UROLOGY JOURNAL Vol. 11 No. 04 July - August 2014 1806 Diagnosis and Treatment of Ureteral Endometriosis: Study Of 23 Cases Dawei Mu,1 Xuesong Li,2 Gaobiao Zhou,1 Heqing Guo1 1Department of Urology, Air Force General Hospital, Beijing, 100142, China. 2Department of Urology, Pe- king University First Hospital, Institute of Urology, Peking University, Beijing, 100034, China. Corresponding Author: Heqing Guo, MD Department of Urology, Air Force General Hospital, Bei- jing, 100142, China. Tel: +86 029 84777443 Fax: +86 029 84777443 E-mail: heqingguo010@163. com Received August 2013 Accepted May 2014 Purpose: To describe our experience in the diagnosis and treatment of 23 patients with ureteral endometriosis. Materials and Methods: We performed a retrospective analysis of 23 cases of ureteral endometriosis with histopathological results from 2002 to 2011. Results: In patients with ureteral endometriosis, 23 cases were diagnosed by ultrasound, 21 by intravenous urography, 11 by retrograde urography, 16 by computed tomography, and 8 with magnetic resonance imaging. All cases were treated by operative treatment. The treatments included ureterolysis in 3 cases, partial ureteral resection and ureteroneocystostomy in 6 cases, partial ureteral resection and end-to-end ureteral anastomosis in 12 cases, and endoscopic resection of ureteral endometriosis lesion in 2 cases. All of the pathologic exam- ination results were endometriosis. Conclusion: Our findings suggest that surgery is an effective treatment option in most patients with ureteral endometriosis exhibiting mild or moderate to severe hydronephrosis. The type of technique depends on the location and depth of the lesion. Keywords: endometriosis; surgery; diagnosis; complications; treatment outcome; abnormalities; ureteral dis- eases. FEMALE UROLOGY Preoperative evaluation included, assessment with the evaluation of ureteral endometriosis related pain using a visual analogue scale (VAS) (10 point rating scale: 0 = absent, 10 = unbearable)11 for six components of disease related pain: dyspareunia, low back pain, menoxenia, hypogastralgia, hematuria and dysmenorrhea. Surgical and clinical data of all cases were collected and recorded in a com- puterized database. Some patients had previous medical and surgical treatment six months before surgery, whereas none were given hor- monal treatment in this period. All patients were preoperatively exam- ined by ultrasonography, and some patients also underwent intrave- nous urography (21 cases), retrograde urography (11 cases), computed tomography (CT) (16 cases) or magnetic resonance imaging (MRI) (8 cases) examinations to assist in confirming the disease. The results revealed that all cases had hydronephrosis. All cases were treated by surgical therapy, including open surgery and laparoscopic surgery. The treatments included ureterolysis in 3 cases, segmental ureterecto- my and ureteroneocystostomy in 6 cases, segmental ureterectomy and ureteroureterostomy in 12 cases, unilateral ovarian cyst excision in 9 cases and laparoscopy fulguration in 2 cases. The cases with negligible adherent involvement that required no spe- cific procedures were excluded. Follow-up included clinical evalua- tion and radiologic assessments (urography or ultrasonography exam- ination) every 3 months for 2 years and then every year. Main outcome measures were preoperative findings, operative details (type and site of ureteral endometriosis, type of intervention), postop- erative urinary function, pain relief, hydronephrosis relief and com- plications. RESULTS Of 1135 patients with endometriosis in the study period from 2002 to 2011, twenty-three cases of ureteral endometriosis were observed, a prevalence of 2.03%. Table 1 shows the preoperative characteristics and findings of the 23 patients in the study. In most patients, the main symptoms were low back pain (17 cases, 73.9%) and hypogastralgia (15 cases, 65.2%). Of the 23 patients, 9 patients (39.13%) had previous medical treatments, such as danazol (3 cases), progesterone (1 case) and gonadotropin-releasing hormone analogue (GnRH)-α (5 cases); 10 patients (43.48%) had previous surgical treatment, which consisted of ipsilateral ureterolysis (3 