Pregnancy outcomes and obstetrical complications of twin pregnancies with endometriosis: A single center cohort study

doi:10.21203/rs.3.rs-2376445/v1

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Pregnancy outcomes and obstetrical complications of twin pregnancies with endometriosis: A single center cohort study

https://doi.org/10.21203/rs.3.rs-2376445/v1

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Background: There are many studies regarding the increased relationship between pregnancy outcomes and obstetrical complications of singleton with endometriosis such as preterm birth, preeclampsia, placenta previa, and small for gestational age. However, there was limited evidence of twin pregnancies with endometriosis. The objective of this study was to compare the pregnancy outcomes and obstetrical complications in twin pregnancies with endometriosis or without endometriosis in single institution.

Methods: Between January 2011 and July 2022, a cohort of twin pregnancies delivered at single institution was retrospectively analyzed. Patients who underwent surgical treatment before pregnancy and had histological confirmation; had visual or histological confirmation during cesarean section; and those with antenatal ultrasonographic findings of typical ovarian endometriosis and underwent vaginal delivery were included in the endometriosis group. Pregnancy outcomes and obstetrical complications were compared between the two groups.

Results: A total of 1,951 patients were examined, of whom 143 (7.3%) were included in the endometriosis group. Maternal body mass index (BMI) was significantly lower in the endometriosis group (p<0.001). However, there were no significant differences in maternal age, mode of conception, and chorionicity. There were also no significant differences in pregnancy outcomes: gestational age at delivery (p=0.619), rate of delivery before 37weeks (p=0.728), and mode of delivery (p=0.698). However, some obstetrical complications showed significantly higher rates in the endometriosis group: placenta previa (p=0.038), small for gestational age <10% (p=0.039), and postpartum hemorrhage (p=0.006). Logistic regression analyses performed after adjusted for BMI showed that patient with endometriosis had a higher risk of developing placenta previa (odds ratios (OR) 2.191; 95% confidence intervals (CI) 1.051-4.568), and postpartum hemorrhage (OR, 2.506; 95% CI, 1.444-4.348). After multivariable analyses, postpartum hemorrhage was significantly higher in patients with endometriosis (OR, 2.264; 95% CI, 1.265-4.054).

Conclusions: Twin pregnancies with endometriosis had a significantly higher risk of postpartum hemorrhage. To confirm these outcomes, further large prospective studies are required.

Trial registration : retrospectively registered

Twin pregnancy

endometriosis

pregnancy outcome

placenta previa

small for gestational age

postpartum hemorrhage

Endometriosis, defined as the presence of endometrial tissue outside of the uterus, is a chronic, estrogen-dependent inflammatory disorder (1). It is a common gynecologic condition that occurs in approximately 10–20% of women of reproductive age (2) and up to 50% of women with infertility (3). Pregnancy had beneficial effects on endometriosis due to various pregnancy related metabolic, hormonal, immunologic and angiogenetic changes (4). However, according to a report by Leeners et al., during pregnancy, 15–50% of lesions disappeared completely, 34-64.7% regressed, 25% remained stable, and 8.8–39% progressed (5). Additionally, in women with endometriosis, the risk of first trimester miscarriage and ectopic pregnancy were increased (4), and there was a possible increased risk of obstetrical complications of singleton pregnancies with endometriosis, such as preterm birth, preeclampsia, placenta previa, peripartum hemorrhage, and small for gestational age (6–10). However, limited studies are available on twin pregnancies with endometriosis-related pregnancy outcomes and obstetrical complications. Therefore, this study aimed to compare the pregnancy outcomes and obstetrical complications in twin pregnancies with or without endometriosis at a single institution.

Inclusion and exclusion criteria

We performed a retrospective review of patients who delivered twins at CHA Gangnam Medical Center between January 2011 and July 2022. Inclusion criteria were as follows: (1) twin deliveries at ≥ 24 weeks of gestational age, (2) initial ≥ triplet pregnancy, which was reduced to twin pregnancy at the time of delivery due to missed abortion or selective abortion of fetus(es) before 14weeks. During antenatal ultrasound examinations, the presence of typical ovarian endometrioma was evaluated. The endometriosis group included patients who underwent surgical treatment before pregnancy and had histological confirmation; visual or histological confirmation during cesarean section; and antenatal ultrasonographic findings that showed typical ovarian endometriosis, for patients who underwent vaginal delivery. Exclusion criteria were as follows: patients with (1) monochorionic monoamniotic twins; (2) previous cervical conization; (3) associated uterine anomalies, such as didelphys, septate, unicornuate, and bicornuate uterus; and (4) unknown chorionicity or mode of pregnancy. All twin pregnancies were managed according to a standardized institutional protocol. During the first trimester, we confirmed the gestational age, chorionicity, and adnexal lesions by using transvaginal ultrasonography. If the patient first visited the clinic after late second trimester and the chorionicity was unclear, we confirmed the chorionicity using pathological examination of the placenta. However, some emergency cases were excluded from the study due to missed placenta pathology.

