA+ Health Education Center — https://www.lgbtqiahealtheducation.org/.

16. Services UDoHaH. LGBTQI+ Resources — https://www.hhs.gov/programs/topic-sites/lgbtqi/resources/index.html.

Introduction

Inflammatory bowel disease (IBD) is a chronic, relapsing and remitting disorder that is becoming increasingly prevalent worldwide.¹ Despite major advances in this area, many patients with moderate to severe IBD do not achieve disease remission with immunosuppressive therapy.² Dysplasia and fibrostenosis are two common consequences of uncontrolled chronic inflammation and these structural complications are often the primary reasons for surgical interventions.³ While there is certainly a time and a place for surgery in IBD, this approach is invasive and postoperative recrudescence of disease is common.⁴ Moreover patients with complex surgical or medical histories may not make optimal surgical candidates.

Thanks to advancements in a variety of endoscopic technologies, nonoperative therapies are now available and provide a solution for patients who would otherwise fall outside of conventional treatment options. Over the last several years, applications of endoscopic therapies in IBD have been gaining traction and the need for these therapies is expected to continue to rise over time. As such, understanding the domains of available endoscopic options in IBD is important for the modern-day gastroenterologist. In this article, we will discuss some of the recent advancements in endoscopic therapies for IBD and how we may position these in clinical practice.
 

Protecting against colitis dysplasia and colon cancer

IBD is a risk factor for colorectal cancer because of the dysplasia-carcinoma sequence arising from chronic colitis. Endoscopic resection is the first-line treatment for conventional colitis-associated dysplasia (CAD).^5,6 However, larger or complex lesions may not have been previously amenable to this organ-preserving approach. The application of newer techniques has extended the indication for endoscopic resection to include most CAD lesions, as an alternative to proctocolectomy. Endoscopic mucosal resection (EMR) is the most commonly used technique and its outcomes for CAD greater than 2 cm have been excellent (Figure 1).⁷ However, employing EMR for lesions greater than 2 cm in size may require piecemeal resection and this has been associated with a small risk of local recurrence.⁸ Endoscopic submucosal dissection (ESD) is an alternate method of endoscopic tissue resection that can reliably achieve en bloc (single specimen) resections even in larger lesions.⁹

Courtesy Dr. Genere and colleagues

Restoring gastrointestinal tract transit

Crohn’s strictures may lead to acute intestinal obstructions or facilitate the onset of penetrating disease, such as fistula formation or abscess. These strictures are often characterized by a combination of inflammation and layered fibrosis, which requires the application of medical therapies alongside structural remodeling to successfully manage. Not all strictures may be clinically overt due to variances in visceral sensitivity, yet experts believe that treatment of all strictures should be considered to avoid occurrence of delayed complications.¹⁴ Endoscopic balloon dilation (EBD) is a well-established treatment for Crohn’s strictures up to 4-5 cm in length (Figure 2). This treatment involves inflating a balloon within the narrowed section of intestine, thereby stretching and disrupting the layered fibrotic bands to widen the stricture. EBD improves symptoms 70% of the time and successfully avoids the medium-term need for surgery in most, although it often requires repeat endoscopic procedures.¹⁵ In fact, up to 74% of patients will require repeat dilation over 2 years and 43% will require salvage surgery after EBD.¹⁶

Courtesy Dr. Genere and colleagues

The future for endoscopic therapy is bright

Structural complications of IBD are common and can pose a significant detriment to quality of life and general well-being for patients. From mucosal resection of CAD to surgery-sparing therapies for intestinal strictures, endoscopic therapies are valuable and effective options for managing disease-related sequelae within the scope of interventional IBD practice. We can expect the availability of these options to grow as the scope of endoscopy training incorporates principles of interventional IBD, along with the concurrent development of additional therapeutic applications beyond the categories discussed here (including perianal disease, fistulas, and abscess formation). It is noteworthy to mention that while endoscopic therapies are separate treatment modalities, should not be considered mutually exclusive; endotherapies are best viewed as a complement to existing medical and surgical approaches. Thus, Interventional IBD endoscopy can serve as an integral part of the multidisciplinary IBD framework to provide comprehensive care for our patients with IBD.

Juan Reyes Genere, MD, is an assistant professor of medicine in gastroenterology at Washington University in St. Louis. He served as the corresponding author of this article. Michael Rubeiz, MD, is a physician in the internal medicine residency program at Washington University in St. Louis. Kemmian Johnson, MD, MPH, is a gastroenterologist at Washington University in St. Louis specializing in inflammatory bowel disease. Dr. Genere is a consultant for Edulis Therapeutics. Dr. Rubeiz and Dr. Johnson had no personal or financial conflicts of interest. Dr. Johnson can be reached on Instagram @KJ.1906; Dr. Rubeiz is on X @MichaelRubeiz1 and Dr. Genere can be reached via X @JPGenereMD.

References

1. Ng SC et al. Lancet. 2017;390(10114):2769-78.

2. Gordon JP et al. Eur J Gastroenterol Hepatol. 2015;27(7):804-12.

3. Sica GS and Biancone L. World J Gastroenterol. 2013;19(16):2445-8.

4. Iborra M et al. Gastroenterol Rep (Oxf). 2019;7(6):411-8.

5. Annese V et al. J Crohns Colitis. 2013;7(12):982-1018.

6. Laine L et al. Gastrointest Endosc. 2015;81(3):489-501.e426.

7. Mohan BP et al. Gastrointest Endosc. 2021;93(1):59-67.e10.

8. Briedigkeit A et al. World J Gastrointest Endosc. 2016;8(5):276-81.

9. Manta R et al. J Crohns Colitis. 2021;15(1):165-8.

10. Mohapatra S et al. Endosc Int Open. 2022;10(5):E593-601.

11. Ngamruengphong S et al. Endosc Int Open. 2022;10(4):E354-60.

12. Baker G et al. Cureus. 2022 May 3;14(5):e24688.

13. Yadav S et al. Endosc Int Open. 2019;7(8):E994-1001.

14. Schwartz DA. Gastrointestinal Endoscopy. 2023;97(5):974-6.

15. Morar PS et al. Aliment Pharmacol Ther. 2015;42(10):1137-48.

16. Bettenworth D et al. Inflamm Bowel Dis. 2017;23(1):133-42.

17. Lan N and Shen B. Inflamm Bowel Dis. 2018;24(4):897-907.

18. Loras C et al. Lancet Gastroenterol Hepatol. 2022;7(4):332-41.

19. Genere JR et al. Lancet Gastroenterol Hepatol. 2022;7(6):503-4.

Introduction

Inflammatory bowel disease (IBD) is a chronic, relapsing and remitting disorder that is becoming increasingly prevalent worldwide.¹ Despite major advances in this area, many patients with moderate to severe IBD do not achieve disease remission with immunosuppressive therapy.² Dysplasia and fibrostenosis are two common consequences of uncontrolled chronic inflammation and these structural complications are often the primary reasons for surgical interventions.³ While there is certainly a time and a place for surgery in IBD, this approach is invasive and postoperative recrudescence of disease is common.⁴ Moreover patients with complex surgical or medical histories may not make optimal surgical candidates.

Thanks to advancements in a variety of endoscopic technologies, nonoperative therapies are now available and provide a solution for patients who would otherwise fall outside of conventional treatment options. Over the last several years, applications of endoscopic therapies in IBD have been gaining traction and the need for these therapies is expected to continue to rise over time. As such, understanding the domains of available endoscopic options in IBD is important for the modern-day gastroenterologist. In this article, we will discuss some of the recent advancements in endoscopic therapies for IBD and how we may position these in clinical practice.
 

Protecting against colitis dysplasia and colon cancer

IBD is a risk factor for colorectal cancer because of the dysplasia-carcinoma sequence arising from chronic colitis. Endoscopic resection is the first-line treatment for conventional colitis-associated dysplasia (CAD).^5,6 However, larger or complex lesions may not have been previously amenable to this organ-preserving approach. The application of newer techniques has extended the indication for endoscopic resection to include most CAD lesions, as an alternative to proctocolectomy. Endoscopic mucosal resection (EMR) is the most commonly used technique and its outcomes for CAD greater than 2 cm have been excellent (Figure 1).⁷ However, employing EMR for lesions greater than 2 cm in size may require piecemeal resection and this has been associated with a small risk of local recurrence.⁸ Endoscopic submucosal dissection (ESD) is an alternate method of endoscopic tissue resection that can reliably achieve en bloc (single specimen) resections even in larger lesions.⁹

Courtesy Dr. Genere and colleagues

Restoring gastrointestinal tract transit

Crohn’s strictures may lead to acute intestinal obstructions or facilitate the onset of penetrating disease, such as fistula formation or abscess. These strictures are often characterized by a combination of inflammation and layered fibrosis, which requires the application of medical therapies alongside structural remodeling to successfully manage. Not all strictures may be clinically overt due to variances in visceral sensitivity, yet experts believe that treatment of all strictures should be considered to avoid occurrence of delayed complications.¹⁴ Endoscopic balloon dilation (EBD) is a well-established treatment for Crohn’s strictures up to 4-5 cm in length (Figure 2). This treatment involves inflating a balloon within the narrowed section of intestine, thereby stretching and disrupting the layered fibrotic bands to widen the stricture. EBD improves symptoms 70% of the time and successfully avoids the medium-term need for surgery in most, although it often requires repeat endoscopic procedures.¹⁵ In fact, up to 74% of patients will require repeat dilation over 2 years and 43% will require salvage surgery after EBD.¹⁶

Courtesy Dr. Genere and colleagues

The future for endoscopic therapy is bright

Structural complications of IBD are common and can pose a significant detriment to quality of life and general well-being for patients. From mucosal resection of CAD to surgery-sparing therapies for intestinal strictures, endoscopic therapies are valuable and effective options for managing disease-related sequelae within the scope of interventional IBD practice. We can expect the availability of these options to grow as the scope of endoscopy training incorporates principles of interventional IBD, along with the concurrent development of additional therapeutic applications beyond the categories discussed here (including perianal disease, fistulas, and abscess formation). It is noteworthy to mention that while endoscopic therapies are separate treatment modalities, should not be considered mutually exclusive; endotherapies are best viewed as a complement to existing medical and surgical approaches. Thus, Interventional IBD endoscopy can serve as an integral part of the multidisciplinary IBD framework to provide comprehensive care for our patients with IBD.

