Endometriosis of the ureter and bladder are not associated diseases

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1 ENDOMETRIOSIS Endometriosis of the ureter and bladder are not associated diseases Mauricio Simoes Abrao, M.D., Ph.D., a,b Joao Antonio Dias, Jr, M.D., a,b Patrick Bellelis, M.D., a Sergio Podgaec, M.D., Ph.D., a,b Carlos Ricardo Bautzer, M.D., b and Celso Gromatsky, M.D., Ph.D. b a Department of Obstetrics and Gynecology, University of S~ao Paulo Medical School, and b Sirio Libanes Hospital, S~ao Paulo, Brazil Objective: To verify whether bladder and ureter had the same clinical features and disease behavior. Design: Case-control study. Setting: Multidisciplinary group in Sao Paulo, Brazil. Patient(s): A total of 690 patients were submitted to laparoscopy with histologically diagnosis of between July 1999 and December Twelve of these patients had lesions affecting the ureter and 26 had lesions affecting the bladder. A control group consisted of 652 patients in whom was not affecting either the ureter or the bladder. Intervention(s): None. Main Outcome Measure(s): Clinical and surgical features of patients with ureteral or bladder. Result(s): No patients with ureteral had lesions affecting the bladder. Compared with the control group, patients with ureteral had more advanced disease (Stages III and IV) according to the American Society of Reproductive Medicine (ASRM) staging classification (100% vs. 65.5%); they also had more retrocervical (83.3% vs. 21.6%) and rectum-sigmoid lesions (91.7% vs. 17.9%). Compared with the control group, more patients with bladder had cyclic dysuria and/or hematuria (34.6% vs. 9.8%), more advanced stages of the disease (88.4% vs. 65.5%), and an association with of the rectum-sigmoid (65.3% vs. 17.9%). Conclusion(s): Ureter is not associated with the bladder disease; however, it is associated with advanced ASRM stages and with retrocervical and rectum-sigmoid lesions. (Fertil Steril Ò 2009;91: Ó2009 by American Society for Reproductive Medicine.) Key Words: Ureteral, bladder, of the urinary tract, deeply infiltrating Endometriosis is a common gynecologic affliction that affects between 5% and 15% of women of reproductive age and up to 3% 5% of postmenopausal women (1). It is characterized by implantation of the stroma and/or endometrial glandular epithelium outside the uterus (2) and may affect various sites, including the ovaries, peritoneum, uterosacral ligaments, retrocervical region, and the rectovaginal septum, as well as the rectum/sigmoid, bladder, and other portions of the digestive tract. The foci of may be classified as superficial, when they reach a depth <5 mm, or deep,when reaching a depth >5 mm, the depth of the lesion reflecting the severity of symptoms and guiding therapeutic management (3). Received December 4, 2007; revised and accepted February 21, 2008; published online April 14, M.S.A. has nothing to disclose. J.A.D. has nothing to disclose. P.B. has nothing to disclose. S.P. has nothing to disclose. C.R.B. has nothing to disclose. C.G. has nothing to disclose. Reprint requests: Mauricio Simoes Abrao, Ph.D., Rua S~ao Sebasti~ao 550, , S~ao Paulo, SP, Brazil (FAX: þ ; msabrao@attglobal.net). Endometriosis of the urinary tract is rare, occurring in approximately 1% of all patients with (4). The first case of causing obstructive uropathy was described by Cullen in 1917 (5). A classic evaluation of 147 patients with showed that in patients in whom the urinary tract is affected, the most frequently affected sites are the bladder in approximately 84% of cases, followed by the ureter in 10%, the kidney in 4%, and the urethra in 2% (6). When affects the bladder, its symptoms include suprapubic pain accompanied by polyuria (41%), dysuria (21%), and hematuria (19%). Repeated urinary infections may also occur (7). Ureteral is generally characterized by nonspecific urinary symptoms, occasionally evolving insidiously to kidney failure. In the majority of cases, it is diagnosed fortuitously during surgery carried out to treat extensive endometriotic lesions (8). No reports have been published in the literature on studies in which patients with involving the urinary tract were evaluated with respect to clinical status or the 1662 Fertility and Sterility â Vol. 91, No. 5, May /09/$36.00 Copyright ª2009 American Society for Reproductive Medicine, Published by Elsevier Inc. doi: /j.fertnstert