cases), nephrostomy for ureteral obstruc- tion (4 cases), open ureteroneocystostomy (1 case) and ipsilateral dila- tation of ureteral stenosis (2 cases). However, no patients had received hormonal therapy six months before surgical treatment. The 23 patients all were examined by ultrasonography before surgery; the results showed that all patients had hydronephrosis to a certain extent and ureterectasia. Moreover, the ultrasonography examination also showed an ovarian cyst in 9 of the 23 patients and uterine myoma in 7 of the 23 patients. Twenty-one patients underwent preoperative intravenous urography, which revealed a stricture of the lowest portion of the ureter that was 1.5 to 4.3 cm long. Thirteen patients had mild (5 cases) or moderate to severe (8 cases) hydronephrosis. The results INTRODUCTION Ureteral endometriosis is a rare yet important condition and it is estimated that less than 1% of women with endometriosis also have ureteral endometriosis.(1) There is some evidence that the incidence of ureteral endometriosis is about 1%,(2) whereas other studies reported an incidence of only 0.1%.(3) Although ureteral endometriosis is relatively uncommon and accounts for a small mi- nority of cases, it can lead to renal failure because of the silent ob- struction of the ureter. Ureteral endometriosis can be subcategorized into two types: intrinsic or extrinsic.(4) Intrinsic ureteral endometriosis is rare and characterized by the presence of endometriotic tissue in the ureteral wall. However, extrinsic ureteral endometriosis is more frequent and represented by the presence of endometrial stromal and glandular in the ureteral submucosa and adventitia.(5) Ureteral endometriosis presents a clinical challenge both in diagnosis and treatment. The frequency of ureteral endometriosis is sometimes negligible and missed because patients do not display typical symp- toms. Frequently, nonspecific symptoms are those typically connected with endometriosis, including dyspareunia, dysmenorrhea and pelvic pain.(6,7) However, the indicative symptoms such as cyclic colicky flank pain and renal colic is relatively rare and about 50% of patients are asymptomatic.(8) Therefore, it is very difficult to diagnose ureteral endometriosis before surgical procedures. The surgical treatment of ureteral endometriosis remains the gold standard which should relieve ureteral obstruction and avoid the recurrence.(9) Different conservative surgeries have been proposed according to the pathological conditions of ureteral endometriosis, including laparoscopic management,(10) which could remove the pathologic tissue. The preoperative diagnosis and choice of an appropriate surgical approach are both essential for the treatment of patients with ureteral endometriosis. Therefore, the aim of this study was to report the clinical, pathologic, diagnostic and management findings in a retrospective cohort of 23 cases undergoing various types of surgery for ureteral endometriosis. MATERIALS AND METHODS Twenty-three cases of ureteral endometriosis were gathered from the urinary surgery department in the Air Force General Hospital and Peking University First Hospital between January 2002 and October 2011. All of the women who underwent surgery with pathological ex- amination confirmation of ureteral endometriosis were included in this study. Patients who had medication treatment for ureteral endometrio- sis or undergone surgery for other types of endometriosis were exclud- ed. Patient’s age, body mass index (BMI, kg/m2), history of previous medical treatment and surgical treatment, presenting symptoms and site of involvement were obtained by review of the medical records and pathology reports wherever available. Slides from all cases were summarized for pattern of ureteral involvement (intrinsic or extrinsic) and for any additional related pathologic findings. The affected side was the right and left in 9 and 14 cases, respectively. There was no bilateral case. 1807 Female Urology UROLOGY JOURNAL Vol. 11 No. 04 July - August 2014 1808 Ureteral Endometriosis-Mu et al Of the 23 patients, follow-up data were obtained for 20 patients, while 3 cases were lost to follow-up (Table 2). The 20 patients were sub- mitted