Abstract
Purpose
This study sought to report on the route and gestational age at delivery of gestational carrier (GC) pregnancies with respect to the GCs’ prior obstetric history.
Methods
A retrospective analysis of all GC pregnancies from one of the largest surrogacy agencies in California between 2008 and 2018 was performed. Available demographic data and obstetric history, including a history of prior cesarean section (CS) and preterm birth (PTB), were collected for each GC and correlated to outcomes of the index GC pregnancy. Primary outcomes for the index GC pregnancies included delivery route and gestational age at delivery.
Results
Eight-hundred-thirty-six GCs were included in our analysis. 319 (38.2%) delivered via CS, and 517 (61.8%) delivered vaginally. 60 (18.8%) of the CS deliveries were due to multifetal gestation. Primary CS rate in singleton GC pregnancies was 38.5%. In women without a history of CS, neither age, BMI, interpregnancy interval, prior parity, nor year of delivery impacted the primary singleton CS rate (all, P > 0.05). Of GCs with a history of a prior CS (n = 350, 41.9%), 218 (62.3%) had a vaginal delivery after CS (VBAC) and 132 (37.7%) had a repeat CS. Women who had successful VBACs were significantly younger than those who had repeat CS (mean 33.7 vs. 35.2 years, P = .003). BMI was lower in patients who had a VBAC compared to those that had a repeat CS (mean BMI 24.6 vs. 25.5, P = 0.074), although this did not reach statistical significance. In GCs with a history of CS, interpregnancy interval, year of delivery, prior parity, and multiple gestation in the index GC pregnancy did not impact mode of delivery. VBAC rates did not change over the study period (P = 0.757). Overall PTB rate was 15.1%. Most PTB in GC pregnancies were in those with a history of PTB, and PTB was more likely in singletons rather than multifetal gestations (76.7% in singletons vs. 30% in multiples) in patients with history of PTB (P < 0.001). Those with no history of PTB and who carried multiples had a low rate of PTB; in fact, in this group, only 1 out of 35 patients had a PTB with multiples.
Conclusions
Both primary CS and PTB rates in singleton GC pregnancies are higher than national averages. CS rates are independent of age, BMI, and interpregnancy interval. In GCs with a history of a CS, VBAC rates well exceed national averages and are higher in younger GCs with a lower BMI. PTB rates are impacted primarily by the GCs obstetric history. In those GCs without a history of PTB, rates of PTB are low, even in those with a multifetal gestation.
Keywords: Gestational carriers, Pre-term birth, Cesarean section, Third party reproduction
Introduction
Gestational carrier (GC) pregnancies are an option for persons who cannot carry their own pregnancy because of a uterine factor, medical condition that makes pregnancy dangerous, or in same sex couples [1]. The GC is a woman who agrees to carry a pregnancy derived via in vitro fertilization (IVF) from the gametes of other individuals, either the intended parents (IP) or donors. GC pregnancies resulting from IVF were first described in 1985 in the USA by Utian et al. [2]. Since then, GC pregnancies conceived in the USA have accounted for approximately 2% of all ART cycles between 1999 and 2013, resulting in 13,380 deliveries and 18,400 infants, and use of GCs continues to increase [3]. Given increasing utilization of GCs in ART, an analysis of the obstetrical and perinatal risks associated with this unique population is important.
Adverse perinatal outcomes are associated with the use of ART, even in singleton pregnancies [4–8]. As ART is typically used in infertile women, much study has been devoted to parsing out whether risk is attributable to infertility itself versus the processes involved in ART. It is now well established that rates of preterm birth (PTB), preeclampsia, low birth weight, and cesarean section (CS) are all increased in infertile women with and without the use of fertility treatments [4, 5, 9]. A recent study estimated that the adjusted odds of severe maternal morbidity, a validated measure developed by the Centers for Disease Control and Prevention to study potentially life-threatening pregnancy- and childbirth-related complications, was 1.84 (95% confidence interval 1.63–2.08) for women who had pregnancies conceived with ART compared to those who spontaneously conceived [10]. The exact mechanism by which both maternal and fetal morbidity increases in ART pregnancies is unknown but may be due to altered placental function or poor oocyte quality in the infertile woman. When infertile women pursue ART, laboratory manipulation of the pre-implantation embryo or the non-physiologic hormonal milieu in the endometrium as a result of controlled ovarian stimulation and exogenous steroid hormones has also been hypothesized to contribute to adverse obstetrical risk [11].
