Impact of IVF/ICSI on Grades of Placenta Accreta Spectrum Disorders and Pregnancy Outcomes

doi:10.21203/rs.3.rs-4983277/v1

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Research Article

Impact of IVF/ICSI on Grades of Placenta Accreta Spectrum Disorders and Pregnancy Outcomes

https://doi.org/10.21203/rs.3.rs-4983277/v1

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Objective

To investigate the impact of IVF/ICSI on grades of placenta accreta spectrum disorders and pregnancy outcomes.

Methods

Placenta accreta spectrum disorders patients who underwent cesarean section at a single clinical center from January 2018 to March 2023 were retrospectively included in this study. Baseline characteristics and outcomes were compared between the IVF/ICSI group and the spontaneous conception group. Binary logistic regression was used to explore the risk factors associated with adverse outcomes related to IVF/ICSI. A 1:1 ratio propensity score matching (PSM) was conducted to minimize selection bias between the two groups. Data analysis was performed using SPSS (version 25.0) software.

Results

No increase in the incidence of grades placenta was detected for IVF/ICSI group, and the difference is not statistically significant (P = 0.290). PAS grading is not associated with IVF/ICSI (OR = 0.76, 95%CI: 0.45 ~ 1.27, P = 0.290). In contrast, a significant risk factor for postpartum hemorrhage (OR = 9.20, 95%CI: 2.68 ~ 9.22, P < 0.001) and red cells transfusion ≥ 4U (OR = 3.71,95%CI:1.21 ~ 11.33, P = 0.021) was observed in IVF/ICSI group. No additional adverse pregnancy outcomes arose as a result of IVF/ICSI.

Conclusion

It is necessary to further investigation into the potential risk factors that might impact PAS grading. It has been shown that IVF/ICSI treatment is associated with a higher risk of postpartum hemorrhage and blood transfusion requirements. Therefore, in order to provide patients the best chance of recovery, professionals must carefully evaluate the patient's health as well as the available treatment options.

IVF/ICSI

grades of placenta

outcomes

postpartum hemorrhage

transfusion

Placenta accreta spectrum (PAS) disorders refer to a group of conditions characterized by the abnormal invasion of placental villi into the uterine muscle to varying degrees (Jauniaux and Ayres-de-Campos, 2018). According to the clinical diagnostic criteria established by the International Federation of Obstetrics and Gynecology (FIGO) in 2019, PAS can be classified into grades 1–3. Grade 1 is termed adherent placenta, indicating that the placental villi adhere to the surface of the uterine muscle, while grades 2–3 are referred to as invasive placenta, signifying that the placental villi implant and penetrate into the uterine muscle (Jauniaux et al., 2019). PAS can result in serious adverse outcomes such as preterm birth, postpartum hemorrhage, acute organ failure, hemorrhagic shock, disseminated intravascular coagulation (DIC), and even maternal mortality (Fonseca and Ayres, 2021). Accumulating evidence has established a firm link between the depth of placental villous invasion and poor prognosis (Marcellin et al., 2018; Zhang et al., 2019; Riveros-Perez and Wood, 2018).

PAS is associated with primary uterine abnormalities or secondary structural damage to the uterine wall (jauniaux et al., 2018). Recent years have seen an increase in individuals conceiving through in vitro fertilization (IVF) or intracytoplasmic sperm injection (ICSI) (hanevik and hessen, 2022). Some studies suggest that these patients are at a higher risk to suffer (or develop) PAS (fitzpatrick et al., 2012, sugai et al., 2023). However, whether invasive placenta is the cause remains an area requiring further investigation. Given the rising utilization of IVF/ICSI in China (qiao et al., 2021), it is clinically significant to explore the impact of these assisted reproductive technologies on grades of PAS and pregnancy outcomes.

Patients

The Department of Obstetrics and Gynecology at the Third Affiliated Hospital of Guangzhou Medical University serves as the critical care center for obstetrics and gynecology in Guangdong Province, providing comprehensive treatment to critically ill patients from across the region. We conducted a retrospective study on patients with PAS who underwent cesarean section delivery at our hospital between January 1, 2018 and March 31, 2023. The study adhered to the principles outlined in the World Medical Association Declaration of Helsinki and received approval from the Ethics Committee of the Third Affiliated Hospital of Guangzhou Medical University (approval number: 20221106). All participants provided informed consent during their hospitalization, granting permission for their clinical data to be used in research while safeguarding their privacy.

