Degree of Housing Instability Shows Independent “Dose-Response” With Virologic Suppression Rates Among People Living With Human Immunodeficiency Virus

Degree of Housing Instability Shows Independent “Dose-Response” With Virologic Suppression... Open Forum Infectious Diseases BRIEF REPORT recent evaluation of viral suppression rates among PLHIV in Degree of Housing Instability Shows clinics receiving Ryan White Care funding used a 3-level cat- Independent “Dose-Response” egorization of housing (stable, temporary, unstable) and found With Virologic Suppression Rates that the rate of virologic suppression decreased as housing instability increased [7]. Among People Living With Human To perform a more granular evaluation of the impact of var- Immunodeficiency Virus ious states of housing stability on HIV treatment outcomes, we 1 1 1 1,2 Angelo Clemenzi-Allen, Elvin Geng, Katerina Christopoulos, Hali Hammer, performed a large study examining the association between 6 1,2 1 1 Susan Buchbinder, Diane Havlir, and Monica Gandhi different categories of living arrangements and virologic sup- Division of HIV, Infectious Diseases and Global Medicine, University of California, San 2 pression rates among PLHIV receiving care in a large San Francisco; San Francisco Department of Public Health, California Francisco-based HIV clinic. Housing instability negatively impacts outcomes in people [liv- METHODS ing] with human immunodeficiency virus (PLHIV), yet the effect of diverse living arrangements has not previously been In 2017, patients self-reported dwelling type upon appoint- evaluated. Using 6 dwelling types to measure housing status, we ment check-in at a safety-net HIV clinic providing HIV and found a strong inverse association between housing instability primary care in San Francisco (“Ward 86”) by circling cur- and viral suppression across a spectrum of unstable housing rent housing status on a pictorial survey (see Supplementary arrangements. Figure) depicting 6 different living arrangements: (1) Rent/ Keywords: homelessness; housing status; disparities; viro- Own; (2) Treatment/Transitional Program; (3) Hotel/Single logic suppression. Room Occupancy (SRO); (4) Staying with Friend (“Couch- Surfing”); (5) Homeless Shelter; (6) Outdoors/In Vehicle. Viral load (VL) measurements performed closest to survey Housing instability constitutes a major structural barrier to completion ±90 days were abstracted from the medical record. treatment outcomes among people living with human immu- We defined virologic suppression as HIV ribonucleic acid nodeficiency virus (PLHIV) [1–3], and it severely restricts the level <200 copies/mL. Patients without VL measures within benefits of achieving complete virologic suppression for both this window were categorized as nonsuppressed. We tabulated the individual and for public health in terms of reducing rates descriptive statistics of baseline demographics. We calculated of forward transmission [4]. Nationally, and specifically in the the proportion achieving virologic suppression and mean VL West, homelessness and housing instability are on the rise [5], in each housing status category. Using logistic regression, we threatening the benefits of antiretroviral therapy for PLHIV [6]. then calculated the unadjusted and adjusted odds of virologic However, of the current studies evaluating the impact of suppression by the 6-category variable of housing status, while housing status among PLHIV, oversimplification of living controlling for age by decade (<30, 30–40, 40–50, >50 years), arrangements that constitute homelessness or marginal hous- gender (female/male), and race/ethnicity (Black, White, ing introduces imprecision to these evaluations. Most of the Latino, or other). Two sensitivity analyses were performed to research to date has dichotomized housing status into homeless (1) exclude participants with missing VL data from the sam- versus not, which may underestimate the nuanced effects of dis- ple and (2) categorize participants with missing VLs within parate living arrangements (eg, transitional housing, shelters, 90  days of the housing survey as virologically suppressed hotels, “couch surfing,” living outdoors) on outcomes. A  more instead of nonsuppressed. RESULTS From February to July 2017, 1222 patients at Ward 86 com- Received 3 January 2018; editorial decision 22 January 2018; accepted 22 February 2018. pleted the survey, 31 of whom had no VL data within the pre- Correspondence: A.  