Higher severe acute respiratory syndrome coronavirus 2 infection rate in pregnant patients





Background


During the early months of the coronavirus disease 2019 pandemic, risks associated with severe acute respiratory syndrome coronavirus 2 in pregnancy were uncertain. Pregnant patients can serve as a model for the success of clinical and public health responses during public health emergencies as they are typically in frequent contact with the medical system. Population-based estimates of severe acute respiratory syndrome coronavirus 2 infections in pregnancy are unknown because of incomplete ascertainment of pregnancy status or inclusion of only single centers or hospitalized cases. Whether pregnant women were protected by the public health response or through their interactions with obstetrical providers in the early months of pandemic is not clearly understood.


Objective


This study aimed to estimate the severe acute respiratory syndrome coronavirus 2 infection rate in pregnancy and to examine the disparities by race and ethnicity and English language proficiency in Washington State.


Study Design


Pregnant patients with a polymerase chain reaction–confirmed severe acute respiratory syndrome coronavirus 2 infection diagnosed between March 1, 2020, and June 30, 2020 were identified within 35 hospitals and clinics, capturing 61% of annual deliveries in Washington State. Infection rates in pregnancy were estimated overall and by Washington State Accountable Community of Health region and cross-sectionally compared with severe acute respiratory syndrome coronavirus 2 infection rates in similarly aged adults in Washington State. Race and ethnicity and language used for medical care of pregnant patients were compared with recent data from Washington State.


Results


A total of 240 pregnant patients with severe acute respiratory syndrome coronavirus 2 infections were identified during the study period with 70.7% from minority racial and ethnic groups. The principal findings in our study were as follows: (1) the severe acute respiratory syndrome coronavirus 2 infection rate was 13.9 per 1000 deliveries in pregnant patients (95% confidence interval, 8.3–23.2) compared with 7.3 per 1000 (95% confidence interval, 7.2–7.4) in adults aged 20 to 39 years in Washington State (rate ratio, 1.7; 95% confidence interval, 1.3–2.3); (2) the severe acute respiratory syndrome coronavirus 2 infection rate reduced to 11.3 per 1000 deliveries (95% confidence interval, 6.3–20.3) when excluding 45 cases of severe acute respiratory syndrome coronavirus disease 2 detected through asymptomatic screening (rate ratio, 1.3; 95% confidence interval, 0.96–1.9); (3) the proportion of pregnant patients in non-White racial and ethnic groups with severe acute respiratory syndrome coronavirus disease 2 infection was 2- to 4-fold higher than the race and ethnicity distribution of women in Washington State who delivered live births in 2018; and (4) the proportion of pregnant patients with severe acute respiratory syndrome coronavirus 2 infection receiving medical care in a non-English language was higher than estimates of pregnant patients receiving care with limited English proficiency in Washington State (30.4% vs 7.6%).


Conclusion


The severe acute respiratory syndrome coronavirus 2 infection rate in pregnant people was 70% higher than similarly aged adults in Washington State, which could not be completely explained by universal screening at delivery. Pregnant patients from nearly all racial and ethnic minority groups and patients receiving medical care in a non-English language were overrepresented. Pregnant women were not protected from severe acute respiratory syndrome coronavirus 2 infection in the early months of the pandemic. Moreover, the greatest burden of infections occurred in nearly all racial and ethnic minority groups. These data coupled with a broader recognition that pregnancy is a risk factor for severe illness and maternal mortality strongly suggested that pregnant people should be broadly prioritized for coronavirus disease 2019 vaccine allocation in the United States similar to some states.


Introduction


In the early months of the coronavirus disease 2019 (COVID-19) pandemic, risks associated with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection in pregnancy were uncertain. As pregnant patients are typically in frequent contact with the medical system, they can serve as a model for the success of the clinical and public health responses during public health emergencies. Outside US urban centers with high infection rates, studies in the early months of the COVID-19 pandemic reported low SARS-CoV-2 infection prevalence in pregnant patients undergoing universal screening at admission to the hospital for delivery. Population-based estimates of SARS-CoV-2 infections in pregnancy are lacking because of incomplete ascertainment of pregnancy status or inclusion of only single centers or hospitalized cases. Furthermore, a disproportionate impact of COVID-19 on racial and ethnic minorities, including pregnant patients, has been reported. , However, Centers for Disease Control and Prevention data are missing pregnancy status for 65% of their COVID-19 case report forms, making it impossible to estimate infection rates in the US pregnant population. Population-based studies of COVID-19 in pregnancy with comprehensive data regarding race, ethnicity, and language are essential to developing effective interventions for populations disproportionately affected by COVID-19.



