{"paper_id":"03e102e3-4a09-4003-8571-541f9939094a","body_text":"Ascites and Encapsulating Peritonitis in Endometriosis:\na Systematic Review with a Case Report\nEndometriose com ascite e pe ritonite encapsulante: uma\nrevisão sistemática com descrição de um caso clínico\nThais Fontes de Magalhães 1 Kathiane Lustosa Augusto 1,2 Livia Ponte Mota 3 Arthur Ribeiro da Costa 3\nRainardo Antonio Puster 3 Leonardo Robson Pinheiro Sobreira Bezerra 1\n1 Department of Gynecology, Universidade Federal do Ceará,\nFortaleza, CE, Brazil\n2 Department of Gynecology, Universidade de Fortaleza, Fortaleza,\nCE, Brazil\n3 Department of Internal Medicine, Universidade Federal do Ceará,\nFortaleza, Brazil\nRev Bras Ginecol Obstet 2018;40:147 –155.\nAddress for correspondence Thais Fontes de Magalhães, MD,\nDepartmento de Ginecologia, Universidade Federal do Ceara,\nRua Alexandre Barauna 949, Fortaleza, CE, 60430-160, Brazil\n(e-mail: thaisfdemagalhaes@gmail.com).\nKeywords\n► endometriosis\n► ascites\n► peritonitis\n► systematic review\n► treatment\nAbstract Endometriosis can have several different presentations, including overt ascites and\nperitonitis; increased awareness can improve diagnostic accuracy and patient outcomes.\nWe aim to provide a systematic review and report a case of endometriosis with this unusual\nclinical presentation. The PubMed/MEDLINE database was systematically reviewed until\nOctober 2016. Women with histologically-proven endometriosis presenting with clinically\nsignificant ascites and/or frozen abdomen and/or encapsulating peritonitis were included;\nthose with potentially confounding conditions were excluded. Our search yielded 37 articles\ndescribing 42 women, all of reproductive age. Ascites was mostly hemorrhagic, recurrent\nand not predicted by cancer antigen 125 (CA-125) levels. In turn, dysmenorrhea, dyspar-\neunia and infertility were not consistently reported. The treatment choices and outcomes\nwere different across the studies, and are described in detail. Endometriosis should be a\ndifferential diagnosis of massive hemorrhagic ascites in women of reproductive age.\nPalavras-chave\n► endometriose\n► ascite\n► peritonite\n► revisão sistemática\n► tratamento\nResumo A endometriose pode ter várias apresentações, incluindo ascite e peritonite, que são\napresentações incomuns. O aumento da conscientização sobre essa doença pode melhorar\na precisão diagnóstica e os resultados das pacientes. Nosso objetivo é fornecer uma revisão\nsistemática e relatar um caso de endometriose com esta apresentação clínica incomum. O\nbanco de dados PubMed/MEDLINE foi revisado sistematicamente até outubro de 2016.\nForam incluídas mulheres com endometriose demonstrada histologicamente, com presença\nde ascite clinicamente significativa e/ou abdômen congelado e/ou peritonite encapsulante;\nforam excluídas aquelas com comorbidades que pudessem provocar confusão. A pesquisa\nselecionou 37 artigos que descrevem 42 mulheres, todas em idade reprodutiva. A ascite foi\nprincipalmente hemorrágica, recorrente, e não indicada pelos níveis de antígeno associado\nao câncer 125 (AC -125). Por sua vez, a dismenorreia, a dispareunia e a infertilidade não foram\nrelatadas de forma consistente. As escolhas e os resultados do tratamento foram diferentes\nentre os estudos, e são descritos em detalhes. A endometriose deveria ser um diagnóstico\ndiferencial de ascite hemorrágica maciça em mulheres em idade reprodutiva.\nreceived\nSeptember 12, 2017\naccepted\nDecember 20, 2017\npublished online\nMarch 19, 2018\nDOI https://doi.org/\n10.1055/s-0038-1626700.\nISSN 0100-7203.\nCopyright © 2018 by Thieme Revinter\nPublicações Ltda, Rio de Janeiro, Brazil\nTHIEME\nReview Article 147\n\n\nIntroduction\nEndometriosis is de fined as the presence of endometrial\ntissue outside of the uterine cavity, which, like the eutopic\nendometrium, responds to hormonal stimuli. 1 Although the\nsymptoms related to endometriosis may be associated with\nthe location of the implant, they are unrelated to the extent of\nthe disease, and a variety of clinical presentations have been\ndescribed, including the presence of a small amount of\nperitoneal fluid.\n2 It is very rare, however, for endometriosis\nto present as overt ascites, and the presence of such a\ncondition should prompt the investigation of differential\ndiagnoses, such as malignancy.\n3 The occurrence of encapsu-\nlating peritonitis, described as the encapsulation of bowel\nloops by a thick fibrinogenous case, is even rarer, with only\nfive cases previously described in the medical literature.\n3–8\nWomen who present with ascites due to endometriosis\noften undergo multiple diagnostic procedures, including\ninvasive ones, before the underlying cause for ascites is\nfound.9 This results in increased patient risks and health\ncare costs. 