{"paper_id":"79f682ae-d97c-4c89-b069-b47fb9b04bbe","body_text":"Review began\n 06/08/2022 \nReview ended\n 06/12/2022 \nPublished\n 06/22/2022\n© Copyright \n2022\nPandraklakis et al. This is an open access\narticle distributed under the terms of the\nCreative Commons Attribution License CC-\nBY 4.0., which permits unrestricted use,\ndistribution, and reproduction in any\nmedium, provided the original author and\nsource are credited.\nClinicopathological Characteristics and Outcomes\nof Patients With Endometriosis-Related\nHemorrhagic Ascites: An Updated Systematic\nReview of the Literature\nAnastasios Pandraklakis \n \n, \nAnastasia Prodromidou \n \n, \nDimitrios Haidopoulos \n \n, \nAnna Paspala \n \n, \nMaria D.\nOikonomou \n \n, \nNikolaos Machairiotis \n \n, \nAlexandros Rodolakis \n \n, \nNikolaos Thomakos \n1.\n First Department of Obstetrics and Gynecology, Alexandra Hospital, National and Kapodistrian University of Athens,\nAthens, GRC \n2.\n Third Department of Surgery, Attikon University Hospital, National and Kapodistrian University of\nAthens, Athens, GRC \n3.\n Homerton Fertility Centre, Homerton University Hospital NHS Trust, London, GBR \n4.\nDepartment of Obstetrics and Gynaecology, Accredited Endometriosis Centre, Northwick Park Hospital, London North\nWest University Healthcare, London, GBR\nCorresponding author: \nAnastasios Pandraklakis, \ntasospandraklakis@hotmail.com\nAbstract\nThe presence of ascites is a common clinical presentation in gynecologic oncology patients. Hemorrhagic\nascites (HA) due to endometriosis is a rare presentation that can be easily misdiagnosed as ovarian\nmalignancies. The present study aims to update the currently available knowledge on the characteristics of\npatients presenting with HA due to endometriosis.\nA systematic search was conducted for articles published from January 2000 to July 2020 using the Medline,\nScopus, and Google Scholar databases along with the references of the full-text articles retrieved. Papers\ndescribing cases of women over 18 years with or without previous history of endometriosis were assessed.\nOnly cases with histologically proven hemorrhagic ascites of endometriosis origin were included.\nTwenty-nine studies (27 case reports and two case series) comprising 32 patients were evaluated. The\nmean patients’ age was 32 years, while six of the patients had a previous history of endometriosis. The mean\namount of drained ascitic fluid was 4,200 mL, whereas three patients underwent thoracentesis due to pleural\neffusions. The treatment options included not only medical but also surgical therapies. Fertility preservation\nwas achieved in 27 patients, while two of them achieved pregnancy with in vitro fertilization (IVF)\ntechniques.\nEndometriosis-related hemorrhagic ascites is a relatively rare expression of the disease. Endometriosis-\nrelated hemorrhagic ascites should be considered in the differential diagnosis (DD) of women with ascites\nand clinical suspicion of endometriosis. The available literature is limited to case reports and case series and\nthus indicates further research in the field to decode the pathophysiology of the disease and decide on the\noptimal treatment.\nCategories:\n Obstetrics/Gynecology\nKeywords:\n hemorrhagic, ascites, hemoperitoneum, ovarian cancer, endometriosis\nIntroduction And Background\nAscites is the accumulation of fluid in the peritoneal cavity and are typically presented with abdominal\ndistension, tenderness, dyspnea, and fatigue \n[1]\n. The differential diagnosis (DD) of ascites is complicated by\natypical symptoms and the wide variety of diseases included and thus disabling the final diagnosis \n[2]\n. In\nthat setting, the most common cause of ascites is hepatic cirrhosis due to portal hypertension, which\naccounts for approximately 80% of ascites DD \n[3]\n. Among the other causes, peritoneal disease (cancerous,\ninfectious, or inflammatory), hypoalbuminemia (nephrotic syndrome), and rare conditions (chylous,\npancreatic, urinary, and hemoperitoneum) have also been reported in the etiology of peritoneal fluid\nconcentration \n[4]\n. Hemorrhagic (or bloody) ascites have been reported as the presence of red blood cells\n(RBC) ≥ 10,000 per mm\n3\n, while in dark blood-colored ascitic fluid, about 50,000 RBCs per mm\n3\n have been\nmeasured \n[5]\n.\nFrom the point of view of gynecology, ascites is a frequent presentation in women with ovarian\nmalignancies investigated in gynecologic oncology clinics \n[6]\n. In addition to this, there are also various\nbenign gynecologic diseases that have been characterized by the presence of ascites, including ovarian\nhyperstimulation syndrome, Meigs syndrome, benign ovarian tumors, fibroids, and endometriosis, which\nmakes the final diagnosis difficult to be established \n[7]\n. Paracentesis and cytological examination of the\nascitic fluid is a simple procedure but with limited diagnostic accuracy.