AJOG at a Glance


Why was this study conducted?


To determine the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection rate in pregnant patients and to assess racial and ethnic disparities in a multicenter, retrospective cohort study in Washington State.


Key findings


The SARS-CoV-2 infection rate was significantly higher in pregnant people (N=240; 13.9 per 1000 deliveries) than people aged 20 to 39 years (7.3 per 1000; rate ratio, 1.7; 95% confidence interval, 1.3–2.3) in Washington State. Compared with the distribution of women in Washington State who delivered live births in 2018, the proportion of pregnant women from racial and ethnic minority groups with SARS-CoV-2 infection was 2- to 4-fold higher.


What does this add to what is known?


The SARS-CoV-2 infection rate in pregnant patients was higher than nonpregnant adults in Washington State, and nearly all non-White racial and ethnic groups were disproportionately affected.



Washington State provided a valuable case study evaluating the impact of COVID-19 on pregnant individuals. In addition, Washington State was the first state to detect community transmission of SARS-CoV-2 and imposed a shelter-in-place order. Here, we aimed to estimate and compare the infection rates between pregnant patients and similarly aged adults in Washington State and to examine the disparities by race and ethnicity and language use.


Materials and Methods


Study population


The Washington State COVID-19 in Pregnancy Collaborative (WA-CPC) identified pregnant women (≥18 years) with SARS-CoV-2 infection confirmed using a polymerase chain reaction test from 35 hospitals and clinics in Washington State between March 1, 2020, and June 30, 2020 ( Figure ; Supplemental Table 1 ). Each site identified patients with an infection during any trimester of pregnancy irrespective of pregnancy outcome, abstracted clinical and SARS-CoV-2 testing data from medical records, and reported number of annual deliveries, actual number of deliveries during the study period, and SARS-CoV-2 testing strategies employed over time. Pregnant women were tested for several reasons during the study period, including exposure to a known SARS-CoV-2 case, universal screening before procedures or delivery, symptoms, travel, and personal requests. Testing occurred in the general population for similar reasons, including universal testing before medical procedures, with increasing test availability over time. Race and ethnicity data abstracted from medical records were self-reported by patients.




Figure


Number of study sites, proportion of deliveries, and number of COVID-19 cases

A, The number of study sites ( circles ) and proportion of deliveries ( color gradient ) captured by the Washington State COVID-19 in Pregnancy Collaborative is depicted within each Washington State Department of Health ACH region. B, The number of COVID-19 cases in pregnant patients within each ACH region is shown numerically and by circle size with infection rate in pregnancy depicted by the color gradient .

ACH , Accountable Community of Health; COVID-19 , coronavirus disease 2019.

Lokken et al. Severe acute respiratory syndrome coronavirus 2 infection rate in pregnancy. Am J Obstet Gynecol 2021.


This multisite medical record review was approved by the institutional review boards (IRBs) at the University of Washington (study number 00009701, approved March 6, 2020) and Swedish Medical Center (study number 2020000172, approved March 19, 2020). All other sites entered into reliance agreements with the University of Washington IRB. The IRB waived the need for informed consent. Data provided by each site were deidentified.


Statistical analysis


To estimate statewide coverage of annual deliveries captured at WA-CPC sites and the SARS-CoV-2 infection rates in pregnancy, we assessed site-specific data (SARS-CoV-2 cases, number of deliveries) within the Washington State Accountable Community of Health (ACH) regions. , Because of small case numbers in some of the 9 ACH regions, we collapsed geographically close regions to yield 6 regions for analysis ( Figure ). To estimate the proportion of annual statewide deliveries captured by collaborating sites, the number of total site-reported annual deliveries was divided by the number of live births in 2018 in Washington State and by ACH region using Washington State Department of Health (WA-DOH) data.


