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Cited by 9Endometriosis Research and TreatmentMaternal and fetal healthcareEctopic Pregnancy Diagnosis and Management

Women with Endometriosis—Who Is at Risk for Complications Associated with Pregnancy and Childbirth? A Retrospective Case–Control Study

Open access
Gruber, Teresa Mira, Ortlieb, Laura, Henrich, Wolfgang, Mechsner, Sylvia·2024·Journal of Clinical Medicine
DOI 10.3390/jcm13020414PMC PMC10816776
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Abstract

Women with endometriosis (EM), particularly the manifestations of adenomyosis (AM) and deep infiltrating endometriosis (DIE), suffer from pain and sterility. DIE also appears with several specific obstetric complications. To determine the risk profile, we designed a retrospective case–control study. Primary outcomes were defined as the risk of preterm birth and caesarean delivery (CD). Primiparous singleton pregnancies in women with DIE were compared with controls without EM. We matched for mode of conception and maternal age. A total of 41 women diagnosed with DIE and 164 controls were recruited. A total of 92.7% of the cases were also diagnosed with AM. Preterm birth occurred in 12.2% of cases and in 6.7% of controls. The difference was not statistically significant (OR: 1.932; 95% CI: 0.632–5.907). The rate of CD was similar in both groups. Remarkably, placental implantation disorders in the form of placenta praevia were eight times more frequent in women with DIE (9.8%) than in controls (1.2%, OR: 8.757; 95% CI: 1.545–49.614). Neonatal outcome was similar in both groups. Four out of fourteen cases reported abdominal wall endometriosis after CD. Women with DIE/AM and with placenta praevia are at risk of bleeding complications. After CD, they can develop abdominal wall EM. We therefore suggest evaluating the birth mode in each woman with DIE/AM.

AI snapshot

Written from the paper’s full text.

TL;DR

In a retrospective matched case–control study of primiparous singleton pregnancies, women with deep infiltrating endometriosis (DIE) had a nonsignificant higher rate of preterm birth and a similar caesarean delivery rate compared with controls without endometriosis. Placenta praevia was significantly more frequent in DIE cases, and abdominal wall endometriosis was reported after caesarean delivery in 4/14 cases.

Key findings

  • Preterm birth occurred in 12.2% (5/41) of DIE cases vs 6.7% (11/164) controls; OR 1.932, 95% CI 0.632–5.907, not statistically significant. Birth before 34+0 weeks occurred in 4.9% vs 3.7%.
  • Caesarean delivery rates were similar: 34.1% (14/41) cases vs 31.7% (52/164) controls.
  • Placenta praevia was 9.8% (4/41) in cases vs 1.2% in controls; OR 8.757, 95% CI 1.545–49.614, p = 0.004.
  • Among cases who had caesarean delivery, 4/14 (29%; also reported as 28.6%) reported abdominal wall endometriosis at the caesarean scar; none in vaginal-birth cases or controls. Neonatal outcomes were similar (median birth weight 3330 g vs 3323 g).

Methods

  • Retrospective case–control study at the Charité Endometriosis Centre, Berlin; 41 women with DIE and 164 controls without EM, matched 1:4 on maternal age (+/−2 years) and ART use (IVF/ICSI).
  • Cases were primiparous singleton pregnancies with live or dead infant >500 g and documented DIE diagnosis; controls came from electronic clinic records 2015–2019. Exclusions included unclear DIE, serious maternal illness before pregnancy, uterine surgery opening the cavity, and multiple pregnancies.
  • Univariable logistic regression for primary endpoints (preterm birth and caesarean delivery), with Bonferroni–Holm adjustment for the two primary endpoints.

Limitations

  • Stated: response rate was 36% (74/205 questionnaires returned with consent; 41 cases included); German-language materials excluded potential participants with little/no German; retrospective data may cause misattribution and recall bias; non-participation could confound in either direction.
  • Stated: controls could not be definitively ruled out for EM/AM, and recruitment from a tertiary care hospital could bias toward the null; cases and controls differed by pregnancy year (cases 1988–2020, controls 2015–2019) and birth hospital, potentially biasing caesarean delivery results; placenta praevia findings were exploratory because primary endpoints were preterm birth and CD.
  • Evident from text: small case sample (41) and wide confidence intervals; because 92.7% of cases also had adenomyosis, effects of DIE and AM cannot be distinguished.

