Michelle A. Wood, DO

About 10% of all reproductive-aged women and 35% to 50% of women with pelvic pain and infertility are affected by endometriosis.^1,2 The disease typically involves the reproductive tract organs, anterior and posterior cul-de-sacs, and uterosacral ligaments. However, disease outside of the reproductive tract occurs frequently and has been found on all organs except the spleen.³

The bowel is the most common site for extragenital endometriosis, affected in an estimated 3.8% to 37% of patients with known endometriosis.^4-7 Implants may be superficial, involving the bowel serosa and subserosa (FIGURE 1), or they can manifest as deeply infiltrating lesions involving the muscularis and mucosa (FIGURE 2). The rectosigmoid colon is the most common location for bowel endometriosis, followed by the rectum, ileum, appendix, and cecum^4,8 (FIGURES 3, 4, and 5). Case reports also have described endometrial implants on the stomach and transverse colon.⁹ Although isolated bowel involvement has been recognized, most patients with bowel endometriosis have concurrent disease elsewhere.^2,4 

Historically, segmental resection was performed regardless of the anatomical location of the lesion.¹⁰ Even today, many surgeons continue to routinely perform segmental bowel resection as a first-line surgical approach.¹¹ Unnecessary segmental resection, however, places patients at risk for short- and long-term postoperative morbidity, including the possibility of permanent ostomy. Modern surgical techniques, such as shaving excision and disc resection, have been performed to successfully treat bowel endometriosis with excellent long-term outcomes and fewer complications when compared with traditional segmental resection.^2,12-16

In this article, we focus on the clinical indications and surgical techniques for video-laparoscopic management, but first we describe the pathophysiology, clinical presentation, and diagnosis of bowel endometriosis.

Pathophysiology of bowel endometriosis

The pathogenesis of endometriosis remains unknown, as no single mechanism explains all clinical cases of the disease. The most popular proposed theory describes retrograde menstruation through the fallopian tubes.¹⁷ Once inside the peritoneal cavity, endometrial cells attach to and invade healthy peritoneum, establishing a blood supply necessary for growth and survival.

In the case of bowel endometriosis, deposition of effluxed endometrial cells may lead to an inflammatory response that increases the risk of adhesion formation, leading to potential cul-de-sac obliteration. Lesions may originate as Allen-Masters peritoneal defects, developing into deeply infiltrative rectovaginal septum lesions. The anatomical shelter theory contributes to lesions within the pelvis, with the rectosigmoid colon blocking the cephalad flow of effluxed menstrual blood from the pelvis, thus leading to a preponderance of lesions in the pelvis and along the rectosigmoid colon.²

Continue to: Clinical presentation and diagnosis...

Clinical presentation and diagnosis

Women presenting with endometriosis of the bowel are typically of reproductive age and commonly report symptoms of dysmenorrhea, chronic pelvic pain, dyspareunia, and dyschezia. Some women also experience catamenial diarrhea, constipation, hematochezia, and bloating.² The differential diagnosis of these symptoms is broad and includes irritable bowel disease, ischemic colitis, inflammatory bowel disease, diverticulitis, pelvic inflammatory disease, and malignancy.

Because of its nonspecific symptoms, bowel endometriosis is often misdiagnosed and the disease goes untreated for years.¹⁸ Therefore, it is imperative that clinicians maintain a high index of suspicion when evaluating reproductive-aged women with gastrointestinal symptoms and pelvic pain.

Physical examination can be helpful in making the diagnosis of endometriosis. During bimanual examination, findings such as a fixed, tender, or retroverted uterus, uterosacral ligament nodularity, or an enlarged adnexal mass representing an ovarian endometrioma may be appreciated. Rectovaginal exam can identify areas of tenderness and nodularity along the rectovaginal septum. Speculum exam may reveal a laterally displaced cervix or blue powder-burn lesions along the cervix or posterior fornix.¹⁹ Rarely, endometriosis is found on the perineum within an episiotomy scar.²⁰

Imaging studies can be used in conjunction with physical examination findings to aid in the diagnosis of endometriosis. Images also guide preoperative planning by characterizing lesions based on their size, location, and depth of invasion. Hudelist and colleagues found transvaginal ultrasound (TVUS) to have an overall sensitivity of 71% to 98% and a specificity of 92% to 100%.²¹ However, it was noted that the accuracy of the diagnosis was directly related to the experience of the sonographer, and lesions above the sigmoid colon were generally unable to be diagnosed. Other imaging modalities that have been reported to have high sensitivity and specificity for diagnosing bowel endometriosis include rectal water contrast TVUS,^22,23 rectal endoscopic sonography,²² magnetic resonance imaging,²² and barium enema.²⁴

Medical management

Medical therapy for patients with endometriosis is utilized with the goal of suppressing ovulation, lowering circulating hormone levels, and inducing endometrial atrophy. Medications commonly employed include gonadotropin-releasing hormone agonists and antagonists, anabolic steriods such as danazol, combined oral contraceptive pills, progestins, and aromatase inhibitors.

Continue to: To date, no optimal hormonal regimen...

To date, no optimal hormonal regimen has been established for the treatment of bowel endometriosis. Vercellini and colleagues demonstrated that progestins with and without low-dose estrogen improved symptoms of dysmenorrhea and dyspareunia.²⁵ Ferrero and colleagues reported that 2.5 mg of norethindrone daily resulted in 53% of women with colorectal endometriosis reporting improved gastrointestinal symptoms.²⁶ However, by 12 months of follow-up, 33% of these patients had elected to undergo surgical management.

Gonadotropin-releasing hormone agonists, such as leuprolide acetate, also can be used to mitigate symptoms of bowel endometriosis or to decrease disease burden at the time of surgery, and they can be used with add-back norethindrone acetate. The use of these medications is limited by adverse effects, such as vasomotor symptoms and decreased bone mineral density when used for longer than 6 months.²

Medical therapy is commonly used for patients with mild to moderate symptoms and in those who are poor surgical candidates or decline surgical intervention. Medical therapy is especially useful when employed postoperatively to suppress the regrowth of microscopic ectopic endometrial tissue.

Patients must be counseled, however, that even with medical management, they may still require surgery in the future to control their symptoms and/or to preserve organ function.²

Surgical management

Surgical treatment for bowel endometriosis depends on the disease location, the size and depth of the lesion, the presence or absence of stricture, and the surgeon’s level of expertise.^2,12,27-30

In our group, we advocate for video-laparoscopy, with or without robotic as sistance. Minimally invasive surgery offers reduced blood loss, shorter recovery time, and fewer postoperative complications compared with laparotomy.^{2,16,27,31-33} The conversion rate to laparotomy has been reported to be about 3% when performed by an experienced surgeon.¹²

Darai and colleagues conducted a randomized trial of 52 patients undergoing surgery for colorectal endometriosis via either laparoscopic or open colon resection.³³ Blood loss was significantly lower in the laparoscopy group (1.6 vs 2.7 mg/L, P <.05). No difference was noted in long-term outcomes. In a retrospective study of 436 cases, Ruffo and colleagues showed that those who underwent laparoscopic colorectal resection had higher postoperative pregnancy rates compared with those who had laparotomy (57.6% vs 23.1%, P <.035).³²

The goal of surgical management of bowel endometriosis is to remove as many of the endometriotic lesions as possible while minimizing short- and long-term complications. Three surgical approaches have been described: shaving excision, disc resection, and segmental resection.²

Some surgeons prefer traditional segmental resection of the bowel regardless of the anatomical site, citing reduced disease recurrence with this approach; however, traditional segmental resection confers increased risk of complications. Increasingly, in an effort to reduce morbidity, more surgeons are advocating for the less aggressive methods of shaving excision and disc resection.

Aggressive resection at the level of the low rectum requires extensive surgical dissection of the retrorectal space, with the potential for inadvertent injury to surrounding neurovascular structures, such as the pelvic splanchnic nerves and superior and inferior hypogastric plexus.²⁹ Injury to these structures can lead to significant complications, including bowel stenosis, fistula formation, constipation, and urinary retention. Complete resection of other areas, such as the small bowel, do not carry the same risks and may have more significant benefit to the patient than less aggressive techniques.

Our group recommends carefully balancing the risks and benefits of aggressive surgical treatment for each individual and treating the patient with the appropriate technique. Regardless of technique, surgical treatment of bowel endometriosis can lead to long-term improvements in pain and infertility.^29,30,34,35

Continue to: Shaving excision...

Shaving excision

The most conservative approach to resection of bowel endometriosis is shaving excision; this involves removing endometriotic tissue layer-by-layer until healthy, underlying tissue is encountered.² With bowel endometriosis, the goal of shaving excision is to remove as much of the diseased tissue as possible while leaving behind the mucosal layer and a portion of the muscularis.^{2,15,16,36-38} This is the most conservative of the 3 surgical techniques and is associated with the lowest complication rate.^{2,14,15,36,37}

Our group reported on 185 women who underwent shaving excision for bowel endometriosis. At the time of surgery, 80 women had complete obliteration of the cul-de-sac (FIGURE 6). Of the study patients, 174 patients were available for follow-up, with 93% reporting moderate to complete pain relief.¹⁵

In a retrospective analysis of 3,298 surgeries for rectovaginal endometriosis in which shaving excision was used on all but 1% of patients, Donnez and colleagues reported a very low complication rate, with 1 case of rectal perforation, 1 case of fecal peritonitis, and 3 cases of ureteral injury.³⁹

Roman and colleagues described the use of shaving excision for rectal endometriosis using plasma energy (n = 54) and laparoscopic scissors (n = 68).⁴⁰ Only 4% of patients reported experiencing symptom recurrence, and the pregnancy rate was 65.4%, with 59% of those patients spontaneously conceiving. Two cases of rectal fistula were noted.

Disc resection

Laparoscopic disc excision has been described in the literature since the 1980s, and the technique involves the full-thickness removal of the diseased portion of the bowel, followed by closure of the remaining defect.^{2,12-14,28,29,31,41-45} To be appropriate for this technique, a lesion should involve only a portion of the bowel wall and, preferably, less than one-half of the bowel circumference.^2,42 Disc excision results in excellent outcomes with fewer postoperative complications than segmental resection, but with more complications when compared to shaving excision.^{2,12,13,29,45,46}

We reported on a series of 141 women with bowel endometriosis who underwent disc excision.² At 1-month follow-up, 87% of patients experienced an improvement in their symptoms. No cases required conversion to laparotomy or were complicated by rectovaginal fistula formation, ureteral injury, bowel perforation, or pelvic abscess.²

Continue to: Segmental resection...

Segmental resection

The most aggressive surgical approach, segmental resection involves complete removal of a diseased portion of bowel, followed by side-to-side or end-to-end reanastomosis of the adjacent segments.² For this procedure, a multidisciplinary approach is recommended, with involvement of a colorectal surgeon or gynecologic oncologist trained in performing bowel resections. Segmental resection is indicated for lesions that are larger than 3 cm, circumferential, obstructive, or multifocal.

Given the higher complication rate associated with this procedure and the good outcomes associated with less invasive techniques, we avoid segmental resection whenever possible, especially for lesions near the anal verge.²

Complications associated with surgical approach

In 2005, our group reported on a cohort of 178 women who underwent laparoscopic treatment of deeply infiltrative bowel endometriosis with shaving excision (n = 93), disc excision (n = 38), and segmental resection (n = 47).³⁴ The major complication rate was significantly higher for those undergoing segmental resection (12.5%, P <.001); only 7.7% of those who underwent disc resection experienced a major complication; and none were observed in the group treated with shaving excision.

In 2011, De Cicco and colleagues conducted a systematic review of 1,889 patients who underwent segmental bowel resection.³⁵ The major complication rate was 11%, with a leakage rate of 2.7%, fistula rate of 1.8%, major obstruction rate of 2.7%, and hemorrhage rate of 2.5%. Many of these complications, however, occurred in patients who had low rectal resections.

Regardless of surgical approach, the complication rate is related to the surgeon’s ability to preserve the superior and inferior hypogastric plexuses and the sympathetic and parasympathetic nerve bundles (FIGURE 7). Nerve-sparing techniques should be used to decrease the incidence of postoperative bowel, bladder, and sexual function complications.² 

Our group’s preferences

In our practice, we emphasize that the choice of surgical technique depends on the location, size, and depth of the lesion, as well as the extent of bowel wall circumferential invasion.²

We categorize lesions by their anatomic location: those above the sigmoid colon, on the sigmoid colon, on the rectosigmoid colon, and on the rectum. For lesions above the sigmoid colon, segmental or disc resection is appropriate.² We recommend segmental resection for multifocal lesions, lesions larger than 3 cm, or for lesions involving more than one-third of the bowel lumen.^37,44,45,47 Disc resection is appropriate for lesions smaller than 3 cm even if the bowel lumen is involved.^44,45,48 If endometriosis is encountered in any location along the bowel, appendectomy can be performed even without visible disease, due to a high incidence of occult disease of the appendix.^49,50

When lesions involve the sigmoid colon, we prefer utilizing shaving excision when possible to limit dissection of the retrorectal space and pelvic sidewall nerves.² Segmental resection at or below the sigmoid colon has been associated with postoperative surgical site leakage⁵¹ and long-term bowel and bladder dysfunction with risk of permanent colostomy.^52,53 For lesions smaller than 3 cm or involving less than one-third of the bowel lumen, disc resection can be performed. Segmental resection is required if multifocal disease or obstruction are present, if lesions are larger than 3 cm, or if more than one-third of the bowel lumen is involved.

For lesions along the rectosigmoid colon, we prefer utilizing shaving excision when possible.² Disc excision can be performed utilizing a transanal approach, being mindful to minimize dissection of the retroperitoneal space and pelvic sidewall nerves.⁴⁸ Segmental resection is avoided even with lesions larger than 3 cm, unless prior surgery has failed. Approaches for segmental resection can utilize laparoscopy or the natural orifices of the rectum or vagina.^31,51

For lesions on the rectum, we strongly advise shaving excision.² Evidence fails to show that the benefits of segmental resection outweigh the risks when compared to conservative techniques at the rectum.^30,39,54 There is evidence indicating that aggressive surgery 5 to 8 cm from the anal verge is predictive of postoperative complications.⁵⁵ In our group, we use shaving excision to remove as much disease as possible without compromising the integrity of the bowel wall or surrounding neurovascular structures. We err on the side of caution, leaving some of the disease on the rectum to avoid rectal perforation, and plan for postoperative hormonal suppression in these patients.

