Abstract
Objectives
To compare gestational weight gain (GWG) during pregnancy and obesity-related maternal morbidity between three months of the first year of the COVID-19 pandemic and three months of the previous year.
Methods
A retrospective comparative study was conducted in a tertiary university-affiliated hospital. GWG, obesity rates and pregnancy complications were compared between the time periods.
Results
Among women with class I obesity, GWG was higher during the pandemic (n = 1071) than the previous year (n = 1194): 11.16 vs. 8.69 kg, p = 0.04. Women during the pandemic compared to the previous year were less likely to be diagnosed with gestational diabetes (odds ratio [OR] = 0.66, 95% confidence interval [CI] 0.47–0.91, p = 0.01) or hypertensive disorders of pregnancy (OR = 0.63, 95% CI 0.35–1.0, p = 0.05) after adjustment for parity, mode of conception and advanced maternal age.
Conclusions
Gestational weight gain increased during the pandemic, yet rates of obesity-related complications were notably fewer. This is likely attributed to decreased detection consequent to limited antenatal care.
Keywords: COVID-19 pandemic, hypertensive disorders of pregnancy, gestational diabetes, obesity, prenatal care
Introduction
The COVID-19 pandemic has had profound effects on various aspects of pregnant women's lives. Pregnant women represent a high-risk group for severe COVID-19 morbidity and are at a higher risk of mortality. 1 During the pandemic, pregnant women have been subject to disruptions in prenatal care, which have increased rates of stillbirth in a number of countries.2,3 The pandemic has also affected the psychological well-being of pregnant women; and high levels of maternal stress, especially anxiety and depression, have been reported.4,5
Importantly, the adverse effects of the COVID-19 pandemic on maternal and perinatal health are not limited to the morbidity and mortality caused directly by the disease itself. COVID-19 restrictions, such as social distancing, lockdown and quarantine, resulted in limited individual mobility. As several studies of the pandemic period have shown, pregnant women were less engaged in physical activity and had higher sedentary behavior levels. 6 A single-center Canadian study showed an increase in maternal obesity rate after the emergence of the COVID-19 pandemic. 7 In an Italian study, higher rates of gestational diabetes mellitus (GDM) were found during the COVID-19 pandemic compared with the pre-pandemic period, independent of maternal age, parity, socio-educational attainment and maternal body mass index (BMI), prior to and at the time of pregnancy. 8 In that study, GDM was more prevalent among women who experienced lockdown during the first trimester.
The first case of COVID-19 in Israel was confirmed on 21 February 2020. A state of national emergency was declared on March 19, due to the increasing number of confirmed cases. During the year 2020, the most intensive and restrictive governmental strategies were applied to contain the virus; these included several lockdowns and the use of mass-surveillance technologies, which led to substantial restrictions in mobility. 9
This study aimed to compare between three months during the first year of the COVID-19 pandemic and the same three months in the previous year: (1) the maternal obesity rate and weight gain during pregnancy in labouring women, and (2) obesity-related pregnancy morbidity including GDM, hypertensive disorders of pregnancy and macrosomia.
Materials and methods
Study design
This is a retrospective comparative study conducted at the Galilee Medical Center, a tertiary-care university affiliated hospital in northern Israel. The study sample comprised a diverse population of Jews, Muslims, Christians and Druze. The study group consisted of pregnant women who delivered between 1 December 2020 and 28 February 2021. For these women, their pregnancy course included several lockdowns and significant restrictions on individual mobility applied by the Israeli government. The control group consisted of women who delivered during the same three-month period in the previous year (1 December 2019 to 28 February 2020), before COVID-19 restrictions were applied in Israel. Women with severe fetal malformations and those who underwent termination of pregnancy after 24 weeks were excluded from the study.
Maternal characteristics and pregnancy outcomes
Maternal data included: maternal age, gravity and parity. To track changes in maternal gestational weight gain (GWG), we collected the following data: pre-pregnancy maternal weight, maternal height, pre-pregnancy BMI, maternal weight at admission to the delivery room, pre-delivery BMI and calculated maternal GWG [GWG was calculated as the following: pre-delivery maternal weight - pre-pregnancy maternal weight (kilograms)]. A BMI of 25–29.9 kg/m2 was classified as overweight, 30–34.99 was classified as class I obesity, 35–39.99 class II obesity and BMI > 40 as class III obesity. Pregnancy data included: caesarean section (CS) rate, gestational age at delivery, birthweight, Apgar scores and stillbirth rates.