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

Integrity signals

Registry

Crossref · 10.3390/jcm13020414

Cites

37 of 37 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 27 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    The rate of caesarean delivery was similar in women with DIE and controls (34.1% vs 31.7%).

    “The rate of CD was similar in both groups.”
    • Also stated in: § 3.2. Birth Mode · plain
      “Regarding birth modes, 14 of 41 cases (34.1%) and 52 of 164 controls (31.7%) gave birth by CD (OR: 1117, CI: 0.541–2.305).”
    • Also stated in: § 4.3. Mode of Delivery · plain
      “Interestingly, we did not find an increased rate of CD in women with DIE compared with controls without EM (34.1% vs. 31.7%; p = 0.765), despite the number of women with placenta praevia.”
    Quote in the paperSubstantial claim
  • Findingown data

    Three of five preterm births in the case group were due to placenta praevia with haemorrhage.

    “In the case group, three of the five preterm births (60%) were due to placenta praevia with haemorrhage.”
    Quote in the paperNot a substantial claim
  • Findingown data

    Four out of fourteen cases who had a caesarean delivery reported development of abdominal wall endometriosis after CD (29%).

    “Four out of fourteen cases reported abdominal wall endometriosis after CD.”
    • Also stated in: § 3.2. Birth Mode · plain
      “As an incidental finding, four out of fourteen participants (29%) who had a CD reported the development of abdominal wall EM at the caesarean scar.”
    • Also stated in: § 4.4. Abdominal Wall Endometriosis Post CD · plain
      “Almost a third of the case patients in our case–control study who gave birth by CD (four out of fourteen) reported the development of abdominal wall EM after CD.”
    Quote in the paperSubstantial claim
  • Findingown data

    No women in the case group who gave birth vaginally or in the control group reported abdominal wall EM after CD.

    “This was not reported by any of the women in the case group who gave birth vaginally or in the control group.”
    Quote in the paperSubstantial claim
  • Findingown data

    92.7% of women with DIE were also diagnosed with AM.

    “A total of 92.7% of the cases were also diagnosed with AM.”
    • Also stated in: § 3. Results · plain
      “A total of 92.7% were also diagnosed with AM, and 73.2% were diagnosed with rASRM III-IV (revised Classification of the American Society for Reproductive Medicine for endometriosis) (Table 2).”
    Quote in the paperNot a substantial claim
  • May combine two claims. 15
  • Classified as probably not a substantial claim. 17

  • May combine two claims.

    Findingown data

    Preterm birth occurred in 12.2% of women with DIE and 6.7% of controls; the difference was not statistically significant (OR 1.932; 95% CI 0.632-5.907).

    “Preterm birth occurred in 12.2% of cases and in 6.7% of controls. The difference was not statistically significant (OR: 1.932; 95% CI: 0.632–5.907).”
    • Also stated in: § 3.1. Preterm Birth · plain
      “Five of forty-one participants with DIE (12.2%) and eleven of one hundred and sixty-four controls (6.7%) gave birth before 37 + 0 weeks gestation. The OR for preterm birth in women with DIE was 1.932 but was not statistically significant (95% CI: 0.632–5.907).”
    • Also stated in: § 4.2. Preterm Birth · plain
      “Our participants were almost twice as likely to have a preterm birth (12.2%) than controls without EM (6.7%), but this difference was not statistically significant (p = 0.241).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Uterine rupture, spontaneous intestinal perforation, spontaneous hematoperitoneum during pregnancy, and placenta increta or percreta did not occur in the cohort.

    “Uterine rupture, spontaneous intestinal perforation, spontaneous hematoperitoneum during pregnancy or placenta increta or percreta did not occur in our cohort.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Cases with an inpatient stay during pregnancy spent a median of five nights in hospital, whereas controls spent a median of three nights.

