Abstract
Aim
To explore the impact of the Omicron variant on maternal and neonatal outcomes.
Design
Cross‐sectional cohort study of women giving live birth in a single hospital in Shanghai in December 2022.
Methods
Demographic characteristics, maternal and neonatal outcomes and laboratory testing results were retrieved from medical records. Propensity score matching was used to match COVID‐19‐positive and ‐negative women. Differential analysis was used to assess associations between COVID‐19 and in‐hospital maternal and neonatal outcomes.
Results
A total of 1508 women were included, comprising 729 natural births, 741 caesarean sections and 38 forceps deliveries. After 1:1 matching, 310 clients were included for analysis with each 155 in COVID‐19‐positive and ‐negative groups. Higher maternal fever was found in all modes of delivery, and higher preterm birth and lower pH value of blood gas of the umbilical artery in the vaginal delivery subgroup (p < 0.05). Other maternal and neonatal outcomes showed no significant difference between COVID‐19‐positive and ‐negative clients.
Keywords: COVID‐19, maternal outcome, neonatal outcome, propensity score matching
1. INTRODUCTION
In December 2021, mainland China experienced the Omicron wave of the COVID‐19 pandemic (CDC, 2022), following the abandonment of the ‘dynamic zero COVID’ strategy. Despite the limited number of deaths reported due to strict criteria, it was speculated that a massive death toll was a possibility (Ioannidis et al., 2023). Mothers and infants have been deemed as vulnerable populations and are at risk of severe COVID‐19 and complications. Studies have revealed an increased risk of maternal mortality and serious complications from obstetric issues and a slight rise in some neonatal morbidities (Metz et al., 2022; Norman et al., 2021). However, the data reported were the results related to early strains of COVID‐19. It is believed that the impact of this more transmissible Omicron variant may not be as severe as the previous strains (Jarraya, Kammoun, Bouhamed, et al., 2023; Shuai et al., 2022; Suzuki et al., 2022). So far, there are limited reports of its impacts on maternal and neonatal outcomes during birth because of potential selection biases and small sample sizes. Lacking knowledge of these impacts might possibly result in potential excessive obstetrical interventions. To address these gaps, we conducted a cross‐sectional cohort study and analysed the maternal and neonatal outcomes associated with Omicron infection, and especially discussed its impact on vaginal delivery. Through this study, we sought to provide insights for clinical practice in midwifery care.
2. METHODS
2.1. Participants and ethics
We included all women giving live birth between 1 December 2022 and 31 December 2022, in a tertiary specialized hospital in China. Among all the 1508 women included, there were 729 natural births, 741 caesarean sections and 38 forceps deliveries. Either a positive nucleic acid test or a repeated positive antigen test of the clients before the day of birth was redeemed as infected. Clients with intrapartum COVID‐19 infection were assigned to the case group, otherwise, the clients were assigned to the control group.
2.2. Intrapartum management
Acetaminophen and antibiotics were prescribed for those infected with high fever. On signs of unrelieved fetal distress before the active phase of labour, caesarean section was considered by obstetricians. Obstetrical procedures were implemented according to institutional routine and labour phases. During natural delivery, partners were allowed to accompany the birthing mothers. After birth, infants of positive test mothers were separated during the hospital stay and discharged with the postpartum mother after 2–3 days.
2.3. Data collection
Two investigators independently collected data regarding clinical characteristics, maternal and neonatal outcomes and laboratory testing results from medical records. Specifically, emergent caesarean section was defined as operations conducted in the active phase of labour, starting from 3 cm of cervical dilation. Neonatal asphyxia was defined as Apgar score ≤7 at 1 min. Induction of labour included any usage of the balloon catheter, prostaglandin E2 and oxytocin.
2.4. Data analysis
Data were analysed using SPSS software, version 24.0. To assess any association between COVID‐19 and in‐hospital maternal and neonatal outcomes, and to rule out potential biases, each infected client was matched with a negative test using propensity score matching on parity. The nearest neighbour was sampled with a maximum calliper width of 0.02 and 1:1 matching (Austin et al., 2018). Normality was assessed using the Shapiro–Wilk test. T‐test facilitated the comparison between groups for normally distributed data, whereas the Mann–Whitney U test for non‐normally distributed continuous data. Categorical variables were compared between groups with Fisher's exact test. In addition to standardized differences between groups, we made a subgroup analysis of the matched data with a further focus on vaginal birth, as per the midwifery practice. The significance threshold was set at p < 0.05 in two‐sided tests.
3. RESULTS
A total of 155 of the 1508 clients (10.3%) were included in the case group. Our analysis included 310 pairs of women matched on parity (Table 1) with comparable baseline characteristics. Only significant increases were observed in maternal fever (25.2% vs. 10.3%) in the infected population (p < 0.05). There was no statistically significant difference in maternal outcomes between three delivery modes, even with a slight increase in premature rupture of membrane, preterm delivery and caesarean rate in positive group (Table 2).