Ethical approval and informed consent for study.

The study protocol was approved by the Institutional Review Board (IRB) of CHA Gangnam Medical Center (GCI-2022-11-001). Data were anonymized and de-identified before analysis; therefore, informed consent was not required, and the IRB agreed for the study to be conducted without informed consent from patients. The requirement for informed consent was waived by the IRB of CHA Gangnam Medical Center because of the retrospective nature of the study. All procedures for patients were conducted in accordance with the approved protocol at CHA Gangnam Medical Center.

Patient characteristics and clinical definitions

The following data were extracted from the patients’ medical records: maternal age at delivery; body mass index (BMI) at delivery; pre-pregnancy history of hypertension or diabetes mellitus; parity; mode of conception; chorionicity; gestational age at delivery; delivery mode; birth weight of newborns; and obstetric complications, such as preterm labor, premature rupture of membranes, preeclampsia, gestational diabetes, placenta previa, incompetent internal os of cervix (IIOC), intrauterine fetal death (IUFD) after the second trimester, small for gestational age (SGA: defined as neonatal birth weight in the <10th percentile for gestational age) (11), placenta abruption, postpartum hemorrhage (estimated blood loss over 500ml during vaginal delivery, and over 1000ml during cesarean delivery), peripartum transfusion, and peripartum intensive care unit admission. The sum of birth weights of twins and weight difference were calculated in patients without IUFD.

Statistical analysis

Statistical analyses were performed using SPSS 26.00 (IBM, Armonk, NY, USA). Descriptive data are expressed as mean ± standard deviation and median, range. Chi-square and Fisher’s exact tests were used to analyze categorical variables. Quantitative variables were compared using the Mann-Whitney U test according to the Shapiro-Wilk test for normal distribution. Logistic regression was used to calculate the odds ratio (OR), presented with 95% confidence intervals (CI), to evaluate the association between endometriosis and pregnancy outcomes and obstetrical complications, before and after adjustment for BMI. Variables with a p-value < 0.05, identified using univariable analysis, were subjected to multiple logistic regression. A p-value of < 0.05 was considered statistically significant.

A total of 1,951 twin pregnancies met the inclusion criteria (Figure 1), and the endometriosis group comprised 143 (7.3%) patients.

Baseline characteristics of patients with or without endometriosis were compared in Table 1. Maternal BMI was significantly lower in the endometriosis group (p<0.001). However, there were no significant differences in maternal age, pre-pregnancy medical history, parity, mode of conception, and chorionicity.

Pregnancy outcomes and obstetric complications are compared in Table 2. There were no significant differences in pregnancy outcomes: gestational age at delivery (p=0.619), rate of delivery before 37weeks (p=0.728), and mode of delivery (p=0.698). However, some obstetrical complications showed significantly higher rates in the endometriosis group: placenta previa (p=0.038), SGA <10% (p=0.039), and postpartum hemorrhage (p=0.006).

Table 3 shows the results of the univariable logistic regression analyses: placenta previa (crude OR, 2.314; 95% CI, 1.115-4.802; p=0.024), SGA (crude OR, 1.610; 95% CI, 1.035-2.505; p=0.035), and postpartum hemorrhage (crude OR, 2.257; 95% CI, 1.309-3.889; p=0.003) were higher in endometriosis group. After adjusting for BMI, patients with endometriosis had a higher risk of developing placenta previa (OR, 2.191; 95% CI, 1.051-4.568), and postpartum hemorrhage (OR, 2.506; 95% CI, 1.444-4.348).

After multivariable analyses, postpartum hemorrhage was significantly higher in patients with endometriosis (OR, 2.264; 95% CI, 1.265-4.054) (Table 4).

