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In vitro fertilization as an independent risk factor for placenta accreta spectrum

Published:April 30, 2020DOI:https://doi.org/10.1016/j.ajog.2020.04.026

      Background

      Placenta accreta spectrum is well known for its association with catastrophic maternal outcomes. However, its pathophysiology is not well defined. There have been emerging data that in vitro fertilization may be a risk factor for placenta accreta spectrum.

      Objective

      We investigated the hypothesis that in vitro fertilization is an independent risk factor for placenta accreta spectrum.

      Study Design

      A retrospective analysis of all deliveries in a prospective, population-based cohort (2012–2019) was performed in a tertiary academic center. Primary outcome variable was placenta accreta spectrum. Univariate analysis was performed on potential risk factors for predicting placenta accreta spectrum, and a multivariate model was designed to best fit the prediction of placenta accreta spectrum adjusted for risk factors such as cesarean delivery, placenta previa, age, and parity. History of previous cesarean delivery was known as a risk factor for both placenta previa and placenta accreta spectrum; hence, the interaction between “placenta previa” and “previous cesarean delivery” was included in the final model. Odds ratios were calculated as exponential of beta coefficients from the multivariate regression analysis.

      Results

      A total of 37,461 deliveries were included in this analysis, 5464 (15%) of which had a history of cesarean delivery, 281 (0.7%) had placenta previa in their index pregnancy, and 571 (1.5%) had in vitro fertilization pregnancy. The frequency of placenta accreta spectrum was 230 (0.6%). Independent risk factors for placenta accreta spectrum were in vitro fertilization pregnancy (adjusted odds ratio, 8.7; 95% confidence interval, 3.8–20.3), history of previous cesarean delivery (adjusted odds ratio, 21.1; 95% confidence interval, 11.4–39.2), and presence of placenta previa (adjusted odds ratio, 94.6; 95% confidence interval, 29.3–305.1). After adjustment for number of previous cesarean deliveries, the correlation persisted for in vitro fertilization (adjusted odds ratio, 6.7; 95% confidence interval, 2.9–15.6).

      Conclusion

      Our data suggested that in vitro fertilization is an independent risk factor for placenta accreta spectrum, although its relative clinical importance compared with that of the presence of placenta previa and history of cesarean delivery is small. The pathophysiology behind this relationship remains to be investigated.

      Key words

      Placenta accreta spectrum (PAS) is a potentially life-threatening obstetrical condition with an increasing prevalence. Major risk factors for the development of PAS are well recognized, and most cases occur in the setting of placenta previa and 1 or more previous cesarean deliveries.
      • Silver R.M.
      • Landon M.B.
      • Rouse D.J.
      • et al.
      Maternal morbidity associated with multiple repeat cesarean deliveries.
      • Clark S.L.
      • Koonings P.P.
      • Phelan J.P.
      Placenta previa/accreta and prior cesarean section.
      • Fitzpatrick K.E.
      • Sellers S.
      • Spark P.
      • Kurinczuk J.J.
      • Brocklehurst P.
      • Knight M.
      Incidence and risk factors for placenta accreta/increta/percreta in the UK: a national case-control study.
      • Miller D.A.
      • Chollet J.A.
      • Goodwin T.M.
      Clinical risk factors for placenta previa-placenta accreta.
      However, determining additional risk factors will aid in counseling women regarding risks in both current and future pregnancies and will facilitate the detection of population at risk. This is crucial because antenatal diagnosis and development of a multidisciplinary management plan before the onset of labor or bleeding with PAS have been shown to improve outcomes and limit morbidity.
      • Shamshirsaz A.A.
      • Fox K.A.
      • Salmanian B.
      • et al.
      Maternal morbidity in patients with morbidly adherent placenta treated with and without a standardized multidisciplinary approach.
      • Erfani H.
      • Fox K.A.
      • Clark S.L.
      • et al.
      Maternal outcomes in unexpected placenta accreta spectrum disorders: single-center experience with a multidisciplinary team.
      • Shamshirsaz A.A.
      • Fox K.A.
      • Erfani H.
      • et al.
      Multidisciplinary team learning in the management of the morbidly adherent placenta: outcome improvements over time.

      Why was this study conducted?