\n1\n1\n1\n2\n3\n4\n1\n1\n \n Open Access Review\nArticle\n \nDOI:\n 10.7759/cureus.26222\nHow to cite this article\nPandraklakis A, Prodromidou A, Haidopoulos D, et al. (June 22, 2022) Clinicopathological Characteristics and Outcomes of Patients With\nEndometriosis-Related Hemorrhagic Ascites: An Updated Systematic Review of the Literature. Cureus 14(6): e26222. \nDOI 10.7759/cureus.26222\n\nEndometriosis is a common benign gynecologic disorder that is mainly found in women of reproductive age\nand is defined as the presence of endometriotic tissue in areas outside the uterine cavity \n[8]\n. The pelvic\nstructures and organs are the most prevalent sites of endometriosis despite the fact that in rare cases\nendometriotic lesions can grow in extrapelvic sites \n[9]\n. Hemorrhagic ascites (HA) associated with\nendometriosis is a rare entity that creates diagnostic dilemmas for gynecologists and complicates the\nmanagement of the disease.\nThe aim of the present study was to update the currently available knowledge on the characteristics of\npatients presenting with HA due to endometriosis. More specifically, given the lack of specific guidelines\nand consensus on the appropriate management, we sought to investigate the potential mechanisms of\nendometriosis-related ascites formation, clinical presentation, and disease characteristics, as well as\nthe type of interventions for the management of the disease and postoperative outcomes.\nReview\nMaterials and methods\nStudy Design and Eligible Studies\nThe present systematic review was performed in accordance with the guidelines of the Preferred Reporting\nItems for Systematic Reviews and Meta-Analyses (PRISMA) according to the authors’ predetermined\ninclusion criteria \n[10]\n. Three authors (APr, APan, and NT) independently and meticulously searched the\nliterature, excluded overlaps, and structured the tables with the selected indices. All appropriate\nobservational studies (prospective and retrospective) and case reports and case series of patients with a\ndiagnosis of endometriosis-related HA were considered eligible for inclusion in the present study. The cases\nwith hemorrhagic peritoneal fluid due to endometriosis were considered eligible, while cases of\nhemoperitoneum related to rupture of ovarian endometrioma or other endometriotic nodules were\nexcluded. Additionally, those reported respective cases of HA and hemoperitoneum during pregnancy were\nalso not included. Cases describing the identification of ascetic fluid in which the paracentesis revealed\n“yellow” fluid were also not included. Review articles, conference papers, abstracts, letters to the editor, and\nanimal studies were excluded from analysis and tabulation. Additionally, video articles that were\naccompanied by abstracts with insufficient data were also excluded. Only articles written in the English\nlanguage were included.\nSearch Strategy and Data Collection\nWe performed a meticulous and systematic search of the literature for articles published from January 2000\nto July 2020 using the Medline (2000-2020), Scopus (2000-2020), and Google Scholar (2000-2020) databases\nalong with the references of the articles that were retrieved in full text. The following keywords were used\nfor the search: “endometriosis,” “hemorrhagic ascites,” “hemoperitoneum,” and “bloody ascites.” A\nminimum number of search keywords were utilized in an attempt to assess an eligible number that could be\neasily searched while simultaneously minimizing the potential loss of articles. Articles that fulfilled or were\ndeemed to fulfill the inclusion criteria were retrieved; all articles describing cases of women aged >18 years\nwith or without previous history of endometriosis who were diagnosed with HA that was histologically\nproven to be of endometriosis origin were included. The PRISMA flow diagram schematically presents the\nprocess of article selection (Figure \n1\n).\n2022 Pandraklakis et al. Cureus 14(6): e26222. DOI 10.7759/cureus.26222\n2\n of \n13\n\nFIGURE\n 1: Search flow diagram\nOur search strategy included the following MeSH terms: (“blood” (MeSH Subheading) OR “blood” (All Fields)\nOR “blood” (MeSH Terms) OR “bloods” (All Fields) OR “haematology” (All Fields) OR “hematology” (MeSH\nTerms) OR “hematology” (All Fields) OR “haematoma” (All Fields) OR “hematoma” (MeSH Terms) OR\n“hematoma” (All Fields) OR “haemorrhage” (All Fields) OR “hemorrhage” (MeSH Terms) OR “hemorrhage”\n(All Fields) OR “haemorrhages” (All Fields) OR “hemorrhages” (All Fields) OR “haemorrhagic” (All Fields)\nOR “haemorrhaging” (All Fields) OR “hematologies” (All Fields) OR “haematomas” (All Fields) OR\n“hematomas” (All Fields) OR “hematomas” (All Fields) OR “hematomae” (All Fields) OR “hemorrhaged” (All\nFields) OR “hemorrhagic” (All Fields) OR “hemorrhagical” (All Fields) OR “hemorrhaging” (All Fields)) AND\n(“ascite” (All Fields) OR “ascites” (MeSH Terms) OR “ascites” (All Fields) OR “ascitic” (All Fields)) AND\n(“endometriosis” (MeSH Terms) OR “endometriosis” (All Fields) OR “endometrioses” (All Fields)).\nOutcomes Retrieved\nThe management of the disease and recurrences and reoperation rates during follow-up were set as the main\noutcomes of the present study. Concerning the secondary findings of our study, the characteristics of the\ndisease, including the concomitant presence of pleural effusion, clinical presentation and symptomatology,\ntype of diagnostic procedure, amount of fluid drained recurrence rates, and follow-up after the last\ntreatment, were appraised. Additionally, levels of CA 125 (for studies with multiple values, we considered\nthe highest one) and hemoglobin were evaluated. Data on patient characteristics included age, ethnicity,\nparity, and gravidity of women.