{"paper_id":"9b15c2be-5339-42c9-b2ca-2e1fea2b6b8d","body_text":"Review began\n 03/29/2024 \nReview ended\n 04/08/2024 \nPublished\n 04/11/2024\n© Copyright \n2024\nMatalliotakis 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.\nCo-existence of Ovarian Teratomas With Other\nGynecological Tumors\nMichail \nMatalliotakis \n, \nCharoula Matalliotaki \n, \nIoannis \nTsakiridis \n, \nThemistoklis \nDagklis \n,\nGeorgios Michos \n, \nAndreas Romanos \n, \nKonstantinos Krithinakis \n, \nIoannis A. Kalogiannidis \n1.\n Obstetrics and Gynecology, Venizeleio General Hospital, Heraklion, GRC \n2.\n Third Department of Obstetrics and\nGynecology, Aristotle University of Thessaloniki, Thessaloniki, GRC\nCorresponding author: \nMichail \nMatalliotakis, \nmihalismat@hotmail.com\nAbstract\nIntroduction: This study aims to investigate the co-existence of ovarian teratomas with other benign or\nmalignant gynecological tumors in women who underwent gynecological surgery.\nMethods: We retrospectively reviewed all women who underwent gynecological surgery over a 15-year\nperiod. Pre-operative, surgical, and histological records were obtained from women who presented with\ngynecological pathology, aiming to discover a possible link between ovarian teratomas and other\ngynecological tumors.\nResults: Of the total patient sample, 288 (8.2%) had a mature teratoma, and 9 (0.3%) had an immature\nteratoma. The mean age was 38.0±13.3 years and 30.9±11.1 years, respectively. Women with mature\nteratoma showed a positive correlation with struma ovarii (SO, p=0.001). Moreover, we reported a positive\nlinear relationship between struma ovarri and thecoma. Of the 288 women with a mature teratoma, 1 (0.3%)\nhad co-existent endometrioid ovarian cancer, and 1 (0.3%) had borderline cancer. There were 14 women\n(4.9%) with a co-existent serous cystadenoma, 7 (2.4%) with a mucin cystadenoma, 1 (0.3%) with a thecoma,\n4 (1.4%) with struma ovarii, 3 (1.0%) had Brenner cyst, 3 (1.0%) had ovarian fibroma, 2 had endometriosis\n(0.7%), and 8 (2.8%) had endometriomas. Of a total of nine women with immature teratomas, one (11.1%)\nhad a serous cystadenoma.\nConclusions: Ovarian teratomas may co-exist with other gynecological diseases. Our study reports various\ncases of the co-existence of several gynecological tumors with teratomas.\nCategories:\n Obstetrics/Gynecology, Oncology\nKeywords:\n cancer, benign gynecological disease, ovarian mass, immature teratoma, benign mature cystic teratoma\nIntroduction\nOvarian teratomas are germ cell tumors (GCTs) of the ovaries that are characterized by three subtypes,\nincluding mature teratoma (dermoid cyst), immature teratoma, and monodermal teratoma.\nMature teratoma constitutes the most common subtype of GCTs, with an incidence of about 1.2-14.2 cases\nper 100,000 people yearly. It accounts for about 95% of teratomas and 10% of all ovarian tumors. Even\nthough they are benign, rarely in older women, there is a risk of malignant transformation (between 0.5%\nand 3%) \n[1]\n. Immature teratoma, mostly seen in younger ages, represents a rare entity and accounts for less\nthan 1% of ovarian cancers. Due to its rarity, the incidence varies, but it signifies 10% of GCTs, 36% of GCTs\nin young adults, and about half of malignant GCTs \n[2]\n. The least frequent subtype, monodermal ovarian\nteratoma, includes mainly struma ovarii (SO) that are benign, although there is a risk of 5-10% for\nmalignancy \n[3]\n.\nClinically, patients with ovarian teratomas can be asymptomatic or manifest pelvic pain or discomfort upon\nexamination, which may present as a complication due to torsion, rupture, or a complicated peritoneal\ninfection. These overlapping symptoms can also be a manifestation of other concomitant gynecologic\nconditions that can be detected by sonographic imaging, CT scan, or MRI; however, the diagnosis is\nconfirmed by histology \n[1,2,4,5,6,7]\n.