2 existence of other sites affected by. Therefore, the objectives of the present study were to establish the clinical and surgical characteristics of patients with ureteral and bladder, establishing comparisons between these patients and wtih patients with in other sites. PATIENTS AND METHODS Between July 1999 and December 2006, 690 consecutive patients were submitted to videolaparoscopy with diagnosis of in the Endometriosis Division of the Department of Gynecology, Teaching Hospital of the School of Medicine, University of S~ao Paulo. During the laparoscopy, peritoneal, ovarian, and deep that was removed was submitted to histologic analysis, including for the disease compromising the ureteres and bladder. The clinical suspicion and indication for surgery were based on the symptoms reported by the patients, physical examination, and/or data obtained from imaging examinations (pelvic or transvaginal sonography and/or pelvic magnetic resonance imaging). In 12 of the 690 patients, was found to be affecting the ureter, and in another 26 the disease was found to be affecting the bladder. These organs were considered to be affected when, in the case of the bladder, the disease had reached the muscular layers, and, in the case of ureter, when the lesions infiltrated the ureteral wall or when external ureteral compression by lesions was responsible for a ureteral obstruction. The study was approved by the Internal Review Board of the institution. All patients evaluated in this study answered a questionnaire given preoperatively in which information on their demographic data, clinical status, principal symptoms, and any previous treatment was requested. Pain intensity was classified into four subtypes: mild, moderate, severe, or incapacitating. It was defined as mild when no medication was required for its control, moderate when over-the-counter analgesics administered at home were capable of controlling it, severe when parenteral medication administered in a hospital was required, and incapacitating when it prevented the patient from carrying out routine activities. For the purposes of tabulation and statistical analysis, only symptoms classified as severe or incapacitating were considered in this study. Patients were considered to be infertile if they had been trying to become pregnant for at least a year while having a regular sex life and not using contraceptive methods. Cyclic bowel or urinary symptoms were defined as the presence of bowel or urinary pain and/or bleeding that occurred only during menstruation. All patients were submitted to videolaparoscopy, and all surgical findings were recorded and tabulated. The American Society for Reproductive Medicine (ASRM) classification (1996) was used to stage the disease (9). The number of sites of, the presence of ovarian and the side of the affected ovary,and the presence of peritoneal or of the deep form of the disease (>5 mm of depth) in the retrocervical and rectum-sigmoid sites were evaluated, as well as the presence of lesions in the bladder and ureter. Histologic confirmation was carried out for all these sites, including the superficial peritoneal lesions. These data were stored and tabulated, together with the intraoperative and postoperative findings, in a database using the Access software program (Microsoft Office 2004 for Windows). The clinical and surgical findings of three groups were compared: the first group consisted of patients in whom the ureter was affected (n ¼ 12), the second group comprised patients in whom the bladder was affected (n ¼ 26), and the third, considered to be the control group, consisted of patients with in whom neither the ureter nor the bladder was affected (n ¼ 652). Statistical analysis was carried out using the SPSS software program. The results were compared using the following two-sided tests: analysis of variance, Kruskal-Wallis, chi-squared, Fisher exact, and the likelihood ratio