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Racial/Ethnic and Income Disparities in the Prevalence of Comorbidities that Are Associated With Risk for Severe COVID-19 Among Adults Receiving HIV Care, United States, 2014–2019

Supplemental Digital Content is Available in the Text.


BACKGROUND
Contrary to the early prediction that COVID-19 would be "the great equalizer," 1 the disease burden in the United States falls disproportionately on non-Hispanic Blacks or African Americans (Blacks), Hispanics or Latinos of any race (Hispanics), people with low income, and those with certain chronic illnesses.
Relative to their proportion of the US population, Blacks and Hispanics have higher COVID-19 attack rates and hospitalization rates, and Blacks have higher death rates than non-Hispanic Whites (Whites). [2][3][4][5][6][7][8][9] Blacks constitute 13% of the US population but accounted for 16% of COVID-19 cases and 20% of COVID-19 deaths, as of November 15, 2020. 9 Hispanics, at 18% of the population, accounted for 26% of cases and 16% of deaths nationwide. Among those with diagnosed COVID-19, Blacks and people with low income are more likely to have severe illness and die. [10][11][12][13] Among people with HIV, those who are Black or Hispanic, or have low income, are also disproportionately affected by 15 In addition to these sociodemographic risk factors, several chronic health conditions increase the risk of COVID-19 requiring hospitalization, eg, obesity, chronic kidney disease (CKD), type 2 diabetes, chronic obstructive pulmonary disease (COPD), immunocompromised state from solid organ transplantation, heart disease, and sickle cell disease. 13,16 Hospitalizations are 6 times higher and deaths 12 times higher for people with underlying illnesses. 7 Although the Centers for Disease Control and Prevention (CDC) lists an immunocompromised state due to HIV as a condition that might increase the risk for severe illness from COVID-19, 16 the available literature in North America and Europe suggests that HIV, in itself, does not increase the risk of SARS-CoV-2 infection or severe illness. [17][18][19][20][21][22] However, several studies have found that most people with diagnosed HIV and COVID-19 have other comorbidities, 14,15,17,20,23 suggesting these conditions, rather than HIV, may be the driver of severe illness in this population.
With HIV, as with COVID-19, Blacks, Hispanics, and people with low income bear a disproportionate burden of disease in the United States. 24 Compared with Whites, the prevalence of HIV in 2018 was 7.2 times higher among Blacks and 3.0 times higher among Hispanics. 25 Among those with recent HIV infection, 42% were Black and 28% Hispanic. Blacks and Hispanics have poorer outcomes than Whites at all stages of the HIV care continuum, including linkage to HIV care, retention in care, and viral suppression. 26 HIV is also a disease of poverty. Among adults with diagnosed HIV, 43% had a household income below the poverty threshold and one in 5 went without food during the past year because of lack of money. 27 The burden of poor health outcomes from HIV in heavily affected communities may be compounded by similar patterns in the distribution of COVID-19 and by disparities in the prevalence of comorbidities associated with an increased risk for severe illness from COVID-19 among people with HIV. 28 To examine the prevalence of these comorbidities among people with HIV, we analyzed HIV surveillance data on adults receiving HIV care to determine the percentage with $1 diagnosed comorbidity and assessed differences by race/ ethnicity, income level, and health insurance type.