GCs represent a unique and important population to study, as these women carry a pregnancy that resulted from IVF, yet they are not typically infertile. In fact, GCs are often selected based on prior favorable obstetric histories. As such, the study of GCs is a potential opportunity to understand the impact of assisted reproduction on obstetric outcomes, minimizing any potential confounding impact of infertility itself. There is also a profound lack of information regarding outcomes in GC pregnancies and potential risk factors to inform both intended parents and prospective gestational carriers. Guidelines and evidence for selecting gestational carriers notably lack of information regarding a GC’s prior obstetric history, including a history of preterm birth, prior pregnancy- or childbirth-related morbidity, and prior modes of delivery, as well as key demographic characteristics, such as body mass index (BMI), that may impact a current or future GC pregnancy.
The objective of the present study was to examine CS rates and incidence of PTB in GC pregnancies, taking into account each carrier’s obstetrical history during her previous, spontaneously conceived pregnancies.
Materials and methods
This was a retrospective cohort analysis of route of and gestational age at delivery for GC pregnancies initiated at one large California surrogacy agency. GCs who were matched to IP couples between August 14, 2007 and April 5, 2018 were included in our study. Of note, although enrollment dates for matched intended parents and GCs began in 2007, the first deliveries were in 2008, and the results are reported as such. GCs were excluded from the analysis if there was no live birth information available. Institutional Review Board (IRB) approval was obtained from the University of Southern California (HS-19–00,687).
GCs’ obstetric history was ascertained from the intake form completed by the potential carrier. Data collected included age of the GC at time of enrollment and embryo transfer, height and weight, number of prior spontaneous and GC pregnancies, year of last delivery, histories of multifetal gestation, CS, and PTB (less than 37 weeks gestation). Information regarding the current GC pregnancy and delivery, termed the index pregnancy, was provided to the agency from the intended parents. Data collected included route of delivery, number of infants delivered, and gestational age at delivery. For analyses of route of delivery and PTB only patients who had all the pertinent data available for analysis were included.
Chi-squared was used for dichotomous variables and student’s t-test for continuous variables. Binary logistic regression was used for delivery route, taking into consideration significant covariates on univariate analysis. All statistical analyses were based on two-sided hypotheses, with a p-value of less than 0.05 considered statistically significant. Analyses were conducted with Statistical Package for Social Sciences (SPSS, Version 25, Armonk, NY, USA).
Results
We identified 836 index GC deliveries for our analysis. Demographic data is shown in Table 1. The mean age of GCs was 33.92 ± 4.61 years, and 43.9% of GCs were ≥ 35 years of age, thus classified as advanced maternal age. The majority of GCs were non-obese; 223 (26.7%) and 52 (6.2%) were classified as overweight and obese based on BMI, respectively. All but 1 GC were multiparous, and 118 (14%) had grand multiparity (≥ 5 deliveries). In addition, 35.9% of GCs had served as a GC in a prior pregnancy. 82 (9.8%) had a history of a prior PTB.
Table 1.
