Association of Sickle Cell Disease With Racial Disparities and Severe Maternal Morbidities in Black Individuals

Nansi S Boghossian; Lucy T Greenberg; George R Saade; Jeannette Rogowski; Ciaran S Phibbs; Molly Passarella; Jeffrey S Buzas; Scott A Lorch

doi:10.1001/jamapediatrics.2023.1580

. 2023 Jun 5;177(8):808–817. doi: 10.1001/jamapediatrics.2023.1580

Association of Sickle Cell Disease With Racial Disparities and Severe Maternal Morbidities in Black Individuals

Nansi S Boghossian ^1,^✉, Lucy T Greenberg ², George R Saade ³, Jeannette Rogowski ⁴, Ciaran S Phibbs ^5,⁶, Molly Passarella ⁷, Jeffrey S Buzas ⁸, Scott A Lorch ^7,⁹

¹Department of Epidemiology and Biostatistics, Arnold School of Public Health, University of South Carolina, Columbia

²Vermont Oxford Network, Burlington, Vermont

³Department of Obstetrics and Gynecology, Eastern Virginia Medical School, Norfolk

⁴Department of Health Policy and Administration, The Pennsylvania State University, State College

⁵Health Economics Resource Center and Center for Implementation to Innovation, Veterans Affairs Palo Alto Health Care System, Menlo Park, California

⁶Perinatal Epidemiology and Health Outcomes Research Unit, Division of Neonatology, Department of Pediatrics, Stanford University School of Medicine, Stanford, California

⁷Roberts Center for Pediatric Research, Children’s Hospital of Philadelphia, Philadelphia, Pennsylvania

⁸Department of Mathematics and Statistics, University of Vermont, Burlington

⁹Leonard Davis Institute of Health Economics, Wharton School, University of Pennsylvania, Philadelphia

Accepted for Publication: April 3, 2023.

Published Online: June 5, 2023. doi:10.1001/jamapediatrics.2023.1580

^✉

Corresponding Author: Nansi S. Boghossian, PhD, Department of Epidemiology and Biostatistics, University of South Carolina, 915 Greene St, Room 447, Columbia, SC 29208 (nboghoss@mailbox.sc.edu).

Author Contributions: Ms Greenberg 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: Boghossian, Saade, Rogowski, Phibbs, Lorch.

Acquisition, analysis, or interpretation of data: All authors.

Drafting of the manuscript: Boghossian, Buzas.

Critical revision of the manuscript for important intellectual content: Boghossian, Greenberg, Saade, Rogowski, Phibbs, Passarella, Lorch.

Statistical analysis: Greenberg, Phibbs, Passarella.

Obtained funding: Boghossian, Saade, Rogowski, Phibbs, Lorch.

Administrative, technical, or material support: Boghossian, Saade.

Supervision: Boghossian, Buzas.

Conflict of Interest Disclosures: None reported.

Funding/Support: This study was supported by grant R01MD016012 from the National Institute on Minority Health and Health Disparities.

Role of the Funder/Sponsor: The funder had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

Disclaimer: The contents of this article, including the data analysis, interpretation, and conclusions, are solely the responsibility of the authors and do not represent the official views of the Michigan Department of Health and Human Services or Missouri Department of Health and Senior Services. This information is from the records of the South Carolina Revenue and Fiscal Affairs office, Health and Demographics Section. The authors’ authorization to release this information does not imply endorsement of this study or its findings by either the Revenue and Fiscal Affairs Office or data oversight council. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. The views expressed in this article are those of the authors and do not necessarily reflect the position or policy of the Department of Veterans Affairs of the US government.

Data Sharing Statement: See Supplement 2.

^✉

Corresponding author.

PMCID: PMC10242511 PMID: 37273202

Key Points

Question

What is the association of sickle cell disease (SCD) with racial disparities in severe maternal morbidity (SMM) and with SMM among Black birthing individuals?

Findings

In this cohort study of 8 693 616 individuals from 5 states, SCD accounted for 8.9% and 14.3% of the Black-White disparity in SMM and nontransfusion SMM, respectively. Although SCD complicated 0.37% of the pregnancies among Black individuals, it contributed to 4.3% of SMM and to 6.9% of nontransfusion SMM cases.

Meaning

These findings suggest that SCD may be an important contributor to racial disparities in SMM and to SMM among Black patients; thus, new interventions for individuals with SCD are urgently needed.

This cohort study examines the association between sickle cell disease and severe maternal morbidity among Black individuals.

Abstract

Importance

Little is known about the association between sickle cell disease (SCD) and severe maternal morbidity (SMM).

Objective

To examine the association of SCD with racial disparities in SMM and with SMM among Black individuals.

Design, Setting, and Participants

This cohort study was a retrospective population-based investigation of individuals with and without SCD in 5 states (California [2008-2018], Michigan [2008-2020], Missouri [2008-2014], Pennsylvania [2008-2014], and South Carolina [2008-2020]) delivering a fetal death or live birth. Data were analyzed between July and December 2022.

Exposure

Sickle cell disease identified during the delivery admission by using International Classification of Diseases, Ninth Revision and Tenth Revision codes.

Main Outcomes and Measures

The primary outcomes were SMM including and excluding blood transfusions during the delivery hospitalization. Modified Poisson regression was used to estimate risk ratios (RRs) adjusted for birth year, state, insurance type, education, maternal age, Adequacy of Prenatal Care Utilization Index, and obstetric comorbidity index.