\nDefinitions\nHemorrhagic ascites is defined as the detection of more than 10,000 red blood cells (RBC) per \nμ\nL in\nthe ascitic fluid. However, when RBC count in the ascitic fluid was not available, the diagnosis of HA was\nbased on the radiographic findings and/or macroscopic appearance of the bloody/dark red color of the fluid\ndrained.\nQuality Assessment\n2022 Pandraklakis et al. Cureus 14(6): e26222. DOI 10.7759/cureus.26222\n3\n of \n13\n\nCase reports and case series are associated with elevated bias due to the nature of those types of studies \n[11]\n.\nNonetheless, in the case where data on a certain condition is limited, evidence from those studies is\nconsidered of clinical importance. We evaluated the quality of the enrolled studies by adopting the quality\nassessment tool for case reports and case series proposed by Murad et al. \n[11]\n. More specifically, the\nmethodological quality of the studies was assessed based on the criteria, including the domains of\nascertainment, causality, selection, and reporting. The sum of the scores derived from eight critical\nquestions that referred to the domains was used to evaluate the quality of each study and the reviewer’s\njudgment on the presence of the most important domains according to a certain clinical case.\nStatistical Analysis\nContinuous variables were interpreted as median and range, while categorical variables as frequencies and\npercentages. The level of statistical significance was set at p < 0.05.\nResults\nIncluded and Excluded Studies\nA total of 34 full-text articles were assessed to figure out the eligible studies. Among them, 29 studies (27\ncase reports and two case series) that recruited 32 patients were considered eligible for inclusion \n[12-40]\n,\nwhile the remaining five were excluded with reasons \n[41-45]\n. The study by Kishino et al. was excluded due to\nthe fact that the hemorrhagic peritoneal fluid was attributed to retrograde menstruation, whereas the study\nby Bean et al. was excluded due to insufficient data \n[41,45]\n. More specifically, three studies were excluded\ndue to the fact that the full text could not be reached despite multiple attempts to contact the journal and\nauthors \n[42-44]\n.\nPatient Characteristics\nThe median age of the 32 included patients was 32 years (range: 21-46 years). Data concerning ethnicity was\navailable for 14 patients. More specifically, nine patients were of African origin (African-American, Afro-\nBrazilian, Afro- Caribbean, and Nigerian), while two patients were Caucasian, one was Hispanic, and two\nwere Asian. Regarding the 26 patients with parity information available, 19 patients were nulliparous,\nwhereas four were primiparous, and the remaining three were multiparous. Six patients reported a previous\nhistory of endometriosis, five of whom underwent an exploratory laparoscopy for the diagnosis and\nmanagement of the disease. The median CA 125 values were 184 U/L (range: 22 to >5,009), as reported by 16\nstudies, while the median values for hemoglobin were 9.8 g/dL (range: 6.9-12.9 g/dL), which were data from\n12 studies. Six patients were diagnosed with the presence of concomitant pleural effusion. Abdominal\ndistention and progressively worsened discomfort were reported as the main symptoms, followed by\nabdominal pain, weight loss, anorexia, fever, nausea, and breathing difficulty (Table \n1\n).\nAuthor\nand year\nAge\nEthnicity\nHistory of EM\nG/P\nPleural\neffusion\nCA 125\n(U/mL) \nHb\n(g/dL)\nClinical symptoms\nClinical examination\nfindings\nDiagnosis\n(imaging or\ndrainage)\nBhojawala\net al.\n(2000) \n[12]\n34\nBlack\nNo\nG0P0\nYes\nN/A\n11.4\nAbdominal distension (four months), malaise,\nloose stools, nausea and vomiting (two\nweeks), shortness of breath, appetite loss\nTense and distended\nabdomen, hyperactive\nbowel sounds, positive fluid\nthrill \nLaparotomy\nDias et al.\n(2000) \n[13]\n41\nBlack\nNo\nG0P0\nNo\nN/A\nN/A\nNo\nN/A\nExploratory\nlaparotomy\nCheong et\nal. (2003)\n[14]\n41\nMalay\nNo\nP1\nYes\nNormal\nNormal\nWorsening abdominal distension\nGross ascites\nParacentesis\nGoumenou\net al.\n(2006) \n[15]\n46\nN/A\nYes, laparoscopy (30\nyears old), infertility\nG3P0\nYes,\nbilateral \n3,504\n10.2\nProgressive dyspnea, abdominal distension,\nnausea, 7 kg weight loss\nTachypnea, ↓breath\nsounds, abdominal\ndistension, fever\nThoracocentesis,\nparacentesis\nAlabi et al.\n(2007) \n[16]\n30\nBlack\nAfrican\nYes, vaginal EM, six\nmonths, GnRH analog\nand goserelin \nN/A\nNo\n56\n8.5\nAbdominal distension and pain during IVF\ntreatment with GnRH agonist\n N/A\nParacentesis\nPalayekar\net al.\n(2007) \n[17]\nN/A\nAfrican-\nAmerican\nNo\nP1\nNo\n33.6\nN/A\nAbdominal distension, anemia\nModerate abdominal\ndistension\nParacentesis\nSantos et\nYes, laparoscopy\n2022 Pandraklakis et al. Cureus 14(6): e26222. DOI 10.7759/cureus.26222\n4\n of \n13\n\nal. (2007)\n[18]\n40\nBrazilian\n(longstanding\namenorrhea)\nG0P0\nNo\nN/A\nN/A\nUpper abdominal pain, vomiting and weight\nloss of 11 kg, anemia\nN/A\nParacentesis\nSait (2008)\n[19]\n26\nN/A\nNo\nP0\nNo\n3,140\nN/A\nIncreased abdominal girth\nDistended abdomen\nLaparotomy\nUssia et al.