Obstetric and gynecological surgical procedures, and surgical site infections as risk for the development of endometriosis: a multicenter study

Endometriosis is an estrogen-dependent and multifac- torial, chronic inflammatory disease in women. Women with endometriosis are at elevated risk for serious ad- verse outcomes [1-4]. According to the literature, women with endometrio- sis had higher odds of gestational hypertension and/or pre-eclampsia, gestational diabetes, gestational cholestasis, placenta praevia, antepartum hemorrhage, antepartum hospital admissions, and malpresentation [5,6]. In addition, in women with endometriosis were also more likely to have preterm birth and neonatal death [7]. Among women who conceived with the use of assisted reproductive technology, endometriosis associated with preterm birth [8, 9]. Obstetric and gynecological surgical procedures, and surgical site infections as risk for the development of endometriosis: a multicenter study Aidyn G. Salmanov1,2, Volodymyr V. Artyomenko3, Olena A. Dyndar4, Iryna M. Lypko4, Victor O. Rud5, Lidiya V. Suslikova6, Andrey O. Semenyuk6, Oleksandr V. Zabudskyi6, Svitlana M. Korniyenko3, Olga V. Gorbunova6, Vitalii S. Strakhovetskyi7,8, Yuliia V. Strakhovetska8, Olena O. Lytvak9, Khrystyna V. Zarichanska6, Andriy I. Chubatyy4, Olexandr P . Kononets6, Mykhailo V. Knyhin8 1UKRAINIAN CENTER OF MATERNITY AND CHILDHOOD OF THE NATIONAL ACADEMY OF MEDICAL SCIENCES OF UKRAINE, KYIV , UKRAINE 2THE ZARIFA ALIYEVA INTERNATIONAL CENTER OF MEDICAL SCIENCE, KYIV , UKRAINE 3ODESA NATIONAL MEDICAL UNIVERSITY , ODESA, UKRAINE 4BOGOMOLETS NATIONAL MEDICAL UNIVERSITY , KYIV , UKRAINE 5NATIONAL PIROGOV MEMORIAL MEDICAL UNIVERSITY , VINNYTSIA, UKRAINE 6SHUPYK NATIONAL HEALTHCARE UNIVERSITY OF UKRAINE, KYIV , UKRAINE 7KHARKIV NATIONAL MEDICAL UNIVERSITY , KHARKIV , UKRAINE 8MEDICAL CENTRE “ASHERA” , KHARKIV , UKRAINE 9 CLINICAL AND PREVENTIVE MEDICINE STATE INSTITUTION OF SCIENCE CENTER OF INNOVATIVE HEALTHCARE TECHNOLOGIES STATE ADMINISTRATIVE DEPARTMENT , KYIV , UKRAINE

Aim: Aim this study was to evaluate the incidence of endometriosis in women with a recent history of surgical site infections (SSIs), and obstetric and gyne - cological surgical procedures.

A retrospective multicenter cohort was conducted on patients who have had obstetric or gynecological surgical procedures performed from January 2022 to December 2024 in 16 hospitals from six Ukrainian regions. Definitions of SSIs were adapted from the Centers for Disease Control and Prevention’s National Healthcare Safety Network. The criteria for endometriosis were adapted from the ESHRE endometriosis guideline.

The study included 33,126 reproductive women with endometriosis who had 16,724 obstetric and 32,383 gynecologic surgical procedures. The inci- dence of endometriosis in women with history of obstetric and gynecologic surgical procedures, and SSIs was 25.5% [95% confidence interval (CI), 24.3-26.4], 33.3% (95% CI, 33.0-33.6), and 22,1% (20.8-24.2), respectively. Multivariate analysis identified SSIs, obstetric and gynecological surgical procedures as three factors positively associated with the risk of endometriosis. Factors that increased the odds of endometriosis was SSIs (adjusted odds ratio [AOR], 3.76; 95% CI, 2.29–6.20), and obstetric and gynecological surgical procedures (AOR, 7.91; 95% CI, 3.68–37.3). An SSIs and obstetric and gynecological surgery history increased the odds of an endometriosis >7-fold in the cohort (AOR, 7.96; 95% CI, 3.64–37.2).

