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Impact of vaccination and the omicron variant on COVID-19 severity in pregnant women

  • Haemin Kim
    Affiliations
    Department of Obstetrics and Gynecology, Kyungpook National University Hospital, Kyungpook National University, School of Medicine, Daegu, Korea
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  • Hyo-Shin Kim
    Affiliations
    Department of Obstetrics and Gynecology, Kyungpook National University Hospital, Kyungpook National University, School of Medicine, Daegu, Korea
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  • Hyun Mi Kim
    Affiliations
    Department of Obstetrics and Gynecology, Kyungpook National University Hospital, Kyungpook National University, School of Medicine, Daegu, Korea
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  • Mi Ju Kim
    Affiliations
    Department of Obstetrics and Gynecology, Kyungpook National University Hospital, Kyungpook National University, School of Medicine, Daegu, Korea
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  • Ki Tae Kwon
    Affiliations
    Division of Infectious Diseases, Department of Internal Medicine, Kyungpook National University, School of Medicine, Kyungpook National University Chilgok Hospital, Daegu, Korea
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  • Author Footnotes
    ⁎ Hyun-Hwa Cha and Won Joon Seong contributed equally to this work as co-corresponding authors.
    Hyun-Hwa Cha
    Correspondence
    Correspondence: Hyun-Hwa CHA, MD, PhD, Department of Obstetrics and Gynecology, Kyungpook National University Chilgok Hospital, Kyungpook National University School of Medicine, 807 Hoguk-ro, Buk-gu 702-720, Daegu, South Korea
    Footnotes
    ⁎ Hyun-Hwa Cha and Won Joon Seong contributed equally to this work as co-corresponding authors.
    Affiliations
    Department of Obstetrics and Gynecology, Kyungpook National University Hospital, Kyungpook National University, School of Medicine, Daegu, Korea
    Search for articles by this author
  • Author Footnotes
    ⁎ Hyun-Hwa Cha and Won Joon Seong contributed equally to this work as co-corresponding authors.
    Won Joon Seong
    Correspondence
    Won Joon SEONG, MD, PhD, Department of Obstetrics and Gynecology, Kyungpook National University Chilgok Hospital, Kyungpook National University School of Medicine, 807 Hoguk-ro, Buk-gu 702-720, Daegu, South Korea
    Footnotes
    ⁎ Hyun-Hwa Cha and Won Joon Seong contributed equally to this work as co-corresponding authors.
    Affiliations
    Department of Obstetrics and Gynecology, Kyungpook National University Hospital, Kyungpook National University, School of Medicine, Daegu, Korea
    Search for articles by this author
  • Author Footnotes
    ⁎ Hyun-Hwa Cha and Won Joon Seong contributed equally to this work as co-corresponding authors.

      Highlights

      • In Omicron era, the infectivity of COVID-19 was stronger than before Omicron.
      • The disease severity of COVID-19 was lower in Omicron era.
      • Compared to non-vaccinated patients, vaccinated patients were better protected against COVID-19.

      Abstract

      We compared the clinical course of pregnant women with coronavirus disease 2019 (COVID-19) before and after the emergence of the omicron variant and based on vaccination status. We retrospectively reviewed the electronic medical charts of 224 patients and 82 deliveries from November 1, 2020, to March 7, 2022; of these, 42% were diagnosed during the omicron dominance period. Disease severity and morbidity of COVID-19 were significantly decreased during the omicron era. The vaccination rates among the patients were higher after omicron emergence (31.9%) than before (6.9%). Overall, 4.1% and 25% of patients had severe symptoms, and 2.6% and 16.2% required oxygen therapy in the vaccination and non-vaccination groups, respectively. Overall, patients had a more favorable clinical course in the omicron era; moreover, vaccinated patients were better protected than non-vaccinated patients, indicating the importance of vaccination against COVID-19.

      Key words

      Introduction

      Since the emergence of coronavirus disease 2019 (COVID-19) in February 2020, the number of pregnant women infected with the virus and delivering by cesarean section has been steadily increasing in South Korea.
      • Yang S
      • Jang J
      • Park SY
      • Ahn SH
      • Kim S-S
      • Park SB
      • et al.
      COVID-19 outbreak report from January 20, 2020 to January 19, 2022 in the Republic of Korea.
      Additionally, pregnancy is considered a high-risk factor for severe COVID-19,
      • Kim SH
      • Choi Y
      • Lee D
      • Lee H
      • Kim JH
      • Choi ES
      • et al.
      Impact of COVID-19 on pregnant women in South Korea: Focusing on prevalence, severity, and clinical outcomes.
      especially in case of infection with the delta variant of SARS-CoV-2 (severe acute respiratory syndrome coronavirus 2). Despite reports showing a more favorable disease outcome with the omicron variant, little is known about its clinical course in pregnant women.
      • Wang L
      • Berger NA
      • Kaelber DC
      • Davis PB
      • Volkow ND
      • Xu R.
      COVID infection rates, clinical outcomes, and racial/ethnic and gender disparities before and after Omicron emerged in the US.
      ,
      • Iuliano AD
      • Brunkard JM
      • Boehmer TK
      • Peterson E
      • Adjei S
      • Binder AM
      • et al.
      Trends in Disease Severity and Health Care Utilization During the Early Omicron Variant Period Compared with Previous SARS-CoV-2 High Transmission Periods — United States, December 2020–January 2022.
      Moreover, because little is known about the effectiveness of COVID-19 vaccines in pregnant women in Korea, the vaccination rate is low at only 9.8%.