For patients desiring fertility, successful pregnancy is often achieved using the shaving technique.⁴¹

About 10% of all reproductive-aged women and 35% to 50% of women with pelvic pain and infertility are affected by endometriosis.^1,2 The disease typically involves the reproductive tract organs, anterior and posterior cul-de-sacs, and uterosacral ligaments. However, disease outside of the reproductive tract occurs frequently and has been found on all organs except the spleen.³

The bowel is the most common site for extragenital endometriosis, affected in an estimated 3.8% to 37% of patients with known endometriosis.^4-7 Implants may be superficial, involving the bowel serosa and subserosa (FIGURE 1), or they can manifest as deeply infiltrating lesions involving the muscularis and mucosa (FIGURE 2). The rectosigmoid colon is the most common location for bowel endometriosis, followed by the rectum, ileum, appendix, and cecum^4,8 (FIGURES 3, 4, and 5). Case reports also have described endometrial implants on the stomach and transverse colon.⁹ Although isolated bowel involvement has been recognized, most patients with bowel endometriosis have concurrent disease elsewhere.^2,4 

Historically, segmental resection was performed regardless of the anatomical location of the lesion.¹⁰ Even today, many surgeons continue to routinely perform segmental bowel resection as a first-line surgical approach.¹¹ Unnecessary segmental resection, however, places patients at risk for short- and long-term postoperative morbidity, including the possibility of permanent ostomy. Modern surgical techniques, such as shaving excision and disc resection, have been performed to successfully treat bowel endometriosis with excellent long-term outcomes and fewer complications when compared with traditional segmental resection.^2,12-16

In this article, we focus on the clinical indications and surgical techniques for video-laparoscopic management, but first we describe the pathophysiology, clinical presentation, and diagnosis of bowel endometriosis.

Pathophysiology of bowel endometriosis

The pathogenesis of endometriosis remains unknown, as no single mechanism explains all clinical cases of the disease. The most popular proposed theory describes retrograde menstruation through the fallopian tubes.¹⁷ Once inside the peritoneal cavity, endometrial cells attach to and invade healthy peritoneum, establishing a blood supply necessary for growth and survival.

In the case of bowel endometriosis, deposition of effluxed endometrial cells may lead to an inflammatory response that increases the risk of adhesion formation, leading to potential cul-de-sac obliteration. Lesions may originate as Allen-Masters peritoneal defects, developing into deeply infiltrative rectovaginal septum lesions. The anatomical shelter theory contributes to lesions within the pelvis, with the rectosigmoid colon blocking the cephalad flow of effluxed menstrual blood from the pelvis, thus leading to a preponderance of lesions in the pelvis and along the rectosigmoid colon.²

Continue to: Clinical presentation and diagnosis...

Clinical presentation and diagnosis

Women presenting with endometriosis of the bowel are typically of reproductive age and commonly report symptoms of dysmenorrhea, chronic pelvic pain, dyspareunia, and dyschezia. Some women also experience catamenial diarrhea, constipation, hematochezia, and bloating.² The differential diagnosis of these symptoms is broad and includes irritable bowel disease, ischemic colitis, inflammatory bowel disease, diverticulitis, pelvic inflammatory disease, and malignancy.

Because of its nonspecific symptoms, bowel endometriosis is often misdiagnosed and the disease goes untreated for years.¹⁸ Therefore, it is imperative that clinicians maintain a high index of suspicion when evaluating reproductive-aged women with gastrointestinal symptoms and pelvic pain.

Physical examination can be helpful in making the diagnosis of endometriosis. During bimanual examination, findings such as a fixed, tender, or retroverted uterus, uterosacral ligament nodularity, or an enlarged adnexal mass representing an ovarian endometrioma may be appreciated. Rectovaginal exam can identify areas of tenderness and nodularity along the rectovaginal septum. Speculum exam may reveal a laterally displaced cervix or blue powder-burn lesions along the cervix or posterior fornix.¹⁹ Rarely, endometriosis is found on the perineum within an episiotomy scar.²⁰

Imaging studies can be used in conjunction with physical examination findings to aid in the diagnosis of endometriosis. Images also guide preoperative planning by characterizing lesions based on their size, location, and depth of invasion. Hudelist and colleagues found transvaginal ultrasound (TVUS) to have an overall sensitivity of 71% to 98% and a specificity of 92% to 100%.²¹ However, it was noted that the accuracy of the diagnosis was directly related to the experience of the sonographer, and lesions above the sigmoid colon were generally unable to be diagnosed. Other imaging modalities that have been reported to have high sensitivity and specificity for diagnosing bowel endometriosis include rectal water contrast TVUS,^22,23 rectal endoscopic sonography,²² magnetic resonance imaging,²² and barium enema.²⁴

Medical management

Medical therapy for patients with endometriosis is utilized with the goal of suppressing ovulation, lowering circulating hormone levels, and inducing endometrial atrophy. Medications commonly employed include gonadotropin-releasing hormone agonists and antagonists, anabolic steriods such as danazol, combined oral contraceptive pills, progestins, and aromatase inhibitors.

Continue to: To date, no optimal hormonal regimen...

To date, no optimal hormonal regimen has been established for the treatment of bowel endometriosis. Vercellini and colleagues demonstrated that progestins with and without low-dose estrogen improved symptoms of dysmenorrhea and dyspareunia.²⁵ Ferrero and colleagues reported that 2.5 mg of norethindrone daily resulted in 53% of women with colorectal endometriosis reporting improved gastrointestinal symptoms.²⁶ However, by 12 months of follow-up, 33% of these patients had elected to undergo surgical management.

Gonadotropin-releasing hormone agonists, such as leuprolide acetate, also can be used to mitigate symptoms of bowel endometriosis or to decrease disease burden at the time of surgery, and they can be used with add-back norethindrone acetate. The use of these medications is limited by adverse effects, such as vasomotor symptoms and decreased bone mineral density when used for longer than 6 months.²

Medical therapy is commonly used for patients with mild to moderate symptoms and in those who are poor surgical candidates or decline surgical intervention. Medical therapy is especially useful when employed postoperatively to suppress the regrowth of microscopic ectopic endometrial tissue.

Patients must be counseled, however, that even with medical management, they may still require surgery in the future to control their symptoms and/or to preserve organ function.²

Surgical management

Surgical treatment for bowel endometriosis depends on the disease location, the size and depth of the lesion, the presence or absence of stricture, and the surgeon’s level of expertise.^2,12,27-30

In our group, we advocate for video-laparoscopy, with or without robotic as sistance. Minimally invasive surgery offers reduced blood loss, shorter recovery time, and fewer postoperative complications compared with laparotomy.^{2,16,27,31-33} The conversion rate to laparotomy has been reported to be about 3% when performed by an experienced surgeon.¹²

Darai and colleagues conducted a randomized trial of 52 patients undergoing surgery for colorectal endometriosis via either laparoscopic or open colon resection.³³ Blood loss was significantly lower in the laparoscopy group (1.6 vs 2.7 mg/L, P <.05). No difference was noted in long-term outcomes. In a retrospective study of 436 cases, Ruffo and colleagues showed that those who underwent laparoscopic colorectal resection had higher postoperative pregnancy rates compared with those who had laparotomy (57.6% vs 23.1%, P <.035).³²

The goal of surgical management of bowel endometriosis is to remove as many of the endometriotic lesions as possible while minimizing short- and long-term complications. Three surgical approaches have been described: shaving excision, disc resection, and segmental resection.²

Some surgeons prefer traditional segmental resection of the bowel regardless of the anatomical site, citing reduced disease recurrence with this approach; however, traditional segmental resection confers increased risk of complications. Increasingly, in an effort to reduce morbidity, more surgeons are advocating for the less aggressive methods of shaving excision and disc resection.

Aggressive resection at the level of the low rectum requires extensive surgical dissection of the retrorectal space, with the potential for inadvertent injury to surrounding neurovascular structures, such as the pelvic splanchnic nerves and superior and inferior hypogastric plexus.²⁹ Injury to these structures can lead to significant complications, including bowel stenosis, fistula formation, constipation, and urinary retention. Complete resection of other areas, such as the small bowel, do not carry the same risks and may have more significant benefit to the patient than less aggressive techniques.

Our group recommends carefully balancing the risks and benefits of aggressive surgical treatment for each individual and treating the patient with the appropriate technique. Regardless of technique, surgical treatment of bowel endometriosis can lead to long-term improvements in pain and infertility.^29,30,34,35

Continue to: Shaving excision...

Shaving excision

The most conservative approach to resection of bowel endometriosis is shaving excision; this involves removing endometriotic tissue layer-by-layer until healthy, underlying tissue is encountered.² With bowel endometriosis, the goal of shaving excision is to remove as much of the diseased tissue as possible while leaving behind the mucosal layer and a portion of the muscularis.^{2,15,16,36-38} This is the most conservative of the 3 surgical techniques and is associated with the lowest complication rate.^{2,14,15,36,37}

Our group reported on 185 women who underwent shaving excision for bowel endometriosis. At the time of surgery, 80 women had complete obliteration of the cul-de-sac (FIGURE 6). Of the study patients, 174 patients were available for follow-up, with 93% reporting moderate to complete pain relief.¹⁵

In a retrospective analysis of 3,298 surgeries for rectovaginal endometriosis in which shaving excision was used on all but 1% of patients, Donnez and colleagues reported a very low complication rate, with 1 case of rectal perforation, 1 case of fecal peritonitis, and 3 cases of ureteral injury.³⁹

Roman and colleagues described the use of shaving excision for rectal endometriosis using plasma energy (n = 54) and laparoscopic scissors (n = 68).⁴⁰ Only 4% of patients reported experiencing symptom recurrence, and the pregnancy rate was 65.4%, with 59% of those patients spontaneously conceiving. Two cases of rectal fistula were noted.

Disc resection

Laparoscopic disc excision has been described in the literature since the 1980s, and the technique involves the full-thickness removal of the diseased portion of the bowel, followed by closure of the remaining defect.^{2,12-14,28,29,31,41-45} To be appropriate for this technique, a lesion should involve only a portion of the bowel wall and, preferably, less than one-half of the bowel circumference.^2,42 Disc excision results in excellent outcomes with fewer postoperative complications than segmental resection, but with more complications when compared to shaving excision.^{2,12,13,29,45,46}

We reported on a series of 141 women with bowel endometriosis who underwent disc excision.² At 1-month follow-up, 87% of patients experienced an improvement in their symptoms. No cases required conversion to laparotomy or were complicated by rectovaginal fistula formation, ureteral injury, bowel perforation, or pelvic abscess.²

Continue to: Segmental resection...

Segmental resection

The most aggressive surgical approach, segmental resection involves complete removal of a diseased portion of bowel, followed by side-to-side or end-to-end reanastomosis of the adjacent segments.² For this procedure, a multidisciplinary approach is recommended, with involvement of a colorectal surgeon or gynecologic oncologist trained in performing bowel resections. Segmental resection is indicated for lesions that are larger than 3 cm, circumferential, obstructive, or multifocal.

Given the higher complication rate associated with this procedure and the good outcomes associated with less invasive techniques, we avoid segmental resection whenever possible, especially for lesions near the anal verge.²

Complications associated with surgical approach

In 2005, our group reported on a cohort of 178 women who underwent laparoscopic treatment of deeply infiltrative bowel endometriosis with shaving excision (n = 93), disc excision (n = 38), and segmental resection (n = 47).³⁴ The major complication rate was significantly higher for those undergoing segmental resection (12.5%, P <.001); only 7.7% of those who underwent disc resection experienced a major complication; and none were observed in the group treated with shaving excision.

In 2011, De Cicco and colleagues conducted a systematic review of 1,889 patients who underwent segmental bowel resection.³⁵ The major complication rate was 11%, with a leakage rate of 2.7%, fistula rate of 1.8%, major obstruction rate of 2.7%, and hemorrhage rate of 2.5%. Many of these complications, however, occurred in patients who had low rectal resections.

Regardless of surgical approach, the complication rate is related to the surgeon’s ability to preserve the superior and inferior hypogastric plexuses and the sympathetic and parasympathetic nerve bundles (FIGURE 7). Nerve-sparing techniques should be used to decrease the incidence of postoperative bowel, bladder, and sexual function complications.² 

Our group’s preferences

In our practice, we emphasize that the choice of surgical technique depends on the location, size, and depth of the lesion, as well as the extent of bowel wall circumferential invasion.²

We categorize lesions by their anatomic location: those above the sigmoid colon, on the sigmoid colon, on the rectosigmoid colon, and on the rectum. For lesions above the sigmoid colon, segmental or disc resection is appropriate.² We recommend segmental resection for multifocal lesions, lesions larger than 3 cm, or for lesions involving more than one-third of the bowel lumen.^37,44,45,47 Disc resection is appropriate for lesions smaller than 3 cm even if the bowel lumen is involved.^44,45,48 If endometriosis is encountered in any location along the bowel, appendectomy can be performed even without visible disease, due to a high incidence of occult disease of the appendix.^49,50

When lesions involve the sigmoid colon, we prefer utilizing shaving excision when possible to limit dissection of the retrorectal space and pelvic sidewall nerves.² Segmental resection at or below the sigmoid colon has been associated with postoperative surgical site leakage⁵¹ and long-term bowel and bladder dysfunction with risk of permanent colostomy.^52,53 For lesions smaller than 3 cm or involving less than one-third of the bowel lumen, disc resection can be performed. Segmental resection is required if multifocal disease or obstruction are present, if lesions are larger than 3 cm, or if more than one-third of the bowel lumen is involved.

For lesions along the rectosigmoid colon, we prefer utilizing shaving excision when possible.² Disc excision can be performed utilizing a transanal approach, being mindful to minimize dissection of the retroperitoneal space and pelvic sidewall nerves.⁴⁸ Segmental resection is avoided even with lesions larger than 3 cm, unless prior surgery has failed. Approaches for segmental resection can utilize laparoscopy or the natural orifices of the rectum or vagina.^31,51

For lesions on the rectum, we strongly advise shaving excision.² Evidence fails to show that the benefits of segmental resection outweigh the risks when compared to conservative techniques at the rectum.^30,39,54 There is evidence indicating that aggressive surgery 5 to 8 cm from the anal verge is predictive of postoperative complications.⁵⁵ In our group, we use shaving excision to remove as much disease as possible without compromising the integrity of the bowel wall or surrounding neurovascular structures. We err on the side of caution, leaving some of the disease on the rectum to avoid rectal perforation, and plan for postoperative hormonal suppression in these patients.

For patients desiring fertility, successful pregnancy is often achieved using the shaving technique.⁴¹

About 10% of all reproductive-aged women and 35% to 50% of women with pelvic pain and infertility are affected by endometriosis.^1,2 The disease typically involves the reproductive tract organs, anterior and posterior cul-de-sacs, and uterosacral ligaments. However, disease outside of the reproductive tract occurs frequently and has been found on all organs except the spleen.³

The bowel is the most common site for extragenital endometriosis, affected in an estimated 3.8% to 37% of patients with known endometriosis.^4-7 Implants may be superficial, involving the bowel serosa and subserosa (FIGURE 1), or they can manifest as deeply infiltrating lesions involving the muscularis and mucosa (FIGURE 2). The rectosigmoid colon is the most common location for bowel endometriosis, followed by the rectum, ileum, appendix, and cecum^4,8 (FIGURES 3, 4, and 5). Case reports also have described endometrial implants on the stomach and transverse colon.⁹ Although isolated bowel involvement has been recognized, most patients with bowel endometriosis have concurrent disease elsewhere.^2,4 

Historically, segmental resection was performed regardless of the anatomical location of the lesion.¹⁰ Even today, many surgeons continue to routinely perform segmental bowel resection as a first-line surgical approach.¹¹ Unnecessary segmental resection, however, places patients at risk for short- and long-term postoperative morbidity, including the possibility of permanent ostomy. Modern surgical techniques, such as shaving excision and disc resection, have been performed to successfully treat bowel endometriosis with excellent long-term outcomes and fewer complications when compared with traditional segmental resection.^2,12-16

In this article, we focus on the clinical indications and surgical techniques for video-laparoscopic management, but first we describe the pathophysiology, clinical presentation, and diagnosis of bowel endometriosis.