Clemenzi-Allen, MD, Division of HIV, Infectious Diseases and Global Medicine, Zuckerberg San Francisco General Hospital, University of California San Francisco, specified window. Median age was 51 years (interquartile range, 995 Potrero Ave, San Francisco, CA 94110 (angelo.clemenzi-allen@ucsf.edu). 41–58): 13% were female, 40% were white, 25% were black, 26% Open Forum Infectious Diseases were Latino, and 9% were other. As assessed by the pictorial © The Author(s) 2018. Published by Oxford University Press on behalf of Infectious Diseases Society of America. This is an Open Access article distributed under the terms of the Creative Commons survey, 62% of patients rented/owned their place of residence, Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted 6% were in rehabilitation, 13% were in an SRO/hotel, 12% were reuse, distribution, and reproduction in any medium, provided the original work is properly cited. staying with friends, and 7% were staying in a shelter or on the DOI: 10.1093/ofid/ofy035 BRIEF REPORT • OFID • 1 Downloaded from https://academic.oup.com/ofid/article-abstract/5/3/ofy035/4934745 by Ed 'DeepDyve' Gillespie user on 16 March 2018 streets. Across a continuum of housing types, virologic suppres- this clinic-based cohort and likely significant collinearity with sion rates ranged from 85% (rent/own) to 42% (outdoors), and housing status. the mean VL varied from 7004 copies/mL (rent/own) to 87 109 CONCLUSIONS copies/mL (outdoors) (Figure). Greater housing instability was associated with lower rates of virologic suppression and higher The National HIV/AIDS Strategy and the HIV/AIDS Bureau of mean VL in a “dose-response” fashion. Health Resources Service Administration supports increasing sta- In both unadjusted and adjusted models (retaining age, race/ ble housing for PLHIV. Two oft-quoted randomized controlled ethnicity, gender, see Supplementary Table for models), an trials of the impact of housing interventions on virologic outcomes increasing degree of unstable housing (eg, SRO/hotel, staying among PLHIV experiencing homelessness demonstrated little with friends, shelter and outdoors) was associated with a statis- improvement by providing permanent “housing alone”, however, tically significant lower odds of achieving virologic suppression likely reflecting the complications of defining housing status and compared with those who rented/owned (all P < .005) (Figure). concomitant conditions (both predisposing and causative) not The odds of virologic suppression for those staying in an SRO/ solely addressed by providing nontemporary shelter [10, 11]. As hotel was half the odds for those who rented/owned (odds ratio our study suggests, evaluation of the causes of virologic nonsup- [OR], 0.49; 95% confidence interval [CI], 0.32–0.73); the OR pression by dwelling type will address a fundamental research gap, for virologic suppression for those living outside was 0.16 (95% which, in turn, should enhance our ability to design interventions CI, 0.09–0.30). The odds of achieving virologic suppression for to increase virologic suppression across a spectrum of unstable those who lived in supportive treatment/transitional housing housing arrangements, not just among those living on the street. was not statistically significantly different than in those who Incremental improvements in housing stability may improve viro- rented/owned (P  =  .76). Being African American was associ- logic suppression and reduce transmission rates among PLHIV, ated with lower rates of virologic suppression compared with and further evaluation of predisposing factors that lead to a vari- being white, even when adjusting for housing status (OR, 0.67; ety of unstable housing arrangements is indicated. 95% CI, 0.46–0.99; P = .044). These differences were not seen Supplementary Data in those of Latino ethnicity (OR, 0.90; 95% CI, 0.61–1.33; Supplementary materials are available at Open Forum Infectious Diseases P = .17) or “other” race/ethnicity (OR, 0.98; 95% CI, 0.57–1.69; online. Consisting of data provided by the authors to benefit the reader, P  =  .20). Age and gender did not demonstrate a statistically the posted materials are not copyedited and are the sole responsibility of significant relationship to virologic suppression in both unad- the authors, so questions or comments should be addressed to the corre- sponding author. justed and adjusted models (results not shown). Overall results remain unchanged in both sensitivity analyses. Acknowledgments Financial support. This study was funded by National Institutes of DISCUSSION Health Training Grant 5T32AI060530-12 (to A. C.