test. Statistical significance was defined as P<.05. The variables with statistical differences were adjusted in a multiple logistic regression. RESULTS Table 1 shows the preoperative clinical data of the patients in this study. Cyclic urinary symptoms were not related to the presence of foci of in the ureter (2 of 12 [16.7%] in the group of patients with ureteral compared with 64 of 652 [9.8%] in the control group). There was a greater prevalence of cyclic urinary symptoms (9 of 26, 34.6%) in patients with bladder compared with the control group (64 of 652, 9.8%) and with the group with of the ureter (P<.05). On the other hand, patients with ureteral had a greater prevalence of severe or incapacitating dysmenorrhea (9 of 12, 75%) compared with patients with bladder (10 of 26, 38.5%) and with the patients in the control group (162 of 652, 24.8%) (P<.05). There was a greater prevalence of cyclic bowel symptoms among the patients with bladder compared with the control group; however, there were no differences with respect to the prevalence of cyclic bowel symptoms when the patients with ureteral were compared with the patients in the control group or with those with bladder. No differences were found between the study groups with respect to obstetric history or history of previous surgeries for. The intraoperative findings are summarized in Table 2. The bladder was not affected by in any of the patients with ureteral. Lesions were unilateral in all patients with ureteral, and all the lesions were localized in the lower third of the ureter. The patients with ureteral and bladder were found to have more advanced stages of the disease (III and IV) compared Fertility and Sterility â 1663

3 TABLE 1 Clinical characteristics of the patients operated. A. Ureteral (n [ 12) B. Bladder (n [ 26) C. Endometriosis not affecting the urinary tract (n [ 652) P value Age (mean SD) ,2,3: >.05 Severe/incapacitating dysmenorrhea (n %) 9 (75.0%) 10 (38.5%) 162 (24.8%) 1,3: <.5 2: >.05 Acyclic pain (n %) 9/12 (75%) 16 (61.5%) 367 (56.3) 1,2,3: >.05 Deep dyspareunia (n %) 7 (58.3%) 17 (65.4%) 367/644 (57%) a 1,2,3: >.05 Cyclic urinary changes (n %) 2 (16.7%) 9 (34.6%) 64 (9.8%) 1,3: >.05; 2:<.05 Cyclic bowel changes (n%) 6 (50%) 14 (53.8%) 164 (25.1%) 2:.001 1,3: >.05 Infertility (n %) 6/8 (75%) 14/18 (77.8%) 257/467 (55.1%) 1: 1.0; 2: 0.057; 3:.3 Previous surgeries for ,2,3: >.05 (mean SD) Number of previous pregnancies ,2,3: >.05 (mean SD) Number of previous deliveries ,2,3: >.05 (mean SD) Cesarean deliveries ,2,3: >.05 (mean SD) Abortions (mean SD) ,2,3: >.05 Note: Comparisons: 1) A vs. B; 2) B vs. C; 3) A vs. C. a Eight patients with no active sexual life. Abrao. Ureter and bladder. Fertil Steril with patients in the control group (100%, 88.5%, and 65.4%, respectively; P<.05). There were no differences in the stage of the disease between the patients with ureteral and bladder. Regarding the number of sites affected by the disease, the patients with ureteral had a greater number of lesions ( ) compared with the patients with bladder ( ) and compared with the control group ( ) (P<.05). The patients with bladder also had significantly more lesions compared with the control group (P<.05). Regarding the site of the associated lesions, retrocervical lesions were more frequently found in patients with ureteral (83.3%) compared with the patients with bladder (19.2%) and with the control group (21.6%) (P<.05). There were no statistically significant differences in the coexistence of retrocervical lesions between the patients with bladder and the control group. The coexistence of rectum-sigmoid lesions was found more frequently in patients with of the ureter (91.7%) compared with the control group (17.9%) (P<.05). The patients with bladder also had more lesions of the rectumsigmoid (65.4%) compared with the control group (P<.05). There were no statistically significant differences in the coexistence of lesions of the rectum-sigmoid between patients with bladder and ureteral. The group of patients with ureteral was compared with the control group using multivariate analysis of the data obtained. The patients with severe or incapacitating