\n(2008) \n[20]\n26\nCaucasian\nYes, thoracic and\ndiaphragmatic\nG0P0\nNo\nΝ/A\nN/A\nAscites\nN/A\nLaparoscopy\n23\nN/A\nNo\nG0P0\nYes\nN/A\nN/A\nSevere dysmenorrhea and menstrual R\nshoulder pain\n N/A\nThoracocentesis\n(twice)\nDay et al.\n(2009) \n[21]\n24\nN/A\nNo, EM-related\nsymptoms\nG0P0\nNo\nN/A\n10.7\nTwo-year abdominal pain, nausea, vomiting,\nconstipation, infertility\nN/A\nParacentesis\nturbid brown\nfluid \nLin et al.\n(2010) \n[22]\n29\nN/A\nNo\nG2P2\nYes \nN/A\n12.9\nLight-headedness, palpitations\nHypovolemic shock\nParacentesis\nSuchetha\net al.(2010)\n[23]\n36\nN/A\nNo\nParous\nNo\n>5,000\nN/A\nMassive ascites\nNodularity in Douglas\nParacentesis,\nlaparotomy\nFernandes\net al.\n(2011) \n[25]\n28\nAfro-\nBrazilian\nNo\nG0P0\nNo\nN/A\n9.5\nProgressive increase in abdominal girth, weight\nloss\nDistended, nontender\nabdomen, positive shifting\ndullness\nParacentesis\nShabeerali\net al.\n(2012) \n[24]\n28\nN/A\nNo\nN/A\nNo\nN/A\nN/A\nAbdominal distension (five weeks)\nAscites and mild\ntenderness\nParacentesis\n30\nN/A\nNo\nP2\nNo\n96\nN/A\nProgressive abdominal distension and weight\nloss\nN/A\nParacentesis\n40\nN/A\nNo\nG6P4\nNo\nN/A\nN/A\nAscites\nAscites\nParacentesis\nMorgan et\nal. (2013)\n[26]\n27\nAfrican\nYes, COC\nG0P0\nNo\nN/A\n7\nR neck and flank pain, light-headedness, and\npalpitations\nMildly distended abdomen,\ntender in the RUQ\nParacentesis\nMumtahana\net al.\n(2014) \n[27]\n36\nChinese\nYes\nG0P0\nNo\n78.23,\n86.6,\n5,009 \nN/A\nAscites, anemia\nAbdominal distension\nParacentesis\nAppleby et\nal. (2014)\n[28]\n34\nNigerian\nNo\nN/A\nNo\nN/A\n9.6 \nAbdominal distention, 4 kg weight loss\nGross ascites\nDrainage\nAsano et\nal. (2014)\n[29]\n35\nJapanese\nNo\nG0P0\nNo\n22\n10\nDysmenorrhea, abdominal distention\nAbdominal distention\nDrainage\nBignall et\nal. (2014)\n[30]\n36\nAfro-\nCaribbean\nNo\nG0P0\nNo\n1123\n10.8 \nSeven-month dysmenorrhea, deep\ndyspareunia, constipation\nAbdominal tenderness and\ndistention\nParacentesis\nCosma et\nal. (2014)\n[31]\n36\nN/A\nDeep pelvic EM\nN/A\nNo\n184\nN/A\nDysmenorrhea, dyschezia, epigastric\nmenstrual pain\nN/A\nDrainage\nHasdemir\net al.\n(2014) \n[32]\n32\nN/A\nYes, EM (laparoscopic\nbiopsies)\nN/A\nYes\n47\nN/A\nAbdominal distension and shortness of breath\nMassive ascites\nLaparoscopy,\ndrainage\nHinduja et\nal. (2015)\n[33]\n34\nN/A\nNo\nP1A1\nNo\nN/A\nN/A\nAbdominal bloating\nN/A\nTransvaginal\naspiration of\nDouglas \nSetubal et\nal. (2015)\n[40]\n26\nCaucasian\nNo\nG0P0\nNo\n100\nN/A\nUpper abdominal pain and distention\nN/A\nParacentesis\nDun et al.\n26\nNigerian\nYes\nP0\nNo\nN/A\nN/A\nAscites\nN/A\nDrainage\n2022 Pandraklakis et al. Cureus 14(6): e26222. DOI 10.7759/cureus.26222\n5\n of \n13\n\n(2016) \n[34]\nPereira et\nal. (2017)\n[35]\n21\nN/A\nNo\nG0P0\nNo\nN/A\n7.5\nAbdominal distension, dyspnea\nN/A\nLaparoscopy\nMagalhães\net al.\n(2018) \n[36]\n28\nN/A\nNo\nN/A\nNo\n107.8,\n889.6 \nN/A\nWasting syndrome, ↑abdominal girth,\nshortness of breath,c↓appetite\nN/A\nDiagnostic\nlaparoscopy\nPang et al.\n(2019) \n[37]\n40\nN/A\nNo\nG1P0\nNo\n372.4\nN/A\nLower abdominal pain, pelvic mass,\ndysmenorrhea\nPalpable pelvic mass\nLaparoscopy\nWang et al.\n(2019) \n[38]\n24\nNigerian\nNo\nG0P0\nNo\n41.54,\n113\n6.9 \nRapidly enlarging abdominal distension\nMassive ascites\nN/A\nGonzalez\net al.\n(2020) \n[39]\n32\nHispanic\nYes, massive\nhemorrhagic ascites\nNull\nN/A\nN/A\nN/A\nMalaise, abdominal distension, loss of\nappetite, diffuse abdominal pain, breathing\ndifficulty\nN/A\nParacentesis\nTABLE\n 1: Main characteristics of the included studies\nR: right, RUQ: right upper quadrant, EM: endometriosis, G: gravidity, P: parity, Hb: hemoglobin, N/A: not available, COC: combined oral contraceptives\nAdditionally, endometriosis-related symptoms including dysmenorrhea, dyspareunia, and dyschezia were\nalso recorded. Clinical examination revealed abdominal tenderness and distention with shifting dullness in\npalpation, palpable pelvic mass if present, and diminished breath sound in patients with simultaneous\npleural effusion. In critically ill patients, signs of hemodynamic instability were also noted. In 19 cases, the\ndiagnosis was established with an examination of the percutaneously drained HA, while in one patient, a\ntransvaginal paracentesis through the pouch of Douglas was performed. Five patients underwent an\nexploratory laparoscopy and drainage, whereas an open surgical approach was applied to three women.\nQuality Assessment\nBased on the type of the included clinical cases, we considered the score of 5 points as the highest that could\nbe assessed when excluding the three questions (from 4 to 6) from the quality assessment tool that attributed\nto cases of adverse drug events. A mean score of 3.5 (SD: ±0.85) was calculated, whereas the overall\njudgment on the quality of the recruited studies was that they were of moderate quality.