Juan Reyes Genere, MD, is an assistant professor of medicine in gastroenterology at Washington University in St. Louis. He served as the corresponding author of this article. Michael Rubeiz, MD, is a physician in the internal medicine residency program at Washington University in St. Louis. Kemmian Johnson, MD, MPH, is a gastroenterologist at Washington University in St. Louis specializing in inflammatory bowel disease. Dr. Genere is a consultant for Edulis Therapeutics. Dr. Rubeiz and Dr. Johnson had no personal or financial conflicts of interest. Dr. Johnson can be reached on Instagram @KJ.1906; Dr. Rubeiz is on X @MichaelRubeiz1 and Dr. Genere can be reached via X @JPGenereMD.

References

1. Ng SC et al. Lancet. 2017;390(10114):2769-78.

2. Gordon JP et al. Eur J Gastroenterol Hepatol. 2015;27(7):804-12.

3. Sica GS and Biancone L. World J Gastroenterol. 2013;19(16):2445-8.

4. Iborra M et al. Gastroenterol Rep (Oxf). 2019;7(6):411-8.

5. Annese V et al. J Crohns Colitis. 2013;7(12):982-1018.

6. Laine L et al. Gastrointest Endosc. 2015;81(3):489-501.e426.

7. Mohan BP et al. Gastrointest Endosc. 2021;93(1):59-67.e10.

8. Briedigkeit A et al. World J Gastrointest Endosc. 2016;8(5):276-81.

9. Manta R et al. J Crohns Colitis. 2021;15(1):165-8.

10. Mohapatra S et al. Endosc Int Open. 2022;10(5):E593-601.

11. Ngamruengphong S et al. Endosc Int Open. 2022;10(4):E354-60.

12. Baker G et al. Cureus. 2022 May 3;14(5):e24688.

13. Yadav S et al. Endosc Int Open. 2019;7(8):E994-1001.

14. Schwartz DA. Gastrointestinal Endoscopy. 2023;97(5):974-6.

15. Morar PS et al. Aliment Pharmacol Ther. 2015;42(10):1137-48.

16. Bettenworth D et al. Inflamm Bowel Dis. 2017;23(1):133-42.

17. Lan N and Shen B. Inflamm Bowel Dis. 2018;24(4):897-907.

18. Loras C et al. Lancet Gastroenterol Hepatol. 2022;7(4):332-41.

19. Genere JR et al. Lancet Gastroenterol Hepatol. 2022;7(6):503-4.

Introduction

Inflammatory bowel disease (IBD) is a chronic, relapsing and remitting disorder that is becoming increasingly prevalent worldwide.¹ Despite major advances in this area, many patients with moderate to severe IBD do not achieve disease remission with immunosuppressive therapy.² Dysplasia and fibrostenosis are two common consequences of uncontrolled chronic inflammation and these structural complications are often the primary reasons for surgical interventions.³ While there is certainly a time and a place for surgery in IBD, this approach is invasive and postoperative recrudescence of disease is common.⁴ Moreover patients with complex surgical or medical histories may not make optimal surgical candidates.

Thanks to advancements in a variety of endoscopic technologies, nonoperative therapies are now available and provide a solution for patients who would otherwise fall outside of conventional treatment options. Over the last several years, applications of endoscopic therapies in IBD have been gaining traction and the need for these therapies is expected to continue to rise over time. As such, understanding the domains of available endoscopic options in IBD is important for the modern-day gastroenterologist. In this article, we will discuss some of the recent advancements in endoscopic therapies for IBD and how we may position these in clinical practice.
 

Protecting against colitis dysplasia and colon cancer

IBD is a risk factor for colorectal cancer because of the dysplasia-carcinoma sequence arising from chronic colitis. Endoscopic resection is the first-line treatment for conventional colitis-associated dysplasia (CAD).^5,6 However, larger or complex lesions may not have been previously amenable to this organ-preserving approach. The application of newer techniques has extended the indication for endoscopic resection to include most CAD lesions, as an alternative to proctocolectomy. Endoscopic mucosal resection (EMR) is the most commonly used technique and its outcomes for CAD greater than 2 cm have been excellent (Figure 1).⁷ However, employing EMR for lesions greater than 2 cm in size may require piecemeal resection and this has been associated with a small risk of local recurrence.⁸ Endoscopic submucosal dissection (ESD) is an alternate method of endoscopic tissue resection that can reliably achieve en bloc (single specimen) resections even in larger lesions.⁹

Courtesy Dr. Genere and colleagues

Restoring gastrointestinal tract transit

Crohn’s strictures may lead to acute intestinal obstructions or facilitate the onset of penetrating disease, such as fistula formation or abscess. These strictures are often characterized by a combination of inflammation and layered fibrosis, which requires the application of medical therapies alongside structural remodeling to successfully manage. Not all strictures may be clinically overt due to variances in visceral sensitivity, yet experts believe that treatment of all strictures should be considered to avoid occurrence of delayed complications.¹⁴ Endoscopic balloon dilation (EBD) is a well-established treatment for Crohn’s strictures up to 4-5 cm in length (Figure 2). This treatment involves inflating a balloon within the narrowed section of intestine, thereby stretching and disrupting the layered fibrotic bands to widen the stricture. EBD improves symptoms 70% of the time and successfully avoids the medium-term need for surgery in most, although it often requires repeat endoscopic procedures.¹⁵ In fact, up to 74% of patients will require repeat dilation over 2 years and 43% will require salvage surgery after EBD.¹⁶

Courtesy Dr. Genere and colleagues

The future for endoscopic therapy is bright

Structural complications of IBD are common and can pose a significant detriment to quality of life and general well-being for patients. From mucosal resection of CAD to surgery-sparing therapies for intestinal strictures, endoscopic therapies are valuable and effective options for managing disease-related sequelae within the scope of interventional IBD practice. We can expect the availability of these options to grow as the scope of endoscopy training incorporates principles of interventional IBD, along with the concurrent development of additional therapeutic applications beyond the categories discussed here (including perianal disease, fistulas, and abscess formation). It is noteworthy to mention that while endoscopic therapies are separate treatment modalities, should not be considered mutually exclusive; endotherapies are best viewed as a complement to existing medical and surgical approaches. Thus, Interventional IBD endoscopy can serve as an integral part of the multidisciplinary IBD framework to provide comprehensive care for our patients with IBD.

Juan Reyes Genere, MD, is an assistant professor of medicine in gastroenterology at Washington University in St. Louis. He served as the corresponding author of this article. Michael Rubeiz, MD, is a physician in the internal medicine residency program at Washington University in St. Louis. Kemmian Johnson, MD, MPH, is a gastroenterologist at Washington University in St. Louis specializing in inflammatory bowel disease. Dr. Genere is a consultant for Edulis Therapeutics. Dr. Rubeiz and Dr. Johnson had no personal or financial conflicts of interest. Dr. Johnson can be reached on Instagram @KJ.1906; Dr. Rubeiz is on X @MichaelRubeiz1 and Dr. Genere can be reached via X @JPGenereMD.

References

1. Ng SC et al. Lancet. 2017;390(10114):2769-78.

2. Gordon JP et al. Eur J Gastroenterol Hepatol. 2015;27(7):804-12.

3. Sica GS and Biancone L. World J Gastroenterol. 2013;19(16):2445-8.

4. Iborra M et al. Gastroenterol Rep (Oxf). 2019;7(6):411-8.

5. Annese V et al. J Crohns Colitis. 2013;7(12):982-1018.

6. Laine L et al. Gastrointest Endosc. 2015;81(3):489-501.e426.

7. Mohan BP et al. Gastrointest Endosc. 2021;93(1):59-67.e10.

8. Briedigkeit A et al. World J Gastrointest Endosc. 2016;8(5):276-81.

9. Manta R et al. J Crohns Colitis. 2021;15(1):165-8.

10. Mohapatra S et al. Endosc Int Open. 2022;10(5):E593-601.

11. Ngamruengphong S et al. Endosc Int Open. 2022;10(4):E354-60.

12. Baker G et al. Cureus. 2022 May 3;14(5):e24688.

13. Yadav S et al. Endosc Int Open. 2019;7(8):E994-1001.

14. Schwartz DA. Gastrointestinal Endoscopy. 2023;97(5):974-6.

15. Morar PS et al. Aliment Pharmacol Ther. 2015;42(10):1137-48.

16. Bettenworth D et al. Inflamm Bowel Dis. 2017;23(1):133-42.

17. Lan N and Shen B. Inflamm Bowel Dis. 2018;24(4):897-907.

18. Loras C et al. Lancet Gastroenterol Hepatol. 2022;7(4):332-41.

19. Genere JR et al. Lancet Gastroenterol Hepatol. 2022;7(6):503-4.

Introduction

Historically, the role of endoscopy in hepatology has been limited to intraluminal and bile duct interventions, primarily for the management of varices and biliary strictures. Recently, endoscopic ultrasound (EUS) has broadened the range of endoscopic treatment by enabling transluminal access to the liver parenchyma and associated vasculature. In this review, we will address recent advances in the expanding field of endohepatology.