We retrieved the following data using our electronic databases of the women included in the study: demographic and biometric details, and data concerning certain components of the metabolic syndrome. The latter included non-fasting triglycerides, total cholesterol, low-density lipoprotein (LDL), high-density lipoprotein (HDL) and glucose. Systolic and diastolic blood pressure measurements on admission were collected; and hemoglobin levels (Hb) as an indirect assessment tool of maternal nutrition. Additionally, we collected data on variables that could be associated with excessive maternal GWG, including the rates of: macrosomia (birthweight > 4000 grams), shoulder dystocia (defined as head to body interval > 60 s or the requirement of any additional manoeuvres to deliver the fetus), hypertensive disorders of pregnancy (gestational hypertension was defined as systolic hypertension ≥ 140 mmHg and/or diastolic blood pressure ≥ 90 mmHg beyond 20 weeks of gestation, preeclampsia was defined as elevated blood pressure as mentioned above and the presence of proteinuria) and GDM (defined as an two abnormal plasma glucose values on 100-grams oral glucose tolerance test after 24 weeks of gestation).
Ethics
The study protocol was reviewed and approved by the institutional review board of our medical center (NHR-21-0142).
Statistics
Continuous variables were compared with the t-test, and categorical variables with the chi-square test or Fisher's exact test, as appropriate. Rank sum analysis (Mann–Whitney) was utilized as appropriate. A p value < 0.05 was considered significant.
Sample size determination
According to reports of the Israeli National Center for Disease Control published a few years before the pandemic, the proportion of women aged 21–45 years with BMI ≥30 kg/m2 was 12.5%. 10 We assumed that the restrictions of the pandemic on lifestyle during pregnancy would increase the proportion of pregnant women with BMI ≥30 kg/m2 by 5%. Based on these estimates, using a two-sided alpha of 0.05% and a beta of 0.20 (power of 80%), we calculated that a sample size of 814 women is required from each period.
Results
The characteristics of the study and control groups are presented in Table 1. The median pre-conceptional maternal weight and height measures were similar for the two groups. The mean parity was lower in the study than the control group (median of 2 (1–8) compared with 2 (1–11), p < 0.001). For the study compared to the control group, the mean systolic blood pressure was lower (120.23 vs. 121.57 mmHg, p = 0.012), a higher proportion had Hb ≥10 g/dL before delivery (89.6% vs. 85.2%, p = 0.003) and the median HDL was higher (67.3 vs. 64.9, p = 0.006). Glucose, triglycerides, LDL and total cholesterol levels were similar in the two groups.
Table 1.
Background data, blood pressure measurements and blood tests results on admission to the delivery room, for pregnant women during the COVID-19 pandemic (study group) and during the previous year (control group)
|
Study group (N = 1071) |
Control group (N = 1194) |
P value | |
|---|---|---|---|
| Maternal age, in years, mean (±SD) | 30.4 (±5.1) | 30.2 (±5.3) | 0.409 |
| Parity, median (range) | 2 (1–8) | 2 (1–11) | <0.001 |
| Primiparity, n. (%) | 298 (27.9) | 301 (25.2) | 0.17 |
| Conception by ART, n. (%) | 17 (1.8) | 57 (4.8) | <0.001 |
| Maternal height, mean (±SD) | 163.1 (6.1) | 162.3 (7.5) | 0.867 |
| Pre-conceptional weight, kg, median (range) | 61 (37–130) | 63 (38–158) | 0.090 |
| Pre-delivery weight, kg, median (range) | 75 (44–149) | 76 (45–139) | 0.476 |
| SBP, mmHg, mean (±SD) | 120.2±12.2 | 121.6±11.1 | 0.012 |
| DBP, mmHg, mean (±SD) | 71.8 (9.4) | 71.6 (9.6) | 0.568 |
