{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T12:31:06Z","timestamp":1790857866229,"version":"4.1.0"},"reference-count":30,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2022,2,27]],"date-time":"2022-02-27T00:00:00Z","timestamp":1645920000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJERPH"],"abstract":"<jats:p>Endometriosis is a gynecological condition caused by the development of endometrial tissue outside the uterine cavity. Naturally, it commonly occurs at locations such as the ovaries and pelvic peritoneum. However, ectopic endometrial tissue may be discovered outside of the typical sites, suggesting the possibility of iatrogenic seeding after gynecological operations. Based on this hypothesis, we developed a study aiming to establish the root cause of atypical implantation of endometrial foci, as the main end point, and to determine diagnostic features and risk factors for this condition, as a secondary target. The research followed a retrospective design, including a total of 126 patients with endometriosis who met the inclusion criteria. A group of 71 patients with a history of c-section was compared with a control group of patients with endometriosis and no history of c-section. Endometriosis that developed inside or in close proximity to surgical incisions of asymptomatic patients before surgical intervention was defined as iatrogenic endometriosis. Compared with patients who did not have a c-section, the c-section group had significantly more minimally invasive pelvic procedures and multiple adhesions and endometriosis foci at intraoperative look (52.1% vs. 34.5%, respectively 52.1% vs. 29.1%). The most common location for endometriosis lesions in patients with prior c-section was the abdominal wall (42.2% vs. 5.4%), although the size of foci was significantly smaller by size and weight (32.2 mm vs. 34.8 mm, respectively 48.6 g vs. 53.1 g). The abdominal wall endometriosis was significantly associated with minimally invasive pelvic procedures (correlation coefficient = 0.469, p-value = 0.001) and c-section (correlation coefficient = 0.523, p-value = 0.001). A multivariate regression analysis identified prior c-section as an independent risk factor for abdominal wall endometriosis (OR = 1.85, p-value &lt; 0.001). We advocate for strict protocols to be implemented and followed during c-section and minimally invasive procedures involving the pelvic region to ensure minimum spillage of endometrial cells. Further research should be developed to determine the method of abdominal and surgical site irrigation that can significantly reduce the risk of implantation of viable endometrial cells. Understanding all details of iatrogenic endometriosis will lead to the development of non-invasive disease diagnosis and minimally invasive procedures that have the potential to reduce postoperative complications.<\/jats:p>","DOI":"10.3390\/ijerph19052791","type":"journal-article","created":{"date-parts":[[2022,2,27]],"date-time":"2022-02-27T20:47:17Z","timestamp":1645994837000},"page":"2791","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["Challenges in Diagnosis and Prevention of Iatrogenic Endometriosis as a Long-Term Surgical Complication after C-Section"],"prefix":"10.3390","volume":"19","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-4114-1582","authenticated-orcid":false,"given":"Radu","family":"Neamtu","sequence":"first","affiliation":[{"name":"Discipline of Obstetrics and Gynecology, \u201cVictor Babes\u201d University of Medicine and Pharmacy Timisoara, 300041 Timisoara, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"George","family":"Dahma","sequence":"additional","affiliation":[{"name":"Discipline of Obstetrics and Gynecology, \u201cVictor Babes\u201d University of Medicine and Pharmacy Timisoara, 300041 Timisoara, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adelina Geanina","family":"Mocanu","sequence":"additional","affiliation":[{"name":"Discipline of Obstetrics and Gynecology, \u201cVictor Babes\u201d University of Medicine and Pharmacy Timisoara, 300041 Timisoara, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elena","family":"Bernad","sequence":"additional","affiliation":[{"name":"Discipline of Obstetrics and Gynecology, \u201cVictor Babes\u201d University of Medicine and Pharmacy Timisoara, 300041 Timisoara, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carmen-Ioana","family":"Silaghi","sequence":"additional","affiliation":[{"name":"Discipline of Obstetrics and Gynecology, \u201cVictor Babes\u201d University of Medicine and Pharmacy Timisoara, 300041 Timisoara, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lavinia","family":"Stelea","sequence":"additional","affiliation":[{"name":"Discipline of Obstetrics and Gynecology, \u201cVictor Babes\u201d University of Medicine and Pharmacy Timisoara, 300041 Timisoara, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3730-6527","authenticated-orcid":false,"given":"Cosmin","family":"Citu","sequence":"additional","affiliation":[{"name":"Discipline of Obstetrics and Gynecology, \u201cVictor Babes\u201d University of Medicine and Pharmacy Timisoara, 300041 Timisoara, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5736-572X","authenticated-orcid":false,"given":"Amadeus","family":"Dobrescu","sequence":"additional","affiliation":[{"name":"Discipline of General