{"paper_id":"08eabedd-1604-427d-a8e6-cb8857ee19bd","body_text":"Ital J Gynaecol Obstet  2023, 35, N.2\n196\nPredictive risk factors for occurrence of tubo-ovarian abscess in patients with \novarian endometriosis: a prospective comparative study\nAhmed Mahmoud Abdou 1, Ahmed M. Fahmy 2, Ola A. Harb 3,*, Abdel-Razik El-Sayed Abdel-Razik 1\n1 Department of Gynecology and Obstetrics, Faculty of Medicine, Zagazig University, Zagazig, Egypt.\n2 Department of Anesthesia and Intensive care, Faculty of Medicine, Zagazig University, Zagazig, Egypt.\n3 Department of Pathology, Faculty of Medicine, Zagazig University, Zagazig, Egypt.\nGynæcology & Obstetrics\nItalian Journal of\nORIGINAL ARTICLE\nJune 2023 - Vol. 35 - N. 2 - Quarterly - ISSN 2385 - 0868\nARTICLE INFO\nHistory\nReceived:  20 April 2022\nReceived in revised form: 17 June 2022 \nAccepted: 31 August 2022\nAvailable online: 07 June 2023\nDOI: 10.36129/jog.2022.57\n*Corresponding author: Ola Harb, Professor, M.D. \nDepartment of Pathology, Faculty of Medicine, Zag-\nazig University, Tolba Street, Zagazig, Egypt. \nEmail: olaharb2015@gmail.com. \nORCID: 0000-0002-4396-3101.\nCopyright 2023\nABSTRACT\nObjective. To assess demographical and clinical criteria of patients with tu-\nbo-ovarian abscesses (TOAs) to evaluate predictive risk factors of occurrence \nof ovarian endometriosis-tubo-ovarian abscess (OE-TOA).\nPatients and Methods. In the current case control comparative study, 200 \npatients with OE were included and divided into the first group (the case) \n(composed of 80 patients with OE-TOA) and the second group (the control) \n(composed of 120 patients with OE but no TOA). Then we compared between \nboth groups regarding all parameters.\nResults. There is statistically significant relation between occurrence of com-\nbined OE and TOA and spontaneous rupture of ovarian cyst (p = 0.026), his-\ntory of PID (p = 0.26) and presence of DM (p = 0.32). Spontaneous rupture of \novarian cyst and history of PID are significantly associated with combined OE \nand TOA. \nLower genital tract infections were diagnosed in 8 (66.7%) of patients in the \nfirst group (OE-TOAs) and were diagnosed in only 4 (33.3%) patients with OE \nwithout TOAs (p = 0.042). \nHistory of spontaneous rupture of OE cyst and PID independently increased \nrisk of TOA+ OE by 2.819 and 2.547 folds, respectively.\nConclusions. We found that predictive risk factors of OE-TOA were rupture \nof OE cysts spontaneously in addition to lower genital tract infections, low \nimmunity and neglected pelvic inflammatory diseases. \nKey words \nTubo-ovarian abscess; ovarian endometriosis; \nrisk factors.\n\n197\nTubo‑ovarian abscess in patients with ovarian endometrios Ahmed Mahmoud Abdou, Ahmed M. Fahmy, Ola A. Harb, Abdel‑Razik El‑Sayed Abdel‑Razik\nINTRODUCTION\nPelvic inflammatory diseases (PIDs) are group of \ninfections of the uterus, fallopian tubes and the \novaries [1].\nPIDs clinical importance was studied due to their \nsequels that include infertility, persistent pelvic \npain and ectopic pregnancy. Additionally, inade-\nquate treatment of PIDs might be complicated by \npyosalpinx and tubo-ovarian abscesses (TOAs) \nwhich are severe complications that were reported \nin 15-34% of patients with PIDs [2, 3]. It was previ-\nously hypothesized that PID and TOA have more \nliability to occur in severe degrees in patients with \nendometriosis more than in those without endo-\nmetriosis [4]. Pelvic peritoneal endometriosis is an \nimportant cause of marked pelvic pain [5].\nEndometriosis is as a disabling condition which \nworsen social, sexuality and mental health that \nmight be caused by acute immunological reactions \nwithin the microenvironment of endometriosis le-\nsions [6]. Smoking could increase endometriosis \nrisk mainly in infertile nulliparae patients [7].\nMoreover, when TOAs were associated with ovar-\nian endometriosis (OE-TOA), it occurs in a severe \nand even life-threatening form [8].