Compared with singleton pregnancy, twin pregnancies are widely known to significantly increase the risk of pre-eclampsia, preterm labor, placenta previa, and postpartum hemorrhage. Therefore, twin pregnancy alone was considered a confounding factor for the analysis of pregnancy outcomes in endometriosis and resulted in limited data for twin pregnancy outcomes with endometriosis. Our study, which was the largest cohort study of twin pregnancies with endometriosis, suggested that the endometriosis was related to adverse effects, such as postpartum hemorrhage; however, there was no relationship with preterm birth, preeclampsia, placenta previa, and SGA.

There were several possible mechanisms for preterm delivery in endometriosis. Increased levels of prostaglandins and cytokines, indicating the presence of inflammatory markers, have been found in peritoneal fluid (12). Significantly increased levels of prostaglandin E₂, cyclooxygenase 2, and various cytokines have been found in endometriotic tissue than in normal endometrium (13). These increased inflammatory markers may stimulate myometrial contractions and cervical ripening, leading to preterm labor.

The eutopic endometrium in the patients with endometriosis also showed aberrant expression of integrins and HOX-genes, which may affect endometrial receptivity and subsequent placentation (13, 14). The junctional zone also showed abnormal molecular and functional levels, such as progesterone resistance, which lead to impairment of endometrial growth, maturation and decidualization, conversion of the uterine spiral arteries into uteroplacental vessels, and deep placentation (15-17). Abnormal placentation may cause increased risks of antepartum hemorrhage and placental complications. Moreover, the normal frequency and amplitude of uterine contractions are altered in women with endometriosis, this uterine dysperistalsis changes embryo transportation and implantation and increases the risk of placenta previa (18, 19). In vitro fertilization procedures due to endometriosis-related infertility are also related to the risk of placenta previa in singleton pregnancy (20). Defective artery remodeling is related to preeclampsia, preterm labor, and SGA (15, 16).

However, in our study, there were no statistical differences in the rate of preterm labor and preeclampsia in patients with or without endometriosis. It is well known that endometriosis is a hormone responsive disease, and an anti-estrogenic environment suppresses disease progression. Therefore, the possibility of elevated levels of steroid hormones in twin pregnancies overcomes the negative effect of endometriosis in preterm labor and preeclampsia.

In our study, patients with twin pregnancy with endometriosis had a lower BMI than those without endometriosis, which correlated with a study by Stepahnsson et al. on singleton pregnancy with endometriosis (21). In a crude univariable analysis, placenta previa, SGA, and postpartum hemorrhage were significant obstetrical complications in twin pregnancies with endometriosis. Due to a lower BMI related to SGA, SGA was excluded as obstetrical complications in twin pregnancies with endometriosis, after adjusting for BMI.

Endometriosis increased the risk of postpartum hemorrhage in this study, which may have resulted from the stretching and tearing of endometriosis related adhesions during delivery. Additionally, decidualized endometriosis tissue in the pelvic cavity is usually friable and showed easy touch bleeding.

A major strength of our study was the inclusion of a large cohort of twin patients. Furthermore, this study was the first comparative study on twin pregnancy with or without endometriosis. However, this study had some limitations. First, the diverse characteristics of endometriosis, including location, stage, and cyst size (in cases of ovarian endometriosis) were not compared. Due to the small sample size of twin pregnancies with endometriosis, the definitive conclusion of obstetric outcomes in twin pregnancy with endometriosis was difficult to determine. Second, the data were collected retrospectively, an inherent bias was present. Patients with a history of gynecologic surgery, such as myomectomy or ovarian cystectomy, had a possibility of combined pelvic endometriosis. However, the exact surgical findings were not identified in all patients, which may have resulted in selection bias. Third, we did not evaluate the first trimester pregnancy loss rates. Many clinicians and patients have been interested in the possibility of implantation failure and early pregnancy loss in the first trimester with endometriosis. However, this data retrospectively obtained from the twin delivery registry of our hospital; therefore, accurate data related to early pregnancy loss could not be obtained. Additionally, twin pregnancy alone had a higher risk of early pregnancy loss than singleton pregnancies. Future, prospective study can overcome these limitations of the important issue.

Overall, our study suggests that endometriosis was related to significantly higher risks of postpartum hemorrhage in patients with twin pregnancy. Endometriosis alone was related to infertility; therefore, the possibility of requiring assisted reproductive technology (ART) and subsequent increase of twin pregnancies was increased. Our data can be used to provide adequate intrapartum management plans of twin pregnancies with endometriosis. Additional large-scaled multicenter studies may be required to confirm our results.