      To investigate in vitro fertilization as an independent risk factor for placenta accreta spectrum and its clinical significance in association with other major risk factors

      Key findings

      In vitro fertilization increases the odds for placenta accreta spectrum; however, the association is less considerable than major risk factors including history of cesarean delivery and presence of placenta previa.

      What does this add to what is known?

      This study provides meaningful clinical data for patient counseling and delivery preparation in the setting of equivocal radiologic findings suggesting possible placenta accreta in a pregnancy conceived through in vitro fertilization.
      Although the complete pathophysiology underlying abnormally adherent placentation is not fully understood, the currently recognized mechanisms involve disruptions in the endometrial decidua basalis and subsequent abnormal uterine invasion by extravillous trophoblasts.
      • Tantbirojn P.
      • Crum C.P.
      • Parast M.M.
      Pathophysiology of placenta creta: the role of decidua and extravillous trophoblast.
      ,
      • Jauniaux E.
      • Collins S.
      • Burton G.J.
      Placenta accreta spectrum: pathophysiology and evidence-based anatomy for prenatal ultrasound imaging.
      At present, it is unclear whether serum estrogen and/or progesterone levels at the time of implantation play a role in either mitigating or modulating the depth or nature of invasion at the site of implantation in the presence of concomitant uterine scarring. Several studies have suggested that in vitro fertilization (IVF) and in particular cryopreserved embryo transfer cycles may increase the risk of PAS.
      • Fitzpatrick K.E.
      • Sellers S.
      • Spark P.
      • Kurinczuk J.J.
      • Brocklehurst P.
      • Knight M.
      Incidence and risk factors for placenta accreta/increta/percreta in the UK: a national case-control study.
      ,
      • Kaser D.J.
      • Melamed A.
      • Bormann C.L.
      • et al.
      Cryopreserved embryo transfer is an independent risk factor for placenta accreta.
      ,
      • Esh-Broder E.
      • Ariel I.
      • Abas-Bashir N.
      • Bdolah Y.
      • Celnikier D.H.
      Placenta accreta is associated with IVF pregnancies: a retrospective chart review.
      We hypothesized that patients who undergo IVF are at risk of developing PAS. This study aimed to investigate any independent association between IVF and PAS in the presence of major risk factors including placenta previa and previous cesarean delivery.

      Materials and Methods

      We used an institutional review board (IRB)–approved, prospectively collected perinatal database (PeriBank).
      • Antony K.M.
      • Hemarajata P.
      • Chen J.
      • et al.
      Generation and validation of a universal perinatal database and biospecimen repository: PeriBank.
      • Chu D.M.
      • Aagaard J.
      • Levitt R.
      • et al.
      Cohort analysis of immigrant rhetoric on timely and regular access of prenatal care.
      • Mendez-Figueroa H.
      • Chauhan S.P.
      • Tolcher M.C.
      • et al.
      Peripartum outcomes before and after hurricane Harvey.
      Trained research personnel maintained this database, and all women delivering at any of our university hospitals were approached to actively participate. Data on several variables including maternal and neonatal information were collected. The rate of enrollment into the perinatal database among qualified patients did not change considerably throughout the study period. Regular quarterly audits were performed to ensure data accuracy. All patients were approached and consented in their native language.
      Our study was a retrospective analysis that included a prospective cohort of patients from 2012 to 2019. Women with 2 or more deliveries within this time frame had their latest delivery selected for inclusion. There were no exclusion criteria. Approval from the IRB was obtained. All deliveries were investigated for PAS risk factors including age, number of previous cesarean deliveries, and presence of placenta previa in their index pregnancy. Our data also included pregnancy that resulted from IVF. We have a diverse patient population and received referral from several IVF practices.
      The primary outcome variable was PAS. Only subjects with histopathologic confirmation of placenta accreta, increta, or percreta were included. All risk factors were investigated as exposures including number of previous cesarean deliveries, placenta previa, age, and parity. Pregnancies complicated by placenta previa had routine serial maternal-fetal medicine ultrasound examinations throughout the second and third trimester to confirm persistent previa. We did not have the IVF protocol data available for all subjects; IVF pregnancies were included regardless of fresh or cryopreserved embryo transfers, medication protocols, or endometrial preparation methods used.
      IBM SPSS software platform version 22 was used for statistical analysis. Data were compared as appropriate using χ2 or Fisher exact test for categorical variables and Mann-Whitney U test for continuous variables. Univariate analysis was performed on potential risk factors for prediction of PAS; adjusted odds ratios (aORs), 95% confidence intervals (CIs), and 2-sided P values were calculated. Differences were considered statistically considerable if the effect estimate excluded 1.0 from the 95% CI and the 2-sided P value was <.05. A multivariate model was designed to best fit the prediction of PAS. It was adjusted for major PAS risk factors such as cesarean delivery and placenta previa and other risk factors such as age and parity. Because history of previous cesarean delivery was known as a risk factor for both placenta previa and PAS, the interaction between placenta previa and previous cesarean delivery was included in the final model. The same was implemented for the interaction between placenta previa and IVF. aORs were calculated as exponential of beta coefficients from the multivariate regression analysis. Other multivariate model subanalyses were calculated for the number of previous cesarean deliveries (none, 1, 2, 3, and 4 or more) with and without placenta previa because of the known positive association of increasing number of cesarean deliveries with PAS.