Pathophysiology of bowel endometriosis

The pathogenesis of endometriosis remains unknown, as no single mechanism explains all clinical cases of the disease. The most popular proposed theory describes retrograde menstruation through the fallopian tubes.¹⁷ Once inside the peritoneal cavity, endometrial cells attach to and invade healthy peritoneum, establishing a blood supply necessary for growth and survival.

In the case of bowel endometriosis, deposition of effluxed endometrial cells may lead to an inflammatory response that increases the risk of adhesion formation, leading to potential cul-de-sac obliteration. Lesions may originate as Allen-Masters peritoneal defects, developing into deeply infiltrative rectovaginal septum lesions. The anatomical shelter theory contributes to lesions within the pelvis, with the rectosigmoid colon blocking the cephalad flow of effluxed menstrual blood from the pelvis, thus leading to a preponderance of lesions in the pelvis and along the rectosigmoid colon.²

Continue to: Clinical presentation and diagnosis...

Clinical presentation and diagnosis

Women presenting with endometriosis of the bowel are typically of reproductive age and commonly report symptoms of dysmenorrhea, chronic pelvic pain, dyspareunia, and dyschezia. Some women also experience catamenial diarrhea, constipation, hematochezia, and bloating.² The differential diagnosis of these symptoms is broad and includes irritable bowel disease, ischemic colitis, inflammatory bowel disease, diverticulitis, pelvic inflammatory disease, and malignancy.

Because of its nonspecific symptoms, bowel endometriosis is often misdiagnosed and the disease goes untreated for years.¹⁸ Therefore, it is imperative that clinicians maintain a high index of suspicion when evaluating reproductive-aged women with gastrointestinal symptoms and pelvic pain.

Physical examination can be helpful in making the diagnosis of endometriosis. During bimanual examination, findings such as a fixed, tender, or retroverted uterus, uterosacral ligament nodularity, or an enlarged adnexal mass representing an ovarian endometrioma may be appreciated. Rectovaginal exam can identify areas of tenderness and nodularity along the rectovaginal septum. Speculum exam may reveal a laterally displaced cervix or blue powder-burn lesions along the cervix or posterior fornix.¹⁹ Rarely, endometriosis is found on the perineum within an episiotomy scar.²⁰

Imaging studies can be used in conjunction with physical examination findings to aid in the diagnosis of endometriosis. Images also guide preoperative planning by characterizing lesions based on their size, location, and depth of invasion. Hudelist and colleagues found transvaginal ultrasound (TVUS) to have an overall sensitivity of 71% to 98% and a specificity of 92% to 100%.²¹ However, it was noted that the accuracy of the diagnosis was directly related to the experience of the sonographer, and lesions above the sigmoid colon were generally unable to be diagnosed. Other imaging modalities that have been reported to have high sensitivity and specificity for diagnosing bowel endometriosis include rectal water contrast TVUS,^22,23 rectal endoscopic sonography,²² magnetic resonance imaging,²² and barium enema.²⁴

Medical management

Medical therapy for patients with endometriosis is utilized with the goal of suppressing ovulation, lowering circulating hormone levels, and inducing endometrial atrophy. Medications commonly employed include gonadotropin-releasing hormone agonists and antagonists, anabolic steriods such as danazol, combined oral contraceptive pills, progestins, and aromatase inhibitors.

Continue to: To date, no optimal hormonal regimen...

To date, no optimal hormonal regimen has been established for the treatment of bowel endometriosis. Vercellini and colleagues demonstrated that progestins with and without low-dose estrogen improved symptoms of dysmenorrhea and dyspareunia.²⁵ Ferrero and colleagues reported that 2.5 mg of norethindrone daily resulted in 53% of women with colorectal endometriosis reporting improved gastrointestinal symptoms.²⁶ However, by 12 months of follow-up, 33% of these patients had elected to undergo surgical management.

Gonadotropin-releasing hormone agonists, such as leuprolide acetate, also can be used to mitigate symptoms of bowel endometriosis or to decrease disease burden at the time of surgery, and they can be used with add-back norethindrone acetate. The use of these medications is limited by adverse effects, such as vasomotor symptoms and decreased bone mineral density when used for longer than 6 months.²

Medical therapy is commonly used for patients with mild to moderate symptoms and in those who are poor surgical candidates or decline surgical intervention. Medical therapy is especially useful when employed postoperatively to suppress the regrowth of microscopic ectopic endometrial tissue.

Patients must be counseled, however, that even with medical management, they may still require surgery in the future to control their symptoms and/or to preserve organ function.²

Surgical management

Surgical treatment for bowel endometriosis depends on the disease location, the size and depth of the lesion, the presence or absence of stricture, and the surgeon’s level of expertise.^2,12,27-30

In our group, we advocate for video-laparoscopy, with or without robotic as sistance. Minimally invasive surgery offers reduced blood loss, shorter recovery time, and fewer postoperative complications compared with laparotomy.^{2,16,27,31-33} The conversion rate to laparotomy has been reported to be about 3% when performed by an experienced surgeon.¹²

Darai and colleagues conducted a randomized trial of 52 patients undergoing surgery for colorectal endometriosis via either laparoscopic or open colon resection.³³ Blood loss was significantly lower in the laparoscopy group (1.6 vs 2.7 mg/L, P <.05). No difference was noted in long-term outcomes. In a retrospective study of 436 cases, Ruffo and colleagues showed that those who underwent laparoscopic colorectal resection had higher postoperative pregnancy rates compared with those who had laparotomy (57.6% vs 23.1%, P <.035).³²

The goal of surgical management of bowel endometriosis is to remove as many of the endometriotic lesions as possible while minimizing short- and long-term complications. Three surgical approaches have been described: shaving excision, disc resection, and segmental resection.²

Some surgeons prefer traditional segmental resection of the bowel regardless of the anatomical site, citing reduced disease recurrence with this approach; however, traditional segmental resection confers increased risk of complications. Increasingly, in an effort to reduce morbidity, more surgeons are advocating for the less aggressive methods of shaving excision and disc resection.

Aggressive resection at the level of the low rectum requires extensive surgical dissection of the retrorectal space, with the potential for inadvertent injury to surrounding neurovascular structures, such as the pelvic splanchnic nerves and superior and inferior hypogastric plexus.²⁹ Injury to these structures can lead to significant complications, including bowel stenosis, fistula formation, constipation, and urinary retention. Complete resection of other areas, such as the small bowel, do not carry the same risks and may have more significant benefit to the patient than less aggressive techniques.

Our group recommends carefully balancing the risks and benefits of aggressive surgical treatment for each individual and treating the patient with the appropriate technique. Regardless of technique, surgical treatment of bowel endometriosis can lead to long-term improvements in pain and infertility.^29,30,34,35

Continue to: Shaving excision...

Shaving excision

The most conservative approach to resection of bowel endometriosis is shaving excision; this involves removing endometriotic tissue layer-by-layer until healthy, underlying tissue is encountered.² With bowel endometriosis, the goal of shaving excision is to remove as much of the diseased tissue as possible while leaving behind the mucosal layer and a portion of the muscularis.^{2,15,16,36-38} This is the most conservative of the 3 surgical techniques and is associated with the lowest complication rate.^{2,14,15,36,37}

Our group reported on 185 women who underwent shaving excision for bowel endometriosis. At the time of surgery, 80 women had complete obliteration of the cul-de-sac (FIGURE 6). Of the study patients, 174 patients were available for follow-up, with 93% reporting moderate to complete pain relief.¹⁵

In a retrospective analysis of 3,298 surgeries for rectovaginal endometriosis in which shaving excision was used on all but 1% of patients, Donnez and colleagues reported a very low complication rate, with 1 case of rectal perforation, 1 case of fecal peritonitis, and 3 cases of ureteral injury.³⁹

Roman and colleagues described the use of shaving excision for rectal endometriosis using plasma energy (n = 54) and laparoscopic scissors (n = 68).⁴⁰ Only 4% of patients reported experiencing symptom recurrence, and the pregnancy rate was 65.4%, with 59% of those patients spontaneously conceiving. Two cases of rectal fistula were noted.

Disc resection

Laparoscopic disc excision has been described in the literature since the 1980s, and the technique involves the full-thickness removal of the diseased portion of the bowel, followed by closure of the remaining defect.^{2,12-14,28,29,31,41-45} To be appropriate for this technique, a lesion should involve only a portion of the bowel wall and, preferably, less than one-half of the bowel circumference.^2,42 Disc excision results in excellent outcomes with fewer postoperative complications than segmental resection, but with more complications when compared to shaving excision.^{2,12,13,29,45,46}

We reported on a series of 141 women with bowel endometriosis who underwent disc excision.² At 1-month follow-up, 87% of patients experienced an improvement in their symptoms. No cases required conversion to laparotomy or were complicated by rectovaginal fistula formation, ureteral injury, bowel perforation, or pelvic abscess.²

Continue to: Segmental resection...

Segmental resection

The most aggressive surgical approach, segmental resection involves complete removal of a diseased portion of bowel, followed by side-to-side or end-to-end reanastomosis of the adjacent segments.² For this procedure, a multidisciplinary approach is recommended, with involvement of a colorectal surgeon or gynecologic oncologist trained in performing bowel resections. Segmental resection is indicated for lesions that are larger than 3 cm, circumferential, obstructive, or multifocal.

Given the higher complication rate associated with this procedure and the good outcomes associated with less invasive techniques, we avoid segmental resection whenever possible, especially for lesions near the anal verge.²

Complications associated with surgical approach

In 2005, our group reported on a cohort of 178 women who underwent laparoscopic treatment of deeply infiltrative bowel endometriosis with shaving excision (n = 93), disc excision (n = 38), and segmental resection (n = 47).³⁴ The major complication rate was significantly higher for those undergoing segmental resection (12.5%, P <.001); only 7.7% of those who underwent disc resection experienced a major complication; and none were observed in the group treated with shaving excision.

In 2011, De Cicco and colleagues conducted a systematic review of 1,889 patients who underwent segmental bowel resection.³⁵ The major complication rate was 11%, with a leakage rate of 2.7%, fistula rate of 1.8%, major obstruction rate of 2.7%, and hemorrhage rate of 2.5%. Many of these complications, however, occurred in patients who had low rectal resections.

Regardless of surgical approach, the complication rate is related to the surgeon’s ability to preserve the superior and inferior hypogastric plexuses and the sympathetic and parasympathetic nerve bundles (FIGURE 7). Nerve-sparing techniques should be used to decrease the incidence of postoperative bowel, bladder, and sexual function complications.² 

Our group’s preferences

In our practice, we emphasize that the choice of surgical technique depends on the location, size, and depth of the lesion, as well as the extent of bowel wall circumferential invasion.²

We categorize lesions by their anatomic location: those above the sigmoid colon, on the sigmoid colon, on the rectosigmoid colon, and on the rectum. For lesions above the sigmoid colon, segmental or disc resection is appropriate.² We recommend segmental resection for multifocal lesions, lesions larger than 3 cm, or for lesions involving more than one-third of the bowel lumen.^37,44,45,47 Disc resection is appropriate for lesions smaller than 3 cm even if the bowel lumen is involved.^44,45,48 If endometriosis is encountered in any location along the bowel, appendectomy can be performed even without visible disease, due to a high incidence of occult disease of the appendix.^49,50

When lesions involve the sigmoid colon, we prefer utilizing shaving excision when possible to limit dissection of the retrorectal space and pelvic sidewall nerves.² Segmental resection at or below the sigmoid colon has been associated with postoperative surgical site leakage⁵¹ and long-term bowel and bladder dysfunction with risk of permanent colostomy.^52,53 For lesions smaller than 3 cm or involving less than one-third of the bowel lumen, disc resection can be performed. Segmental resection is required if multifocal disease or obstruction are present, if lesions are larger than 3 cm, or if more than one-third of the bowel lumen is involved.

For lesions along the rectosigmoid colon, we prefer utilizing shaving excision when possible.² Disc excision can be performed utilizing a transanal approach, being mindful to minimize dissection of the retroperitoneal space and pelvic sidewall nerves.⁴⁸ Segmental resection is avoided even with lesions larger than 3 cm, unless prior surgery has failed. Approaches for segmental resection can utilize laparoscopy or the natural orifices of the rectum or vagina.^31,51

For lesions on the rectum, we strongly advise shaving excision.² Evidence fails to show that the benefits of segmental resection outweigh the risks when compared to conservative techniques at the rectum.^30,39,54 There is evidence indicating that aggressive surgery 5 to 8 cm from the anal verge is predictive of postoperative complications.⁵⁵ In our group, we use shaving excision to remove as much disease as possible without compromising the integrity of the bowel wall or surrounding neurovascular structures. We err on the side of caution, leaving some of the disease on the rectum to avoid rectal perforation, and plan for postoperative hormonal suppression in these patients.

For patients desiring fertility, successful pregnancy is often achieved using the shaving technique.⁴¹

Endometriosis is a benign disease characterized by endometrial glands and stroma outside of the uterine cavity. It is commonly associated with pelvic pain and infertility. Ectopic endometrial tissue is predominantly located in the pelvis, but it can appear anywhere in the body, where it is referred to as extragenital endometriosis. The bowel and urinary tract are the most common sites of extragenital endometriosis.¹

Laparoscopic management of extragenital endometriosis has been described since the 1980s.² However, laparoscopic management of genitourinary endometriosis is still not widespread.^3,4 Physicians are often unfamiliar with the signs and symptoms of genitourinary endometriosis and fail to consider it when a patient presents with bladder pain or hematuria, which may or may not be cyclic. Furthermore, many gynecologists do not have the experience to correctly identify the various forms of endometriosis that may appear on the pelvic organ, including the serosa and peritoneum, as variable colored spots, blebs, lesions, or adhesions. Many surgeons are also not adequately trained in the advanced laparoscopic techniques required to treat genitourinary endometriosis.⁴

In this article, we describe the clinical presentation and diagnosis of genitourinary endometriosis and discuss laparoscopic management strategies with and without robotic assistance.

Clinical presentation and diagnosis of genitourinary endometriosis

While ureteral and bladder endometriosis are both diseases of the urinary tract, they are not always found together in the same patient. The bladder is the most commonly affected organ, followed by the ureter and kidney.^3,5,6 Endometriosis of the bladder usually presents with significant lower urinary tract symptoms. In contrast, ureteral endometriosis is usually silent with no apparent urinary symptoms.