-A.). Additional support came from the San Francisco Department of Public Health. Our study demonstrates a strong association between dwell- Potential conifl cts of interest. All authors: No reported conflicts of ing type and virologic suppression rates among PLHIV across interest. All authors have submitted the ICMJE Form for Disclosure of a continuum of unstable housing arrangements, a finding that Potential Conflicts of Interest. has not previously been described using multiple categoriza- References tions of housing. Although living outdoors was associated with 1. Garcia B, Aragon T, Scheer S. HIV Epidemiology Annual Report 2016. San the lowest likelihood of virologic suppression, other forms of Francisco Department of Public Health Population Health Division; 2017. instability (including living in a shelter, couch-surfing, and Available at: https://www.sfdph.org/dph/files/reports/RptsHIVAIDS/Annual- Report-2016-20170831.pdf. Accessed 27 October 2017. being in an SRO) were also associated with lower rates of viro- 2. Aidala AA, Wilson MG, Shubert V, et al. Housing status, medical care, and health logic suppression compared with being stably housed. outcomes among people living with HIV/AIDS: a systematic review. Am J Public Health 2016; 106:e1–23. Our study is consistent with national and municipal epi- 3. Wohl AR, Benbow N, Tejero J, et  al. Antiretroviral prescription and viral sup- demiologic data showing a strong and persistent association of pression in a representative sample of HIV-infected persons in care in 4 large virologic outcomes with housing status, but it provides more metropolitan areas of the United States, Medical Monitoring Project, 2011–2013. J Acquir Immune Defic Syndr 1999 2017; 76:158–70. granularity on housing type than any prior evaluation [1, 7]. 4. Walensky RP, Borre ED, Bekker LG, et al. The anticipated clinical and economic Moreover, our study confirms persistent disparities in virologic effects of 90-90-90 in South Africa. Ann Intern Med 2016; 165:325. 5. Henry M, Watt R, Rosenthal L, et al. The 2016 Annual Homeless Assessment Report outcomes by race, a finding that is independent of housing sta- (AHAR) to Congress NOVEMBER 2016. U.S. Department of Housing and Urban tus in this large urban clinic population. Race disparities in out- Development Office of Community Planning and Developement; 2016. Available at: https://www.hudexchange.info/resources/documents/2016-AHAR-Part-1.pdf. comes has been seen in multiple previous studies and is an area Accessed 22 November 2017. of active investigation [8, 9], including by our group. Of note, 6. Cohen MS, Chen YQ, McCauley M, et  al. Prevention of HIV-1 infection with early antiretroviral therapy. N Engl J Med 2011; 365:493–505. one limitation of our analysis is that we did not adjust for every 7. Doshi RK, Milberg J, Jumento T, et al. For many served by the Ryan White HIV/ factor that could be associated with virologic suppression (eg, AIDS program, disparities in viral suppression decreased, 2010-14. Health Aff adherence) due to lack of availability of such covariate data in (Millwood) 2017; 36:116–23. 2 • OFID • BRIEF REPORT Downloaded from https://academic.oup.com/ofid/article-abstract/5/3/ofy035/4934745 by Ed 'DeepDyve' Gillespie user on 16 March 2018 8. Lesko CR, Cole SR, Miller WC, et al. Ten-year survival by race/ethnicity and sex 10. Buchanan D, Kee R, Sadowski LS, Garcia D. The health impact of supportive among treated, HIV-infected adults in the United States. Clin Infect Dis 2015; housing for HIV-positive homeless patients: a randomized controlled trial. Am J 60:1700–7. Public Health 2009; 99(Suppl 3):S675–80. 9. Dailey AF, Johnson AS, Wu B. HIV care outcomes among blacks with diag- 11. Wolitski RJ, Kidder DP, Pals SL, et al. Randomized trial of the effects of housing nosed HIV—United States, 2014. MMWR Morb Mortal Wkly Rep 2017; assistance on the health and risk behaviors of homeless and unstably housed peo- 66:97–103. ple living with HIV. AIDS Behav 2010; 14:493–503. BRIEF REPORT • OFID • 3 Downloaded from https://academic.oup.com/ofid/article-abstract/5/3/ofy035/4934745 by Ed 'DeepDyve' Gillespie user on 16 March 2018 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Open Forum Infectious Diseases Oxford University Press