TABLE 1.
Baseline characteristics of maternities between groups.
| Characteristic | COVID‐19 negative (n = 155) | COVID‐19 positive (n = 155) | t/X 2 | p‐Value |
|---|---|---|---|---|
| Age, mean (SD) | 30.8 (3.9) | 31.3 (3.6) | −0.950 | 0.343 |
| Body mass index | 0.182 | 0.913 | ||
| <18.5 | 11 (7.1%) | 13 (8.4%) | ||
| ≥18.5 | 130 (83.9%) | 128 (82.6%) | ||
| >24 | 14 (9.0%) | 14 (9.0%) | ||
| Gestation | 1.7 (1.0) | 1.7 (1.0) | 0.172 | 0.864 |
| Multiparity | 40 (25.8%) | 42 (27.1%) | 0.066 | 0.797 |
| Epidural anaesthesia | 132 (85.2%) | 128 (82.6%) | 0.382 | 0.537 |
| Comorbidity | ||||
| Diabetes | 22 (14.2%) | 13 (8.4%) | 2.609 | 0.106 |
| Hypertension | 6 (3.9%) | 6 (3.9%) | 0 | 1 |
| Anaemia | 16 (10.3%) | 14 (9.0%) | 0.148 | 0.701 |
| Thyroid diseases | 13 (8.4%) | 15 (9.7%) | 0.157 | 0.692 |
TABLE 2.
Maternal outcomes between groups.
| Characteristic | COVID‐19 negative (n = 155) | COVID‐19 positive (n = 155) | t/X 2 | p‐Value |
|---|---|---|---|---|
| Premature rupture of membrane | 24 (15.5%) | 29 (18.7%) | 0.569 | 0.451 |
| Preterm birth | 5 (3.2%) | 13 (8.4%) | 3.775 | 0.052 |
| Mode of delivery | ||||
| Natural birth | 104 (67.1%) | 103 (66.5%) | 1.175 | 0.556 |
| Forceps delivery | 6 (3.9%) | 3 (1.9%) | ||
| Caesarean section | 45 (29.0%) | 49 (31.6%) | ||
| Emergent caesarean section | 2/45 (4.4%) | 2/49 (4.1%) | 0.008 | 0.931 |
| Intrapartum fever | 16 (10.3%) | 39 (25.2%) | 11.693 | 0.001 |
However, on analysis of the subgroup with vaginal birth, a higher incidence of preterm labour and a lower level of pH in blood gas of the umbilical artery were noticed, yet this did not create a difference in neonatal asphyxia. Other maternal and neonatal outcomes between groups in vaginal delivery were comparable in both groups (p > 0.05, shown in Table 3).
TABLE 3.
Maternal and neonatal outcomes between subgroups in vaginal delivery.
| Outcomes | COVID‐19 negative (n = 110) | COVID‐19 positive (n = 106) | Odds ratio (95% CI)/T | p‐Value |
|---|---|---|---|---|
| Preterm birth | 2 (1.8%) | 9 (8.5%) | 1.729 (1.263–2.367) | 0.026 |
| Episiotomy | 17 (15.5%) | 25 (23.6%) | 1.616 (0.814–3.208) | 0.170 |
| Neonatal morbidities | 10 (9.1%) | 17 (16.0%) | 1.834 (0.797–4.216) | 0.154 |
| Amniotic fluid contamination | 38 (34.5%) | 35 (33.0%) | 0.967 (0.736–1.272) | 0.886 |
| Induction of labour | 54 (49.1%) | 47 (44.3%) | 0.911 (0.701–1.183) | 0.484 |
| Neonatal asphyxia | 1 (1.0%) | 0 (0.0%) | 0.507 (0.44–0.578) | 0.325 |
| Length of labour, mean (SD), min | ||||
| Stage 1 | 434.6 (243.5) | 411.6 (221.8) | −0.724 | 0.470 |
| Stage 2 | 28.3 (20.2) | 26.7 (23.0) | −0.547 | 0.585 |
| Stage 3 | 6.1 (3.9) | 6.7 (3.5) | 1.338 | 0.182 |
| Total length | 469.5 (254.1) | 445.0 (226.8) | −0.746 | 0.457 |
| Blood loss at 2 h postpartum, mean (SD), mL | 347.7 (177.9) | 366.6 (189.4) | 0.753 | 0.452 |
| Postpartum haemorrhage at 24 h | 2.630 | 0.283 | ||
| Postpartum haemorrhage | 15 (13.6%) | 11 (10.4%) | ||
| Severe postpartum haemorrhage | 2 (1.8%) | 6 (5.7%) | ||
| Apgar 1, mean (SD) | 9.4 (0.7) | 9.3 (0.5) | −1.058 | 0.291 |
| Apgar 5, mean (SD) | 9.8 (0.5) | 9.8 (0.5) | 0.149 | 0.882 |
| Analysis of blood gas, mean (SD) | ||||
| pH | 7.277 (0.069) | 7.255 (0.075) | 0.918 | 0.030 |
| BE | −4.968 (2.877) | −4.896 (2.874) | 0.040 | 0.968 |
| LAC | 5.338 (1.894) | 5.088 (1.777) | −0.949 | 0.344 |
4. DISCUSSION
Our data showed that fever could occur in COVID‐19‐positive mothers, although epidural anaesthesia can also cause fever (Jia et al., 2021), but this contributing factor has been removed after matching. Therefore, the leading cause of maternal fever is COVID‐19 infection. Nevertheless, those positive mothers did not manifest hypoxemia, which was similar to former findings (Li et al., 2020). The caesarean rate in our study was much lower than those with Delta infection or Omicron infection reported by Jarraya, Kammoun, Bouhamed, et al. (2023), indicating that the severity of COVID could impact the mode of delivery (Di Mascio et al., 2021) and the COVID might become mild as time goes by.