Ureteral endometriosis. Cyclic hematuria is present in less than 15% of patients with ureteral endometriosis. Some patients experience cyclic, nonspecific colicky flank pain.^7-9 Otherwise, most patients present with the usual symptoms of endometriosis, such as pelvic pain and dysmenorrhea. In a systematic review, Cavaco-Gomes and colleagues described 700 patients with ureteral endometriosis; 81% reported dysmenorrhea, 70% had pelvic pain, and 66% had dyspareunia.¹⁰ Rarely, ureteral endometriosis can result in silent kidney loss if the ureter becomes severely obstructed without treatment.^11,12

Continue to: The lack of symptoms makes...

The lack of symptoms makes the early diagnosis of ureteral endometriosis difficult. As with all types of endometriosis, histologic evaluation of a biopsy sample is diagnostic. Multiple imaging modalities have been used to preoperatively diagnose ureteral involvement, including computed tomography,¹³ magnetic resonance imaging (MRI),¹⁴ intravenous pyelogram (IVP), and pelvic ultrasonography. However, each of these imaging modalities is limited in both sensitivity and the ability to characterize depth of tissue invasion.

In a study of 245 women undergoing pelvic ultrasonography, Pateman and colleagues reported that an experienced sonographer was able to visualize the bilateral ureters in 93% of cases.¹⁵ Renal ultrasonography is indicated in any woman suspected of having genitourinary tract involvement with the degree of hydroureter and level of obstruction noted during the exam.¹⁶

In our group, we perform renography to assess kidney function when hydroureter is noted preoperatively. Studies suggest that if greater than 10% of normal glomerular filtration rate remains, the kidney is considered salvageable, and near-normal function often returns following resection of disease. If preoperative kidney function is noted to be less than 10%, consultation with a nephrologist for possible nephrectomy is warranted.

We find that IVP is often helpful for preoperatively identifying the level and degree of ureteral involvement, and it also can be used postoperatively to evaluate for ureteral continuity (FIGURE 1). Sillou and colleagues showed MRI to be adequately sensitive for the detection of intrinsic ureteral endometriosis, but they reported that MRI often overestimates the frequency of disease.¹⁷ Authors of a 2016 Cochrane review of imaging modalities for endometriosis, including 4,807 women in 49 studies, reported that no imaging test was superior to surgery for diagnosing endometriosis.¹⁸ However, the review notably excluded genitourinary tract endometriosis, as surgery is not an acceptable reference standard, given that many surgeons cannot reliably identify such lesions.¹⁸

Bladder endometriosis. Unlike patients with ureteral endometriosis, those with bladder endometriosis are typically symptomatic and experience dysuria, hematuria, urinary frequency, and suprapubic tenderness.^7,19 Urinary tract infection, interstitial cystitis, and cancer must be considered in the differential diagnosis. Urinalysis and urine culture should be performed, and other diagnostic procedures such as ultrasonography, MRI, and cystoscopy should be considered to evaluate for endometriosis of the bladder.

Ultrasound and MRI of the bladder both demonstrate a high specificity for detecting bladder endometriosis, but they lack sensitivity for lesions less than 3 cm.²⁰ Deep infiltrating endometriosis of the bladder can be identified at the time of cystoscopy, which can assist in determining the need for ureteroneocystostomy if lesions are within 2 cm of the urethral opening.²⁰ Cystoscopy also allows for biopsy to be performed if underlying malignancy is of concern.¹⁹

In our group, when bladder endometriosis is suspected, we routinely perform preoperative bladder ultrasonography to identify the lesion and plan to perform intraoperative cystoscopy at the time of laparoscopic resection.^19,21

Continue to: Treatment...

Treatment

Medical management

Empiric medical therapies for endometriosis are centered around the idea that ectopic endometrial tissue responds to treatment in a similar manner as normal eutopic endometrium. The goals of treatment are to reduce or eliminate cyclic menstruation, thereby decreasing peritoneal seeding and suppressing the growth and activity of established ectopic implants. Medical therapy commonly involves the use of gonadotropin-releasing hormone agonists or antagonists, danazol, combined oral contraceptives, progestins, and aromatase inhibitors.

Medical therapy is commonly employed for patients with mild or early-stage disease and in those who are poor surgical candidates or decline surgery. Medical management alone clearly is contraindicated in the setting of ureteral obstruction and—in our opinion—may not be a good option for those with endometriosis of the ureter, given the potential for recurrence and potential serious sequelae of reduced renal function.²² Therefore, surgery has become the standard approach to therapy for mild to moderate cases of ureteral endometriosis.³

Medical therapy for patients with endometriosis of the bladder is generally considered a temporary solution as hormonal suppression, with its associated adverse effects, must be maintained throughout menopause. However, if endometriosis lesions lie within close proximity to the trigone, medical management is preferred, as surgical excision in the area of the trigone may predispose patients to neurogenic bladder and retrograde bladder reflux.^23,24

Surgical management

The objectives of surgical treatment for genitourinary tract endometriosis are to excise all visible disease, to prevent or delay recurrence of the disease to the extent possible, and to avoid any further morbidity—in particular, to preserve renal function in cases of ureteral endometriosis—and to avoid iatrogenic injury to surrounding pelvic nervous structures^25-27 (FIGURE 2). The surgical approach depends on the technical expertise of the surgeon and the availability of necessary instrumentation. In our experience, laparoscopy with or without robotic assistance is the preferred surgical approach.^{3,4,6,11,28-32}

Others have reported on the benefits of laparoscopy over laparotomy for the surgical management of genitourinary endometriosis. In a review of 61 patients who underwent either robot-assisted laparoscopic (n = 25) or open (n = 41) ureteroneocystostomy (n = 41), Isac and colleagues reported the procedure was longer in the laparoscopic group (279 min vs 200 min, P<.001), but the laparoscopic group had a shorter hospital stay (3 days vs 5 days, P<.001), used fewer narcotics postoperatively (P<.001), and had lower intraoperative blood loss (100 mL vs 150 mL, P<.001).³² No differences in long-term outcomes were observed in either cohort.

In a systematic review of 700 patients undergoing laparoscopic surgery for ureteral endometriosis, Cavaco-Gomes and colleagues reported that conversion to laparotomy occurred in only 3% to 7% of cases.¹⁰ In instances of ureteral endometriosis, laparoscopy provides greater visualization of the intraperitoneal contents over laparotomy, enabling better evaluation and treatment of lesions.^3,29,33,34 Robot-assisted laparoscopy provides the additional advantages of 3D visualization, potential for an accelerated learning curve over traditional laparoscopy, improvement in dissection technique, and ease of suturing technique.^6,35,36

Continue to: Extrinsic disease...

Extrinsic disease. In our group, we perform ureterolysis for extrinsic disease.²⁵ The peritoneal incision is made in an area unaffected by endometriosis. Using the suction irrigator, a potential space is developed under the serosa of the ureter by injecting normal saline or lactated Ringer’s solution. By creating a fluid barrier between the serosa and underlying tissues, the depth of surgical incision and lateral thermal spread are minimized. Grasping forceps are used to peel the peritoneum away.^25,37,38

Intrinsic disease. Unlike extrinsic disease, intrinsic disease can infiltrate the muscularis, lamina propria, and ureteral lumen, resulting in proximal dilation of the ureter with strictures.⁸ In this situation, ureteral compromise is likely and resection of the ureter is indicated^3,28 (FIGURE 3). Intrinsic disease can be suggested by preoperative imaging or when there is evidence of deep infiltrating disease on physical exam, such as rectovaginal nodularity.^30,39 When intrinsic ureteral disease is known, consultation with a urologist to plan a joint procedure is advisable. The procedure chosen to re-establish a functional ureter following resection depends on the location and extent of the involved ureter. Resection in close proximity to the bladder may be repaired by ureteroneocystostomy with or without psoas hitch,^30,39,40 whereas resection of more proximal ureter may be repaired using Boari flap, ileal interposition, or autotransplantation. Lesions in the upper third or middle ureter may be repaired using ureterouretral anastomosis.^6,7,30,41-43

Continue to: Bladder endometriosis...

Bladder endometriosis. Surgical treatment for bladder endometriosis depends on the depth of invasion and the location of the lesion (FIGURE 4). Lesions of the superficial aspect of the bladder identified at the time of laparoscopy can be treated with either excision or fulguration^28,35,44 In our group, we perform excision over fulguration to remove the entire lesion and obtain a pathologic diagnosis. Deeper lesions involving the detrusor muscle are likely to be an endometrioma of the bladder. In these cases, laparoscopic excision is recommended.⁷ Rarely, lesions close to the interureteric ridge may require ureteroneocystostomy.^19,45

In our experience, laparoscopic resection of bladder endometriomas is associated with better results in terms of symptom relief, progression of disease, and recurrence risk compared with other approaches. When performing laparoscopic excision of bladder lesions, we concomitantly evaluate the bladder lesion via cystoscopy to ensure adequate margins are obtained. Double-J stent placement is advised when lesions are within 2 cm of the urethral meatus to ensure ureteral patency during the postoperative period.⁴⁵ A postoperative cystogram routinely is performed 7 to 14 days after surgery to ensure adequate repair prior to removing the urinary catheter.^9,25,46,47

Postsurgical follow-up

Follow-up after treatment of genitourinary tract endometriosis should include monitoring the patient for symptoms of recurrence. Regular history and physical examination, renal function testing, and, in some instances, pelvic ultrasonography, all have a role in surveillance for recurrent ureteric disease. IVP or MRI may be warranted if a recurrence is suspected. A high index of suspicion should be maintained on the part of the clinician to avoid the devastating consequences of silent kidney loss. Patients should be counseled about the risk of disease recurrence, especially in those not undergoing postoperative hormonal suppression.

In conclusion

While endometriosis of the genitourinary tract is rare, patients can experience significant morbidity. Medical management of the disease is often limited by substantial adverse effects that limit treatment duration and is best used postoperatively after excision. An adequate physical exam and preoperative diagnostic imaging can be employed to characterize the extent of disease. When extensive disease involving the ureter is suspected, preoperative consultation with a urologist is encouraged to plan a multidisciplinary approach to surgical resection.

The ideal approach to surgery is laparoscopic resection with or without robotic assistance. Treatment of ureteral disease most commonly involves ureterolysis for cases of extrinsic disease but may require total resection of the ureter with concurrent ureteral reconstruction when disease is intrinsic to the ureter. Surgery for bladder endometriosis depends on the depth of invasion and location of the lesion. Superficial bladder lesions can be treated with fulguration or excision, while deeper lesions involving the detrusor muscle require excision. Lesions in close proximity to the interureteric ridge may require ureteroneocystostomy. Follow-up after excisional procedures involves monitoring the patient for signs and symptoms of disease recurrence, especially in cases of ureteral involvement, to avoid the devastating consequences of silent kidney loss.

Endometriosis is a benign disease characterized by endometrial glands and stroma outside of the uterine cavity. It is commonly associated with pelvic pain and infertility. Ectopic endometrial tissue is predominantly located in the pelvis, but it can appear anywhere in the body, where it is referred to as extragenital endometriosis. The bowel and urinary tract are the most common sites of extragenital endometriosis.¹

Laparoscopic management of extragenital endometriosis has been described since the 1980s.² However, laparoscopic management of genitourinary endometriosis is still not widespread.^3,4 Physicians are often unfamiliar with the signs and symptoms of genitourinary endometriosis and fail to consider it when a patient presents with bladder pain or hematuria, which may or may not be cyclic. Furthermore, many gynecologists do not have the experience to correctly identify the various forms of endometriosis that may appear on the pelvic organ, including the serosa and peritoneum, as variable colored spots, blebs, lesions, or adhesions. Many surgeons are also not adequately trained in the advanced laparoscopic techniques required to treat genitourinary endometriosis.⁴

In this article, we describe the clinical presentation and diagnosis of genitourinary endometriosis and discuss laparoscopic management strategies with and without robotic assistance.

Clinical presentation and diagnosis of genitourinary endometriosis

While ureteral and bladder endometriosis are both diseases of the urinary tract, they are not always found together in the same patient. The bladder is the most commonly affected organ, followed by the ureter and kidney.^3,5,6 Endometriosis of the bladder usually presents with significant lower urinary tract symptoms. In contrast, ureteral endometriosis is usually silent with no apparent urinary symptoms.

Ureteral endometriosis. Cyclic hematuria is present in less than 15% of patients with ureteral endometriosis. Some patients experience cyclic, nonspecific colicky flank pain.^7-9 Otherwise, most patients present with the usual symptoms of endometriosis, such as pelvic pain and dysmenorrhea. In a systematic review, Cavaco-Gomes and colleagues described 700 patients with ureteral endometriosis; 81% reported dysmenorrhea, 70% had pelvic pain, and 66% had dyspareunia.¹⁰ Rarely, ureteral endometriosis can result in silent kidney loss if the ureter becomes severely obstructed without treatment.^11,12

Continue to: The lack of symptoms makes...

The lack of symptoms makes the early diagnosis of ureteral endometriosis difficult. As with all types of endometriosis, histologic evaluation of a biopsy sample is diagnostic. Multiple imaging modalities have been used to preoperatively diagnose ureteral involvement, including computed tomography,¹³ magnetic resonance imaging (MRI),¹⁴ intravenous pyelogram (IVP), and pelvic ultrasonography. However, each of these imaging modalities is limited in both sensitivity and the ability to characterize depth of tissue invasion.

In a study of 245 women undergoing pelvic ultrasonography, Pateman and colleagues reported that an experienced sonographer was able to visualize the bilateral ureters in 93% of cases.¹⁵ Renal ultrasonography is indicated in any woman suspected of having genitourinary tract involvement with the degree of hydroureter and level of obstruction noted during the exam.¹⁶

In our group, we perform renography to assess kidney function when hydroureter is noted preoperatively. Studies suggest that if greater than 10% of normal glomerular filtration rate remains, the kidney is considered salvageable, and near-normal function often returns following resection of disease. If preoperative kidney function is noted to be less than 10%, consultation with a nephrologist for possible nephrectomy is warranted.

We find that IVP is often helpful for preoperatively identifying the level and degree of ureteral involvement, and it also can be used postoperatively to evaluate for ureteral continuity (FIGURE 1). Sillou and colleagues showed MRI to be adequately sensitive for the detection of intrinsic ureteral endometriosis, but they reported that MRI often overestimates the frequency of disease.¹⁷ Authors of a 2016 Cochrane review of imaging modalities for endometriosis, including 4,807 women in 49 studies, reported that no imaging test was superior to surgery for diagnosing endometriosis.¹⁸ However, the review notably excluded genitourinary tract endometriosis, as surgery is not an acceptable reference standard, given that many surgeons cannot reliably identify such lesions.¹⁸

Bladder endometriosis. Unlike patients with ureteral endometriosis, those with bladder endometriosis are typically symptomatic and experience dysuria, hematuria, urinary frequency, and suprapubic tenderness.^7,19 Urinary tract infection, interstitial cystitis, and cancer must be considered in the differential diagnosis. Urinalysis and urine culture should be performed, and other diagnostic procedures such as ultrasonography, MRI, and cystoscopy should be considered to evaluate for endometriosis of the bladder.