\nThe purpose of our study was to evaluate a possible clinically important coexistence between mature and\nimmature ovarian teratomas and other benign and malignant gynecological conditions in a large number of\nwomen who underwent gynecological surgery.\nMaterials And Methods\nThis retrospective study was carried out at the Department of Obstetrics and Gynecology at Venizeleio\nGeneral Hospital of Heraklion, Crete, and the Third Department of Obstetrics and Gynecology at Aristotle\n1\n1\n2\n2\n2\n2\n1\n2\n \n Open Access Original\nArticle\n \nDOI:\n 10.7759/cureus.58068\nHow to cite this article\nMatalliotakis M, Matalliotaki C, Tsakiridis I, et al. (April 11, 2024) Co-existence of Ovarian Teratomas With Other Gynecological Tumors. Cureus\n16(4): e58068. \nDOI 10.7759/cureus.58068\n\nUniversity of Thessaloniki. All women who underwent gynecologic surgery from 2005 to 2020, such as total\nabdominal hysterectomy (TAH) with or without unilateral (USO) or bilateral salpingo-oophorectomy (BSO),\nhysteroscopy, and/or dilation and curettage, were eligible to participate in the study.\nClinical, preoperative, surgical, and pathological records were obtained from 3490 women who presented\nwith one or more gynecological conditions. The aim was to discover a possible link between mature and\nimmature teratomas and other gynecological pathologies. Gynecological conditions included cysts,\ncystadenomas, endometriomas, endometriosis, fibroids, and ovarian malignancies.\nAll demographic and histological data were retrieved from the medical records. We excluded cases with\ninadequate medical records and those lacking histological diagnoses. The Ethics Committee of both\ndepartments approved the study protocol (no. 124/17/2019, no. 94/23-4-20).\nStatistical analysis\nStatistical analyses were performed using SPSS software version 25 (SPSS, Inc., Chicago, USA). Descriptive\nstatistics were used to calculate the mean, average, and standard deviation of all the data. Values were\nconsidered statistically significant at p<0.05. The results are reported as mean ± SD or as percentages, where\nappropriate. Graphs were generated using GraphPad Prism (GraphPad Software, La Jolla, CA).\nResults\nOf a total series of 3490 cases, 288 (8.20%) had mature teratoma, and 9 (0.30%) had immature teratoma, with\na mean age of 38.0±13.3 years (range 15-81 years; Figure \n1\n) and 30.9±11.1 years (range 17-54 years),\nrespectively.\nFIGURE\n 1: Age distribution in women with mature teratoma.\nOf the 288 cases with mature teratoma, 11 (3.8%) were isolated findings, whereas in 96.2%, there was\nadditional gynecological pathology. Of the 288 women with mature teratoma, 1 had ovarian cancer (0.3%),\nspecifically endometrioid, 1 (0.3%) had borderline cancer, 14 women (4.9%) had serous cystadenoma, 7\n(2.4%) had mucin cystadenoma, 1 (0.3%) had thecoma, 4 (1.4%) had struma ovarii, 3 (1.0%) had Brenner cyst,\n3 (1.0%) had ovarian fibroma, 2 had endometriosis (0.7%), and 8 (2.8%) had endometriomas. Of a total of\nnine women with immature teratomas, one (11.1%) had serous cystadenoma (Figures \n2\n-\n3\n).\n2024 Matalliotakis et al. Cureus 16(4): e58068. DOI 10.7759/cureus.58068\n2\n of \n7\n\nFIGURE\n 2: Most common gynecological conditions detected in the\nwhole sample of teratomas.\nTotal = 42. The total number of gynecological conditions co-existed with teratomas.\nFIGURE\n 3: Coexistence of teratomas with various benign, borderline,\nand malignant ovarian masses.\nWomen with mature teratomas showed a positive correlation with struma ovarii (p=0.001). A negative linear\nrelationship was noticed with the presence of serous cystadenoma (p=0.002), paraovarian cyst (p=0.001),\nmorgani cyst (p=0.010), and endometrioma (p<0.001). A negative correlation was also noticed regarding\ncervical and endometrial cancer (p<0.001), endometrial hyperplasia with and without atypia (p=0.013 and\np=0.007, respectively), fibroids (p<0.001), endometriosis (p=0.002), and adenomyosis (p<0.001). No\ncorrelation was noticed with either ovarian cancer (p=0.106) or ovarian tumors of borderline malignancy\n(p=0.463). Immature teratomas did not show a significant correlation coefficient. Upon further examination\nof the data regarding struma ovarii, in the total sample of 3490 women, 12 cases were identified with a mean\nage of 50.4±17.7 years (range 26-69 years). Pearson’s correlation coefficient revealed a positive linear\nrelationship with thecoma (p=0.001).