Obstetric and gynecological surgical injury, and the inflammation resulting from SSIs may play a role in developing endometriosis. KEY WORDS: endometriosis, obstetric and gynecological surgery, surgical site infections, risk factor, Ukraine Wiad Lek. 2025;78(7):1291-1297. doi: 10.36740/WLek/208988 DOI ORIGINAL ARTICLE CONTENTS Aidyn G. Salmanov et al. 1292 Endometriosis disease is the cause of depression. This pathology leads to a loss of productivity at work. According to the literature, medical cost range of en- dometriosis from US$1459 to US$20,239 [10]. Currently, the pathophysiology and risk factors of the disease are not fully understood. Previous studies have shown that inflammation related to genital tract infec- tion and surgical injury may cause endometriosis [11, 12]. According to the literature, in patients with a pre- vious cesarean section presented a twofold increased risk of endometriosis. Also, it has been reported that dissemination of endometrial cells may occur during cesarean section after entry into the uterine cavity [13]. According to the literature, Inflammation in the pel- vic cavity is one of the leading factors an important pathologic process of endometriosis. Both pathogens and physical injury of tissue may cause inflammation [11]. Several researchers have focused on revealing the relationship between inflammation and endometrio - sis. Researchers reported that intrauterine microbial colonization and bacterial endotoxin were associated with endometriosis [14]. Similar studies have not been conducted in Ukraine. A previous study has focused on the prevalence of endometriosis and adverse pregnan- cy outcomes associated with endometriosis [3, 4, 9]. AIM The aim of this study was to evaluate the incidence of endometriosis in women with a recent history of SSIs and obstetric and gynecological surgical procedures.

STUDY DESIGN, SETTING AND PATIENTS A retrospective multicenter cohort study based on surveillance data for endometriosis was conducted on patients who have had obstetric or gynecological surgical procedures performed from January 2022 to December 2024 in 16 hospitals from six Ukrainian regions (Kharkiv, Odessa, Kyiv, Vinnytsya, Lviv, Lutsk). This study included patients after a clinical suspect of endometriosis confirmed by ultrasound or magnetic resonance imaging, and in case of laparoscopic diagno- sis with histopathological confirmation of stage III or IV according to the r-ASRM (revised American Society for Reproductive Medicine) classification for endometriosis with ovarian localization. Patients were excluded: (a) in case of a history of surgeries for endometriosis, and (b) laparotomy, for staging or restaging of ovarian, tubal, or primary peritoneal malignancy (second look), with or without omentectomy, peritoneal washing, biopsy of abdominal and pelvic peritoneum, diaphragmatic assessment with pelvic and limited para-aortic lymph- adenectomy. Ultrasound evidence of DIE was confirmed by magnetic resonance imaging. DEFINITION An SSI was defined as an infection arising >48 h after surgical procedures. The criteria for specific SSI site after obstetric or gynecological surgical procedures were adapted from the CDC/NHSN (Centers for Dis- ease Control and Prevention’s and National Healthcare Safety Network’s) case definitions [15]. The postsurgical residual was defined as visible evidence of unresectable endometriotic lesions. Ovarian endometriosis was iden- tified as an ovarian cyst with a regular wall containing thick-brown fluid. Peritoneal endometriosis was identi- fied as superficial black, dark-brown, or bluish-puckered lesions, nodules, or small cysts containing old hemor - rhage surrounded by fibrosis. Deeply infiltrative endo- metriosis (DIE) was identified as nodules infiltrating the pouch of Douglas, vagina, posterior vaginal fornices, lateral vaginal