Ultrasound and MRI of the bladder both demonstrate a high specificity for detecting bladder endometriosis, but they lack sensitivity for lesions less than 3 cm.²⁰ Deep infiltrating endometriosis of the bladder can be identified at the time of cystoscopy, which can assist in determining the need for ureteroneocystostomy if lesions are within 2 cm of the urethral opening.²⁰ Cystoscopy also allows for biopsy to be performed if underlying malignancy is of concern.¹⁹

In our group, when bladder endometriosis is suspected, we routinely perform preoperative bladder ultrasonography to identify the lesion and plan to perform intraoperative cystoscopy at the time of laparoscopic resection.^19,21

Continue to: Treatment...

Treatment

Medical management

Empiric medical therapies for endometriosis are centered around the idea that ectopic endometrial tissue responds to treatment in a similar manner as normal eutopic endometrium. The goals of treatment are to reduce or eliminate cyclic menstruation, thereby decreasing peritoneal seeding and suppressing the growth and activity of established ectopic implants. Medical therapy commonly involves the use of gonadotropin-releasing hormone agonists or antagonists, danazol, combined oral contraceptives, progestins, and aromatase inhibitors.

Medical therapy is commonly employed for patients with mild or early-stage disease and in those who are poor surgical candidates or decline surgery. Medical management alone clearly is contraindicated in the setting of ureteral obstruction and—in our opinion—may not be a good option for those with endometriosis of the ureter, given the potential for recurrence and potential serious sequelae of reduced renal function.²² Therefore, surgery has become the standard approach to therapy for mild to moderate cases of ureteral endometriosis.³

Medical therapy for patients with endometriosis of the bladder is generally considered a temporary solution as hormonal suppression, with its associated adverse effects, must be maintained throughout menopause. However, if endometriosis lesions lie within close proximity to the trigone, medical management is preferred, as surgical excision in the area of the trigone may predispose patients to neurogenic bladder and retrograde bladder reflux.^23,24

Surgical management

The objectives of surgical treatment for genitourinary tract endometriosis are to excise all visible disease, to prevent or delay recurrence of the disease to the extent possible, and to avoid any further morbidity—in particular, to preserve renal function in cases of ureteral endometriosis—and to avoid iatrogenic injury to surrounding pelvic nervous structures^25-27 (FIGURE 2). The surgical approach depends on the technical expertise of the surgeon and the availability of necessary instrumentation. In our experience, laparoscopy with or without robotic assistance is the preferred surgical approach.^{3,4,6,11,28-32}

Others have reported on the benefits of laparoscopy over laparotomy for the surgical management of genitourinary endometriosis. In a review of 61 patients who underwent either robot-assisted laparoscopic (n = 25) or open (n = 41) ureteroneocystostomy (n = 41), Isac and colleagues reported the procedure was longer in the laparoscopic group (279 min vs 200 min, P<.001), but the laparoscopic group had a shorter hospital stay (3 days vs 5 days, P<.001), used fewer narcotics postoperatively (P<.001), and had lower intraoperative blood loss (100 mL vs 150 mL, P<.001).³² No differences in long-term outcomes were observed in either cohort.

In a systematic review of 700 patients undergoing laparoscopic surgery for ureteral endometriosis, Cavaco-Gomes and colleagues reported that conversion to laparotomy occurred in only 3% to 7% of cases.¹⁰ In instances of ureteral endometriosis, laparoscopy provides greater visualization of the intraperitoneal contents over laparotomy, enabling better evaluation and treatment of lesions.^3,29,33,34 Robot-assisted laparoscopy provides the additional advantages of 3D visualization, potential for an accelerated learning curve over traditional laparoscopy, improvement in dissection technique, and ease of suturing technique.^6,35,36

Continue to: Extrinsic disease...

Extrinsic disease. In our group, we perform ureterolysis for extrinsic disease.²⁵ The peritoneal incision is made in an area unaffected by endometriosis. Using the suction irrigator, a potential space is developed under the serosa of the ureter by injecting normal saline or lactated Ringer’s solution. By creating a fluid barrier between the serosa and underlying tissues, the depth of surgical incision and lateral thermal spread are minimized. Grasping forceps are used to peel the peritoneum away.^25,37,38

Intrinsic disease. Unlike extrinsic disease, intrinsic disease can infiltrate the muscularis, lamina propria, and ureteral lumen, resulting in proximal dilation of the ureter with strictures.⁸ In this situation, ureteral compromise is likely and resection of the ureter is indicated^3,28 (FIGURE 3). Intrinsic disease can be suggested by preoperative imaging or when there is evidence of deep infiltrating disease on physical exam, such as rectovaginal nodularity.^30,39 When intrinsic ureteral disease is known, consultation with a urologist to plan a joint procedure is advisable. The procedure chosen to re-establish a functional ureter following resection depends on the location and extent of the involved ureter. Resection in close proximity to the bladder may be repaired by ureteroneocystostomy with or without psoas hitch,^30,39,40 whereas resection of more proximal ureter may be repaired using Boari flap, ileal interposition, or autotransplantation. Lesions in the upper third or middle ureter may be repaired using ureterouretral anastomosis.^6,7,30,41-43

Continue to: Bladder endometriosis...

Bladder endometriosis. Surgical treatment for bladder endometriosis depends on the depth of invasion and the location of the lesion (FIGURE 4). Lesions of the superficial aspect of the bladder identified at the time of laparoscopy can be treated with either excision or fulguration^28,35,44 In our group, we perform excision over fulguration to remove the entire lesion and obtain a pathologic diagnosis. Deeper lesions involving the detrusor muscle are likely to be an endometrioma of the bladder. In these cases, laparoscopic excision is recommended.⁷ Rarely, lesions close to the interureteric ridge may require ureteroneocystostomy.^19,45

In our experience, laparoscopic resection of bladder endometriomas is associated with better results in terms of symptom relief, progression of disease, and recurrence risk compared with other approaches. When performing laparoscopic excision of bladder lesions, we concomitantly evaluate the bladder lesion via cystoscopy to ensure adequate margins are obtained. Double-J stent placement is advised when lesions are within 2 cm of the urethral meatus to ensure ureteral patency during the postoperative period.⁴⁵ A postoperative cystogram routinely is performed 7 to 14 days after surgery to ensure adequate repair prior to removing the urinary catheter.^9,25,46,47

Postsurgical follow-up

Follow-up after treatment of genitourinary tract endometriosis should include monitoring the patient for symptoms of recurrence. Regular history and physical examination, renal function testing, and, in some instances, pelvic ultrasonography, all have a role in surveillance for recurrent ureteric disease. IVP or MRI may be warranted if a recurrence is suspected. A high index of suspicion should be maintained on the part of the clinician to avoid the devastating consequences of silent kidney loss. Patients should be counseled about the risk of disease recurrence, especially in those not undergoing postoperative hormonal suppression.

In conclusion

While endometriosis of the genitourinary tract is rare, patients can experience significant morbidity. Medical management of the disease is often limited by substantial adverse effects that limit treatment duration and is best used postoperatively after excision. An adequate physical exam and preoperative diagnostic imaging can be employed to characterize the extent of disease. When extensive disease involving the ureter is suspected, preoperative consultation with a urologist is encouraged to plan a multidisciplinary approach to surgical resection.

The ideal approach to surgery is laparoscopic resection with or without robotic assistance. Treatment of ureteral disease most commonly involves ureterolysis for cases of extrinsic disease but may require total resection of the ureter with concurrent ureteral reconstruction when disease is intrinsic to the ureter. Surgery for bladder endometriosis depends on the depth of invasion and location of the lesion. Superficial bladder lesions can be treated with fulguration or excision, while deeper lesions involving the detrusor muscle require excision. Lesions in close proximity to the interureteric ridge may require ureteroneocystostomy. Follow-up after excisional procedures involves monitoring the patient for signs and symptoms of disease recurrence, especially in cases of ureteral involvement, to avoid the devastating consequences of silent kidney loss.

Endometriosis is a benign disease characterized by endometrial glands and stroma outside of the uterine cavity. It is commonly associated with pelvic pain and infertility. Ectopic endometrial tissue is predominantly located in the pelvis, but it can appear anywhere in the body, where it is referred to as extragenital endometriosis. The bowel and urinary tract are the most common sites of extragenital endometriosis.¹

Laparoscopic management of extragenital endometriosis has been described since the 1980s.² However, laparoscopic management of genitourinary endometriosis is still not widespread.^3,4 Physicians are often unfamiliar with the signs and symptoms of genitourinary endometriosis and fail to consider it when a patient presents with bladder pain or hematuria, which may or may not be cyclic. Furthermore, many gynecologists do not have the experience to correctly identify the various forms of endometriosis that may appear on the pelvic organ, including the serosa and peritoneum, as variable colored spots, blebs, lesions, or adhesions. Many surgeons are also not adequately trained in the advanced laparoscopic techniques required to treat genitourinary endometriosis.⁴

In this article, we describe the clinical presentation and diagnosis of genitourinary endometriosis and discuss laparoscopic management strategies with and without robotic assistance.

Clinical presentation and diagnosis of genitourinary endometriosis

While ureteral and bladder endometriosis are both diseases of the urinary tract, they are not always found together in the same patient. The bladder is the most commonly affected organ, followed by the ureter and kidney.^3,5,6 Endometriosis of the bladder usually presents with significant lower urinary tract symptoms. In contrast, ureteral endometriosis is usually silent with no apparent urinary symptoms.

Ureteral endometriosis. Cyclic hematuria is present in less than 15% of patients with ureteral endometriosis. Some patients experience cyclic, nonspecific colicky flank pain.^7-9 Otherwise, most patients present with the usual symptoms of endometriosis, such as pelvic pain and dysmenorrhea. In a systematic review, Cavaco-Gomes and colleagues described 700 patients with ureteral endometriosis; 81% reported dysmenorrhea, 70% had pelvic pain, and 66% had dyspareunia.¹⁰ Rarely, ureteral endometriosis can result in silent kidney loss if the ureter becomes severely obstructed without treatment.^11,12

Continue to: The lack of symptoms makes...

The lack of symptoms makes the early diagnosis of ureteral endometriosis difficult. As with all types of endometriosis, histologic evaluation of a biopsy sample is diagnostic. Multiple imaging modalities have been used to preoperatively diagnose ureteral involvement, including computed tomography,¹³ magnetic resonance imaging (MRI),¹⁴ intravenous pyelogram (IVP), and pelvic ultrasonography. However, each of these imaging modalities is limited in both sensitivity and the ability to characterize depth of tissue invasion.

In a study of 245 women undergoing pelvic ultrasonography, Pateman and colleagues reported that an experienced sonographer was able to visualize the bilateral ureters in 93% of cases.¹⁵ Renal ultrasonography is indicated in any woman suspected of having genitourinary tract involvement with the degree of hydroureter and level of obstruction noted during the exam.¹⁶

In our group, we perform renography to assess kidney function when hydroureter is noted preoperatively. Studies suggest that if greater than 10% of normal glomerular filtration rate remains, the kidney is considered salvageable, and near-normal function often returns following resection of disease. If preoperative kidney function is noted to be less than 10%, consultation with a nephrologist for possible nephrectomy is warranted.

We find that IVP is often helpful for preoperatively identifying the level and degree of ureteral involvement, and it also can be used postoperatively to evaluate for ureteral continuity (FIGURE 1). Sillou and colleagues showed MRI to be adequately sensitive for the detection of intrinsic ureteral endometriosis, but they reported that MRI often overestimates the frequency of disease.¹⁷ Authors of a 2016 Cochrane review of imaging modalities for endometriosis, including 4,807 women in 49 studies, reported that no imaging test was superior to surgery for diagnosing endometriosis.¹⁸ However, the review notably excluded genitourinary tract endometriosis, as surgery is not an acceptable reference standard, given that many surgeons cannot reliably identify such lesions.¹⁸

Bladder endometriosis. Unlike patients with ureteral endometriosis, those with bladder endometriosis are typically symptomatic and experience dysuria, hematuria, urinary frequency, and suprapubic tenderness.^7,19 Urinary tract infection, interstitial cystitis, and cancer must be considered in the differential diagnosis. Urinalysis and urine culture should be performed, and other diagnostic procedures such as ultrasonography, MRI, and cystoscopy should be considered to evaluate for endometriosis of the bladder.

Ultrasound and MRI of the bladder both demonstrate a high specificity for detecting bladder endometriosis, but they lack sensitivity for lesions less than 3 cm.²⁰ Deep infiltrating endometriosis of the bladder can be identified at the time of cystoscopy, which can assist in determining the need for ureteroneocystostomy if lesions are within 2 cm of the urethral opening.²⁰ Cystoscopy also allows for biopsy to be performed if underlying malignancy is of concern.¹⁹

In our group, when bladder endometriosis is suspected, we routinely perform preoperative bladder ultrasonography to identify the lesion and plan to perform intraoperative cystoscopy at the time of laparoscopic resection.^19,21

Continue to: Treatment...

Treatment

Medical management

Empiric medical therapies for endometriosis are centered around the idea that ectopic endometrial tissue responds to treatment in a similar manner as normal eutopic endometrium. The goals of treatment are to reduce or eliminate cyclic menstruation, thereby decreasing peritoneal seeding and suppressing the growth and activity of established ectopic implants. Medical therapy commonly involves the use of gonadotropin-releasing hormone agonists or antagonists, danazol, combined oral contraceptives, progestins, and aromatase inhibitors.

Medical therapy is commonly employed for patients with mild or early-stage disease and in those who are poor surgical candidates or decline surgery. Medical management alone clearly is contraindicated in the setting of ureteral obstruction and—in our opinion—may not be a good option for those with endometriosis of the ureter, given the potential for recurrence and potential serious sequelae of reduced renal function.²² Therefore, surgery has become the standard approach to therapy for mild to moderate cases of ureteral endometriosis.³

Medical therapy for patients with endometriosis of the bladder is generally considered a temporary solution as hormonal suppression, with its associated adverse effects, must be maintained throughout menopause. However, if endometriosis lesions lie within close proximity to the trigone, medical management is preferred, as surgical excision in the area of the trigone may predispose patients to neurogenic bladder and retrograde bladder reflux.^23,24

Surgical management

The objectives of surgical treatment for genitourinary tract endometriosis are to excise all visible disease, to prevent or delay recurrence of the disease to the extent possible, and to avoid any further morbidity—in particular, to preserve renal function in cases of ureteral endometriosis—and to avoid iatrogenic injury to surrounding pelvic nervous structures^25-27 (FIGURE 2). The surgical approach depends on the technical expertise of the surgeon and the availability of necessary instrumentation. In our experience, laparoscopy with or without robotic assistance is the preferred surgical approach.^{3,4,6,11,28-32}

Others have reported on the benefits of laparoscopy over laparotomy for the surgical management of genitourinary endometriosis. In a review of 61 patients who underwent either robot-assisted laparoscopic (n = 25) or open (n = 41) ureteroneocystostomy (n = 41), Isac and colleagues reported the procedure was longer in the laparoscopic group (279 min vs 200 min, P<.001), but the laparoscopic group had a shorter hospital stay (3 days vs 5 days, P<.001), used fewer narcotics postoperatively (P<.001), and had lower intraoperative blood loss (100 mL vs 150 mL, P<.001).³² No differences in long-term outcomes were observed in either cohort.