10 General and emergency physicians, as well as\ngynecologists, should be aware of endometriosis as a poten-\ntial cause of ascites and encapsulating peritonitis to prompt-\nly diagnose it.\nWith this in mind, this study aims to bring attention to the\ncase of a woman presenting with encapsulating peritonitis\nand multiple episodes of massive ascites. We also provide a\nsystematic review of the literature regarding the association\nbetween histologically-proven endometriosis and clinically-\nsignificant ascites, frozen abdomen or encapsulating perito-\nnitis, including detailed characteristics of their presenta-\ntions, proposed treatments and outcomes.\nMethods\nFor this systematic review, we used the protocol outlined by\nthe Preferred Reporting Items for Systematic Reviews and\nMeta-analyses (PRISMA) Statement (\n►Fig. 1 ). The electronic\nPubMed database was searched until October 2016 using the\ndetailed strategy described in ►Table 1 . The case of a woman\nwith endometriosis, recurrent ascites and encapsulating\nperitonitis observed at our clinic is also described. The\nreview has been approved by the Ethics in Research Com-\nmittee under the protocol number 006.01.2017.\nEligibility Criteria\nOriginal articles, clinical trials, case series and case reports of\nwomen of any age with histologically-proven endometriosis,\npresenting with clinically signi ficant ascites and/or frozen\nabdomen and/or encapsulating peritonitis, published in\nEnglish, Portuguese, French or Spanish, were eligible for\nthis review.\nBecause other causes that may occur concurrently with\nendometriosis can cause the clinical presentations de-\nscribed, we excluded papers describing patients with: cancer\nof the ovaries, appendix or peritoneum, or other intra-\nabdominal cancers; tuberculosis; ovarian hyperstimulation\nsyndrome; ovarian induction or other known causes of\nmassive ascites; and ascites beginning in the immediate or\nearly post-operative period of exploratory laparotomy/lapa-\nroscopy. Animal studies; articles published in languages\nother than the aforementioned ones; and reviews of the\nliterature were also excluded.\nStudy Selection\nThe references retrieved were independently screened by two\ninvestigators, KA and TM. Initially, the screening was made by\ntitle and abstract; then, the full-text versions of the selected\npapers were obtained, and each article was reviewed for final\ninclusion. If a consensus could not be reached, another author\n(LB) made the final decision regarding inclusion.\nData Extraction\nA standardized table was used for data extraction on each\nselected paper, and information regarding the first author,\nthe country of origin, the journal and year of publication, the\nstudy type, patient/sample age, patient origin or ethnicity,\nthe clinical presentation, the proposed treatment, and the\noutcome were included. The characteristics of the ascitic\nfluid and data regarding the presence or absence of encap-\nsulating peritonitis were also recorded. Data extraction was\nperformed independently by two investigators (KA and TM).\nCase Description\nA 28-year-old woman presented to the internal medicine\nclinic at our institution with wasting syndrome, increased\nabdominal girth, progressive shortness of breath, dark stools\nand decreased appetite. She also complained of progressive\nabdominal and thoracic pain during menses, as well as cyclic\ndyspareunia that had started five years before. She denied\ninfertility or any other chronic medical conditions. Her\ncancer antigen 125 (CA-125) values were 107.8 and 889.6\non two measurements performed when she was an internal\nmedicine inpatient.\nAbdominal ultrasound and contrasted computed tomog-\nraphy (CT) studies showed loculated, cystic -like ascites pro-\nducing a mass effect. A paracentesis procedure revealed a\nthick, hemorrhagic fluid with low albumin, high cellularity\nand large concentration of red blood cells (\n►Fig. 2 ). The fluid\nanalysis was negative for bacterial growth or cancer cells.\nDuring the diagnostic laparoscopy, multiple adhesions and\nperitoneal lesions were noticed, and the patient ’sa b d o m e n\nwas described as “frozen,” due to the presence of encapsu-\nlating peritonitis, which did not enable the separation of the\nperitoneal layers and the confection of the pneumoperito-\nneum. Eight liters of fluid were removed. Histopathology of a\nperitoneal biopsy taken at this time described chronic peri-\ntonitis and scarce hemosiderin deposits.