\nMain Outcomes\nThe median amount of fluid drained was 4,200 mL (range: 1,500-9,400 mL), and four patients underwent\ntwo or more sessions of paracentesis. Concomitant thoracentesis was performed three patients due to\npleural effusion. The main treatment modalities included hormonal therapy, other medications for\nsymptomatic relief, and surgical procedures. Various hormonal modalities were adopted, including GnRH\nagonists/analogs (goserelin and leuprorelin), combined oral contraceptives (COC), luteinizing hormone (LH)\nagonists, dienogest, medroxyprogesterone, and norethindrone. GnRH agonist treatment was used in 17\npatients, GnRH antagonists in one patient, COC in three patients, LH agonist in one patient, dienogest\nin two patients, and medroxyprogesterone and norethindrone in one patient. There is a case that was\ntreated with chemotherapeutic agents for suspected ovarian cancer \n[15]\n and two cases that were initially\ntreated with antituberculous agents for suspected tuberculous ascites \n[24,38]\n. Therapy with fertility-\npreserving management was decided in all but five patients at the initial management and included\nresection of all visible endometriotic nodules, adhesiolysis, and respective repairs of the affected organs\nsuch as colectomies and anastomosis, as shown in Table \n2\n. However, fertility was finally preserved in 27\npatients. Seven patients underwent bilateral salpingo-oophorectomy with hysterectomy along with excision\nof all macroscopic pelvic endometriotic nodules and other procedures including omentectomy,\nappendectomy, and lymphadenectomy (Table \n2\n). In 13 patients, an open approach was applied, whereas 24\npatients had laparoscopic procedures. Six of them underwent both laparoscopic and laparotomic evaluation.\nPregnancy outcomes were available for two patients who achieved a single and twin pregnancy \n[30,40]\n. Both\nof them conceived with the use of in vitro fertilization (IVF) techniques and delivered preterm through\ncesarean section at 32 and 35 weeks of gestation, respectively. Two of the patients had postoperative ileus;\namong them, one died due to peritonitis and sepsis after intestinal obstruction and enterocutaneous\nfistulae.\nAuthor\nAmount\nof fluid\nManagement\nHistology\nFollow-up (recurrence-\n2022 Pandraklakis et al. Cureus 14(6): e26222. DOI 10.7759/cureus.26222\n6\n of \n13\n\nand year\ndrained\nPrimary treatment\nSecondary treatment\nreoperation)\nBhojawala\net al.\n(2000) \n[12]\n9,000\nLaparotomy, TAH-RSO, adhesions\nN/A\nEndometriosis\nof the cervix, R\nfallopian tube,\nand ovary\nOne mo - R exploratory\nthoracotomy, decortication\nof the R lung, and parietal\npleurectomy; six wks - NED\nDias et al.\n(2000) \n[13]\nN/A\nGnRH analog\nN/A\nN/A\nSix mo - progressive ↓ of\nascites\nCheong et\nal. (2003)\n[14]\n5,600\nExploratory laparotomy-peritoneal\nbiopsies\nYes, medical\nEM\nN/A\nGoumenou\net al.\n(2006) \n[15]\n4,000\nFirst-line chemotherapy\n(carboplatin/taxol), suspected\nmalignancy\nTwo mo - exploratory\nlaparotomy\ndebulking/TAH-BSO,\nomentectomy,\nappendectomy,\nbiopsies, L pelvic\nlymphadenectomy\nInflammation\nand EM\nSix mo - NED\nAlabi et al.\n(2007) \n[16]\n5,000\nEmergent diagnostic laparoscopy,\nextensive pelvic EM including the bowel\nSecond laparoscopy\nafter one wk,\nadhesiolysis, and\nbowel mobilization\nEM\nTwo mo - ascites (2.5 L),\nrecurrence; one mo -\nlaparoscopy multiple\nbiopsies; spontaneous\nconceive\nPalayekar\net al.\n(2007) \n[17]\n4,000-\n6,000\nExploratory laparotomy - advanced\npelvic EM, TAH-BSO\nDeclined hormonal\ntherapy\nEM\n12 mo - NED\nSantos et\nal. (2007)\n[18]\nN/A\nLaparoscopy (nondiagnostic),\nlaparotomy - adhesiolysis, encapsulating\nperitonitis\nN/A\nEM\nFive mo - intestinal\nobstruction,\nenterocutaneous fistulae,\nDOD (peritonitis and\nsepsis)\nSait (2008)\n[19]\n5,000\nLaparotomy - bilateral ovarian\ncystectomy, multiple biopsies\nGnRH analog for six\nmo, maintenance with\nCOC\nEM\n12 mo - NED\nUssia et al.\n(2008) \n[20]\n1,000,\n>1,000,\n2,000,\n1,500\nThree laparoscopies during three yrs,\ntwo mo laparotomy - massive\nadhesiolysis, appendicectomy,\nomentectomy, USO\nGnRH\nEM\n36 mo - NED\n1,500\nLaparoscopy - ascites, frozen pelvis,\nbowel adhesions, and EM spots; second\nlaparoscopy (one yr after GnRH agonist)\n- ascites, adhesions, DIE, rectovaginal\nnodule excision, ureterolysis, resection\nsigmoid anastomosis\nGnRH agonist and\nintermittent\ncorticosteroids\nEM\nNED\nDay et al.\n(2009) \n[21]\n4,000\nExploratory laparoscopy - stage IV\nASRM EM, multiple biopsies\nLeuprolide acetate\n11.25 mg\nEM\nIleus PO (44-d admission -\nconservative management),\nthree mo - NED\nLin et al.\n(2010) \n[22]\n2,000\nDiagnostic laparoscopy -\nelectrocauterization EM of the L broad\nligament\nN/A\nN/A\nN/A\nSuchetha\net al.(2010)\n[23]\n6,000\nDiagnostic laparotomy - abdominal\ncocoon, biopsies of the adnexa, bladder,\nperitoneum, omentum, and stomach\nOne yr - leuprolide\n \nThree mo - bilateral ovarian\nmasses, hydronephrosis -\nomentectomy\nFernandes\net al.\n9,400\nLaparoscopy - adhesions, mesosigmoid\nbiopsy\nThree mo - GnRH\nanalog estrogen and\nthen continuous\nFibrosis and\nextensive\nhemosiderin\ndeposition,\n12 mo - NED\n2022 Pandraklakis et al. Cureus 14(6): e26222. DOI 10.7759/cureus.26222\n7\n of \n13\n\n(2011) \n[25]\nestrogen-progestin\nendometrial\nglands and\nstroma\nShabeerali\net al.