Endoscopic-ultrasound guided liver biopsy

Liver biopsies are a critical tool in the diagnostic evaluation and management of patients with liver disease. Conventional approaches for obtaining liver tissue have been most commonly through the percutaneous or vascular approaches. In 2007, the first EUS-guided liver biopsy (EUS-LB) was described.¹ EUS-LB is performed by advancing a line-array echoendoscope to the duodenal bulb to access the right lobe of the liver or proximal stomach to sample the left lobe. Doppler is first used to identify a pathway with few intervening vessels. Then a 19G or 20G needle is passed and slowly withdrawn to capture tissue (Figure 1). Careful evaluation with Doppler ultrasound to evaluate for bleeding is recommended after EUS-LB and if persistent, a small amount of clot may be reinjected as a blood or “Chang” patch akin to technique to control oozing postlumbar puncture.²

Jennifer Phan, MD

While large prospective studies are needed to compare the methods, it appears that specimen adequacy acquired via EUS-LB are comparable to percutaneous and transjugular approaches.^3-5 Utilization of specific needle types and suction may optimize samples. Namely, 19G needles may provide better samples than smaller sizes and contemporary fine-needle biopsy needles with Franseen tips are superior to conventional spring-loaded cutting needles and fork tip needles.^6-8 The use of dry suction has been shown to increase the yield of tissue, but at the expense of increased bloodiness. Wet suction, which involves the presence of fluid, rather than air, in the needle lumen to lubricate and improve transmission of negative pressure to the needle tip, is the preferred technique for EUS-LB given improvement in the likelihood of intact liver biopsy cores and increased specimen adequacy.⁹

There are several advantages to EUS-LB (Table 1). When compared with percutaneous liver biopsy (PC-LB) and transjugular liver biopsy (TJ-LB), EUS-LB is uniquely able to access both liver lobes in a single setting, which minimizes sampling error.³ EUS-LB may also have an advantage in sampling focal liver lesions given the close proximity of the transducer to the liver.¹⁰ Another advantage over PC-LB is that EUS-LB can be performed in patients with a large body habitus. Additionally, EUS-LB is better tolerated than PC-LB, with less postprocedure pain and shorter postprocedure monitoring time.^4,5
 

Dr. James Buxbaum and Dr. Aileen Bui

Rates of adverse events appear to be similar between the three methods. Similar to PC-LB, EUS-LB requires capsular puncture, which can lead to intraperitoneal hemorrhage. Therefore, TJ-LB is preferred in patients with significant coagulopathy. While small ascites is not an absolute contraindication for EUS-LB, large ascites can obscure a safe window from the proximal stomach or duodenum to the liver, and thus TJLB is also preferred in these patients.¹¹ Given its relative novelty and logistic challenges, other disadvantages of EUS-LB include limited provider availability and increased cost, especially compared with PC-LB. The most significant limitation is that it requires moderate or deep sedation, as opposed to local anesthetics. However, if there is another indication for endoscopy (that is, variceal screening), then “one-stop shop” procedures including EUS-LB may be more convenient and cost-effective than traditional methods. Nevertheless, rigorous comparative studies are needed.
 

EUS-guided portal pressure gradient measurement

The presence of clinically significant portal hypertension (CSPH), defined as hepatic venous pressure gradient (HVPG) greater than or equal to 10 is a potent predictor of decompensation. There is growing evidence to support the use of beta-blockers to mitigate this risk.¹² Therefore, early identification of patients with CSPH has important diagnostic and therapeutic implications. The current gold standard for diagnosing CSPH is with wedged HVPG measurements performed by interventional radiology.

Since its introduction in 2016, EUS-guided portal pressure gradient measurement (EUS-PPG) has emerged as an alternative to wedged HVPG.^13,14 Using a linear echoendoscope, the portal vein is directly accessed with a 25G fine-needle aspiration needle, and three direct measurements are taken using a compact manometer to determine the mean pressure. The hepatic vein, or less commonly the inferior vena cava, pressure is also measured. The direct measurement of portal pressure provides a significant advantage of EUS-PPG over HVPG in patients with presinusoidal and prehepatic portal hypertension. Wedged HVPG, which utilizes the difference between the wedged and free hepatic venous pressure to indirectly estimate the portal venous pressure gradient, yields erroneously low gradients in patients with noncirrhotic portal hypertension.¹⁵ An additional advantage of EUS-PPG is that it obviates the need for a central venous line placement, which is associated with thrombosis and, in rare cases, air embolus.¹⁶

Observational studies indicate that EUS-PPG has a high degree of consistency with HVPG measurements and a strong correlation between other clinical findings of portal hyper-tension including esophageal varices and thrombocytopenia.^13,14 Nevertheless, EUS-PPG is performed under moderate or deep sedation which may impact HVPG measurements.¹⁷ In addition, the real-world application of EUS-PPG measurement on clinical care is undefined, but it is the topic of an ongoing clinical trial (ClinicalTrials.gov – NCT05357599).
 

EUS-guided interventions of gastric varices

Compared with esophageal varices, current approaches to the treatment and prophylaxis of gastric varices are more controversial.¹⁸ The most common approach to bleeding gastric varices in the United States is the placement of a transjugular intrahepatic portosystemic shunt (TIPS). Nevertheless, in addition to risks associated with central venous line placement, 5%-35% of individuals develop hepatic encephalopathy after TIPS and ischemic acute liver failure can occur in rare situations.¹⁹ Cyanoacrylate (CYA) glue injection is the recommended first-line endoscopic therapy for the treatment of bleeding gastric varices, but use has not been widely adopted in the United States because of a lack of an approved Food and Drug Administration CYA formulation, limited expertise, and risk of serious complications. In particular systemic embolization may result in pulmonary or cerebral infarct.^12,18 EUS-guided interventions have been developed to mitigate these safety concerns. EUS-guided coil embolization can be performed, either alone or in combination with CYA injection.²⁰ In the latter approach it acts as a scaffold to prevent migration of the glue bolus. Doppler assessment enables direct visualization of the gastric varix for identification of feeder vessels, more controlled deployment of hemostatic agents, and real-time confirmation of varix obliteration. Fluoroscopy can be used as an adjunct.

EUS-guided interventions in the management of gastric varices appear to be effective and superior to CYA injection under direct endoscopic visualization with improved likelihood of obliteration and lower rebleeding rates, without increase in adverse events.²¹ Additionally, EUS-guided combination therapy improves technical outcomes and reduces adverse events relative to EUS-guided coil or EUS-guided glue injection therapy alone.^21-23 Nevertheless, large-scale prospective trials are needed to determine whether EUS-guided interventions should be considered over TIPS. The role of EUS-guided interventions as primary prophylaxis to prevent bleeding from large gastric varices also requires additional study.²⁴

Future directions

Endohepatology has shown promise in its ability to consolidate the evaluation and treatment of patients with liver disease with the goal of optimizing care and increasing efficiency. In addition to new endoscopic procedures to optimize liver biopsy, portal pressure measurement, and gastric variceal treatment, there are a number of emerging technologies including EUS-guided liver elastography, portal venous sampling, liver tumor chemoembolization, and intrahepatic portosystemic shunts.²⁵ However, the practice of endohepatology faces a number of challenges before widespread adoption, including limited provider expertise and institutional availability. Additionally, more robust, multicenter outcomes and cost-effective analyses comparing these novel procedures with traditional approaches are needed to define their clinical impact.

Dr. Bui is a fellow in gastroenterology in the division of gastroenterology and hepatology, University of Southern California, Los Angeles. Dr. Buxbaum is associate professor of medicine (clinical scholar) in the division of gastroenterology and hepatology, University of Southern California. Dr. Buxbaum is a consultant for Cook Medical, Boston Scientific, and Olympus. Dr. Bui has no disclosures.

References

1. Mathew A. Am J Gastroenterol. 2007;102(10):2354-5.

2. Sowa P et al. VideoGIE. 2021;6(11):487-8.

3. Pineda JJ et al. Gastrointest Endosc. 2016;83(2):360-5.

4. Ali AH et al. J Ultrasound. 2020;23(2):157-67.

5. Shuja A et al. Dig Liver Dis. 2019;51(6):826-30.

6. Schulman AR et al. Gastrointest Endosc. 2017;85(2):419-26.

7. DeWitt J et al. Endosc Int Open. 2015;3(5):E471-8.

8. Aggarwal SN et al. Gastrointest Endosc. 2021;93(5):1133-8.

9. Mok SRS et al. Gastrointest Endosc. 2018;88(6):919-25.

10. Lee YN et al. J Gastroenterol Hepatol. 2015;30(7):1161-6.

11. Kalambokis G et al. J Hepatol. 2007;47(2):284-94.

12. de Franchis R et al. J Hepatol. 2022;76(4):959-74.