The ACH-specific and overall SARS-CoV-2 infection rates in pregnancy (per 1000 deliveries) at WA-CPC sites were estimated using the site-specific infection rate (number of cases divided by number of deliveries during the study period) and Poisson regression (with 95% confidence interval [CI]), with clustering by ACH region for the overall estimate. As a comparison group, the SARS-CoV-2 infection rates in all patients aged 20 to 39 years (females and males) in Washington State during the study period were calculated using publicly available SARS-CoV-2 surveillance data for confirmed cases (numerator) and 2019 population estimates for patients aged 20 to 39 years (denominator); we were unable to exclude cases in men because of limitations of the publicly available surveillance data. , This group served as the best available proxy estimate for the SARS-CoV-2 infection rate for reproductive-aged women. Although women aged <20 and >39 years are fecund, Washington State SARS-CoV-2 surveillance data were only available in wide categories, including 0 to 19 years, 20 to 39 years, 40 to 59 years, and older categories; neither age groups of 0 to 19 years nor 40 to 59 years were appropriate comparison groups for approximating infection rates in most reproductive-age women, and therefore, the 20- to 39-year-old age group was selected for comparison. Rate ratios (RR) and 95% CI were calculated comparing WA-CPC infection rates in pregnancy with overall SARS-CoV-2 infection rates of patients aged 20 to 39 years in Washington State within each ACH region; an ACH-weighted overall RR was also estimated. To assess how infection rates in pregnancy may have been affected by increased access to testing in the pregnant population, we conducted a sensitivity analysis excluding cases of SARS-CoV-2 in pregnancy detected through asymptomatic universal screening before procedures or delivery. We were unable to subtract cases in the general population comparison group similarly identified through preprocedure universal testing. Lastly, the WA-DOH provided SARS-CoV-2 case counts of pregnant females aged 18 to 50 years between March 1, 2020, and June 30, 2020, by ACH region for comparison ; pregnancy status was ascertained through public health department investigation. As a sensitivity analysis, infection rates in pregnancy were calculated, and the DOH-reported case counts and the statewide live births were estimated from March 2020 to June 2020 using Washington State 2018 birth data.


We compared the race and ethnicity distribution of the study population with that of women who delivered live births in 2018 in Washington State. Race and ethnicity data were categorized as American Indian or Alaskan Native, Asian, Black, Hispanic, Native Hawaiian, other Pacific Islander, multiracial, and White; Hispanic was considered a mutually exclusive race and ethnicity group to align with WA-DOH categories. For each race and ethnicity category among pregnant patients in the study population, prevalence and exact 95% CI were estimated with clustering by ACH region. Furthermore, we generated ACH-weighted prevalence ratios (PRs) and 95% CI comparing the race and ethnicity in the study population with the race and ethnicity distribution of women who delivered live births in 2018 in Washington State. In addition, we generated PRs for the King and Greater Columbia ACH regions, which had the highest number of SARS-CoV-2 cases through June 30, 2020. For ACH-specific analyses, race and ethnicity data were repressed when there were <10 cases in alignment with WA-DOH privacy guidelines. Moreover, we compared the proportion of pregnant patients in our study receiving medical care in a non-English language with the proportion of individuals receiving care in Washington State in 2017 with limited English language proficiency (individuals aged >5 years, who speak English “less than very well”) per 2014–2017 American Community Survey data reported by the WA-DOH. Each publicly available data source and how it contributed to these analyses are further described in Supplemental Table 2 .


Results


Capture of pregnancies and severe acute respiratory syndrome coronavirus 2 infections among pregnant patients at Washington State COVID-19 in Pregnancy Collaborative sites


The estimated proportion of annual deliveries in Washington State covered at WA-CPC sites was 61.1%, ranging from 35.0% to 93.0% by region ( Figure ; Table 1 ). Of 35 WA-CPC sites, 22 (62.9%) were hospitals and 13 were clinics providing prenatal care only. Patients were universally screened for SARS-CoV-2 infection using nasopharyngeal swab tests before or at the time of admission for delivery in 14%, 64%, and 76% of hospitals by the end of March, April, and May, respectively. The 5 hospitals without universal testing at delivery by the end of May had initiated universal testing for scheduled delivery admissions only.