dysmenorrhea were found to have a 4.5-fold (95% confidence interval [CI] ) greater chance of having ureteral compared with the control group. The risk of affecting the ureter in patients with in the retrocervical region or the rectum-sigmoid was 7.2 (95% CI ) and 22.1 (95% CI ) times greater, respectively, compared with the control group, as shown in Table 3. Table 4 shows that the patients with urinary pain and/or bleeding during menstruation are more likely to have bladder compared to the group in whom the urinary tract was not affected (odds ratio [OR] 4.5, 95% CI ). Moreover patients with rectum-sigmoid have a greater risk of concomitantly having of the bladder compared with the control group (OR 8.3, 95% CI ) Abrao et al. Ureter and bladder Vol. 91, No. 5, May 2009

4 TABLE 2 Surgical characteristics of the patients operated. A. Ureteral (n [ 12) B. Bladder (n [ 26) C. Endometriosis not affecting the urinary tract (n [ 652) P value Stage I or II 0 3 (11.5%) 225 (34.5%) 1: ns Stage III or IV 12 (100%) 23 (88.5) 427 (65.5%) 2,3: <.05 Number of sites affected by ,2,3:.001 (mean SD) Peritoneum (n %) 7 (58.3%) 11 (42.3%) 353 (54.1%) 1,2,3: >.05 Ovary (n %) 9 (75%) 14 (53.8%) 371 (56.9%) 1,2,3: >.05 Retrocervical (n %) 10 (83.3%) 5 (19.2%) 141 (21.3%) 1,3: <.05 2: >.05 Rectosigmoid (n %) 11 (91.7%) 17 (65.4%) 117 (18%) 2,3: <.05 1: >.05 Note: Comparisons: 1) A vs. B; 2) B vs. C; 3) A vs. C. Abrao. Ureter and bladder. Fertil Steril DISCUSSION Endometriosis of the urinary tract is a rare finding (1% 2%); it is localized in the bladder in 84% of cases and in the lower third of the ureter in 10% (10). The objective of the present study was to verify the clinical behavior of affecting two sites, bladder and ureter, that appear to be similar because they both are part of the urinary tract. In our sample of 690 patients with histologic diagnosis of, there were 38 cases (5.5%) in which the urinary tract was affected, 26 (68.5%) of which with the bladder affected and 12 (31.5%) of which with the lower third of the ureter affected. These rates are higher than those reported by other investigators (11, 12), who found an incidence of 1.2% of involvement of the genitourinary tract with a peak incidence occurring in patients of years of age. This difference may be explained by the fact that this is a tertiary referral center to which advanced cases of the disease are sent from other hospitals in the region. One of the goals of this study was to outline the first step of the diagnosis of this kind of : analysis of the clinical signs of the patient. It has been suggested that when affects the urinary tract, patients could present with nonspecific abdominal and urinary symptoms, mimicking other clinical, surgical, urologic, or gynecologic disorders (11), or they could present with specific symptoms, such as dysuria and hematuria during menstruation, mainly when there were lesions in the bladder (7). A recent study with 41 patients with bladder showed that 53.7% of the patients presented dysuria and that the severity and frequency of this symptom had a positive correlation with, respectively, the diameter and the presence of the lesion in base of the bladder (12). In the present sample, there was a greater prevalence of cyclic urinary symptoms (pain and/ or bleeding) in patients in whom the bladder was affected (34.6%) compared with patients in whom the ureter was affected (16.7%) or those without lesions in urinary tract (9.8%). Similar results were observed by Faucconier et al. (2002), who evaluated, in a retrospective analysis, if specific types of pelvic pain had a correlation with the anatomic locations of deeply infiltrating. Those authors found that lower urinary tract symptoms were more frequent when deep lesions involved the bladder (13). TABLE 3 Multivariate analysis of the patients with ureteral compared with the patients without ureteral. Variable Parameter estimated Standard error Odds ratio 95% CI P value Retrocervical Endometriosis of the rectosigmoid Incapacitating dysmenorrhea Abrao. Ureter and bladder. Fertil Steril Fertility and Sterility â 1665