to clinical and radiological follow-up (ultrasonography and intravenous urography) every 6 months for the first 2 postoperative years and then every year thereafter. Relief from pain was noted in 18 patients (90%). Only 1 of the 20 patients (case no. 18) underwent re- peated laparoscopy after 7 months because of the recurrence of pelvic pain. However, preoperative intravenous urography and ultrasonogra- phy in this woman; did not show ureteral dilatation. In the 20 patients, no relapses of ureteral endometriosis were found within the follow-up period of 41 months (range 7-98 months). Relief from hydronephrosis was observed in all patients and the symptoms of ureteral disease dis- appeared in 12 patients. Additional hormonal medications were given to 8 patients who had severe ureteral endometriosis. According to the follow-up data of all cases, we found that surgery is an effective treat- ment option in patients with ureteral endometriosis exhibiting mild or moderate-to-severe hydronephrosis. After ureterolysis and segmental ureterectomy, there were no relapses of disease during the follow-up period. Our study increased the degree of awareness in clinicians and providing evidence in choosing a more adequate clinical management method for the lesser understood aspects of the disease. DISCUSSION Endometriosis is one of the most common gynecologic disease in women, it usually occurs between menarche and menopause as a re- sult of the fluctuating levels of progesterone and estrogen required for the propagation and stimulation of endometrial proliferation.(12) The insidious onset of endometriosis portends considerable morbidity, and thus, the disease need a high index of suspicion for both urologists and gynecologists.(13) About 10% of women in the reproductive age have involvement of the genitourinary tract by endometriosis, where- as disease affecting the ureter is infrequent, accounting for less than 0.3% of all types of endometriosis. Although the morbidity of ureteral lesions is relatively low, the disease can cause severe silent loss of renal function.(14) In contrast to the literature, in our study, the ureter was involved in 23/1135 (2.03%) cases. The peak incidence of ureteral endometriosis is around 30-45 years, and the patients were either nul- liparous (9 cases, 39.1%) or had one (8 cases, 34.8%) or two children (6 cases, 26.1%), born several years ago. also indicated normal kidney function in 13 patients, which was ac- companied with a filling defect of the lower ureter in 2 of the 13 pa- tients. Moreover, 11 of the 13 patients had a stricture of the lower ureter. Eight patients who had absent or extremely faint kidney images were further examined by retrograde pyelography. The results indicat- ed that 5 patients had hydronephrosis, dilation of upper ureteral and stricture of the lower ureter. Three patients who failed to be examined by retrograde pyelography were assessed using MRI. Sixteen of the 23 patients underwent preoperative CT scan, which revealed that 14 of the patients had strictures of the lower ureter and a soft-tissue mass around the tube wall, and 2 patients had a mass in the lumen of the ure- ter. As shown in Figure, enhanced CT scan imaging shows the space occupying lesion in lower part of left ureter. Retrograde pyelography of patients shows hydronephrosis in left kidney, dilatation in upper part of ureter, and filling defect in lower part of left ureter. Ureteroscopy shows the papillary neoplasm in lower part of left ureter. Eight patients underwent preoperative MRI; the results showed that all patients had dilatation of the upper ureter and hydronephrosis. The results of clinical evaluation support the notion that all patients may suffer from ureteral endometriosis. In 15 cases, endometriosis involved the left ureter, whereas the right ureter was involved in 9 cases. No patient had bilateral involvement. All patients were affected in the distal third of the ureter. Moreover, ureteral involvement by endometriosis was extrinsic in 18 cases, but intrinsic in 5 cases. All cases were treated by surgical therapy, includ- ing open surgery and laparoscopic surgery; the surgical methods are summarized in Table 2. Intra- and post-operative