\nMacrophages are classified into pro-inflammatory \nM1 and M2 which induce immunotolerance and \nangiogenesis. Both were significantly higher in en-\ndometriosis [9].\nThere are many reported risk factors for PIDs and \nTOAs as young age of the patient, uterine instru-\nmentation, sexually transmitted infections, multi-\nple sexual partners, hysterosalpingography, and \nin vitro fertilization (IVF) [10, 11]. AntiMullerian \nhormone (AMH) levels have a significant accuracy \nin pregnancy prediction in patients with ovarian \nendometriosis [12]. The role of neurotrophins in \neutopic endometrium from endometriosis-patients \nwas investigated and no differences were found \nbetween patients with and without endometriosis \nwith regards to the neurite outgrowth of sensory \nganglia [13]. Pelvic nerve-sparing surgery is effec-\ntive in improving intestinal symptoms after per -\nforming radical surgery for endometriosis which \nneeded segmental intestinal resection [14].\nHowever, there is a need for more comprehensive \nstudies that assessed the risk factors for OE-TOA [15].\nThe aims of the present study were to assess de-\nmographical and clinical criteria of patients with \nTOAs, to evaluate incidence of occurrence of TOAs \nin patients with ovarian endometriosis, to evalu-\nate predictive risk factors of occurrence of OE-TOA \nand finally to correlate between TOAs patients \nwith and without endometriosis to allow early di-\nagnosis, prevention, and adequate treatment.\nMATERIALS AND METHODS\nThe current prospective comparative study is per -\nformed in Gynecology and Obstetrics Department, \nFaculty of Medicine, Zagazig University after tak-\ning an approval from the local ethical committee \nand written informed consents from all patients.\nWe included all cases with clinical, radiological \nand pathological evidence of endometriosis with \nor without TOAs who were surgically operated \nby laparotomy or laparoscopy in the period from \nMarch 2016 till March 2021.\nInclusion and exclusion criteria of the study\nThe surgical indications for all patients were pres-\nence of an adnexal mass (greater than 4 cm in size). \nCriteria of inclusion of patients in the first group \n(the case) were detected pus during surgery then \npathological confirmation of the presence of OE-\nTOA by detecting endometrial glands/stroma or \nhemosiderin laden macrophages in the detected \ntubo-ovarian cyst, in addition to detection of heavy \ninfiltrate of neutrophils in the capsule of the ovari-\nan cyst and the tube.\nCriteria of inclusion of patients in the second group \n(the control) were no detected pus during surgery \nand pathological confirmation of the presence of \nonly OE cysts without the presence of TOAs. \nThe exclusion criteria were malignant tumour of \nany pelvic organs, suppurative appendicitis with \nor without appendicular abscesses and patients \nwith incomplete or with lost data.\nAfter application of inclusion criteria, 200 patients \nwith OE were included and were divided into the \nfirst group (the case) (composed of 80 patients with \nOE-TOA) and the second group (the control) (com-\nposed of 120 patients with OE but no TOA).\nWe collected all demographic and clinical data of \nall patients in addition to collection of possible pre-\ndictive risk factors for OE-TOA. The collected data \nincludes age, marital status, parity, primary or sec-\nondary infertility, past history of PID or ectopic preg-\nnancy and history of previous OE cysts removal. We \ncollected data about any previous performed sur -\ngery within 15 days as appendectomy, caesarean de-\n\nItal J Gynaecol Obstet  2023, 35, N.2\n198\nTubo‑ovarian abscess in patients with ovarian endometrios\nlivery or uterine cavity surgery within 15 days. We \nrecorded the presence of lower genital tract infection \nor spontaneous rupture of OE cysts, dysmenorrhea, \nand any co-existent medical disease as diabetes mel-\nlitus or hypertension in addition to monitoring lev-\nels of carbohydrate antigen 125 (CA125).