Table 1

WA-CPC statewide coverage of pregnancies and cases of severe acute respiratory syndrome coronavirus 2 reported to the WA-DOH























































































































ACH region WA-CPC SARS-CoV-2 cases in pregnancy
Sites Annual deliveries at sites a Live births in WA in 2018 b Cases detected by WA-CPC Cases reported to the WA-DOH c
n n (%) n (%) Percentage captured by WA-CPC, % n (%) n (%) Percentage captured by WA-CPC, d %
Better Health Together or North Central 7 3832 (7.3) 10,129 (11.8) 37.8 14 (5.8) 23 (6.6) 60.9
Greater Columbia 10 7720 (14.7) 9438 (11.0) 81.8 88 (36.7) 135 (39.0) 65.2
King 9 22,623 (43.1) 24,337 (28.3) 93.0 94 (39.2) 98 (28.3) 95.9
North Sound 3 7460 (14.2) 14,265 (16.6) 52.3 16 (6.7) 60 (17.3) 26.7
Pierce 2 5148 (9.8) 11,462 (3.3) 44.9 17 (7.1) 20 (5.8) 85.0
SW Washington State Regional Health, Olympic, or Cascade Pacific Action Alliance 4 5725 (10.9) 16,375 (19.0) 35.0 11 (4.6) 10 (2.9) 110.0
Washington State total 35 52,508 (100) 86,006 e (100) 61.1 240 346 69.4

Adapted from Washington State Department of Health.

ACH , Accountable Community of Health; COVID-19 , coronavirus disease 2019; SARS-CoV-2 , severe acute respiratory syndrome coronavirus 2; WA-CPC , Washington State COVID-19 in Pregnancy Collaborative; WA-DOH , Washington State Department of Health.

Lokken et al. Severe acute respiratory syndrome coronavirus 2 infection rate in pregnancy. Am J Obstet Gynecol 2021.

a Approximate annual deliveries were reported by each site


b 2018 data from the WA-DOH birth data dashboard tool (Birth Certificate Data, 2000–2018, Community Health Assessment Tool)


c Case counts of confirmed SARS-CoV-2 cases among females aged 18 to 50 years who were pregnant at the time of infection were provided by the WA-DOH from March 1, 2020, to June 30, 2020. Pregnancy status was ascertained through case interviews or by local health jurisdiction investigation. In 35% of SARS-CoV-2 case records among females aged 18 to 50 years, pregnancy status was unknown or missing


d Direct linking of WA-CPC and WA-DOH cases was not possible, so the exact overlap of WA-CPC and WA-DOH identified cases is unknown


e The total number of live births in Washington State in 2018 was 84,046, but 40 cases were not attributed to an ACH region.



A total of 240 cases of SARS-CoV-2 infections in pregnancy were detected at WA-CPC sites. Most SARS-CoV-2 cases in pregnancy were detected in the King (94 [39.2%]) and Greater Columbia (88 [36.7%]) ACH regions ( Figure ; Table 1 ). Of the WA-CPC cases, 38 (15.8%) were detected in the first trimester of pregnancy, 67 (27.9%) in the second trimester of pregnancy, and 135 (56.3%) in the third trimester of pregnancy, as previously reported. Of the 240 cases, 45 (18.8%) were diagnosed through asymptomatic screening strategies (preprocedure and universal screening before delivery); this screening strategy excludes patients who were asymptomatic but were tested due to having a known exposure to COVID-19.


During the study period, the WA-DOH identified 346 cases of SARS-CoV-2 infections in pregnancy throughout Washington State, but pregnancy status was missing for 35% of the cases in females aged 18 to 50 years. The WA-CPC captured 240 of 346 SARS-CoV-2 infections (69.4%) in pregnancy that were reported to the WA-DOH, ranging from 26.7% to 110.0% of cases at the ACH region level ( Table 1 ). However, direct linking of the WA-CPC and WA-DOH cases was not possible, so the exact overlap of the WA-CPC– and WA-DOH–identified cases is unknown.