complications are reported in Table 3. There were no cases of complications requiring re-intervention. In- traoperative complications include bladder injury in 1 case (4.3%), ureteral injury in 3 cases (13.0%), hemorrhage in one case (4.3%) and large vessel injury in one patient (4.3%). After surgery, 2 patients dis- played dysuria, blood loss causing anemia occurred in 3 cases, hema- turia occurred in one patient, 4 patients developed fever, and vaginal infection and urinary infection occurred in 1 and 2 cases, respectively. Follow-up ranged from 7 to 98 months. The median follow-up was 3.42 years (3 years, 5 months). The maximum follow-up was 8.17 years (8 years, 2 months) and the minimum follow-up was 7 months. Figure. (A) Enhanced computed tomography scan of patients. White arrow shows the space occupying lesion in lower part of left ureter. (B) Retrograde pyelog- raphy of patients. White arrow shows hydronephrosis in left kidney and dilatation in upper part of ureter. Black arrow shows the filling defect in lower part of left ureter. (C) Ureteroscopy shows the papillary neoplasm in lower part of left ureter. types.(15,16) The extrinsic form (70%-80% of cases) is characterized by Ureteral endometriosis can be divided into extrinsic and intrinsic Case no. Age BMI Previous Medical Treatment Previous Surgical Treatment Presenting Symptoms (years) (kg/m2) 1 42 21.3 + Dyspareunia, Menoxenia, Low back pain 2 34 22.6 + Low back pain, Hypogas- tralgia 3 45 23.1 + Dysmenorrhea, Menoxenia, Low back pain, Hypogastralgia 4 42 22.6 + Dyspareunia, Menoxenia 5 23 18.6 + Hematuria, Hypogastralgia 6 50 22.4 + Low back pain, Hypogastralgia 7 45 23.5 + Dyspareunia, Low back pain 8 37 23.3 + Dysmenorrhea, Menoxenia, Hypogastralgia 9 43 22.2 Low back pain, Hypogastralgia 10 44 24.0 + Hematuria, Low back pain Hypogastralgia 11 41 21.9 + + Dyspareunia,Low back pain 12 26 18.8 Menoxenia, Hypogastralgia 13 33 23.7 Menoxenia, Low back pain 14 29 21.5 + Dysmenorrhea, Low back pain, Hypogastralgia 15 27 20.9 + + Dysmenorrhea, Menoxenia Low back pain, Hypogastralgia 16 47 22.4 Dyspareunia,Low back pain 17 39 21.7 Hypogastralgia 18 33 19.9 + Low back pain, Hypogastralgia 19 35 23.6 + Hematuria, Low back pain, Hypogastralgia 20 22 18.9 + Dysmenorrhea, Menoxenia, Low back pain 21 34 20.5 Dyspareunia,Low back pain Hypogastralgia 22 21 20.7 + Hypogastralgia Hematuria 23 40 22.5 + Dysmenorrhea,Low back pain, Hypogastralgia Mean 36.2(SD = 4.5) 36.2 (SD = 2.6) ----- Table 1. Characteristics of cases in the study. Abbreviation: BMI, Body mass index. 1809 Female Urology UROLOGY JOURNAL Vol. 11 No. 04 July - August 2014 1810 the surrounding organs or structures. The intrinsic form (20%-30% of cases) is less common than the extrinsic form. The intrinsic ureteral endometriosis always occurred in the ureteral mucosa or the muscular layer, because of hematogenous metastasis or lymphatic metastasis. ureteral obstruction caused by external compression by surrounding endometriosis. In the extrinsic form, patients were found to have ureter strictures, ureteral obstruction and hydronephrosis, because endome- triosis lesions affect the external ureteral tunics through adherence to Case no. Surgical Therapy Duration of Surgery Follow-up Intraoperative Complication Post operative- (min) (month) Complication 1 Left ureteroureterostomy and 150 33 Ureter injury, hemorrhage Anemia left ovarian cyst resection 2 Right ureteroureterostomy 195 Lost to follow-up None None 3 Right ureteroureterostomy and 237 31 Bladder injury Hematuria right ovarian cyst resection 4 Left ureteroneocystostomy and 359 56 None Dysuria, Fever left ovarian cyst resection 5 Right ureterolysis 187 48 None None 6 Right ureteroureterostomy 285 51 None None 7 Left ureteroureterostomy 169 98 Ureter injury UTI, Vaginal infection, Fever 8 Right ureteroneocystostomy and 415 45 Large vessel injury Anemia right ovarian cyst resection 9 Left ureteroureterostomy 177 68 None None 10 Left ureteroneocystostomy and 430 40 Ureter injury None left ovarian cyst resection 11 Right ureteroureterostomy 265 54 None Anemia 12 Left ureteroureterostomy and 345 35 None UTI, Fever left ovarian cyst resection 13 Left ureterolysis 280 42 None None 14 Right ureteroureterostomy 