| Non-fasting glucose, mg/dL, median (range) | 87.4 (54.3–185.6) | 86.4 (52.6–246.1) | 0.944 |
| Hb, g/dL, median (range) | 11.8 (6.6–15.7) | 11.7 (5.5–16.1) | 0.048 |
| Hb<10 g/dL, mean (±SD) | 101.0 (10.4) | 175.0 (14.8) | 0.003 |
| Triglycerides, mmol/L, median (range) | 145.4 (44.7–849.4) | 143.1 (43.6–545.3) | 0.125 |
| LDL, mmol/L, median (range) | 81.6 (11.5–243.2) | 83.6 (13.0–244.0) | 0.054 |
| Cholesterol, mmol/L, median (range) | 157.9 (70.0–318.8) | 155.7 (51.5–329.0) | 0.384 |
| HDL, mmol/L, median (range) | 41.8 (11.7–84.2) | 40.2 (13.4–72.7) | 0.006 |
| SBP ≥140 and/or DBP ≥ 90 at admission to delivery, n. (%) | 43 (5.0) | 57 (5.5) | 0.68 |
SD standard deviation, ART artificial reproductive technologies, SBP, systolic blood pressure; DBP, diastolic blood pressure; Hb, hemoglobulin; HDL, high-density lipoprotein; LDL, low-density lipoprotein
Table 2 presents obstetrical and neonatal outcomes of the study and control groups. For the study compared to the control group, the CS rate was lower (19.7% vs. 24.1%, p = 0.016), and a smaller proportion of women was diagnosed with hypertensive disorders of pregnancy (2.2% vs. 3.9%, p = 0.02). For the study and control groups, 71 (6.6%) and 119 (19%) women, respectively, p = 0.05 were diagnosed with GDM. Women in the study group were less likely to have a diagnosis of gestational diabetes (odds ratio [OR] = 0.66, 95% confidence interval [CI] 0.47–0.91, p = 0.01) or hypertensive disorders of pregnancy (OR = 0.63, 95% CI 0.35–1.0, p = 0.05) after adjustment for parity, mode of conception and advanced maternal age. No difference was found between the groups in the rates of shoulder dystocia and macrosomia. Intrauterine fetal death rates were similar between the groups. Differences were not found between the groups in preterm birth (<37 weeks, <34 weeks or <32 weeks). The rates of low birthweight (LBW) and very LBW (VLBW) were higher in the study than the control group (7.8% vs. 6.0%, p = 0.04 one-sided and 1.5% vs. 0.8%, p = 0.018, respectively). Apgar scores <7 were more prevalent in the study than the control group (2.0% vs. 0.7%, p = 0.013).
Table 2.
Obstetrical and neonatal outcomes of pregnant women during the COVID-19 pandemic (study group) and during the previous year (control group)
|
Study group (N = 1071) |
Control group (N = 1194) |
P value | |
|---|---|---|---|
| Cesarean section, n. (%) | 184 (19.7) | 288 (24.1) | 0.016 |
| Hypertensive disorders of pregnancy, n. (%) | 24 (2.2) | 47 (3.9) | 0.022 |
| GDM, n. (%) | 71 (6.6) | 119 (10.0) | 0.005 |
| Shoulder dystocia, n. (%) | 3 (0.3) | 2 (0.2) | 0.672 |
| GA at delivery, median (range) | 39.4 (23.0–42.4) | 39.4 (23.7–43.1) | 0.215 |
| Preterm birth <37 weeks, n. (%) | 92 (8.6) | 95 (8.0) | 0.758 |
| Male newborn, n. (%) | 575 (53.7) | 601 (50.3) | 0.119 |
| Birthweight, gram, mean (±SD) | 3251.3 (584.0) | 3265.0 (535.7) | 0.562 |
| Macrosomia > 4000 grams, n. (%) | 69 (6.4) | 84 (7.0) | 0.615 |
| LBW < 2500 grams, n. (%) | 84 (7.8) | 71 (6.0) | 0.038* |
| VLBW < 1500 grams, n. (%) | 16 (1.5) | 10 (0.8) | 0.018 |
| 5-minute Apgar score < 7, n. (%) | 21 (2.0) | 8 (0.7) | 0.013 |
| Stillbirth, n. (%) | 6 (0.6) | 4 (0.4) | 0.531 |
GDM gestational diabetes, GA gestational age, LBW low birthweight, VLBW very low birthweight, SD standard deviation
*p value one-sided
Mean pre-delivery BMI and GWG did not differ significantly between the study and control groups (Table 3). Among women with class I obesity (pre-conceptional BMI of 30–34.99 kg/m2) in the study group compared to women with class I obesity in the control group, the mean GWG was higher (11.16 vs. 8.69 kg, p = 0.04).
Table 3.