Demographic data of GC cohort
| n | |
|---|---|
| Age (years) (mean ± SD) | 33.92 ± 4.61 |
| Age (years) (mean, %) | |
| ≤ 25 | 29 (3.5) |
| 26–30 | 180 (21.5) |
| 31–35 | 315 (37.7) |
| 36–40 | 241 (28.8) |
| > 40 | 71 (8.5) |
| Year (mean, %) | |
| 2008–2010 | 85 (10.2) |
| 2011–2013 | 224 (26.8) |
| 2014–2016 | 322 (38.5) |
| 2017–2019 | 200 (23.9) |
| Unknown | 5 (0.6) |
| BMI (m2/kg) (mean ± SD) | 24.68 ± 3.46 |
| BMI (m2/kg) (mean, %) | |
| < 20 | 29 (3.5) |
| 21–24 | 268 (32.1) |
| 25–29 | 223 (26.7) |
| 30–34 | 52 (6.2) |
| ≥ 35 | 0 (0.0) |
| Unknown | 264 (31.6) |
| Prior Parity (mean ± SD) | 3.00 ± 1.38 |
| 0 (mean, %) | 1 (0.1) |
| 1 | 105 (12.6) |
| 2 | 230 (27.5) |
| 3 | 234 (28.0) |
| 4 | 148 (17.7) |
| ≥ 5 | 118 (14.0) |
| Interpregnancy Interval (years) (mean ± SD) | 4.20 ± 3.10 |
| < 1(mean, %) | 5 (0.6) |
| 1–2 | 281 (33.6) |
| 3–4 | 288 (34.4) |
| 5–6 | 117 (14.0) |
| ≥ 7 | 139 (16.6) |
| Unknown | 6 (0.7) |
| Number of embryos transferred (mean ± SD) | 1.66 ± 0.68 |
| 1 (mean, %) | 320 (38.3) |
| 2 | 376 (45.0) |
| 3 | 32 (3.8) |
| 4 | 10 (1.2) |
| ≥ 5 | 4 (0.5) |
| Unknown | 94 (11.2) |
| Indication for gestation carrier (mean, %) | |
| Intended mother advanced age | 170 (20.3) |
| Same-sex couple | 129 (15.4) |
| Failed IVF | 19 (2.3) |
| Intended mother gynecologic problem | 57 (6.8) |
| Intended mother hysterectomy | 41 (4.9) |
| Repeat GC pregnancy | 34 (4.1) |
| Recurrent miscarriage | 2 (0.2) |
| Other/unknown | 350 (41.9) |
| Repeat GC pregnancies (mean, %) | |
| First-time GC | 536 (64.1) |
| Repeat GC | 300 (35.9) |
| Singleton vs. Multiple gestation (mean, %) | |
| Singleton | 649 (77.6) |
| Twins | 183 (21.9) |
| Triplets | 3 (0.4) |
| Quadruplets | 1 (0.1) |
| History of PTB (mean, %) | |
| Yes | 82 (9.8) |
| No | 570 (68.2) |
| Unknown | 184 (22.0) |
| History of CS (mean, %) | |
| Yes | 350 (41.9) |
| No | 486 (58.1) |
Route of delivery for the index GC pregnancy is described in Table 2. Overall, 61.8% (n = 517) had spontaneous vaginal deliveries and 38.2% (n = 319) were delivered via CS (CS), with 60 (18.8%) of these being in pregnancies with multifetal gestations. The CS rate was 40% for singleton deliveries compared with 32% for multifetal deliveries. Vaginal birth after CS (VBAC) was common among the 350 (41.9%) women who had a history of a prior CS; 62.3% of GCs with a history of a prior CS delivered vaginally with the index GC pregnancy compared to 37.7% who had a repeat CS. The primary CS rate in singleton GC pregnancies was 38.5%. In those without a prior history of CS, neither age, BMI, interpregnancy interval, prior parity, nor year of delivery impacted primary CS rates (all p > 0.05).
Table 2.
Route of delivery in GC pregnancies
| Route of delivery in current GC pregnancy n(%) |
||
|---|---|---|
| Vaginal delivery | CS | |
| No history of CS | 299 (61.5) | 187 (38.5) |
| History of 1 or more CS | 218 (62.3) | 132 (37.7) |
| Total | 517 (61.8) | 319 (38.2) |
In women with a history of CS, factors associated with VBAC are shown in Table 3. The only significant variable associated with VBAC was age, as mentioned previously (p = 0.012). VBAC rates did not change over the study period (P = 0.758). Women who had a successful VBAC were significantly younger than those who had repeat CS (mean 33.7 vs. 35.2 years, P = 0.003). Women ≥ 35 years of age were less likely to have a successful VBAC (OR 0.569 95% CI 0.368–0.881, P = 0.011). BMI was lower in patients who had a VBAC compared to those that had a repeat CS, yet this did not reach statistical significance (mean BMI 24.6 vs. 25.5, P = 0.074). In those with a history of CS, inter-pregnancy interval, year of delivery, prior parity, gestational age, and multifetal gestation in the index GC pregnancy did not impact mode of delivery.
