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. Author manuscript; available in PMC: 2022 Dec 16.
Published in final edited form as: Am J Perinatol. 2021 Dec 2;39(8):830–835. doi: 10.1055/s-0041-1740212

Changes in the Antenatal Utilization of High-Risk Obstetric Services and Stillbirth Rate during the COVID-19 Pandemic

Megan C Oakes 1, Fan Zhang 1, Lori Stevenson 2, Bree Porcelli 1, Ebony B Carter 1, Nandini Raghuraman 1, Jeannie C Kelly 1
PMCID: PMC9757080  NIHMSID: NIHMS1766350  PMID: 34856612

Abstract

Objective

The primary objective of this study was to evaluate coronavirus 2019 (COVID-19) pandemic–related changes in the antenatal utilization of high-risk obstetric services. Our secondary objective was to characterize change in stillbirth rate during the pandemic.

Study Design

This is a retrospective, observational study performed at a single, tertiary care center. Maternal-Fetal Medicine (MFM) visits, ultrasounds, and antenatal tests of fetal well-being during the pandemic epoch (2020), which spans the first 12 weeks of the year to include pandemic onset and implementation of mitigation efforts, were compared with the same epoch of the three preceding years visually and using general linear models to account for week and year effect. An analysis of stillbirth rate comparing the pandemic time period to prepandemic was also performed.

Results

While there were decreased MFM visits and antenatal tests of fetal well-being during the pandemic epoch compared with prepandemic epochs, only the decrease in MFM visits by year was statistically significant (p < 0.001). The stillbirth rate during the pandemic epoch was not significantly different when compared with the prepandemic period and accounting for both week (p = 0.286) and year (p = 0.643) effect.

Conclusion

The COVID-19 pandemic resulted in a significant decrease in MFM visits, whereas obstetric ultrasounds and antenatal tests of fetal well-being remained unchanged. While we observed no change in the stillbirth rate compared with the prepandemic epoch, our study design and sample size preclude us from making assumptions of association. Our findings may support future work investigating how changes in prenatal care for high-risk obstetric patients influence perinatal outcomes.

Keywords: COVID-19, SARS-CoV-2, SARS, coronavirus, high-risk pregnancy, maternal-fetal medicine, antenatal, ultrasound

The coronavirus 2019 (COVID-19) pandemic has taken an unprecedented toll on the U.S. health care delivery system. Across all specialties, the sudden and severe nature of the pandemic has forced health care providers and patients to reconsider the frequency and manner in which care is delivered. Consequently, various obstetric care clinical guidelines and pathways emerged, offering recommendations for streamlining visits, ultrasounds, and antenatal tests of fetal well-being (nonstress tests, biophysical profiles, and umbilical artery Doppler studies) to mitigate exposure risk for both the pregnant patient and provider.1–6 While practical and necessary, the implications of pared back obstetric care, particularly for high-risk patients, have yet to be fully explored.

Across the world, several studies have cited an alarming increased incidence in stillbirth during the COVID-19 pandemic that is not attributable to acute maternal COVID-19 infection.7–16 However, the heterogeneity of these studies makes it challenging to identify factors that might contribute to these findings. Several authors have posited that modifications to prenatal care may have a role; yet, the extent of how these have influenced stillbirth rates remains to be clarified.17 Our primary objective was to characterize changes in antenatal utilization of high-risk obstetric services and, secondarily, evaluate changes in total stillbirth rate during the COVID-19 pandemic compared with prepandemic.

Materials and Methods

This is a retrospective observational study performed at a single, urban tertiary care center. Antenatal utilization of high-risk obstetric services and stillbirth rate were compared between the COVID-19 pandemic and pre-COVID-19 pandemic. The study was approved by the Washington University in St. Louis School of Medicine Human Research Protection Office (#202008027).

The COVID-19 pandemic epoch was defined as week 1 to 30 of 2020 (January 6 through July 27). This epoch follows identification of the first global case of COVID-19 in December 2019 but includes 2 months prior to the first COVID-19 case in Missouri (March 7, 2020) to account for patient and provider behavioral change related to the developing global pandemic.18 Further, this epoch spans approximately 4 months following the transmission mitigation efforts, and captures efforts to streamline prenatal ultrasound and test of fetal well-being based upon the recommendations set forth by Boelig et al within our own Maternal-Fetal Medicine Division at Washington University in St. Louis (March 21, 2020, during week 12 of 2020), the first formal “stay at home order” for the city of St. Louis (March 23, 2020, during week 12 of 2020), and the initiation of prenatal visit restructuring to incorporate telehealth visits (April 6, 2020, during week 14 of 2020).5 The 6-month span of this epoch also allows us to account for some of the underlying temporal trends, seasonal variation, and other potential time-dependent factors that may influence pregnancy-related care. The COVID-19 pandemic epoch was compared with the corresponding weeks 1 to 30 of 2017 (January 2 through July 31), 2018 (January 1 through July 30), and 2019 (December 31 through July 29).