Design and Data Collection
The Medical Monitoring Project (MMP) is an annual cross-sectional survey designed to produce nationally representative estimates of the behavioral and clinical characteristics of adults with diagnosed HIV in the United States. This analysis presents estimates of adults receiving HIV care drawn from this sample. MMP data collection constitutes routine public health surveillance and was thus determined by the CDC to be nonresearch. This activity was conducted consistent with the applicable federal law and CDC policy. 29 When required, participating states or territories obtained local institutional review board approval to collect data. All participants provided informed consent. MMP uses 2-stage sampling in which, during the first stage, 16 states and one territory, including 6 separately funded metropolitan areas within selected states, were sampled from all states, the District of Columbia, and Puerto Rico. During the second stage, simple random samples of people with diagnosed HIV aged $18 years were drawn annually for each participating area from the National HIV Surveillance System, a census of people with diagnosed HIV in the United States. People sampled during the 2016-2018 data collection cycles were recruited for a phone or face-to-face interview and medical record abstraction at their usual place of HIV medical care. Data were collected beginning in June of each cycle until the following May. Medical record data included selected laboratory test results and all diagnoses recorded in the problem list or assessment section of medical encounters during a 2-year, retrospective observation period ending on the interview date. For the 2016-2018 data collection cycles, this period spanned June 2014-May 2019.
All sampled areas and separately funded jurisdictions within states participated in the MMP, including California (including Los Angeles County and San Francisco), Delaware, Florida, Georgia, Illinois (including Chicago), Indiana, MI, Mississippi, New Jersey, New York (including New York City), North Carolina, Oregon, Pennsylvania (including Philadelphia), Puerto Rico, Texas (including Houston), Virginia, and Washington. Annual response rates for adults with diagnosed HIV were 44%-45%. During the 2016-2018 data collection cycles, 12,310 sampled people were interviewed ( Fig. 1). Of these, 12,189 reported receiving HIV medical care or had medical record documentation of at least one element of HIV care (eg, an HIV laboratory result or antiretroviral prescription) during the past 24 months. We excluded 627 participants without a medical record abstraction containing at least one diagnosed condition. The analytic data set included 11,562 participants who received HIV medical care in the past 24 months and had diagnosis data abstracted (referred to as "adults receiving HIV care").

Measures
Sociodemographic variables included age, race/ethnicity (non-Hispanic American Indian/Alaska Native, Asian, Black, Native Hawaiian/other Pacific Islander, White, or multiracial, and Hispanic of any race), household income above or below the federal poverty threshold during the past 12 months, and health insurance or coverage type during the past 12 months [any private insurance, public insurance alone, Ryan White HIV/ AIDS Program (RWHAP) assistance alone, unspecified, and no insurance/coverage]. We ascertained whether facilities identified by participants as their usual place of HIV care received any funding from the RWHAP. 30 Clinical variables included diagnosed comorbidities identified by the CDC on July 15, 2020, as associated with an increased risk of severe illness from COVID-19, defined as requiring hospitalization (obesity, CKD, diabetes, COPD, immunocompromised from solid organ transplantation, heart disease, and sickle cell disease) 16 as well as diagnosed AIDS-defining illnesses. 31 We ascertained obesity from recorded diagnoses of obesity, without consideration of body mass index. Because medical records often do not differentiate type 1 and type 2 diabetes, 32 we measured diagnosed diabetes, irrespective of type. Diagnosed heart disease included atherosclerotic heart disease, congestive heart failure, cardiomyopathy, pulmonary hypertension or cor pulmonale, and arrhythmia. Other clinical variables included CD4 + T-lymphocyte cell count (CD4 count) and HIV RNA level.

Outcomes
The primary outcome was having $1 diagnosed comorbidity associated with an increased risk for severe illness from COVID-19 recorded in the medical record during the 24 months before being interviewed. Because the risk increases with age 33 and possibly with immunocompromised state secondary to HIV, secondary outcomes included having $1 diagnosed comorbidity along with combinations of older age ($50 or $65 years) and poorly controlled HIV, defined as lowest CD4 count ,200 cells/ mL, any HIV RNA $200 copies/mL, or diagnosis of an AIDSdefining illness during the past 24 months.

Statistical Analysis
Data were weighted based on known probabilities of selection at the state or territory and person levels, adjusted for nonresponse, and poststratified to known population totals by age, race/ethnicity, and sex from the National HIV Surveillance System. This design allows inference to all adults with diagnosed HIV in the United States. 27 We estimated the prevalence, with 95% confidence intervals (CIs), of having $1 diagnosed comorbidity associated with an increased risk for severe illness from COVID-19 by race/ethnicity, income, type of health insurance, and RWHAP facility funding. We used logistic regression with predicted marginals to estimate prevalence differences (PDs), with corresponding 95% CIs and t test P values, for having $1 comorbidity by race/ethnicity, income, health insurance type, and RWHAP facility funding.
Because the median age of Whites was higher than for other race/ethnicities and older adults are more likely to have diagnosed comorbidities, we adjusted the association between race/ethnicity and having $1 diagnosed comorbidity for age. To assess whether the association between race/ethnicity and having $1 diagnosed comorbidity differed by income level, we added poverty as an interaction term to the race/ethnicity model. For income, health insurance type, and RWHAP-funding status, we reported unadjusted measures of association. We considered a PD $5 percentage points to be meaningful from a public health perspective.

