Extragenital endometriosis in the differential diagnosis of non-gynecological diseases

Endometriosis is a chronic, benign disease that affects approximately 10% of women of childbearing age. Its characteristic clinical features are dysmenorrhea, dyschezia, dysuria, dyspareunia, and infertility. The manifestations of extragenital endometriosis (EE) are a diagnostic challenge, as this disease can mimic other diseases due to its unusual location with infiltration of various organs and corresponding symptoms.

This review is based on publications retrieved by a selective search of the literature on the commonest extragenital sites of endometriosis, including the relevant current guideline.

Current evidence on the treatment of extragenital endometriosis consists largely of cohort studies and cross-sectional studies. The treatment is either surgical and/or conservative (e.g., hormonal therapy). Gastrointestinal endometriosis is the most common form of EE, affecting the rectum and sigmoid colon in nearly 90% of cases and typically presenting with dyschezia. Urogenital endometriosis is the second most common form of EE. It affects the bladder in more than 85% of cases and may present with dysuria, hematuria, or irritable bladder syndrome. The diaphragm is the most common site of thoracic endometriosis, potentially presenting with period-associated shoulder pain or catamenial pneumothorax. Endometriosis affecting a nerve often presents with sciatica. In abdominal wall endometriosis, painful nodules arise in scars from prior abdominal surgery.

There is, as yet, no causally directed treatment for chronic endometriosis. The treatment is decided upon individually in discussion with the patient, in consideration of risk factors and after assessment of the benefits and risks. Timely diagnosis is essential. Endometriosis is defined as the presence of endometrial tissue outside the uterine cavity. An estimated 10% of women of childbearing age are affected by endometriosis. In Germany, its prevalence is approximately 8.1 per 1000 women, with a peak in the age group 35 to 44 years (1). Known risk factors include (2): - early menarche and late menopause - short menstrual cycles - low body mass index (BMI) - low parity. The etiopathogenesis of endometriosis is not yet fully understood. Uterine hyperperistalsis and hyperestrogenism are considered potential risk factors; however, genetic factors, implantation theory and cellular metaplasia, among others, are also under discussion (3). Despite the fact that in Germany endometriosis is the reason for about 25 000 hospital admissions annually, general awareness of the disease is low (3, 4). The classical clinical presentation of endometriosis with dysmenorrhea, dyspareunia, infertility, and menstrual cycle-related lower abdominal pain can lead to the correct diagnosis. Yet, endometriosis is still diagnosed in Germany with a delay of up to 10 years�and the suspected reason for this is misdiagnosis (5). This applies in particular to extragenital endometriosis (EE), which occurs in about 9% of women with endometriosis (6). The majority of cases with EE are primarily presented to non-gynecological specialties (7). Delayed diagnosis and resulting chronic pain can cause dysregulation of the nervous system and lead to an abnormal pain pattern, requiring an even more complex differential diagnostic work-up (8, 9). For the patients, this has physical, but also psychological and social consequences (4). Therefore, it is crucial to recognize the symptoms of EE as early as possible and initiate proper treatment. The diagnostic process starts with taking the patient�s clinical history and exploring whether symptoms are linked with the phases of the menstrual cycle. Clinical examination is performed according to the symptoms and includes speculum examination, palpation, including rectovaginal palpation, transvaginal ultrasound, and renal ultrasound. Diagnostic laparoscopy is considered to be the gold standard for histological confirmation of the diagnosis. Given the chronic clinical course of endometriosis, a long-term and personalized treatment plan is required that comprises both conservative (symptomatic and hormonal) and surgical treatment, potentially with integration of complementary medicine approaches. Indications for surgical treatment include organ destruction, differential diagnostic work-up for sterility as well as persistent pain; considering the impact on the patient�s quality of life, a complete laparoscopic resection should be attempted (3). With regard to endometriosis-associated pain, cohort and cross-sectional studies did not find a clear advantage of surgical treatment over pharmacotherapy (3). The goal of pharmacotherapy is to achieve secondary amenorrhea. Except for the surgical indications mentioned above, pharmacotherapy may be attempted as primary treatment. Dienogest, the drug of first choice, showed a positive effect on endometriosis-associated symptoms in four randomized controlled trials; adverse events, including headache, mood swings and intermenstrual bleeding, occurred in less than 10% of patients (3). Second-line options include combined oral contraceptives, gonadotropin-releasing hormone (GnRH) analogs and progestins which can be used locally (3). Unless pregnancy is desired immediately after surgery, the current guideline recommends subsequent hormonal therapy to reduce recurrence rates (3). Details of the specific diagnostic assessment and the surgical treatment of EE are provided in the respective sections of this article. In this article, we would like to present the clinical picture of EE. As early as 1989, Markham et al. proposed to divide EE into four categories (6, 10) (Table 1): - Gastrointestinal endometriosis (32.3%) - Urogenital endometriosis (5.9%) - Thoracic endometriosis - Other locations, including nerves and skin (in total 61.8%). While this classification does not conform to the current guideline, it provides a better didactic overview. The aim of our review article is to increase diagnostic awareness of the wide variety of symptoms of endometriosis so that greater consideration is given to the condition during the differential diagnostic work-up� even beyond the field of gynecology.