\nWe treated all patients with one of the following 2 \nantibiotic regimens according to Centers for Dis-\nease Control (CDC) guidelines: 1) IV doxycycline \n100 mg every 12 h, IV cefoxitin 2 g every 6 h 2) IV \nclindamycin 900 mg every 8 h and gentamycin 1.5 \nmg/kg [9]. \nIn case of lack of clinical improvement of the pa-\ntient, in addition to failure of medical treatment re-\nsponse within 48-72 h surgery was performed.\nThen we divided all included patients into two \ngroups according to clinical and pathologic find-\nings: the first group includes patients with histo-\npathologically confirmed OE-TOAs and those with \nonly OE without TOAs then we compared between \nboth groups regarding all parameters.\nEthical approval to perform the manuscript was \ntaken from local ethical committee of Faculty of \nmedicine Zagazig University.\nThis manuscript conforms the Enhancing the \nQUAlity and Transparency Of health Research \n(EQUATOR) network guidelines.\nStatistical analyses were performed with SPSS \nversion 17 (SPSS Inc., Chicago, IL, USA). We used \nKolmogorov-Smirnov and Shapiro-Wilk tests for \nassessment of normality of data.\nWe detected mean ± standard deviation (SD) for \nevaluating normally distributed data. We used in-\ndependent samples t-test, Mann-Whitney U test \nand Kruskal-Wallis tests for comparing the groups \naccording variables distribution. We used chi-\nsquared test for comparing categorical variables. \nBinary regression analysis was used to measure \nodds of risk factor in producing TOAs. Statistical \nsignificance was set at p < 0.05 for all tests.\nRESULTS\nA total of 200 women were evaluated in this study. \nAmong these women, 80 were diagnosed with OE-\nTOA and 120 patients were diagnosed with OE \nwithout TOAs. \nThe collected demographic data of both groups \nwere found and compared in Table 1.\nPatients age ranges from 19 to 59 years with mean \nage 41.4 years and mean BMI was 24.92 kg/m 2. \nAbout 77% were married, out of them, 19% had pre-\nvious CS and 34% of them were infertile. Forty per-\ncent of the studied patients had OE-TOA. Diabetes \nand hypertension occurred in 6% and 5% of patients \nTable 1. Baseline data of the studied patients.\nParameter n = 200\nAge\nMean ± SD\nRange \n41.4 ± 7.72\n19-59\nBMI\nMean ± SD\nRange \n24.92 ± 3.11\n20-30\nGravity\nMedian (IQR)\nRange \nNulligravida \n2 (1-3)\n0-5\n24 (12%)\nParity \nMedian (IQR)\nRange \nNullipara \n1 (1-2)\n0-5\n24 (12%)\nMarital status\nUnmarried\nMarried \n47 (23.5%)\n153 (76.5%)\nInfertility\nAbsent\nPresent  \nn = 153 (%)\n101 (66%)\n52 (34%)\nHistory of ovarian cyst removal\nAbsent\nPresent \n175 (87.5%)\n25 (12.5%)\nPrevious appendectomy\nAbsent\nPresent\n186 (93.0%)\n14 (7.0%)\nPrevious CS\nAbsent\nPresent\nn = 105\n85 (81.0%)\n20 (19.0%)\nHistory of uterine surgery within 15 days\nAbsent\nPresent\n190 (95%)\n10 (5%)\nHistory of IVF\nAbsent\nPresent\n191 (95.5%)\n9 (4.5%)\nHistory of PID\nAbsent\nPresent\n185 (92.5%)\n15 (7.5%)\nSpontaneous rupture of OE cyst\nAbsent\nPresent\n187 (93.5%)\n13 (6.5%)\nMenstrual irregularities\nAbsent\nPresent\n185 (92.5%)\n15 (7.5%)\nLower UTI\nAbsent\nPresent\n188 (94%)\n12 (6%)\nDM\nAbsent\nPresent\n188 (94%)\n12 (6%)\nHypertension\nAbsent\nPresent\n190 (95%)\n10 (5%)\n\n199\nTubo‑ovarian abscess in patients with ovarian endometrios Ahmed Mahmoud Abdou, Ahmed M. Fahmy, Ola A. Harb, Abdel‑Razik El‑Sayed Abdel‑Razik\nrespectively. Concerning past history, 7%, 5%, 4.5%, \n7.5%, 6.5%, 7.5% and 6% had history of previous \nappendectomy, uterine surgery within previous 15 \ndays, IVF, PID, spontaneous rupture of OE, men-\nstrual irregularities, and lower UTI (Table 2).