\nOne month after the initial imaging exam, another con-\ntrasted abdominal CT suggested the presence of sclerosing\nencapsulating peritonitis (\n►Fig. 3 ). At this point, the patient\nwas referred to our gynecology clinic due to suspected\nendometriosis. This diagnosis was further suggested by a\ngynecological exam, ultrasound mapping and a magnetic\nresonance imaging (MRI) scan, which showed evidence of\nfibrosis in the anterior vaginal fornix, multiple peritoneal\nRev Bras Ginecol Obstet Vol. 40 No. 3/2018\nAscites and Encapsulating Peritonitis in Endometriosis Magalhães et al.148\n\n\nnodules, and apparently hemorrhagic bilateral ovarian cysts.\nThe chest CT and the colonoscopy at that time were normal.\nA new laparoscopy was performed, and a biopsy con-\nfirmed the diagnosis of endometriosis. Due to peritoneal\nadhesions, it was not possible to access the pelvic and\nabdominal organs. This patient was treated with goserelin\nacetate, with good clinical response. At the six-month follow-\nup, she was asymptomatic and had regained a considerable\namount of weight.\nResults\nStudy Characteristics\nOur systematic review yielded 37 articles describing 42\npatients with clinically signi ficant ascites, encapsulating\nperitonitis, or frozen abdomen. One author had a series of\nthree cases, while another had a series of four cases; all of the\nremaining articles reported only one case each.\n11,12 The\npublication dates ranged from 1978 to 2016.\nPatient Characteristics and Clinical Presentation\nThe ages of the women who ful filled the eligibility criteria\nranged from 20 years to 47 years. 13,14\nA total of 8 women in the included articles were\ndescribed as “black”;3 ,a s “African-American ”;a n d2 ,a s\n“Afro-Caribbean. ”12,13,15–22 One patient described herself as\n“African;” another patient, as “caucasian;” a third one, as\n“Hispanic;” and another one, as “negro.”23–26 Seven studies\ndid not describe ethnicity, but reported that the patients\nwere Nigerian ( n ¼ 3), Malay ( n ¼ 2), Brazilian ( n ¼ 1) or\nJapanese ( n ¼ 1).\n3,6,8,27–30 Ethnicity or origin was not de-\nscribed at all for the remaining 16 patients. 5,7,11,14,31 –42\nRecords identified through a database \nsearch\n(n = 234)\nScreeningIncluded Eligibility Identification\nAdditional records identified through \nother sources\n(n = 2)\nRecords after duplicates were removed\n(n = 233)\nRecords screened\n(n = 233)\nRecords excluded\n(n = 163)\nFull-text articles assessed for \neligibility\n(n=70)\nFull-text articles excluded, with \nreasons (n = 33):\n- Full-texts unavailable online (21)\n- No histologically-proven \nendometriosis (3)\n- Ascites not clinically significant \n(3)\n- Post-operative ascites (2)\n- Post-chemotherapy ascites (1)\n- Post ovarian stimulation ascites \n(1)\n- Post-trauma ascites (1)\n- Presence of abdominopelvic \nabscess (1)\nStudies included in the \nqualitative synthesis\n(n = 37)\nFig. 1 Flow diagram describing the steps in the study sel ection for inclusion in this systematic review.\nTable 1 Detailed search strategy used in the advanced tool of\nthe PubMed/MEDLINE database\nSearch Keywords\n#1 peritoneal fibrosis OR encapsulating\nperitoneal sclerosis OR sclerosing\nencapsulating peritonitis\nOR abdominal cocoon OR frozen\nabdomen OR ascites\n#2 endometriosis OR endometrioma OR\nendometriotic OR hemosiderophage\nFinal search #1 AND #2\nRev Bras Ginecol Obstet Vol. 40 No. 3/2018\nAscites and Encapsulating Peritonitis in Endometriosis Magalhães et al. 149\n\n\nThe ascites was of acute onset in 8 women, and gradual in\n24 patients ( ►Supplementary Material 1) . The type of onset\nwas not reported in six cases.\nIn most patients, the ascites was described as “hemor-\nrhagic” and “recurrent,” but descriptions such as “yellow,”\n“clear yellow, ”“ brownish green ” and “loculated” were also\nobserved.3,6,8,13,25,32,33 Ascites was present but not charac -\nterized in five cases. 5,14,15,19,34\nThe volume of asciticfluid was not shown in some studies, but\nthere are reports of 4.2 L, 4.8 L, 5.0 L and 7 L.13,29,36,41There was\nassociated pleural effusion in eleven patients.3,12,18,19,21,23,32,33,40\nLiver involvement by endometriosis was cited in four cases,\nincluding one with cysts and another with non-specified focal\nlesions.\n3,34\nTwenty-two articles reported CA-125 levels. Normal\nlevels were observed in six patients. The biomarker was\nelevated (> 35 U/mL) in 14 patients, ranging from 49 U/mL\nto > 5,000 U/mL. One case had normal CA-125 levels at\nfirst, but they became elevated (455 U/mL) after ascites\nrecurrence.\n12\nThe most common main clinical presentation was abdo-\nminal distension, which was sometimes accompanied by\nother symptoms such as abdominal pain, abdominal tender-\nness, abdominal mass, shortness of breath, signs of hypovole-\nmia, weight loss, nausea or vomiting, asthenia, malaise,\ncachexia or loss of appetite. In 25 of the 42 women described,\nat least one symptom of the classic dysmenorrhea, dyspareunia\nand infertility triad was reported. Of these, dysmenorrhea\nwas the most common, and it was reported in 20\nwomen.