Cited by 12Endometriosis Research and TreatmentIntestinal and Peritoneal AdhesionsGynecological conditions and treatments

Challenges in Diagnosis and Prevention of Iatrogenic Endometriosis as a Long-Term Surgical Complication after C-Section

Open access
Neamtu, Radu, Dahma, George, Mocanu, Adelina Geanina, Bernad, Elena, Silaghi, Carmen-Ioana, Stelea, Lavinia, Citu, Cosmin, Dobrescu, Amadeus +7 more·2022·International Journal of Environmental Research and Public Health

Abstract

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 < 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.

AI snapshot

Written from the paper’s full text.

TL;DR

In a retrospective single-center study of 126 patients with endometriosis, prior cesarean section was associated with abdominal wall endometriosis and was an independent risk factor (OR = 1.85, p < 0.001). The authors conclude that c-section can seed endometrial tissue and call for strict surgical protocols and further research on prevention.

Key findings

  • Among 71 patients with endometriosis after c-section, the most common lesion location was the abdominal wall (42.2% vs. 5.4% in the no-c-section group); c-section patients had smaller foci by size and weight (32.2 mm vs. 34.8 mm; 48.6 g vs. 53.1 g).
  • The c-section group had significantly more minimally invasive pelvic procedures (52.1% vs. 34.5%, p = 0.049) and more multiple adhesions and endometriosis foci intraoperatively (52.1% vs. 29.1%, p = 0.017); 80% of patients without prior c-section had no adhesions vs. 53.6% in the c-section group (p = 0.002).
  • Abdominal wall endometriosis correlated with minimally invasive pelvic procedures (rho = 0.469, p = 0.001) and c-section (rho = 0.523, p = 0.001); multivariate regression identified prior c-section (OR = 1.85, p < 0.001) and number of pregnancies (OR = 1.32, CI 1.01–1.64, p = 0.038) as significant risk factors.
  • Baseline c-section group characteristics: mean age 33 years, mean age at surgery 28 years, latency 27.5 months from intervention to diagnosis, and >30 months from diagnosis to treatment; 59% had a single cesarean delivery, 87.3% had a Pfannenstiel incision, >80% had multiple endometriomas, and 42.2% had lesions at the incision site (fascia 56.3%, muscular layer 21.1%); cyclic pelvic/mid-abdominal pain was reported by 87.3%, dysmenorrhea by 69.1%, and abdominal mass by 61.9%.

Methods

  • Retrospective observational single-center study using the database of the University Clinic of Obstetrics and Gynecology Bega, Timisoara, Romania, from January 2010 to November 2021; ethical approval was granted in November 2021 (A59). It included 126 patients with endometriosis: 71 with a history of c-section meeting criteria (at least one c-section, no pre-surgery endometriosis complaints, no macroscopic endometriosis during c-section, symptoms after delivery, surgically excised foci, and histopathological diagnosis of endometriosis) and 55 controls with endometriosis and no prior pelvic surgical interventions (abstract describes no history of c-section).
  • Data were retrieved from hospital databases and paper records, including ICD-10 diagnoses and CPT procedures; variables included age, parity, abortion/delivery history, incision type, symptoms, mass size, latency period, imaging, operative findings, and histology. After clinical/imaging diagnosis, patients underwent laparoscopic or laparotomy excision and biopsy; tissue was fixed in 10% buffered formalin, paraffin embedded, and stained with hematoxylin-eosin.
  • Analysis used SPSS v26.0 and MedCalc v19; tests included Student’s t-test, Mann–Whitney U-test, Kruskal–Wallis test, chi-square/Fisher exact tests, Pearson/Spearman correlations, and multivariate regression for abdominal wall endometriosis, with alpha = 0.05.

Limitations

  • The paper states the retrospective approach and the need to correlate rare findings with uterine surgical procedures; it also states that “a group of controls was not included to facilitate the statistical analysis, leaving the findings at an observational level,” despite describing a 55-patient comparison group.
  • Evident from the text: the single-center retrospective design and reliance on existing records limit generalizability and causal inference; the control group is described inconsistently (abstract: no history of c-section; methods: no prior pelvic surgical interventions), and no long-term follow-up or prevention intervention is reported.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.3390/ijerph19052791

Cites

28 of 28 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 19 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    In patients with endometriosis, those with a prior c-section had significantly more multiple adhesions and endometriosis foci at intraoperative look than those without a prior c-section (52.1% vs. 29.1%, p=0.017).