RESULTS
The sociodemographic characteristics of people receiving HIV care during June 2014-May 2019 are displayed in Table 1. †Poverty guidelines as defined by the Department of Health and Human Services: https://aspe.hhs.gov/frequently-askedquestions-related-poverty-guidelines-and-poverty ‡Participants could select more than 1 response for health insurance or coverage for medications (including antiretroviral medications).
§Whether the usual place of care where participants received HIV care during the past 24 months received any funding from the RWHAP (parts A, B, C, D, or F).

DISCUSSION
More than one-third of adults receiving HIV care in the United States (37.9%) had $1 diagnosed comorbidity associated with an increased risk for severe illness from COVID-19. Those with low income or public insurance alone and Blacks (adjusting for age) with income either above or below the poverty threshold were more likely to have $1 diagnosed comorbidity.
To the best of our knowledge, these are the first population-based data exploring these issues among people with HIV. In the general adult population, based on data from the Behavioral Risk Factor Surveillance System, a slightly higher percent (40.7%) of adults reported having $1 of these comorbidities. 34 However, methodologic differences between the 2 surveys (self-reported data for the Behavioral Risk Factor Surveillance System and medical record review for the MMP) prevent direct comparison of the prevalence of comorbidities in the general population and people receiving HIV care.
Our finding that Blacks (but not Hispanics) receiving HIV care were more likely than Whites to have $1 diagnosed comorbidity is consistent with an analysis of surveillance data exploring racial/ethnic disparities in progression of COVID-19 from mild illness to hospitalization and death. 35 Holtgrave constructed a continuum of COVID-19 outcomes, modeled on the HIV care continuum, 36 and found that although infection rates were higher for Blacks and Hispanics than Whites, hospitalization rates (given infection) were higher for Blacks but not Hispanics. Together, our findings suggest that different interventions may be needed to build COVID-19 health equity in Black and Hispanic communities. Reducing the burden of severe illness from COVID-19 in both communities may require addressing factors related to exposure, eg, housing density, food and housing insecurity, dependence on public transportation, and reliance on front-line jobs that makes physical distancing difficult. To reduce burden in Black communities, structural changes to mitigate the higher prevalence of underlying health conditions may also be needed, including increased access to medical care and supportive services, healthy food options, and recreational spaces. 37,38 Findings from a study of 6916 patients with COVID-19 at the Kaiser Permanente of Southern California support this assumption. 39 In contrast to most population-based studies, the risk of death from COVID-19, once diagnosed, was comparable among Black and White adults, suggesting that equalized access to health care within an integrated health care system may mitigate the high COVID-19 case fatality rate among Blacks. Although many of the structural barriers that underlie the higher prevalence of comorbidities among Blacks receiving HIV care are linked to poverty, we found a higher prevalence of comorbidities among Blacks with incomes above and below the poverty threshold, suggesting that factors in addition to poverty (eg, segregation and discrimination) may limit access to health services, health messaging, and healthy lifestyle options in Black communities.
The intersection of poverty with HIV and COVID-19 is complex. People with low income are at increased risk for acquiring and having poor outcomes from both illnesses, for many of the reasons discussed above. In turn, COVID-19 has caused unemployment and loss of employer-based health insurance for millions of Americans, 40 potentially weakened the health safety net, 41 and challenged recent efforts to end the HIV epidemic. 42 Interrupting the mutually reinforcing cycle of HIV, COVID-19, and poverty may require sustained economic support to prevent worsening of income and health disparities.
About half of US adults with HIV have Medicaid and/ or Medicare as their only health insurance, 43 and this proportion may increase as people who lose employer-based insurance during the pandemic become newly eligible for Medicaid. 44 We found that adults receiving HIV care who had public insurance alone were more likely than those with private insurance to have $1 diagnosed comorbidity (43.4% vs. 33.1%), suggesting Medicare and Medicaid programs may bear increased responsibility as payers of care for adults with HIV at increased risk of severe illness from COVID-19. Conversely, we found that those whose only health coverage was RWHAP assistance were less likely than those with private insurance to have comorbidities, at least in part because they are, on average, younger than others. Because a large proportion of patients receiving HIV care at Ryan White-funded facilities have social determinants associated with poor health outcomes, 45 we expected a higher percentage of patients at those facilities to have comorbidities. However, there was no difference, again at least in part, because RWHAP-funded facilities serve younger patients. However, any conclusion about the burden of severe illness from COVID-19 among patients receiving HIV care at RWHAP-funded facilities should be tempered by knowledge that Blacks and Hispanics, who comprise three-quarters of HIV patients at these facilities, 45 die from COVID-19 at younger ages than Whites. 8