13. Choi AY et al. J Gastroenterol Hepatol. 2022;37(7):1373-9.

14. Zhang W et al. Gastrointest Endosc. 2021;93(3):565-72.

15. Seijo S et al. Dig Liver Dis. 2012;44(10):855-60.

16. Vesely TM. J Vasc Interv Radiol. 2001;12(11):1291-5.

17. Reverter E et al. Liver Int. 2014;34(1):16-25.

18. Henry Z et al. Clin Gastroenterol Hepatol. 2021;19(6):1098-107.e1091.

19. Ripamonti R et al. Semin Intervent Radiol. 2006;23(2):165-76.

20. Rengstorff DS and Binmoeller KF. Gastrointest Endosc. 2004;59(4):553-8.

21. Mohan BP et al. Endoscopy. 2020;52(4):259-67.

22. Robles-Medranda C et al. Endoscopy. 2020;52(4):268-75.

23. McCarty TR et al. Endosc Ultrasound. 2020;9(1):6-15.

24. Kouanda A et al. Gastrointest Endosc. 2021;94(2):291-6.

25. Bazarbashi AN et al. 2022;24(1):98-107.

Introduction

Historically, the role of endoscopy in hepatology has been limited to intraluminal and bile duct interventions, primarily for the management of varices and biliary strictures. Recently, endoscopic ultrasound (EUS) has broadened the range of endoscopic treatment by enabling transluminal access to the liver parenchyma and associated vasculature. In this review, we will address recent advances in the expanding field of endohepatology.

Endoscopic-ultrasound guided liver biopsy

Liver biopsies are a critical tool in the diagnostic evaluation and management of patients with liver disease. Conventional approaches for obtaining liver tissue have been most commonly through the percutaneous or vascular approaches. In 2007, the first EUS-guided liver biopsy (EUS-LB) was described.¹ EUS-LB is performed by advancing a line-array echoendoscope to the duodenal bulb to access the right lobe of the liver or proximal stomach to sample the left lobe. Doppler is first used to identify a pathway with few intervening vessels. Then a 19G or 20G needle is passed and slowly withdrawn to capture tissue (Figure 1). Careful evaluation with Doppler ultrasound to evaluate for bleeding is recommended after EUS-LB and if persistent, a small amount of clot may be reinjected as a blood or “Chang” patch akin to technique to control oozing postlumbar puncture.²

Jennifer Phan, MD

While large prospective studies are needed to compare the methods, it appears that specimen adequacy acquired via EUS-LB are comparable to percutaneous and transjugular approaches.^3-5 Utilization of specific needle types and suction may optimize samples. Namely, 19G needles may provide better samples than smaller sizes and contemporary fine-needle biopsy needles with Franseen tips are superior to conventional spring-loaded cutting needles and fork tip needles.^6-8 The use of dry suction has been shown to increase the yield of tissue, but at the expense of increased bloodiness. Wet suction, which involves the presence of fluid, rather than air, in the needle lumen to lubricate and improve transmission of negative pressure to the needle tip, is the preferred technique for EUS-LB given improvement in the likelihood of intact liver biopsy cores and increased specimen adequacy.⁹

There are several advantages to EUS-LB (Table 1). When compared with percutaneous liver biopsy (PC-LB) and transjugular liver biopsy (TJ-LB), EUS-LB is uniquely able to access both liver lobes in a single setting, which minimizes sampling error.³ EUS-LB may also have an advantage in sampling focal liver lesions given the close proximity of the transducer to the liver.¹⁰ Another advantage over PC-LB is that EUS-LB can be performed in patients with a large body habitus. Additionally, EUS-LB is better tolerated than PC-LB, with less postprocedure pain and shorter postprocedure monitoring time.^4,5
 

Dr. James Buxbaum and Dr. Aileen Bui

Rates of adverse events appear to be similar between the three methods. Similar to PC-LB, EUS-LB requires capsular puncture, which can lead to intraperitoneal hemorrhage. Therefore, TJ-LB is preferred in patients with significant coagulopathy. While small ascites is not an absolute contraindication for EUS-LB, large ascites can obscure a safe window from the proximal stomach or duodenum to the liver, and thus TJLB is also preferred in these patients.¹¹ Given its relative novelty and logistic challenges, other disadvantages of EUS-LB include limited provider availability and increased cost, especially compared with PC-LB. The most significant limitation is that it requires moderate or deep sedation, as opposed to local anesthetics. However, if there is another indication for endoscopy (that is, variceal screening), then “one-stop shop” procedures including EUS-LB may be more convenient and cost-effective than traditional methods. Nevertheless, rigorous comparative studies are needed.
 

EUS-guided portal pressure gradient measurement

The presence of clinically significant portal hypertension (CSPH), defined as hepatic venous pressure gradient (HVPG) greater than or equal to 10 is a potent predictor of decompensation. There is growing evidence to support the use of beta-blockers to mitigate this risk.¹² Therefore, early identification of patients with CSPH has important diagnostic and therapeutic implications. The current gold standard for diagnosing CSPH is with wedged HVPG measurements performed by interventional radiology.

Since its introduction in 2016, EUS-guided portal pressure gradient measurement (EUS-PPG) has emerged as an alternative to wedged HVPG.^13,14 Using a linear echoendoscope, the portal vein is directly accessed with a 25G fine-needle aspiration needle, and three direct measurements are taken using a compact manometer to determine the mean pressure. The hepatic vein, or less commonly the inferior vena cava, pressure is also measured. The direct measurement of portal pressure provides a significant advantage of EUS-PPG over HVPG in patients with presinusoidal and prehepatic portal hypertension. Wedged HVPG, which utilizes the difference between the wedged and free hepatic venous pressure to indirectly estimate the portal venous pressure gradient, yields erroneously low gradients in patients with noncirrhotic portal hypertension.¹⁵ An additional advantage of EUS-PPG is that it obviates the need for a central venous line placement, which is associated with thrombosis and, in rare cases, air embolus.¹⁶

Observational studies indicate that EUS-PPG has a high degree of consistency with HVPG measurements and a strong correlation between other clinical findings of portal hyper-tension including esophageal varices and thrombocytopenia.^13,14 Nevertheless, EUS-PPG is performed under moderate or deep sedation which may impact HVPG measurements.¹⁷ In addition, the real-world application of EUS-PPG measurement on clinical care is undefined, but it is the topic of an ongoing clinical trial (ClinicalTrials.gov – NCT05357599).
 

EUS-guided interventions of gastric varices

Compared with esophageal varices, current approaches to the treatment and prophylaxis of gastric varices are more controversial.¹⁸ The most common approach to bleeding gastric varices in the United States is the placement of a transjugular intrahepatic portosystemic shunt (TIPS). Nevertheless, in addition to risks associated with central venous line placement, 5%-35% of individuals develop hepatic encephalopathy after TIPS and ischemic acute liver failure can occur in rare situations.¹⁹ Cyanoacrylate (CYA) glue injection is the recommended first-line endoscopic therapy for the treatment of bleeding gastric varices, but use has not been widely adopted in the United States because of a lack of an approved Food and Drug Administration CYA formulation, limited expertise, and risk of serious complications. In particular systemic embolization may result in pulmonary or cerebral infarct.^12,18 EUS-guided interventions have been developed to mitigate these safety concerns. EUS-guided coil embolization can be performed, either alone or in combination with CYA injection.²⁰ In the latter approach it acts as a scaffold to prevent migration of the glue bolus. Doppler assessment enables direct visualization of the gastric varix for identification of feeder vessels, more controlled deployment of hemostatic agents, and real-time confirmation of varix obliteration. Fluoroscopy can be used as an adjunct.

EUS-guided interventions in the management of gastric varices appear to be effective and superior to CYA injection under direct endoscopic visualization with improved likelihood of obliteration and lower rebleeding rates, without increase in adverse events.²¹ Additionally, EUS-guided combination therapy improves technical outcomes and reduces adverse events relative to EUS-guided coil or EUS-guided glue injection therapy alone.^21-23 Nevertheless, large-scale prospective trials are needed to determine whether EUS-guided interventions should be considered over TIPS. The role of EUS-guided interventions as primary prophylaxis to prevent bleeding from large gastric varices also requires additional study.²⁴

Future directions

Endohepatology has shown promise in its ability to consolidate the evaluation and treatment of patients with liver disease with the goal of optimizing care and increasing efficiency. In addition to new endoscopic procedures to optimize liver biopsy, portal pressure measurement, and gastric variceal treatment, there are a number of emerging technologies including EUS-guided liver elastography, portal venous sampling, liver tumor chemoembolization, and intrahepatic portosystemic shunts.²⁵ However, the practice of endohepatology faces a number of challenges before widespread adoption, including limited provider expertise and institutional availability. Additionally, more robust, multicenter outcomes and cost-effective analyses comparing these novel procedures with traditional approaches are needed to define their clinical impact.

Dr. Bui is a fellow in gastroenterology in the division of gastroenterology and hepatology, University of Southern California, Los Angeles. Dr. Buxbaum is associate professor of medicine (clinical scholar) in the division of gastroenterology and hepatology, University of Southern California. Dr. Buxbaum is a consultant for Cook Medical, Boston Scientific, and Olympus. Dr. Bui has no disclosures.

References

1. Mathew A. Am J Gastroenterol. 2007;102(10):2354-5.

2. Sowa P et al. VideoGIE. 2021;6(11):487-8.

3. Pineda JJ et al. Gastrointest Endosc. 2016;83(2):360-5.

4. Ali AH et al. J Ultrasound. 2020;23(2):157-67.

5. Shuja A et al. Dig Liver Dis. 2019;51(6):826-30.

6. Schulman AR et al. Gastrointest Endosc. 2017;85(2):419-26.

7. DeWitt J et al. Endosc Int Open. 2015;3(5):E471-8.

8. Aggarwal SN et al. Gastrointest Endosc. 2021;93(5):1133-8.

9. Mok SRS et al. Gastrointest Endosc. 2018;88(6):919-25.

10. Lee YN et al. J Gastroenterol Hepatol. 2015;30(7):1161-6.

11. Kalambokis G et al. J Hepatol. 2007;47(2):284-94.

12. de Franchis R et al. J Hepatol. 2022;76(4):959-74.