330 65 None ` None 15 Left ureteroneocystostomy 385 49 None Dysuria, Fever 16 Left ureteroureterostomy and 430 37 None None left ovarian cyst resection 17 Right ureteroneocystostomy 210 40 None None 18 Left laparoscopy fulguration 240 12 None None 19 Left ureterolysis 335 9 None None 20 Left ureteroneocystostomy and 395 Lost to follow-up None None Left ovarian cyst resection 21 Left ureteroureterostomy 248 11 None None 22 Right laparoscopy fulguration 155 7 None None 23 Left ureteroureterostomy and 310 Lost to Follow-up None None left ovarian cyst resection Mean/median ----- 284 (mean) 41 (median) ----- (SD = 3.69) (7 ~ 98 months) Table 2. Surgical and follow-up data of study subjects. Abbreviation: UTI, urinary tract infection. Ureteral Endometriosis-Mu et al quires demonstration of endometrial tissue on a pathology specimen. The general principles of treatment for ureteral endometriosis should be considered to relieve the ureteral obstruction and symptoms, and to protect renal function. The therapeutic methods for endometri- osis include medical and surgical therapy.(17) Surgical therapy is the paramount consideration for the patients with hydronephrosis; most scholars argue that ureterolysis is the first choice for treating patients with hydronephrosis.(18) Bosev and colleagues believe that ureteroly- sis is an effective treatment option in vast majority of cases that can be safely accomplished, even in patients with moderate to severe hy- dronephrosis.(10,19) However, the management of ureteral endometrio- sis in cases of moderate to severe hydronephrosis is still contentious; some researchers believe that ureterolysis is more suited to cases with mild hydronephrosis, whereas patients with moderate to severe hydronephrosis should be treated by resection of the diseased ureter and subsequent ureteroneocystostomy or ureteroureterostomy, which can prevent further renal damage.(20,21) Pelvic endometriosis should be treated if the patients have ureteral endometriosis accompanied with pelvic endometriosis. In cases with severe local lesions, perioperative auxiliary treatment with hormones (such as progestone, nemestran or danazol) can reduce tissue edema, narrow lesions and reduce the re- currence rate. In the current study, preoperative assessment by CT scan and MRI examination and intraoperative ascertainment of 23 patients revealed that 5 patients had lesser degrees of obstruction and mild hydronephro- sis. These patients were treated by relatively conservative ureterolysis and laparoscopy fulguration. The other patients (18 cases) suffered from high degrees of obstruction and moderate to severe hydronephro- sis. Of the 18 patients, segmental ureteral resection and ureteroneocys- tostomy were performed in 6 cases, segmental ureteral resection and ureteroureterostomy were carried out in 12 patients and ovarian cyst resection was performed in 9 cases in the corresponding period. Of the 23 patients, follow-up data were obtained for 20 patients, ultraso- nography and intravenous urography were performed to recheck for symptoms, and the results showed that the hydronephrosis has been alleviated in all patients. The symptoms of 12 cases disappeared af- ter surgery; 8 cases were observed to have serious lesions intraopera- tively, auxiliary treatment with hormones was given after surgery, but there was no recurrence during the follow-up period. Overall, these results revealed that the surgical management is a better choice for patients with hydronephrosis. The effects of surgical management is associated with a number of factors, such as patient’s age, symptoms, degree of obstruction, the surgery thoroughness, adjuvant therapy and the desire to preserve reproductive function. CONCLUSION We concluded that ureterolysis is an effective treatment option for patients with lesser degrees of obstruction and mild hydronephrosis, whereas resection of the diseased ureter and subsequent ureteroneo- cystostomy or ureteroureterostomy were more suitable for patients Ureteral endometriosis is often asymmetrical, more commonly in- volving the distal segment of the left ureter.