This review is based on publications retrieved by a selective search of the PubMed and Google Scholar databases for the four groups of EE, including the current German guideline �Diagnosis and Treatment of Endometriosis� (3). On this basis, information relevant to clinical practice is summarized in the following, particularly for non-gynecologists. Gastrointestinal endometriosis Gastrointestinal endometriosis (GIE) is the most common location of EE, affecting about 23% of all patients with deep infiltrating endometriosis (DIE) (11). Both superficial peritoneal and deep infiltrating endometriosis lesions are found in the gastrointestinal tract (12). With a proportion of 83.1%, the rectosigmoid colon is the most common site, followed by appendix (6.4%), small intestine (4.7%), cecum (4.1%), and other section of the gastrointestinal tract (1.7%) (11). The characteristic clinical features of GIE include dyschezia, period-related diarrhea, hematochezia or constipation, dyspareunia associated with deep penetration, as well as pain while seated, radiating into the perineum (13). Endometriosis can also cause nonspecific symptoms, such as chronic abdominal pain and flatulence, as they are found, for example, in irritable bowel syndrome (14). According to a retrospective analysis, 36% of female patients with irritable bowel syndrome also suffer from endometriosis (15). Symptoms characteristic of appendicitis as well as ultrasonographic abnormalities in the right lower abdomen may occur in patients with appendiceal endometriosis (16). A population-based study found a significant increase in the likelihood of ileus in patients with GIE (odds ratio (OR): 14.6; 95% confidence interval [11.4; 18.8]) (17). In the diagnostic workup, endometriosis lesions can occasionally be palpated during rectovaginal examination (18). Magnetic resonance imaging (MRI) may be performed if GIE is suspected (19) (Figure 1). However, in the diagnosis of endometriosis of the rectosigmoid colon both MRI and transvaginal ultrasound have a sensitivity of 85% to 90% and a specificity of 96% (20). Although colonoscopy is usually unremarkable in patients with GIE, even in cases with menstrual cycle-related hematochezia (19), colonoscopy is still recommended to rule out other GI conditions in the differential diagnosis of GIE. Furthermore, any stenosis can be reliably detected by colonoscopy (21). Pharmacotherapy of GIE is the same as the usual drug treatment of endometriosis (13, 18). Surgical treatment of GIE is recommended if symptoms cannot be adequately controlled with medication and, as a rule, is determined by the severity of the symptoms, the size of the endometriosis lesion, as well as the expected complications (13). In a prospective study, 33% of patients with GIE decided to undergo surgery after 12 months of drug treatment due to inadequate improvement with medical therapy (22). A retrospective case-control study found that GIE patients with bowel involvement suffering from infertility can benefit from surgical treatment performed prior to the initiation of reproductive treatment in the form of higher pregnancy and live-birth rates (live-birth rates after three cycles of fertility treatment of 70.6% versus 54.9%) (23). Surgical treatment options for endometriosis of the bowel include shaving, discoid resection and segmental resection; the choice of surgical technique depends on the size and location of the lesions (21). For deep rectal lesions up to 5�8 cm from the anal verge, it is of particular importance to weigh the risks of discoid resection or segmental resection against the benefits of such surgery (13, 18). A systematic review found that serious postoperative complications, such as urinary retention and fistulas, occur in about 11% of patients (24) (Table 2). Urogenital endometriosis Endometriosis of the urogenital tract (UGE) is the second most common form of EE. It affects the bladder in over 85% of cases and the ureters, kidneys, and urethra in 10%, 4% and 2% of cases, respectively (25). UGE typically occurs in women aged between 30 and 45 (26). Prior surgery in the lesser pelvis is considered a risk factor for UGE; in addition, familial aggregation has been reported (27). According to a retrospective analysis, patients with low BMI and infiltrating endometriosis involving the parametrium are at an increased risk of ureteral infiltration (OR 2.94; [1.24; 6.97] (28). A