Degree of Housing Instability Shows Independent “Dose-Response” With Virologic Suppression Rates Among People Living With Human Immunodeficiency Virus

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Abstract

Open Forum Infectious Diseases BRIEF REPORT recent evaluation of viral suppression rates among PLHIV in Degree of Housing Instability Shows clinics receiving Ryan White Care funding used a 3-level cat- Independent “Dose-Response” egorization of housing (stable, temporary, unstable) and found With Virologic Suppression Rates that the rate of virologic suppression decreased as housing instability increased [7]. Among People Living With Human To perform a more granular evaluation of the impact of var- Immunodeficiency Virus ious states of housing stability on HIV treatment outcomes, we 1 1 1 1,2 Angelo Clemenzi-Allen, Elvin Geng, Katerina Christopoulos, Hali Hammer, performed a large study examining the association between 6 1,2 1 1 Susan Buchbinder, Diane Havlir, and Monica Gandhi different categories of living arrangements and virologic sup- Division of HIV, Infectious Diseases and Global Medicine, University of California, San 2 pression rates among PLHIV receiving care in a large San Francisco; San Francisco Department of Public Health, California Francisco-based HIV clinic. Housing instability negatively impacts outcomes in people [liv- METHODS ing] with human immunodeficiency virus (PLHIV), yet the effect of diverse living arrangements has not previously been In 2017, patients self-reported dwelling type upon appoint- evaluated. Using 6 dwelling types to measure housing status, we ment check-in at a safety-net HIV clinic providing HIV and found a strong inverse association between housing instability primary care in San Francisco (“Ward 86”) by circling cur- and viral suppression across a spectrum of unstable housing rent housing status on a pictorial survey (see Supplementary arrangements. Figure) depicting 6 different living arrangements: (1) Rent/ Keywords: homelessness; housing status; disparities; viro- Own; (2) Treatment/Transitional Program; (3) Hotel/Single logic suppression. Room Occupancy (SRO); (4) Staying with Friend (“Couch- Surfing”); (5) Homeless Shelter; (6) Outdoors/In Vehicle. Viral load (VL) measurements performed closest to survey Housing instability constitutes a major structural barrier to completion ±90 days were abstracted from the medical record. treatment outcomes among people living with human immu- We defined virologic suppression as HIV ribonucleic acid nodeficiency virus (PLHIV) [1–3], and it severely restricts the level <200 copies/mL. Patients without VL measures within benefits of achieving complete virologic suppression for both this window were categorized as nonsuppressed. We tabulated the individual and for public health in terms of reducing rates descriptive statistics of baseline demographics. We calculated of forward transmission [4]. Nationally, and specifically in the the proportion achieving virologic suppression and mean VL West, homelessness and housing instability are on the rise [5], in each housing status category. Using logistic regression, we threatening the benefits of antiretroviral therapy for PLHIV [6]. then calculated the unadjusted and adjusted odds of virologic However, of the current studies evaluating the impact of suppression by the 6-category variable of housing status, while housing status among PLHIV, oversimplification of living controlling for age by decade (<30, 30–40, 40–50, >50 years), arrangements that constitute homelessness or marginal hous- gender (female/male), and race/ethnicity (Black, White, ing introduces imprecision to these evaluations. Most of the Latino, or other). Two sensitivity analyses were performed to research to date has dichotomized housing status into homeless (1) exclude participants with missing VL data from the sam- versus not, which may underestimate the nuanced effects of dis- ple and (2) categorize participants with missing VLs within parate living arrangements (eg, transitional housing, shelters, 90  days of the housing survey as virologically suppressed hotels, “couch surfing,” living outdoors) on outcomes. A  more instead of nonsuppressed. RESULTS From February to July 2017, 1222 patients at Ward 86 com- Received 3 January 2018; editorial decision 22 January 2018; accepted 22 February 2018. pleted the survey, 31 of whom had no VL data within the pre- Correspondence: A.  