(5) In the current study, in all cases of ureteral endometriosis involving the distal segment of the ureter and occurring on a single side, the affected side was the left in fourteen and the right in nine of the twenty-three cases, where- as, bilateral involvement was not found in the twenty-three patients. Of the 23 patients, 18 cases (78.3%) presented with extrinsic ureteral endometriosis, whereas 5 of the 23 patients presented with intrinsic form. The ratio of extrinsic and intrinsic forms was consistent with the literature reports.(16) The onset of ureteral endometriosis is latent. Indeed, clinical symp- toms and signs are often silent (52.2% of our cases), owing to the non-specific symptoms; the disease always progressed to silent ob- struction and the loss of renal function. Therefore, the diagnosis of ureteral endometriosis is very difficult. Along with extensive pelvic endometriosis, some patients presented the clinical symptoms of dys- menorrhea, dyspareunia, pelvic pain, infertility and repeated urinary tract infections. Also, symptoms of chronic pelvic inflammation, in- terstitial cystitis, irritable bowel syndrome and other diseases often co-occurred. Thus, the surgeon should distinguish ureteral endometri- osis from other diseases. The preoperative diagnosis is very difficult when specific symptoms of ureteral endometriosis are lacking. Ureteral endometriosis is in- creasingly recognized with the greater the awareness of it. On clinical examination, ureteral endometriosis can be easily missed. A delay in diagnosis can lead to significant morbidity,(17) such as a consequent worsening of hydronephrosis and silent renal function loss. Therefore, early diagnosis is very important for this disease. Multiple diagnostic tests can be used to confirm the existence of ureteral endometriosis. Ultrasonography, laparoscopy, intravenous urography, ureteroscopy with endoluminal ultrasound, CT scan and MRI are common diagnos- tic tools.(14) In the current study, the 23 cases were examined by ultra- sonography, laparoscopy, intravenous urography, CT scan and MRI. Based on the medical history, signs, results of imaging modalities and ureteroscopy of the patients, we suspected that all cases suffered from ureteral endometriosis. However, the final diagnosis of the disease re- Intraoperative Postoperative Complication Number (%) Complication Number (%) Bladder injury 1 4.3 Dysuria 2 8.7 Ureter injury 3 13.0 Anemia 3 13.0 Hemorrhage 1 4.3 Hematuria 1 4.3 Large vessel injury 1 4.3 Vaginal infection 4.3 UTI 2 8.7 Fever 4 17.4 Table 3. Intraoperative and postoperative complications. Abbreviation: UTI, urinary tract infection. 1811 Female Urology UROLOGY JOURNAL Vol. 11 No. 04 July - August 2014 1812 the same pathogenesis. Obstet Gynecol Surv. 2009;64:830-42. 18. Camanni M, Delpiano EM, Bonino L, Deltetto F. Laparoscopic conser vative management of ureteral endometriosis. Curr Opin Obstet Gynecol. 2010;22:309-14. 19. Bosev D, Nicoll LM, Bhagan L, et al: Laparoscopic Management of Ure- teral Endometriosis: The Stanford University Hospital Experience With 96 Consecutive Cases. J Urol. 2009;182:2748-2752. 20. Marco C, Luca B, Elena D, et al. Laparoscopic conservative management of ureteral endometriosis: a survey of eighty patients submitted to urete- rolysis. Reprod Biol Endocrinol. 200912;7:109. 21. Chapron C, Chiodo I, Leconte M, et al. Severe ureteral endometriosis: the intrinsic type is not so rare after complete surgical exeresis of deep endometriotic lesions. Fertil Steril. 2010;93:2115-120. with moderate to severe hydronephrosis. CONFLICT OF INTEREST None declared. REFERENCES 1. Gabriel B, Nassif J, Trompoukis P, Barata S, Wattiez A. Prevalence and management of urinary tract endometriosis:a clinical case series. Uro- logy. 2011;78:1269-74. 2. Nezhat C, Nezhat F, Nezhat CH, Nasserbakht F, Rosati M, Seidman DS. Urinary tract endometriosis treated by laparoscopy. Fertil Steril. 1996;66:920-4. 3. Donnez J, Brosens I. Definition of ureteral endometriosis? Fertil Steril. 1997;68:178-80. 4. Blaustein’s Pathology of The Female Genital Tract. 5th ed., Springer- Verlag, New York, 2002. p 1193-1247. 5. Yohannes P. 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Ureteral and vesical endometriosis: two different clinical entities sharing Ureteral Endometriosis-Mu et al