\n(2012) \n[24]\nN/A\nDiagnostic laparoscopy conversion to\nlaparotomy, dense adhesions with small\nand large bowel, biopsies; second\noperation TAH-BSO\nOne yr - GnRH\nanalogs (partial\nresponse), TAH-BSO\nN/A\n12 mo - NED\nN/A\nLaparoscopy - ascites, peritoneal\nbiopsies\nSubtotal\nhysterectomy and\nBSO\nEM\n12 mo - NED\n2,500,\n3,000\nTwo laparoscopies - suspected\ntuberculosis (antituberculosis\ntreatment); third laparoscopy - ascites,\nadhesions, biopsies\nGnRH analogs\nEndometrial\nglands and\nendometrioid\nstroma\nNED\nMorgan et\nal. (2013)\n[26]\n4,500\nLeuprolide\nN/A\nN/A\nN/A\nMumtahana\net al.\n(2014) \n[27]\n3,000,\n2,500\nExploratory laparoscopy, dense\nadhesions, bilateral ovarian masses,\nDouglas nodules\nGoserelin acetate/mo\nEM\nNED\nAppleby et\nal. (2014)\n[28]\nN/A\nLaparoscopy - endometrial ovarian and\nfallopian tube deposits (biopsies)\nGnRH antagonist\nEM\nSix mo - NED\nAsano et al.\n(2014) \n[29]\n5,500\nExploratory laparotomy - adhesions,\nbiopsies of brown omental nodules\nstage IV EM\nEight y - GnRH\nagonist and ascites\ndrainage (13 times) -\nswitch to DNG\nEM\n12 mo - NED\nBignall et\nal. (2014)\n[30]\n3,500,\n1,600\nLaparoscopy - biopsies of uterosacral\nligament and bowel nodules stage IV\nEM\nGnRH analogs\nCyclical\nendometrium in\nproliferative\nphase\nPregnancy achieved (IVF) -\nlive birth at 32 wks\nemergent CS/two wks\nrecurrent ascites - 5 GnRH\ninjections NED\nCosma et\nal. (2014)\n[31]\n4,200,\n250\nLaparoscopy - adhesions, excision of\npelvic EM, colectomies, three\nanastomoses, and temporarily ileostomy\nSecond-look\nlaparoscopy and\nileostomy closing (22\ndays)\nEM\n48 mo - NED\nHasdemir\net al.\n(2014) \n[32]\n2,500\nParacentesis and six mo leuprorelin\nN/A\nEM by\nparacentesis\nThree mo - recurrence -\nDNG\nHinduja et\nal. (2015)\n[33]\n4,500,\n2,500,\n3,000,\n4,000,\n3,500\nDiagnostic laparoscopy - biopsies of\nomental and bowel nodules\nThree mo - leuprolide\n3.75 mg\nEM\nSix mo - multiple\nrecurrences of ascites,\nrecurrence of ascites after\nTAH-BSO with vaginal\ndischarge/one y - NED\nSetubal et\nal. (2015)\n[40]\n2,500,\n1,000\nDiagnostic laparoscopy - pelvic\nadhesions, rectal and ovarian implants,\nomental retractions, hematic liver\nimplants, multiple biopsies\nThree mo - COC\nEM\nThree mo - ascites\nrecurrence-GnRH agonist;\nsecond laparoscopy - DIE,\nGnRH agonist; pregnancy\nachieved, live birth of twins\nat 35 weeks/NED on COC\nDun et al.\n(2016) \n[34]\n7,000,\n7,800\nExploratory laparotomy - biopsies\nThree mo - goserelin\nand oral and one y\noral\nmedroxyprogesterone\nEM\nThree mo - recurrence,\nunsuccessful conceive\nattempt; laparoscopy, EM\nresection with peritoneal\nstripping, laser excision,\nablation; six mo - NED\nPereira et\nLaparoscopy (third laparoscopy) -\n2022 Pandraklakis et al. Cureus 14(6): e26222. DOI 10.7759/cureus.26222\n8\n of \n13\n\nal. (2017)\n[35]\n4,000\nextensive EM adhesions in the pelvis,\nbipolar and monopolar excision of EM\nMonophasic oral\ncontraceptive pills\nEM\nNED\nMagalhães\net al.\n(2018) \n[36]\n8,000\nDiagnostic laparoscopy - multiple\nadhesions and encapsulating peritonitis\n(nondiagnostic); second laparoscopy -\nbiopsies\nGoserelin acetate\nChronic\nperitonitis and\nhemosiderin\ndeposits\nSix mo - NED\nPang et al.\n(2019) \n[37]\n2,000\nLaparoscopy converted to laparotomy\n(bleeding) - TAH BSO, R broad ligament\nmass excision\nNo\nMass with a\nmonolayer of\nnormal-looking\nendometrial\nglands and\nstroma\nThree mo - NED\nWang et al.\n(2019) \n[38]\nN/A\nGnRH analogs (leuprorelin) for three mo\nand then droperidol\n \nand ethinyl estradiol\ntb for eight mo\nNo\nEndometrial\nglandular cells\nand surrounding\nstromal cells\n(core needle\nbiopsy of the\nomentum)\nFive mo - stable ascites -\nsymptom improvement\nTABLE\n 2: Main outcomes\nN/A: not available, EM: endometriosis, R: right, L: left, PO: postoperative, wk: week, mo: months, yr: year, TAH: total abdominal hysterectomy, BSO:\nbilateral salpingo-oophorectomy, USO: unilateral salpingo-oophorectomy, COC: combined oral contraceptive, CS: cesarean section, NED: no evidence of\ndisease, DOD: die of disease, DIE: deep infiltrating endometriosis, DNG: dienogest\nDiscussion\nIn the present study, we analyzed the characteristics of 32 women with EM-related hemorrhagic ascites. The\nmajority of patients were nulliparous, while abdominal distention and progressively worsened discomfort\nwere recorded as the main symptoms at presentation. The mean amount of drained ascitic fluid was 4,200\nmL. The treatment options included not only medical-hormonal but also surgical therapeutic modalities.\nFertility preservation was achieved in 27 patients, while two of them achieved pregnancy with IVF\ntechniques. Two cases of postoperative ileus were reported and one postoperative death due to peritonitis.\nThe role of elevated CA 125 levels is debatable; there have been reports indicating elevated CA 125 levels in\npatients with ascites that are non-cancer-related, such as cirrhotic or even in heart failure \n[46,47]\n. According\nto the findings of the present study, CA 125 levels ranged from 22 to 5,000, which could be considered\nconflicting given the high suspicion of malignancy in patients with ascites and elevated CA 125 levels.