Change in the Incidence of Stillbirth and Preterm Delivery During the COVID-19 Pandemic | Neonatology | JAMA | JAMA Network
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Table 1.  Comparison of Maternal and Pregnancy Characteristics Between the Prepandemic Period (October 1, 2019, to January 31, 2020) and the Pandemic Period (February 1, 2020, to June 14, 2020)
Comparison of Maternal and Pregnancy Characteristics Between the Prepandemic Period (October 1, 2019, to January 31, 2020) and the Pandemic Period (February 1, 2020, to June 14, 2020)
Table 2.  Comparison of the Study Outcomes Between the Prepandemic Period (October 1, 2019, to January 31, 2020) and the Pandemic Period (February 1, 2020, to June 14, 2020)
Comparison of the Study Outcomes Between the Prepandemic Period (October 1, 2019, to January 31, 2020) and the Pandemic Period (February 1, 2020, to June 14, 2020)
1.
Khalil  A, Kalafat  E, Benlioglu  C,  et al.  SARS-CoV-2 infection in pregnancy: a systematic review and meta-analysis of clinical features and pregnancy outcomes.   EClinicalMedicine. Published online July 3, 2020. doi:10.1016/j.eclinm.2020.100446Google Scholar
2.
Knight  M, Bunch  K, Vousden  N,  et al; UK Obstetric Surveillance System SARS-CoV-2 Infection in Pregnancy Collaborative Group.  Characteristics and outcomes of pregnant women admitted to hospital with confirmed SARS-CoV-2 infection in UK: national population based cohort study.   BMJ. 2020;369:m2107. doi:10.1136/bmj.m2107PubMedGoogle ScholarCrossref
3.
Campbell  KH, Tornatore  JM, Lawrence  KE,  et al.  Prevalence of SARS-CoV-2 among patients admitted for childbirth in Southern Connecticut.   JAMA. Published online May 26, 2020. doi:10.1001/jama.2020.8904PubMedGoogle Scholar
4.
Sutton  D, Fuchs  K, D’Alton  M, Goffman  D.  Universal screening for SARS-CoV-2 in women admitted for delivery.   N Engl J Med. 2020;382(22):2163-2164. doi:10.1056/NEJMc2009316PubMedGoogle ScholarCrossref
5.
Khalil  A, Hill  R, Ladhani  S, Pattisson  K, O’Brien  P.  Severe acute respiratory syndrome coronavirus 2 in pregnancy: symptomatic pregnant women are only the tip of the iceberg.   Am J Obstet Gynecol. Published online May 7, 2020. doi:10.1016/j.ajog.2020.05.005PubMedGoogle Scholar
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    1 Comment for this article
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    Consideration for Increased Antenatal Scan Capacity
    Sunday Ameh, MBBS, MRCOG | Royal Bolton Hospital, Bolton, United Kingdom
    We commend Khalid A. et al for their recent work that demonstrated a significant increase in the incidence of stillbirth during the COVID-19 pandemic vs the prepandemic period (1), and wish to raise some observations having looked at related data in our unit. As noted, the high stillbirth rate during the pandemic may have resulted from a number of indirect factors including a reduction in antenatal ultrasound scans and may not be related entirely to the direct consequent of maternal-fetal SARS-CoV-2 infection. Interestingly, contrary to findings from Khalid A. et al, no significant difference in stillbirth rates prepandemic and during the pandemic was observed in our unit although a trend towards increase adverse perinatal outcome (preterm births, stillbirth, early neonatal deaths, and neonatal unit admissions) was observed in the pandemic. We believe one key factor based on our findings responsible for this difference is the significant increase in antenatal ultrasound scans carried out in our unit during the pandemic. Furthermore, it is worthy of note that despite the significant reduction in antenatal in-patient admissions and face-to-face antenatal consultations during the pandemic which are established risk factors for adverse obstetric outcomes (2,3), the obstetric outcomes (perinatal and maternal) prepandemic vs during the pandemic are comparable. We believe the increase in antenatal ultrasound scans during the pandemic may have played a key role in mitigating the resultant adverse impacts from these risk factors. Consequently, as the pandemic lingers with the possibility of a potential second wave, it is important to consider maintaining and/or increasing local antenatal scan capacity, a key obstetric intervention in preventing adverse obstetric outcome.