fornices, retrocervical area, uterosacral ligaments, rectovaginal septum, bladder, rectosigmoid junction, or rectum [16]. DATA COLLECTION In this study, we analyzed the inpatient data medical records patients with endometriosis to identify and describe the type of surgical procedures and post - operative SSIs. Medical records and epidemiological data were used to find risk factors for endometriosis in patients with SSIs after obstetric and gynecological surgical procedures. The surgical procedures involved the abdominal hysterectomy (includes that by laparo- scope), Cesarean section, Laparotomy, Vaginal hysterec- tomy, and Ovarian surgery. In this study, all participants were queried regarding history of SSIs after obstetric or gynecological surgical procedures, sociodemographic characteristics, reproductive and medical history. ETHICS The Zarifa Aliyeva International Center of Medical Science (Kyiv, Ukraine) approved this study. Patients agreed to participate in this study. STATISTICAL ANALYSIS All statistical analyses were performed using Microsoft® Excel (Microsoft Corporation, Redmond, WA, USA). The data are presented as numbers and percentages. Pearson’s 1293 Obstetric and gynecological surgical procedures, and surgical site infections as risk for the development... chi-square (χ2) test was performed to check the matching performance between the case and comparison groups and compare the differences between groups for categor- ical variables. The Cox model calculated the hazard ratio (HR) and 95% confidence interval (CI) of endometriosis in patients undergoing SSIs or obstetric and gynecological surgical procedures compared to the comparison group. Logistic regression estimated the adjusted odds ratios (AORs) and 95% confidence intervals for each cohort. The P value under 0.05 was considered significant. RESUL TS The study included 33,126 reproductive women with endometriosis who had 16,724 obstetric and 32,383 gynecologic surgical procedures. Of all endometri- osis cases, 18.7% (6,195/33,126) were peritoneal/ superficial endometriosis, 67.4% (22,327/33,126) were ovarian endometriotic cyst/endometrioma and 13.9% (4,603/33,126) were deep infiltrating endometriosis. The incidence of endometriosis in women with his- tory of obstetric and gynecologic surgical procedures, and SSIs was 25.5% [95% confidence interval (CI), 24.3- 26.4], 33.3% (95% CI, 33.0-33.6), and 22,1% (20.8-24.2), respectively. Most cases (28.6%, 95% CI, 27.2-29.3) of all endometriosis was diagnosed in women with history of operations on ovary and related structures. Endome- triosis in women with history of vaginal hysterectomy, abdominal hysterectomy and obstetrical delivery by cesarean section was 9.3%, 5.3%, and 3.7%, respectively. A total 33,126 women with endometriosis had 11,042 histories of SSIs. The highest number (>30%) of SSIs was Table 1. Incidence of surgical site infections (SSIs) after obstetrical and gynecological surgery procedures in Ukraine (2022-2024) Type of procedure Number of proce- dures, n SSIs Incidence of SSIs (95% CI) Yes No n % n % Abdominal hysterotomy (e.g., for hydatidiform mole, abortion) 1,748 367 21.1 1381 79.0 20.0 – 22.0 Operative vaginal delivery 985 218 22.1 767 77.9 20,9 – 23.4 Cesarean delivery 2,431 618 25.4 1,823 74.6 24.5 – 26.4 Postpartum hemorrhage 2,017 362 17.9 1,655 82.1 17.1 – 18.8 Genital tract lacerations after vaginal delivery 987 211 21.4 776 78.6 20.1 – 22.7 Manual removal of the placenta (vaginal or cesarean delivery) 1,887 488 25.9 1,399 74.1 24.9 – 26.9 Multiple vaginal examinations after vaginal delivery 2,711 1,024 37.8 1,687 62.2 36.9 – 38.7 Induced abortion with cervical dilation and hysterotomy 1,812 659 36.4 1,153 63.6 35.3 – 37.5 Surgical curettage after vaginal delivery 2,146 817 38.1 1,329 61.9 37.1 – 39.2 Abdominal hysterectomy (corpus and cervix), with or without