Severe acute respiratory syndrome coronavirus 2 infection rates


The overall infection rate in pregnancy at WA-CPC sites was 13.9 per 1000 deliveries (95% CI, 8.3–23.2). At the ACH region level, infection rates in pregnancy at WA-CPC sites ranged from 6.2 per 1000 (95% CI, 3.2–11.2) to 33.2 per 1000 deliveries (95% CI, 26.9–40.9) ( Figure ; Table 2 ). In the King ACH region, where capture rates of annual deliveries and state reported SARS-CoV-2 cases in pregnancy were >90%, the infection rate in pregnancy at WA-CPC sites was 12.9 per 1000 deliveries (95% CI, 10.5–15.8). Compared with the SARS-CoV-2 infection rate among patients aged 20 to 39 years in Washington State of 7.3 per 1000 (95% CI, 7.2–7.4), the overall infection rate in pregnancy at WA-CPC sites was 1.7 times higher (ACH-weighted RR, 1.7; 95% CI, 1.3–2.3) ( Table 2 ). The result equates to an absolute risk difference of 5.4 per 1000 (95% CI, 0.8–10.0). Moreover, there were significantly higher infection rates in pregnancy in some, but not all, ACH regions ( Table 2 ). For example, in the King ACH region, there was a 2.2 times higher rate of SARS-CoV-2 infections in pregnant women at WA-CPC sites compared with individuals aged 20 to 39 years (RR, 2.2; 95% CI, 1.8–2.8). In the sensitivity analysis estimating the infection rate in pregnancy using the WA-DOH–reported SARS-CoV-2 infections in pregnancy case counts, the statewide infection rate in pregnancy was similar to that estimated using data from WA-CPC sites (WA-DOH, 12.1 per 1000 deliveries; 95% CI, 10.8–13.4) and was 1.7 times higher than that of individuals aged 20 to 39 years in Washington State (95% CI, 1.4–2.2) ( Supplemental Table 3 ). Finally, when excluding the 45 cases of SARS-CoV-2 infections in pregnancy that were detected through asymptomatic screening strategies (preprocedure and universal testing at delivery) at WA-CPC sites, the overall infection rate in pregnancy at WA-CPC sites was 11.3 per 1000 deliveries (95% CI, 6.3–20.3), which was 30% higher than the infection rate of individuals aged 20 to 39 years in Washington State (ACH-weighted RR, 1.3; 95% CI, 0.96–1.9) ( Supplemental Table 4 ).



Table 2

Severe acute respiratory syndrome coronavirus 2 infection rates in pregnancy in Washington State







































































































































ACH region Washington State COVID-19 in Pregnancy Collaborative Washington State: 20–39 y RR
Cases in pregnancy Deliveries during the study period SARS-CoV-2 infection rate per 1000 deliveries Cases a Population b
n
SARS-CoV-2 infection rate per 1000
n (%) n (%) Rate (95% CI) n (%) Rate (95% CI) RR (95% CI)
Better Health Together or North Central 14 (5.8) 1318 (7.6) 10.6 (6.3–17.9) 1746 (11.5) 214,300 8.1 (7.8–8.5) 1.3 (0.7–2.2)
Greater Columbia 88 (36.7) 2653 (15.4) 33.2 (26.9–40.9) 5459 (35.8) 193,851 28.2 (27.4–28.9) 1.2 (0.9–1.4)
King 94 (39.2) 7283 (42.3) 12.9 (10.5–15.8) 4274 (28.0) 744,386 5.7 (5.6–5.9) 2.2 (1.8–2.8)
North Sound 16 (6.7) 2506 (14.5) 6.4 (3.9–10.4) 1752 (11.5) 325,671 5.4 (5.1–5.6) 1.2 (0.7–1.9)
Pierce 17 (7.1) 1696 (9.8) 10.0 (6.2–16.1) 1173 (7.7) 239,814 4.9 (4.6–5.2) 2.0 (1.2–3.3)
SW Washington State Regional Health, Olympic, or Cascade Pacific Action Alliance 11 (4.6) 1777 (10.3) 6.2 (3.4–11.2) 834 (5.5) 358,226 2.3 (2.2–2.5) 2.7 (1.3–4.8)
Washington State total 240 17,233 13.9 (8.3–23.2) c 15,238 d 2,076,248 7.3 (7.2–7.4) 1.7 (1.3–2.3) e

Adapted from the Washington State Department of Health and the Washington State Office of Financial Management. ,

ACH , Accountable Community of Health; CI , confidence interval; COVID-19 , coronavirus disease 2019; RR , rate ratio; SARS-CoV-2 , severe acute respiratory syndrome coronavirus 2.