13. Choi AY et al. J Gastroenterol Hepatol. 2022;37(7):1373-9.

14. Zhang W et al. Gastrointest Endosc. 2021;93(3):565-72.

15. Seijo S et al. Dig Liver Dis. 2012;44(10):855-60.

16. Vesely TM. J Vasc Interv Radiol. 2001;12(11):1291-5.

17. Reverter E et al. Liver Int. 2014;34(1):16-25.

18. Henry Z et al. Clin Gastroenterol Hepatol. 2021;19(6):1098-107.e1091.

19. Ripamonti R et al. Semin Intervent Radiol. 2006;23(2):165-76.

20. Rengstorff DS and Binmoeller KF. Gastrointest Endosc. 2004;59(4):553-8.

21. Mohan BP et al. Endoscopy. 2020;52(4):259-67.

22. Robles-Medranda C et al. Endoscopy. 2020;52(4):268-75.

23. McCarty TR et al. Endosc Ultrasound. 2020;9(1):6-15.

24. Kouanda A et al. Gastrointest Endosc. 2021;94(2):291-6.

25. Bazarbashi AN et al. 2022;24(1):98-107.

Introduction

Historically, the role of endoscopy in hepatology has been limited to intraluminal and bile duct interventions, primarily for the management of varices and biliary strictures. Recently, endoscopic ultrasound (EUS) has broadened the range of endoscopic treatment by enabling transluminal access to the liver parenchyma and associated vasculature. In this review, we will address recent advances in the expanding field of endohepatology.

Endoscopic-ultrasound guided liver biopsy

Liver biopsies are a critical tool in the diagnostic evaluation and management of patients with liver disease. Conventional approaches for obtaining liver tissue have been most commonly through the percutaneous or vascular approaches. In 2007, the first EUS-guided liver biopsy (EUS-LB) was described.¹ EUS-LB is performed by advancing a line-array echoendoscope to the duodenal bulb to access the right lobe of the liver or proximal stomach to sample the left lobe. Doppler is first used to identify a pathway with few intervening vessels. Then a 19G or 20G needle is passed and slowly withdrawn to capture tissue (Figure 1). Careful evaluation with Doppler ultrasound to evaluate for bleeding is recommended after EUS-LB and if persistent, a small amount of clot may be reinjected as a blood or “Chang” patch akin to technique to control oozing postlumbar puncture.²

Jennifer Phan, MD

While large prospective studies are needed to compare the methods, it appears that specimen adequacy acquired via EUS-LB are comparable to percutaneous and transjugular approaches.^3-5 Utilization of specific needle types and suction may optimize samples. Namely, 19G needles may provide better samples than smaller sizes and contemporary fine-needle biopsy needles with Franseen tips are superior to conventional spring-loaded cutting needles and fork tip needles.^6-8 The use of dry suction has been shown to increase the yield of tissue, but at the expense of increased bloodiness. Wet suction, which involves the presence of fluid, rather than air, in the needle lumen to lubricate and improve transmission of negative pressure to the needle tip, is the preferred technique for EUS-LB given improvement in the likelihood of intact liver biopsy cores and increased specimen adequacy.⁹

There are several advantages to EUS-LB (Table 1). When compared with percutaneous liver biopsy (PC-LB) and transjugular liver biopsy (TJ-LB), EUS-LB is uniquely able to access both liver lobes in a single setting, which minimizes sampling error.³ EUS-LB may also have an advantage in sampling focal liver lesions given the close proximity of the transducer to the liver.¹⁰ Another advantage over PC-LB is that EUS-LB can be performed in patients with a large body habitus. Additionally, EUS-LB is better tolerated than PC-LB, with less postprocedure pain and shorter postprocedure monitoring time.^4,5
 

Dr. James Buxbaum and Dr. Aileen Bui

Rates of adverse events appear to be similar between the three methods. Similar to PC-LB, EUS-LB requires capsular puncture, which can lead to intraperitoneal hemorrhage. Therefore, TJ-LB is preferred in patients with significant coagulopathy. While small ascites is not an absolute contraindication for EUS-LB, large ascites can obscure a safe window from the proximal stomach or duodenum to the liver, and thus TJLB is also preferred in these patients.¹¹ Given its relative novelty and logistic challenges, other disadvantages of EUS-LB include limited provider availability and increased cost, especially compared with PC-LB. The most significant limitation is that it requires moderate or deep sedation, as opposed to local anesthetics. However, if there is another indication for endoscopy (that is, variceal screening), then “one-stop shop” procedures including EUS-LB may be more convenient and cost-effective than traditional methods. Nevertheless, rigorous comparative studies are needed.
 

EUS-guided portal pressure gradient measurement

The presence of clinically significant portal hypertension (CSPH), defined as hepatic venous pressure gradient (HVPG) greater than or equal to 10 is a potent predictor of decompensation. There is growing evidence to support the use of beta-blockers to mitigate this risk.¹² Therefore, early identification of patients with CSPH has important diagnostic and therapeutic implications. The current gold standard for diagnosing CSPH is with wedged HVPG measurements performed by interventional radiology.

Since its introduction in 2016, EUS-guided portal pressure gradient measurement (EUS-PPG) has emerged as an alternative to wedged HVPG.^13,14 Using a linear echoendoscope, the portal vein is directly accessed with a 25G fine-needle aspiration needle, and three direct measurements are taken using a compact manometer to determine the mean pressure. The hepatic vein, or less commonly the inferior vena cava, pressure is also measured. The direct measurement of portal pressure provides a significant advantage of EUS-PPG over HVPG in patients with presinusoidal and prehepatic portal hypertension. Wedged HVPG, which utilizes the difference between the wedged and free hepatic venous pressure to indirectly estimate the portal venous pressure gradient, yields erroneously low gradients in patients with noncirrhotic portal hypertension.¹⁵ An additional advantage of EUS-PPG is that it obviates the need for a central venous line placement, which is associated with thrombosis and, in rare cases, air embolus.¹⁶

Observational studies indicate that EUS-PPG has a high degree of consistency with HVPG measurements and a strong correlation between other clinical findings of portal hyper-tension including esophageal varices and thrombocytopenia.^13,14 Nevertheless, EUS-PPG is performed under moderate or deep sedation which may impact HVPG measurements.¹⁷ In addition, the real-world application of EUS-PPG measurement on clinical care is undefined, but it is the topic of an ongoing clinical trial (ClinicalTrials.gov – NCT05357599).
 

EUS-guided interventions of gastric varices

Compared with esophageal varices, current approaches to the treatment and prophylaxis of gastric varices are more controversial.¹⁸ The most common approach to bleeding gastric varices in the United States is the placement of a transjugular intrahepatic portosystemic shunt (TIPS). Nevertheless, in addition to risks associated with central venous line placement, 5%-35% of individuals develop hepatic encephalopathy after TIPS and ischemic acute liver failure can occur in rare situations.¹⁹ Cyanoacrylate (CYA) glue injection is the recommended first-line endoscopic therapy for the treatment of bleeding gastric varices, but use has not been widely adopted in the United States because of a lack of an approved Food and Drug Administration CYA formulation, limited expertise, and risk of serious complications. In particular systemic embolization may result in pulmonary or cerebral infarct.^12,18 EUS-guided interventions have been developed to mitigate these safety concerns. EUS-guided coil embolization can be performed, either alone or in combination with CYA injection.²⁰ In the latter approach it acts as a scaffold to prevent migration of the glue bolus. Doppler assessment enables direct visualization of the gastric varix for identification of feeder vessels, more controlled deployment of hemostatic agents, and real-time confirmation of varix obliteration. Fluoroscopy can be used as an adjunct.

EUS-guided interventions in the management of gastric varices appear to be effective and superior to CYA injection under direct endoscopic visualization with improved likelihood of obliteration and lower rebleeding rates, without increase in adverse events.²¹ Additionally, EUS-guided combination therapy improves technical outcomes and reduces adverse events relative to EUS-guided coil or EUS-guided glue injection therapy alone.^21-23 Nevertheless, large-scale prospective trials are needed to determine whether EUS-guided interventions should be considered over TIPS. The role of EUS-guided interventions as primary prophylaxis to prevent bleeding from large gastric varices also requires additional study.²⁴

Future directions

Endohepatology has shown promise in its ability to consolidate the evaluation and treatment of patients with liver disease with the goal of optimizing care and increasing efficiency. In addition to new endoscopic procedures to optimize liver biopsy, portal pressure measurement, and gastric variceal treatment, there are a number of emerging technologies including EUS-guided liver elastography, portal venous sampling, liver tumor chemoembolization, and intrahepatic portosystemic shunts.²⁵ However, the practice of endohepatology faces a number of challenges before widespread adoption, including limited provider expertise and institutional availability. Additionally, more robust, multicenter outcomes and cost-effective analyses comparing these novel procedures with traditional approaches are needed to define their clinical impact.