Results

From a sample of 8 693 616 patients (mean [SD] age, 28.5 [6.1] years), 956 951 were Black individuals (11.0%), of whom 3586 (0.37%) had SCD. Black individuals with SCD vs Black individuals without SCD were more likely to have Medicaid insurance (70.2% vs 64.6%), to have a cesarean delivery (44.6% vs 34.0%), and to reside in South Carolina (25.2% vs 21.5%). Sickle cell disease accounted for 8.9% and for 14.3% of the Black-White disparity in SMM and nontransfusion SMM, respectively. Among Black individuals, SCD complicated 0.37% of the pregnancies but contributed to 4.3% of the SMM cases and to 6.9% of the nontransfusion SMM cases. Among Black individuals with SCD compared with those without, the crude RRs of SMM and nontransfusion SMM during the delivery hospitalization were 11.9 (95% CI, 11.3-12.5) and 19.8 (95% CI, 18.5-21.2), respectively, while the adjusted RRs were 3.8 (95% CI, 3.3-4.5) and 6.5 (95% CI, 5.3-8.0), respectively. The SMM indicators that incurred the highest adjusted RRs included air and thrombotic embolism (4.8; 95% CI, 2.9-7.8), puerperal cerebrovascular disorders (4.7; 95% CI, 3.0-7.4), and blood transfusion (3.7; 95% CI, 3.2-4.3).

Conclusions and Relevance

In this retrospective cohort study, SCD was found to be an important contributor to racial disparities in SMM and was associated with an elevated risk of SMM among Black individuals. Efforts from the research community, policy makers, and funding agencies are needed to advance care among individuals with SCD.

Introduction

Severe maternal morbidity (SMM), defined as unintended consequences of labor and delivery resulting in short- or long-term adverse health outcomes, is a major public health crisis and has been increasing in the US.^1,2 Black individuals bear the disproportionate burden of SMM and are more than 1.5 times more likely to have an SMM than White individuals.³ Some of the increased SMM risk among Black individuals is attributed to a higher prevalence of clinical risk factors, such as preeclampsia, chronic hypertension, and preexisting diabetes.^4,5,6 However, previous studies examining racial disparities in SMM have overlooked a major risk factor for SMM, namely sickle cell disease (SCD), that is predominantly present among Black individuals.

Sickle cell disease is one of the most common genetic disorders, affecting more than 100 000 individuals in the US and 20 million people worldwide.⁷ Among African American births in the US, the mean frequency of SCD is 1 in 360 live births.⁸ Given advances in clinical care and the improved survival of individuals with SCD, an increasing number are reaching reproductive age⁹ and attempting pregnancy. Previous studies examining pregnancy outcomes among individuals with SCD have reported increased risks for maternal mortality, preeclampsia, stillbirth, preterm delivery, and small for gestational age.^10,11,12,13 However, very few studies have examined SMM risk among individuals with SCD.^14,15 Thus, we examined (1) the contribution of SCD to racial disparities in SMM and (2) the risk of mortality, SMM, and SMM indicators among Black individuals with SCD vs those without.

Methods

Study Sample

In this cohort study, we used birth and fetal death certificates showing a gestational age between 22 and 44 weeks linked to maternal hospital records from California (2008-2018), Michigan (2008-2020), Missouri (2008-2014), Pennsylvania (2008-2014), and South Carolina (2008-2020). These states were selected based on data availability. Delivery hospitalizations were examined for all 5 states. Inpatient hospitalizations during pregnancy and through 365 days post partum were only available for California, Michigan, and South Carolina. State health departments provided the deidentified linked data. The institutional review boards of the Children’s Hospital of Philadelphia, University of South Carolina, and health departments of the 5 states approved the study. The study was considered nonhuman participant research since the records were deidentified; thus, informed consent was not obtained. This study followed the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) reporting guideline.

Study Variables

The primary outcomes were SMM and nontransfusion SMM occurring during the delivery hospitalization. We defined SMM using the International Classification of Diseases, Ninth Revision (ICD-9) or Tenth Revision (ICD-10) diagnosis and procedure codes used by the Centers for Disease Control and Prevention, which include 16 life-threatening maternal conditions (eg, heart failure, sepsis, SCD crisis) and 5 life-saving procedures (eg, ventilation, blood transfusion).¹⁶ To help bridge the transition from ICD-9 to ICD-10, we used the Maternal and Child Health Bureau Federally Available Data Resource document.¹⁷ Nontransfusion SMM was also examined because blood transfusion, the most common SMM indicator, is not reflective of the condition’s severity without the number of transfused units. Secondary outcomes included in-hospital mortality during the delivery hospitalization; SMM, nontransfusion SMM, and nontransfusion SMM excluding SCD crisis during pregnancy and within 42 or 365 days post partum; readmission within 42 or 365 days post partum; and SMM indicators. Severe maternal morbidity beyond the delivery hospitalization and readmission were only available for California, Michigan, and South Carolina.

The main exposure was the presence or absence of SCD based on ICD-9 and ICD-10 codes (eTable 1 in Supplement 1). All individuals were female; data on self-identified gender were not available. Maternal race on the birth or fetal death certificate was based on self-identification and was categorized into Asian, Black, White, and other or multiracial. Race was examined given that SCD affects Black individuals at disproportionate rates compared with other races.⁸

Statistical Analysis

We first examined the distribution of SCD by race and the contribution of SCD to racial disparities in SMM. Given that the majority of SCD cases occur among Black individuals, subsequent analyses were restricted to Black individuals to examine the crude risk ratios (RRs) and adjusted RRs (ARRs) of the primary and secondary outcomes comparing individuals with and without SCD. We also examined the crude population attributable risk (PAR) and adjusted PAR (APAR) of SMM and nontransfusion SMM among individuals with SCD vs those without. We used modified Poisson regression to get the ARR¹⁸ and the Greenland and Drescher method and bootstrap CIs to get the APAR.¹⁹ Models were adjusted for birth year, state, insurance type (private, Medicaid, self-pay, other), education (no high school, some high school, high school diploma or General Educational Development test, some college, 4-year college degree, more than 4-year college degree), maternal age, Adequacy of Prenatal Care Utilization Index,²⁰ and obstetric comorbidity index score.²¹ The previously validated obstetric comorbidity index score includes 27 patient-level risk factors for SMM²¹ (eTable 2 in Supplement 1). In supplemental analyses (eMethods, eResults, eTable 5, and eTable 6 in Supplement 1), we examined the main study objectives by state. Statistical analyses were conducted between July and December 2022 using R, version 4.0.5 software (R Foundation for Statistical Computing).