\n8,11–13,15,16,18,20,22–24,27,30–32,36,38–41 Infertility was\nreported in 11 patients. 11,18,19,22–24,29–31,40,41 Dyspareunia\nwas reported in 4 patients. 15,22,24,36 All three symptoms\nwere present in two studies. 22,24 However, in 15 articles\n(describing 17 patients), the presence or absence of dysmenor-\nrhea was not mentioned at all.\n5–7,12,14,19,21,25,26,28,29,33–35,37 A\ntotal of 33 studies (with 38 patients) were regarding the\npresence or absence of dyspareunia,3,5–8,11–14,16–21,25–35,37–42\nand 25 studies (with 28 patients) were regarding the presence\nor absence of infertility.3,5–8,11–17,21,25–28,32–39 Fifteen articles\ndid not mention if any of these three symptoms were present or\nabsent in the cases they reported.\n5–7,12,14,21,25,26,28,33–35,37\nBesides our patient, only five cases of encapsulating\nperitonitis due to endometriosis have been described in\nthe medical literature.\n3,5–8\nTreatments Used and Outcomes\nThe treatment choices for the patients included in this\nreview involved hormonal therapies, surgery, anti-in flam-\nmatory drugs (steroidal or non-steroidal) or a combination of\nFig. 2 Thick, hemorrhagic ascitic fluid sample.\nFig. 3 Contrasted computed tomography (CT) showing massive ascites, centrally encased bowels, and thickened peritoneum.\nRev Bras Ginecol Obstet Vol. 40 No. 3/2018\nAscites and Encapsulating Peritonitis in Endometriosis Magalhães et al.150\n\n\nTable 2 Treatment choices and respective outcomes in each study. Outcomes written as described in each article\nTreatment for ascites Outcome\nDun et al, 2016 29 Leuprolide þ oral norethindrone Ascites persisted\nLaparoscopic evacuation of ascites and\nexcision of endometriosis\nNo recurrence (6-month follow-up)\nHasdemir et al, 2015 40 Leuprorelin acetate for 6 months Resolution of symptoms until 2 months\nafter cessation\nDienogest Resolution of symptoms (3-month follow-\nup)\nHinduja et al, 2016 42 Leuprolide 3.75 mg monthly Recurrence after 6 months\nTAH þ BSO Ascitic fluid leakage through vaginal suture\nl i n e( 1 0d a y sa f t e rt h eo p e r a t i o n )\nShort-acting GnRH agonist þ oral danazol\nfollowed by GnRH only\nNo recurrence (1-year follow-up)\nSetubal et al, 2015 24 Continuous OCP for 3 months Ascites persisted\nGnRH agonist, then laparoscopic excision\nof lesions followed by GnRH agonist\nMinimal ascites\nUnderwent IVF protocol Minimal ascites\nOCP Symptom-free\nAppleby et al, 2014 28 GnRH antagonist No recurrence (6-month follow-up)\nAsano et al, 2014 30 GnRH agonist Ascites recurred\nOral dienogest No recurrence (1-year follow-up)\nBignall et al, 2014\n22 GnRH agonists Ascites recurred\nGnRH agonists þ tibolone þ NSAIDs þ\npregabalin\nSymptoms well-controlled\nCosma et al, 2014 41 Laparoscopic excision of lesions Modest recurrence (250 mL) after 42 days\nShabeerali et al, 2012 11 CASE 1: GnRH analogue No recurrence (6-month follow-up)\nCASE 2: Subtotal abdominal\nhysterectomy þ BSO\nNo recurrence (1-year follow-up)\nCASE 3: GnRH analogues for 1 year; then,\nTAH þ BSO\nPartial response; then, relatively asympto-\nmatic at 1-year follow-up\nFerrero and Remorgida, 2011\n36 Norethindrone acetate (25 mg daily) No recurrence (1-year follow-up)\nIgnacio et al, 2010 18 GnRH analogue No recurrence (8-month follow-up)\nLin et al, 2010 37 Laparoscopic electrocauterization of\nlesions\nCondition stabilized\nSuchetha et al, 2010 7 GnRH analogues for 1 year Good response\nPark et al, 2009 39 Laparoscopic excision of endometrioma\nþ GnRH agonist for 6 months þ tibolone\nNo recurrence (1-year follow-up)\nSait, 2008 38 Bilateral ovarian cystectomies þ GnRH\nanalogue for 6 months followed by OCP\nNo recurrence (2-year follow-up)\nSantos et al, 2007 6 Laparoscopy þ laparotomy NR. Patient died after 5 months\nPalayekar et al, 2007 20 TAH þ BSO No recurrence (1-year follow-up)\nFortier et al, 2005 23 Ovarian cystectomy þ GnRH analogue for\n6m o n t h sþ laparoscopic excision of\nlesions þ oral progesterone for 6 months\nTwo recurrences\nCeased treatment and started clomiphene\ndue to pregnancy desire\nAscites recurrence\nGnRH for 2 months Ascites recurrence\nGnRH for 6 months Ascites recurrence\nMohd Noor et al, 2004 8 Laparotomy þ excision of lesions No recurrence (4-week follow-up)\nZeppa et al, 2004 35 NR NR\n(Continued )\nRev Bras Ginecol Obstet Vol. 40 No. 3/2018\nAscites and Encapsulating Peritonitis in Endometriosis Magalhães et al. 151\n\n\nthem. Ascites recurrence or persistence was frequent. Three\narticles did not report how the patients were managed\n(►Table 2 ).3,14,35\nThe hormonal therapies used included long-acting go-\nnadotropin-releasing hormone (GnRH) agonists (namely\ngoserelin and leuprolide), short-acting GnRH agonists,\nGnRH antagonists, progestational hormones (speci fically\ndienogest, medroxyprogesterone and norethindrone), estra-\ndiol, conjugated estrogens, synthetic combined hormones\n(namely tibolone), steroids with antigonadotropic and anti-\nestrogenic activity (danazol), and oral contraceptive pills\n(OCPs).