removal of tube(s) or ovary(s)1,229 348 28.3 881 71.7 27.0 – 29.6 Supracervical abdominal hysterectomy, with or without removal of tube(s) or ovary(s) 816 117 14.3 699 85.7 13.1 – 15.5 Laparoscopy, surgical, supracervical hysterectomy, with removal of tube(s) and/or ovary(s) 1,533 336 21.9 1,197 78.1 20.8 – 23.0 Laparoscopy, surgical, supracervical hysterectomy, with removal of tube(s) and/or ovary(s) 2,118 301 14.2 1817 85.8 13.4 – 15.0 Laparoscopy, surgical, with vaginal hysterectomy, with removal of tubes(s) and /or ovary(s)1,926 411 21.3 1,515 78.7 20.4 – 22.2 Laparoscopy, surgical, with lysis of adhesions (salpingolysis, ovariolysis) (separate procedure)1,422 231 16.2 1,191 83.8 15.2 – 17.2 Laparoscopy, surgical; with removal of adnexal structures (oophorectomy or salpingectomy)1,184 112 9.5 1,072 90.5 8.7 – 10.4 Laparoscopy, surgical, with excision of lesions of the ovary, pelvic viscera, or peritoneal surface10,228 1,856 18.1 8,372 81.9 17.7 – 18.5 Salpingo-oophorectomy, complete or partial, unilateral or bilateral (separate procedure) 512 85 16.6 427 83.4 15.0 – 18.2 Lysis of adhesions (salpingolysis, ovariolysis) 1,046 123 11.8 923 88.2 10.8 – 12.8 Drainage of ovarian cyst(s), unilateral or bilateral (vaginal approach) 1,207 211 17.5 996 82.5 16.4 – 18.6 Drainage of ovarian cyst(s), unilateral or bilateral (abdominal approach) 1,127 109 9.7 1,018 90.3 8.8 – 10.6 Drainage of ovarian abscess (vaginal approach, open) 1,401 211 15.1 1,190 84.9 14.1 – 16.1 Drainage of ovarian abscess (abdominal approach) 1,126 211 18.7 915 81.3 17.5 – 19.9 Biopsy of ovary, unilateral or bilateral (separate procedure) 1,452 547 37.7 905 62.3 36.4 – 39.0 Ovarian cystectomy, unilateral or bilateral 1,283 427 33.3 856 66.7 32.0 – 34.6 Closure of vesicouterine fistula; with hysterectomy 1,024 257 25.1 767 74.9 23.8 – 26.5 Vaginal hysterectomy, with removal of tube(s), and/or ovary(s) 986 233 23.6 753 76.4 22.3 – 25.0 Vaginal hysterectomy, with or without endoscopic control 763 152 19.9 611 80.1 27.1 – 28.2 Total 49,107 11,042 22,5 38,065 77,5 22.3 – 22.7 SSIs, surgical site infections; CI, confidence interval Aidyn G. Salmanov et al. 1294 found after surgical curettage (38.1%, 95% CI, 37.1-39.2), multiple vaginal examinations after vaginal delivery (37.8%, 95% CI, 36.9- 38.7), biopsy of ovary (37.7%, 95% CI, 36.4-39.0), induced abortion with cervical dilation and hysterotomy (36.4%, 95% CI, 35.3-37.5), and ovarian cystectomy (33.3% 95% CI,32.0-34.6). The analysis of post-operative infections (SSIs) is presented in Table 1. Analysis of the structure of SSIs showed that post - operative infections have different localizations of the pathological process. The most common types of SSI were endometritis after induced abortion (15,4%, 95% CI, 4.5-16.3), endometritis after multiple vaginal exam- inations (12,5%, 95% CI, 11,6-13.4), endometritis after cesarean delivery (12%, 95% CI, 11.1-12.9), oophoritis (9,3% 95% CI, 8.4-10.2), and tubo-ovarian abscess (8,7%, 95% CI, 7.8-9.6), followed by salpingitis (7.5%, 95% CI, 6.6-8.4), episiotomy infections (7.2%, 95% CI, 6.3-8.1), and vaginal cuff infections (6.6%, 95% CI, 5.7-7.5). Other types of infections accounted for less than 5% (Table 2). We analysed the history of any surgical procedures grouped by laparotomy, laparoscopy, gynecologically and obstetric related procedures. Multivariate analysis identified SSIs, obstetric and gynecological surgical pro- cedures as three factors positively associated with the risk of endometriosis. Factors that increased the odds of endometriosis was SSIs (adjusted odds ratio [AOR], 3.76; 95% CI, 2.29–6.20), and obstetric and gynecolog- ical surgical procedures (AOR, 7.91; 95% CI, 3.68–37.3). An SSIs and obstetric and gynecological surgery history increased the odds of an endometriosis >7-fold in the cohort (AOR, 7.96; 95% CI, 3.64–37.2) (Table 3).