Dr. Bui is a fellow in gastroenterology in the division of gastroenterology and hepatology, University of Southern California, Los Angeles. Dr. Buxbaum is associate professor of medicine (clinical scholar) in the division of gastroenterology and hepatology, University of Southern California. Dr. Buxbaum is a consultant for Cook Medical, Boston Scientific, and Olympus. Dr. Bui has no disclosures.

References

1. Mathew A. Am J Gastroenterol. 2007;102(10):2354-5.

2. Sowa P et al. VideoGIE. 2021;6(11):487-8.

3. Pineda JJ et al. Gastrointest Endosc. 2016;83(2):360-5.

4. Ali AH et al. J Ultrasound. 2020;23(2):157-67.

5. Shuja A et al. Dig Liver Dis. 2019;51(6):826-30.

6. Schulman AR et al. Gastrointest Endosc. 2017;85(2):419-26.

7. DeWitt J et al. Endosc Int Open. 2015;3(5):E471-8.

8. Aggarwal SN et al. Gastrointest Endosc. 2021;93(5):1133-8.

9. Mok SRS et al. Gastrointest Endosc. 2018;88(6):919-25.

10. Lee YN et al. J Gastroenterol Hepatol. 2015;30(7):1161-6.

11. Kalambokis G et al. J Hepatol. 2007;47(2):284-94.

12. de Franchis R et al. J Hepatol. 2022;76(4):959-74.

13. Choi AY et al. J Gastroenterol Hepatol. 2022;37(7):1373-9.

14. Zhang W et al. Gastrointest Endosc. 2021;93(3):565-72.

15. Seijo S et al. Dig Liver Dis. 2012;44(10):855-60.

16. Vesely TM. J Vasc Interv Radiol. 2001;12(11):1291-5.

17. Reverter E et al. Liver Int. 2014;34(1):16-25.

18. Henry Z et al. Clin Gastroenterol Hepatol. 2021;19(6):1098-107.e1091.

19. Ripamonti R et al. Semin Intervent Radiol. 2006;23(2):165-76.

20. Rengstorff DS and Binmoeller KF. Gastrointest Endosc. 2004;59(4):553-8.

21. Mohan BP et al. Endoscopy. 2020;52(4):259-67.

22. Robles-Medranda C et al. Endoscopy. 2020;52(4):268-75.

23. McCarty TR et al. Endosc Ultrasound. 2020;9(1):6-15.

24. Kouanda A et al. Gastrointest Endosc. 2021;94(2):291-6.

25. Bazarbashi AN et al. 2022;24(1):98-107.

Evolving endpoints and treat-to-target strategies in inflammatory bowel disease (IBD) incorporate a need for more frequent assessments of the disease, including objective measures of inflammation.^1,2 Intestinal ultrasound (IUS) is a noninvasive, well-tolerated,³ repeatable, point-of-care (POC) test that is highly sensitive and specific in detection of bowel inflammation, transmural healing,^4,5 and response to therapy in both Crohn’s disease (CD) and ulcerative colitis (UC).^6-8These unique features allow IUS to be an optimal tool for the current era of disease modification and tight disease control in IBD. As IUS is taking hold in the United States, there is a great need to teach the next generation of gastroenterologists about its value, how to incorporate it into clinical practice, and how to become appropriately trained and maintain competency.

Why incorporate IUS in the United States now?

Jordan Porter-Woodruff/University of Chicago

As IBD management has evolved, so has the appreciation for the value of bedside IUS as a tool that addresses very real needs for the field. Unlike other parts of the world in which ultrasound skills are part of the training curriculum, this has not been the case in internal medicine and gastroenterology training in the United States. In addition, there have been no specific billing codes or clear renumeration processes outlined for IUS,⁹ nor have there been any local training opportunities. Because of these challenges, it was not until recently that several leaders in IBD in the United States championed the potential of this technology and incorporated it into IBD management. Subsequently, a number of gastroenterologists have been trained and are now leading the effort to disseminate this tool throughout the United States. A consequence of these efforts resulted in support from the Helmsley Charitable Trust (Helmsley) and the creation of the Intestinal Ultrasound Group of the United States and Canada to address the gaps unique to North America as well as to strengthen the quality of IUS research through collaborations across the continent.

What is IUS, and when is it performed?

IUS is a sonographic exam performed by a gastroenterology-trained professional who scans the abdominal wall (and perineum when the rectum and perineal disease is evaluated), using both a convex low-frequency probe and linear high-frequency probe to evaluate the small intestine, colon, and rectum. The bowel is composed of five layers with alternating hyperechoic and hypoechoic layers: the mucosal-lumen interface (not a true part of the bowel wall), deep mucosa, submucosa, muscularis propria, and serosa. (Figure)

Dr. Noa Krugliak Cleveland

The most sensitive parameter for assessment of IBD activity is bowel wall thickness (≤ 3 mm in the small bowel and colon and ≤ 4 mm in the rectum are considered normal in adults).^8,10 The second key parameter is the assessment of vascularization, in which presence of hyperemia suggests active disease.¹¹ There are a number of indices to quantify hyperemia, with the most widely used being the Limberg score.¹² Additional parameters include assessment of loss of the delineation of the bowel wall layers (loss of stratification signifies active inflammation), increased thickness of the submucosa,¹³ increased mesenteric fatty proliferation (with increased inflammation, mesenteric fat proliferation will appear as a hyperechoic area surrounding the bowel), lymphadenopathy, bowel strictures, and extramural complications such as fistulae and abscess. Shear wave elastography may be an effective way to differentiate severe fibrotic strictures, but this is an area that requires more investigation.¹⁴

IUS has been shown to be an excellent tool in not only assessing disease activity and disease complication (with higher sensitivity than the Harvey-Bradshaw Index, serum C-reactive protein),¹⁵ but, unique to IUS, can provide early prediction of response in moderate to severe active UC.^6,7 This has also been shown with transperineal ultrasound in patients with UC, with the ability to predict response to therapy as early as 1 week from induction therapy.¹⁶ Furthermore, it can be used to assess transmural healing, which has been shown to be associated with improved outcomes in Crohn’s patient, such as lower rates of hospitalizations, surgery, medication escalation, and need for corticosteroids.¹⁷ IUS is associated with great patient satisfaction and greater understanding of disease-related symptoms when the patient sees the inflammation of the bowel. (Table)

How can you get trained in IUS?

Training in IUS varies across the globe, from incorporation of IUS into the standard training curriculum to available training programs that can be followed and attended outside of medical training. In the United States, interested gastroenterologists can now be trained by becoming a member of the International Bowel Ultrasound Group (IBUS Group) and applying to the workshops now available. The IBUS Group has developed an IUS-specific training curriculum over the last 16 years, which is comprised of three modules: a 2-day hands-on workshop (Module 1) with final examination of theoretical competency, a preceptorship at an “expert center” with an experienced sonographer for a total of 4 weeks to complete 40 supervised IUS examinations (Module 2), and didactics and a final examination (Module 3). Also with support from Helmsley, the first Module 1 to be offered in the United States was hosted at Mount Sinai Medical Center in New York in 2022, the second was hosted at the University of Chicago in March 2023, and the third is planned to take place at Cedars-Sinai Medical Center in Los Angeles in March 2024.¹⁸ With the growing interest and demand for IUS training in the United States, U.S. experts are working to develop new training options that will be less time consuming, scalable, and still provide appropriate training and competency assessment.

University of Chicago

How do you integrate IUS into your practice?

The keys to integrating IUS are a section chief or practice manager’s support of a trainee or faculty member for both funding of equipment and protected time for training and building of the program, as well as a permissive environment and collegial relationship with radiology. An ultrasound machine and additional transducers may range in price from $50,000-$120,000. Funding may be a limiting step for many, however. A detailed business plan is imperative to the success and investment of funds in an IUS program. With current billing practices in place that include ”limited abdominal ultrasound” (76705) and “Doppler ultrasound of the abdomen” (93975),¹⁹ reimbursement should include a technical fee, professional fee, and if in a hospital-based clinic, a facility fee. IUS pro-fee combined with technical fee is reimbursed at approximately 0.80 relative value units. When possible, the facility fee is included for approximately $800 per IUS visit. For billing and compliance with HIPAA, all billed IUS images must be stored in a durable and accessible format. It is recommended that the images and cine loops be digitally stored to the same or similar platform used by radiologists at the same institution. This requires early communication with the local information technology department for the connection of an ultrasound machine to the storage platform and/or electronic health record. Reporting results should be standardized with unique or otherwise available IUS templates, which also satisfy all billing components.⁹ The flow for incorporation of IUS into practice can be at the same time patients are seen during their visit, or alternatively, in a dedicated IUS clinic in which patients are referred by other providers and scheduled back to back.

Conclusions

In summary, the confluence of treat-to-target strategies in IBD, new treatment options in IBD, and successful efforts to translate IUS training and billing practices to the United States portends a great future for the field and for our patients.

Dr. Cleveland and Dr. Rubin, of the University of Chicago’s Inflammatory Bowel Disease Center, are speakers for Samsung/Boston Imaging.