\nThere is statistically non-significant relation be-\ntween combined OE and TOA and either age of \npatients, BMI, gravity, parity, marital status, ec-\ntopic pregnancy, surgical history, past history of \nremoval of OE cysts, previous appendectomy, \nprevious caesarean delivery or previous uterine \ncavity surgery.\nThere is statistically significant relation between \noccurrence of combined OE and TOA and spon-\ntaneous rupture of ovarian cyst (p = 0.26), history \nof PID (p = 0.26) and presence of DM (p = 0.32). \nSpontaneous rupture of ovarian cyst and history \nof PID are significantly associated with combined \nOE and TOA. \nThere is statistically non-significant relation be-\ntween combined OE and TOA and either infertility, \nprevious CS, menstrual irregularities, hypertension, \nhistory of ovarian cyst removal, previous appendec-\ntomy, history of uterine surgery (Table 3).\nThe number of patients in the first group (OE-\nTOAs) using IUDs was more than that in the oth-\ner group (OE) only without TOAs (p = 0.042). \nLower genital tract infections were diagnosed in \n8 (66.7%) of patients in the first group (OE-TOAs) \nand were diagnosed in only 4 (33.3%) patients \nwith OE without TOAs (p = 0.042). \nIn multivariate analysis we showed that the most \nsignificant predictive risk factors for OE-TOAs are \ninfections in the lower genital tract, OE cysts spon-\ntaneous rupture and concomitant DM.\nTreatment options include hysterectomy in addi-\ntion to adnexectomy through laparotomy was per-\nformed for all post-menopausal patients and for \nsome patients older than 40 years. Adnexectomy \nwithout total hysterectomy or ovarian cystectomy \nwas performed in the remaining patients (68.6%) \nthrough laparoscopy (17.8%) or laparotomy (0.8%). \nBinary logistic regression analysis of factors associ-\nated with combined OE+TAH among the studied \npatients (Table 4).\nHistory of spontaneous rupture of OE cyst and PID \nindependently increased risk of TAH+ OE by 2.819 \nand 2.547 folds, respectively\nDISCUSSION\nOE is a relatively common gynaecological disor -\nder, but OE complicated by formation of secondary \nTOAs is relatively uncommon pathological finding \nthat was reported to range from 2.15% in 1981 to \n2.3% in 1997 [17, 18]. Of the 5,595 patients with OE \nin this study, 44 (0.79%) were diagnosed with OE-\nTOA. The incidence in Gao et al. [2] was markedly \nlower than that was reported in previous studies. \nDespite rarity of such disorder, it is considered a \nserious and even fatal disease sometimes fatal [1].\nWith advancement in using broad-spectrum antibi-\notics therapy, TOAs incidence and fatality decreased \nbut about 12.5-35% of females complained of PID \nwere still in a need for surgical intervention [19].\nTable 2. Relation between occurrence of combined OE and TOA and demographic data.\nParameter Total\nn = 200\nGroup Test\nOE+non-TOA OE+TOA\nt p\nn = 120 (%) n = 80 (%)\nAge\nMean ± SD\nRange \n41.4 ± 7.72\n19-59\n40.34 ± 7.38\n40-59\n42.24 ± 8.11\n19-43\n-1.117 0.089\nBMI\nMean ± SD\nRange \n24.91 ± 3.11\n20-30\n24.92 ± 3.14\n20-30\n24.91 ± 3.08\n20-30\n0.009 0.993\nGravity\nMedian (IQR)\nRange \n2 (1-3)\n0-5\n2 (1-3)\n0-5\n2 (1-3)\n0-5\n-0.109¥ 0.913\nParity \nMedian (IQR)\nRange \n1 (1-2)\n0-5\n1 (1-2)\n0-5\n1 (1-2)\n0-5\n-0.093¥ 0.926\nMarital status\nUnmarried\nMarried \n47 (23.5%)\n153 (76.5%)\n32 (68.1%)\n88 (57.5%)\n15 (31.9%)\n65 (42.5%)\n1.673∞ 0.196\n¥Mann Whitney test; t: independent ample t-test; ∞ chi square test.\n\nItal J Gynaecol Obstet  2023, 35, N.2\n200\nTubo‑ovarian abscess in patients with ovarian endometrios\nIt was found that patients with OE are more sus-\nceptible to TOA [18]. According to recent reports, \nendometriosis was found to be a risk factor for \nTOAs occurrences [20, 21].\nIt was hypothesized that the initiating factor in \nTOA formation is invasion of the epithelium of \nfallopian tube by an organism that damaged the \ntissues causing necrosis thus abscess formation. \nThere are several incriminated risk factors for \nTOAs other than OE as the sexual habits, old age \nand lower immunity [20, 21].