    “Multiple adhesions and endometriosis foci were discovered intraoperatively in patients with previous c-sections (52.1%), while only 29.1% had multiple lesions in the group of patients without a history of c-section (p-value = 0.017) (Table 2).”
    Quote in the paperSubstantial claim
  • Findingown data

    In patients with endometriosis, those with a prior c-section had significantly more minimally invasive pelvic procedures than those without a prior c-section (52.1% vs. 34.5%, p=0.049).

    “By comparing the group of patients with a positive history of cesarean section with the patients without previous c-sections, we observed a significant difference in the minimally invasive procedures, where the first group of patients had significantly more interventions (52.1% vs. 34.5%, p-value = 0.049).”
    Quote in the paperNot a substantial claim
  • Findingown data

    The most common location for endometriosis lesions in patients with prior c-section was the abdominal wall (42.2%), compared with 5.4% in patients without prior c-section.

    “The most common location for endometriosis lesions in patients with prior c-section was the abdominal wall (42.2% vs. 5.4%)”
    • Also stated in: § 4. Discussion · plain
      “Although 42.2% of patients with a history of cesarean section were identified as having abdominal wall endometriosis, and although it is an insignificant percentage, it is worth mentioning that 5.4% of abdominal wall endometriosis was also found in patients with no history of cesarean section.”
    Quote in the paperSubstantial claim
  • Findingown data

    Other variables that were significantly associated with abdominal wall location of endometriosis foci in the previous correlation analysis were not identified as significant risk factors.

    “Other variables that were significantly associated with abdominal wall location of endometriosis foci in the previous correlation analysis were not identified as significant risk factors (Table 4).”
    Quote in the paperNot a substantial claim
  • Findingown data

    C-section was significantly positively associated with abdominal wall location of endometriosis (rho=0.523, p=0.001).

    “Additionally, we observed a significant positive association between c-section and abdominal wall location of the endometriosis (rho value = 0.523, p-value = 0.001) and the number of endometriosis foci (rho value = 0.488, p-value = 0.001), while the correlation with foci size was significantly negative (rho value = −0.258, p-value = 0.003).”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim. 8
  • May combine two claims. 6
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Pneumoperitoneum used in laparoscopic surgery was a major factor contributing to tumor cell implantation.

    “It is also believed that pneumoperitoneum used in laparoscopic surgery was the major factor that contributed to tumor cell implantation [28,29].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [28] Marras, 2019, Abdominal wall endometriosis: An 11-year retrospective observational cohort study, Eur. J. Obstet. Gynecol. Reprod. Biol. X

      Not checked in the free run.

    • cites [29] Zayyan, 1998, Port site metastasis after laparoscopic assisted vaginal hysterectomy for endometrial cancer: Possible mechanism and prevention, Gynecol. Oncol. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Some studies raise the hypothesis of post-cesarean scar endometriosis.

    “with some of them raising the hypothesis of post-cesarean scar endometriosis [19].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [19] Tatar, 2018, Post-cesarean scar endometriosis, Turk. J. Obstet. Gynecol. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The majority of research includes instances of gynecologic surgery for benign conditions such as adenomyosis, uterine leiomyomas, and fibroids.

    “The majority of research includes instances of gynecologic surgery for benign conditions such as adenomyosis, uterine leiomyomas, and fibroids [17,18]”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [17] Rindos, 2017, Diagnosis and management of abdominal wall endometriosis: A systematic review and clinical recommendations, Obstet. Gynecol. Surv. source

      Not checked in the free run.

    • cites [18] Guo, S.-W. (2020). The Pathogenesis of Adenomyosis vis-à-vis Endometriosis. J. Clin. Med., 9. source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Abdominal wall endometriosis in patients without prior c-section can be explained by endometrial seeding from other invasive procedures identified in the study or by other causes not explained by the current evidence.