\nDiscussion\nAlthough various reports have been published on ovarian teratomas, this large study investigated a possible\nnoteworthy co-existence between 297 cases of ovarian teratomas and several benign, premalignant, or\nmalignant gynecological diseases in women who have undergone surgery due to a gynecological condition.\n2024 Matalliotakis et al. Cureus 16(4): e58068. DOI 10.7759/cureus.58068\n3\n of \n7\n\nEven though various theories have been linked to the pathogenesis of teratomas, the germ cell theory is\nwidely accepted due to the anatomic distribution of the tumors and the fact that the tumor occurs during the\nreproductive years. Although the exact pathogenesis of ovarian teratomas is still obscure, they are believed\nto develop due to faulty meiosis type II in totipotent germ cells. Rarely, triploidy, trisomy, and mosaicism\nhave been detected in ovarian teratomas; however, most of them have a normal 46, XX karyotype \n[3]\n.\nMature teratomas present mostly as unilocular cysts, localized unilaterally with a variable size, characterized\nby a well-defined capsule. They can originate from ectoderm, mesoderm, or endodermal layers and can\ncomprise hair, skin, sebaceous substances, and neural tissue. According to Peterson et al. and Whitecar et al.,\nthey appear mainly in the reproductive years and account for 30% of adnexal masses diagnosed during\npregnancy \n[8,9]\n.\nImmature teratomas tend to be moderately larger than mature teratomas and are typically detected in\nadolescence. They are mostly solid with a non-well-defined capsule and differ from mature teratomas in the\npresence of embryonic elements, frequently primitive neuroepithelium. They are histologically graded\ndepending on the neural elements, and this grading indicates a prognostic survival factor \n[3]\n.\nTeratomas represent around 11% of all ovarian masses in the literature, with mature teratomas accounting\nfor 95% of all teratomas \n[1]\n. Our findings are similar, with teratomas accounting for 8.60% of all ovarian\nmasses and mature teratomas for 96.9% of all teratomas. Ovarian teratomas are usually present in\nadolescent and premenarchal girls or are incidentally diagnosed later in life during imaging for other\nindications, with similar age groups in appearance for both mature and immature teratomas \n[10,11]\n. In our\nstudy, mature teratomas showed a mean age of 38.0±13.3 years and immature teratomas 30.9±11.1 years.\nThis trend towards the higher age margin can be explained by the study design, given that the participants\nwere women undergoing a surgical procedure that has specific indications when concerning children or\nadolescent patients \n[11,12]\n.\nRegarding the co-existence of mature teratomas and other benign gynecological conditions, few case\nreports of collision tumors exist in the literature. Pearson’s analysis of our sample corroborates this since it\nrevealed a negative linear relationship with most tumors. The most reported entity appears to be mucin\ncystadenoma, with seven cases \n[13-16]\n. Of our patients, seven had mucin cystadenoma and mature\nteratoma. Serous cystadenoma has also previously been reported in five cases \n[13,17-20]\n. Our data showed\nthat 14 women had serous cystadenoma and mature teratoma, while 1 woman had immature teratoma.