\nMechanisms of occurrence of TOAs due to OE are: \n1) OE is considered an immunodeficiency condi-\ntion which impairs the ability of the immune sys-\ntem to remove and overcome infections, thus leads \nto TOA; 2) the capsule of endometriotic ovarian \nTable 3. Relation between occurrence of combined OE and TOA and both medical and clinical characteristics.\nParameter Total\nn = 200\nGroup Test\nOE+non-TOA OE+TOA\nt p\nn = 120 (%) n = 80 (%)\nInfertility\n    Absent\n    Present  \nn = 153 (%)\n101 (66%)\n52 (34%)\n56 (55.4%)\n32 (61.5%)\n45 (44.6%)\n20 (38.5%)\n0.522∞ 0.47\nHistory of ovarian cyst removal\n    Absent\n    Present \n175 (87.5%)\n25 (12.5%)\n109 (62.3%)\n11 (44.0%)\n66 (37.7%)\n14 (56.0%)\n3.048∞ 0.081\nPrevious appendicectomy\n    Absent\n    Present\n186 (93.0%)\n14 (7.0%)\n112 (60.2%)\n8 (57.1%)\n74 (39.8%)\n6 (42.9%)\n0.051∞ 0.821\nPrevious CS\n    Absent\n    Present\nn = 105\n85 (81.0%)\n20 (19.0%)\n51 (60.0%)\n8 (40.0%)\n32 (40.0%)\n12 (60.0%)\n2.631∞ 0.105\nHistory of uterine surgery\n    Absent\n    Present\n190 (95%)\n10 (5%)\n115 (60.5%)\n5 (50.0%)\n75 (39.5%)\n5 (%50.0%)\n0.439∞ 0.508\nHistory of IVF\n    Absent\n    Present\n191 (95.5%)\n9 (4.5%)\n117 (61.3%)\n3 (33.3%)\n74 (38.7%)\n6 (66.7%)\nFisher∞ 0.19\nHistory of PID\n    Absent\n    Present\n185 (92.5%)\n15 (7.5%)\n115 (62.2%)\n5 (33.3%)\n70 (37.8%)\n10 (66.7%)\n4.805∞ 0.028*\nSpontaneous rupture\n    Absent\n    Present\n187 (93.5%)\n13 (6.5%)\n116 (62.0%)\n4 (30.8%)\n71 (38.0%)\n9 (69.2%)\n4.95∞ 0.026*\nMenstrual irregularities\n    Absent\n    Present\n185 (92.5%)\n15 (7.5%)\n113 (61.1%)\n7 (46.7%)\n72 (38.9%)\n8 (53.3%)\n1.201∞ 0.273\nLower UTI\n    Absent\n    Present\n188 (94%)\n12 (6%)\n116 (61.7%)\n4 (33.3%)\n72 (38.3%)\n8 (66.7%)\n3.783∞ 0.042\nDM\n    Absent\n    Present\n188 (94%)\n12 (6%)\n116 (61.7%)\n4 (33.3%)\n72 (38.3%)\n8 (66.7%)\n3.783∞ 0.032\nHypertension\n    Absent\n    Present\n190 (95%)\n10 (5%)\n115 (70.5%)\n5 (50%)\n75 (39.5%)\n5 (50%)\n0.439∞ 0.508\n¥Mann Whitney test; t: independent ample t-test; ∞ chi square test; *p < 0.05 is statistically significant.\nTable 4. Binary logistic regression analysis of factors associated with combined OE+TAH among the studied patients.\nβ Wald p AOR\n95%CI\nLower Upper\nSpontaneous rupture of cyst 1.037 2.567 0.109 2.819 0.793 10.018\nPrevious history of PID 0.935 2.47 0.116 2.547 0.794 8.175\nAOR: adjusted odds ratio; CI: confidence interval.\n\n201\nTubo‑ovarian abscess in patients with ovarian endometrios Ahmed Mahmoud Abdou, Ahmed M. Fahmy, Ola A. Harb, Abdel‑Razik El‑Sayed Abdel‑Razik\ncyst is thin which allow easy penetration of the \nbacteria; 3) blood content of the OE is a perfect me-\ndia for bacterial invasion and growth [22]; 4) the \n“bacterial contamination hypothesis” which states \nthat occurrence of intrauterine bacterial coloniza-\ntion is higher in females with endometriosis [23]. \nGao et al. [2] observed an increase in risk factors of \nOE-TOA after lower genital tract infection due to \nimpairment in the cervical mucosal barrier during \ninfection, so infection could easily spread to oth-\ner pelvic organs as tubes and ovaries which is a \nclassic spread pattern [24]. It was found that the \ncommonest incriminated organism for TOA was \nNeisseria gonorrhoeae in addition to Chlamydia tra-\nchomatis [25, 26]. Recent study demonstrated that \nEnterobacteriaceae and Streptococcus are the most \nfrequently detected organisms in TOAs-OE [27]. \nWe showed in the present study that detection \nrate of lower genital tract microbial infection in the \nlower genital tract was higher in the cases than in \ncontrols; additionally, the most detected organisms \nwere Escherichia coli (50%), Mycoplasma genitalium \n(21.4%) and Gardnerella vaginalis (21.4%). These re-\nsults were in line with results of Gao et al. [2], con-\nfirming the need to a prompt evaluation, diagnosis \nand treatment of these infections with suitable an-\ntibiotics before occurrence of ascending infections.