Mortality Among Minority Populations with Systemic Lupus Erythematosus, Including Asian and Hispanic/Latino Persons — California, 2007–2017

Systemic lupus erythematosus (SLE) is a multisystem autoimmune disease with manifestations that vary widely in severity. Although minority populations are at higher risk for SLE and have more severe outcomes (1), population-based estimates of mortality by race and ethnicity are often lacking, particularly for Asian and Hispanic/Latino persons. Among 812 patients in the California Lupus Surveillance Project (CLSP) during 2007–2009 (2,3), who were matched to the 2007–2017 National Death Index (NDI), 16.6% had died by 2017. This proportion included persons of White (14.4%), Black (25%), Asian (15.3%), and Hispanic/Latino (15.5%) race/ethnicity. Standardized mortality ratios (SMRs) of observed-to-expected deaths among persons with SLE within each racial/ethnic group were 2.3, 2.0, 3.8, and 3.9, respectively. These findings provide the first population-based estimates of mortality among Asian and Hispanic/Latino persons with SLE. Coordination of robust care models between primary care providers and rheumatologists could ensure that persons with SLE receive a timely diagnosis and appropriate treatments that might help address SLE-associated mortality.

CLSP included residents of San Francisco County, California, during January 1, 2007–December 31, 2009. Potential patients were identified using community rheumatology and nephrology clinics, community hospitals, and integrated health care systems (2,3). Clinical information was ascertained through review of medical records.* The State of California Institutional Review Board granted a waiver for this public health surveillance activity, and the project was reviewed and approved by the University of California, San Francisco, Institutional Review Board. This activity was also reviewed by CDC and conducted consistent with applicable federal law and CDC policy.^† Patients were not contacted for this linkage study.

Patients with SLE were defined using either the American College of Rheumatology (ACR) classification criteria (at least four of the 11 revised criteria as defined in 1982 and updated in 1997) (4,5) or two alternative definitions: SLE diagnosed by the patient’s treating rheumatologist plus three ACR criteria or lupus-related kidney disease (World Health Organization class II–VI lupus nephritis upon biopsy or documented record of SLE diagnosis and dialysis or renal transplantation). SLE patients in CLSP were submitted to the 2007–2017 NDI to search for potential matches (general sensitivity of 81.2%–97.9% and specificity of approximately 100%) (6). Matching required at least one of the following data items or combinations: first and last name and social security number, first and last name and month and year of birth, social security number, or full date of birth and sex. If none of these combinations was available, the case had insufficient information for submission to NDI and was excluded from analyses. Among the 909 patients with SLE in CLSP, 812 (89%) had sufficient information to be able to be linked with the 2007–2017 NDI. Patients were considered a match based on provided information including social security number.^§ Multivariable-adjusted risk ratios examining factors associated with mortality were estimated using a Poisson regression model adjusting for age group, sex, race, Hispanic/Latino ethnicity, and number of years since diagnosis. Population estimates by age group, sex, race, and Hispanic/Latino ethnicity for San Francisco County during 2007–2017 were obtained from CDC Wonder^¶ and were used to calculate SMRs using indirect age standardization in 11 age groups, as the ratio of observed deaths among persons with SLE to expected deaths in the San Francisco County population. Expected deaths were calculated by multiplying the overall age-specific death rate of the general population in San Francisco County by the total number of SLE patients in each age group; age-specific death rates of the general population by sex, race, and ethnicity were also calculated. Two-sided hypothesis tests were conducted controlling for the type I error rate at 5% (α = 0.05) and estimated 95% confidence intervals. Stata (version 16.0; StataCorp) was used to conduct all analyses.

Among the 812 SLE patients analyzed, 731 (90%) were female; race/ethnicities included White (38%), Black (20%), Asian (36%), and Hispanic/Latino (17%), and 5% of persons were of mixed/other race. A total of 135 (16.6%) deaths were identified. Mean age at diagnosis among all SLE patients was 34.9 years (range = 19.0–50.8 years), and mean age at death was 62.0 years (range = 46.2–77.8 years). Mortality increased with age. The highest percentage of deaths (25%) occurred among Black SLE patients; this group had a significantly increased risk for mortality after adjusting for age group, sex, ethnicity, and disease duration (Table 1). On average, Black persons died 6.8 years earlier than did White persons (p = 0.05); persons of Hispanic/Latino ethnicity died 9.5 years earlier than did persons who were not of Hispanic/Latino ethnicity (p = 0.02).

Overall, SMRs were three times higher among SLE patients than among those in the general population of San Francisco County (Table 2). Compared with SMRs among their non-SLE counterparts, SMRs among patients with SLE were four times higher in females and among persons of Asian and Hispanic/Latino race/ethnicity, three times higher among males, and two times higher among White and Black persons. Among females, SMRs were especially high among Asian (4.1) and Hispanic/Latina (5.8) patients.

Acknowledgment

Russell/Engleman Medical Research Center for Arthritis, University of California, San Francisco.

Corresponding author: Milena A. Gianfrancesco, Milena.Gianfrancesco@ucsf.edu

¹Division of Rheumatology, Department of Medicine, School of Medicine, University of California, San Francisco; ²Division of Population Health, National Center for Chronic Disease Prevention and Health Promotion, CDC.

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Abbreviations: CI = confidence interval; NA = not available.
* Population estimates by age group, sex, race, and ethnicity for San Francisco County during 2007–2017 were obtained from CDC Wonder (https://wonder.cdc.gov). Data are from the Multiple Cause of Death Files, 1999–2019 accessed March 21, 2020 (https://wonder.cdc.gov/mcd.html).
^† Risk ratios estimated using a multivariable Poisson model that modeled sex, age group, race (White, Black, Asian, other), ethnicity (non-Hispanic/Latino or Hispanic/Latino) simultaneously, adjusting for years since diagnosis. A total of 104 patients were excluded from the multivariable model: 19 (including two deaths) were missing race information, and 85 (including four deaths) were missing Hispanic/Latino ethnicity status.
^§ Hispanic/Latino ethnicity is considered a distinct concept from race; therefore, it was collected and reported separately from race.

Abbreviation: CI = confidence interval
* SMR is a ratio between the observed number of deaths in those with SLE and the number of deaths expected, based on age groups defined in CDC Wonder (https://wonder.cdc.gov). Sex, race and Hispanic/Latino ethnicity specific rates in San Francisco County were used, depending on the particular characteristic examined. CIs are calculated for each estimated SMR by assuming a Poisson distribution.
^† Age in 2008 was used for adjustment.
^§ Forty-one patients were excluded from race-specific analyses, including four who died: 22 had missing race information and 19 identified as a race other than White, Black or Asian, for which estimates are not available through CDC Wonder.
^¶ Eighty-five patient records missing Hispanic/Latino ethnicity status, including four deaths, were excluded from ethnicity-specific estimates.
** For female-specific race and ethnicity analyses, crude rates for age group <15 years were not provided by CDC Wonder or were unreliable and therefore not included in calculations; there was insufficient sample size to generate specific race/ethnic estimates for men.