\nFurther research is required to explore the pathway through which ovarian teratomas are negatively\nassociated with a number of benign and malignant gynecological pathologies. An interesting example of this\nwould be a previously confirmed left lateral anatomical distribution of endometriomas versus a right lateral\nanatomical distribution of ovarian teratomas \n[5]\n. Endometriosis is reported in six previously published\narticles with mature teratomas \n[21-26]\n. In our case, two women with mature teratomas also had\nendometriosis, and eight women had endometriomas.\nThecoma is the next most reported tumor, with three cases described by Morimitsu et al. and Emeka et al.\n[27,28]\n. One woman, in our case, had thecoma and mature teratoma. Also, Borges et al. report the co-\nexistence of a Brenner tumor, which was found in three women in our study \n[14]\n.\nAs far as the negative correlation of teratomas with fibroids is concerned, according to the literature,\nfibroids are fueled by gene mutations, whereas ovarian teratomas evolve through changes in gene\nexpression; thus, these two pathologies present distinct entities \n[29]\n.\nAccounting for the presence of malignant tumors with mature teratomas, 10 cases of ovarian carcinoma are\nreported, one case of adenomatoid tumor, and one case of fibrothecoma, which are occasionally malignant\n[13,30-40]\n. Of our patients, one had endometrioid cancer, and one had borderline cancer.\nMonodermal teratomas are well-differentiated unilateral neoplasms and have a predominance of a single\ntissue type that gives rise to a struma ovarii tumor, an ovarian carcinoid tumor, or an ovarian teratoma with\nneural differentiation \n[3]\n.\nStruma ovarii represents the most common type of monodermal teratoma. Upon macroscopical examination,\nthe tumor appears solid, solid-cystic, or cystic with a solid component. It appears mainly during\nperimenopause and comprises less than 1% of all ovarian tumors, 2% of GCTs, and about 3% of dermoid\ntumors. It appears as a unilateral mass of various sizes \n[41,42]\n.\nWell, of note, in 1889, Boetlin, in 1895 von Kahlden, and Gottschalk, almost 5 years later, were the first\nauthors who described SO as a rare ovarian mass that is histologically composed of thyroid tissue\noriginating from the ovarian follicles. SO is also called ovarian goiter since the proportion of thyroid tissue\noccupies more than half of the specimen, compared to mature cystic teratomas, where the thyroid tissue\ninvolved is less than 15%. SOs are mostly benign, with a risk of malignant transformation of less than 5%\n[43]\n. Usually, asymptomatic SO is found incidentally on the surgical specimen of a teratoma or upon clinical\n2024 Matalliotakis et al. Cureus 16(4): e58068. DOI 10.7759/cureus.58068\n4\n of \n7\n\nexamination and/or sonographic evaluation. Occasionally, larger masses may be complicated with ascites,\nwith or without pleural effusion (Pseudo-Meigs syndrome), which disappears after the operation. Rarely, a\nhormonally active SO is associated with thyrotoxicosis \n[41-43]\n. There are few case reports that report the\ncoexistence of mature teratomas and SO \n[44,45]\n. In our series, out of 288 cases with mature teratoma, we\nconfirmed the co-existence of mature teratoma and SO in four specimens. The results of Pearson’s\ncorrelation coefficient showed a positive correlation between women with mature teratoma and SO\n(p=0.001). Recently, in 2019, we investigated retrospectively the association between teratomas and\nendometriomas. In that study, we detected 14 cases of SO out of 172 women with dermoid cysts \n[5]\n.\nMoreover, according to the current literature, a small number of case reports and case series confirm the co-\nexistence of SO with other ovarian masses, such as mucinous or serous cystadenoma, Brenner tumor,\nthecoma, and ovarian fibroma \n[46-50]\n. In our total sample of 3490 women, we detected 12 cases of SO.\nPearson’s correlation coefficient revealed a positive linear relationship with thecoma (p=0.001).