This study is the first to report an increased risk of en- dometriosis in women with a recent history of obstetric and gynecological surgical procedures and post-oper- ative healthcare-associated infections data. We inves- tigated the incidence of endometriosis in women with a recent history of SSIs, obstetric and gynecological surgical procedures, or both. Inflammation is one of the leading factors and an important pathologic process of endometriosis. Inflammation related to post-operative infection and surgical injury may cause endometriosis. Therefore, we investigated the incidence of endome - triosis in women with a recent history of SSIs, pelvic surgery, or both. This study was undertaken to test the hypothesis that obstetric and gynecological surgical procedures and SSIs increases the risk of endometriosis. We recruited patients with endometriosis and retrieved information on the history of any surgical procedures, grouped by obstetrical delivery by cesarean section (CSES), abdominal hysterectomy (includes that by laparoscope), operations on ovary and related struc - tures, and vaginal hysterectomy (excludes the use of laparoscope) and cases of SSIs after these procedures. We then evaluated the association, if any, between endometriosis and history of surgical procedures and SSIs. This study showed that a history of obstetric and gynecological surgical procedures and SSIs increases the future incidence of endometriosis. Endometriosis is an estrogen-dependent and mul- tifactorial, chronic inflammatory disease in women, characterized by the presence of endometrial tissue outside the uterine cavity. Endometriosis most com- monly affects peritoneal surfaces, ovaries and uterine ligaments and even may affect the vulva, vagina [17]. Endometriosis usually occurs in the pelvis. According to the literature, endometriosis usually develops in a previous surgical scar [18] However, few publications have focused on obstetric and gynecological surgical procedure as risk factor for endometriosis. According to the literature, сesarean scar endometriosis is the most common type of abdominal wall endometriosis [19]. Gunes M, et al. [20] reported 11 cases of incisional endo- metriosis after CSES, perineal episiotomy incision or the vaginal cuff after hysterectomy, and other gynecologic procedures. In addition, Díaz-Barreiro G, et al. reported a case of external endometriosis, pelvi-genital (vagina) and extrapelvic (on episiotomy scar) presentation [21]. Maillard C, et al. [22] reported that 95.3% presenting with vulvo-perineal endometriosis have undergone either episiotomy, perineal trauma or vaginal injury or surgery. Only 4.7% developed vulvo-vaginal endometri- osis spontaneously. The examination which confirmed the diagnosis of endometriosis. Andolf et al. [23] and Liu et al. [24] reported that patients who underwent a previous CS presented a high risk for endometriosis compared with patients with vaginal deliveries only. Those studies focused on the surgical history before endometriosis diagnosis. According to the literature, the presence of ectopic endometrial tissue embedded in the subcutaneous adipose layer and the muscles of the abdominal wall association with a previous surgical procedure [25]. Zhang P , et al. suggested that during CD (cesarean delivery), the endometrial tissue is inoculated directly in the cesarean incision [19]. Inflammation is an important factor pathologic process of endometriosis, and several researchers have focused on revealing the relationship between inflammation and endometriosis. According to the literature, both pathogens and surgical injury of tissue may cause inflammation. Khan et al. proposed a new concept. They reported that intrauterine microbial colonization and bacterial endotoxin were associated 1295 Obstetric and gynecological surgical procedures, and surgical site infections as risk for the development... effect of unavailable confounding factors, which could increase the risk of having both a surgical procedures and endometriosis. These findings should be supported by other cohort studies.