Results

From the original study sample of 9 221 581 hospital discharge records, we excluded 527 965 records (eFigure 1 in Supplement 1), resulting in 8 693 616 individuals (61% from California, 16%, Michigan; 6%, Missouri; 10%, Pennsylvania; 7%, South Carolina), among whom 4336 had SCD. The sample included 956 951 Black individuals (11.0%), among whom 3586 (0.37%) had SCD (1068 [30%] from California; 1052 [29%], Michigan; 246 [7%], Missouri; 315 [9%], Pennsylvania; 905 [25%], South Carolina).

Among all individuals (mean [SD] age, 28.5 [6.1] years), 1.57% had SMM (Asian, 1.62%; Black, 2.52%; White, 1.40%; other or multiracial, 1.69%), while 0.70% had nontransfusion SMM (Asian, 0.72%; Black, 1.12%; White, 0.63%; other or multiracial, 0.73%) (Table 1). Among Black individuals, those with SCD SMM contributed to 4.28% (1033 of 24 128) of all SMM and to 6.93% (745 of 10 751) of nontransfusion SMM cases, while among White individuals, those with SCD contributed to only 0.06% (51 of 87 205) and 0.08% (33 of 39 040) of all SMM and nontransfusion SMM cases, respectively. Sickle cell disease accounted for 8.9% of the Black-White disparity in SMM (the SMM Black-White disparity decreased from 1.12 to 1.02 after removing the subset of individuals with SCD [SMM rate, 2.52% among Black individuals vs 1.40% among White individuals; excluding SCD cases decreased the SMM rate to 2.42% among Black vs 1.40% among White individuals]) and for 14.3% of the disparity in nontransfusion SMM (Table 1). Rates of disparity by state are presented in the eResults in Supplement 1.

Table 1. Overall Severe Maternal Morbidity (SMM) and Nontransfusion SMM During the Delivery Hospitalization by Race, Including and Excluding Patients With Sickle Cell Disease (SCD)^a .

Race	Overall					SCD, No.	Excluding SCD
Race	No.	SMM, No. (%)	SCD SMM, No. (% of all SMM cases)	Nontransfusion SMM, No. (%)	SCD nontransfusion SMM, No. (% of all nontransfusion SMM cases)	SCD, No.	No.	SMM, No. (%)	Nontransfusion SMM, No. (%)
All	8 693 616	136 084 (1.57)	1151 (0.85)	60 684 (0.70)	824 (1.36)	4336	8 689 280	134 933 (1.55)	59 860 (0.69)
Asian	869 539	14 072 (1.62)	11 (0.08)	6252 (0.72)	6 (0.10)	130	869 409	14 061 (1.62)	6246 (0.72)
Black	956 951	24 128 (2.52)	1033 (4.28)	10 751 (1.12)	745 (6.93)	3586	953 365	23 095 (2.42)	10 006 (1.05)
White	6 235 359	87 205 (1.40)	51 (0.06)	39 040 (0.63)	33 (0.08)	346	6 235 013	87 154 (1.40)	39 007 (0.63)
Other^b	631 767	10 679 (1.69)	56 (0.52)	4641 (0.73)	40 (0.86)	274	631 493	10 623 (1.68)	4601 (0.73)

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^{^a}

Data from California, Michigan, Missouri, Pennsylvania, and South Carolina.

^{^b}

Other includes birthing individuals of multiple races and individuals who did not identify as Asian, Black, or White.

Newborns to Black individuals with SCD compared with those without had a lower median gestational age at delivery (median [IQR], 38 [37-39] vs 39 [38-40] weeks, respectively) and were more likely to have Medicaid insurance (2516 [70.2%] vs 615 745 [64.6%]), to have a cesarean delivery (1600 [44.6%] vs 324 204 [34.0%]), to have a nonobese body mass index (2531 [74.6%] vs 579 795 [64.8%]), to reside in South Carolina (905 [25.2%] vs 205 342 [21.5%]) (Table 2), and to have comorbidities (eTable 3 in Supplement 1). A total of 619 individuals (17.3%) had inadequate prenatal care, of whom 501 (80.9%%) had Medicaid insurance, vs 1604 (67.9%) with adequate or adequate plus care.

Table 2. Maternal Characteristics Among Black Individuals With vs Without Sickle Cell Disease (SCD).

Characteristic^a	No. (%)
Characteristic^a	No SCD (n = 953 365)	SCD (n = 3586)
Maternal age, y
<20	119 046 (12.5)	379 (10.6)
20-24	299 867 (31.5)	1192 (33.2)
25-34	427 439 (44.8)	1642 (45.8)
≥35	107 013 (11.2)	373 (10.4)
Gestational age at delivery, median (IQR), wk	39 (38-40)	38 (37-39)
Smoker^b	83 426 (12.5)	271 (10.8)
Insurance
Private	303 946 (31.9)	983 (27.4)
Medicaid	615 745 (64.6)	2516 (70.2)
Self-pay	13 333 (1.4)	28 (0.8)
Other	10 614 (1.1)	34 (0.9)
Education
No high school	22 783 (2.4)	92 (2.6)
Some high school	7988 (0.8)	8 (0.2)
High school diploma/GED	160 784 (16.9)	600 (16.7)
At least some college	325 505 (34.1)	1219 (34.0)
4-y College	323 989 (34.0)	1259 (35.1)
>4-y College	73 875 (7.7)	283 (7.9)
Missing	38 441 (4.0)	125 (3.5)
Cesarean delivery	324 204 (34.0)	1600 (44.6)
Preeclampsia	68 573 (7.2)	535 (14.9)
Gestational hypertension	48 822 (5.1)	204 (5.7)
Gestational diabetes	52 098 (5.5)	146 (4.1)
Diabetes	15 269 (1.6)	65 (1.8)
SMM comorbidity index score with transfusion, median (IQR)^c	3 (0-9)	13 (9-20)
SMM comorbidity index nontransfusion score, median (IQR)^c	3 (0-12)	11 (6-23)
Multiple gestation	18 825 (2.0)	101 (2.8)
Adequacy of Prenatal Care Utilization Index
Inadequate	176 986 (18.6)	619 (17.3)
Intermediate	113 809 (11.9)	369 (10.3)
Adequate	298 012 (31.3)	956 (26.7)
Adequate plus	299 124 (31.4)	1407 (39.2)
Missing	65 434 (6.9)	235 (6.6)
Obese body mass index	315 228 (35.2)	862 (25.4)
State source of data
California	283 542 (29.7)	1068 (29.8)
Michigan	265 043 (27.8)	1052 (29.3)
Missouri	72 460 (7.6)	246 (6.9)
Pennsylvania	126 978 (13.3)	315 (8.8)
South Carolina	205 342 (21.5)	905 (25.2)

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Abbreviation: GED, General Educational Development test.