LIMITATIONS
For several reasons, our primary outcome likely underestimates the increased risk of severe illness from COVID-19 among adults receiving HIV care. First, to measure comorbidities, we used only diagnosis data instead of supplementing with medical record information that can identify some conditions, even when not diagnosed, eg, laboratory data for CKD and height and weight for obesity. Our estimate of diagnosed obesity (12.3%) is lower than a previous MMP estimate that calculated the prevalence of body mass index $30 kg/m 2 using height and weight documented in the medical record (19% of men and 42% of women were obese). 46 Because some conditions (eg, COPD) can only be identified using diagnosis data, for consistency, we measured all comorbidities in the same way to avoid information bias of the prevalence of comorbidities, relative to each other. Second, we included comorbidities known to increase the risk of severe illness as of July 15, 2020, and there may have been subsequent additions to the list. We did not include diagnosed conditions that might be associated with the risk for severe illness, but for which there is currently insufficient evidence to support inclusion on the CDC list of conditions that definitely increase the risk, 16 including poorly controlled HIV, which affects one in 3 adults receiving HIV care.
Third, we did not include older age as a risk factor for severe illness from COVID-19. Because the relationship between age and risk is continuous, 33 we did not include an age cut-off when formulating the primary outcome.
For these reasons, our estimate that 37.9% of adults receiving HIV care had $1 diagnosed comorbidity should be considered a minimum estimate of disease burden. Underestimation of risk could have biased our estimates of PDs across race/ethnicities, income levels, and types of health insurance. However, because several of the comorbidities we assessed are more prevalent among Blacks than Whites with HIV, 32,46,47 underestimation of their prevalence would likely have biased differences toward the null. A, Race/ethnicity, adjusted for age, reference group is White, non-Hispanic adults. B, Income at or below the poverty threshold, unadjusted, reference is income above the poverty threshold. C, Type of health insurance, unadjusted, reference is any private insurance. D, Ryan White HIV/AIDS Program funding of the usual place of care (health care facility), unadjusted, reference is no funding. Dashed red line is the meaningful threshold of increased prevalence. Dashed blue line is the meaningful threshold of decreased prevalence. Solid black line is the null threshold. a Unstable estimate (coefficient of variation is $0.3, absolute confidence interval is $30, and/or relative confidence interval is .130%). b Poverty guidelines as defined by the Department of Health and Human Services: https://aspe. hhs.gov/frequently-askedquestions-related-poverty-guidelines-and-poverty. c Participants could select more than 1 response for health insurance or coverage for medications. d Any RWHAP funding (parts A, B, C, D, or F).
Strengths of our study included population-based sampling and weighting designed to produce nationally representative estimates of a wide range of sociodemographic and clinical characteristics of adults with diagnosed HIV, of which those receiving HIV care is a subset. The large sample size allows reasonably precise estimates of subgroup characteristics. Although not all sampled persons participated, results were adjusted for nonresponse using the standard methodology. 48,49 Even with suboptimal response rates, there is still value in results obtained from unbiased sampling methods. 50

CONCLUSIONS
Among adults receiving HIV care, those with low income or public insurance alone and Blacks with income either above or below the poverty threshold were more likely to have $1 diagnosed comorbidity associated with severe illness from COVID-19. Building health equity during the cooccurring epidemics of COVID-19 and HIV may require structural changes to mitigate the burden of these underlying health conditions in Black and low-income communities, including increased access to medical care and supportive services, healthy food options, and recreational spaces.

ACKNOWLEDGMENTS
The authors thank MMP participants, providers, facilities, and project area staff as well as members of the MMP advisory boards. The authors also acknowledge the contributions of the Clinical Outcomes Team and the Behavioral and Clinical Surveillance Branch at the CDC. The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the CDC. Funding for the MMP is provided by a cooperative agreement (PS09-937) from the CDC.