Lokken et al. Severe acute respiratory syndrome coronavirus 2 infection rate in pregnancy. Am J Obstet Gynecol 2021.

a Case data were calculated from March 1, 2020, to June 28, 2020 (closest available date to June 30, 2020) using the “COVID-19 in Washington State: Confirmed Cases, Hospitalizations and Deaths by Week of Illness Onset, County, and Age” data set available from the Washington State Department of Health at https://www.doh.wa.gov/Emergencies/COVID19/DataDashboard . Counts include females and males


b Population estimate calculated using the 2019 postcensal population estimates from the Washington State Office of Financial Management


c Infection rates were calculated with Poisson regression with additional clustering by ACH for the statewide estimate


d The overall number of SARS-CoV-2 cases through June 28, 2020 was 15,238, but 20 cases were not assigned to an ACH region


e The statewide rate ratio is an ACH-weighted state estimate.



Racial and ethnic groups


Among the 240 SARS-CoV-2 cases in pregnancy detected at WA-CPC sites, most cases were among women from racial and ethnic minority groups, including 126 Hispanic women (52.5%), 20 Black women (8.3%), 8 American Indian or Alaska Native women (3.3%), 8 Asian women (3.3%), and 8 Native Hawaiian or other Pacific Islander women (3.3%) ( Table 3 ). Compared with the distribution of women in Washington State who delivered live births in 2018, the proportion of pregnant women from racial and ethnic minority groups with SARS-CoV-2 infection was 2.0- to 3.9-fold higher ( Table 3 ). For example, the proportion of pregnant Hispanic women with SARS-CoV-2 infection was 2.1 times higher (ACH-weighted PR, 2.1; 95% CI, 1.4–3.1) than the proportion of Hispanic women who delivered live births in 2018 in Washington State (52.5% vs 18.6%) ( Table 3 ). In contrast, the proportion of White and Asian pregnant women with SARS-CoV-2 infection was lower than expected based on 2018 birth data (White ACH-weighted PR, 0.6; 95% CI, 0.3–1.1; Asian ACH-weighted PR, 0.4; 95% CI, 0.1–1.5).



Table 3

Race and ethnicity among pregnant patients with severe acute respiratory syndrome coronavirus 2 infections compared with individuals in Washington State



























































































Variable Washington State COVID-19 in Pregnancy Collaborative (N=240) a Washington State 2018 live births (N=86,046) b PR c
Race and ethnicity n (%) (95% CI) n (%) PR (95% CI)
Hispanic 126 (52.5) (11.9–90.7) 16,010 (18.6) 2.1 (1.4–3.1)
American Indian or Alaska Native, non-Hispanic 8 (3.3) (0.1–16.2) 1206 (1.4) 3.8 (1.3–9.7)
Asian, non-Hispanic 8 (3.3) (0.3–12.6) 8843 (10.3) 0.4 (0.1–1.5)
Native Hawaiian or Other Pacific Islander, non-Hispanic 8 (3.3) (0.4–11.6) 1195 (1.4) 3.9 (0.8–13.0)
Black, non-Hispanic 20 (8.3) (0.3–36.4) 4151 (4.8) 2.0 (1.1–3.7)
White, non-Hispanic 51 (21.3) (5.8–46.9) 49,513 (57.6) 0.6 (0.3–1.1)
Multiracial or other d 5 (2.1) (0.04–11.8) 3772 (4.4) 1.3 (0.4–3.1)
Unknown 14 (5.8) (1.1–17.0) 1356 (1.6) 5.9 (2.4–13.3)

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Jul 5, 2021 | Posted by in GYNECOLOGY | Comments Off on Higher severe acute respiratory syndrome coronavirus 2 infection rate in pregnant patients

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