\nWe showed that rupture of endometriotic ovarian \ncyst was incriminated in increasing risks of OE-\nTOA and incidence of TOAs was more common \nin females with ruptured endometriotic cysts that \nfemales without rupture which was similar to \nresults of Gao et al. [2], but the exact mechanism \nwas not clarified yet. \nPossible explanations were previously demon-\nstrated, as that the wall of the endometriotic cyst \ncould easily rupture due bleeding inside it during \nmenstruation, which increased intra-cystic pres-\nsure [28]. Additionally, after rupture of the cyst, \npouring chocolate like material inside the abdom-\ninal cavity lead to peritonitis and abscess later on, \nmoreover, cystic blood content is a suitable medi-\num for flourishing bacterial infections [29].\nIf there was prompt initiation of treatment this will \nprogress to more severe infections and TOAs.\nOnce clinical diagnosis of OE-TOA is established \nearly surgical intervention by drainage in addition \nto intravenous antibiotics is needed [30]. \nTOAs were found to be a rare disease in postmeno-\npausal females in comparison with females in the \nreproductive period [2]. It was previously found \nthat incidence of TOAs in postmenopausal females \nranged from 12% and 18% by researchers previ-\nously and was similar to our study (17.8%) [30, 31]. \nWe showed that roles of endometriosis in causing \nTOAs were not only restricted to females in the re-\nproductive period, but were found in post-meno-\npausal females. Similarly results of Gao et al. [2], \nwhich could be explained by considering that en-\ndometriosis is a disease of dysregulation of both \nthe endocrine and immune systems [32, 33]. \nPoints of strengths of the study\nIn the present prospective study, we highlighted \nthe fact that suspecting TOAs showed be done \nin any case of OE which allowed early and better \nmanagement for detected cases.\nLimitations of the study include inclusion of a rel-\natively few patient number due to performing the \nstudy in a single centre.\nCONCLUSIONS\nIn the present study we showed an association \nbetween OE and TOAs in both females in the re-\nproductive period and post-menopausal females, \nand we found that predictive risk factors of OE-\nTOA were rupture of ovarian endometriotic cysts \nspontaneously, in addition to lower genital tract \ninfections, low immunity and neglected pelvic in-\nflammatory diseases. \nWe recommend giving prophylactic broad spec-\ntrum antibiotics to high risk and suspected pa-\ntients to decrease rate of occurrence and complica-\ntions of OE-TOA and improve patients prognosis. \nAdditionally, we advise performing dramatic ap-\npropriate surgical drainage of diagnosed abscess.\nCOMPLIANCE WITH ETHICAL STANDARDS\nAuthors contribution\nA.M.A.: Conceptualization, data curation. A.M.F.: \nProject administration, resources, software, super-\nvision. O.H.: Validation, visualization, writing – \noriginal draft, writing – review & editing. A.E.A.: \nFormal analysis, investigation, methodology, con-\nceptualization, data curation, funding acquisition, \nproject administration, resources, software, super-\nvision, validation, visualization, writing – original \ndraft, writing – review & editing.\n\nItal J Gynaecol Obstet  2023, 35, N.2\n202\nTubo‑ovarian abscess in patients with ovarian endometrios\nFunding\nNone.\nStudy registration\nZag 101998.\nDisclosure of interests\nthe authors declare that they have no conflict of in-\nterests.\nEthical approval \nIt was obtained from local ethical committee of \nFaculty of Medicine Zagazig University.\nInformed consent\nA written informed consent was obtained from all \nparticipants in the study.\nData sharing\nData are available under reasonable request to the \ncorresponding author.\nREFERENCES\n1. Tasa EE, Keskinb HL, Akcay GF, Ismayilovab U, \nYavuza AF.  