According to our data, the incidence of preterm birth was significantly higher in COVID‐19‐positive clients who conducted vaginal delivery, and such difference diminished in all modes of delivery. This phenomenon might be explained by fewer caesarean choices for preterm infants, which midwives should take into consideration when delivering COVID‐19‐positive clients. Another difference between COVID‐positive and ‐negative clients was the umbilical cord artery blood pH levels. However, the process of the influence of COVID‐19‐positive mothers on neonates' pH levels remains unclear. Though research has shown that adverse fetal outcomes in COVID‐19‐positive women were more severe compared with COVID‐19‐negative women (Jarraya, Kammoun, Bouhamed, et al., 2023), there was no difference in the incidence of neonatal hyperbilirubinemia, pneumonia or asphyxia in the two groups in our study.
Incidences of postpartum haemorrhage after vaginal delivery were similar in COVID‐positive and ‐negative clients, which was opposite from previous research (Metz et al., 2022) conducted in 2020. One of the possible reasons might be the continuous decrease of fusogenicity and pathogenicity of SARS‐CoV‐2 variants (Suzuki et al., 2022). Evidence in our study demonstrated that COVID‐19‐positive mothers did not yield more adverse maternal and neonatal outcomes. Therefore, excessive obstetrical interventions are not necessary in practice, while more mental support for COVID‐19‐positive mothers could be provided to alleviate their stress.
Our study was limited by data from one hospital in China; thus, external validity in other medical centres is needed. In addition, it has been proven that providing complete vaccination is beneficial to improve maternal and neonatal outcomes (Jarraya, Kammoun, Kanoun, et al., 2022), yet the vaccination statuses of our subjects were not compared, considering a contraindication of pregnancy for the COVID‐19 vaccine recommended by the government at that time.
5. CONCLUSIONS
This study, which examined maternal and neonatal outcomes with a primary focus on vaginal births through December 2022, revealed that the Omicron infection was associated with higher maternal fever, and higher preterm birth in the vaginal delivery subgroup. Our data highlighted a much smaller impact on the birth of Omicron than previous strains. Thus, midwives may provide more intrapartum supportive care rather than excessive obstetrical intervention.
AUTHOR CONTRIBUTIONS
Liu Ying had full access to all the data in the study and took responsibility for the integrity of the data and the accuracy of the data analysis. Concept and design: Shan, Jiang, Ying. Acquisition, analysis, or interpretation of data: Liang, Zhang, Shan, Liu. Drafting of the manuscript: Liu, Shan. Statistical analysis: Liu. Obtained funding: Liu. Supervision: Jiang, Ying.
FUNDING INFORMATION
Clinical Research Project in the Health Industry of Shanghai Municipal Health Commission (No. 20204Y0231), The Reservoir Talent Project of Shanghai First Maternity and Infant Hospital.
CONFLICT OF INTEREST STATEMENT
None reported.
ETHICS STATEMENT
The study was approved by the Institutional Review Board (No. KS22327) and followed the STROBE reporting guideline. All clients had signed the institutional broad consent for clinical research.
ACKNOWLEDGEMENTS
The authors have no acknowledgement.
Ying, L. , Mengmeng, L. , Lan, Z. , Hao, Y. , Hui, J. , & Shanshan, S. (2024). COVID‐19 Omicron variant infection has minimal impact on maternal and neonatal outcomes: A cross‐sectional cohort study. Nursing Open, 11, e2072. 10.1002/nop2.2072
DATA AVAILABILITY STATEMENT
Data are available on request from the authors.