    REFERENCES

    1. Khalil A, von Dadelszen P, Draycott T, Ugwumadu A, O’Brien P, Magee L. Change in the Incidence of Stillbirth and Preterm Delivery During the COVID-19 Pandemic. JAMA. Published online July 10, 2020. doi:10.1001/jama.2020.12746.

    2. Dowswell T, Carroli G, Duley L, et al. Alternative versus standard packages of antenatal care for low-risk pregnancy. Cochrane Database Syst Rev 2015(7):CD000934. doi: 10.1002/14651858.

    3. Ayres A, Chen R, Mackle T, Ballard E, Patterson S, Bruxner G, et al. Engagement with perinatal mental health services: a cross-sectional questionnaire survey. BMC Pregnancy Childbirth 2019; 19:170.
    CONFLICT OF INTEREST: None Reported
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    Research Letter
    July 10, 2020

    Change in the Incidence of Stillbirth and Preterm Delivery During the COVID-19 Pandemic

    Author Affiliations
    • 1Fetal Medicine Unit, St George’s University of London, London, United Kingdom
    • 2School of Life Course Sciences, King’s College London, London, United Kingdom
    • 3Department of Women’s Health, North Bristol NHS Trust, Westbury on Trym, United Kingdom
    • 4Department of Women’s Health, University College London Hospitals, London, United Kingdom
    JAMA. 2020;324(7):705-706. doi:10.1001/jama.2020.12746

    High rates of preterm birth and cesarean delivery have been reported in women with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection.1 However, studies have inadequate power to assess uncommon outcomes like stillbirth (fetal death ≥24 weeks’ gestation). The UK Obstetric Surveillance System reported 3 stillbirths among 247 completed pregnancies in women with confirmed coronavirus disease 2019 (COVID-19) vs the national rate (12.1 per 1000 births vs 4-5 per 1000 births).2 We assessed the change in stillbirth and preterm delivery rates during the pandemic.

    Methods

    We compared pregnancy outcomes at St George’s University Hospital, London, in 2 epochs: from October 1, 2019, to January 31, 2020 (preceding the first reported UK cases of COVID-19), and from February 1, 2020, to June 14, 2020. Outcomes included stillbirth, preterm birth, cesarean delivery, and neonatal unit admission. We investigated all stillbirths and repeated the analysis after excluding late terminations for fetal abnormalities, as the definition of stillbirth in the UK includes late termination at 24 weeks’ gestation or beyond.

    Group comparisons were made using Mann-Whitney and Fisher exact tests. The analysis was performed using Stata 11, release 11.2 (StataCorp) and GraphPad Prism 5.0 for Windows (InStata, GraphPad Software Inc). A 2-sided P < .05 defined statistical significance. Ethics committee approval and informed consent were not required per the UK Health Research Authority.

    Results

    There were 1681 births (1631 singleton, 22 twin, and 2 triplet pregnancies) in the prepandemic period and 1718 births (1666 singleton and 26 twin pregnancies) in the pandemic period. There were fewer nulliparous women (45.6% vs 52.2%; P < .001) in the pandemic period than in the prepandemic period and fewer women with hypertension (3.7% vs 5.7%; P = .005) in the pandemic period than the prepandemic period, and there were no significant differences in other maternal characteristics (Table 1).

    The incidence of stillbirth was significantly higher during the pandemic period (n = 16 [9.31 per 1000 births]; none associated with COVID-19) than during the prepandemic period (n = 4 [2.38 per 1000 births]) (difference, 6.93 [95% CI, 1.83-12.0] per 1000 births; P = .01) (Table 2), and the incidence of stillbirth was significantly higher when late terminations for fetal abnormality were excluded during the pandemic period (6.98 per 1000 births vs 1.19 per 1000 births in the prepandemic period; difference, 5.79 [95% CI, 1.54-10.1]; P = .01). There were no significant differences over time in births before 37 weeks’ gestation, births after 34 weeks’ gestation, neonatal unit admission, or cesarean delivery (Table 2).

    During the pandemic period, 19 patients with COVID-19 were hospitalized in the study site maternity department. None of the pregnant women who experienced stillbirth had symptoms suggestive of COVID-19, nor did the postmortem or placental examinations suggest SARS-CoV-2 infection. Universal testing for SARS-CoV-2 started on May 28, 2020, and only 1 pregnant woman, who had a live birth, had a positive test result.