Association Between Endometrio-\nsis and Tubo-Ovarian Abscess J Clin Gynecol \nObstet. 2016;5(1):17-22. doi: 10.14740/jcgo388w\n2. Gao Y, Qu P , Zhou Y, Ding W. Risk factors for the \ndevelopment of tubo-ovarian abscesses in wom-\nen with ovarian endometriosis: a retrospective \nmatched case-control study. BMC Womens Health. \n2021;21(1):43. doi: 10.1186/s12905-021-01188-6.\n3. Brunham RC, Gottlieb SL, Paavonen J. Pelvic in-\nflammatory disease. N Engl J Med. 2015;372:2039–\n48. DOI: 10.1056/NEJMra1411426.\n4. Grammatikakis I, Evangelinakis N, Salamalekis \nG, Tziortzioti V , Samaras C, Chrelias C, et al. \nPrevalence of severe pelvic inflammatory dis-\nease and endometriotic ovarian cysts: a 7-year \nretrospective study. Clin Exp Obstet Gynecol. \n2009;36(4):235-6. Available at: https://pubmed.\nncbi.nlm.nih.gov/20101855/.\n5. Candiani M, Canis M, Giambelli E, Natale A, \nBaraldini V , Busacca M, et al. Laparoscopic \nmanagement of pelvic pain and adnexal masses \nin adolescent and paediatric patients. Ital J Gy-\nnaecol Obstet. 1997;9(2);82-6.\n6. Scheerer C, Bauer P , Chiantera V , Sehouli J, \nKaufmann A, Mechsner S. Characterization \nof endometriosis-associated immune cell in-\nfiltrates (EMaICI). Arch Gynecol Obstet. 2016 \n;294(3):657-64. doi: 10.1007/s00404-016-4142-6.\n7. Garavaglia E, Ricci E, Cioffi R, Trojano G, Bul-\nfoni A, Parazzini F, et al.  Smoking habits and en-\ndometriosis risk among infertile women: Results \nfrom a case control study. Ital J Gynaecol Obstet. \n2017;29(3):15-8. doi: 10.14660/2385-0868-72.\n8. To J, Aldape D, Frost A, Goldberg GL, Levie M, \nChudnoff S. Image-guided drainage versus antibiot-\nic-only treatment of pelvic abscesses: short-term and \nlong-term outcomes. Fertil Steril. 2014;102(4):1155-\n9. doi: 10.1016/j.fertnstert.2014.06.025.\n9. Laganà AS, Salmeri FM, Frangež HB, Ghez-\nzi  F, Vrtačnik-Bokal E, Granese R. Evaluation \nof M1 and M2 macrophages in ovarian en-\ndometriomas from women affected by endo-\nmetriosis at different stages of the disease. \nGynecol Endocrinol. 2020;36(5):441-4. doi: \n10.1080/09513590.2019.1683821.\n10. Ross J, Guaschino S, Cusini M, Jensen J. 2017 \nEuropean guideline for the management of \npelvic inflammatory disease. Int J STD AIDS. \n2018;29(2):108-14. doi: 10.1177/0956462417744099.\n11. Brun JL, Graesslin O, Fauconnier A, Verdon R, \nAgostini A, Bourret A, et al. Updated French \nguidelines for diagnosis and management of pel-\nvic inflammatory disease. Int J Gynaecol Obstet. \n2016;134(2):121-5. doi: 10.1016/j.ijgo.2015.11.028.\n12. Fouks Y, Cohen Y, Tulandi T, Meiri A, Levin I, \nAlmog B, et al. Complicated Clinical Course and \nPoor Reproductive Outcomes of Women with \nTubo-Ovarian Abscess after Fertility Treatments. \nJ Minim Invasive Gynecol. 2019;26(1):162-8. doi: \n10.1016/j.jmig.2018.06.004.\n13. Hosseini E, Nikmard F, Aflatoonian B, Vesali S, \nAlenabi T, Aflatoonian A, et al. Controlled ovar-\nian stimulation in endometriosis patients can be \nindividualized by anti-müllerian hormone lev-\nels. Acta Endocrinol (Buchar). 2017;13(2):195-\n202. doi: 10.4183/aeb.2017.195.\n14. De Arellano ML, Arnold J, Sacher F, Blöchle M, \nStaube M, Bartley J, et al. Eutopic endometri-\num from women with endometriosis does not \nexhibit neurotrophic properties. J Neuroimmu -\nnol. 2012;249(1-2):49-55. doi: 10.1016/j.jneuro-\nim.2012.04.020.\n\n203\nTubo‑ovarian abscess in patients with ovarian endometrios Ahmed Mahmoud Abdou, Ahmed M. Fahmy, Ola A. Harb, Abdel‑Razik El‑Sayed Abdel‑Razik\n15. Raffaelli R, Garzon S, Baggio S, Genna M, Pomi-\nni P , Laganà AS, et al. Mesenteric vascular and \nnerve sparing surgery in laparoscopic segmen-\ntal intestinal resection for deep infiltrating en-\ndometriosis. Eur J Obstet Gynecol Reprod Biol. \n2018;231:214-9. doi: 10.1016/j.ejogrb.2018.10.057.