\nOther conservative treatments used were isolated pred-\nnisolone, which did not prevent ascites recurrence, and\nTable 2 (Continued )\nTreatment for ascites Outcome\nCheong and Lim, 2003 3 NR NR\nJeanes et al, 2002 34 Double hysterectomy þ left oophorect-\nomy followed by estradiol for 6 months\nfollowed by goserelin\nNo recurrence (3-year follow-up)\nMoffatt and Mitchell, 2002 19 Leuprolide þ premarin Recurrence after 4 weeks\nTAH þ BSO þ leuprolide No recurrence (9-month follow-up)\nBhojawala et al, 2000 17 TAH þ RSO No recurrence (6-week follow-up)\nSamora-Mata and Feste, 1999 25 TAH þ RSO NR\nMyneyyirci-Delale et al, 1998 12 Laparoscopic excision of lesions followed\nby GnRH agonist for 6 months; then,\nexcision of new ovarian cyst þ danazol\ndaily for 6 months followed by norethin-\ndrone acetate\nRecurrence after 1 year; then, no recur-\nrence (3-year follow-up)\nLaparotomy þ monthly depo provera\ninjections; then, TAH þ BSO\nRecurrence after 3 years; then, no recur-\nrence (6-month follow-up)\nAppendectomy and left ovarian wedge\nresection þ lupron\nNo recurrence\nL y s i so fa d h e s i o n sþ LSO followed by\nlupron followed by norethindrone acetate\nNR\nFrigerio et al, 1997\n5 TAH þ BSO þ appendectomy þ omen-\ntectomy\nNo recurrence (3-year follow-up)\nMejia et al, 1997 16 Laparotomy No recurrence (15-month follow-up)\nFlanagan and Barnes, 1996 21 Laparotomy þ GnRH agonist for 6 months Recurrence (twice in 1 year)\nPrednisolone 30 mg daily Recurrence\nLeuprorelin for 5 months Recurrence\nMyers et al, 1995\n33 TAH þ BSO þ lysis of adhesions No recurrence (8-month follow-up)\nJose et al, 1994 32 LSO Recurrence after 1 year\nLaparotomy þ danazol NR\nSchlueter an McClennan, 1994\n13 Leuprolide acetate monthly No recurrence (3-month follow-up)\nWilliams and Wagaman, 1991 15 Medroxyprogesterone acetate Recurrence after 1 month\nDepot lupron for 3 months Some ascites\nTAH þ BSO Recurrence after 3 months\nTenckhoff catheter placed for 2 weeks No recurrence (9-month follow-up)\nChichareon and Wattanakitkrailert,\n1988\n31\nTAH þ BSO No recurrence (6-month follow-up)\nOlubuyide et al, 1988 27 Oral norethisterone No recurrence (1-year follow-up)\nNaraynsingh et al, 1985 26 Depo provera for 6 months No recurrence (4-year follow-up)\nCantor et al, 1979 14 NR NR\nAbbreviations: BSO, bilateral salpingo-oophorectomy; GnRH, gonadotrop in-releasing hormone; IVF, in vitro fertilization; LSO, left salpingo-\noophorectomy; NR, not reported; NSAIDs, non-steroidal anti-in flammatory drugs; OCP, oral contraceptive pills; RSO, right salpingo-oophorectomy;\nTAH, total abdominal hysterectomy.\nRev Bras Ginecol Obstet Vol. 40 No. 3/2018\nAscites and Encapsulating Peritonitis in Endometriosis Magalhães et al.152\n\n\nnonsteroidal anti-in flammatory drugs (NSAIDs) in combina-\ntion with pregabalin and hormonal therapies, which were\neffective in controlling the symptoms.\nThe surgical procedures involved drainage of the ascites,\nexcision or electrocauterization of the endometriotic lesions\nthrough laparotomy or laparoscopy, lysis of adhesions, abdom-\ninal hysterectomy, uni- or bilateral salpingo-oophorectomy,\novarian cystectomy, omentectomy, appendectomy, placement\nof Tenckhoff catheter and/or ovarian wedge resection.\nAfter the initial treatment, due to the desire to achieve\npregnancy, one woman underwent in vitro fertilization (IVF),\nwith minimal ascites afterwards.\n24 Another patient started\nclomiphene, with ascites recurrence. 23\nA summary of the treatments used for ascites and its\nrespective outcomes, including the time until recurrence, is\nshown in ►Table 2 .\nDiscussion\nAll patients shown in this review were of childbearing age,\nlikely due to hormonal levels and occurrence of menses. This\nis, indeed, the most common age range for the presentation\nof endometriosis in general, which can also rarely occur in\nolder women.\n43 Endometriosis most commonly affected\nwomen of African descent, but it was present in patients\nof multiple other ethnicities, implying that this diagnosis\nshould not be restricted to patient origin, and must be\nsuspected if the clinical presentation is suitable.\nFluid accumulation was most commonly progressive, but\nacute onset of symptoms has also been described. The\nreasons for such a presentation remain unclear, but can be\nrelated to the rapid accumulation of fluid and to the sponta-\nneous rupture of a cyst.