Pre-conception and pre-delivery body mass index of pregnant women during the COVID-19 pandemic (study group) and during the previous year (control group)
| Study group | Control group | P value | |
|---|---|---|---|
| Pre-conceptional BMI, mean (±SD) | 24.3 (±4.9) | 24.6 (±5.1) | 0.08 |
| BMI <19.99, n. (%) | 153 (17.6) | 168 (17.1) | |
| BMI 20-24.99, n. (%) | 411 (47.4) | 431 (43.8) | |
| BMI 25-29.99, n. (%) | 183 (21.1) | 242 (24.6) | |
| BMI 30-34.99, n. (%) | 84 (9.7) | 105 (10.7) | |
| BMI >35, n. (%) | 36 (4.2) | 37 (3.8) | |
| BMI at delivery, mean (±SD) | 29.2 (±4.9) | 29.4 (±5.1) | 0.28 |
| BMI at delivery ≥30, n. (%) | 201 (27.2) | 258 (31.3) | 0.08 |
| Difference in BMI (pre-conceptional and pre-delivery), mean (±SD | 4.9 (2.5) | 4.8 (2.7) | 0.273 |
| GWG, kg, mean (±SD | 13.2 (6.9) | 12.8 (7.4) | 0.231 |
| GWG according to pre-conceptional BMI, kg, mean (±SD) | |||
| BMI <19.99 | 14.8 (5.5) | 13.8 (5.1) | 0.217 |
| BMI 20-24.99 | 14.1 (5.9) | 14.1 (5.71) | 0.981 |
| BMI 25-29.99 | 11.9 (5.75) | 12.5 (6.8) | 0.329 |
| BMI 30-34.99 | 11.2 (7.4) | 8.7 (8.7) | 0.042 |
| BMI >35 | 7.0 (9.5) | 5.5 (17.4) | 0.661 |
BMI body mass index (kg/m2), SD standard deviation, GWG gestational weight gain
Discussion
Main findings
For women with class I obesity who delivered during the pandemic compared to women with class I obesity who delivered the previous year, GWG was higher. Among women who delivered during the pandemic compared to women who delivered the previous year, mean pre-delivery Hb and HDL levels were higher. GDM and hypertensive disorders of pregnancy were significantly less diagnosed in the pandemic period.
Comparison with previous studies
Gestational weight gain and pre-delivery BMI were similar in the two periods. However, among women who delivered during the pandemic compared to the previous year, the mean GWG of those with pre-conceptional class I obesity was higher. A cohort study from Beijing, China, found that during the COVID-19 pandemic, more women manifested either insufficient or excessive GWG in accordance with the Institute of Medicine criteria. 11 In a cross-sectional study conducted in the United States showed that the COVID-19 pandemic was associated with a decrease in GWG. 12 Using an online questionnaire, a Chinese investigation revealed that emotional eating increased during the pandemic, and correlated with maternal stress and reduced physical activity. Emotional eating was also found to be associated with higher GMG and less fish intake. 13 Other factors that might have affected GWG during the COVID-19 pandemic are decreased physical activity and increased hours spent sitting. 14 A randomized controlled trial reported less weight gain among women who participated in a virtually supervised exercise program three times per week throughout pregnancy, compared to a control group. 15
We report that during the pandemic period compared to the previous year, the proportion of patients with Hb levels less than 10 g/dL was lower, and non-fasting HDL levels were higher. However, non-fasting LDL, triglycerides and total cholesterol levels were similar between the two periods. We do not have information on the diets of the women during and before the pandemic. Among 700 pregnant women in the US who responded to an internet survey, 17% reported that their diets worsened during the COVID-19 pandemic, 42% reported improvements and 41% reported no change. 16 In contrast, 90 Spanish pregnant women mostly reported maintaining good adherence to their Mediterranean diet during the pandemic. 14
We report a 34% lower proportion of women diagnosed with GDM during the pandemic compared with the pre-pandemic period (6.6% vs. 10.0%, p = 0.005). This is despite similar maternal age, primiparity rates, GWG and pre-conceptional BMI in the two periods. Several studies have reported higher GDM rates during the pandemic, probably due to increased maternal obesity. For example, a retrospective study from Italy reported higher GDM incidence during the pandemic than a pre-pandemic period (9.3% vs. 3.4%, p < 0.001). 17 Higher GDM rates were related to higher mean maternal GWG (9.3 vs. 6.6 kg, p = 0.007) and increased mean BMI at delivery (31.3 vs. 28.4 kg/m2, p = 0.02). Accordingly, the COVID-19 pandemic was reported as associated with higher GDM rates (OR = 1.22, 95% CI: 1.17–1.27). 18 However, others have reported a drop in oral glucose tolerance tests performed during the pandemic due to restrictions in personal mobility during lockdowns and maternal fear of infection. 19 Additionally, various professional bodies adopted changes in GDM diagnosis criteria during the pandemic, which led to an underdiagnosis of GDM. 19 As the Israeli diagnostic criteria for GDM did not change during the pandemic, the drop in GDM diagnosis observed between the study periods could be attributed to inadequate antenatal screening. The lack of information on the frequency of antenatal visits at community clinics precluded confirming this possibility. However, a 2022 report of the Israel Ministry of Health 20 revealed that antenatal screening test performance declined significantly during the COVID-19 pandemic. The data for that report were collected by our group two months before the initiation of the current study. The trend was most pronounced among multiparous women with low-risk pregnancies and those from minority ethnic backgrounds.