The Division of Maternal-Fetal Medicine at Washington University in St. Louis provides full-scope obstetric care, offering both consultative and primary obstetric care, and managing all formal prenatal ultrasounds. The antenatal high-risk obstetric services analyzed in this study include pregnancy-related visits, ultrasounds, and antenatal tests of fetal well-being. Pregnancy-related visits were defined as Maternal-Fetal Medicine preconception consultations, Maternal-Fetal Medicine and Fetal Care Center antenatal consultations, and new and return Maternal-Fetal Medicine patient visits.

First-trimester ultrasound visits were captured using the following current procedural terminology (CPT) codes: 76813 and 76814 (nuchal translucency), and 76801 and 76802 (transabdominal ultrasound < 14 weeks). Midtrimester anatomic survey visits were captured using the following CPT codes: 76805 (standard anatomic evaluation), 76811 and 76812 (detailed fetal anatomic evaluation). Visits for fetal growth surveillance were captured using the following CPT code: 76816 (follow-up evaluation of fetal size). Finally, antenatal tests of fetal well-being were captured using the following CPT codes: 76819 (biophysical profile [BPP]), 76820 (umbilical artery Doppler study), and 59205 (fetal nonstress tests [NST]). During both the pre-COVID-19 pandemic epoch and pandemic epoch, all patients were allowed to have more than one visit per day (example: Maternal-Fetal Medicine visit and biophysical profile or fetal growth surveillance ultrasound and umbilical artery Doppler study).

Stillbirth was defined as any fetal demise ≥200/7 weeks’ gestation, dated by a patient’s last menstrual period and/or earliest ultrasound.19 Stillbirth data were generated from the following International Classification of Diseases, tenth edition (ICD-10) codes: O36.4XX1 (maternal care for intrauterine fetal death), P95 (stillbirth), O02.1 (missed abortion), Z37.1 (single stillborn), Z37.3 (twins, one live born and one stillborn), Z37.4 (twins, both stillborn), Z37.7 (other multiples, all stillborn) either from inpatient or outpatient encounters. Individual charts were accessed for patients with a stillbirth to confirm pregnancy dating, to ensure patients were only counted once, and to determine if stillbirth was attributable to acute maternal COVID-19 infection. All cases of stillbirth were confirmed by chart review performed by trained members of the research team. The stillbirth rate was defined as any stillbirth ≥ 20 weeks’ gestation per 1,000 live-born deliveries at Barnes-Jewish Hospital, the primary delivery hospital for the Washington University in St. Louis Division of Maternal-Fetal Medicine.

For the outcomes of antenatal high-risk obstetric services and stillbirth, events for each week 1 to 30 were summed. Trends over time were visualized graphically. General linear models were used to further assess those outcomes that showed a change in trend to account for both year and week effects. No additional factors were included in the model as potential confounders, as the exposure (a pregnancy during the COVID-19 pandemic) was considered to be nonmodifiable. A two-sided p-value < 0.05 defined statistical significance. SAS software version 9.4 (SAS Institute Inc., Cary, NC) was used for statistical analyses.

Results

A total of 36,723 antenatal visits and 7,858 deliveries were analyzed for this retrospective study from the prepandemic and pandemic epochs. A chart review of each case of fetal loss during the pandemic revealed that no cases (0/24, 0%) were attributable to maternal COVID-19 infection.

The cumulated totals of Maternal-Fetal Medicine visits, ultrasounds, and antenatal tests of fetal well-being are represented graphically in ►Fig. 1. Visually, there were notable decreases in Maternal-Fetal Medicine visits and antenatal tests of fetal well-being compared with the same time period in 2017, 2018, and 2019, with a deflection point approximately at week 12 when division-wide transmission mitigation efforts were initiated and a formal city-wide “stay at home” order was instituted. No prominent changes were noted when comparing first-trimester ultrasounds, anatomic survey ultrasounds, fetal growth ultrasounds, and total deliveries during the pandemic epoch to prepandemic epoch (►Fig. 1).