5 TABLE 4 Multivariate analysis of the patients with bladder compared with those without bladder. Variable Parameter estimated Standard error Odds ratio 95% CI P value Cyclic dysuria and/or hematuria Endometriosis of the rectosigmoid Abrao. Ureter and bladder. Fertil Steril The symptoms related to ureter involvement are often mild, but approximately 50% of the women in whom the ureter is affected by have some kind of symptomatology (14). In the present study, the patients in the group in whom the ureter was affected had a greater incidence of severe or incapacitating dysmenorrhea (75%) compared with patients with bladder (38.5%) or those in whom the urinary tract was not affected (24.8%), a finding that had not been reported in any previous publication. This condition could occur owing to the great extension of disease that is usually associated with ureteral. In a study that tried to verify the relation between the severity of dysmenorrhea and the extent of disease, a multivariate analysis was performed in several features of 209 patients with deep infiltrating (DIE) and concluded that the presence of a rectal or vaginal infiltration by the posterior DIE and extensiveness of adnexal adhesion were factors related to dysmenorrhea severity (15). Despite the greater prevalence of severe or incapacitating dysmenorrhea, the present findings showed that when the ureter is affected, symptoms are no different from the classic symptoms of. Unfortunately, owing to the vague and nonspecific clinical data, in a great number of patients with ureteral an insidious, chronic, and obstructive uropathy can develop and kidney failure may even occur (16). Concerning cyclic bowel symptoms, the present results showed that there was a greater prevalence of these symptoms among patients with bladder compared with the control group. This association may occur because 65.8% of the patients that had bladder also had lesions affecting the rectum-sigmoid, which is concordant with the affirmation that endometriotic nodules of the bladder are often associated with other forms of the disease, including deeply infiltrating lesions (17). However, there were no differences related to these symptoms when patients with ureteral were compared with patients in the control group or with those with bladder. In their study, Faucconier at el. did not find any differences in patients with gastrointrestinal symptoms when the urinary tract was affected (13). During the laparoscopic procedures, it was also found that patients with ureteral and bladder were found to have more advanced stages of the disease (III and IV according to ASRM 1996) compared with patients in the control group (100%, 88.5%, and 65.4%, respectively). This observation is coherent with the data concerning the sites of the associated endometriotic lesions. Retrocervical lesions were more frequently found in patients with ureteral (83.3%) compared with patients with bladder (19.2%) and the control group (21.6%), rectum-sigmoid lesions were found more frequently in patients with of the ureter (91.7%) compared with the control group (17.9%), and patients with bladder also had more lesions of the rectum-sigmoid (65.4%) compared with the control group. These results also allow us to observe that that compromises the urinary tract cannot be considered to be primary lesions from these organs. Multivariate analysis showed that the patients with cyclic pain or hematuria had an OR of 4.5 of having bladder compared with patients with in whom the bladder was not affected, confirming this symptom as predictive of the bladder being affected by. Whereas in the majority of cases of bladder published in the literature there was a report of previous pelvic or abdominal surgery (4), in the present sample of patients with bladder this was not found. A positive correlation was observed between ureteral and the chance of having incapacitating dysmenorrhea and associated lesions of the retrocervical region or the rectum-sigmoid. According to the results, patients with incapacitating dysmenorrhea had a 4.5-fold greater risk of having ureteral. Donnez et al. found similar results concerning the possibility of ureteral in patients with significant dysmenorrheal (18). Besides, patients