\nIn all ovarian teratomas, the optimal follow-up regime after excision will result in early evaluation of\nrecurrence or malignant transformation. Harada et al. retrospectively indicated that younger age, larger\ncysts, and bilateral occurrence of mature teratomas are prognostic factors for recurrence \n[51]\n.\nChiang et al. concluded that long-term follow-up is suggested for mature teratomas with a diagnosis of a\nlarger tumor or those with a tumor containing a solid component since there is a risk of malignant\ntransformation to squamous cell carcinoma \n[52]\n.\nThe retrospective nature of the study and the lack of follow-up denote its limitations. However, the large\nnumber of specimens and the histological confirmation of all cases present the strengths of our work.\nConclusions\nTeratomas, although rare, may co-exist with other ovarian tumors. Such a scenario poses a challenge to\nclinicians due to the difficulty of distinguishing them solely by imaging. This should raise awareness so that\nthe therapeutic approach is based on the masses with a higher risk of malignancy. Long-term follow-up of\novarian teratoma cases would help to validate and reinforce the research results. To the best of our\nknowledge, the present study is the first to report a significant number of cases of co-existence of various\ngynecological tumors with teratomas, almost doubling the number of existing reports in the literature.\nAdditional Information\nAuthor Contributions\nAll authors have reviewed the final version to be published and agreed to be accountable for all aspects of the\nwork.\nConcept and design:\n  \nMichail \nMatalliotakis, Andreas Romanos, Ioannis A. Kalogiannidis\nAcquisition, analysis, or interpretation of data:\n  \nMichail \nMatalliotakis, Charoula Matalliotaki, Ioannis\nTsakiridis, Themistoklis \nDagklis, Konstantinos Krithinakis, Ioannis A. Kalogiannidis, Georgios Michos\nDrafting of the manuscript:\n  \nMichail \nMatalliotakis, Charoula Matalliotaki, Konstantinos Krithinakis,\nIoannis A. Kalogiannidis\nCritical review of the manuscript for important intellectual content:\n  \nMichail \nMatalliotakis, Ioannis\nTsakiridis, Themistoklis \nDagklis, Andreas Romanos, Ioannis A. Kalogiannidis, Georgios Michos\nDisclosures\nHuman subjects:\n Consent was obtained or waived by all participants in this study. The Ethics Committee of\nDepartment of Obstetrics and Gynecology at Venizeleio General Hospital of Heraklion Crete and the Third\nDepartment of Obstetrics and Gynecology of Aristotle University of Thessaloniki issued approval\n124/17/2019 and 94/23-4-20. \nAnimal subjects:\n All authors have confirmed that this study did not involve\nanimal subjects or tissue. \nConflicts of interest:\n In compliance with the ICMJE uniform disclosure form, all\nauthors declare the following: \nPayment/services info:\n All authors have declared that no financial support\nwas received from any organization for the submitted work. \nFinancial relationships:\n All authors have\ndeclared that they have no financial relationships at present or within the previous three years with any\norganizations that might have an interest in the submitted work. \nOther relationships:\n All authors have\ndeclared that there are no other relationships or activities that could appear to have influenced the\nsubmitted work.\nAcknowledgements\nWe would like to thank all the clinicians and pathologists for providing the data used in this study.\n2024 Matalliotakis et al. 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Eur J Obstet Gynecol Reprod Biol. 2013, 171:325-8.\n10.1016/j.ejogrb.2013.09.004\n52\n. \nChiang AJ, Chen MY, Weng CS, et al.: \nMalignant transformation of ovarian mature cystic teratoma into\nsquamous cell carcinoma: a Taiwanese Gynecologic Oncology Group (TGOG) study\n. J Gynecol Oncol. 2017,\n28:e69. \n10.3802/jgo.2017.28.e69\n2024 Matalliotakis et al. Cureus 16(4): e58068. DOI 10.7759/cureus.58068\n7\n of \n7","source_license":"CC0","license_restricted":false}