    “This can be explained by endometrial seeding from other invasive procedures that were identified in this study or other causes that cannot be explained with the existing evidence presented by the current research.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: Patients with prior c-section who developed endometriosis after surgery and had no documented endometriosis before or during c-section had iatrogenic endometriosis caused by the c-section.
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Obesity can offer a wide surgical surface for the entrapment of endometrial cells and may impact iatrogenic endometriosis and its severity.

    “Some studies suggest that obesity can offer a wide surgical surface for the entrapment of endometrial cells and may impact iatrogenic endometriosis and its severity [30].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [30] Wang, 1997, Port site metastasis after laparoscopic-assisted vaginal hysterectomy for endometrial cancer: Possible mecanisms and prevention, Gynecol. Oncol. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Women with a record of laparoscopic supracervical hysterectomy might have a higher risk of scar endometriosis because the pelvic cavity can be exposed to endometrial cells, especially if morcellation is performed without a containment device.

    “Even though, statistically speaking, scar endometriosis occurs most often after obstetric interventions; some studies suggest that women who have a record of laparoscopic supracervical hysterectomy might have a higher risk of advancing into scar endometriosis because the pelvic cavity can be exposed to endometrial cells, especially if morcellation is performed without a containment device [27].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [27] Wang, 2003, Wound endometriosis: Risk factor evaluation and treatment, J. Chin. Med. Assoc.

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Cesarean section can expose many endometrial cells during surgery, which can be caught in the freshly manipulated abdominal wound.

    “Cesarean section can expose many endometrial cells during the surgery, which can be caught in the freshly manipulated abdominal wound.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [25] Scott, 1954, Clinical external endometriosis: Probable viability of menstrually shed fragments of endometrium, Obstet. Gynecol.

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Endometrial cells present in the wound healing process can benefit from nutrition and a protective barrier provided by clot formation, and growth can be sustained by secretion of growth factor α by suppression of local immune response.

    “Previous research describes the hypothesis of endometrial cells being present in the wound healing process, and these newly implanted endometrial cells can benefit when it comes to the source of nutrition and protective barrier provided by clot formation; growth can be sustained by the secretion of growth factor α by suppression of local immune response.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [25] Scott, 1954, Clinical external endometriosis: Probable viability of menstrually shed fragments of endometrium, Obstet. Gynecol.

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    C-section is an important independent factor associated with abdominal wall endometriosis and can be regarded as a form of iatrogenic endometriosis.

    “As the causality of endometriosis in the studied patients cannot be linked entirely to the cesarean section intervention, the significant correlation and risk factor analysis place c-sections as an important independent factor associated with this condition.”
    • Also stated in: § 5. Conclusions · plain
      “Cesarean sections are an independent risk factor for abdominal wall seeding of endometrial tissue, which can be regarded as a form of iatrogenic endometriosis.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Patients with prior c-section who developed endometriosis after surgery and had no documented endometriosis before or during c-section had iatrogenic endometriosis caused by the c-section.
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Mechanical transplantation is responsible for the evolution of iatrogenic endometriosis, according to two reports.

    “However, according to two reports, it is believed that mechanical transplantation is responsible for the evolution of iatrogenic endometriosis as the great majority of the cases of iatrogenic endometriosis occur after the incision of the gravid uterus [24].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [24] Gunes, 2005, Incisional endometriosis after Cesarean section, episiotomy, and other gynaecologic procedures, J. Obstet. Gynaecol. Res. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Endometrium during pregnancy creates a favorable microenvironment that makes transplantation and implantation particularly successful.

    “In addition, in an old case report, it has been suggested that endometrium during pregnancy creates a favorable microenvironment with certain characteristics that make transplantation and implantation particularly successful [24].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [24] Gunes, 2005, Incisional endometriosis after Cesarean section, episiotomy, and other gynaecologic procedures, J. Obstet. Gynaecol. Res. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    After hysterectomy, iatrogenic endometriosis is reported to occur at an incidence of 1.4 percent.