^{^a}

Missing data: gestational age, 1381 no SCD (0.1%) and 3 SCD (0.1%); smoking excluding California, 3051 no SCD (0.5%) and 16 SCD (0.6%); insurance, 9727 no SCD (1.0%) and 25 SCD (0.7%); multiple gestation, 2054 no SCD (0.2%) and 11 SCD (0.3%); and body mass index, 58 342 no SCD (6.1%) and 193 SCD (5.4%).

^{^b}

Smoking status missing in California.

^{^c}

Higher score indicates more morbidity.

There were 14 deaths per 10 000 among individuals with SCD and 1 death per 10 000 among individuals without SCD. The most common nontransfusion SMM indicators among individuals with SCD included respiratory distress syndrome and acute kidney failure (Figure). Table 3 shows the rates and RRs of maternal mortality, SMM, and SMM indicators during the delivery hospitalization among Black individuals with SCD vs those without from the 5 states. The rate of nontransfusion SMM among individuals with SCD was 2078 per 10 000, which dropped to 583 per 10 000 after excluding SCD crisis. The crude RR of mortality among individuals with SCD vs those without was 13.8 (95% CI, 5.6-34.0), while the ARR was 2.2 (95% CI, 0.6-7.9). The crude RR of SMM among individuals with SCD vs those without was 11.9 (95% CI, 11.3-12.5), while the ARR was 3.8 (95% CI, 3.3-4.5). The ARR of nontransfusion SMM among patients with SCD was 6.5 (95% CI, 5.3-8.0) but decreased to 1.6 (95% CI, 1.1-2.2) after excluding SCD crisis. For each SMM indicator, the crude RR was higher among individuals with SCD. After full adjustment, air and thrombotic embolism incurred the highest RR (ARR, 4.8; 95% CI, 2.9-7.8) followed by puerperal cerebrovascular disorders (ARR, 4.7; 95% CI, 3.0-7.4) and blood transfusion (ARR, 3.7; 95% CI, 3.2-4.3). Other SMM indicators with significantly elevated RRs included sepsis, adult respiratory distress syndrome, and eclampsia.

Figure. — Data included are from California, Michigan, Missouri, Pennsylvania, and South Carolina.

Table 3. Crude and Adjusted Relative Risks (RRs) of Mortality, Severe Maternal Morbidity (SMM), and SMM Indicators During the Delivery Hospitalization Among Black Individuals With vs Without Sickle Cell Disease (SCD)^a.

Outcome during delivery hospitalization	Cases per 10 000 deliveries		RR (95% CI)
Outcome during delivery hospitalization	No SCD (n = 953 365)	SCD (n = 3586)	Crude	Adjusted^b	Adjusted plus comorbidity index^c
In-hospital mortality	1	14	13.8 (5.6-34.0)	12.6 (5.2-30.7)	2.2 (0.6-7.9)
SMM	242	2881	11.9 (11.3-12.5)	11.6 (11.0-12.2)	3.8 (3.3-4.5)
Nontransfusion SMM	105	2078	19.8 (18.5-21.2)	19.3 (18.0-20.7)	6.5 (5.3-8.0)
Nontransfusion SMM excluding SCD crisis	105	583	5.6 (4.9-6.3)	5.4 (4.7-6.2)	1.6 (1.1-2.2)
SMM indicators
SCD crisis	0	1852	NA	NA	NA
Blood transfusion	161	1757	10.9 (10.1-11.7)	10.6 (9.9-11.4)	3.7 (3.2-4.3)
Adult respiratory distress syndrome	14	212	14.7 (11.7-18.4)	13.6 (10.8-17.2)	2.6 (1.6-4.2)
Acute kidney failure	19	125	6.6 (4.9-8.8)	6.1 (4.6-8.2)	0.9 (0.5-1.7)
Sepsis	11	114	10.6 (7.8-14.5)	9.8 (7.2-13.4)	2.9 (2.0-4.3)
Puerperal cerebrovascular disorders	5	92	17.9 (12.6-25.4)	17.4 (12.3-24.8)	4.7 (3.0-7.4)
Disseminated intravascular coagulation	31	89	2.9 (2.0-4.1)	2.9 (2.0-4.1)	0.8 (0.5-1.3)
Ventilation	10	86	8.8 (6.2-12.6)	8.4 (5.9-12.0)	1.4 (0.8-2.8)
Pulmonary edema/acute heart failure	12	64	5.2 (3.5-7.9)	5.0 (3.3-7.6)	0.8 (0.4-1.5)
Air and thrombotic embolism	4	61	16.7 (10.9-25.7)	16.3 (10.6-25.0)	4.8 (2.9-7.8)
Eclampsia	14	59	4.1 (2.7-6.3)	4.1 (2.6-6.3)	1.8 (1.1-2.8)
Hysterectomy	12	42	3.4 (2.0-5.6)	3.3 (2.0-5.5)	0.7 (0.3-1.3)
Shock	5	14	2.7 (1.1-6.6)	2.5 (1.1-6.1)	0.6 (0.2-1.7)
Severe anesthesia complications	2	8	4.5 (1.4-14.1)	4.7 (1.5-14.7)	1.6 (0.5-5.4)
Cardiac arrest/ventricular fibrillation	1	8	5.6 (1.8-17.6)	5.2 (1.6-16.2)	0.6 (0.1-2.8)
Conversion of cardiac rhythm	2	6	3.6 (0.9-14.4)	3.3 (0.8-13.2)	0.4 (0.1-2.4)
Acute myocardial infarction	1	3	4.0 (0.6-28.6)	3.8 (0.5-27.8)	0.5 (0.0-5.2)
Temporary tracheostomy	0	3	9.2 (1.2-67.3)	8.8 (1.2-63.2)	1.1 (0.1-12.2)
Amniotic fluid embolism	1	0	NA	NA	NA
Heart failure/arrest during surgery or procedure	1	0	NA	NA	NA
Aneurysm	0	0	NA	NA	NA

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Abbreviation: NA, not available (cannot be calculated).