\n37\nEndometriosis-associated ascites is rare, and encapsulat-\ning peritonitis is even less common. Since we excluded\nwomen with potentially confounding conditions, it appears\nthat endometriosis itself is the cause of such clinical pre-\nsentations. It has been hypothesized that the peritoneal\nirritation caused by endometriosis results in extensive fibro-\nsis and in flammation, further optimizing the microenviron-\nment for more secondary implants, which in turn exacerbate\ninflammation. In fact, this theory could also explain the high\nrate of recurrence of ascites due to endometriosis (\n►Table 2 ),\nultimately resulting in encapsulating peritonitis, which is\ndescribed in our case and in four other ones.\nAbdominal distension related to ascites was the most\ncommon clinical sign, but non-speci fic signs and symptoms\nsuch as malaise and weight loss were also described\n(►Supplementary Material 1 ). Additionally, most women\nhad symptoms suggestive of endometriosis, but these were\nnot always reported, bringing attention to the high level of\nsuspicion needed to diagnose this condition. Not all women\npresent with classic symptoms; however, in order for diag-\nnostic accuracy to be improved, physicians in general (in-\ncluding emergency room physicians) need to ask about them\nspecifically during history-taking.\nMoreover, in some cases, ascitic volume was large and\nrelated to pleural effusion, resembling Meigs syndrome.\nGreat volumes can be caused by the rapid production of\nfluid, in association with the obstruction of subdiaphrag-\nmatic lymph vessels. In turn, pleural fluid may be due to the\ntransdiaphragmatic flow of ascites through the lymphatic\nchannels, as has been proposed by Meigs et al,\n44 or due to\nlocal reactive in flammation.38\nThe fluid was generally hemorrhagic, but could have\ndifferent aspects, such as clear yellow or green-brownish\ncolor. On this matter, Bernstein proposed a mechanism by\nwhich chocolate cysts would rupture into the peritoneal\ncavity, leading to irritation and ascites formation; corre-\nspondingly, other explanations relate to excessive ovarian\ntransudation, super ficial endometriosis, open endometriosis\nlesions or angiogenesis.\n45–47\nPart of the included studies also measured and reported\nserum CA-125 levels. This biomarker is known to not be\naccurate for the diagnosis of endometriosis in general;\nlikewise, it was not reliable in the diagnosis of endometriosis\npresenting with ascites. Although no statistical comparisons\nwere made, it is clear that the values were not intimately\ncorrelated to the characteristics of ascites. Furthermore,\nendometriosis caused CA-125 levels > 5,000 U/mL in one\ncase, which commonly indicates malignancy; this further\ncontributes to the need of including endometriosis in the list\nof differentials of suspected malignancies due to massive\nascites.\nSeveral treatment choices were observed in the included\narticles; the options were similar to the therapies available\nfor endometriosis in general. For the speci fic treatment of\nwomen presenting with ascites, no speci fic protocol exists,\nand empirical data does not evidently favor one therapy over\nanother (\n►Table 2 ).\nAmong the strengths of our review are the fact that only\narticles with histologically proven endometriosis were se-\nlected; the exclusion of patients with conditions that com-\nmonly cause ascites; and the systematic approach. It is\nlimited, however, in that articles in only four languages\nwere included, and in the fact that some older articles\ninitially screened could not be included because they were\nnot available online, even for purchase. Further research is\nneeded to better de fine optimal diagnostic and therapeutic\napproaches in women with unusual presentations of\nendometriosis.\nConclusion\nClinically signi ficant ascites, frozen abdomen and/or encap-\nsulating peritonitis related to endometriosis are rare con-\nditions. It can present with abdominal distension, symptoms\nclassically related to endometriosis, and other non-speci fic\nsymptoms. The clinical presentations were heterogeneous.\nEndometriosis should be a differential diagnosis of massive\nhemorrhagic ascites in women of reproductive age, but the\nexclusion of other potential causes, especially malignancy, is\nneeded for the diagnosis of this condition. The treatment\noptions include hormonal therapy, anti-in flammatory drugs\nand/or surgery. There are no speci fic protocols for the\ntreatment of this condition.