References

1. Turner D et al. Gastroenterology. Apr 2021;160(5):1570-83. doi: 10.1053/j.gastro.2020.12.031

2. Hart AL and Rubin DT. Gastroenterology. Apr 2022;162(5):1367-9. doi: 10.1053/j.gastro.2022.02.013

3. Rajagopalan A et al. JGH Open. Apr 2020;4(2):267-72. doi: 10.1002/jgh3.12268

4. Calabrese E et al. Clin Gastroenterol Hepatol. Apr 2022;20(4):e711-22. doi: 10.1016/j.cgh.2021.03.030

5. Ripolles T et al. Inflamm Bowel Dis. Oct 2016;22(10):2465-73. doi10.1097/MIB.0000000000000882

6. Maaser C et al. Gut. Sep 2020;69(9):1629-36. doi: 10.1136/gutjnl-2019-319451

7. Ilvemark J et al. J Crohns Colitis. Nov 23 2022;16(11):1725-34. doi: 10.1093/ecco-jcc/jjac083

8. Sagami S et al. Aliment Pharmacol Ther. Jun 2020;51(12):1373-83. doi: 10.1111/apt.15767

9. Dolinger MT et al. Guide to Intestinal Ultrasound Credentialing, Documentation, and Billing for Gastroenterologists in the United States. Am J Gastroenterol. 2023.

10. Maconi G et al. Ultraschall Med. Jun 2018;39(3):304-17. doi: 10.1055/s-0043-125329

11. Sasaki T et al. Scand J Gastroenterol. Mar 2014;49(3):295-301. doi: 10.3109/00365521.2013.871744

12. Limberg B. Z Gastroenterol. Jun 1999;37(6):495-508.

13. Miyoshi J et al. J Gastroenterol. Feb 2022;57(2):82-9. doi: 10.1007/s00535-021-01847-3

14. Chen YJ et al. Inflamm Bowel Dis. Sep 15 2018;24(10):2183-90. doi: 10.1093/ibd/izy115

15. Kucharzik T et al. Apr 2017;15(4):535-42e2. doi: 10.1016/j.cgh.2016.10.040

16. Sagami S et al. Aliment Pharmacol Ther. May 2022;55(10):1320-9. doi: 10.1111/apt.16817

17. Vaughan R et al. Aliment Pharmacol Ther. Jul 2022;56(1):84-94. doi: 10.1111/apt.16892

18. International Bowel Ultrasound Group. https://ibus-group.org/

19. American Medical Association. CPT (Current Procedural Terminology). https://www.ama-assn.org/amaone/cpt-current-procedural-terminology




 

Evolving endpoints and treat-to-target strategies in inflammatory bowel disease (IBD) incorporate a need for more frequent assessments of the disease, including objective measures of inflammation.^1,2 Intestinal ultrasound (IUS) is a noninvasive, well-tolerated,³ repeatable, point-of-care (POC) test that is highly sensitive and specific in detection of bowel inflammation, transmural healing,^4,5 and response to therapy in both Crohn’s disease (CD) and ulcerative colitis (UC).^6-8These unique features allow IUS to be an optimal tool for the current era of disease modification and tight disease control in IBD. As IUS is taking hold in the United States, there is a great need to teach the next generation of gastroenterologists about its value, how to incorporate it into clinical practice, and how to become appropriately trained and maintain competency.

Why incorporate IUS in the United States now?

Jordan Porter-Woodruff/University of Chicago

As IBD management has evolved, so has the appreciation for the value of bedside IUS as a tool that addresses very real needs for the field. Unlike other parts of the world in which ultrasound skills are part of the training curriculum, this has not been the case in internal medicine and gastroenterology training in the United States. In addition, there have been no specific billing codes or clear renumeration processes outlined for IUS,⁹ nor have there been any local training opportunities. Because of these challenges, it was not until recently that several leaders in IBD in the United States championed the potential of this technology and incorporated it into IBD management. Subsequently, a number of gastroenterologists have been trained and are now leading the effort to disseminate this tool throughout the United States. A consequence of these efforts resulted in support from the Helmsley Charitable Trust (Helmsley) and the creation of the Intestinal Ultrasound Group of the United States and Canada to address the gaps unique to North America as well as to strengthen the quality of IUS research through collaborations across the continent.

What is IUS, and when is it performed?

IUS is a sonographic exam performed by a gastroenterology-trained professional who scans the abdominal wall (and perineum when the rectum and perineal disease is evaluated), using both a convex low-frequency probe and linear high-frequency probe to evaluate the small intestine, colon, and rectum. The bowel is composed of five layers with alternating hyperechoic and hypoechoic layers: the mucosal-lumen interface (not a true part of the bowel wall), deep mucosa, submucosa, muscularis propria, and serosa. (Figure)

Dr. Noa Krugliak Cleveland

The most sensitive parameter for assessment of IBD activity is bowel wall thickness (≤ 3 mm in the small bowel and colon and ≤ 4 mm in the rectum are considered normal in adults).^8,10 The second key parameter is the assessment of vascularization, in which presence of hyperemia suggests active disease.¹¹ There are a number of indices to quantify hyperemia, with the most widely used being the Limberg score.¹² Additional parameters include assessment of loss of the delineation of the bowel wall layers (loss of stratification signifies active inflammation), increased thickness of the submucosa,¹³ increased mesenteric fatty proliferation (with increased inflammation, mesenteric fat proliferation will appear as a hyperechoic area surrounding the bowel), lymphadenopathy, bowel strictures, and extramural complications such as fistulae and abscess. Shear wave elastography may be an effective way to differentiate severe fibrotic strictures, but this is an area that requires more investigation.¹⁴

IUS has been shown to be an excellent tool in not only assessing disease activity and disease complication (with higher sensitivity than the Harvey-Bradshaw Index, serum C-reactive protein),¹⁵ but, unique to IUS, can provide early prediction of response in moderate to severe active UC.^6,7 This has also been shown with transperineal ultrasound in patients with UC, with the ability to predict response to therapy as early as 1 week from induction therapy.¹⁶ Furthermore, it can be used to assess transmural healing, which has been shown to be associated with improved outcomes in Crohn’s patient, such as lower rates of hospitalizations, surgery, medication escalation, and need for corticosteroids.¹⁷ IUS is associated with great patient satisfaction and greater understanding of disease-related symptoms when the patient sees the inflammation of the bowel. (Table)

How can you get trained in IUS?

Training in IUS varies across the globe, from incorporation of IUS into the standard training curriculum to available training programs that can be followed and attended outside of medical training. In the United States, interested gastroenterologists can now be trained by becoming a member of the International Bowel Ultrasound Group (IBUS Group) and applying to the workshops now available. The IBUS Group has developed an IUS-specific training curriculum over the last 16 years, which is comprised of three modules: a 2-day hands-on workshop (Module 1) with final examination of theoretical competency, a preceptorship at an “expert center” with an experienced sonographer for a total of 4 weeks to complete 40 supervised IUS examinations (Module 2), and didactics and a final examination (Module 3). Also with support from Helmsley, the first Module 1 to be offered in the United States was hosted at Mount Sinai Medical Center in New York in 2022, the second was hosted at the University of Chicago in March 2023, and the third is planned to take place at Cedars-Sinai Medical Center in Los Angeles in March 2024.¹⁸ With the growing interest and demand for IUS training in the United States, U.S. experts are working to develop new training options that will be less time consuming, scalable, and still provide appropriate training and competency assessment.

University of Chicago

How do you integrate IUS into your practice?

The keys to integrating IUS are a section chief or practice manager’s support of a trainee or faculty member for both funding of equipment and protected time for training and building of the program, as well as a permissive environment and collegial relationship with radiology. An ultrasound machine and additional transducers may range in price from $50,000-$120,000. Funding may be a limiting step for many, however. A detailed business plan is imperative to the success and investment of funds in an IUS program. With current billing practices in place that include ”limited abdominal ultrasound” (76705) and “Doppler ultrasound of the abdomen” (93975),¹⁹ reimbursement should include a technical fee, professional fee, and if in a hospital-based clinic, a facility fee. IUS pro-fee combined with technical fee is reimbursed at approximately 0.80 relative value units. When possible, the facility fee is included for approximately $800 per IUS visit. For billing and compliance with HIPAA, all billed IUS images must be stored in a durable and accessible format. It is recommended that the images and cine loops be digitally stored to the same or similar platform used by radiologists at the same institution. This requires early communication with the local information technology department for the connection of an ultrasound machine to the storage platform and/or electronic health record. Reporting results should be standardized with unique or otherwise available IUS templates, which also satisfy all billing components.⁹ The flow for incorporation of IUS into practice can be at the same time patients are seen during their visit, or alternatively, in a dedicated IUS clinic in which patients are referred by other providers and scheduled back to back.

Conclusions

In summary, the confluence of treat-to-target strategies in IBD, new treatment options in IBD, and successful efforts to translate IUS training and billing practices to the United States portends a great future for the field and for our patients.

Dr. Cleveland and Dr. Rubin, of the University of Chicago’s Inflammatory Bowel Disease Center, are speakers for Samsung/Boston Imaging.

References

1. Turner D et al. Gastroenterology. Apr 2021;160(5):1570-83. doi: 10.1053/j.gastro.2020.12.031

2. Hart AL and Rubin DT. Gastroenterology. Apr 2022;162(5):1367-9. doi: 10.1053/j.gastro.2022.02.013

3. Rajagopalan A et al. JGH Open. Apr 2020;4(2):267-72. doi: 10.1002/jgh3.12268

4. Calabrese E et al. Clin Gastroenterol Hepatol. Apr 2022;20(4):e711-22. doi: 10.1016/j.cgh.2021.03.030

5. Ripolles T et al. Inflamm Bowel Dis. Oct 2016;22(10):2465-73. doi10.1097/MIB.0000000000000882

6. Maaser C et al. Gut. Sep 2020;69(9):1629-36. doi: 10.1136/gutjnl-2019-319451

7. Ilvemark J et al. J Crohns Colitis. Nov 23 2022;16(11):1725-34. doi: 10.1093/ecco-jcc/jjac083

8. Sagami S et al. Aliment Pharmacol Ther. Jun 2020;51(12):1373-83. doi: 10.1111/apt.15767

9. Dolinger MT et al. Guide to Intestinal Ultrasound Credentialing, Documentation, and Billing for Gastroenterologists in the United States. Am J Gastroenterol. 2023.