^{^a}

Data from California, Michigan, Missouri, Pennsylvania, and South Carolina.

^{^b}

Adjusted for birth year, state, insurance type, education, maternal age, and adequacy of prenatal care.

^{^c}

Adjusted for birth year, state, insurance type, education, maternal age, adequacy of prenatal care, and obstetric comorbidity index.

Black individuals with SCD had multiple SMM indicators during the delivery hospitalization, with more than 11% having at least 2 SMM indicators compared with only 0.4% among individuals without SCD. An examination of nontransfusion SMM showed that more than 4% of individuals with SCD had at least 2 SMM indicators compared with only 0.2% among individuals without SCD (eTable 4 and eFigure 2 in Supplement 1).

The crude PARs (cases per 10 000) due to SCD for SMM and nontransfusion SMM during the delivery hospitalization were 9.9 (95% CI, 9.3-10.5) and 7.4 (95% CI, 6.8-7.9), respectively. The APARs were 8.1 (95% CI, 7.5-8.7) and 6.6 (95% CI, 6.1-7.2), respectively.

Table 4 shows the RRs of SMM during pregnancy, delivery, and post partum; for SMM indicators during post partum; and for postpartum readmissions among Black individuals with vs without SCD from California, Michigan, and South Carolina. The ARR was more than 4-fold higher for SMM (4.7; 95% CI, 4.3-5.2) and more than 8-fold higher for nontransfusion SMM (8.5; 95% CI, 7.6-9.5) at any time during pregnancy, delivery, or at any time during pregnancy, delivery or within 365 days post partum. The ARR decreased to 2.8 (95% CI, 2.3-3.3) when restricting to nontransfusion SMM excluding SCD crisis. The ARR postdischarge within 365 days post partum was 12.3 (95% CI, 11.4-13.3) for overall SMM, 13.8 (95% CI, 12.8-14.9) for nontransfusion SMM, and 3.9 (95% CI, 3.3-4.5) for nontransfusion SMM excluding SCD crisis. During the postpartum period, all SMM indicators were higher among individuals with SCD. The SMM indicators with the greatest ARR included blood transfusion (22.1; 95% CI, 19.4-25.2), sepsis ( 7.0; 95% CI, 5.7-8.6), air and thrombotic embolism (5.2; 95% CI; 3.6-7.4), and disseminated intravascular coagulation (5.0; 95% CI, 2.9-8.6). Readmission within 42 days and 365 days post partum was elevated among individuals with SCD (ARR, 2.8 [95% CI, 2.5-3.1] and 3.3 [95% CI, 3.1-3.5], respectively).

Table 4. Crude and Adjusted Relative Risks (RRs) of Severe Maternal Morbidity (SMM), SMM Indicators, and Readmission After Discharge Among Black Individuals With vs Without Sickle Cell Disease (SCD)^a.