\n16. Walker CK, Wiesenfeld HC. Antibiotic therapy for \nacute pelvic inflammatory disease: the 2006 Centers \nfor Disease Control and Prevention sexually trans-\nmitted diseases treatment guidelines. Clin Infect \nDis. 2007;44(Suppl 3):S111-22. doi: 10.1086/511424.\n17. Schmidt CL, Demopoulos RI, Weiss G. Infect-\ned endometriotic cysts: clinical characterization \nand pathogenesis. Fertil Steril. 1981;36(1):27-30. \ndoi: 10.1016/s0015-0282(16)45613-x.\n18. Kubota T, Ishi K, Takeuchi H. A study of tu-\nbo-ovarian and ovarian abscesses, with a focus \non cases with endometrioma. J Obstet Gynae-\ncol Res. 1997;23(5):421-6. doi: 10.1111/j.1447-\n0756.1997.tb00867.x.\n19. Tasa EE, Keskinb HL, Feykan G,  Akcayb Y, Ismay-\nilova U, Yavuza AF. Association Between Endome-\ntriosis and Tubo-Ovarian Abscess. J Clin Gynecol \nObstet. 2016;5(1):17-22. doi: 10.14740/jcgo388w.\n20. Lareau SM, Beigi RH. Pelvic inflammatory dis-\nease and tubo-ovarian abscess. Infect Dis Clin \nNorth Am. 2008;22(4):693-708. doi: 10.1016/j.\nidc.2008.05.008.\n21. Chen MJ, Yang JH, Yang YS, Ho HN. Increased \noccurrence of tubo-ovarian abscesses in wom-\nen with stage III and IV endometriosis. Fertil \nSteril. 2004;82(2):498-9. doi: 10.1016/j.fertn-\nstert.2004.01.032.\n22. Vichinsartvichai P . Bilateral tubo-ovarian ab-\nscesses presenting with huge pelvic mass after \nrepeated intrauterine inseminations in a woman \nwith severe endometriosis. J Obstet Gynaecol \nRes. 2018;44(4):792-6. doi: 1 0.1111/jog.13570.\n23. Khan KN, Fujishita A, Hiraki K, Kitajima M, Na-\nkashima M, Fushiki S, Kitawaki J. Bacterial con-\ntamination hypothesis: a new concept in endo-\nmetriosis. Reprod Med Biol. 2018;17(2):125-33. \ndoi: 10.1002/rmb2.12083.\n24. Tai FW, Chang CY, Chiang JH, Lin WC, Wan \nL. Association of Pelvic Inflammatory Disease \nwith Risk of Endometriosis: A Nationwide Co-\nhort Study Involving 141,460 Individuals. J Clin \nMed. 2018;7(11):379. doi: 10.3390/jcm7110379.\n25. Bevan CD, Johal BJ, Mumtaz G, Ridgway GL, \nSiddle NC. Clinical, laparoscopic and micro-\nbiological findings in acute salpingitis: report \non a United Kingdom cohort. Br J Obstet Gy-\nnaecol. 1995;102(5):407-14. doi: 10.1111/j.1471-\n0528.1995.tb11294.x.\n26. Cohen CR, Mugo NR, Astete SG, Odondo R, Man-\nhart LE, Kiehlbauch JA, et al. Detection of Myco-\nplasma genitalium in women with laparoscopical-\nly diagnosed acute salpingitis. Sex Transm Infect. \n2005;81(6):463-6. doi: 10.1136/sti.2005.015701. \n27. Akiyama K, Nishioka K, Khan KN, Tanaka Y, Mori \nT, Nakaya T, et al. Molecular detection of microbi-\nal colonization in cervical mucus of women with \nand without endometriosis. Am J Reprod Immu-\nnol. 2019;82(2):e13147. doi: 10.1111/aji.13147.\n28. Brosens IA. Endometriosis--a disease because \nit is characterized by bleeding. Am J Obstet \nGynecol. 1997;176(2):263-7. doi: 10.1016/s0002-\n9378(97)70482-4.\n29. Lipscomb GH, Ling FW, Photopulos GJ. Ovarian \nabscess arising within an endometrioma. Obstet \nGynecol. 1991 Nov;78(5 Pt 2):951-4. Available at: \nhttps://pubmed.ncbi.nlm.nih.gov/1923238/.\n30. Villette C, Bourret A, Santulli P , Gayet V , \nChapron C, de Ziegler D. Risks of tubo-ovarian \nabscess in cases of endometrioma and assisted \nreproductive technologies are both under- and \noverreported. Fertil Steril. 2016;106(2):410-5. doi: \n10.1016/j.fertnstert.2016.04.014.\n31. Protopapas AG, Diakomanolis ES, Milingos SD, \nRodolakis AJ, Markaki SN, Vlachos GD, et al. Tu-\nbo-ovarian abscesses in postmenopausal women: \ngynecological malignancy until proven otherwise? \nEur J Obstet Gynecol Reprod Biol. 2004;114(2):203-\n9. doi: 10.1016/j.ejogrb.2003.10.032.\n32. Hsiao SM, Hsieh FJ, Lien YR. Tuboovarian ab-\nscesses in postmenopausal women. Taiwan J \nObstet Gynecol. 2006;45(3):234-8. doi: 10.1016/\nS1028-4559(09)60231-X.\n33. Kralickova M, Vetvicka V . Immunological aspects of  \nendometriosis: a review. Ann Transl Med. \n2015;3(11):153. doi: 10.3978/j.issn.2305-5839. \n2015.06.08.","source_license":"CC0","license_restricted":false}