    “Case patients reported more hospital admission during pregnancy than controls (22% vs. 13.4%). Cases with an inpatient stay during pregnancy spent a median of five nights in hospital, whereas controls with an inpatient stay during pregnancy spent a median of only three nights. The differences were not significant (Table 4).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Case patients reported more hospital admission during pregnancy than controls (22% vs 13.4%), but the differences were not significant.

    “Case patients reported more hospital admission during pregnancy than controls (22% vs. 13.4%). Cases with an inpatient stay during pregnancy spent a median of five nights in hospital, whereas controls with an inpatient stay during pregnancy spent a median of only three nights. The differences were not significant (Table 4).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    No differences were found in hypertensive disorders, including preeclampsia, PPROM, placental abruption, or foetal presentation between women with DIE and controls without EM.

    “We found no differences in hypertensive disorders, including preeclampsia (PE), PPROM, placental abruption or foetal presentation between women with DIE and controls without EM. Foetal presentation was similar in both groups (Table 4).”
    Quote in the paperSubstantial claim

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

    Findingown data

    73.2% of cases were diagnosed with rASRM III-IV.

    “A total of 92.7% were also diagnosed with AM, and 73.2% were diagnosed with rASRM III-IV (revised Classification of the American Society for Reproductive Medicine for endometriosis) (Table 2).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    The distributions of foetal presentation at birth and sex of neonates were equal.

    “The distributions of the foetal presentation at birth and the sex of the neonates were equal.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    The median birth weight, median weight percentile, Apgar scores, and rate of infants with umbilical artery pH below 7.20 or 7.10 were similar in cases and controls.

    “The median birth weight, the median weight percentile, the Apgar scores and the rate of infants with an umbilical artery pH below 7.20 or 7.10 were similar in the cases and the controls.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Study design and conductreasoning

    EM or AM could not be ruled out with certainty in included controls, which could lead to underestimation of the presumed increased risk in case patients.

    “However, EM or AM could not be ruled out with certainty in the included controls. This could lead to an underestimation of the presumed increased risk in the case patients, i.e., a confounding in the direction of the null hypothesis.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationnone given

    Most patients with DIE appear to have uncomplicated vaginal births with a good outcome for both mother and child.

    “Most patients with DIE appear to have uncomplicated vaginal births with a good outcome for both mother and child.”
    Quote in the paperSubstantial claim

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

    Premisecitation

    Maternal age is a risk factor for several obstetric complications, including gestational hypertension and CD.

    “Two: maternal age. It is a risk factor for several obstetric complications, including gestational hypertension and CD [8].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [8] Fuchs, F., Monet, B., Ducruet, T., Chaillet, N., and Audibert, F. (2018). Effect of maternal age on the risk of preterm birth: A large cohort study. PLoS ONE, 13. source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductnone given

    The study adjusted for the two main confounders, ART and maternal age.

    “We adjusted for the two main confounders, namely ART and maternal age.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Study design and conductreasoning

    Data on cases and controls were collected retrospectively, which may have biased results due to misattribution and recall bias.

    “Data on cases and controls were collected retrospectively. This may have biased the results due to misattribution and recall bias.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationcitation

    CD in women with DIE is more difficult and associated with more complications than CD in women without EM.

    “CD in women with DIE is more difficult and associated with more complications than CD in women without EM.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [18] Exacoustos, 2016, Complications during pregnancy and delivery in women with untreated rectovaginal deep infiltrating endometriosis, Fertil. Steril. source

      Not checked in the free run.

    • cites [20] Thomin, 2018, Maternal and neonatal outcomes in women with colorectal endometriosis, BJOG Int. J. Obstet. Gynaecol. source

      Not checked in the free run.

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

    Study design and conductreasoning

    The results on placenta praevia are exploratory and would need to be confirmed in the future.

    “As the primary endpoints of this case–control study were preterm birth and CD rate, the results on placenta praevia are exploratory and would need to be confirmed in the future.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Study design and conductnone given

    Cases and controls were matched in a ratio of one to four based on maternal age (+/− two years) and ART use IVF and ICSI.

    “Cases and controls were matched in a ratio of one to four based on maternal age (+/− two years) and ART use IVF and ICSI.”
    Quote in the paperSubstantial claim

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

    Premisecitation

    Posterior adhesions may be a risk factor for bleeding complications.