\nRev Bras Ginecol Obstet Vol. 40 No. 3/2018\nAscites and Encapsulating Peritonitis in Endometriosis Magalhães et al. 153\n\n\nContributors\nMagalhaes TF, Augusto KL, Mota LP, Costa AR, Puster RA,\nand Bezerra LRPS contributed with the project and inter-\npretation of data, writing of the article, critical review of\nthe intellectual content and final approval of the version\nto be published.\nConflicts of Interest\nThe authors have no con flicts of interest to declare.\nReferences\n1 Chen P, Wang DB, Liang YM. Evaluation of estrogen in endome-\ntriosis patients: Regulation of GATA-3 in endometrial cells and\neffects on Th2 cytokines. J Obstet Gynaecol Res 2016;42(06):\n669–677. Doi: 10.1111/jog.12957\n2 Vinci G, Arkwright S, Audebourg A, et al. Correlation between the\nclinical parameters and tissue phenotype in patients affected by\ndeep-infiltrating endometriosis. Reprod Sci 2016;23(09):1258-\n–1268. Doi: 10.1177/1933719116638188\n3 Cheong EC, Lim DT. Massive ascites –an uncommon presentation\nof endometriosis. Singapore Med J 2003;44(02):98 –100\n4 Obaid O, Alhalabi D, Ghonami M. Intestinal obstruction in a\npatient with sclerosing encapsulating peritonitis. Case Rep Surg\n2017;2017:8316147\n5 Frigerio L, Taccagni GL, Mariani A, Mangili G, Ferrari A. Idiopathic\nsclerosing peritonitis associated with florid mesothelial hyper-\nplasia, ovarian fibromatosis, and endometriosis: a new disorder of\nabdominal mass. Am J Obstet Gynecol 1997;176(03):721 –722.\nDoi: 10.1016/S0002-9378(97)70581-7\n6 Santos VM, Barbosa ER Jr, Lima SH, Porto AS. Abdominal cocoon\nassociated with endometriosis. Singapore Med J 2007;48(09):\ne240–e242\n7 Suchetha S, Rema P, Mathew AP, Sebastian P. Endometriosis with\nmassive hemorrhagic ascites. Indian J Cancer 2010;47(02):\n224–225. Doi: 10.4103/0019-509X.63004\n8 Mohd Noor NH, Zaki NM, Kaur G, Naik VR, Zakaria AZ. Abdominal\ncocoon in association with adenomyosis and leiomyomata of the\nuterus and endometriotic cyst : unusual presentation. Malays J\nMed Sci 2004;11(01):81 –85\n9 Gupta D, Hull ML, Fraser I, et al. Endometrial biomarkers for the\nnon-invasive diagnosis of endometriosis. Cochrane Database\nSyst Rev 2016;4:CD012165. Doi: 10.1002/14651858.CD012165\n10 Liu E, Nisenblat V, Farquhar C, et al. Urinary biomarkers for the\nnon-invasive diagnosis of endometriosis. Cochrane Database Syst\nRev 2015;(12):CD012019. Doi: 10.1002/14651858.CD012019\n11 Shabeerali TU, Rajan R, Kuruvilla AP, et al. Hemorrhagic ascites:\nare we missing endometriosis? Indian J Gastroenterol 2012;31\n(04):195–197. Doi: 10.1007/s12664-012-0221-1\n12 Muneyyirci-Delale O, Neil G, Serur E, Gordon D, Maiman M, Sedlis\nA. Endometriosis with massive ascites. Gynecol Oncol 1998;69\n(01):42–46. Doi: 10.1006/gyno.1998.4953\n13 Schlueter FJ, McClennan BL. Massive ascites and pleural effusions\nassociated with endometriosis. Abdom Imaging 1994;19(05):\n475–476\n14 Cantor JO, Fenoglio CM, Richart RM. A case of extensive abdominal\nendometriosis. Am J Obstet Gynecol 1979;134(07):846 –847. Doi:\n10.1016/0002-9378(79)90958-X\n15 Williams RS, Wagaman R. Endometriosis associated with massive\nascites and absence of pelvic peritoneum. Am J Obstet Gynecol\n1991;164(1 Pt 1):45 –46. Doi: 10.1016/0002-9378(91)90621-W\n16 Mejia EM, Alvarez OA, Lee M. Endometriosis with massive bloody\nascites. J Am Board Fam Pract 1997;10(01):59 –61\n17 Bhojawala J, Heller DS, Cracchiolo B, Sama J. Endometriosis\npresenting as bloody pleural effusion and ascites-report of a\ncase and review of the literature. Arch Gynecol Obstet 2000;\n264(01):39–41. Doi: 10.1007/PL00007484\n18 Ignacio MM, Joseph N, Hélder F, Mamourou K, Arnaud W. Massive\nascites, pleural effusion, and diaphragmatic implants in a patient\nwith endometriosis. Eur J Obstet Gynecol Reprod Biol 2010;149\n(01):117–118. Doi: 10.1016/j.ejogrb.2009.10.017\n19 Moffatt SD, Mitchell JD. Massive pleural endometriosis. Eur J\nCardiothorac Surg 2002;22(02):321 –323. Doi: 10.1016/S1010-\n7940(02)00277-4\n20 Palayekar M, Jenci J, Carlson JA Jr. Recurrent hemorrhagic ascites:\na rare presentation of endometriosis. Obstet Gynecol 2007;110(2\nPt 2):521 –522\n21 Flanagan KL, Barnes NC. Pleural fluid accumulation due to intra-\nabdominal endometriosis: a case report and review of the litera-\nture. Thorax 1996;51(10):1062–1063. Doi: 10.1136/thx.51.10.1062\n22 Bignall J, Arambage K, Vimplis S. Endometriosis: a rare and\ninteresting cause of recurrent haemorrhagic ascites. BMJ Case\nRep 2014;2014:bcr2013010052. Doi: 10.1136/bcr-2013-010052\n23 F o r t i e rD ,D e d e c k e rF ,G a b r i e l eM ,G r a e s s l i nO ,B a r a uG .