Fig. 1.

Fig. 1

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Cumulated totals of antenatal high-risk obstetric services during the COVID-19 pandemic epoch. (a) Maternal-Fetal Medicine visits. (b) First-trimester ultrasounds. (c) Anatomic survey ultrasounds. (d) Fetal growth ultrasounds. (e) Antenatal tests of fetal well-being. (f) Total liveborn deliveries. (g) Stillbirth rate (defined as 1 stillbirth per 1,000 live-born deliveries).

The changes in Maternal-Fetal Medicine visits and antenatal tests of fetal well-being were further analyzed using general linear models. There was a significant interaction between year and Maternal-Fetal Medicine visits (►Fig. 2) (p < 0.01). There was a notable decrease in visits during the pandemic epoch (2020) compared with the corresponding time period in 2019; however, this did not reach statistical significance (p = 0.07). In mid-2018, the addition of a new building increased the capacity for patient care, which is reflected by a statistically significant increase in patient visits in 2019 (n = 1,036) as compared with both 2017 (n = 529, p < 0.01) and 2018 (n = 643, p < 0.01). The effect of week of the year on visit number was not statistically significant (p = 0.6). There was no significant association between year (p = 0.190) or week (p = 0.662) with antenatal tests of fetal well-being (►Fig. 3). There was no overall difference in stillbirth between year (p = 0.634) or week (p = 0.286) (►Fig. 4).

Fig. 2.

Fig. 2

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General linear model of Maternal-Fetal Medicine visits, accounting for year and week effect.

Fig. 3.

Fig. 3

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General linear model of stillbirth, accounting for year and week effect.

Fig. 4.

Fig. 4

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General linear model of antenatal test of fetal well-being, accounting for year and week effect.

Comment

Principal Findings

The COVID-19 pandemic resulted in significantly decreased numbers of Maternal-Fetal Medicine visits, while the number of obstetric ultrasounds and antenatal tests of fetal well-being remained relatively unchanged. In an evaluation of the total stillbirth rate, no significant changes were noted between the prepandemic and pandemic epochs.

Results

While several previously published studies have captured changes in utilization of general obstetrics and gynecology services (such as emergency services and surgery), this is the first study evaluating utilization of high-risk obstetric services during the COVID-19 pandemic to our knowledge.8,20,21 After searching the PubMed database (search terms “prenatal care” AND “COVID-19” and “maternal care” AND “COVID-19”), no studies directly evaluating how the COVID-19 pandemic has influenced prenatal care utilization in a high-risk obstetric population and related obstetric outcomes were found.

Data are beginning to emerge on patient and provider perception and acceptance of prenatal care modifications during the COVID-19 pandemic.22–24 In one survey study by Peahl et al, the authors evaluated a redesigned prenatal care pathway centered around essential services with flexibility for additional psychosocial support. Both patients and providers expressed satisfaction with a modified prenatal visit schedule and incorporation of virtual visits, which resulted in a 16.1% decrease in weekly visits.22 While these studies are promising, only low-risk obstetric patients were included. Patient and provider acceptability are important considerations for designing prenatal care delivery but only when the downstream maternal and fetal implications are more intensively studied for patients at highest risk for adverse outcomes.

Our study did not demonstrate a significant change in stillbirth rate during the pandemic compared with prepandemic. While early reports noted an increased incidence of stillbirth during the COVID-19 pandemic, subsequent reports have offered contradictory findings that are similar to our own results.10,16 In a recently published systematic review and meta-analysis, Chmielewska et al noted a significant increase in stillbirth (odds ratio, 1.28; 95% confidence interval, 1.22–1.53); yet note the significant heterogeneity that exists among the studies (I2 = 63%), including variability within the definition of stillbirth, pandemic mitigation efforts, and health care system efficiency.16,25,26 Our findings of an unchanged stillbirth rate are similar to those recently published by Handley et al, who found that among the deliveries at two urban Pennsylvania hospitals, there was no change in stillbirth rate (intrauterine fetal demise ≥ 20 weeks’ gestation) when comparing the pandemic period to prepandemic periods.27

Clinical Implications

Several previously published studies have suggested that decreased frequency and intensity of prenatal care secondary to transmission mitigation efforts and reluctance to seek medical care may have resulted in increased stillbirth during the pandemic.10,16,17 We noted a nonsignificant change in stillbirth rate during the pandemic epoch compared with the prepandemic epoch in spite of decreased numbers in the Maternal-Fetal Medicine visits. While our study design and power does not allow for conclusions to be drawn in regard to the association of changes in prenatal care and stillbirth, the data call for exploration of factors other than a reduction in prenatal care frequency to explain changes in obstetric outcomes such as stillbirth.