Inclusion and exclusion criteria

A total of 1007 patients were diagnosed with PAS and underwent cesarean section delivery. The classification system for PAS conforms to the clinical diagnosis criteria issued by FIGO in 2019 (Jauniaux et al., 2019). Exclusion criteria included gestational age less than 28 weeks (n = 33) and incomplete clinical data (n = 0). A total of 974 patients meet the inclusion criteria and are included in the study.

Data collection

Through the "Perinatal Medicine Database" and "Reproductive Medicine Database" established by the Third Affiliated Hospital of Guangzhou Medical University, we collected basic clinical characteristics of enrolled patients including age, body mass index, gravidity, parity, number of vaginal deliveries, number of cesarean sections, number of induced abortions, other etiologies of accreta placentation, progesterone supplementation in miscarriage prevention, scar pregnancy, placental location, vaginal bleeding, and placenta previa; maternal outcomes including PAS grades, postpartum hemorrhage, red blood cells transfusion ≥ 4U, and hysterectomy; and neonatal outcomes including preterm birth, neonatal birth weight, neonatal admission to NICU.

Propensity score matching

We used propensity score matching (PSM) to balance the clinical baseline characteristics between spontaneous conception group and IVF/ICSI group, thereby minimizing bias. The matching ratio is 1:1, with a caliper value of 0.02 SD. In the matching process, we took into consideration the clinical baseline characteristics, including age, body mass index, gravidity, parity, number of vaginal deliveries, number of cesarean sections, number of induced abortions, other etiologies of accreta placentation, progesterone supplementation in miscarriage prevention, scar pregnancy, placental location, vaginal bleeding and placenta previa.

Statistical analysis

The SPSS 25.0 software was utilized for data analysis. Quantitative data with non-normal distribution was denoted as M(P25 ~ P75), and inter-group comparisons were conducted using non-parametric tests. Frequency and rate are reported for the counting data, with inter-group comparisons performed using the χ2 test or Fisher’s exact test. Conditional logistic regression analysis was utilized to calculate odds ratios (OR) and corresponding 95% confidence intervals (CI) to explore the impact of IVF/ICSI on the grading of PAS; and pregnancy outcomes. A significance level of P < 0.05 is adopted.

A total of 974 eligible patients were enrolled in the study based on predefined inclusion and exclusion criteria. Among them, 820 (84.2%) patients belonged to the spontaneous conception group, with 154 (15.8%) the IVF/ICSI group. After propensity score matching, each group is comprised of 123 patients. The matching rate for the IVF/ICSI group is 79.87%. (Refer to Fig. 1)

Assessment of the efficacy of PSM on correcting baseline characteristics bias

Before propensity score matching (PSM), the IVF/ICSI group exhibits significantly higher age (P = 0.001), a greater number of advanced age cases (P = 0.001), and increased progesterone supplementation in miscarriage prevention (P < 0.001) compared to the spontaneous conception group. Conversely, the spontaneous conception group demonstrates significantly higher gravidity (P < 0.001), parity (P < 0.001), cesarean sections (P < 0.001), induced abortions (P < 0.001), anterior placenta (P < 0.001), and placenta previa (P < 0.001) than the IVF/ICSI group. After PSM, no statistically significant differences were observed in all baseline characteristics between the two groups (P > 0.05). (Refer to Table 1)