retroverted uterus appears to be a protective factor of bladder endometriosis (27). The bladder dome is the part of the bladder most commonly affected by endometriosis. Ureteral endometriosis more frequently affects the left ureter and its distal part due to anatomical differences between the right and left lower abdomen (28). What is treacherous about UGE is that it is asymptomatic in up to 50% of affected patients. Case reports indicate that it can lead to complete loss of function of the upstream kidney, although this very rarely occurs in patients with ureteral endometriosis (29). In addition to the symptoms described above, bladder endometriosis can present with dysuria, recurrent urinary tract infections, hematuria, and symptoms of irritable bladder, as well as vesical tenesmus and even incontinence (30). According to a systematic review, about 40% of women with bladder endometriosis experience perimenstrual symptoms (31). Only 15% of women with ureteral endometriosis are symptomatic, e.g. experiencing costovertebral angle pain or hematuria (25). According to an analysis of 13 patients, 70% of cases of hydronephrosis with UGE were discovered by the treating primary care physician (32). In the diagnostic evaluation, the relation of the symptoms to the menstrual cycle plays a particularly important role. The UGE can present as palpable nodules in the vagina and/or the bowel as well as shortening of the parametrium. According to Carfagna et al., UGE of the bladder wall or ureter may appear as hyperechoic lesions on ultrasound in certain cases (sensitivity nearly 56%, specificity 100%) (e1). Urine examination, including urine cytology, may need to be supplemented by cystoscopy with biopsy to obtain a specimen for histopathological evaluation, especially to aid the differential diagnosis of space-occupying lesions in the bladder area (31). MRI may be helpful if intrinsic ureteral endometriosis or small bladder lesions are suspected. (3). Bladder endometriosis can be treated with medication on a case-by-case basis; however, the current guideline recommends surgical resection of the lesions (3). Hydronephrosis is an absolute indication for surgery. Ureterolysis, aimed at freeing the ureter, should be performed promptly after diagnosis and is successful in 86.7% of cases, according to a meta-analysis (33). Further treatment options include ureteral resection and re-implantation. Risks, such as the postoperative development of a fistula or stenosis, as well as the recurrence rates after surgical treatment of UGE were analyzed in a systematic review (33) (Table 2). Thoracic endometriosis Thoracic endometriosis (TE) is a rare disorder. A systematic review comprising 628 patients showed that TE most commonly affects the diaphragm (44.5%), followed by the pleura (12.7%) and the lungs (4.5%); however, simultaneous involvement of multiple structures is common. Genital involvement is found in 53% to 84% of women with TE (7). Compared to genital endometriosis, the age at onset of the TE is higher by about 5 years (age 30 to 34 years) (34). A typical symptom is menstrual cycle-related, usually right-sided pain in the thoracic, scapular or shoulder region, which can be explained by the common innervation of the diaphragm via segment C5. According to a systematic review, about 10% of patients are affected (7). Another clinical feature of TE is menstrual cycle-related (catamenial) pneumothorax (occurs 24 h before to 72 h after the onset of menstrual bleeding). According to a systematic review, 7.3% to 36.7% of cases of spontaneous pneumothorax in women of childbearing age are due to endometriosis (35). In 93% of all cases, the pneumothorax occurs on the right side, less frequently on the left or bilaterally; the reason for the side preference is not yet fully understood (7, 34). Furthermore, a pneumothorax can also occur without relation to the menstrual cycle, as it is the case in about 25% of all patients with TE (7). In addition to the symptoms associated with involvement of the lung or pleura, hemoptysis, in particular in cases with endometriosis of the lung (82%), cough and dyspnea can occur (7). Diagnosis is based on the association of shoulder/thoracic pain with menstruation as well as diagnostic radiology examination, where MRI showed the highest specificity in the T1 fat-suppressed sequence (36). Bronchoscopy may be helpful in cases of