In a systematic review of 700 patients undergoing laparoscopic surgery for ureteral endometriosis, Cavaco-Gomes and colleagues reported that conversion to laparotomy occurred in only 3% to 7% of cases.¹⁰ In instances of ureteral endometriosis, laparoscopy provides greater visualization of the intraperitoneal contents over laparotomy, enabling better evaluation and treatment of lesions.^3,29,33,34 Robot-assisted laparoscopy provides the additional advantages of 3D visualization, potential for an accelerated learning curve over traditional laparoscopy, improvement in dissection technique, and ease of suturing technique.^6,35,36

Continue to: Extrinsic disease...

Extrinsic disease. In our group, we perform ureterolysis for extrinsic disease.²⁵ The peritoneal incision is made in an area unaffected by endometriosis. Using the suction irrigator, a potential space is developed under the serosa of the ureter by injecting normal saline or lactated Ringer’s solution. By creating a fluid barrier between the serosa and underlying tissues, the depth of surgical incision and lateral thermal spread are minimized. Grasping forceps are used to peel the peritoneum away.^25,37,38

Intrinsic disease. Unlike extrinsic disease, intrinsic disease can infiltrate the muscularis, lamina propria, and ureteral lumen, resulting in proximal dilation of the ureter with strictures.⁸ In this situation, ureteral compromise is likely and resection of the ureter is indicated^3,28 (FIGURE 3). Intrinsic disease can be suggested by preoperative imaging or when there is evidence of deep infiltrating disease on physical exam, such as rectovaginal nodularity.^30,39 When intrinsic ureteral disease is known, consultation with a urologist to plan a joint procedure is advisable. The procedure chosen to re-establish a functional ureter following resection depends on the location and extent of the involved ureter. Resection in close proximity to the bladder may be repaired by ureteroneocystostomy with or without psoas hitch,^30,39,40 whereas resection of more proximal ureter may be repaired using Boari flap, ileal interposition, or autotransplantation. Lesions in the upper third or middle ureter may be repaired using ureterouretral anastomosis.^6,7,30,41-43

Continue to: Bladder endometriosis...

Bladder endometriosis. Surgical treatment for bladder endometriosis depends on the depth of invasion and the location of the lesion (FIGURE 4). Lesions of the superficial aspect of the bladder identified at the time of laparoscopy can be treated with either excision or fulguration^28,35,44 In our group, we perform excision over fulguration to remove the entire lesion and obtain a pathologic diagnosis. Deeper lesions involving the detrusor muscle are likely to be an endometrioma of the bladder. In these cases, laparoscopic excision is recommended.⁷ Rarely, lesions close to the interureteric ridge may require ureteroneocystostomy.^19,45

In our experience, laparoscopic resection of bladder endometriomas is associated with better results in terms of symptom relief, progression of disease, and recurrence risk compared with other approaches. When performing laparoscopic excision of bladder lesions, we concomitantly evaluate the bladder lesion via cystoscopy to ensure adequate margins are obtained. Double-J stent placement is advised when lesions are within 2 cm of the urethral meatus to ensure ureteral patency during the postoperative period.⁴⁵ A postoperative cystogram routinely is performed 7 to 14 days after surgery to ensure adequate repair prior to removing the urinary catheter.^9,25,46,47

Postsurgical follow-up

Follow-up after treatment of genitourinary tract endometriosis should include monitoring the patient for symptoms of recurrence. Regular history and physical examination, renal function testing, and, in some instances, pelvic ultrasonography, all have a role in surveillance for recurrent ureteric disease. IVP or MRI may be warranted if a recurrence is suspected. A high index of suspicion should be maintained on the part of the clinician to avoid the devastating consequences of silent kidney loss. Patients should be counseled about the risk of disease recurrence, especially in those not undergoing postoperative hormonal suppression.

In conclusion

While endometriosis of the genitourinary tract is rare, patients can experience significant morbidity. Medical management of the disease is often limited by substantial adverse effects that limit treatment duration and is best used postoperatively after excision. An adequate physical exam and preoperative diagnostic imaging can be employed to characterize the extent of disease. When extensive disease involving the ureter is suspected, preoperative consultation with a urologist is encouraged to plan a multidisciplinary approach to surgical resection.

The ideal approach to surgery is laparoscopic resection with or without robotic assistance. Treatment of ureteral disease most commonly involves ureterolysis for cases of extrinsic disease but may require total resection of the ureter with concurrent ureteral reconstruction when disease is intrinsic to the ureter. Surgery for bladder endometriosis depends on the depth of invasion and location of the lesion. Superficial bladder lesions can be treated with fulguration or excision, while deeper lesions involving the detrusor muscle require excision. Lesions in close proximity to the interureteric ridge may require ureteroneocystostomy. Follow-up after excisional procedures involves monitoring the patient for signs and symptoms of disease recurrence, especially in cases of ureteral involvement, to avoid the devastating consequences of silent kidney loss.

CASE
A 28-year-old patient presents for evaluation and management of her chronic pelvic pain, dysmenorrhea, and menorrhagia. She previously tried ibuprofen with no pain relief. She also tried oral and long-acting reversible contraceptives but continued to be symptomatic. She underwent pelvic sonography, which demonstrated a large globular uterus with myometrial thickening and myometrial cysts with increased hypervascularity. Subsequent magnetic resonance imaging indicated a thickened junctional zone. Feeling she had exhausted medical manegement options with no significant improvement, she desired surgical treatment, but wanted to retain her future fertility. As a newlywed, she and her husband were planning on building a family so she desired to retain her uterus for potential future pregnancy.

How would you address this patient’s disruptive symptoms, while affirming her long-term plans by choosing the proper intervention?

Adenomyosis is characterized by endometrial-like glands and stroma deep within the myometrium of the uterus and generally is classified as diffuse or focal. This common, benign gynecologic condition is known to cause enlargement of the uterus secondary to stimulation of ectopic endometrial-like cells.^1-3 Although the true incidence of adenomyosis is unknown because of the difficulty of making the diagnosis, prevalence has been variously reported at 6% to 70% among reproductive-aged women.^4,5

In this review, we first examine the clinical presentation and diagnosis of adenomyosis. We then discuss clinical indications for, and surgical techniques of, adenomyomectomy, including our preferred uterine-sparing approach for focal disease or when the patient wants to preserve fertility: video laparoscopic resection with or without robotic assistance, aided by minilaparotomy when indicated.

Treatment evolved in a century and a half

Adenomyosis was first described more than 150 years ago; historically, hysterectomy was the mainstay of treatment.^2,6 Conservative surgical treatment for adenomyosis has been reported since the early 1950s.^6-8 Surgical treatment initially became more widespread following the introduction of wedge resection, which allowed for partial excision of adenomyotic nodules.⁹

More recent developments in diagnostic technologies and capabilities have allowed for the emergence of additional uterine-sparing and minimally invasive surgical treatment options for adenomyosis.^3,10 Although the use of laparoscopic approaches is limited because a high level of technical skill is required to undertake these procedures, such approaches are becoming increasingly important as more and more patients seek fertility conservation.^11-13

How does adenomyosis present?

Adenomyosis symptoms commonly consist of abnormal uterine bleeding and dysmenorrhea, affecting approximately 40% to 60% and 15% to 30% of patients with the condition, respectively.¹⁴ These symptoms are considered nonspecific because they are also associated with other uterine abnormalities.¹⁵ Although menorrhagia is not associated with extent of disease, dysmenorrhea is associated with both the number and depth of adenomyotic foci.¹⁴

Other symptoms reported with adenomyosis include chronic pelvic pain, dyspareunia, as well as infertility. Note, however, that a large percentage of patients are asymptomatic.^16,17

On physical examination, patients commonly exhibit a diffusely enlarged, globular uterus. This finding is secondary to uniform hyperplasia and hypertrophy of the myometrium, caused by stimulation of ectopic endometrial cells.² A subset of patients experience significant uterine tenderness.¹⁸ Other common findings associated with adenomyosis include uterine abnormalities, such as leiomyomata, endometriosis, and endometrial polyps.

Continue to: Two-pronged route to diagnosis and a differential...

Two-pronged route to diagnosis and a differential

Histology

Adenomyosis is definitively diagnosed based on histologic findings of endometrial-like tissue within the myometrium. Historically, histologic analysis was performed on specimens following hysterectomy but, more recently, has utilized specimens obtained from hysteroscopic and laparoscopic myometrial biopsies.¹⁹ Importantly, although hysteroscopic and laparoscopic biopsies are taken under direct visualization, there are no pathognomonic signs for adenomyosis; a diagnosis can therefore be missed if adenomyosis is not present at biopsied sites.¹ The sensitivity of random biopsy at laparoscopy has been found to be as low as 2% to as high as 56%.²⁰

Imaging

Imaging can be helpful in clinical decision making and to guide the differential diagnosis. Transvaginal ultrasonography (TVUS) is often the first mode of imaging used for the investigation of abnormal uterine bleeding or pelvic pain. Diagnosis by TVUS is difficult because the modality is operator dependent and standard diagnostic criteria are lacking.⁵

The most commonly reported ultrasonographic features of adenomyosis are^21,22:

• a globally enlarged uterus
• asymmetry
• myometrial thickening with heterogeneity
• poorly defined foci of hyperechoic regions, surrounded by hypoechoic areas that correspond to smooth-muscle hyperplasia
• myometrial cysts.

Doppler ultrasound examination in patients with adenomyosis reveals increased flow to the myometrium without evidence of large blood vessels.

3-dimensional (3-D) ultrasonography. Integration of 3-D ultrasonography has allowed for identification of the thicker junctional zone that suggests adenomyosis. In a systematic review of the accuracy of TVUS, investigators reported a pooled sensitivity and specificity for 2-dimensional ultrasonography of 83.8% and 63.9%, respectively, and a pooled sensitivity and specificity for 3-dimensional ultrasonography of 88.9% and 56.0%, respectively.²²

Magnetic resonance imaging (MRI) is also used in the evaluation of adenomyosis. Although MRI is considered a more accurate diagnostic modality because it is not operator dependent, expense often prohibits its use in the work-up of abnormal uterine bleeding and chronic pelvic pain.^2,23

The most commonly reported MRI findings in adenomyosis include a globular or asymmetric uterus, heterogeneity of myometrial signal intensity, and thickening of the junctional zone²⁴ (FIGURE 1). In a systematic review, researchers reported a pooled sensitivity and specificity of 77% and 89%, respectively, for the diagnosis of adenomyosis using MRI.²⁵

Approaches to treatment

Medical management

No medical therapies or guidelines specific to the treatment of adenomyosis exist.⁹ Often, nonsteroidal anti-inflammatory drugs (NSAIDs) are employed to combat cramping and pain associated with increased prostaglandin levels.²⁶ A systematic review found that NSAIDs are significantly better at treating dysmenorrhea than placebo alone.²⁶

Moreover, adenomyosis is an estrogen-dependent disease; consequently, many medical treatments are targeted at suppressing the hypothalamic–pituitary–ovarian axis and inducing endometrial atrophy. Medications commonly used (off-label) for this effect include combined or progestin-only oral contraceptive pills, gonadotropin-releasing hormone (GnRH) agonists, levonorgestrel-releasing intrauterine devices, danazol, and aromatase inhibitors.

Use of a GnRH agonist, such as leuprolide, is limited to a short course (<6 months) because menopausal-like symptoms, such as hot flashes, vaginal atrophy, and loss of bone-mineral density, can develop.¹⁶ Symptoms of adenomyosis often return upon cessation of hormonal treatment.¹

Novel therapies are under investigation, including GnRH antagonists, selective progesterone-receptor modulators, and antiplatelet therapy.²⁷

Although there are few data showing the effectiveness of medical therapy on adenomyosis-specific outcomes, medications are particularly useful in patients who are poor surgical candidates or who may prefer not to undergo surgery. Furthermore, medical therapy has considerable use in conjunction with surgical intervention; a prospective observational study showed that women who underwent GnRH agonist treatment following surgery had significantly greater improvement of their dysmenorrhea and menorrhagia, compared with those who underwent surgery only.²⁸ In addition, preoperative administration of a GnRH agonist or danazol several months prior to surgery has been shown to reduce uterine vascularity and, thus, blood loss at surgery.^29,30

Continue to: Surgery

Surgery

The objective of surgical management is to ameliorate symptoms in a conservative manner, by excision or cytoreduction of adenomyotic lesions, while preserving, even improving, fertility.^3,11,31 The choice of procedure depends, ultimately, on the location and extent of disease, the patient’s desire for uterine preservation and fertility, and surgical skill.³

Historically, hysterectomy was used to treat adenomyosis; for patients declining fertility preservation, hysterectomy remains the definitive treatment. Since the early 1950s, several techniques for laparotomic reduction have been developed. Surgeries that achieve partial reduction include:

Wedge resection of the uterine wall entails removal of the seromuscular layer at the identified location of adenomyotic tissue, with subsequent repair of the remaining muscular and serosal layers surrounding the wound.^3,32 Because adenomyotic tissue can remain on either side of the incision in wedge resection, clinical improvement in symptoms of dysmenorrhea and menorrhagia are modest, and recurrence is possible.⁷

Modified reduction surgery. Modifications of reduction surgery include slicing adenomyotic tissue using microsurgery and partial excision.³³

Transverse-H incision of the uterine wall involves a transverse incision on the uterine fundus, separating serosa and myometrium, followed by removal of diseased tissue using an electrosurgical scalpel or scissors. Tensionless suturing is used to close the myometrial layers in 1 or 2 layers to establish hemostasis and close the defect; serosal flaps are closed with subserosal interrupted sutures.³⁴ Data show that, following surgery with this technique, 21.4% to 38.7% of patients who attempt conception achieve clinical pregnancy.⁷

Complete, conservative resection in cases of diffuse and focal adenomyosis is possible using the triple-flap method, in which total resection is achieved by removing diseased myometrium until healthy, soft tissue—with normal texture, color, and vascularity—is reached.² Repair with this technique reduces the risk of uterine rupture by reconstructing the uterine wall using a muscle flap prepared by metroplasty.⁷ In a study of 64 women who underwent triple-flap resection, a clinical pregnancy rate of 74% and a live birth rate of 52% were reported.⁷

Minimally invasive approaches. Although several techniques have been developed for focal excision of adenomyosis by laparotomy,⁷ the trend has been toward minimally invasive surgery, which reduces estimated blood loss, decreases length of stay, and reduces adhesion formation—all without a statistically significant difference in long-term clinical outcomes, compared to other techniques.^35-39 Furthermore, enhanced visualization of pelvic organs provided by laparoscopy is vital in the case of adenomyosis.^3,31

How our group approaches surgical management. A challenge in laparoscopic surgery of adenomyosis is extraction of an extensive amount of diseased tissue. In 1994, our group described the use of simultaneous operative laparoscopy and minilaparotomy technique as an effective and safe alternative to laparotomy in the treatment of myomectomy⁶; the surgical principles of that approach are applied to adenomyomectomy. The technique involves treatment of pelvic pathology with laparoscopy, removal of tissue through the minilaparotomy incision, and repair of the uterine wall defect in layers.