      National Health Insurance Service. 9 out of 10 pregnant women who were vaccinated against COVID-19 were not vaccinated. Financial today Available at: http://www.ftoday.co.kr/news/articleView.html?idxno=231340 Accessed 1 April 2022.

      Herein, we aimed to review the clinical outcomes of pregnancies in women with COVID-19 to evaluate whether the emergence of the omicron variant and vaccination status influence disease severity.

      Methods

      We retrospectively reviewed the electronic medical charts of all pregnant women admitted to our institution for COVID-19 infection between November 1, 2020 and March 7, 2022. The study cohort was stratified into two groups based on whether their admission date was before or after the omicron variant emergence. The omicron group comprised patients who were admitted to our hospital after January 17, 2022, when omicron became the dominant SARS-CoV-2 strain according to the Korea Disease Control and Prevention Agency. In addition, the groups were classified according to vaccination status to compare the clinical outcomes. Because of the low vaccination rate among pregnant women, the vaccinated group was defined as patients who received at least one vaccination dose. Clinical severity was classified as “asymptomatic to mild” or “moderate to serious,” based on the patient's oxygen demand, chest radiograph pneumonia findings, the need for intensive care from infection medical specialists, and intensive care requirement, as per the guidelines of the National Institutes of Health.
      COVID-19 Treatment Guidelines Panel
      Coronavirus Disease 2019 (COVID-19) Treatment Guidelines.
      Maternal morbidities included pneumonia diagnosed on chest radiograph during the admission period, the need for pulmonology expert transfer, intensive care requirement, and preterm birth (defined as delivery before 37 weeks). Statistical analyses were performed using IBM SPSS version 28.0 (IBM Corp., Armonk, NY, USA) software. The Chi-square test and Fisher's exact test were used to analyze categorical variables. Continuous variables were analyzed using the Kruskal–Wallis test, Student's t-test, and Mann–Whitney U test. The statistical significance threshold was set at a p-value < 0.05.
      The Institutional Review Board and Ethics Committee of Kyungpook National University Hospital (No. 2022-03-027) approved this study. The board waived the requirement for informed consent.

      Results

      A total of 224 pregnancies and 82 quarantine deliveries were documented. Table 1 shows the characteristics of the pregnant women before and after omicron emergence. Despite the relatively short period of omicron variant dominance, 42% of patients were classified into the omicron group. The average age of the before-omicron and omicron groups were 32.3±4.9 and 32.1±4.3 years, respectively. In both groups, the proportion of pregnant women in the 3rd trimester was significantly higher than that in any other trimester (53.1% and 73.4%, in the before-omicron and omicron groups, respectively). This could be because many of the patients were admitted for delivery. Interestingly, the vaccination rate was higher in the omicron group (6.9% vs. 31.9%, p < 0.001), which may be reflective of the late start of COVID-19 vaccination uptake among pregnant women in Korea. The rates of “moderate-to-severe” disease and maternal morbidity were reduced after the emergence of the omicron variant (30.0% vs. 10.6%, p < 0.001; 27.7% vs. 13.8%, p = 0.013, respectively). Oxygen demand was also higher in the before-omicron group (20.0% vs. 5.3%, p = 0.002).
      Table 1Comparisons of maternal characteristics and clinical outcomes before and after the emergence of omicron variant
      CHARACTERISTICSBEFORE OMICRON(N=130)AFTER OMICRON(N=94)P
      Age32.3 ± 4.932.1 ± 4.30.754
      Nulliparity* (%)66 (51.6)47 (50.0)0.818
      GA at admission
      1st trimester, n (%)

      2nd trimester, n (%)

      3rd trimester, n (%)
      19 (14.6)

      42 (32.3)

      69 (53.1)
      13 (13.8)

      12 (12.8)

      69 (73.4)
      0.002
      Number of Vaccine doses (%)
      None

      First

      Second

      Boosted
      121 (93.1)

      3 (2.3)

      6 (4.6)

      -
      64 (68.1)

      6 (6.4)

      21 (22.3)

      3 (3.2)
      < 0.001
      Co-morbidity (%)
      Obesity

      DM

      HTN

      Asthma
      14 (10.8)

      10 (7.7)

      4 (3.1)

      3 (2.3)
      12 (12.8)

      9 (9.6)

      3 (3.2)

      1 (1.1)
      0.645

      0.618

      1.000

      0.641
      Clinical severity during admission (%)
      Asymptomatic or Mild

      Moderate or Serious
      91 (70.0)