[ E n d o m e t r i o s i s\nwith ascites and pleural effusion: a case report]. Gynecol Obstet Fertil\n2005;33(7-8):508–510. Doi: 10.1016/j.gyobfe.2005.05.014\n24 Setubal A, Sidiropoulou Z, Soares S, Barbosa C. Endometriosis and\nascites: a strategy to achieve pregnancy. J Minim Invasive Gynecol\n2015;22(06):1104–1108. Doi: 10.1016/j.jmig.2015.05.013\n25 Samora-Mata J, Feste JR. Endometriosis ascites: a case report. JSLS\n1999;3(03):229–231\n26 Naraynsingh V, Raju GC, Ratan P, Wong J. Massive ascites due to\nomental endometriosis. Postgrad Med J 1985;61(716):539 –540.\nDoi: 10.1136/pgmj.61.716.53\n27 Olubuyide IO, Adebajo AO, Adeleye JA, Solanke TF. Massive ascites\nassociated with endometriosis in a Nigerian African. Int J Gynae-\ncol Obstet 1988;27(03):439 –441. Doi: 10.1016/0020-7292(88)\n90127-0\n28 Appleby R, Saroya H, Postgate A, Meer Z. A young woman with\nabdominal distension. BMJ Case Rep 2014;2014:bcr2014203726.\nDoi: 10.1136/bcr-2014-203726\n29 Dun EC, Wong S, Lakhi NA, Nehzat CH. Recurrent massive ascites\ndue to mossy endometriosis. Fertil Steril 2016;106(06):e14. Doi:\n10.1016/j.fertnstert.2016.07.1119\n30 Asano R, Nakazawa T, Hirahara F, Sakakibara H. Dienogest was\neffective in treating hemorrhagic ascites caused by endometrio-\nsis: a case report. J Minim Invasive Gynecol 2014;21(06):1110-\n–1112. Doi: 10.1016/j.jmig.2014.04.014\n31 Chichareon SB, Wattan akitkrailert S. Endometriosis with asci tes.\nActa Obstet Gynecol Scand 1988;67(02):187 –188. Doi: 10.3109/\n00016348809004198\n32 Jose R, George SS, Seshadri L. Massive ascites associated with\nendometriosis. Int J Gynaecol Obstet 1994;44(03):287 –288. Doi:\n10.1016/0020-7292(94)90185-6\n33 Myers TJ, Arena B, Granai CO. Pelvic endometriosis mimicking\nadvanced ovarian cancer: presentation with pleural effusion,\nascites, and elevated serum CA 125 level. Am J Obstet Gynecol\n1995;173(3 Pt 1):966 –967\n34 Jeanes AC, Murray D, Davidson B, Hamilton M, Watkinson AF. Case\nreport: hepatic and retro-peritoneal endometriosis presenting as\nobstructive jaundice with ascites: a case report and review of the\nliterature. Clin Radiol 2002;57(03):226 –229. Doi: 10.1053/\ncrad.2001.0667\n35 Zeppa P, Vetrani A, Cozzolino I, Palombini L. Endometrial glands in\nascites secondary to endometriosis. Diagn Cytopathol 2004;30\n(02):131–132. Doi: 10.1002/dc.10390\n36 Ferrero S, Remorgida V. Endometriosis presenting with hemor-\nrhagic ascites. Arch Gynecol Obstet 2011;283(06):1429 –1430.\nDoi: 10.1007/s00404-010-1796-3\n37 Lin JN, Lin HL, Huang CK, et al. Endometriosis presenting as bloody\nascites and shock. J Emerg Med 2010;38(01):30–32. Doi: 10.1016/\nj.jemermed.2008.03.031\nRev Bras Ginecol Obstet Vol. 40 No. 3/2018\nAscites and Encapsulating Peritonitis in Endometriosis Magalhães et al.154\n\n\n38 Sait KH. Massive ascites as a presentation in a young woman with\nendometriosis: a case report. Fertil Steril 2008;90(05):2015.e17-\n–2015.e19\n39 Park BJ, Kim TE, Kim YW. Massive peritoneal fluid and markedly\nelevated serum CA125 and CA19-9 levels associated with an\novarian endometrioma. J Obstet Gynaecol Res 2009;35(05):\n935–939. Doi: 10.1111/j.1447-0756.2009.01122.x\n40 Hasdemir PS, Ikiz N, Ozcakir HT, Kara E, Guvenal T. Endometriosis\nassociated with relapsing ascites and pleural effusions. J Obstet\nGynaecol 2015;35(04):419. Doi: 10.3109/01443615.2014.948823\n41 Cosma S, Ceccaroni M, Benedetto C. A pseudoneoplastic finding of\ndeep endometriosis: laparoscopic triple segmental bowel resec -\ntion. Wideochir Inne Tech Malo Inwazyjne 2014;9(03):463 –467.\nDoi: 10.5114/wiitm.2014.41617\n42 Hinduja I, Kapadia K, Udwadia F, Bhilawadikar R, Adhe A, Zaveri K.\nUnusual presentation of endometriosis with haemorrhagic\nascites - A case report. J Obstet Gynaecol 2016;36(01):133 –134.\nDoi: 10.3109/01443615.2015.1030605\n43 Streuli I, Gaitzsch H, Wenger JM, Petignat P. Endometriosis after\nmenopause: physiopathology and management of an uncommon\ncondition. Climacteric 2017;20(02):138 –143. Doi: 10.1080/\n13697137.2017.1284781\n44 Meigs JV, Armstrong SH, Hamilton HH. A further contribution to\nthe syndrome of fibroma of the ovary with fluid in the abdomen\nand chest, Meigs’ syndrome. Am J Obstet Gynecol 1943;46:19 –37.\nDoi: 10.1016/S0002-9378(16)40440-0\n45 Bernstein JS, Perlow V, Brenner JJ. Massive ascites due to endo-\nmetriosis. Am J Dig Dis 1961;6:1 –6. Doi: 10.1007/BF02239240\n46 Sherer DM, Eliakim R, Abula fia O. The role of angiogenesis in the\naccumulation of peritoneal fluid in benign conditions and the\ndevelopment of malignant ascites in the female. Gynecol Obstet\nInvest 2000;50(04):217 –224. Doi: 10.1159/00001032\n47 Ussia A, Betsas G, Corona R, De Cicco C, Koninckx PR. Patho-\nphysiology of cyclic hemorrhagic ascites and endometriosis.\nJ Minim Invasive Gynecol 2008;15(06):677 –681. Doi: 10.1016/j.\njmig.2008.08.012\nRev Bras Ginecol Obstet Vol. 40 No. 3/2018\nAscites and Encapsulating Peritonitis in Endometriosis Magalhães et al. 155","source_license":"CC0","license_restricted":false}