      Results

      A total of 37,461 deliveries were included in this analysis, 5464 (15%) of which had a history of at least 1 cesarean delivery, 281 (0.8%) had placenta previa, and 571 (1.5%) had undergone IVF in their index pregnancy. The frequency of PAS was 230 (0.6%). Average patients with PAS delivered 5 weeks earlier than patients without PAS (P<.001). The baseline distribution of major risk factors for PAS is summarized in Table 1. Consistent with existent reports in the literature, patients with PAS were older, delivered earlier, had a higher rate of at least 1 cesarean delivery, and were more likely to have had placenta previa in their index pregnancy. Of particular interest to our hypothesis, patients with PAS were more likely to have had an IVF pregnancy (5% vs 1.5%) (P=.003). There were more PAS subjects with increasing number of cesarean deliveries (P<.001). The characteristics of patients who had IVF pregnancy with and without PAS are listed in Table 2.
      Table 1Baseline distribution of major risk factors for placenta accreta spectrum
      Risk factorsPASNo PASP value
      n=230n=37,231
      Age33 (22, 53)30 (13, 67)<.001
      Cesarean delivery213 (93)5251 (14)<.001
      Placenta previa169 (73)112 (0.3)<.001
      IVF12 (5)559 (1.5).003
      Number of previous cesarean deliveries2 (0, 7)0 (0, 10)<.001
       017 (7)30,038 (81)<.001
       156 (24)4599 (12)
       277 (33)1928 (5)
       356 (24)479 (1)
       4 or more24 (10)187 (0.5)
      Univariate statistics for PAS factors. Data are expressed as number (%) and median (range).
      IVF, in vitro fertilization; PAS, placenta accreta spectrum.
      Salmanian et al. In vitro fertilization as an independent risk factor for placenta accreta spectrum. Am J Obstet Gynecol 2020.
      Table 2Demographic information of patients who had in vitro fertilization pregnancy (n=571) with and without placenta accreta spectrum
      CharacteristicPASNo PASP value
      n=12n=559
      Age38 (29, 53)35 (20, 67).054
      Cesarean delivery7 (58)50 (9)<.001
      Placenta previa5 (49)5 (0.9)<.001
      Number of previous cesarean deliveries1 (0, 3)0 (0, 6)<.001
       05 (42)485 (87)<.001
       16 (50)46 (8)
       20 (0)20 (3)
       31 (8)4 (1)
       4 or more0 (0)4 (1)
      Data are expressed as number (%) and median (range).
      IVF, in vitro fertilization; PAS, placenta accreta spectrum.
      Salmanian et al. In vitro fertilization as an independent risk factor for placenta accreta spectrum. Am J Obstet Gynecol 2020.
      To estimate the independent association of each risk factor for PAS, a multivariate logistic regression model was designed to consider the interaction of placenta previa with history of cesarean delivery and IVF pregnancy. IVF to achieve index pregnancy was found to be an independent risk factor for PAS (aOR, 8.7; 95% CI, 3.8–20.3), as were history of previous cesarean delivery (aOR, 21.1; 95% CI, 11.4–39.2) and presence of placenta previa (aOR, 94.6; 95% CI, 29.3–305.1). When adjusted for the number of previous cesarean deliveries as a continuous variable, the correlation persisted for IVF (aOR, 6.7; 95% CI, 2.9–15.6). The aORs for an increasing number of cesarean deliveries are listed in Table 3. The odds of PAS increased with increasing number of cesarean deliveries from aOR of 10.1 (95% CI, 5.1–20.2) for 1 previous cesarean delivery to aOR of 49.1 (95% CI, 17.0–141.7) for 4 or more cesarean deliveries, when compared with the reference of no previous cesarean deliveries.