10. Maconi G et al. Ultraschall Med. Jun 2018;39(3):304-17. doi: 10.1055/s-0043-125329

11. Sasaki T et al. Scand J Gastroenterol. Mar 2014;49(3):295-301. doi: 10.3109/00365521.2013.871744

12. Limberg B. Z Gastroenterol. Jun 1999;37(6):495-508.

13. Miyoshi J et al. J Gastroenterol. Feb 2022;57(2):82-9. doi: 10.1007/s00535-021-01847-3

14. Chen YJ et al. Inflamm Bowel Dis. Sep 15 2018;24(10):2183-90. doi: 10.1093/ibd/izy115

15. Kucharzik T et al. Apr 2017;15(4):535-42e2. doi: 10.1016/j.cgh.2016.10.040

16. Sagami S et al. Aliment Pharmacol Ther. May 2022;55(10):1320-9. doi: 10.1111/apt.16817

17. Vaughan R et al. Aliment Pharmacol Ther. Jul 2022;56(1):84-94. doi: 10.1111/apt.16892

18. International Bowel Ultrasound Group. https://ibus-group.org/

19. American Medical Association. CPT (Current Procedural Terminology). https://www.ama-assn.org/amaone/cpt-current-procedural-terminology




 

Evolving endpoints and treat-to-target strategies in inflammatory bowel disease (IBD) incorporate a need for more frequent assessments of the disease, including objective measures of inflammation.^1,2 Intestinal ultrasound (IUS) is a noninvasive, well-tolerated,³ repeatable, point-of-care (POC) test that is highly sensitive and specific in detection of bowel inflammation, transmural healing,^4,5 and response to therapy in both Crohn’s disease (CD) and ulcerative colitis (UC).^6-8These unique features allow IUS to be an optimal tool for the current era of disease modification and tight disease control in IBD. As IUS is taking hold in the United States, there is a great need to teach the next generation of gastroenterologists about its value, how to incorporate it into clinical practice, and how to become appropriately trained and maintain competency.

Why incorporate IUS in the United States now?

Jordan Porter-Woodruff/University of Chicago

As IBD management has evolved, so has the appreciation for the value of bedside IUS as a tool that addresses very real needs for the field. Unlike other parts of the world in which ultrasound skills are part of the training curriculum, this has not been the case in internal medicine and gastroenterology training in the United States. In addition, there have been no specific billing codes or clear renumeration processes outlined for IUS,⁹ nor have there been any local training opportunities. Because of these challenges, it was not until recently that several leaders in IBD in the United States championed the potential of this technology and incorporated it into IBD management. Subsequently, a number of gastroenterologists have been trained and are now leading the effort to disseminate this tool throughout the United States. A consequence of these efforts resulted in support from the Helmsley Charitable Trust (Helmsley) and the creation of the Intestinal Ultrasound Group of the United States and Canada to address the gaps unique to North America as well as to strengthen the quality of IUS research through collaborations across the continent.

What is IUS, and when is it performed?

IUS is a sonographic exam performed by a gastroenterology-trained professional who scans the abdominal wall (and perineum when the rectum and perineal disease is evaluated), using both a convex low-frequency probe and linear high-frequency probe to evaluate the small intestine, colon, and rectum. The bowel is composed of five layers with alternating hyperechoic and hypoechoic layers: the mucosal-lumen interface (not a true part of the bowel wall), deep mucosa, submucosa, muscularis propria, and serosa. (Figure)

Dr. Noa Krugliak Cleveland

The most sensitive parameter for assessment of IBD activity is bowel wall thickness (≤ 3 mm in the small bowel and colon and ≤ 4 mm in the rectum are considered normal in adults).^8,10 The second key parameter is the assessment of vascularization, in which presence of hyperemia suggests active disease.¹¹ There are a number of indices to quantify hyperemia, with the most widely used being the Limberg score.¹² Additional parameters include assessment of loss of the delineation of the bowel wall layers (loss of stratification signifies active inflammation), increased thickness of the submucosa,¹³ increased mesenteric fatty proliferation (with increased inflammation, mesenteric fat proliferation will appear as a hyperechoic area surrounding the bowel), lymphadenopathy, bowel strictures, and extramural complications such as fistulae and abscess. Shear wave elastography may be an effective way to differentiate severe fibrotic strictures, but this is an area that requires more investigation.¹⁴

IUS has been shown to be an excellent tool in not only assessing disease activity and disease complication (with higher sensitivity than the Harvey-Bradshaw Index, serum C-reactive protein),¹⁵ but, unique to IUS, can provide early prediction of response in moderate to severe active UC.^6,7 This has also been shown with transperineal ultrasound in patients with UC, with the ability to predict response to therapy as early as 1 week from induction therapy.¹⁶ Furthermore, it can be used to assess transmural healing, which has been shown to be associated with improved outcomes in Crohn’s patient, such as lower rates of hospitalizations, surgery, medication escalation, and need for corticosteroids.¹⁷ IUS is associated with great patient satisfaction and greater understanding of disease-related symptoms when the patient sees the inflammation of the bowel. (Table)

How can you get trained in IUS?

Training in IUS varies across the globe, from incorporation of IUS into the standard training curriculum to available training programs that can be followed and attended outside of medical training. In the United States, interested gastroenterologists can now be trained by becoming a member of the International Bowel Ultrasound Group (IBUS Group) and applying to the workshops now available. The IBUS Group has developed an IUS-specific training curriculum over the last 16 years, which is comprised of three modules: a 2-day hands-on workshop (Module 1) with final examination of theoretical competency, a preceptorship at an “expert center” with an experienced sonographer for a total of 4 weeks to complete 40 supervised IUS examinations (Module 2), and didactics and a final examination (Module 3). Also with support from Helmsley, the first Module 1 to be offered in the United States was hosted at Mount Sinai Medical Center in New York in 2022, the second was hosted at the University of Chicago in March 2023, and the third is planned to take place at Cedars-Sinai Medical Center in Los Angeles in March 2024.¹⁸ With the growing interest and demand for IUS training in the United States, U.S. experts are working to develop new training options that will be less time consuming, scalable, and still provide appropriate training and competency assessment.

University of Chicago

How do you integrate IUS into your practice?

The keys to integrating IUS are a section chief or practice manager’s support of a trainee or faculty member for both funding of equipment and protected time for training and building of the program, as well as a permissive environment and collegial relationship with radiology. An ultrasound machine and additional transducers may range in price from $50,000-$120,000. Funding may be a limiting step for many, however. A detailed business plan is imperative to the success and investment of funds in an IUS program. With current billing practices in place that include ”limited abdominal ultrasound” (76705) and “Doppler ultrasound of the abdomen” (93975),¹⁹ reimbursement should include a technical fee, professional fee, and if in a hospital-based clinic, a facility fee. IUS pro-fee combined with technical fee is reimbursed at approximately 0.80 relative value units. When possible, the facility fee is included for approximately $800 per IUS visit. For billing and compliance with HIPAA, all billed IUS images must be stored in a durable and accessible format. It is recommended that the images and cine loops be digitally stored to the same or similar platform used by radiologists at the same institution. This requires early communication with the local information technology department for the connection of an ultrasound machine to the storage platform and/or electronic health record. Reporting results should be standardized with unique or otherwise available IUS templates, which also satisfy all billing components.⁹ The flow for incorporation of IUS into practice can be at the same time patients are seen during their visit, or alternatively, in a dedicated IUS clinic in which patients are referred by other providers and scheduled back to back.

Conclusions

In summary, the confluence of treat-to-target strategies in IBD, new treatment options in IBD, and successful efforts to translate IUS training and billing practices to the United States portends a great future for the field and for our patients.

Dr. Cleveland and Dr. Rubin, of the University of Chicago’s Inflammatory Bowel Disease Center, are speakers for Samsung/Boston Imaging.

References

1. Turner D et al. Gastroenterology. Apr 2021;160(5):1570-83. doi: 10.1053/j.gastro.2020.12.031

2. Hart AL and Rubin DT. Gastroenterology. Apr 2022;162(5):1367-9. doi: 10.1053/j.gastro.2022.02.013

3. Rajagopalan A et al. JGH Open. Apr 2020;4(2):267-72. doi: 10.1002/jgh3.12268

4. Calabrese E et al. Clin Gastroenterol Hepatol. Apr 2022;20(4):e711-22. doi: 10.1016/j.cgh.2021.03.030

5. Ripolles T et al. Inflamm Bowel Dis. Oct 2016;22(10):2465-73. doi10.1097/MIB.0000000000000882

6. Maaser C et al. Gut. Sep 2020;69(9):1629-36. doi: 10.1136/gutjnl-2019-319451

7. Ilvemark J et al. J Crohns Colitis. Nov 23 2022;16(11):1725-34. doi: 10.1093/ecco-jcc/jjac083

8. Sagami S et al. Aliment Pharmacol Ther. Jun 2020;51(12):1373-83. doi: 10.1111/apt.15767

9. Dolinger MT et al. Guide to Intestinal Ultrasound Credentialing, Documentation, and Billing for Gastroenterologists in the United States. Am J Gastroenterol. 2023.

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