Clemenzi-Allen, MD, Division of HIV, Infectious Diseases and Global Medicine, Zuckerberg San Francisco General Hospital, University of California San Francisco, specified window. Median age was 51 years (interquartile range, 995 Potrero Ave, San Francisco, CA 94110 (angelo.clemenzi-allen@ucsf.edu). 41–58): 13% were female, 40% were white, 25% were black, 26% Open Forum Infectious Diseases were Latino, and 9% were other. As assessed by the pictorial © The Author(s) 2018. Published by Oxford University Press on behalf of Infectious Diseases Society of America. This is an Open Access article distributed under the terms of the Creative Commons survey, 62% of patients rented/owned their place of residence, Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted 6% were in rehabilitation, 13% were in an SRO/hotel, 12% were reuse, distribution, and reproduction in any medium, provided the original work is properly cited. staying with friends, and 7% were staying in a shelter or on the DOI: 10.1093/ofid/ofy035 BRIEF REPORT • OFID • 1 Downloaded from https://academic.oup.com/ofid/article-abstract/5/3/ofy035/4934745 by Ed 'DeepDyve' Gillespie user on 16 March 2018 streets. Across a continuum of housing types, virologic suppres- this clinic-based cohort and likely significant collinearity with sion rates ranged from 85% (rent/own) to 42% (outdoors), and housing status. the mean VL varied from 7004 copies/mL (rent/own) to 87 109 CONCLUSIONS copies/mL (outdoors) (Figure). Greater housing instability was associated with lower rates of virologic suppression and higher The National HIV/AIDS Strategy and the HIV/AIDS Bureau of mean VL in a “dose-response” fashion. Health Resources Service Administration supports increasing sta- In both unadjusted and adjusted models (retaining age, race/ ble housing for PLHIV. Two oft-quoted randomized controlled ethnicity, gender, see Supplementary Table for models), an trials of the impact of housing interventions on virologic outcomes increasing degree of unstable housing (eg, SRO/hotel, staying among PLHIV experiencing homelessness demonstrated little with friends, shelter and outdoors) was associated with a statis- improvement by providing permanent “housing alone”, however, tically significant lower odds of achieving virologic suppression likely reflecting the complications of defining housing status and compared with those who rented/owned (all P < .005) (Figure). concomitant conditions (both predisposing and causative) not The odds of virologic suppression for those staying in an SRO/ solely addressed by providing nontemporary shelter [10, 11]. As hotel was half the odds for those who rented/owned (odds ratio our study suggests, evaluation of the causes of virologic nonsup- [OR], 0.49; 95% confidence interval [CI], 0.32–0.73); the OR pression by dwelling type will address a fundamental research gap, for virologic suppression for those living outside was 0.16 (95% which, in turn, should enhance our ability to design interventions CI, 0.09–0.30). The odds of achieving virologic suppression for to increase virologic suppression across a spectrum of unstable those who lived in supportive treatment/transitional housing housing arrangements, not just among those living on the street. was not statistically significantly different than in those who Incremental improvements in housing stability may improve viro- rented/owned (P  =  .76). Being African American was associ- logic suppression and reduce transmission rates among PLHIV, ated with lower rates of virologic suppression compared with and further evaluation of predisposing factors that lead to a vari- being white, even when adjusting for housing status (OR, 0.67; ety of unstable housing arrangements is indicated. 95% CI, 0.46–0.99; P = .044). These differences were not seen Supplementary Data in those of Latino ethnicity (OR, 0.90; 95% CI, 0.61–1.33; Supplementary materials are available at Open Forum Infectious Diseases P = .17) or “other” race/ethnicity (OR, 0.98; 95% CI, 0.57–1.69; online. Consisting of data provided by the authors to benefit the reader, P  =  .20). Age and gender did not demonstrate a statistically the posted materials are not copyedited and are the sole responsibility of significant relationship to virologic suppression in both unad- the authors, so questions or comments should be addressed to the corre- sponding author. justed and adjusted models (results not shown). Overall results remain unchanged in both sensitivity analyses. Acknowledgments Financial support. This study was funded by National Institutes of DISCUSSION Health Training Grant 5T32AI060530-12 (to A. C.