      Table 3Adjusted odds ratios with 95% confidence interval for placenta accreta spectrum
      Risk factorsaOR (95% CI)
      History of cesarean delivery21.1 (11.4–39.2)
      Placenta previa94.6 (29.3–305.1)
      IVF8.7 (3.8–20.3)
      1 previous cesarean delivery10.1 (5.1–20.2)
      Compared with history of no cesarean delivery.
      2 previous cesarean deliveries13.7 (6.3–29.9)
      Compared with history of no cesarean delivery.
      3 previous cesarean deliveries34.5 (14.1–84.6)
      Compared with history of no cesarean delivery.
      4 or more previous cesarean deliveries49.1 (17.0–141.7)
      Compared with history of no cesarean delivery.
      Numbers represent the multivariate analysis for developing PAS including the following major risk factors: cesarean delivery; previa; age; parity; the interaction between cesarean and placenta previa; and the interaction between IVF and placenta previa. Multivariate model subanalyses were also calculated for the number of previous cesarean deliveries.
      aOR; adjusted odds ratio; CI, confidence interval; IVF, in vitro fertilization.
      Salmanian et al. In vitro fertilization as an independent risk factor for placenta accreta spectrum. Am J Obstet Gynecol 2020.
      a Compared with history of no cesarean delivery.
      Among subjects without a history of cesarean delivery, placenta previa, or IVF, 8 (0.02%) had PAS (Table 4). Among women with PAS, 69.6% had a history of previous cesarean deliveries and concurrent placenta previa, whereas an additional 20% only had a history of previous cesarean deliveries. Among patients who had PAS in the setting of IVF pregnancy, 7 (58%) had at least placenta previa or a history of cesarean delivery, 2 (17%) had a history of uterine surgery other than cesarean delivery without placenta previa, and 3 (25%) did not have any other risk factors including previous uterine surgery of any kind. Of note, there were 5 patients who had previous cesarean deliveries, placenta previa, and IVF in the index pregnancy. All 5 had PAS (100%).
      Table 4Frequency of placenta accreta spectrum with 95% confidence interval based on history of cesarean delivery, presence of placenta previa, in patients with and without in vitro fertilization pregnancy; N=37,461 (the whole cohort)
      Placenta previaHistory of cesarean deliveryTotal numberPAS (%)95% CI
      Patient with IVF pregnancy
      NoNo5095 (1)0.1–1.8
      YesNo50-
      NoYes522 (3.8)−1.4–9.1
      YesYes55 (100)1–1
      Patient without IVF pregnancy
      YesYes179160 (89.4)84.9–93.9
      YesNo924 (4.3)0.2–8.5
      NoYes522846 (0.9)0.6–1.1
      NoNo31,3918 (0.02)0–0.1
      Data are expressed as number (%) with 95% confidence interval (CI).
      CI, confidence interval; IVF, in vitro fertilization; PAS, placenta accreta spectrum.
      Salmanian et al. In vitro fertilization as an independent risk factor for placenta accreta spectrum. Am J Obstet Gynecol 2020.