The results of this study showed that obstetric and gy- necological surgical procedures and post-operative SSI was associated with an increased risk of endometriosis. Endometriosis seems to be common in women who have had a cesarean section, although it does occur after other obstetric and gynecological surgical procedures. Surgical procedure and adverse outcome history as SSIs seem to represent crucial factors in endometriosis pathogenesis through multiple mechanisms. Endometriotic lesions may arise from minimal residual lesions undetected and unremoved from surgery or by de novo implants in the area traumatized during surgery or from spillage and dissemination of endometrial cells during the surgical procedures. Therefore, a different approach to follow up may be necessary for those patients, with closer or more targeted evaluations and wider use of medical therapy with endometriosis [26]. Our previous study showed that post-operative infection (Pelvic abscess or cellulitis, Salpingitis, and Oophoritis) after gynecologic surgical procedures had more risk for endometriosis [27]. In the present study pot-operative infections after obstetric and gynecological surgical procedures were associat - ed with endometriosis. Although many studies have shown the relationship between endometriosis and SSIs after obstetric and gynecological surgical procedures, their causal relationship is unclear. STRENGTHS AND LIMITATION Our study is the first to report an increased risk of en- dometriosis in women with a recent history of post-op- erative healthcare-associated infections after obstetric and gynecological surgical procedures. The strengths of the present study lay in having included a highly selected population of patients who had obstetric and gynecological surgical procedures, and SSIs history to study the association with endometriosis. However, the retrospective nature of the study may have limited this analysis for the reduced possibility of evaluating the Table 2. Distribution of surgical site infections (n=11,042) after obstetric and gynecological surgical procedures by localization of the pathological process in Ukraine (2022-2024) Type of infection SSI 95% CI n % Endometritis after induced abortion 1695 15,4 14.5 – 16.3 Endometritis after multiple vaginal examinations 1382 12,5 11,6 – 13.4 Endometritis after cesarean delivery 1322 12 11.1 – 12.9 Oophoritis 1022 9,3 8.4 – 10.2 Tubo-ovarian abscess 964 8,7 7.8 – 9.6 Salpingitis 823 7,5 6.6 – 8.4 Episiotomy infections 786 7,2 6.3 – 8.1 Vaginal cuff infections 697 6,6 5.7 – 7.5 Endometritis after manual removal of the placenta 649 5,9 5.0 – 6.8 Pelvic abscess or cellulitis 489 4,4 3.5 – 5.3 Cervicitis 417 4,1 3.1 – 5.1 Adnexa utery 412 3,7 2.8 – 4.6 Parametritis 229 2,1 1.2 – 3.1 Other 155 0,7 0.5 – 0.9 SSIs, surgical site infections; CI, confidence interval. Table 3. Logistic multivariate regression analyses of the factors associated with endometriosis in the study participants (2022-2024) Risk factor P value Unadjusted OR (95% CI) P value Adjusted OR (95% CI) Sociodemographic Ref Ref History of SSI <0.001 3.78 (2.36–6.05) <0.001 3.76 (2.29–6.20) History of obstetric and gynecological surgery <0.001 4.44 (2.42–8.16) <0.001 4.47 (2.39–8.38) History of SSI and obstetric and gynecological surgery <0.001 7.13 (1.72–29.6) <0.001 7.91 (1.69–37.2) Aidyn G. Salmanov et al. 1296 inflammatory and immunity-related mechanisms. The inflammation resulting from SSIs after obstetric and gy- necological surgical procedures and surgical injury may play a role in developing endometriosis. Prevention of SSIs and careful surgical procedures to minimize tissue injury may reduce the incidence of endometriosis. after surgical procedures. Obstetric and gynecological surgical procedures and SSIs could increase the risk of endometriosis through two mechanisms: (a) surgery procedures it may promote the intraabdominal spread of endometrial cells after entering the uterine cavity, and (b) it could act through the previously described

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The findings and conclusions in this study are those of the authors. CONFLICT OF INTEREST The Authors declare no conflict of interest CORRESPONDING AUTHOR Aidyn G. Salmanov Ukrainian Center of Maternity and Childhood of the National Academy of Medical Sciences of Ukraine, 9 Dorohozhytska St, 04112 Kyiv, Ukraine e-mail: [email protected] ORCID AND CONTRIBUTIONSHIP Aidyn G. Salmanov: 0000-0002-4673-1154 Volodymyr V. Artyomenko: 0000-0003-2490-375X Olena A. Dyndar: 0000-0002-0440-0410 Iryna M. Lypko: 0009-0006-3338-3484 Victor O. Rud: 0000-0002-0768-6477 Lidiya V. Suslikova: 0000-0002-3039-6494 Andrey O. Semenyuk: 0009-0001-0652-7562 Oleksandr V. Zabudskyi: 0000-0003-1969-7031 Svitlana M. Korniyenko: 0000-0003-3743-426X Olga V. Gorbunova: 0000 0001 7323 5546 Vitalii S. Strakhovetskyi: 0000-0002-7528-1498 Yuliia V. Strakhovetska: 0009-0008-7996-924X Olena O. Lytvak: 0000 0001 5362 670X Khrystyna V. Zarichanska: 0000 0003 0357 3261 Andriy I. Chubatyy: 0000-0003-0375-5556 Olexandr P . Kononets: 0000-0001-6605-6902 Mykhailo V. Knyhin: 0009-0009-8622-338X – Work concept and design, – Data collection and analysis, – Responsibility for statistical analysis, – Writing the article, – Critical review, – Final approval of the article RECEIVED: 11.01.2025 ACCEPTED: 27.06.2025 CREATIVE COMMONS 4.0