	Cases per 10 000 deliveries		RR (95% CI)
	No SCD (n = 753 927)	SCD (n = 3025)	Crude	Adjusted^b	Adjusted plus comorbidity index^c
SMM
During delivery hospitalization	253	2856	11.3 (10.7-12.0)	11.1 (10.5-11.8)	3.7 (3.2-4.4)
At any time during pregnancy, delivery, or within 42 d post partum	340	4159	12.2 (11.7-12.8)	12.0 (11.4-12.5)	4.7 (4.2-5.3)
At any time during pregnancy, delivery, or within 365 d post partum	391	4512	11.5 (11.1-12.0)	11.3 (10.8-11.7)	4.7 (4.3-5.2)
Postdischarge within 42 d post partum	61	902	14.9 (13.3-16.8)	14.3 (12.8-16.1)	8.3 (7.3-9.5)
Postdischarge within 365 d post partum	120	2645	22.1 (20.7-23.5)	21.1 (19.8-22.5)	12.3 (11.4-13.3)
Nontransfusion SMM
During delivery hospitalization	108	2030	18.9 (17.5-20.3)	18.4 (17.1-19.9)	6.1 (4.9-7.7)
At any time during pregnancy, delivery, or within 42 d post partum	184	3669	19.9 (18.9-20.9)	19.2 (18.3-20.2)	8.8 (7.7-9.9)
At any time during pregnancy, delivery, or within 365 d post partum	228	4126	18.1 (17.3-18.9)	17.4 (16.6-18.2)	8.5 (7.6-9.5)
Postdischarge within 42 d post partum	54	856	15.9 (14.1-18.0)	15.2 (13.5-17.2)	8.8 (7.7-10.1)
Postdischarge within 365 d post partum	103	2592	25.2 (23.6-26.8)	23.9 (22.3-25.5)	13.8 (12.8-14.9)
Nontransfusion SMM excluding SCD crisis
During delivery hospitalization	108	605	5.6 (4.9-6.5)	5.5 (4.8-6.3)	1.6 (1.1-2.3)
At any time during pregnancy, delivery, or within 42 d post partum	184	1101	6.0 (5.4-6.6)	5.8 (5.2-6.4)	2.4 (1.9-2.9)
At any time during pregnancy, delivery, or within 365 d post partum	228	1458	6.4 (5.9-7.0)	6.1 (5.6-6.7)	2.8 (2.3-3.3)
Postdischarge within 42 d post partum	54	228	4.2 (3.4-5.4)	4.1 (3.2-5.1)	2.5 (2.0-3.3)
Postdischarge within 365 d post partum	103	701	6.8 (6.0-7.8)	6.4 (5.6-7.4)	3.9 (3.3-4.5)
SMM indicators within 365 d post partum
SCD crisis	0	2436	NA	NA	NA
Blood transfusion	27	1061	39.9 (35.6-44.6)	39.3 (35.2-44.0)	22.1 (19.4-25.2)
Adult respiratory distress syndrome	16	142	8.7 (6.5-11.8)	8.0 (5.9-10.9)	3.8 (2.8-5.2)
Acute kidney failure	18	145	8.3 (6.2-11.2)	7.6 (5.6-10.2)	2.8 (2.0-3.9)
Sepsis	28	360	13.0 (10.7-15.7)	12.2 (10.1-14.8)	7.0 (5.7-8.6)
Puerperal cerebrovascular disorders	9	53	5.7 (3.5-9.4)	5.6 (3.4-9.1)	3.2 (2.0-5.4)
Disseminated intravascular coagulation	5	50	10.7 (6.4-17.9)	10.1 (6.0-16.9)	5.0 (2.9-8.6)
Ventilation	8	30	3.9 (2.0-7.5)	3.7 (1.9-7.1)	1.6 (0.8-3.2)
Pulmonary edema/acute heart failure	27	83	3.0 (2.0-4.5)	2.9 (2.0-4.3)	1.3 (0.9-1.9)
Air and thrombotic embolism	11	109	9.9 (7.0-14.0)	9.3 (6.6-13.2)	5.2 (3.6-7.4)
Eclampsia	8	20	2.4 (1.1-5.3)	2.3 (1.0-5.1)	1.6 (0.7-3.7)
Hysterectomy	5	10	2.0 (0.6-6.1)	2.0 (0.6-6.2)	1.3 (0.4-4.1)
Shock	3	0	NA	NA	NA
Severe anesthesia complications	0	0	NA	NA	NA
Cardiac arrest/ventricular fibrillation	2	17	7.9 (3.3-19.3)	7.4 (3.0-18.0)	3.7 (1.4-9.6)
Conversion of cardiac rhythm	2	10	6.2 (2.0-19.4)	6.1 (1.9-19.4)	2.9 (0.9-10.0)
Acute myocardial infarction	3	10	3.9 (1.2-12.1)	3.6 (1.1-11.2)	1.9 (0.6-6.0)
Temporary tracheostomy	1	0	NA	NA	NA
Amniotic fluid embolism	0	0	NA	NA	NA
Heart failure/cardiac arrest during surgery or procedure	0	0	NA	NA	NA
Aneurysm	0	0	NA	NA	NA
Readmission within 42 d post partum	194	869	4.5 (4.0-5.0)	4.3 (3.9-4.9)	2.8 (2.5-3.1)
Readmission within 365 d post partum	536	2509	4.7 (4.4-5.0)	4.5 (4.3-4.8)	3.3 (3.1-3.5)

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Abbreviation: NA, not available (cannot be calculated).

^{^a}

Data from California, Michigan, and South Carolina.

^{^b}

Adjusted for birth year, state, insurance type, education, maternal age, and adequacy of prenatal care.

^{^c}

Adjusted for birth year, state, insurance type, education, maternal age, adequacy of prenatal care, and obstetric comorbidity index.

Discussion

In this cohort study of more than 8.5 million deliveries in 5 states, we found that SCD accounted for 8.9% and 14.3% of the Black-White disparity in SMM and nontransfusion SMM, respectively. Sickle cell disease also complicated 0.37% of the pregnancies among Black individuals but contributed to 4.3% of SMM and 6.9% of nontransfusion SMM cases during the delivery hospitalization. Sickle cell disease was associated with an almost 4-fold increased ARR of SMM and an 8.1 per 10 000 APAR. Importantly, 11% of Black individuals with SCD experienced more than 1 SMM, and there were 14 deaths per 10 000 deliveries.

Previous studies examining pregnancy outcomes among individuals with SCD have reported increased adverse outcomes for both the mother and newborn. In 2 meta-analyses, pregnant individuals with SCD compared with those without SCD had increased risks or odds for stillbirth, perinatal death, small-for-gestational-age newborns, and preterm delivery.^12,13 A meta-analysis examining maternal outcomes among individuals residing in high-income countries reported that individuals with SCD compared with those without had increased odds for preeclampsia (pooled odds ratio [OR], 1.86; 95% CI, 1.22-2.82), eclampsia (OR, 2.07; 95% CI, 1.43-2.99), cesarean delivery (OR, 1.62; 95% CI, 1.26-2.08), and bacterial infection (OR, 3.03; 95% CI, 1.86-4.92).²² Another study reported increased odds for sepsis (OR, 6.8; 95% CI, 4.4-10.5).¹³ Studies conducted in the US examining maternal mortality reported rates to be 0.07%,¹³ 0.10%,¹¹ 0.13%,¹⁴ and 0.16%.¹⁰ Our rate of 0.14% falls within the range of these studies. However, these rates are underestimated as they only capture in-hospital mortality during the delivery hospitalization. A study examining maternal deaths among patients with SCD in France showed that of 14 maternal deaths with known death timing, 2 occurred ante partum, 6 occurred within 24 hours, and 6 occurred within 23 days post partum mainly due to SCD-related complications.²³