Table 1

Baseline characteristics before and after PSM
Characteristics	Before PSM			After PSM
Characteristics	Spontaneous conception (n = 820)	IVF/ICSI pregnancy (n = 154)	P value	Spontaneous conception (n = 123)	IVF/ICSI pregnancy (n = 123)	P Value
Age [Year,M(P25 ~ P75 )]	34(30 ~ 37)	35(33 ~ 39)	0.001	35(32 ~ 37)	35(33 ~ 38)	0.403
Advanced age [n(%)]	370(45.1)	91(59.1)	0.001	64(52.0)	72(58.5)	0.097
Body mass index [kg/m²,n(%) ]			0.469			0.825
< 18.5	88(10.7)	13(8.4)		13(10.6)	11(8.9)
18.5 ~ 24	555(67.7)	103(66.9)		87(70.7)	88(71.5)
24 ~ 28	140(17.1)	33(21.4)		18(14.6)	21(17.1)
≥ 28	37(4.5)	5(3.3)		5(4.1)	3(2.4)
Gravidity [M(P25 ~ P75)]	4(3 ~ 5)	3(2 ~ 4)	< 0.001	3(2 ~ 4)	3(2 ~ 4)	0.989
Parity [M(P25 ~ P75)]	1(1 ~ 2)	0(0 ~ 1)	< 0.001	0(0 ~ 1)	0(0 ~ 1)	1.000
Number of vaginal deliveries [M(P25 ~ P75)]	0(0 ~ 0)	0(0 ~ 0)	0.332	0(0 ~ 0)	0(0 ~ 0)	0.704
Number of cesarean deliveries [n(%)]			< 0.001			0.899
0	253(30.9)	108(70.1)		79(64.2)	78(63.4)
1	386(47.1)	36(23.4)		35(28.5)	35(28.5)
2	167(20.4)	9(5.8)		7(5.7)	9(7.3)
≥ 3	14(1.7)	1(0.6)		2(1.6)	1(0.8)
Number of induced abortions [n(%)]			0.001			0.693
0	429(52.3)	106(68.8)		70(56.9)	79(64.2)
1	208(25.4)	30(19.5)		33(26.8)	28(22.8)
2	116(14.1)	13(8.4)		13(10.6)	11(8.9)
≥ 3	67(8.2)	5(3.2)		7(5.7)	5(4.1)
Other etiologies of accreta placentation [n(%)]	303(37.0)	64(41.6)	0.279	48(39.0)	49(39.8)	0.896
Progesterone supplementation in miscarriage prevention [n(%)]	156(19.0)	61(39.6)	< 0.001	41(33.3)	41(33.3)	1.000
Scar pregnancy [n(%)]	61(7.4)	8(5.2)	0.319	7(5.7)	6(4.9)	0.776
Placental location [n(%)]			< 0.001			0.258
Anterior wall	462(56.3)	66(42.9)		61(49.6)	59(48.0)
Posterior wall	221(27.0)	66(42.9)		36(29.3)	46(37.4)
Others	137(16.7)	22(14.3)		26(21.1)	18(14.6)
Vaginal bleeding [n(%)]	245(29.9)	43(27.9)	0.626	42(34.1)	33(26.8)	0.213
Placenta previa [n(%)]	531(64.8)	53(34.4)	< 0.001	43(35.0)	48(39.0)	0.509
Advanced age :age ≥ 35years

Other etiologies of accreta placentation: uterine curettage, manual delivery of the placenta,IUD,postpartum endometritis, hysteroscopic surgery, myomectomy for endometrial injury, etc.

Comparison of maternal and neonatal outcomes before and after PSM

Before propensity score matching (PSM), the IVF/ICSI group shows a lower incidence of invasive placenta (P < 0.001), postpartum hemorrhage (P < 0.001), red blood cells transfusion ≥ 4U (P < 0.001), and preterm delivery (P < 0.001) compared to the spontaneous conception group. No significant differences in hysterectomy (P = 0.254), birth weight (P = 0.399), and the number of newborns admitted to the NICU (P = 0.301) between the two groups were detected. After PSM, the IVF/ICSI group exhibits a significantly higher incidence of postpartum hemorrhage (P < 0.001) and red blood cells transfusion ≥ 4U (P = 0.044). In contrast, there are no statistically significant differences in PAS grades (P = 0.290), hysterectomy (P = 0.424), gestational weeks (P = 0.927), birth weight (P = 0.816), and the number of NICU admissions (P = 0.301) between the two groups (refer to Table 2).

Table 2

Maternal and neonatal outcomes before and after PSM
Outcomes	Before PSM			After PSM
Outcomes	Spontaneous conception (n = 820)	IVF/ICSI pregnancy (n = 154)	P value	Spontaneous conception (n = 123)	IVF/ICSI pregnancy (n = 123)	P value
Maternal outcome
PAS Grades [n(%)]			< 0.001			0.290
Placenta crete	313(38.2)	103(66.9)		74(60.2)	82(66.7)
Placenta increta	459(56.0)	50(32.5)		45(36.6)	40(32.5)
Placenta percreta	48(5.9)	1(0.7)		4(3.3)	1(0.8)
Postpartum hemorrhage [n(%)]	313(38.2)	25(16.2)	< 0.001	3(2.4)	23(18.7)	< 0.001
Red blood cells transfusion ≥ 4U [n(%)]	163(19.9)	13(8.4)	< 0.001	5(4.1)	13(10.6)	0.044
Hysterectomy [n(%)]	159(19.4)	6(3.9)	0.254	9(7.3)	6(4.9)	0.424
Neonatal outcome
Birth weeks [wk,n(%)]			< 0.001			0.927
≥ 28 ~ 34*	103(12.6)	22(14.3)		19(15.4)	18(14.6)
34 ~ 37*	377(46.0)	37(24.0)		33(26.8)	31(15.2)
≥ 37	340(41.5)	95(61.7)		71(57.7)	74(60.2)
Birth weight [g,n(%)]			0.399			0.816
<1500	37(4.5)	10(6.5)		8(6.5)	9(7.3)
1500 ~ 2500	224(27.3)	36(23.4)		29(23.6)	25(20.3)
≥ 2500	559(68.2)	108(70.1)		86(69.9)	89(72.4)
NICU [n(%)]	28(3.4)	2(1.3)	0.301	34(27.6)	27(22.0)	0.301

*preterm delivery

Conditional Logistic Regression Analysis

We then carried out conditional logistic regression analysis and found no link between IVF/ICSI treatment and the grades of PAS (OR = 0.76, 95% CI: 0.45–1.27, P = 0.290).