-A.). Additional support came from the San Francisco Department of Public Health. Our study demonstrates a strong association between dwell- Potential conifl cts of interest. All authors: No reported conflicts of ing type and virologic suppression rates among PLHIV across interest. All authors have submitted the ICMJE Form for Disclosure of a continuum of unstable housing arrangements, a finding that Potential Conflicts of Interest. has not previously been described using multiple categoriza- References tions of housing. Although living outdoors was associated with 1. Garcia B, Aragon T, Scheer S. HIV Epidemiology Annual Report 2016. San the lowest likelihood of virologic suppression, other forms of Francisco Department of Public Health Population Health Division; 2017. instability (including living in a shelter, couch-surfing, and Available at: https://www.sfdph.org/dph/files/reports/RptsHIVAIDS/Annual- Report-2016-20170831.pdf. Accessed 27 October 2017. being in an SRO) were also associated with lower rates of viro- 2. Aidala AA, Wilson MG, Shubert V, et al. Housing status, medical care, and health logic suppression compared with being stably housed. outcomes among people living with HIV/AIDS: a systematic review. Am J Public Health 2016; 106:e1–23. Our study is consistent with national and municipal epi- 3. Wohl AR, Benbow N, Tejero J, et  al. Antiretroviral prescription and viral sup- demiologic data showing a strong and persistent association of pression in a representative sample of HIV-infected persons in care in 4 large virologic outcomes with housing status, but it provides more metropolitan areas of the United States, Medical Monitoring Project, 2011–2013. J Acquir Immune Defic Syndr 1999 2017; 76:158–70. granularity on housing type than any prior evaluation [1, 7]. 4. Walensky RP, Borre ED, Bekker LG, et al. The anticipated clinical and economic Moreover, our study confirms persistent disparities in virologic effects of 90-90-90 in South Africa. Ann Intern Med 2016; 165:325. 5. Henry M, Watt R, Rosenthal L, et al. The 2016 Annual Homeless Assessment Report outcomes by race, a finding that is independent of housing sta- (AHAR) to Congress NOVEMBER 2016. U.S. Department of Housing and Urban tus in this large urban clinic population. Race disparities in out- Development Office of Community Planning and Developement; 2016. Available at: https://www.hudexchange.info/resources/documents/2016-AHAR-Part-1.pdf. comes has been seen in multiple previous studies and is an area Accessed 22 November 2017. of active investigation [8, 9], including by our group. Of note, 6. Cohen MS, Chen YQ, McCauley M, et  al. Prevention of HIV-1 infection with early antiretroviral therapy. N Engl J Med 2011; 365:493–505. one limitation of our analysis is that we did not adjust for every 7. Doshi RK, Milberg J, Jumento T, et al. For many served by the Ryan White HIV/ factor that could be associated with virologic suppression (eg, AIDS program, disparities in viral suppression decreased, 2010-14. Health Aff adherence) due to lack of availability of such covariate data in (Millwood) 2017; 36:116–23. 2 • OFID • BRIEF REPORT Downloaded from https://academic.oup.com/ofid/article-abstract/5/3/ofy035/4934745 by Ed 'DeepDyve' Gillespie user on 16 March 2018 8. Lesko CR, Cole SR, Miller WC, et al. Ten-year survival by race/ethnicity and sex 10. Buchanan D, Kee R, Sadowski LS, Garcia D. The health impact of supportive among treated, HIV-infected adults in the United States. Clin Infect Dis 2015; housing for HIV-positive homeless patients: a randomized controlled trial. Am J 60:1700–7. Public Health 2009; 99(Suppl 3):S675–80. 9. Dailey AF, Johnson AS, Wu B. HIV care outcomes among blacks with diag- 11. Wolitski RJ, Kidder DP, Pals SL, et al. Randomized trial of the effects of housing nosed HIV—United States, 2014. MMWR Morb Mortal Wkly Rep 2017; assistance on the health and risk behaviors of homeless and unstably housed peo- 66:97–103. ple living with HIV. AIDS Behav 2010; 14:493–503. BRIEF REPORT • OFID • 3 Downloaded from https://academic.oup.com/ofid/article-abstract/5/3/ofy035/4934745 by Ed 'DeepDyve' Gillespie user on 16 March 2018

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Open Forum Infectious DiseasesOxford University Press

Published: Mar 1, 2018

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