References

1. Struble J, Reid S, Bedaiwy MA. Adenomyosis: a clinical review of a challenging gynecologic condition. J Minim Invasive Gynecol.2016; 23:164-185.
2. García-Solares J, Donnez J, Donnez O, et al. Pathogenesis of uterine adenomyosis: invagination or metaplasia? Fertil Steril.2018;109:371-379.
3. Ferenczy A. Pathophysiology of adenomyosis. Hum Reprod Update. 1998;4:312-322.
4. Gargett CE. Uterine stem cells: what is the evidence? Hum Reprod Update. 2007;13:87-101.
5. Chan RW, Schwab KE, Gargett CE. Clonogenicity of human endometrial epithelial and stromal cells. Biol Reprod. 2004;70:1738-1750.
6. Schwab KE, Chan RWS, Gargett CE. Putative stem cell activity of human endometrial epithelial and stromal cells during the menstrual cycle. Fertil Steril. 2005;84(Suppl 2):1124-1130.
7. Sasson IE, Taylor HS. Stem cells and the pathogenesis of endometriosis. Ann N Y Acad Sci. 2008;1127:106-115.
8. Du H, Taylor HS. Stem cells and female reproduction. Reprod Sci. 2009;16:126-139.
9. Acloque H, Adams MS, Fishwick K, et al. Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease. J Clin Invest. 2009;119:1438-1449.

Continue to: In 57 women who underwent…

In 57 women who underwent this procedure, the mean operative time was 127 minutes; average estimated blood loss was 267 mL.⁴⁰ Overall, laparoscopy with minilaparotomy was found to be a less technically difficult technique for laparoscopic myomectomy; allowed better closure of the uterine defect; and might have required less time to perform.³

We therefore advocate video laparoscopic wedge resection with or without robotic assistance, aided by minilaparotomy when necessary for safe removal of larger adenomyomas, as the preferred uterine-sparing surgical approach for focal adenomyosis or when the patient wants to preserve fertility (FIGURE 2). We think that this technique allows focal adenomyosis to be treated by wedge resection of the diseased myometrium, with subsequent closure of the remaining myometrial defect using a barbed V-Loc (Medtronic, Minneapolis, Minnesota) delayed absorbable suture in layers (FIGURE 3). Minilaparotomy can be utilized when indicated to aid removal of the resected myometrial specimen.

In our extensive experience, we have found that this technique provides significant relief of symptoms and improvements in fertility outcomes while minimizing surgical morbidity.

CASE Resolved

The patient underwent successful wedge resection of her adenomyosis by laparoscopy. She experienced nearly complete resolution of her symptoms of dysmenorrhea, menorrhagia, and pelvic pain. She retained good uterine integrity. Three years later, she and her husband became parents when she delivered their first child by cesarean delivery at full term. After she completed childbearing, she ultimately opted for minimally invasive hysterectomy.

The authors would like to acknowledge Mailinh Vu, MD, Fellow at Camran Nezhat Institute, for reviewing and editing this article.

CASE
A 28-year-old patient presents for evaluation and management of her chronic pelvic pain, dysmenorrhea, and menorrhagia. She previously tried ibuprofen with no pain relief. She also tried oral and long-acting reversible contraceptives but continued to be symptomatic. She underwent pelvic sonography, which demonstrated a large globular uterus with myometrial thickening and myometrial cysts with increased hypervascularity. Subsequent magnetic resonance imaging indicated a thickened junctional zone. Feeling she had exhausted medical manegement options with no significant improvement, she desired surgical treatment, but wanted to retain her future fertility. As a newlywed, she and her husband were planning on building a family so she desired to retain her uterus for potential future pregnancy.

How would you address this patient’s disruptive symptoms, while affirming her long-term plans by choosing the proper intervention?

Adenomyosis is characterized by endometrial-like glands and stroma deep within the myometrium of the uterus and generally is classified as diffuse or focal. This common, benign gynecologic condition is known to cause enlargement of the uterus secondary to stimulation of ectopic endometrial-like cells.^1-3 Although the true incidence of adenomyosis is unknown because of the difficulty of making the diagnosis, prevalence has been variously reported at 6% to 70% among reproductive-aged women.^4,5

In this review, we first examine the clinical presentation and diagnosis of adenomyosis. We then discuss clinical indications for, and surgical techniques of, adenomyomectomy, including our preferred uterine-sparing approach for focal disease or when the patient wants to preserve fertility: video laparoscopic resection with or without robotic assistance, aided by minilaparotomy when indicated.

Treatment evolved in a century and a half

Adenomyosis was first described more than 150 years ago; historically, hysterectomy was the mainstay of treatment.^2,6 Conservative surgical treatment for adenomyosis has been reported since the early 1950s.^6-8 Surgical treatment initially became more widespread following the introduction of wedge resection, which allowed for partial excision of adenomyotic nodules.⁹

More recent developments in diagnostic technologies and capabilities have allowed for the emergence of additional uterine-sparing and minimally invasive surgical treatment options for adenomyosis.^3,10 Although the use of laparoscopic approaches is limited because a high level of technical skill is required to undertake these procedures, such approaches are becoming increasingly important as more and more patients seek fertility conservation.^11-13

How does adenomyosis present?

Adenomyosis symptoms commonly consist of abnormal uterine bleeding and dysmenorrhea, affecting approximately 40% to 60% and 15% to 30% of patients with the condition, respectively.¹⁴ These symptoms are considered nonspecific because they are also associated with other uterine abnormalities.¹⁵ Although menorrhagia is not associated with extent of disease, dysmenorrhea is associated with both the number and depth of adenomyotic foci.¹⁴

Other symptoms reported with adenomyosis include chronic pelvic pain, dyspareunia, as well as infertility. Note, however, that a large percentage of patients are asymptomatic.^16,17

On physical examination, patients commonly exhibit a diffusely enlarged, globular uterus. This finding is secondary to uniform hyperplasia and hypertrophy of the myometrium, caused by stimulation of ectopic endometrial cells.² A subset of patients experience significant uterine tenderness.¹⁸ Other common findings associated with adenomyosis include uterine abnormalities, such as leiomyomata, endometriosis, and endometrial polyps.

Continue to: Two-pronged route to diagnosis and a differential...

Two-pronged route to diagnosis and a differential

Histology

Adenomyosis is definitively diagnosed based on histologic findings of endometrial-like tissue within the myometrium. Historically, histologic analysis was performed on specimens following hysterectomy but, more recently, has utilized specimens obtained from hysteroscopic and laparoscopic myometrial biopsies.¹⁹ Importantly, although hysteroscopic and laparoscopic biopsies are taken under direct visualization, there are no pathognomonic signs for adenomyosis; a diagnosis can therefore be missed if adenomyosis is not present at biopsied sites.¹ The sensitivity of random biopsy at laparoscopy has been found to be as low as 2% to as high as 56%.²⁰

Imaging

Imaging can be helpful in clinical decision making and to guide the differential diagnosis. Transvaginal ultrasonography (TVUS) is often the first mode of imaging used for the investigation of abnormal uterine bleeding or pelvic pain. Diagnosis by TVUS is difficult because the modality is operator dependent and standard diagnostic criteria are lacking.⁵

The most commonly reported ultrasonographic features of adenomyosis are^21,22:

• a globally enlarged uterus
• asymmetry
• myometrial thickening with heterogeneity
• poorly defined foci of hyperechoic regions, surrounded by hypoechoic areas that correspond to smooth-muscle hyperplasia
• myometrial cysts.

Doppler ultrasound examination in patients with adenomyosis reveals increased flow to the myometrium without evidence of large blood vessels.

3-dimensional (3-D) ultrasonography. Integration of 3-D ultrasonography has allowed for identification of the thicker junctional zone that suggests adenomyosis. In a systematic review of the accuracy of TVUS, investigators reported a pooled sensitivity and specificity for 2-dimensional ultrasonography of 83.8% and 63.9%, respectively, and a pooled sensitivity and specificity for 3-dimensional ultrasonography of 88.9% and 56.0%, respectively.²²

Magnetic resonance imaging (MRI) is also used in the evaluation of adenomyosis. Although MRI is considered a more accurate diagnostic modality because it is not operator dependent, expense often prohibits its use in the work-up of abnormal uterine bleeding and chronic pelvic pain.^2,23

The most commonly reported MRI findings in adenomyosis include a globular or asymmetric uterus, heterogeneity of myometrial signal intensity, and thickening of the junctional zone²⁴ (FIGURE 1). In a systematic review, researchers reported a pooled sensitivity and specificity of 77% and 89%, respectively, for the diagnosis of adenomyosis using MRI.²⁵

Approaches to treatment

Medical management

No medical therapies or guidelines specific to the treatment of adenomyosis exist.⁹ Often, nonsteroidal anti-inflammatory drugs (NSAIDs) are employed to combat cramping and pain associated with increased prostaglandin levels.²⁶ A systematic review found that NSAIDs are significantly better at treating dysmenorrhea than placebo alone.²⁶

Moreover, adenomyosis is an estrogen-dependent disease; consequently, many medical treatments are targeted at suppressing the hypothalamic–pituitary–ovarian axis and inducing endometrial atrophy. Medications commonly used (off-label) for this effect include combined or progestin-only oral contraceptive pills, gonadotropin-releasing hormone (GnRH) agonists, levonorgestrel-releasing intrauterine devices, danazol, and aromatase inhibitors.

Use of a GnRH agonist, such as leuprolide, is limited to a short course (<6 months) because menopausal-like symptoms, such as hot flashes, vaginal atrophy, and loss of bone-mineral density, can develop.¹⁶ Symptoms of adenomyosis often return upon cessation of hormonal treatment.¹

Novel therapies are under investigation, including GnRH antagonists, selective progesterone-receptor modulators, and antiplatelet therapy.²⁷

Although there are few data showing the effectiveness of medical therapy on adenomyosis-specific outcomes, medications are particularly useful in patients who are poor surgical candidates or who may prefer not to undergo surgery. Furthermore, medical therapy has considerable use in conjunction with surgical intervention; a prospective observational study showed that women who underwent GnRH agonist treatment following surgery had significantly greater improvement of their dysmenorrhea and menorrhagia, compared with those who underwent surgery only.²⁸ In addition, preoperative administration of a GnRH agonist or danazol several months prior to surgery has been shown to reduce uterine vascularity and, thus, blood loss at surgery.^29,30

Continue to: Surgery

Surgery

The objective of surgical management is to ameliorate symptoms in a conservative manner, by excision or cytoreduction of adenomyotic lesions, while preserving, even improving, fertility.^3,11,31 The choice of procedure depends, ultimately, on the location and extent of disease, the patient’s desire for uterine preservation and fertility, and surgical skill.³

Historically, hysterectomy was used to treat adenomyosis; for patients declining fertility preservation, hysterectomy remains the definitive treatment. Since the early 1950s, several techniques for laparotomic reduction have been developed. Surgeries that achieve partial reduction include:

Wedge resection of the uterine wall entails removal of the seromuscular layer at the identified location of adenomyotic tissue, with subsequent repair of the remaining muscular and serosal layers surrounding the wound.^3,32 Because adenomyotic tissue can remain on either side of the incision in wedge resection, clinical improvement in symptoms of dysmenorrhea and menorrhagia are modest, and recurrence is possible.⁷

Modified reduction surgery. Modifications of reduction surgery include slicing adenomyotic tissue using microsurgery and partial excision.³³

Transverse-H incision of the uterine wall involves a transverse incision on the uterine fundus, separating serosa and myometrium, followed by removal of diseased tissue using an electrosurgical scalpel or scissors. Tensionless suturing is used to close the myometrial layers in 1 or 2 layers to establish hemostasis and close the defect; serosal flaps are closed with subserosal interrupted sutures.³⁴ Data show that, following surgery with this technique, 21.4% to 38.7% of patients who attempt conception achieve clinical pregnancy.⁷

Complete, conservative resection in cases of diffuse and focal adenomyosis is possible using the triple-flap method, in which total resection is achieved by removing diseased myometrium until healthy, soft tissue—with normal texture, color, and vascularity—is reached.² Repair with this technique reduces the risk of uterine rupture by reconstructing the uterine wall using a muscle flap prepared by metroplasty.⁷ In a study of 64 women who underwent triple-flap resection, a clinical pregnancy rate of 74% and a live birth rate of 52% were reported.⁷

Minimally invasive approaches. Although several techniques have been developed for focal excision of adenomyosis by laparotomy,⁷ the trend has been toward minimally invasive surgery, which reduces estimated blood loss, decreases length of stay, and reduces adhesion formation—all without a statistically significant difference in long-term clinical outcomes, compared to other techniques.^35-39 Furthermore, enhanced visualization of pelvic organs provided by laparoscopy is vital in the case of adenomyosis.^3,31

How our group approaches surgical management. A challenge in laparoscopic surgery of adenomyosis is extraction of an extensive amount of diseased tissue. In 1994, our group described the use of simultaneous operative laparoscopy and minilaparotomy technique as an effective and safe alternative to laparotomy in the treatment of myomectomy⁶; the surgical principles of that approach are applied to adenomyomectomy. The technique involves treatment of pelvic pathology with laparoscopy, removal of tissue through the minilaparotomy incision, and repair of the uterine wall defect in layers.

References

1. Struble J, Reid S, Bedaiwy MA. Adenomyosis: a clinical review of a challenging gynecologic condition. J Minim Invasive Gynecol.2016; 23:164-185.
2. García-Solares J, Donnez J, Donnez O, et al. Pathogenesis of uterine adenomyosis: invagination or metaplasia? Fertil Steril.2018;109:371-379.
3. Ferenczy A. Pathophysiology of adenomyosis. Hum Reprod Update. 1998;4:312-322.
4. Gargett CE. Uterine stem cells: what is the evidence? Hum Reprod Update. 2007;13:87-101.
5. Chan RW, Schwab KE, Gargett CE. Clonogenicity of human endometrial epithelial and stromal cells. Biol Reprod. 2004;70:1738-1750.
6. Schwab KE, Chan RWS, Gargett CE. Putative stem cell activity of human endometrial epithelial and stromal cells during the menstrual cycle. Fertil Steril. 2005;84(Suppl 2):1124-1130.
7. Sasson IE, Taylor HS. Stem cells and the pathogenesis of endometriosis. Ann N Y Acad Sci. 2008;1127:106-115.
8. Du H, Taylor HS. Stem cells and female reproduction. Reprod Sci. 2009;16:126-139.
9. Acloque H, Adams MS, Fishwick K, et al. Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease. J Clin Invest. 2009;119:1438-1449.