\nFurthermore, before confirming the presence of ascites with ultrasound, there are also some percussion\nsigns including puddle signs, floating ice, and flank dullness that could be useful \n[48]\n. The reported overall\naccuracy of physical examination maneuvers is approximately 58%, with sensitivity and specificity ranging\nfrom 50% to 94% and from 29% to 82%, respectively \n[49]\n.\nThe differential diagnosis of a woman who presents with ascites is relatively challenging. Besides hepatic\nand renal failure, which are considered the main causes of the formation of ascites, malignant and infectious\nintra-abdominal diseases are also responsible for the concentration of diffusion of peritoneal fluid rich in\nproteins \n[50]\n. With regard to malignant diseases, epithelial ovarian and tubal cancer, primary peritoneal\nserous carcinoma, and endometrial cancer can be associated with ascites formation \n[51]\n. Furthermore,\nbenign ovarian cysts, endometriosis, ovarian hyperstimulation syndrome, peritoneal tuberculosis, and Meigs\nsyndrome should also be considered in the differential diagnosis of female ascites \n[51]\n.\nEndometriosis-related ascites can be easily misdiagnosed as ovarian cancer-related due to the fact that both\nentities share some similar symptoms. To that end, hemorrhagic endometriotic ascites can present with\nabdominal distention and pain, loss of appetite, and weight loss, mimicking atypical cancer symptoms.\nHowever, careful evaluation of patients’ medical history and endometriosis-related symptoms such as\ndysmenorrhea, dyspareunia, and cyclical pain should be thoroughly investigated. Furthermore, high clinical\nsuspicion should be paid to the cases of malignancy arising from endometriosis \n[52]\n. The prevalence of\nmalignancy is about 0.7%-1.6% in patients with endometriosis \n[52]\n. Consequently, the exclusion of\nmalignancy is of critical importance, and thus, it is considered safer to set the final diagnosis after surgical\nevaluation and histological examination of the excised specimens. In that setting, some of the patients\nincluded in the present study underwent a diagnostic laparoscopy with a concomitant aspiration of the\nascitic fluid and peritoneal biopsies. The percutaneous aspiration of the ascites has also been applied in\n2022 Pandraklakis et al. Cureus 14(6): e26222. DOI 10.7759/cureus.26222\n9\n of \n13\n\nsome cases. This first-line diagnostic modality is an easy-to-perform bedside practice and can facilitate a\nmore accurate further management of the disease \n[53]\n. The cytological findings of the aspired ascitic fluid\ncan reveal epithelial and stromal cells in a hemorrhagic environment with hemosiderin and hemofuscin-\nladen macrophages \n[53,54]\n.\nThere are some reports available in the literature indicating the concomitant detection of encapsulating\nperitonitis in patients with endometriosis-related ascites. Encapsulating peritonitis, also known as\nabdominal cocoon or frozen ascites, is a rare entity defined as the formation of a thick fibrin membrane that\nentraps the bowel loops \n[36]\n. According to a recent systematic review by Magalhães et al. on endometriosis-\nrelated ascites and encapsulating peritonitis, only six cases of endometriosis-associated encapsulating\nperitonitis have been recorded in the literature \n[18,36]\n. Additionally, another case of encapsulating\nperitonitis has been recently published by Gonzalez et al. and was attributed to recurrent HA due to\nendometriosis \n[39]\n. A potential theory supports that endometriosis-related inflammation causes peritoneal\nirritation and further enhances fibrosis and inflammation, resulting in the formation of encapsulating\nperitonitis.\nThe exact pathophysiology of the formation of endometriosis-related ascites still remains ill-defined.\nBernstein et al. were the first to study on the pathogenesis of endometriosis-associated ascites. The authors\nclaimed that the presence of endometrial cells in the peritoneal cavity under unknown mechanisms can\nactivate the peritoneal cells to produce ascitic fluid \n[54]\n. Additionally, another theory suggested the\nperitoneal irritation from the spontaneous rupture of endometriotic cysts, which can produce reactive\nperitoneal fluid \n[54]\n. Another potential mechanism is based on the inflammatory response caused by the\neffect of the uterine hormones on the ectopic endometriotic lesions \n[55]\n. The aforementioned theories are\nwell supported by recent studies speculating on the diversity of the biochemical and metabolic profiles of\nthe peritoneal fluid in patients with endometriosis. More specifically, according to Polak et al., the\nhemoglobin levels in the peritoneal fluid of patients with endometriosis were significantly elevated\ncompared to both controls and women with ovarian cysts, while, interestingly, antioxidant parameters were\nsignificantly lower in patients with endometriosis, creating an oxidative intraperitoneal environment \n[56-\n58]\n.