    Discussion

    This study demonstrates an increase in the stillbirth rate during the pandemic. A direct consequence of SARS-CoV-2 infection is possible. Although none of the stillbirths in the pandemic period were among women with COVID-19, surveillance studies in pregnant women reported that as much as 90% of SARS-CoV-2–positive cases were asymptomatic.3-5 Moreover, until recently, UK national policy limited testing to symptomatic individuals requiring hospitalization. Alternatively, the increase in stillbirths may have resulted from indirect effects such as reluctance to go to the hospital when needed (eg, with reduced fetal movements), fear of contracting infection, or not wanting to add to the National Health Service burden. Changes in obstetric services may have played a role secondary to staff shortages or reduced antenatal visits, ultrasound scans, and/or screening. Although differences in the populations in the 2 periods were observed, the lower proportion of nulliparous and hypertensive women during the pandemic period would have been expected to be associated with a lower rather than higher risk of stillbirth. However, hypertension in pregnancy may have been underdiagnosed during the pandemic as women had fewer face-to-face antenatal visits. Other possible explanations include change in referral patterns with more high-risk women referred to St George’s Hospital or chance due to the short time frame of the study.

    Limitations of this study include its retrospective nature, single-center setting, small numbers, short time frame, and lack of information on the causes of stillbirths. Moreover, a comparable period in 2019 was not used, but this should not affect the results as there is no seasonality to stillbirths in the UK.

    Section Editor: Jody W. Zylke, MD, Deputy Editor.
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    Article Information

    Corresponding Author: Asma Khalil, MD, Fetal Medicine Unit, Department of Obstetrics and Gynaecology, St George’s University Hospitals, NHS Foundation Trust, Blackshaw Road, London SW17 0QT, United Kingdom (akhalil@sgul.ac.uk).

    Accepted for Publication: June 29, 2020.

    Published Online: July 10, 2020. doi:10.1001/jama.2020.12746

    Author Contributions: Dr Khalil had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

    Concept and design: Khalil, von Dadelszen, O’Brien, Magee.

    Acquisition, analysis, or interpretation of data: Khalil, Draycott, Ugwumadu, O’Brien, Magee.

    Drafting of the manuscript: Khalil, Draycott, Ugwumadu, O’Brien.

    Critical revision of the manuscript for important intellectual content: All authors.

    Statistical analysis: Khalil.

    Administrative, technical, or material support: Khalil, von Dadelszen, Ugwumadu, Magee.

    Conflict of Interest Disclosures: Dr Draycott reported receipt of grants from Tommy’s Centre for Maternity Improvement outside the submitted work. No other disclosures were reported.

    References
    1.
    Khalil  A, Kalafat  E, Benlioglu  C,  et al.  SARS-CoV-2 infection in pregnancy: a systematic review and meta-analysis of clinical features and pregnancy outcomes.   EClinicalMedicine. Published online July 3, 2020. doi:10.1016/j.eclinm.2020.100446Google Scholar
    2.
    Knight  M, Bunch  K, Vousden  N,  et al; UK Obstetric Surveillance System SARS-CoV-2 Infection in Pregnancy Collaborative Group.  Characteristics and outcomes of pregnant women admitted to hospital with confirmed SARS-CoV-2 infection in UK: national population based cohort study.   BMJ. 2020;369:m2107. doi:10.1136/bmj.m2107PubMedGoogle ScholarCrossref
    3.
    Campbell  KH, Tornatore  JM, Lawrence  KE,  et al.  Prevalence of SARS-CoV-2 among patients admitted for childbirth in Southern Connecticut.   JAMA. Published online May 26, 2020. doi:10.1001/jama.2020.8904PubMedGoogle Scholar
    4.
    Sutton  D, Fuchs  K, D’Alton  M, Goffman  D.  Universal screening for SARS-CoV-2 in women admitted for delivery.   N Engl J Med. 2020;382(22):2163-2164. doi:10.1056/NEJMc2009316PubMedGoogle ScholarCrossref
    5.
    Khalil  A, Hill  R, Ladhani  S, Pattisson  K, O’Brien  P.  Severe acute respiratory syndrome coronavirus 2 in pregnancy: symptomatic pregnant women are only the tip of the iceberg.   Am J Obstet Gynecol. Published online May 7, 2020. doi:10.1016/j.ajog.2020.05.005PubMedGoogle Scholar
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