Table 3.
Factors influencing mode of delivery in GCs with a history of CS
| VBAC n = 218 |
Repeat CS n = 132 |
P-value | |
|---|---|---|---|
| Type of gestation | 0.646 | ||
| Singleton | 128 (58.7) | 87 (65.9) | |
| Multiple gestation | 90 (41.3) | 45 (34.1) | |
| Age (years) | 0.012 | ||
| ≤ 25 | 5 (2.3) | 3 (2.3) | |
| 26–30 | 52 (23.9) | 20 (15.2) | |
| 31–35 | 87 (39.9) | 41 (31.1) | |
| 36–40 | 60 (27.5) | 48 (36.4) | |
| > 40 | 14 (6.4) | 20 (15.2) | |
| Year | 0.758 | ||
| 2008–2010 | 23 (10.6) | 17 (12.9) | |
| 2011–2013 | 66 (30.4) | 38 (28.8) | |
| 2014–2016 | 85 (39.2) | 46 (34.8) | |
| 2017–2019 | 43 (19.8) | 30 (22.7) | |
| Unknown | 1 (0.4) | 1 (0.8) | |
| Body Mass Index (m2/kg) | 0.227 | ||
| < 20 | 10 (4.6) | 3 (2.3) | |
| 21–24 | 66 (30.3) | 34 (25.8) | |
| 25–29 | 59 (27.1) | 35 (26.5) | |
| ≥ 30 | 11 (5.0) | 13 (9.8) | |
| Unknown | 72 (33.0) | 47 (35.6) | |
| Prior Parity | 0.464 | ||
| 1 | 24 (11.0) | 13 (9.8) | |
| 2 | 56 (25.7) | 36 (27.3) | |
| 3 | 66 (30.3) | 34 (25.8) | |
| 4 | 41 (18.8) | 25 (18.9) | |
| ≥ 5 | 31 (14.2) | 24 (18.2) | |
| Interpregnancy Interval (years) | 0.598 | ||
| 1–2 | 80 (36.7) | 46 (34.8) | |
| 3–4 | 69 (31.7) | 43 (32.6) | |
| 5–6 | 27 (12.4) | 23 (17.4) | |
| ≥ 7 | 40 (18.3) | 18 (13.6) | |
| Unknown | 2 (0.9) | 2 (1.5) | |
| Repeat GC pregnancies | 0.396 | ||
| First-time GC | 129 (59.2) | 72 (54.5) | |
| Repeat GC | 89 (40.8) | 60 (45.5) | |
| Singleton vs. Multiple gestation | 0.646 | ||
| Singleton | 128 (58.7) | 87 (65.9) | |
| Twins | 87 (39.9) | 44 (33.3) | |
| Triplets | 2 (0.9) | 1 (0.8) | |
| Quadruplets | 1 (0.5) | 0 (0.0) |
Data on gestational age at delivery for index GC pregnancies was available for 259 deliveries (Table 4). Overall, 15.1% (n = 39) of the index GC deliveries were preterm. The preterm birth rate was 16.7% for singleton pregnancies and 8.0% in multifetal pregnancies. Overall, 34 (84.6%) PTBs occurred in singleton pregnancies, 33 in GCs with a history of PTB and one in a GC with no history of PTB. Put another way, 76.7% of women with a history of a PTB with a current singleton GC pregnancy had another PTB. Only 10% of the PTBs were in multifetal gestations, 3 in GCs with a history of PTB and 1 in a GC without a history of PTB. Of these PTBs, 84.6% (33/39) occurred between 35 + 0 and 36 + 6 weeks of gestation, and the earliest gestational age of delivery was at 30 weeks.