One possible explanation of our findings may be pauses in assisted reproduction as part of COVID-19 transmission mitigation efforts.28 The recommendations of the American Society of Reproductive Medicine (ASRM) early in the COVID-19 pandemic to immediately pause all new infertility treatment cycles inevitably resulted in a decreased number of subsequent high-risk pregnancies and multiple gestation pregnancies. Consequently, there may have been a decrease in the number of pregnancies followed at our institution with an a priori elevated risk for stillbirth that counterbalanced changes in stillbirth rate that may have been attributable to changes in the antenatal utilization of high-risk obstetric services.29,30

Changes in patient and hospital-wide behaviors may have also mitigated changes in stillbirth rates that may have been attributable to changes in antenatal utilization of high-risk obstetric services. For example, a significant decrease in major trauma admissions and trauma severity may have indirectly decreased the risk for stillbirth, mitigating the effects of decreased antenatal utilization of high-risk obstetric services.31–33 This effect may be more prominent in densely populated urban settings. Finally, we considered the possibility of large-scale relocation from urban to suburban or rural areas in the context of our findings. While this phenomenon has been noted in European countries, it is less well-described in the United States and, particularly, in the Missouri.34

Research Implications

The unprecedented nature, global impact of COVID-19, and demand for immediate shifts in the delivery of prenatal care have provided a unique opportunity to observe the downstream effects of these changes on perinatal outcomes in high-risk obstetric populations. Larger studies powered to evaluate rare outcomes, such as stillbirth, are needed to inform how these pandemic-mediated changes in prenatal care and antenatal surveillance influence perinatal outcomes. Such results may be able to inform practice changes that are safe, cost-effective, and acceptable from a both patient and provider perspective.

Strengths and Limitations

A strength of our study is the description of change in the antenatal utilization of outpatient high-risk obstetric services. We based our COVID-19 pandemic epoch on key events in the early pandemic that captured the effects of both informal and formal transmission mitigation efforts. Further, we compared the pandemic epoch to the same corresponding timeframe for the 3 years prior to the pandemic, to better characterize the effect of year on the trend seen during the specified epochs.

This study has potential limitations that must be considered. The retrospective and observational nature of the study precludes the ability to provide conclusive evidence of a causal relationship between changes in antenatal utilization trends and relative lack of influence on the stillbirth rate; however, our study does highlight the unique opportunity to explore with a greater deal of granularity how refining visit and antenatal testing frequency may influence the stillbirth rate of specific underlying diagnoses. Further, our study was not specifically powered to evaluate a difference in stillbirth rate and we acknowledge the possibility of a type 2 error. We did not evaluate changes in missed and cancelled appointments during the pandemic and prepandemic time periods, which may have provided additional perspective on the pandemic-related changes to antenatal care utilization.

Conclusion

The COVID-19 pandemic resulted in a significant decrease in Maternal-Fetal Medicine visits, whereas obstetric ultrasounds and antenatal tests of fetal well-being remained unchanged. While we observed no change in the stillbirth rate compared with the prepandemic epoch, our study design and sample size preclude us from making assumptions of association. Our findings may support future work investigating how changes in prenatal care for high-risk obstetric patients influence perinatal outcomes.

Key Points.

  • MFM visits significantly decreased during the COVID-19 pandemic epoch.

  • The overall stillbirth rate during the COVID-19 pandemic epoch was not significantly changed.

  • Larger studies are needed to capitalize on these changes to evaluate rare outcomes such as stillbirth.

Acknowledgments

We thank Tara Reuter (Financial Analyst, Washington University in St. Louis School of Medicine Department of Obstetrics and Gynecology).

Disclosure of Financial Support and Funding

Research reported in this publication was supported by the National Center for Advancing Translational Sciences of the National Institutes of Health under Award Number UL1 TR002345. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Conflict of Interest

J. C. K.: grants from the PEW Charitable Trusts’ Community Opioid Response and Evaluation (CORE) Project, ID 00033770. M. C. O.: National Center for Advancing Translational Sciences of the National Institutes of Health under Award Number UL1 TR002345.

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