UNAIDS, 2023. Global HIV and AIDS Statistics – Fact Sheet 2023. Available at: https://www.unaids.org/sites/default/files/media_asset/UNAIDS_FactSheet_en.pdf. Accessed September 5, 2023.
Cao G, Wang Y, Wu Y, Jing W, Liu J, Liu M, 2022. Prevalence of anemia among people living with HIV: A systematic review and meta-analysis. EClinicalMedicine 44: 101283.
Abioye AI, Andersen CT, Sudfeld CR, Fawzi WW, 2020. Anemia, iron status, and HIV: A systematic review of the evidence. Adv Nutr 5: 1334–1363.
Groopman JE, 1990. Zidovudine intolerance. Rev Infect Dis 12 (Suppl 5 ):S500–S506.
Marchionatti A, Parisi MM, 2021. Anemia and thrombocytopenia in people living with HIV/AIDS: A narrative literature review. Int Health 2: 98–109.
Volberding PA, Levine AM, Dieterich D, Mildvan D, Mitsuyasu R, Saag M, 2004. Anemia in HIV Working Group. Anemia in HIV infection: Clinical impact and evidence-based management strategies. Clin Infect Dis 10: 1454–1463.
Albrecht S, et al., 2019. Age-related comorbidities and mortality in people living with HIV in rural Tanzania. AIDS 6: 1031–1041.
Belperio PS, Rhew DC, 2004. Prevalence and outcomes of anemia in individuals with human immunodeficiency virus: A systematic review of the literature. Am J Med 116 (Suppl 7A ):27S–43S.
Ezeamama AE, Guwatudde D, Sikorskii A, Kabagambe EK, Spelts R, Vahey G, Fenton JI, Fawzi WW, 2018. Impaired hematologic status in relation to clinical outcomes among HIV-infected adults from Uganda: A prospective cohort study. Nutrients 4: 475.
Gunda DW, Kilonzo SB, Mpondo BC, 2016. Magnitude and correlates of moderate to severe anemia among adult HIV patients receiving first line HAART in Northwestern Tanzania: A cross sectional clinic based study. Pan Afr Med J 23: 26.
Haider BA, Spiegelman D, Hertzmark E, Sando D, Duggan C, Makubi A, Sudfeld C, Aris E, Chalamilla GE, Fawzi WW, 2019. Anemia, iron deficiency, and iron supplementation in relation to mortality among HIV-infected patients receiving highly active antiretroviral therapy in Tanzania. Am J Trop Med Hyg 6: 1512–1520.
Berhane K, Karim R, Cohen MH, Masri-Lavine L, Young M, Anastos K, Augenbraun M, Watts DH, Levine AM, 2004. Impact of highly active antiretroviral therapy on anemia and relationship between anemia and survival in a large cohort of HIV-infected women: Women’s Interagency HIV Study. J Acquir Immune Defic Syndr 2: 1245–1252.
Kiragga AN, Castelnuovo B, Nakanjako D, Manabe YC, 2010. Baseline severe anaemia should not preclude use of zidovudine in antiretroviral-eligible patients in resource-limited settings. J Int AIDS Soc 13: 42.
Johannessen A, Naman E, Gundersen SG, Bruun JN, 2011. Antiretroviral treatment reverses HIV-associated anemia in rural Tanzania. BMC Infect Dis 11: 190.
Takuva S, Maskew M, Brennan AT, Sanne I, Macphail AP, Fox MP, 2013. Anemia among HIV-infected patients initiating antiretroviral therapy in South Africa: Improvement in hemoglobin regardless of degree of immunosuppression and the initiating ART regimen. J Trop Med 2013: 162950.
Akilimali PZ, Kashala-Abotnes E, Musumari PM, Kayembe PK, Tylleskar T, Mapatano MA, 2015. Predictors of persistent anaemia in the first year of antiretroviral therapy: A retrospective cohort study from Goma, the Democratic Republic of Congo. PLoS One 10: e0140240.
Getaneh Z, Wale W, Chanie B, Temesgen E, Abebe M, Walie M, Lemma M, 2021. Magnitude and associated factors of anemia among AZT based HAART experienced adult HIV patients at University of Gondar Comprehensive Specialized Referral Hospital, Northwest, Ethiopia, 2019: A retrospective cohort study. BMC Infect Dis 1: 1016.
Harris RJ, et al., 2008. Prognostic importance of anaemia in HIV type-1-infected patients starting antiretroviral therapy: Collaborative analysis of prospective cohort studies. Antivir Ther 8: 959–967.