with retrocervical were found to have a 7-fold greater chance of having ureteral, and patients with of the rectum-sigmoid had 22-fold greater chance of having ureteral. In our point of view, the most significant data of this study were that the bladder was not affected by in any of the patients with ureteral. This observation confirms that, although ureter and bladder are both part of the urinary tract, endometriotic lesions affecting these sites have a completely different behavior, as shown by the clinical findings of the present study. It is possible to extend these 1666 Abrao et al. Ureter and bladder Vol. 91, No. 5, May 2009

6 observations to the pathogenesis of that is not yet completely clear, but it would appear that ureteral and bladder have two different etiologies. In a continuous series of 426 patients with DIE, Chapron et al. (2006) demonstrated that the distribution of these lesions were asymmetric in the pelvis, mainly because of the anatomic difference between the left and right hemipelvis and to the flow of peritoneal fluid. They support the hypothesis that retrograde menstruation of regurgitated endometrial cells could be implicated in the pathogenesis of DIE (19). The presence of retrocervical and rectum-sigmoid involvement in the majority of the present patients with ureteral allows us to confirm that the origin of ureteral is extrinsic and also to suggest that its pathogenesis is similar to that of cases of DIE of the retrocervical region and rectum-sigmoid. REFERENCES 1. Modesitt SC, Tortolero-Luna G, Robinson JB, Gershenson DM, Wolf JK. Ovarian and extraovarian -associated cancer. Obstet Gynecol 2002;100: Olive DL, Pritts EA. Treatment of. N Engl J Med 2001;345: Cornillie FJ, Oosterlynck D, Lauweryns JM, Koninckx PR. Deeply infiltrating pelvic : histology and clinical significance. Fertil Steril 1990;53: Schneider A, Touloupidis S, Papatsoris AG, Triantafyllidis A, Kollias A, Schweppe KW. Endometriosis of the urinary tract in women of reproductive age. Int J Urol 2006;13: Cullen TS. Adenomyoma of the recto-vaginal septum. Bull Johns Hopkins Hosp 1917;28: Abeshouse BS, Abeshouse G. Endometriosis of the urinary tract: a review of the literature and a report of four cases of vesical. J Int Coll Surg 1960;34: Vercellini P, Meschia M, De Giorgi O, Panazza S, Cortesi I, Crosignani PG. Bladder detrusor : clinical and pathogenetic implications. J Urol 1996;155: Yohannes P. Ureteral. J Urol 2003;170: American Society for Reproductive Medicine. Revised American Society for Reproductive Medicine classification of : Fertil Steril 1997;67: Stanley KE, Utz DC, Dockerty MB. Clinically significant of the urinary tract. Surg Gynecol Obstet 1965;120: Nezhat C, Nezhat F, Nezhat CH, Nasserbakht F, Rosati M, Seidman DS. Urinary tract treated by laparoscopy. Fertil Steril 1996;66: Villa G, Mabrouk M, Guerrini M, Mignemi G, Montanari G, Fabbri E, et al. Relationship of site and size of endometriotic bladder nodules and severity of dysuria. J Minim Invasive Gynecol 2007;14: Fauconnier A, Chapron C, Dubuisson JB, Vieira M, Dousset B, Breart G. Relation between pain symptoms and the anatomic location of deep infiltrating. Fertil Steril 2002;78: Stillwell TJ, Kramer SA, Lee RA. Endometriosis of ureter. Urology 1986;28: Chapron C, Fauconnier A, Dubuisson JB, Barakat H, Vieira M, Breart G. Deep infiltrating : relation between severity of dysmenorrhoea and extent of disease. Hum Reprod 2003;18: Arruda MS, Petta CA, Abrao MS, Benetti-Pinto CL. Time elapsed from onset of symptoms to diagnosis of in a cohort study of Brazilian women. Hum Reprod 2003;18: Somigliana E, Vercellini P, Gattei U, Chopin N, Chiodo I, Chapron C. Bladder : getting closer and closer to the unifying metastatic hypothesis. Fertil Steril 2007;87: Donnez J, Nisolle M, Squifflet J. Ureteral : a complication of rectovaginal endometriotic (adenomyotic) nodules. Fertil Steril 2002;77: Chapron C, Chopin N, Borghese B, Foulot H, Dousset B, Vacher- Lavenu MC, et al. A. Deeply infiltrating : pathogenetic implications of the anatomical distribution. Hum Reprod 2006;21: Fertility and Sterility â 1667

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