Table 4.
Impact of history of PTB (PTB) on gestational age at delivery in GC pregnancies
| Gestational age at current GC delivery | |||||||
|---|---|---|---|---|---|---|---|
| PTB in GC pregnancy | Full term birth in GC pregnancy | All deliveries | Missing | Total | |||
| PTB history | History of PTB | Current singleton gestations | 33 (76.7%) | 10 (23.3%) | 43 (100%) | 29 | 82 |
| Current multiple gestations | 3 (30.0%) | 7 (70.0%) | 10 (100%) | ||||
| All gestations | 36 (67.9%) | 17 (32.1%) | 53 (100%) | ||||
| No history of PTB | Current singleton gestations | 1 (0.7%) | 146 (99.3%) | 147 (100%) | 388 | 570 | |
| Current multiple gestations | 1 (2.9%) | 34 (97.1%) | 35 (100%) | ||||
| All gestations | 2 (1.1%) | 180 (98.9%) | 182 (100%) | ||||
| Missing | 1 (4.2%) | 23 (95.8%) | 24 (100%) | 160 | 184 | ||
| Total | 39 (15.1%) | 220 (84.9%) | 259 (100%) | 577 | 836 | ||
In GCs with a singleton pregnancy with no history of PTB (n = 147), only 1 (0.7%) had a PTB in the index pregnancy. Moreover, those with no history of PTB and who carried multiples (n = 35) had a low rate of PTB (2.9%).
Discussion
In the present study, our principal findings were that primary CS, VBAC, and PTB rates in GC pregnancies were higher than national averages for all births. Choosing a GC who can safely carry a pregnancy to full term is of obvious importance for intended parents, yet selection criteria for a GC remains an area of controversy; some centers have very strict selection criteria while others are less restrictive. Current guidelines for choosing a GC from the American Society of Reproductive Medicine state the ideal carrier should not have more than five previous deliveries or three prior CS and have had at least one term, uncomplicated delivery [12]. These guidelines do not specify other important GC characteristics such as BMI or history of preterm birth. Based on our findings, we believe guidance regarding potential GCs with a history of PTB should be addressed. Specifically, candidates with a history of PTB would be considered with caution given the high rate of recurrent PTB in the current study. In addition, guidance regarding counseling both GCs and IPs on VBAC and repeat CS should be acknowledged.
The primary CS rate in our study was 38%, and 40% for singleton pregnancies, which is higher than national averages, estimated at 32% in 2019 [13]. Thus, even with a history of multiple vaginal deliveries, a GC should be counseled on their increased risk of primary CS and its risks. Moreover, they should be counseled on the impact this has on future pregnancies with regards to risk of uterine rupture during trial of labor after CS and abnormal placentation, should they choose to have more children themselves or become a GC again. Our study mirrors another smaller study of 45 GC pregnancies, also conducted in California that found a 52% CS rate for GC pregnancies compared to 33% among women with natural conceptions [14]. This is in contrast to other studies that report a lower CS rate in GC pregnancies. Swanson et al. reported a 26% CS rate in 361 GC pregnancies. Another study of 34 GC pregnancies in the Netherlands reports a 9% CS rate, although the different study population may limit generalizability to our population [15]. In terms of candidates with a history of CS, our findings support the inclusion of these GCs, given the high rates of VBAC, particularly in younger GCs with normal BMI, a history of CS should not necessarily preclude candidacy for becoming a GC or preclude discussion of VBAC in these pregnancies.