      39 (30.0)
      84 (89.4)

      10 (10.6)
      < 0.001
      Oxygen support requirement (%)26 (20.0)5 (5.3)0.002
      Nasal or Mask

      High frequency

      Invasive Mechanical
      20 (15.4)

      5 (3.8)

      1 (0.8)
      5 (5.3)

      -

      -
      0.001
      Maternal Morbidity (%)36 (27.7)13 (13.8)0.013
      Pneumonia

      Transfer to Medical specialist

      ICU care

      PTB
      , n=82 (before omicron: 40, after omicron: 42); Abbreviations: GA, gestational age; DM, diabetes mellitus; HTN, hypertension; ICU, intensive care unit; PTB, preterm birth
      32 (24.6)

      20 (15.4)

      4 (3.1)

      5 (12.5)
      9 (9.6)

      5 (5.3)

      0 (0.0)

      3 (7.1)
      0.004

      0.018

      0.141

      0.477
      *, n=222;
      , n=82 (before omicron: 40, after omicron: 42); Abbreviations: GA, gestational age; DM, diabetes mellitus; HTN, hypertension; ICU, intensive care unit; PTB, preterm birth
      We further compared the clinical outcomes according to the vaccination status (Table 2). Among all infected pregnant women, 185 and 39 were non-vaccinated and vaccinated, respectively. The rates of “moderate-to-severe” disease and oxygen therapy requirement were significantly lower in the vaccinated group than in the non-vaccinated group (25.4% vs. 4.1%, p = 0.005; 16.2% vs 2.6%, p = 0.025, respectively). Notably, only one patient in the vaccinated group (who had asthma) required oxygen therapy.
      Table 2Comparison of clinical outcomes according to vaccination status
      CHARACTERISTICSNON-VACCINATED (N=185)VACCINATED (N=39)P
      Clinical severity during admission (%)
      Asymptomatic or Mild

      Moderate or Serious
      138 (74.6)

      47 (25.4)
      37 (94.9)

      2 (4.1)
      0.005
      Oxygen support requirement (%)30 (16.2)1 (2.6)0.025
      Nasal or Mask

      High frequency

      Invasive Mechanical
      24 (13.0)

      5 (2.2)

      1 (0.5)
      1 (2.6)

      -

      -
      0.032
      Maternal Morbidity (%)47 (25.4)2 (5.1)0.005
      Pneumonia

      Transfer to Medical specialist

      ICU care

      PTB
      40 (21.6)

      24 (13.0)

      4 (2.2)

      8 (10.4)
      1 (2.6)

      1 (2.6)

      -

      -
      0.005

      0.089

      1.000

      1.000
      n=82 (non-vaccinated: 77vaccinated: 5) Abbreviations: ICU intensive care unit PTB preterm birth

      Discussion

      This study has several limitations. Firstly, we could not detect the specific strain of SARS-CoV-2 in the infected patients. Considering that omicron accounted for more than half of COVID-19 infections after January 17, 2022, in Korea, we expected that the characteristics of the omicron variant would be reflected in the study population. This interval of time was defined as the omicron period for comparison analysis. Among 9 vaccinated women in the before-omicron group, only one who was obese and over 40 years old showed pneumonia on chest X-ray, but did not require oxygen therapy. Nevertheless, our result is insufficient to conclude whether the lower severity in vaccinated women is due to the vaccination or simply a feature of the omicron variant itself. Additionally, the sample size was small because the study was conducted only at a single institution. However, data from a single institution is reliable owing to consistency in treatment guidelines.
      In conclusion, the clinical course of COVID-19 was more favorable in pregnant women in the omicron group than in the before-omicron group. Additionally, disease severity was lower in pregnant women who had received at least one vaccination dose. In fact, more favorable clinical outcomes were observed after the omicron variant dominance. However, more pregnant women were also vaccinated during this period. Further studies are required to identify whether the outcomes improved due to the decreased severity of the disease caused by the omicron variant or the protective effects of vaccination.

      Author Contributions

      Conceptualization: Seong WJ.
      Data curation: Kim H, Kim H-S, Kim HM, Kim MJ, Cha H-H, Kwon KT, Seong WJ.
      Formal analysis: Kim H, Cha H-H.
      Investigation: Kim H, Kim H-S, Kim HM, Kim MJ, Cha H-H, Seong WJ.
      Writing - original draft: Kim H, Cha H-H.
      Writing - review & editing: Cha H-H, Seong WJ

      Ethical statement

      The Institutional Review Board and Ethics Committee of Kyungpook National University Hospital (No. 2022-03-027) approved this study. The board waived the requirement for informed consent.

      Funding statement

      No funding was received for this study.

      Disclosure

      The authors have no potential conflicts of interest to disclose.

      Acknowledgements

      We would like to thank all the staff of the quarantine ward and emergency department at the Kyungpook National University Hospital and Kyungpook National University Chilgok Hospital for their work in the management of pregnancies in women with COVID-19.

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        • COVID-19 Treatment Guidelines Panel
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