    “An association between AM of the posterior uterine wall and placenta praevia has been demonstrated and posterior adhesions may be a risk factor for bleeding complications [33].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [33] Shi, 2023, Effects of localization of uterine adenomyosis on clinical features and pregnancy outcome, Sci. Rep. source

      Not checked in the free run.

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

    Premisecitation

    There is one single origin of EM, DIE and AM, namely archimetrosis.

    “We postulate and follow the theory of Leyendecker et al. that there is one single origin of EM, DIE and AM, namely archimetrosis [13].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [13] Leyendecker, 1998, Endometriosis: A dysfunction and disease of the archimetra, Hum. Reprod. Update source

      Not checked in the free run.

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

    Study design and conductreasoning

    Confounding in both directions due to frequent non-participation of patients with particularly many or few complications cannot be excluded.

    “We cannot exclude the possibility of confounding in both directions due to the frequent non-participation of patients with particularly many or few complications during pregnancy.”
    Quote in the paperNot a substantial claim

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

    Premisecitation

    Women with EM give birth to significantly more low-birth-weight babies than controls without EM.

    “According to Zullo et al., women with EM had a significantly higher incidence of miscarriages, preterm birth, placenta praevia and caesarean delivery (CD), and gave birth to significantly more low-birth-weight babies than the control group [4].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [4] Zullo, 2017, Endometriosis and obstetrics complications: A systematic review and meta-analysis, Fertil. Steril. source

      Not checked in the free run.

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

    Premisecitation

    An association between AM of the posterior uterine wall and placenta praevia has been demonstrated.

    “An association between AM of the posterior uterine wall and placenta praevia has been demonstrated and posterior adhesions may be a risk factor for bleeding complications [33].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [33] Shi, 2023, Effects of localization of uterine adenomyosis on clinical features and pregnancy outcome, Sci. Rep. source

      Not checked in the free run.

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

    Study design and conductown data

    The response rate was 36% (74 of 205 women responded).

    “Of the 205 women who received the questionnaire, 74 responded with signed informed consent, giving a response rate of 36%.”
    Quote in the paperNot a substantial claim

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

    Study design and conductreasoning

    Potential participants with little or no knowledge of German were not able to participate.

    “The questionnaire and participant information were written in German. Potential participants with little or no knowledge of German were not able to participate in the study.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Study design and conductown data

    Cases and controls differed significantly regarding the year in which the cases' pregnancies ended (cases 1988-2020, controls 2015-2019) and the hospitals in which they gave birth.

    “Cases and controls in our study differed significantly regarding the year in which the cases’ pregnancies ended (cases 1988–2020, controls 2015–2019) and the hospitals in which they gave birth (cases in various hospitals throughout Germany, controls at Charité Universitätsmedizin Berlin).”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Study design and conductreasoning

    The p-values of the primary analyses were adjusted according to Bonferroni-Holm, as two primary endpoints were examined.

    “The p-values of the primary analyses were adjusted according to Bonferroni–Holm, as two primary endpoints were examined.”
    Quote in the paperSubstantial claim

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

    Study design and conductcitation

    The study followed the STROBE statement.

    “We followed the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement [11] (Supplementary Data S1).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [11] Altman, 2014, The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) Statement: Guidelines for reporting observational studies, Int. J. Surg. source

      Not checked in the free run.

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

    Study design and conductnone given

    The study included 41 women with a first diagnosis of DIE before or after the case pregnancy and women with or without surgery for DIE before the case pregnancy.

    “We included 41 women with a first diagnosis of DIE before or after the case pregnancy and women with or without surgery for DIE before the case pregnancy.”
    Quote in the paperNot a substantial claim

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

    Premisecitation

    There is evidence that neonates born to mothers with AM are significantly lighter, more likely to be less than 2500 g and 1500 g, and to be below the 10th weight percentile compared to neonates of mothers without EM.