      Comment

      Principal findings and results

      In this study, the prevalence of PAS was found to be 0.6%, which is higher than the previously reported prevalence of 0.17%.
      • Jauniaux E.
      • Bunce C.
      • Grønbeck L.
      • Langhoff-Roos J.
      Prevalence and main outcomes of placenta accreta spectrum: a systematic review and meta-analysis.
      This reflects that our hospital is a PAS referral center. Furthermore, our data support the important role that history of previous cesarean deliveries and placenta previa play in predicting PAS. Similarly, our findings are consistent with previously reported higher prevalence of PAS with increasing number of cesarean deliveries.
      • Silver R.M.
      • Landon M.B.
      • Rouse D.J.
      • et al.
      Maternal morbidity associated with multiple repeat cesarean deliveries.
      ,
      • Clark S.L.
      • Koonings P.P.
      • Phelan J.P.
      Placenta previa/accreta and prior cesarean section.
      ,
      • Jauniaux E.
      • Bunce C.
      • Grønbeck L.
      • Langhoff-Roos J.
      Prevalence and main outcomes of placenta accreta spectrum: a systematic review and meta-analysis.
      Of note, we also reported that IVF is an additional independent risk factor for PAS after adjusting for other factors such as maternal age, placenta previa, and number of previous cesarean deliveries.

      Clinical and research implications

      The mechanism by which IVF might increase the risk of PAS is uncertain. One study found a higher risk of PAS in pregnancies resulting from frozen-thawed embryo transfer during a medicated embryo transfer cycle compared with results of the same procedure performed during a natural ovulatory cycle.
      • Saito K.
      • Kuwahara A.
      • Ishikawa T.
      • et al.
      Endometrial preparation methods for frozen-thawed embryo transfer are associated with altered risks of hypertensive disorders of pregnancy, placenta accreta, and gestational diabetes mellitus.
      This might suggest a possible association with hormonal preparation protocols used during IVF and embryo transfer and the thickness of endometrial lining and decidual layer, the degree of trophoblastic invasion, and/or the extent of vascular remodeling at the time of implantation. Others have suggested that the transfer of cryopreserved embryos itself can be an important independent risk factor for PAS, even after controlling for patient age, previous cesarean deliveries, placenta previa, and/or uterine factor infertility.
      • Kaser D.J.
      • Melamed A.
      • Bormann C.L.
      • et al.
      Cryopreserved embryo transfer is an independent risk factor for placenta accreta.
      Taken together, these observations collectively suggest that there may be heretofore underappreciated interactions between the freeze and/or thaw process and mode of uterine preparation that may lead to increased risk of abnormal implantation resulting in a higher rate of PAS in the resultant pregnancy.
      • Simon C.
      • Domínguez F.
      • Valbuena D.
      • Pellicer A.
      The role of estrogen in uterine receptivity and blastocyst implantation.
      ,
      • Ishihara O.
      • Araki R.
      • Kuwahara A.
      • Itakura A.
      • Saito H.
      • Adamson G.D.
      Impact of frozen-thawed single-blastocyst transfer on maternal and neonatal outcome: an analysis of 277,042 single-embryo transfer cycles from 2008 to 2010 in Japan.
      Several underlying cellular or molecular mechanisms may potentially explain these collective observations, linking IVF (and particularly frozen-thawed embryo transfer IVF) with PAS. One such possibility is that aberrant placentation may be the end result of elevated serum estrogen levels at the time of embryo implantation, which may enhance trophoblastic invasion through the endometrium.
      • Simon C.
      • Domínguez F.
      • Valbuena D.
      • Pellicer A.
      The role of estrogen in uterine receptivity and blastocyst implantation.
      Another possible mechanism that might explain our observed association between frozen-embryo IVF and PAS, both dependent and independent of previous cesarean deliveries, would be that both the degree of trophoblastic invasion and extent of vascular remodeling at the time of implantation may be inversely related to serum estradiol levels.
      • Simon C.
      • Domínguez F.
      • Valbuena D.
      • Pellicer A.
      The role of estrogen in uterine receptivity and blastocyst implantation.
      Lower serum estradiol levels (associated with frozen-embryo transfer cycles compared with fresh cycles) in conjunction with the presence of a thinner decidualized endometrium may result in excessive trophoblastic growth during a prolonged window of implantation, which ultimately manifests as PAS.
      • Kaser D.J.
      • Melamed A.
      • Bormann C.L.
      • et al.
      Cryopreserved embryo transfer is an independent risk factor for placenta accreta.
      A third possible mechanism that may explain our observed association between IVF and PAS is the cellular pathways that are altered when fertilization and early embryo culture occur in vitro. These processes are both inherent and unique to IVF and may change key metabolic pathways in the embryo and eventual trophoblast that signal to alter the endometrial environment in the first week of pregnancy during implantation.
      • Leese H.J.
      • Donnay I.
      • Thompson J.G.
      Human assisted conception: a cautionary tale. Lessons from domestic animals.
      The increased adjusted odds of PAS (aOR, 8.7; 95% CI, 3.8–20.3) in IVF patients among our cohort suggest an independent role of IVF as a risk factor for PAS. This was adjusted for PAS risk factors such as cesarean delivery, placenta previa, age, and parity. However, the magnitude of IVF aOR as a risk factor for PAS is relatively small compared with that of having a history of previous cesarean delivery (aOR, 21.1; 95% CI, 11.4–39.2) and the presence of placenta previa (aOR, 94.6; 95% CI, 29.3–305.1). Indeed, aOR for IVF as a risk factor for PAS is even less than that of 1 previous cesarian delivery without placenta previa (Table 3). However, given that the rate of IVF is increasing nationally, it adds to the clinical implication of this association.