    “while after hysterectomy, IE is reported to occur at an incidence of 1.4 percent [13,14].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [13] Kill, 2011, Progression of pelvic implants to complex atypical endometrial hyperplasia after uterine morcellation, Obstet. Gynecol. source

      Not checked in the free run.

    • cites [14] Schuster, 2012, Endometriosis after laparoscopic supracervical hysterectomy with uterine morcellation: A case control study, J. Minim. Invasive Gynecol. source

      Not checked in the free run.

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  • The paper relies on this without support.

    Patients with prior c-section who developed endometriosis after surgery and had no documented endometriosis before or during c-section had iatrogenic endometriosis caused by the c-section.

    “Endometriosis that developed inside or in close proximity to surgical incisions of asymptomatic patients before surgical intervention was defined as iatrogenic endometriosis.”
    “As the causality of endometriosis in the studied patients cannot be linked entirely to the cesarean section intervention, the significant correlation and risk factor analysis place c-sections as an important independent factor associated with this condition.”
  • The paper relies on this without support.

    The absence of endometriosis symptoms and macroscopic findings before or during c-section means no endometriosis was present before c-section.

    “(2) the patient had no complains related to endometriosis before surgery; (3) no macroscopic findings of endometriosis were observed or documented by the gynecologist while the cesarean section was being performed;”
  • The paper relies on this without support.

    The hospital database and paper records accurately and completely captured baseline characteristics, diagnoses, and procedures.

    “All patients’ baseline characteristics and surgical procedures were documented in the hospital database in addition to paper patient records that were examined by qualified professionals participating in the present research.”
    “We used a computerized database search to determine the exact diagnosis codified by the International Classification of Diseases (ICD-10), and procedures codified by the Current Procedural Terminology (CPT).”
  • The paper relies on this without support.

    The control group of endometriosis patients without prior pelvic surgical interventions is comparable to the c-section group except for c-section history.

    “a control group of patients with endometriosis and no history of pelvic surgical interventions.”
    “By comparing the group of patients with a positive history of cesarean section with the patients without previous c-sections, we observed a significant difference in the minimally invasive procedures, where the first group of patients had significantly more interventions (52.1% vs. 34.5%, p-value = 0.049).”
4 of 4

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Research works printed but not linked: 1

  1. Brandt, W.E., and Helms, C.A. (2007). Genital tract: Radiographic imaging and MR. Fundamentals of Diagnostic Radiology, Lippincott Williams and Wilkins. Chapter 35.

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Authors
Neamtu, R., Dahma, G., Mocanu, A. G., Bernad, E., Silaghi, C.-I., Stelea, L., Citu, C., Dobrescu, A., Bratosin, F., Grigoras, M. L., Motoc, A., Dema, S., Craina, M., Chiriac, V. D., & Gluhovschi, A.
Affiliations
  • Discipline of Obstetrics and Gynecology, “Victor Babes” University of Medicine and Pharmacy Timisoara, 300041 Timisoara, Romania
  • Victor Babeș University of Medicine and Pharmacy Timișoara (RO)
  • Discipline of Anatomy and Embryology, “Victor Babes” University of Medicine and Pharmacy Timisoara, 300041 Timisoara, Romania
Venue
International Journal of Environmental Research and Public Health
Publisher
MDPI AG
Published
2022-02-27
Volume
19
Issue
5
Pages
2791
ISSN
1660-4601 (ISSN-L)
OpenAlex
W4214758826
Cited by
12
References
30
Citations by year
2026: 4 · 2025: 4 · 2024: 3 · 2023: 1
FWCI
1.69
Type
journal article
Language
en
Open access
Locations
  • International Journal of Environmental Research and Public Health (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics
  • Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
  • Health Sciences › Medicine › Surgery › Intestinal and Peritoneal Adhesions
  • Health Sciences › Medicine › Obstetrics and Gynecology › Gynecological conditions and treatments
Keywords
iatrogenic endometriosis, cesarean section, abdominal wall endometriosis, postoperative adhesions, risk factors, surgical irrigation, endometriosis prevention, endometriosis diagnosis
MeSH terms
Cesarean Section, Endometriosis, Female, Humans, Iatrogenic Disease, Pregnancy, Retrospective Studies, Gynecologic Surgical Procedures

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