In addition, IVF/ICSI did not increase the risk of hysterectomy (OR = 0.65, 95% CI: 0.22–1.88, P = 0.427), preterm birth (OR = 0.90, 95% CI: 0.54–1.50, P = 0.697), low birth weight infants (< 2500 g) (OR = 0.89, 95% CI: 0.51–1.54, P = 0.673), or neonates admitted to the NICU (OR = 0.66, 95% CI: 0.11–4.03, P = 0.654). Strikingly, however, IVF/ICSI was identified as a risk factor for postpartum hemorrhage (OR = 9.20, 95% CI: 2.68–9.20, P < 0.001) and red blood cell transfusion ≥ 4U (OR = 3.71, 95% CI: 1.21–11.33, P = 0.021 (Refer to Table 3)

Table 3

Conditional Logistic Regression Analysis
Outcomes	OR	95%CI	P value
PAS grades	0.76	(0.45 ~ 1.27)	0.290
Postpartum hemorrhage	9.20	(2.68 ~ 9.22)	<0.001
Red blood cells transfusion ≥ 4U	3.71	(1.21 ~ 11.33)	0.021
Hysterectomy	0.65	(0.22 ~ 1.88)	0.427
Birth week<37	0.90	(0.54 ~ 1.50)	0.697
Birth weight<2500g	0.89	(0.51 ~ 1.54)	0.673
NICU	0.66	(0.11 ~ 4.03)	0.654

Applying propensity score matching effectively rectify confounding biases

Propensity Score Matching (PSM) effectively mitigates selection bias in observational studies, allowing a more reliable assessment of treatment or intervention impacts on study outcomes. Without PSM, we found that advanced age (P = 0.001) (Yin et al., 2024), progesterone supplementation in miscarriage prevention (P < 0.001) (Matsuzaki et al., 2021), gravidity (P < 0.001) (Zhao et al., 2024), parity (P < 0.001) (Zhao et al., 2024), cesarean sections (P < 0.001) (Calì et al., 2013), induced abortions (P < 0.001) (Li et al., 2023), and anterior wall (P < 0.001) (Zhu and Xie, 2019) and placenta previa (P < 0.001) (Kayem et al., 2024) are associated with PAS. When these baseline features are statistically different and have impacts on PAS, it cannot effectively explain whether PAS is related to IVF/ICSI. By ensuring consistency in individual baseline features across different groups and accounting for the confounding variables, PSM enhances internal validity and credibility of the research results (Huang Lihong and ChenFeng, 2019).

Impact of IVF/ICSI on grades of PAS

Currently, there is a lack of robust evidence regarding risk factors for PAS grades, due to the low incidence of PAS and an overreliance on pathological diagnosis. Over the past 40 years, the incidence rate of PAS has increased tenfold globally, ranging from 0.01–1.1% (Jauniaux et al., 2019). Prior to the publication of clinical grading criteria, the grading of PAS relied solely on the pathologist's conclusions. However, the proportion of patients undergoing partial or total hysterectomy due to PAS remains small. It is plausible that only a portion of the placenta is abnormally implanted, leading to false negatives in pathological diagnoses. Consequently, studies focusing solely on grades of PAS based on pathological findings are scarce.

In recent years, as morbidity and adverse outcomes associated with PAS have risen, attention has shifted toward understanding risk factors for PAS classification. A multicenter retrospective study in the United States revealed that PAS incidence increases with the number of cesarean sections (ranging from 3–67% for 1 to 5 prior cesarean sections) (Calì et al., 2013). However, another meta-analysis found that placenta previa combined with cesarean section histories does not significantly affect PAS classification (Jauniaux and Bhide, 2017).

Considering the impact of placenta previa and cesarean section histories on PAS, we turned our attention to IVF/ICSI. IVF/ICSI conception has been found by several groups to be associated with PAS incidence (Hou et al., 2021, Kyozuka et al., 2019). In our study, we found no statistically significant difference in PAS grades between IVF/ICSI pregnancies and spontaneous pregnancies (P = 0.290). Furthermore, conditional logistic regression analysis also shows that IVF/ICSI does not affect the PAS grades (OR = 0.76, 95% CI: 0.45–1.27, P = 0.290). The effect of IVF/ICSI conception on PAS grades may be related to the endometrial thickness and estrogen levels (Matsuzaki et al., 2021).