\nThe outcomes of the present study indicated a high prevalence of HA in patients of African origin. A\nrespective high prevalence was also observed in the systematic review by Gungor et al. who reported a\nproportion of more than 60% of African ethnicity among women with endometriosis-related ascites \n[54]\n.\nLittle is known with regard to the potential association between endometriosis and race. Despite the fact\nthat the currently available literature provides evidence of a higher prevalence of endometriosis in White\nwomen compared to African, those reports are subjected to significant bias related to diversity in\nsocioeconomic status, access to the healthcare system, and childbearing age \n[59]\n. Additionally, Bougie et\nal. highlighted the potential diversity of symptoms and clinical presentation of endometriosis among\ndifferent ethnicities, which could also explain the elevated prevalence of HA among African populations\nwith endometriosis \n[59,60]\n.\nConcerning the management of endometriosis-associated ascites, it is mainly based on the extent of the\nunderlying endometriosis and is that of endometriosis including surgery or medication or both.\nAdditionally, the drainage of the ascetic fluid is crucial for the alleviation of abdominal distention and\ndiscomfort. Due to the fact that a significant proportion of patients (six in the present study) presented with\nconcomitant pleural effusion, thoracentesis is also indicated for the symptomatic relief of breath discomfort.\nThe majority of the patients in the present study underwent surgery for the management of endometriosis.\nThe extent of surgical procedures is based on the age of the patient and the desire for fertility\npreservation \n[61]\n. Moreover, adjuvant pharmaceutical therapy was administered to 16 patients\npostoperatively. A favorable effect of postoperative medication maintenance therapy has been reported for\nsymptomatic relief and recurrence prevention, but its exact role still remains controversial \n[61,62]\n.\nLimitations\nDespite the plethora of reports, the true prevalence of HA could not be precisely reached since no\nobservational studies are available in the field and thus precluded further research. The fact that our results\nare based only on case reports and two case series constitutes the main limitation of the study and precludes\ngeneralization of the conclusions and further quantitative and qualitative analysis. In addition to this, there\nis no sufficient evidence concerning the pathophysiology of ascites formation, while it is not clear for all\ncases whether the bloody peritoneal fluid was concentrated after the rupture of an ovarian endometrioma or\nwhether other mechanisms similar to those forming malignant ascites are involved. Finally, there is\nsignificant heterogeneity in the included studies, and some parameters were omitted by some studies, which\nwas another limitation and precluded reaching firm results.\nConclusions\nThe present review accumulates the current knowledge with regard to the natural history, characteristics,\nand management of adult females who presented with hemorrhagic ascites due to endometriosis. The\ndifferential diagnosis of a woman who presents with ascites is relatively challenging. Endometriosis-related\n2022 Pandraklakis et al. Cureus 14(6): e26222. DOI 10.7759/cureus.26222\n10\n of \n13\n\nhemorrhagic ascites is a relatively rare expression of the disease. Nonetheless, it should be considered in the\ndifferential diagnosis of women with ascites and clinical suspicion of endometriosis. Additionally, the\nexclusion of malignancy is considered of critical importance. High clinical suspicion should be paid to cases\nof malignancy arising from endometriosis. The exact pathophysiologic pathways of endometriotic\nhemorrhagic ascites formation still remain elusive, despite the plethora of available theories.\nThe management of hemorrhagic ascites should speculate on both alleviation of the abdominal distention\ndue to the presence of ascites and treatment of the underlying disease. The currently available literature is\nlimited to case reports and case series, thus precluding reaching firm conclusions. Further research in the\nfield is needed to decode the pathophysiology of the disease and decide on the optimal treatment.\nAdditional Information\nDisclosures\nConflicts of interest:\n In compliance with the ICMJE uniform disclosure form, all authors declare the\nfollowing: \nPayment/services info:\n All authors have declared that no financial support was received from\nany organization for the submitted work. \nFinancial relationships:\n All authors have declared that they have\nno financial relationships at present or within the previous three years with any organizations that might\nhave an interest in the submitted work. \nOther relationships:\n All authors have declared that there are no\nother relationships or activities that could appear to have influenced the submitted work.\nReferences\n1\n. \nCavazzoni E, Bugiantella W, Graziosi L, Franceschini MS, Donini A: \nMalignant ascites: pathophysiology and\ntreatment\n. 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