hemoptysis, especially to rule out the much more common differential diagnostic conditions. The definite diagnosis is established by histological confirmation of endometriosis lesions. With regard to surgical management, a meta-analysis recommends a two-stage surgical approach followed by medical treatment (37). First, surgical treatment should be performed. Depending on the likelihood that the symptoms are triggered by endometriosis, surgical management comprises video-assisted thoracoscopic surgery (VATS) (in case of low or moderate probability of TE) or VATS plus laparoscopy in an interdisciplinary approach involving a thoracic surgeon and a gynecologist (in case of high probability of TE). In the majority of cases, defects are found in the diaphragm, which are then treated surgically (7, 38) (Figure 2). In the cases where it is not possible to suture the defect, pleurodesis may subsequently be performed (39). Endometriosis of nerves and skin Nerve involvement is also a rare manifestation of EE. According to a review, the nerves most frequently affected are the nerves of the sacral plexus, especially the sciatic nerve (ESN) (40). Approximately 34% of patients showed involvement of nerves alone without evidence of peritoneal endometriosis lesion (40). Whether the etiopathogenesis can be explained by the development of endometriosis lesions from undifferentiated cells within the nerve itself is subject to ongoing discussion (e2). A characteristic symptoms is cyclic (perimenstrual) sciatica. Leaving the condition untreated over a prolonged period of time may lead to constant pain and neurological deficits (e3). In a retrospective analysis of 267 patients, neurological deficits occurred as early as one to three years after the onset of pain, indicating that ESN is a rapidly progressive form of EE. Corresponding to the motor and sensory territory of the affected sacral plexus nerves, patients may develop hip, leg, and pelvic pain, numbness, tingling, and lower extremity pain, as well as motor deficits with gait disorder and muscle atrophy (40). Symptoms are typically unilateral, predominantly on the right side (e4). Unlike in patients with herniated disc, several nerve roots and thus several dermatomes and key muscles are usually affected. During transvaginal examination of the sacral plexus, a positive Hoffmann-Tinel sign with trigger pain and paresthesia can be elicited in individual cases. Although neurophysiological tests can provide evidence of nerve injury patterns, they are not very useful due to their low specificity. MRI is the diagnostic modality of choice, according to a small case series (e5). Alternatively, ultrasonography is described as a suitable method (e6). Reports of successful drug treatment of endometriosis with involvement of the sacral plexus are rare (e6). Surgical treatment with excision of parametrial and peritoneal lesions is reported in smaller retrospective analyses and case series. Surgery significantly improved the patients� quality of life and pain symptoms, with bladder voiding dysfunction described as the most common postoperative complication (e7). A further location of endometriosis is the cutaneous scar after cesarean delivery, hysterectomy or laparoscopy, presenting as nodules in the epifascial tissue; according to a review, less than 1% of women with endometriosis are affected by this pathology (e8). These benign, painful nodules can be easily excised. Table 1 summarizes the most common locations.

Endometriosis is a benign, but chronic disease, affecting various organ systems and causing a wide variety of symptoms. Prompt initiation of treatment, whether conservative or surgical, is critical to successful management. At the basis of this is the diagnosis of endometriosis. Conflict of interest statement The authors declare that no conflict of interest exists. Manuscript received on 2 November 2021; revised version accepted on 30 March 2022 Translated from the original German by Ralf Thoene, MD. Corresponding author Dr. med. Davut Dayan Universit�tsklinikum Ulm Klinik f�r Frauenheilkunde und Geburtshilfe Prittwitzstr. 43 89075 Ulm (Michelsberg), Germany [email protected] Cite this as: Lukac S, Schmid M, Pfister K, Janni W, Sch�ffler H, Dayan D: Extragenital endometriosis in the differential diagnosis of non-gynecological diseases. Dtsch Arztebl Int 2022; 119: 361�7. 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