Continue to: In 57 women who underwent…

In 57 women who underwent this procedure, the mean operative time was 127 minutes; average estimated blood loss was 267 mL.⁴⁰ Overall, laparoscopy with minilaparotomy was found to be a less technically difficult technique for laparoscopic myomectomy; allowed better closure of the uterine defect; and might have required less time to perform.³

We therefore advocate video laparoscopic wedge resection with or without robotic assistance, aided by minilaparotomy when necessary for safe removal of larger adenomyomas, as the preferred uterine-sparing surgical approach for focal adenomyosis or when the patient wants to preserve fertility (FIGURE 2). We think that this technique allows focal adenomyosis to be treated by wedge resection of the diseased myometrium, with subsequent closure of the remaining myometrial defect using a barbed V-Loc (Medtronic, Minneapolis, Minnesota) delayed absorbable suture in layers (FIGURE 3). Minilaparotomy can be utilized when indicated to aid removal of the resected myometrial specimen.

In our extensive experience, we have found that this technique provides significant relief of symptoms and improvements in fertility outcomes while minimizing surgical morbidity.

CASE Resolved

The patient underwent successful wedge resection of her adenomyosis by laparoscopy. She experienced nearly complete resolution of her symptoms of dysmenorrhea, menorrhagia, and pelvic pain. She retained good uterine integrity. Three years later, she and her husband became parents when she delivered their first child by cesarean delivery at full term. After she completed childbearing, she ultimately opted for minimally invasive hysterectomy.

The authors would like to acknowledge Mailinh Vu, MD, Fellow at Camran Nezhat Institute, for reviewing and editing this article.

CASE
A 28-year-old patient presents for evaluation and management of her chronic pelvic pain, dysmenorrhea, and menorrhagia. She previously tried ibuprofen with no pain relief. She also tried oral and long-acting reversible contraceptives but continued to be symptomatic. She underwent pelvic sonography, which demonstrated a large globular uterus with myometrial thickening and myometrial cysts with increased hypervascularity. Subsequent magnetic resonance imaging indicated a thickened junctional zone. Feeling she had exhausted medical manegement options with no significant improvement, she desired surgical treatment, but wanted to retain her future fertility. As a newlywed, she and her husband were planning on building a family so she desired to retain her uterus for potential future pregnancy.

How would you address this patient’s disruptive symptoms, while affirming her long-term plans by choosing the proper intervention?

Adenomyosis is characterized by endometrial-like glands and stroma deep within the myometrium of the uterus and generally is classified as diffuse or focal. This common, benign gynecologic condition is known to cause enlargement of the uterus secondary to stimulation of ectopic endometrial-like cells.^1-3 Although the true incidence of adenomyosis is unknown because of the difficulty of making the diagnosis, prevalence has been variously reported at 6% to 70% among reproductive-aged women.^4,5

In this review, we first examine the clinical presentation and diagnosis of adenomyosis. We then discuss clinical indications for, and surgical techniques of, adenomyomectomy, including our preferred uterine-sparing approach for focal disease or when the patient wants to preserve fertility: video laparoscopic resection with or without robotic assistance, aided by minilaparotomy when indicated.

Treatment evolved in a century and a half

Adenomyosis was first described more than 150 years ago; historically, hysterectomy was the mainstay of treatment.^2,6 Conservative surgical treatment for adenomyosis has been reported since the early 1950s.^6-8 Surgical treatment initially became more widespread following the introduction of wedge resection, which allowed for partial excision of adenomyotic nodules.⁹

More recent developments in diagnostic technologies and capabilities have allowed for the emergence of additional uterine-sparing and minimally invasive surgical treatment options for adenomyosis.^3,10 Although the use of laparoscopic approaches is limited because a high level of technical skill is required to undertake these procedures, such approaches are becoming increasingly important as more and more patients seek fertility conservation.^11-13

How does adenomyosis present?

Adenomyosis symptoms commonly consist of abnormal uterine bleeding and dysmenorrhea, affecting approximately 40% to 60% and 15% to 30% of patients with the condition, respectively.¹⁴ These symptoms are considered nonspecific because they are also associated with other uterine abnormalities.¹⁵ Although menorrhagia is not associated with extent of disease, dysmenorrhea is associated with both the number and depth of adenomyotic foci.¹⁴

Other symptoms reported with adenomyosis include chronic pelvic pain, dyspareunia, as well as infertility. Note, however, that a large percentage of patients are asymptomatic.^16,17

On physical examination, patients commonly exhibit a diffusely enlarged, globular uterus. This finding is secondary to uniform hyperplasia and hypertrophy of the myometrium, caused by stimulation of ectopic endometrial cells.² A subset of patients experience significant uterine tenderness.¹⁸ Other common findings associated with adenomyosis include uterine abnormalities, such as leiomyomata, endometriosis, and endometrial polyps.

Continue to: Two-pronged route to diagnosis and a differential...

Two-pronged route to diagnosis and a differential

Histology

Adenomyosis is definitively diagnosed based on histologic findings of endometrial-like tissue within the myometrium. Historically, histologic analysis was performed on specimens following hysterectomy but, more recently, has utilized specimens obtained from hysteroscopic and laparoscopic myometrial biopsies.¹⁹ Importantly, although hysteroscopic and laparoscopic biopsies are taken under direct visualization, there are no pathognomonic signs for adenomyosis; a diagnosis can therefore be missed if adenomyosis is not present at biopsied sites.¹ The sensitivity of random biopsy at laparoscopy has been found to be as low as 2% to as high as 56%.²⁰

Imaging

Imaging can be helpful in clinical decision making and to guide the differential diagnosis. Transvaginal ultrasonography (TVUS) is often the first mode of imaging used for the investigation of abnormal uterine bleeding or pelvic pain. Diagnosis by TVUS is difficult because the modality is operator dependent and standard diagnostic criteria are lacking.⁵

The most commonly reported ultrasonographic features of adenomyosis are^21,22:

• a globally enlarged uterus
• asymmetry
• myometrial thickening with heterogeneity
• poorly defined foci of hyperechoic regions, surrounded by hypoechoic areas that correspond to smooth-muscle hyperplasia
• myometrial cysts.

Doppler ultrasound examination in patients with adenomyosis reveals increased flow to the myometrium without evidence of large blood vessels.

3-dimensional (3-D) ultrasonography. Integration of 3-D ultrasonography has allowed for identification of the thicker junctional zone that suggests adenomyosis. In a systematic review of the accuracy of TVUS, investigators reported a pooled sensitivity and specificity for 2-dimensional ultrasonography of 83.8% and 63.9%, respectively, and a pooled sensitivity and specificity for 3-dimensional ultrasonography of 88.9% and 56.0%, respectively.²²

Magnetic resonance imaging (MRI) is also used in the evaluation of adenomyosis. Although MRI is considered a more accurate diagnostic modality because it is not operator dependent, expense often prohibits its use in the work-up of abnormal uterine bleeding and chronic pelvic pain.^2,23

The most commonly reported MRI findings in adenomyosis include a globular or asymmetric uterus, heterogeneity of myometrial signal intensity, and thickening of the junctional zone²⁴ (FIGURE 1). In a systematic review, researchers reported a pooled sensitivity and specificity of 77% and 89%, respectively, for the diagnosis of adenomyosis using MRI.²⁵

Approaches to treatment

Medical management

No medical therapies or guidelines specific to the treatment of adenomyosis exist.⁹ Often, nonsteroidal anti-inflammatory drugs (NSAIDs) are employed to combat cramping and pain associated with increased prostaglandin levels.²⁶ A systematic review found that NSAIDs are significantly better at treating dysmenorrhea than placebo alone.²⁶

Moreover, adenomyosis is an estrogen-dependent disease; consequently, many medical treatments are targeted at suppressing the hypothalamic–pituitary–ovarian axis and inducing endometrial atrophy. Medications commonly used (off-label) for this effect include combined or progestin-only oral contraceptive pills, gonadotropin-releasing hormone (GnRH) agonists, levonorgestrel-releasing intrauterine devices, danazol, and aromatase inhibitors.

Use of a GnRH agonist, such as leuprolide, is limited to a short course (<6 months) because menopausal-like symptoms, such as hot flashes, vaginal atrophy, and loss of bone-mineral density, can develop.¹⁶ Symptoms of adenomyosis often return upon cessation of hormonal treatment.¹

Novel therapies are under investigation, including GnRH antagonists, selective progesterone-receptor modulators, and antiplatelet therapy.²⁷

Although there are few data showing the effectiveness of medical therapy on adenomyosis-specific outcomes, medications are particularly useful in patients who are poor surgical candidates or who may prefer not to undergo surgery. Furthermore, medical therapy has considerable use in conjunction with surgical intervention; a prospective observational study showed that women who underwent GnRH agonist treatment following surgery had significantly greater improvement of their dysmenorrhea and menorrhagia, compared with those who underwent surgery only.²⁸ In addition, preoperative administration of a GnRH agonist or danazol several months prior to surgery has been shown to reduce uterine vascularity and, thus, blood loss at surgery.^29,30

Continue to: Surgery

Surgery

The objective of surgical management is to ameliorate symptoms in a conservative manner, by excision or cytoreduction of adenomyotic lesions, while preserving, even improving, fertility.^3,11,31 The choice of procedure depends, ultimately, on the location and extent of disease, the patient’s desire for uterine preservation and fertility, and surgical skill.³

Historically, hysterectomy was used to treat adenomyosis; for patients declining fertility preservation, hysterectomy remains the definitive treatment. Since the early 1950s, several techniques for laparotomic reduction have been developed. Surgeries that achieve partial reduction include:

Wedge resection of the uterine wall entails removal of the seromuscular layer at the identified location of adenomyotic tissue, with subsequent repair of the remaining muscular and serosal layers surrounding the wound.^3,32 Because adenomyotic tissue can remain on either side of the incision in wedge resection, clinical improvement in symptoms of dysmenorrhea and menorrhagia are modest, and recurrence is possible.⁷

Modified reduction surgery. Modifications of reduction surgery include slicing adenomyotic tissue using microsurgery and partial excision.³³

Transverse-H incision of the uterine wall involves a transverse incision on the uterine fundus, separating serosa and myometrium, followed by removal of diseased tissue using an electrosurgical scalpel or scissors. Tensionless suturing is used to close the myometrial layers in 1 or 2 layers to establish hemostasis and close the defect; serosal flaps are closed with subserosal interrupted sutures.³⁴ Data show that, following surgery with this technique, 21.4% to 38.7% of patients who attempt conception achieve clinical pregnancy.⁷

Complete, conservative resection in cases of diffuse and focal adenomyosis is possible using the triple-flap method, in which total resection is achieved by removing diseased myometrium until healthy, soft tissue—with normal texture, color, and vascularity—is reached.² Repair with this technique reduces the risk of uterine rupture by reconstructing the uterine wall using a muscle flap prepared by metroplasty.⁷ In a study of 64 women who underwent triple-flap resection, a clinical pregnancy rate of 74% and a live birth rate of 52% were reported.⁷

Minimally invasive approaches. Although several techniques have been developed for focal excision of adenomyosis by laparotomy,⁷ the trend has been toward minimally invasive surgery, which reduces estimated blood loss, decreases length of stay, and reduces adhesion formation—all without a statistically significant difference in long-term clinical outcomes, compared to other techniques.^35-39 Furthermore, enhanced visualization of pelvic organs provided by laparoscopy is vital in the case of adenomyosis.^3,31

How our group approaches surgical management. A challenge in laparoscopic surgery of adenomyosis is extraction of an extensive amount of diseased tissue. In 1994, our group described the use of simultaneous operative laparoscopy and minilaparotomy technique as an effective and safe alternative to laparotomy in the treatment of myomectomy⁶; the surgical principles of that approach are applied to adenomyomectomy. The technique involves treatment of pelvic pathology with laparoscopy, removal of tissue through the minilaparotomy incision, and repair of the uterine wall defect in layers.

References

1. Struble J, Reid S, Bedaiwy MA. Adenomyosis: a clinical review of a challenging gynecologic condition. J Minim Invasive Gynecol.2016; 23:164-185.
2. García-Solares J, Donnez J, Donnez O, et al. Pathogenesis of uterine adenomyosis: invagination or metaplasia? Fertil Steril.2018;109:371-379.
3. Ferenczy A. Pathophysiology of adenomyosis. Hum Reprod Update. 1998;4:312-322.
4. Gargett CE. Uterine stem cells: what is the evidence? Hum Reprod Update. 2007;13:87-101.
5. Chan RW, Schwab KE, Gargett CE. Clonogenicity of human endometrial epithelial and stromal cells. Biol Reprod. 2004;70:1738-1750.
6. Schwab KE, Chan RWS, Gargett CE. Putative stem cell activity of human endometrial epithelial and stromal cells during the menstrual cycle. Fertil Steril. 2005;84(Suppl 2):1124-1130.
7. Sasson IE, Taylor HS. Stem cells and the pathogenesis of endometriosis. Ann N Y Acad Sci. 2008;1127:106-115.
8. Du H, Taylor HS. Stem cells and female reproduction. Reprod Sci. 2009;16:126-139.
9. Acloque H, Adams MS, Fishwick K, et al. Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease. J Clin Invest. 2009;119:1438-1449.

Continue to: In 57 women who underwent…

In 57 women who underwent this procedure, the mean operative time was 127 minutes; average estimated blood loss was 267 mL.⁴⁰ Overall, laparoscopy with minilaparotomy was found to be a less technically difficult technique for laparoscopic myomectomy; allowed better closure of the uterine defect; and might have required less time to perform.³

We therefore advocate video laparoscopic wedge resection with or without robotic assistance, aided by minilaparotomy when necessary for safe removal of larger adenomyomas, as the preferred uterine-sparing surgical approach for focal adenomyosis or when the patient wants to preserve fertility (FIGURE 2). We think that this technique allows focal adenomyosis to be treated by wedge resection of the diseased myometrium, with subsequent closure of the remaining myometrial defect using a barbed V-Loc (Medtronic, Minneapolis, Minnesota) delayed absorbable suture in layers (FIGURE 3). Minilaparotomy can be utilized when indicated to aid removal of the resected myometrial specimen.

In our extensive experience, we have found that this technique provides significant relief of symptoms and improvements in fertility outcomes while minimizing surgical morbidity.

CASE Resolved

The patient underwent successful wedge resection of her adenomyosis by laparoscopy. She experienced nearly complete resolution of her symptoms of dysmenorrhea, menorrhagia, and pelvic pain. She retained good uterine integrity. Three years later, she and her husband became parents when she delivered their first child by cesarean delivery at full term. After she completed childbearing, she ultimately opted for minimally invasive hysterectomy.

The authors would like to acknowledge Mailinh Vu, MD, Fellow at Camran Nezhat Institute, for reviewing and editing this article.