Surgery, \u201cVictor Babes\u201d University of Medicine and Pharmacy Timisoara, 300041 Timisoara, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4711-4315","authenticated-orcid":false,"given":"Felix","family":"Bratosin","sequence":"additional","affiliation":[{"name":"Discipline of General Surgery, \u201cVictor Babes\u201d University of Medicine and Pharmacy Timisoara, 300041 Timisoara, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mirela Loredana","family":"Grigoras","sequence":"additional","affiliation":[{"name":"Discipline of Anatomy and Embryology, \u201cVictor Babes\u201d University of Medicine and Pharmacy Timisoara, 300041 Timisoara, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrei","family":"Motoc","sequence":"additional","affiliation":[{"name":"Discipline of Anatomy and Embryology, \u201cVictor Babes\u201d University of Medicine and Pharmacy Timisoara, 300041 Timisoara, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sorin","family":"Dema","sequence":"additional","affiliation":[{"name":"Discipline of Radiology, \u201cVictor Babes\u201d University of Medicine and Pharmacy Timisoara, 300041 Timisoara, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marius","family":"Craina","sequence":"additional","affiliation":[{"name":"Discipline of Obstetrics and Gynecology, \u201cVictor Babes\u201d University of Medicine and Pharmacy Timisoara, 300041 Timisoara, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8076-8885","authenticated-orcid":false,"given":"Veronica Daniela","family":"Chiriac","sequence":"additional","affiliation":[{"name":"Discipline of Obstetrics and Gynecology, \u201cVictor Babes\u201d University of Medicine and Pharmacy Timisoara, 300041 Timisoara, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8354-9928","authenticated-orcid":false,"given":"Adrian","family":"Gluhovschi","sequence":"additional","affiliation":[{"name":"Discipline of Obstetrics and Gynecology, \u201cVictor Babes\u201d University of Medicine and Pharmacy Timisoara, 300041 Timisoara, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,2,27]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1186\/s13256-019-2327-x","article-title":"Iatrogenic endometriosis following apical pelvic organ prolapse surgery: A case report","volume":"14","author":"Cubuk","year":"2020","journal-title":"J. Med. Case Rep."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Zhang, P., Sun, Y., Zhang, C., Yang, Y., Zhang, L., Wang, N., and Xu, H. (2019). Cesarean scar endometriosis: Presentation of 198 cases and literature review. BMC Women\u2019s Health, 19.","DOI":"10.1186\/s12905-019-0711-8"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Kapoor, R., Stratopoulou, C.A., and Dolmans, M.-M. (2021). Pathogenesis of Endometriosis: New Insights into Prospective Therapies. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms222111700"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Doroftei, B., Maftei, R., Ilie, O.-D., Simionescu, G., Anton, E., Armeanu, T., Dabuleanu, A.-M., Mihalceanu, E., Condac, C., and Ilea, C. (2021). Transvaginal Ultrasound as a First-Line Approach in Deep Endometriosis: A Pictorial Essay. Diagnostics, 11.","DOI":"10.3390\/diagnostics11030444"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"480","DOI":"10.1002\/uog.8935","article-title":"Transvaginal sonography vs. clinical examination in the preoperative diagnosis of deep infiltrating endometriosis","volume":"37","author":"Hudelist","year":"2011","journal-title":"Ultrasound Obstet. Gynecol."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Practice Committee of the American Society for Reproductive Medicine (2014). Treatment of pelvic pain associated with endometriosis: A committee opinion. Fertil. Steril., 101, 927\u2013935.","DOI":"10.1016\/j.fertnstert.2014.02.012"},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Nawrocka-Rutkowska, J., Szyd\u0142owska, I., Ry\u0142, A., Cie\u0107wie\u017c, S., Ptak, M., and Starczewski, A. (2021). Evaluation of the Diagnostic Accuracy of the Interview and Physical Examination in the Diagnosis of Endometriosis as the Cause of Chronic Pelvic Pain. Int. J. Environ. Res. Public Health, 18.","DOI":"10.3390\/ijerph18126606"},{"key":"ref_8","unstructured":"Brandt, W.E., and Helms, C.A. (2007). Genital tract: Radiographic imaging and MR. Fundamentals of Diagnostic Radiology, Lippincott Williams and Wilkins. Chapter 35."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Kawahara, N., Miyake, R., Yamanaka, S., and Kobayashi, H. (2021). A Novel Predictive Tool for Discriminating Endometriosis Associated Ovarian Cancer from Ovarian Endometrioma: The R2 Predictive Index. Cancers, 13.","DOI":"10.3390\/cancers13153829"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Arnaoutoglou, C., Variawa, R.S., Zarogoulidis, P., Ioannidis, A., and Machairiotis, N. (2021). Advances of Laparoscopy for the Diagnosis of Pelvic Congestion Syndrome. Medicina, 57.","DOI":"10.3390\/medicina57101041"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Kotowska, M., Urbaniak, J., Fal\u0119cki, W.J., \u0141azarewicz, P., Masiak, M., and Szymusik, I. (2021). Awareness of Endometriosis Symptoms\u2014A Cross Sectional Survey among Polish Women. Int. J. Environ. Res. Public Health, 18.","DOI":"10.3390\/ijerph18189919"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"616","DOI":"10.2214\/AJR.04.1619","article-title":"Abdominal