REFERENCES
- Austin, P. C. , Jembere, N. , & Chiu, M. (2018). Propensity score matching and complex surveys. Statistical Methods in Medical Research, 27(4), 1240–1257. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chinese Center for Disease Control and Prevention . (2022). COVID‐19 Clinical and Surveillance Data—December 9, 2022, to February 6, 2023, China. https://weekly.chinacdc.cn/fileCCDCW/cms/news/info/upload//a02c956c‐9323‐4666‐a80f‐160cfed2ac7d.pdf
- Di Mascio, D. , Buca, D. , Berghella, V. , Khalil, A. , Rizzo, G. , Odibo, A. , Saccone, G. , Galindo, A. , Liberati, M. , & D'Antonio, F. (2021). Counseling inmaternal‐fetal medicine: SARS‐CoV‐2 infection in pregnancy. Ultrasound in Obstetrics & Gynecology, 57(5), 687–697. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ioannidis, J. , Zonta, F. , & Levitt, M. (2023). Estimates of COVID‐19 deaths in mainland China after abandoning zero COVID policy. European Journal of Clinical Investigation, 23, e13956. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jarraya, A. , Kammoun, M. , Bouhamed, O. , Ellouze, Y. , Doukali, O. , & Kolsi, K. (2022). Maternal and perinatal outcomes in the COVID‐19 omicron wave in comparison with the Delta wave: A multicenter observational study. Italian Journal of Gynaecology and Obstetrics, 35, 397–405. 10.36129/jog.2022.74 [DOI] [Google Scholar]
- Jarraya, A. , Kammoun, M. , Kanoun, M. , Derbel, M. , Sansa, H. , Chaaben, K. , & Kolsi, K. (2023). Does COVID‐19 vaccination still have a role in maternal and perinatal outcomes during the omicron era? A multicenter observational study. Italian Journal of Gynaecology and Obstetrics, 35(4), 433–441. 10.36129/jog.2022.85 [DOI] [Google Scholar]
- Jia, L. , Cao, H. , Guo, Y. , Shen, Y. , Zhang, X. , Feng, Z. , Liu, J. , Xie, Z. , & Xu, Z. (2021). Evaluation of epidural analgesia use during labor and infection in full‐term neonates delivered vaginally. JAMA Network Open, 4(9), e2123757. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Li, N. , Han, L. , Peng, M. , Lv, Y. , Ouyang, Y. , Liu, K. , Yue, L. , Li, Q. , Sun, G. , Chen, L. , & Yang, L. (2020). Maternal and neonatal outcomes of pregnant women with COVID‐19 pneumonia: A case‐control study. Clinical Infectious Diseases, 71(16), 2035–2041. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Metz, T. D. , Clifton, R. G. , Hughes, B. L. , Sandoval, G. J. , Grobman, W. A. , Saade, G. R. , Manuck, T. A. , Longo, M. , Sowles, A. , Clark, K. , Simhan, H. N. , Rouse, D. J. , Mendez‐Figueroa, H. , Gyamfi‐Bannerman, C. , Bailit, J. L. , Costantine, M. M. , Sehdev, H. M. , Tita, A. T. N. , Macones, G. A. , … Archer, S. W. (2022). Association of SARS‐CoV‐2 infection with serious maternal morbidity and mortality from obstetric complications. JAMA, 327(8), 748–759. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Norman, M. , Navér, L. , Söderling, J. , Ahlberg, M. , Hervius Askling, H. , Aronsson, B. , Byström, E. , Jonsson, J. , Sengpiel, V. , Ludvigsson, J. F. , Håkansson, S. , & Stephansson, O. (2021). Association of Maternal SARS‐CoV‐2 infection in pregnancy with neonatal outcomes. JAMA, 325(20), 2076–2086. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shuai, H. , Chan, J. F. , Hu, B. , Chai, Y. , Yuen, T. T. , Yin, F. , Huang, X. , Yoon, C. , Hu, J. C. , Liu, H. , Shi, J. , Liu, Y. , Zhu, T. , Zhang, J. , Hou, Y. , Wang, Y. , Lu, L. , Cai, J. P. , Zhang, A. J. , … Chu, H. (2022). Attenuated replication and pathogenicity of SARS‐CoV‐2 B.1.1.529 omicron. Nature, 603(7902), 693–699. [DOI] [PubMed] [Google Scholar]
- Suzuki, R. , Yamasoba, D. , Kimura, I. , Wang, L. , Kishimoto, M. , Ito, J. , Morioka, Y. , Nao, N. , Nasser, H. , Uriu, K. , Kosugi, Y. , Tsuda, M. , Orba, Y. , Sasaki, M. , Shimizu, R. , Kawabata, R. , Yoshimatsu, K. , Asakura, H. , Nagashima, M. , … Sato, K. (2022). Attenuated fusogenicity and pathogenicity of SARS‐CoV‐2 omicron variant. Nature, 603(7902), 700–705. [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
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Data Availability Statement
Data are available on request from the authors.