IVF/ICSI potentially raises risk of postpartum bleeding and blood transfusion

In this study, we found that IVF/ICSI conception is associated with an increased risk of postpartum hemorrhage (OR = 9.20, 95% CI: 2.68–9.20, P < 0.001) and red blood cells transfusion ≥ 4U (OR = 3.71, 95% CI: 1.21–11.33, P = 0.021). These findings align with a retrospective cohort study that compared postnatal bleeding in 1064 IVF/ICSI pregnancies with 2059 spontaneous pregnancies. The incidence of severe postnatal bleeding is significantly higher in single pregnancies resulting from IVF/ICSI (aOR = 1.58, 95% CI: 1.12–2.24, P = 0.010) compared to spontaneous conceptions (Nyfløt et al., 2017).

While propensity score matching corrected for confounding factors related to postpartum hemorrhage (such as advanced age, placenta previa, and grades), some variables remain unaccounted for. Detailed records of IVF/ICSI treatment specifics (e.g., anticoagulant drug dosages and withdrawal times) and reasons for using IVF/ICSI (e.g., endometriosis) are not available in the case records. These unmeasured factors may contribute to the increased risk observed. Notably, IVF/ICSI pregnancies represent a high-risk group for postpartum hemorrhage, emphasizing the importance of vigilant hemoglobin management during pregnancy and preparedness for blood product storage. If necessary, transferring patients to hospitals with rescue capabilities is advisable.

Limitations of this study

While this study provides valuable insights, it is essential to acknowledge its limitations. The data are derived from a single-center with a limited sample size. Although propensity score matching adjusts for numerous confounding factors, it only balances observed indicator variables. Additionally, SPSS propensity score matching achieves 1:1 matching between the experimental and control groups based on propensity scores but does not assess the balance of matched data. These limitations may introduce outcome bias. To validate the findings, prospective multi-center, large-sample case-control studies are warranted.

In summary, although IVF/ICSI conception is associated with the incidence of PAS, it does not influence PAS grades. However, it’s imperative to look for de novo risk factors affecting PAS severity. While IVF/ICSI pregnancies adds to the risk of postpartum bleeding and blood transfusion, they do not increase hysterectomy rates or adverse neonatal outcomes. Clinicians should consider patients’ expectations, medical history, local delivery management, and assistance capabilities when assessing IVF/ICSI pregnancy prognosis

Disclosure

Author Contributions: conceptualization, Miao Hu, Lili Du, Shuang Zhang and Dunjin Chen; methodology, Miao Hu and Lizi Zhang; software and analysis, Miao Hu ,Shuang Zhang, Lili Du and Dunjin Chen; Validation, Miao Hu, Lin Lin and Lizi Zhang; resources, Lili Du,Shuang Zhang and Dunjin Chen, data curation, Yuliang Zhang, Shifeng Gu, Zhongjia Gu, JingYing Liang, Siying Lai, Yu Liu, Minshan Huang, Yuanyuan Huang, Qingqing Huang,Shijun Luo.

Founding

National Key R&D Program (2022YFC2704501, 2022YFC2704503)

Institutional Review Board Statement:

The study adheres to the principles outlined in the World Medical Association Declaration of Helsinki and received approval from the Ethics Committee of the Third Affiliated Hospital of Guangzhou Medical University (approval number: 20221106).

Informed Consent Statement: All participants provided informed consent during their hospitalization, granting permission for their clinical data to be used in research while safeguarding their privacy.

Data Availability Statement: Data supporting the study results can be provided by the request to the corresponding author.

Conflicts of Interest: None.

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No competing interests reported.

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Impact of IVF/ICSI on Grades of Placenta Accreta Spectrum Disorders and Pregnancy Outcomes

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Abstract

Objective

Methods

Results

Conclusion

Figures

Introduction

Data and methods

Patients

Inclusion and exclusion criteria

Data collection

Propensity score matching

Statistical analysis

Results

Comparison of maternal and neonatal outcomes before and after PSM

Conditional Logistic Regression Analysis

Discussion

Applying propensity score matching effectively rectify confounding biases

Impact of IVF/ICSI on grades of PAS

IVF/ICSI potentially raises risk of postpartum bleeding and blood transfusion

Limitations of this study

Conclusion

Declarations

References

Additional Declarations

Status:

Version 1