In our study, the rate of hypertensive disorders of pregnancy was lower during the pandemic compared to the pre-pandemic period. Lower rates of hypertension were reported in the pandemic than the pre-pandemic period (3.7% vs. 5.7%, p = 0.005), which were attributed to decreased antenatal visits and to more maternal bed rest. 21 Our findings might imply underdiagnosis of hypertension in pregnancy during the COVID-19 pandemic, consequent to fewer face-to-face antenatal visits. 20 A systematic review that included studies from low- and high-resource settings found no overall significant effect of the pandemic on maternal and neonatal outcomes related to hypertensive disorders. 22 Nevertheless, risks of maternal death and hypertensive disorders of pregnancy were higher in an analysis that included only studies from low-resource settings. This demonstrates considerable disparity in maternal outcomes and antenatal care between high-income and low- and middle-income countries. Barton et al. suggested that during the pandemic, each pregnant woman should be classified as low risk or high risk for hypertensive disorders of pregnancy. 23 Such classification would help determine a recommended number of antenatal visits. The authors also proposed that all pregnant women should obtain a sphygmomanometer, to enable self-measurement of blood pressure when maternal symptoms emerge. Additionally, they recommend omitting the assessment of urinary protein during the pandemic, as the management of gestational hypertension and preeclampsia is the same.
Our findings of higher rates of LBW and VLBW corroborate a previous study, 24 which reported increased risks of LBW and small for gestational age fetuses (adjusted OR (95% CI) = 1.13 (1.02, 1.24) and 1.11 (1.02, 1.21), respectively) during the pandemic. Others reported no change in the rates of LBW or VLBW during the pandemic. 22 Differences between studies in the COVID-19 lockdown regulations that were applied during the periods analysed, and in the responses of the populations, may partially explain the discrepancies in the findings.
We report a 4.4% lower rate in CS during the pandemic period compared to the previous year. A study conducted in England reported higher rates of both emergency and elective CS during the pandemic compared to a previous period. The explanations suggested were that delayed diagnosis of adverse conditions and occupational stress among obstetricians could have led to a more interventionist approach. 25 Nevertheless, similar to our findings, other studies reported no change or lower CS rates during the COVID-19 pandemic. 22 Despite the lower CS rate during the pandemic period, we found higher fetal distress in this period compared with the control group (2.0% vs. 0.7% of the infants had 5-min Apgar scores <7, p = 0.013). This corroborates a reported increase of 11% in fetal distress during the pandemic, after controlling for confounding factors. The increase was attributed to impaired antenatal care during the pandemic and specifically to delayed diagnosis of adverse conditions. 11 However, we did not find any difference in stillbirth rates between the two periods. These findings should be interpreted with caution as the factors influencing obstetrical care and pregnancy outcomes during the COVID-19 pandemic are complex.
Limitations
The study duration was limited to a specific time interval, and random variation of evaluated data across time could have contributed to the differences in GWG. Furthermore, regarding the observed difference in GWG among women with class I obesity, the potential for a type 1 error cannot be ruled out. In addition, the retrospective design precluded assessment of such risk factors as inadequate antenatal care, maternal stress and changes in diet. Moreover, given its retrospective design, our study was subject to several possible biases, namely reporting bias and selection bias.
A strength of this study is the large number of patients whose pregnancy course was under severe local restrictions and several lockdowns. Additionally, clinical, laboratory and demographic information was included, which enabled a broad comparison of maternal and neonatal outcomes between the study periods.
Conclusions
In conclusion, we report increased GWG during the pandemic, among women with certain characteristics. Furthermore, the pandemic was associated with clear drops in diagnoses of GDM and hypertensive disorders of pregnancy and increases in some adverse perinatal outcomes. More research is needed to assess direct factors leading to abnormal GWG and to provide corresponding strategies. Interventional programs to enhance appropriate GWG such as dietitian teleconsultations and online exercise could be useful. Health education programs and adaptive changes in maternal health care facilities should be designed to maintain quality of maternal health service during the pandemic.
Footnotes
Authors contributions: IS - concept and design, acquisition of data, drafting the manuscript; TYF - data collection; LL - critical revision of manuscript; MFW - interpretation of data, critical revision of manuscript.
Data availability statement: The datasets analysed during the current study are available from the corresponding author on reasonable request.
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding: The author(s) received no financial support for the research, authorship, and/or publication of this article.
Ethical approval: Not applicable
Informed consent: Not applicable
ORCID iD: Inshirah Sgayer https://orcid.org/0000-0002-5270-8436
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