      Strengths and limitations

      The strengths of this study include a greater number of gravidae with PAS in our database than in those of previous studies investigating the role of IVF in PAS. We also included only women with PAS who had histopathologic confirmation, thus excluding other morbid conditions that may be clinically labeled as adherent placenta in the presence of postpartum hemorrhage. However, given our status as a level IV referral center for patients with PAS, our data also include a larger percentage of women with deeply invasive disease compared with the general population. We would not expect such a bias to affect our principal observations.
      Our study is not without limitations. First, as with any retrospective analysis, the strength of our findings is limited by the prevalence of rare outcomes. Our dataset did not allow a distinction among risks associated with different types of IVF such as fresh vs cryopreserved embryo transfer, different types of ovarian stimulation medication protocols, or mode of uterine preparation for embryo transfer, which may have affected our results. Thus, potential mechanisms explaining the observed independent association between IVF and PAS remain speculative and will be the focus of future studies.

      Conclusion

      Our data indicate that IVF is an independent risk factor for PAS, although its relative clinical importance compared with that of the presence of placenta previa and history of cesarean delivery is small. However, in the presence of equivocal radiologic findings suggesting possible PAS, a history of IVF conception may appropriately be considered as clinically meaningful in terms of patient counseling and delivery preparation. Although much remains unknown regarding the pathophysiology underlying PAS, the presence of a uterine scar in combination with placenta previa seems to be of a higher clinical relevance than a uterine scar co-occurring in the setting of an IVF pregnancy. Our data do not support withholding IVF in the setting of a previous cesarean delivery for the purpose of reducing the risk of occurrence of PAS in clinically meaningful ways, but we do support counseling patients with objective data before conception to allow full informed consent before IVF.

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      Linked Article

      • In vitro fertilization and placenta accreta spectrum in pregnancies with a history of cesarean delivery
        American Journal of Obstetrics & GynecologyVol. 225Issue 2
        • Preview
          The cesarean delivery (CD) rate in China has risen sharply during the past decade, from 28.8% in 2008 to 36.7% in 2018.1 As China relaxed its 1 child policy, the proportion of pregnant women with a previous CD has almost doubled, increasing from 9.8% in 2012 to 17.7% in 2016.2 The in vitro fertilization (IVF) pregnancies confer an increased risk of adverse obstetrical outcomes. The uterine scar secondary to CD is the main cause of the placenta accreta spectrum (PAS).3 To accurately evaluate the risk of PAS in IVF and non-IVF pregnant women with a previous CD is critical in allowing for proper counseling, preparation, and optimizing outcomes.
        • Full-Text
        • PDF
      • In vitro fertilization as an independent risk factor for placenta accreta spectrum
        American Journal of Obstetrics & GynecologyVol. 225Issue 6
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          Salmanian et al1 discussed the possible effects of less physiological levels of estradiol on the risk of placenta accrete spectrum (PAS) development in in vitro fertilization (IVF) cycles, especially in frozen embryo transfer (FET) cycles, through manipulating the process of normal implantation and placentation. To date, the exact effect of altered levels of estradiol on endometrial microenvironment around the time of implantation remains uncertain. In this letter, we will explain one mechanism by which altered levels of estradiol could modulate the process of normal placentation.
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