Since we initiated our analyses, 2 studies were published examining the association between SCD and SMM.^14,15 One was conducted using the National Inpatient Sample (2012-2018) and reported that during the delivery hospitalization, the SMM rate excluding transfusion and SCD crisis was 5.7% among individuals with SCD and 0.7% among control patients of other than Black race, resulting in an OR of 7.2 (95% CI, 6.3-8.3) after adjusting for hospital and patient sociodemographic characteristics.¹⁴ The other study was conducted at a single center in Atlanta, Georgia (2011-2020), and reported that during the delivery hospitalization, the SMM rate excluding crisis was 65.9% among individuals with SCD and 11.7% among individuals without SCD for an RR of 5.4 (95% CI, 4.6-6.3) after adjusting for age, parity, insurance, chronic hypertension, diabetes, obesity, and multiple gestation.¹⁵ In our study, SCD crisis was the only nontransfusion SMM in 15% of patients with SCD. However, these SMM rates are underreported. When we examined SMM at any time during pregnancy and up to 42 days post partum among Black individuals with SCD in California, Michigan, and South Carolina, our SMM rate excluding crisis increased by 48% among patients with SCD, while it increased by 34% among patients without SCD. Previous studies using population-based data from California and Massachusetts reported that adding antenatal and postpartum hospitalizations through 42 days post partum increased the total SMM rate by 22%.^24,25 Even beyond 42 days post partum, a study reported that by 90 days post partum, patients with SCD compared with those without SCD were 92% (adjusted OR, 1.92; 95% CI, 1.75-2.11) more likely to be readmitted to the hospital.¹¹ We similarly found that the readmission risk among patients with SCD compared with those without SCD continues through 365 days post partum (ARR, 3.3; 95% CI, 3.1-3.5).

That SCD contributed to 4.3% of SMM and 6.9% of nontransfusion SMM among Black individuals and to only 0.1% among White individuals for both SMM and nontransfusion SMM is noteworthy. Previous studies have examined clinical factors such as preeclampsia, diabetes, hypertension,^4,5,6 quality of obstetric care,^26,27 racism,^28,29 and sociodemographic factors³⁰ as contributors to racial disparities in SMM. However, no studies have examined the contribution of SCD, a disease that occurs predominantly among Black individuals, to racial disparities in SMM. We believe that all these factors, particularly the clinical factors, contribute to SMM among individuals with SCD. Indeed, adjusting for the obstetric comorbidity score, which comprises 27 patient-level risk factors for SMM,²¹ attenuates by more than 50% the RR of SMM among Black individuals with SCD compared with those without. Other studies have reported that individuals with SCD have comorbidities that increase their SMM risk,³¹ such as pulmonary hypertension,¹³ the second most severe risk factor in the obstetric comorbidity score associated with increased SMM risk,³¹ placental abruption,¹³ preeclampsia,^13,22 and anemia.¹³ However, it is surprising that SCD—the only risk factor for SCD crisis and 1 of the SMM indicators—is not included in the obstetric comorbidity score. With an ARR of overall SMM of 3.8-fold and of nontransfusion SMM of 6.5-fold among Black individuals, SCD as a risk factor ranks as important as preexisting anemia (ARR, 3.59; 95% CI, 3.46-3.73) for overall SMM³¹ and as important as severe preeclampsia (ARR, 5.74; 95% CI, 5.38-6.13) for nontransfusion SMM³¹ in the obstetric comorbidity score. Future studies should incorporate SCD as a risk factor in the obstetric comorbidity index to improve comparisons of SMM rates across patient populations and hospitals that differ in comorbidity case mix.

Regardless of whether SCD is associated with SMM directly or indirectly through an association with pregnancy complications, it is a condition that is hereditary and present long before pregnancy. Preconception care and management by a multidisciplinary team of obstetricians, hematologists, anesthesiologists, and other health care professionals are critical for improved pregnancy outcomes among patients with SCD.^23,32 Preconception visits should include screening for chronic disease complications, partner testing and genetic counseling, updating immunizations, advising on smoking cessation, and optimizing levels of hemoglobin and hematocrit.^33,34 Unfortunately, preconception care is complicated by high rates of unintended pregnancy, low knowledge of contraceptive efficacy, and low rates of contraception use among individuals with SCD.^34,35 Even during pregnancy, prenatal care among individuals with SCD has been reported to be less than adequate (based on the Adequacy of Prenatal Care Utilization Index) among 22% of individuals in 1 study³⁶ and to be limited (<5 prenatal visits) among 7.4% of individuals in another study.³⁷ We found that 17.3% of patients with SCD had inadequate prenatal care, which potentially reflects socioeconomic status. Indeed, 80.9% of individuals with inadequate care in our study had Medicaid insurance compared with 67.9% with adequate or adequate plus care. A previous study showed that Medicaid insurance is associated with reduced access to high-quality care and increased emergency department use among youth with SCD.³⁸

Despite major improvements in SCD-related childhood mortality and morbidity given the advances in the medical care of patients with SCD, including universal newborn screening, penicillin prophylaxis, vaccinations, and hydroxyurea use,⁹ there are no recommended treatments for patients with SCD during pregnancy. Hydroxyurea is contraindicated during pregnancy because animal studies have suggested possible teratogenic effects on the fetus.³⁹ Management of painful SCD crises during pregnancy can be complex, as depicted in a 2009 Cochrane systematic review that found no randomized trials assessing the effectiveness and safety of different regimens for the treatment of painful SCD crises during pregnancy.⁴⁰ The paucity of evidence is also reflected in another Cochrane systematic review published in 2016 assessing the benefits and harms of prophylactic vs selective blood transfusion in pregnant individuals with SCD.⁴¹ The review only found 1 small, very-low-quality trial that showed that prophylactic compared with selective blood transfusion in pregnant individuals with SCD has no clear benefits on perinatal outcomes.⁴¹ The lack of evidence on improving outcomes of patients with SCD may be attributable to inadequate funding, a byproduct of structural racism,⁴² and subsequent decreased research productivity and drug development.⁴³

Strengths and Limitations

Our study has several strengths, including population-based data from 5 states and 1-year postpartum follow-up for 3 states. Limitations include a lack of data on SCD severity, such as the number of crises. We did not have information on pain management protocols and transfusion practices and whether SMM was present upon admission or occurred during labor and delivery. We did not examine whether there were differences in outcomes by genotype. A meta-analysis has shown that individuals with the hemoglobin SS genotype have worse perinatal outcomes than those with the hemoglobin SC genotype.¹² The contribution of SCD to racial disparities in SMM and to SMM among Black individuals may vary based on the SCD incidence in the examined state,⁸ health care access, and genetic admixture in the Black population.⁴⁴ However, despite these limitations, we contribute new literature on this topic and highlight the urgency of new research to improve maternal outcomes of individuals with SCD.