wall endometriosis: Clinical presentation and imaging features with emphasis on sonography","volume":"186","author":"Hensen","year":"2006","journal-title":"Am. J. Roentgenol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1097\/AOG.0b013e3181f2e0c6","article-title":"Progression of pelvic implants to complex atypical endometrial hyperplasia after uterine morcellation","volume":"117","author":"Kill","year":"2011","journal-title":"Obstet. Gynecol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1016\/j.jmig.2011.09.014","article-title":"Endometriosis after laparoscopic supracervical hysterectomy with uterine morcellation: A case control study","volume":"19","author":"Schuster","year":"2012","journal-title":"J. Minim. Invasive Gynecol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"711","DOI":"10.1097\/GRF.0000000000000320","article-title":"Endometriosis-associated ovarian cancers","volume":"60","author":"Anglesio","year":"2017","journal-title":"Clin. Obstet. Gynecol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1093\/humrep\/dey332","article-title":"Iatrogenic endometriosis harbors somatic cancer-driver mutations","volume":"34","author":"Lac","year":"2019","journal-title":"Hum. Reprod."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"116","DOI":"10.1097\/OGX.0000000000000399","article-title":"Diagnosis and management of abdominal wall endometriosis: A systematic review and clinical recommendations","volume":"72","author":"Rindos","year":"2017","journal-title":"Obstet. Gynecol. Surv."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Guo, S.-W. (2020). The Pathogenesis of Adenomyosis vis-\u00e0-vis Endometriosis. J. Clin. Med., 9.","DOI":"10.3390\/jcm9020485"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"33","DOI":"10.4274\/tjod.90922","article-title":"Post-cesarean scar endometriosis","volume":"15","author":"Tatar","year":"2018","journal-title":"Turk. J. Obstet. Gynecol."},{"key":"ref_20","unstructured":"Robert, L., Janet, T., Elizabeth, S., Jerry, S., Christa, H., Mansoor, N., Konnie, Z., Thomas, H., Shane, K., and Saeid, M.-L. (2020). Guide to Specimen Handling in Surgical Pathology, College of American Pathologists. Version 9.0."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1177\/1066896913517939","article-title":"The wonderful colors of the hematoxylin-eosin stain in diagnostic surgical pathology","volume":"22","author":"Chan","year":"2014","journal-title":"Int. J. Surg. Pathol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1007\/s00266-005-0099-8","article-title":"Abdominal wall endometrioma found during abdominoplasty","volume":"30","author":"Ostric","year":"2006","journal-title":"Aesthetic Plast. Surg."},{"key":"ref_23","first-page":"517","article-title":"Endometriosis in a trocar tract: Is it really a rare condition? A case report","volume":"55","author":"Farace","year":"2005","journal-title":"Minerva Chir."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1111\/j.1447-0756.2005.00322.x","article-title":"Incisional endometriosis after Cesarean section, episiotomy, and other gynaecologic procedures","volume":"31","author":"Gunes","year":"2005","journal-title":"J. Obstet. Gynaecol. Res."},{"key":"ref_25","first-page":"502","article-title":"Clinical external endometriosis: Probable viability of menstrually shed fragments of endometrium","volume":"4","author":"Scott","year":"1954","journal-title":"Obstet. Gynecol."},{"key":"ref_26","first-page":"e2063","article-title":"Skin Endometriosis at the Caesarean Section Scar: A Case Report and Review of the Literature","volume":"10","author":"Fatimah","year":"2018","journal-title":"Cureus"},{"key":"ref_27","first-page":"113","article-title":"Wound endometriosis: Risk factor evaluation and treatment","volume":"66","author":"Wang","year":"2003","journal-title":"J. Chin. Med. Assoc."},{"key":"ref_28","first-page":"100096","article-title":"Abdominal wall endometriosis: An 11-year retrospective observational cohort study","volume":"4","author":"Marras","year":"2019","journal-title":"Eur. J. Obstet. Gynecol. Reprod. Biol. X"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1006\/gyno.1998.5027","article-title":"Port site metastasis after laparoscopic assisted vaginal hysterectomy for endometrial cancer: Possible mechanism and prevention","volume":"70","author":"Zayyan","year":"1998","journal-title":"Gynecol. Oncol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1006\/gyno.1997.4717","article-title":"Port site metastasis after laparoscopic-assisted vaginal hysterectomy for endometrial cancer: Possible mecanisms and prevention","volume":"66","author":"Wang","year":"1997","journal-title":"Gynecol. Oncol."}],"container-title":["International Journal of Environmental Research and Public Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-4601\/19\/5\/2791\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T22:28:52Z","timestamp":1760135332000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-4601\/19\/5\/2791"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,2,27]]},"references-count":30,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2022,3]]}},"alternative-id":["ijerph19052791"],"URL":"https:\/\/doi.org\/10.3390\/ijerph19052791","relation":{},"ISSN":["1660-4601"],"issn-type":[{"value":"1660-4601","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,2,27]]}}}