Both GCs and IPs also should be counseled on risk of PTB, which may lead to NICU admission and have lifelong consequences for a child born via a GC. The rate of PTB was 15% in this study, higher than national averages of 9–10% in the USA [16]. However, our findings mirror another study examining the PTB rate in GC pregnancies. In a large retrospective cohort study including 30,927 GC pregnancies, singleton PTB rates were 14.0% with fresh IP oocytes and 13.6% with fresh donor oocytes, which is similar to our reported rate of PTB [3]. Our study found that PTB rates were largely driven by the GC’s prior obstetric history. It is known that a history of preterm birth is the strongest predictor of recurrent preterm birth despite the fact that the majority of women with a history of PTB will have a full term birth in the next pregnancy [17]. The recurrent preterm birth rate was surprisingly high in this study, nearly 77% in singleton pregnancies in GCs that had a history of PTB, whereas a large meta-analysis published in 2017 showed recurrent spontaneous PTB rates of around 30% [17]. However, 85% of preterm births in this study occurred after 35 weeks, when neonatal morbidity and mortality statistics are quite favorable. Fortunately, in those GCs without a history of PTB, we found a low rate of PTB, even in those with multifetal gestations. Finally, while we advocate for single embryo transfer for patients, there are clinical scenarios in which the transfer of more than one embryo is performed or in which the single embryo results in monozygotic twins. In this study population, we found a reassuringly low rate (2.9%) of PTB in GCs carrying twins who had no history of prior PTB. This rate of PTB is lower than some other studies, possibly because our study was limited to singleton and twin pregnancies [18].
A major strength of our study is the power of the GC model and the number of GC pregnancies included. Studying those who have delivered a healthy, spontaneous pregnancy, but are now carrying a fetus derived from assisted reproduction allows for determining the contribution of uterine environment versus the assisted reproductive process on obstetrical outcomes. Moreover, having prior pregnancy information about the GCs allows for antecedent pregnancies to serve as controls for the index GC pregnancy.
While our study had information on previous modes of delivery and gestational age at delivery, there were several key variables not available for study, including the indication for CS, use of vacuum or forceps for operative delivery in the vaginal delivery group, reason for PTB (iatrogenic or spontaneous), miscarriage and stillbirth, neonatal outcomes, hypertensive disorders of pregnancy, gestational diabetes, and postpartum hemorrhage. Information pertaining to the gamete donors for the GC pregnancy was also not available, i.e. whether the gametes were from the intended parents or from another donor. Characteristics of those individuals, including genetic factors, may contribute to obstetric outcomes. Additionally, missing information was another limitation and may alter the validity of the study, as key variables were missing for many GCs, particularly regarding gestational age at delivery. BMI was also only known for approximately 70% of the study population, which may limit conclusions related to body habitus. Additionally, medical record review for GCs and GC pregnancy outcomes was not feasible to ensure accuracy of the information in the agency database. Finally, practice patterns in assisted reproduction changed over the study period. Notably, with the transition from slow cooling to vitrification for embryo cryopreservation, GC cycles likely shifted from replacement of fresh embryos to programmed frozen embryo transfer cycles. Thus, we are unable to determine whether a specific approach of endometrial preparation and embryo transfer contributed to the outcomes demonstrated in our study.
In conclusion, we found that a history of preterm birth poses a significant risk for a recurrent preterm birth in a GC pregnancy. Among GCs without a history of prior PTB, the risk of a PTB is low, even in twin gestations within our study population. Any history of PTB in a potential GC should be cautiously considered given the high rate of recurrent PTB seen in GCs. Moreover, language regarding history of PTB should be included in guidelines for choosing a GC. Contrastingly, while the primary CS rate was found to be higher than national averages, GCs with a history of a prior CS had a relatively high rate of successful VBAC. This is reassuring regarding candidacy for women with a history of one or potentially two prior CS. Ultimately, the prior obstetric history of the potential GC should be reviewed with the GC and IPs to individualize both candidacy and eventual obstetric management to maximize the chance of a good outcome for all parties involved. Additionally, continued study of GC pregnancies will help delineate the true effect of infertility versus assisted reproductive technology on obstetric outcomes.
Declarations
Conflict of interest
The authors declare no competing interests.
Footnotes
Publisher's note
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Paper Presentation Information
The findings of this research were presented to the American Society for Reproductive Medicine’s annual meeting in Philadelphia, PA from October 12 to 16, 2019. They were also presented to the Pacific Coast Obstetrical and Gynecological Society in Rancho Bernado, CA from October 23 to 27, 2019.
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