    “There is evidence in the literature that neonates born to mothers with AM are significantly lighter, more likely to be less than 2500 g and 1500 g and to be below the 10th weight percentile compared to neonates of mothers without EM [18,19,27,34].”
    Quote in the paperNot a substantial claim0 of 4 sources checked
    • cites [18] Exacoustos, 2016, Complications during pregnancy and delivery in women with untreated rectovaginal deep infiltrating endometriosis, Fertil. Steril. source

      Not checked in the free run.

    • cites [19] Nirgianakis, 2018, Obstetric complications after laparoscopic excision of posterior deep infiltrating endometriosis: A case-control study, Fertil. Steril. source

      Not checked in the free run.

    • cites [27] Mannini, 2017, New adverse obstetrics outcomes associated with endometriosis: A retrospective cohort study, Arch. Gynecol. Obstet. source

      Not checked in the free run.

    • cites [34] Scala, C., Leone Roberti Maggiore, U., Barra, F., Tantari, M., and Ferrero, S. (2019). Impact of Endometriomas and Deep Infiltrating Endometriosis on Pregnancy Outcomes and on First and Second Trimester Markers of Impaired Placentation. Medicina, 55. source

      Not checked in the free run.

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

    Study design and conductnone given

    Twelve potential controls were excluded because pre-existing EM or AM was documented.

    “Twelve potential controls were excluded because pre-existing EM or AM was documented.”
    Quote in the paperNot a substantial claim
29 of 29

  • The authors state this as an assumption.

    The control group is representative of primiparous singleton births in Germany.

    “We assume that our control group is therefore representative of primiparous singleton births in Germany.”

  • The authors state this as an assumption.

    DIE combined with AM leads to an increased risk of pregnancy and birth complications.

    “We believe that DIE combined with AM leads to an increased risk of pregnancy and birth complications, as the uterus and its immediate surroundings are the focus of the disease.”

  • The authors state this as an assumption.

    The greater the architectural changes within the uterus, the greater the influence on the course of pregnancy.

    “We postulate further that the greater the architectural changes within the uterus, the greater the influence on the course of pregnancy.”
3 of 3

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Direct implantation remains the most accepted theory for CSE among proposed etiologies.

    “While retrograde menstruation, coelomic metaplasia, and immune dysregulation are proposed etiologies, direct implantation remains the most accepted theory for CSE [4, 11, 16].”

    From Abdominal wall endometriosis in a cesarean scar: a case report (2025) · cites this paper as [16]

    Section 4.4 discusses caesarean-scar endometriosis and proposes that stem cells can translocate during surgery into abdominal-wall tissue. It does not describe direct implantation as the most accepted theory or compare it with the other proposed etiologies in the citing sentence. (LLM, conf=0.82)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Caesarean-delivery odds ratio falls outside its confidence interval

    Minor

    The reported odds ratio of 1117 cannot have a 95% confidence interval of 0.541-2.305. The stated delivery counts imply an odds ratio of approximately 1.117, suggesting a missing decimal point.

1 of 1

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Related

Authors
Gruber, T. M., Ortlieb, L., Henrich, W., & Mechsner, S.
Affiliations
Humboldt-Universität zu Berlin (DE)
Corresponding author
Gruber, Teresa Mira
ORCID
Venue
Journal of Clinical Medicine
Publisher
MDPI AG
Published
2024-01-11
Volume
13
Issue
2
Pages
414
ISSN
2077-0383 (ISSN-L)
DOI
10.3390/jcm13020414
PMC
PMC10816776
OpenAlex
W4390738583
Semantic Scholar
c31f3928a8ecde224a51af388b55d4a785755572
Cited by
9
References
38
Citations by year
2026: 4 · 2025: 3 · 2024: 2
FWCI
3.55
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Clinical Medicine (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Refubium (Universitätsbibliothek der Freien Universität Berlin) (submittedVersion, cc-by)
  • Universitätsbibliothek der FU Berlin Hochschulschriftenstelle u. Dokumentenserver (cc-by)
Topics
  • Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
  • Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Maternal and fetal healthcare
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Ectopic Pregnancy Diagnosis and Management
Keywords
endometriosis, deep infiltrating endometriosis, adenomyosis, placenta previa, preterm birth, cesarean section, pregnancy complications, abdominal wall endometriosis, postpartum hemorrhage, mode of delivery

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