Conclusions

The findings of this cohort study indicate that pregnant individuals with SCD may be at high risk of mortality and morbidity. To reduce racial disparities, it is imperative to develop new interventions for SCD that consider pregnancy outcomes and whether the patient is pregnant or may become pregnant. The research community, policy makers, and funding agencies are all needed to advance care among individuals with SCD.

Supplement 1.

eTable 1. Classification of Sickle Cell Disease Based on International Classification of Diseases, Ninth Revision (ICD-9) and Tenth Revision (ICD-10) Codes

eTable 2. Risk Scores for Comorbidities in Relation to Severe Maternal Morbidity (SMM) and Nontransfusion SMM

eFigure 1. Study Cohort Exclusions

eTable 3. Comorbidities Included in the Obstetric Comorbidity Index Among Black Individuals With and Without Sickle Cell Disease (SCD)

eTable 4. Number of Severe Maternal Morbidity (SMM) Indicators During the Delivery Hospitalization Among Black Individuals With and Without Sickle Cell Disease (SCD)

eFigure 2. Number of Severe Maternal Morbidity (SMM) Indicators During the Delivery Hospitalization Among Black Individuals With and Without Sickle Cell Disease (SCD)

eMethods.

eResults.

eTable 5. Overall Severe Maternal Morbidity (SMM) and Nontransfusion SMM During the Delivery Hospitalization by State and Race Including and Excluding Individuals With Sickle Cell Disease (SCD)

eTable 6. Crude and Adjusted Relative Risk (RR) of Severe Maternal Morbidity (SMM) During the Delivery Hospitalization by State Among Black Individuals With vs Without Sickle Cell Disease (SCD)

Click here for additional data file.^{(257KB, pdf)}

Supplement 2.

Data Sharing Statement

Click here for additional data file.^{(14.8KB, pdf)}

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplement 1.

eTable 1. Classification of Sickle Cell Disease Based on International Classification of Diseases, Ninth Revision (ICD-9) and Tenth Revision (ICD-10) Codes

eTable 2. Risk Scores for Comorbidities in Relation to Severe Maternal Morbidity (SMM) and Nontransfusion SMM

eFigure 1. Study Cohort Exclusions

eTable 3. Comorbidities Included in the Obstetric Comorbidity Index Among Black Individuals With and Without Sickle Cell Disease (SCD)

eTable 4. Number of Severe Maternal Morbidity (SMM) Indicators During the Delivery Hospitalization Among Black Individuals With and Without Sickle Cell Disease (SCD)

eFigure 2. Number of Severe Maternal Morbidity (SMM) Indicators During the Delivery Hospitalization Among Black Individuals With and Without Sickle Cell Disease (SCD)

eMethods.

eResults.

eTable 5. Overall Severe Maternal Morbidity (SMM) and Nontransfusion SMM During the Delivery Hospitalization by State and Race Including and Excluding Individuals With Sickle Cell Disease (SCD)

eTable 6. Crude and Adjusted Relative Risk (RR) of Severe Maternal Morbidity (SMM) During the Delivery Hospitalization by State Among Black Individuals With vs Without Sickle Cell Disease (SCD)

Click here for additional data file.^{(257KB, pdf)}

Supplement 2.

Data Sharing Statement

Click here for additional data file.^{(14.8KB, pdf)}

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PERMALINK

Association of Sickle Cell Disease With Racial Disparities and Severe Maternal Morbidities in Black Individuals

Nansi S Boghossian, PhD

Lucy T Greenberg, MS

George R Saade, MD

Jeannette Rogowski, PhD

Ciaran S Phibbs, PhD

Molly Passarella, MS

Jeffrey S Buzas, PhD

Scott A Lorch, MD

Key Points

Question

Findings

Meaning

Abstract

Importance

Objective

Design, Setting, and Participants

Exposure

Main Outcomes and Measures

Results

Conclusions and Relevance

Introduction

Methods

Study Sample

Study Variables

Statistical Analysis

Results

Table 1. Overall Severe Maternal Morbidity (SMM) and Nontransfusion SMM During the Delivery Hospitalization by Race, Including and Excluding Patients With Sickle Cell Disease (SCD)a .

Table 2. Maternal Characteristics Among Black Individuals With vs Without Sickle Cell Disease (SCD).

Figure. Severe Maternal Morbidity Indicators During the Delivery Hospitalization Among Black Individuals With vs Without Sickle Cell Disease (SCD).

Table 3. Crude and Adjusted Relative Risks (RRs) of Mortality, Severe Maternal Morbidity (SMM), and SMM Indicators During the Delivery Hospitalization Among Black Individuals With vs Without Sickle Cell Disease (SCD)a.

Table 4. Crude and Adjusted Relative Risks (RRs) of Severe Maternal Morbidity (SMM), SMM Indicators, and Readmission After Discharge Among Black Individuals With vs Without Sickle Cell Disease (SCD)a.

Discussion

Strengths and Limitations

Conclusions

References

Associated Data

Supplementary Materials

ACTIONS

PERMALINK

RESOURCES

Similar articles

Cited by other articles

Links to NCBI Databases

Table 1. Overall Severe Maternal Morbidity (SMM) and Nontransfusion SMM During the Delivery Hospitalization by Race, Including and Excluding Patients With Sickle Cell Disease (SCD)^a .

Table 3. Crude and Adjusted Relative Risks (RRs) of Mortality, Severe Maternal Morbidity (SMM), and SMM Indicators During the Delivery Hospitalization Among Black Individuals With vs Without Sickle Cell Disease (SCD)^a.

Table 4. Crude and Adjusted Relative Risks (RRs) of Severe Maternal Morbidity (SMM), SMM Indicators, and Readmission After Discharge Among Black Individuals With vs Without Sickle Cell Disease (SCD)^a.