IRB : Institutional Review Board

BMI : body mass index

IIOC : incompetent internal os of cervix

IUFD : intrauterine fetal death

SGA : small for gestational age

OR : odds ratio

CI : confidence intervals

ART : assisted reproductive technology

Conflict of interest: The authors report no conflict of interest.

Financial Disclosure: none

Acknowledgements

We would like to thank Statisticspanda for responsible for statistical analysis (https://blog.naver.com/dltpwns85)

Authors’ contributions

JSS and SJK were involved in the data collection or management, data analysis, manuscript writing/editing. JYC, KH were involved in the data collection or management, manuscript editing. SS and YWJ were involved in the statistical analysis. SJS and HSJ were involved in the protocol/project development and manuscript editing. MLK was designed study protocol/project development, supervised manuscript writing and editing. All authors contributed to the interpretation, commented on multiple versions, and approved the final manuscript.

Funding

No specific funding obtained.

Availability of data and materials

Data will be available upon reasonable request from the corresponding author. However, the data cannot be made public to maintain women’s privacy and legal reasons as it contains private health information along with identifiers.

Ethics approval and consent to participate

The study protocol was approved by the Institutional Review Board on the CHA Gangnam Medical Center (GCI-2022-11-0001). Data were anonymized and deidentified before analysis, and therefore, informed consent was not required and IRB agreed to conduct the study without informed consent from the patients. The requirement for informed consent was waived by the IRB of CHA Gangnam Medical Center because of the retrospective nature of the study. All procedures for patients were conducted in accordance with the approved protocol at CHA Gangnam Medical Center.

Consent for publication

Not applicable

Competing interests

The all authors did not report any potential conflicts of interest.

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Table 1. Patient’s characteristics between with or without endometriosis groups in twin pregnancy

With endometriosis

group (n=143)

Without endometriosis

group (n=1808)

P value

Maternal age (year)^a

BMI at delivery (kg/m²)^a

Medical history, n(%)

Prepregnancy HTN^b

Prepregnancy Diabetes^b

Primiparity^b

Mode of conception^c

Natural or TI, COH+TI

IUI or COH+IUI

IVF or T-ET

Chorionicity^b

MCDA

DCDA

35.1±2.9 (35, 30-43)

26.2±2.8 (25.7,20.4-36.9)

1 (0.7%)

0 (0%)

126 (88.1%)

12 (8.4%)

8 (5.6%)

123 (86.0%)

12 (8.4%)

131 (91.6%)

34.6±3.3 (35, 19-48)

27.2±3.3 (26.8, 18.0-41.0)

15 (0.8%)

10 (0.6%)

1556 (86.1%)

260 (14.4%)

129 (7.1%)

1419 (78.5%)

161 (8.9%)

1647 (91.1%)

0.123

<0.001

1.000

0.614

0.09

1.000

^aMann-Whitney U test, ^b Fisher’s exact test, ^c Chi-square test

BMI=body mass index; HTN=hypertension; TI=timed intercourse; COH=controlled ovarian hyperstimulation; IUI=intrauterine insemination; IVF=in vitro fertilization; T-ET=thawing-embryo transfer; MCDA=monochorionic diamniotic; DCDA=dichorionic diamniotic

Table 2. Pregnancy outcomes and obstetric complications

With endometriosis

Group (n=143)

Without endometriosis Group (n=1808)

P value

GA at delivery (weeks)^a

Delivery mode^b

NSVD

Cesarean section

Sum of birth weight of twin

(except IUFD case)^a

Weight difference of twin

(except IUFD case)^a

Delivery <37weeks^b

GA at delivery ^c

Full term

34~<37weeks

<34weeks

Preterm labor^b

PROM^b

Pre-eclampsia^b

Gestational diabetes^b

Placenta previa^b

IIOC^b

>2^nd trimester IUFD^b

SGA (<10%)^b

(excluded IUFD case)

Placenta abruption^b

Placenta accreta^b

Postpartum hemorrhage^b

Peripartum transfusion^b

Postpartum ICU care^b

36.3±1.7 (36.9, 29.7-39)

6 (4.2%)

137 (95.8%)

4796.9±734.7(4850, 2530-6780) (n=141)

290.6±245.0(260,

0-1370) (n=141)

78 (54.5%)

65 (45.5%)

63 (44.0%)

15 (10.5%)

56 (39.2%)

16 (11.2%)

11 (7.7%)

16 (11.2%)

9 (6.3%)

6 (4.2%)

2 (1.4%)

27 (19.1%)

(n=141)

1 (0.7%)

3 (2.1%)

17 (11.9%)

19 (13.3%)

13 (9.1%)

36.2±1.9 (36.9, 24.4-39.7)

98 (5.4%)

1710 (94.6%)

4857.4±791.0(4960, 1280-6920) (n=1778)

287.8±229.4(240,

0-1390) (n=1778)

957 (52.9%)

851 (47.1%)

776 (42.9%)

181 (10.0%)

763 (42.2%)

285 (15.8%)

116 (6.4%)

174 (9.6%)

51 (2.8%)

202 (11.2%)

30 (1.7%)

228 (12.8%)

(n=1778)

10(0.6%)

64 (3.5%)

102 (5.6%)

177 (9.8%)

184 (10.2%)

0.619

0.698

0.113

0.900

0.728

0.931

0.538

0.185

0.097

0.557

0.038

0.091

1.000

0.039

0.568

0.478

0.006

0.192

0.774

^aMann-Whitney U test, ^b Fisher’s exact test, ^c Chi-square test

GA=gestational age; IUFD=intrauterine fetal death; d/t=due to; PPROM=preterm premature rupture of membranes; IIOC=incompetent internal os of cervix; SGA=small for gestational age; ICU=intensive care unit

Table 3. Crude and adjusted ORs for obstetrical complication of twin pregnancies associated endometriosis

	Univariable analysis		Adjusted for BMI
	Crude OR (95% CI)	p-value	Adjusted OR (95% CI)	p-value
PIH	1.183 (0.687-2.036)	0.544	1.345 (0.776-2.331)	0.291
GDM	0.534 (0.268-1.065)	0.075	0.557 (0.279-1.113)	0.098
Placenta previa	2.314 (1.115-4.802)	0.024	2.191 (1.051-4.568)	0.036
IIOC	0.971 (0.416-2.269)	0.946	0.897 (0.382-2.104)	0.802
Preterm labor	0.882 (0.622-1.249)	0.478	0.783 (0.548-1.118)	0.178
Premature rupture of membranes	0.673 (0.394-1.150)	0.147	0.625 (0.365-1.071)	0.087
>2^nd trimester IUFD	0.841 (0.199-3.554)	0.813	0.806 (0.190-3.420)	0.770
Preterm delivery	0.937 (0.666-1.319)	0.710	1.008 (0.714-1.425)	0.962
NSVD vs C/S	1.309 (0.564-3.039)	0.532	1.394 (0.599-3.244)	0.441
SGA	1.610 (1.035-2.505)	0.035	1.509 (0.967-2.355)	0.070
Postpartum hemorrhage	2.257 (1.309-3.889)	0.003	2.506 (1.444-4.348)	0.001
Placenta abruption	1.266 (0.161-9.962)	0.823	0.869 (0.110-6.871)	0.894
Perioperative transfusion	1.412 (0.850-2.345)	0.183	0.680 (0.408-1.132)	0.138
Placenta accreta	1.713 (0.531-5.521)	0.368	1.718 (0.532-5.551)	0.366
Postpartum ICU care	0.883 (0.489-1.592)	0.678	0.946 (0.523-1.712)	0.855

OR=odd ratio; CI=confidence interval; BMI=body mass index; PIH=preeclampsia; GDM=gestational diabetes mellitus; IIOC=incompetent internal os of cervix; IUFD=intrauterine fetal death; NSVD=normal spontaneous vaginal birth; vs=versus; C/S=cesarean section; SGA=small for gestational age; ICU=intensive care unit

Table 4. Multivariable analysis after adjusted for BMI for obstetrical complication of twin pregnancies associated endometriosis

	Univariable analysis after adjusted for BMI		Multivariable analysis after adjusted for BMI
	Adjusted OR (95% CI)	p-value	Adjusted OR (95% CI)	p-value
Placenta previa	2.191 (1.051-4.568)	0.036	1.614 (0.738-3.531)	0.231
Postpartum hemorrhage	2.506 (1.444-4.348)	0.001	2.264 (1.265-4.054)	0.006
OR=odd ratio; CI=confidence interval; BMI=body mass index

No competing interests reported.

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Pregnancy outcomes and obstetrical complications of twin pregnancies with endometriosis: A single center cohort study

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