Kerkhoff AD, Wood R, Cobelens FG, Gupta-Wright A, Bekker LG, Lawn SD, 2014. Resolution of anaemia in a cohort of HIV-infected patients with a high prevalence and incidence of tuberculosis receiving antiretroviral therapy in South Africa. BMC Infect Dis 14: 3860.
Jaganath D, Walker AS, Ssali F, Musiime V, Kiweewa F, Kityo C, Salata R, Mugyenyi P; DART Trial; ARROW Trial, 2014. HIV-associated anemia after 96 weeks on therapy: Determinants across age ranges in Uganda and Zimbabwe. AIDS Res Hum Retroviruses 6: 523–530.
Moh R, et al., 2005. Haematological changes in adults receiving a zidovudine-containing HAART regimen in combination with cotrimoxazole in Côte d’Ivoire. Antivir Ther 5: 615–624.
Tamir Z, Alemu J, Tsegaye A, 2018. Anemia among HIV infected individuals taking ART with and without zidovudine at Addis Ababa, Ethiopia. Ethiop J Health Sci 1: 73–82.
Woldeamanuel GG, Wondimu DH, 2018. Prevalence of anemia before and after initiation of antiretroviral therapy among HIV infected patients at Black Lion Specialized Hospital, Addis Ababa, Ethiopia: A cross sectional study. BMC Hematol 18: 7.
Gelmon K, et al., 1989. Nature, time course and dose dependence of zidovudine-related side effects: Results from the Multicenter Canadian Azidothymidine Trial. AIDS 9: 555–561.
World Health Organization, 2021. Consolidated Guidelines on HIV Prevention, Testing, Treatment, Service Delivery and Monitoring: Recommendations for a Public Health Approach, 2021 Update. Available at: https://apps.who.int/iris/handle/10665/342899. Accessed September 5, 2023.
Tanzania Ministry of Health National AIDS Control Programme, 2019. National Guidelines for the Management of HIV and AIDS, 7th edition. Available from: https://nacp.go.tz/download/national-guidelines-for-the-management-of-hiv-and-aids-april-2019. Accessed September 5, 2023.
Peck RN, Shedafa R, Kalluvya S, Downs JA, Todd J, Suthanthiran M, Fitzgerald DW, Kataraihya JB, 2014. Hypertension, kidney disease, HIV and antiretroviral therapy among Tanzanian adults: A cross-sectional study. BMC Med 12: 125.
Reis KG, Desderius B, Kingery J, Kirabo A, Makubi A, Myalla C, Lee MH, Kapiga S, Peck RN, 2020. Blood pressure, T cells, and mortality in people with HIV in Tanzania during the first 2 years of antiretroviral therapy. J Clin Hypertens (Greenwich) 9: 1554–1562.
World Health Organization, 2012. WHO Steps Instrument. Available at: https://www.who.int/teams/noncommunicable-diseases/surveillance/systems-tools/steps. Accessed June 1, 2015.
Kavishe B, et al., 2015. High prevalence of hypertension and of risk factors for non-communicable diseases (NCDs): A population based cross-sectional survey of NCDS and HIV infection in Northwestern Tanzania and Southern Uganda. BMC Med 13: 126.
Wyatt CM, et al., 2013. Estimating kidney function in HIV-infected adults in Kenya: Comparison to a direct measure of glomerular filtration rate by iohexol clearance. PLoS One 8: e69601.
World Health Organization, 2011. Haemoglobin Concentrations for the Diagnosis of Anaemia and Assessment of Severity. Available at: https://apps.who.int/iris/handle/10665/85839. Accessed June 1, 2016.
Tigabu A, et al., 2022. Incidence and predictors of anemia among adults on HIV care at South Gondar Zone Public General Hospital Northwest Ethiopia, 2020; retrospective cohort study. PLoS One 1: e0259944.
Harding BN, et al., 2020. Antiretroviral drug class and anaemia risk in the current treatment era among people living with HIV in the USA: A clinical cohort study. BMJ Open 3: e031487.
Levine AM, et al., 2001. Prevalence and correlates of anemia in a large cohort of HIV-infected women: Women’s Interagency HIV Study. J Acquir Immune Defic Syndr 1: 28–35.
Semba RD, Shah N, Klein RS, Mayer KH, Schuman P, Vlahov D; Human Immunodeficiency Virus Epidemiology Research Study Group, 2002. Prevalence and cumulative incidence of and risk factors for anemia in a multicenter cohort study of human immunodeficiency virus-infected and -uninfected women. Clin Infect Dis 2: 260–266.
Petraro P, Duggan C, Spiegelman D, Hertzmark E, Makubi A, Chalamilla G, Siril H, Sando D, Aboud S, Fawzi WW, 2016. Determinants of anemia among human immunodeficiency virus-positive adults at care and treatment clinics in Dar es Salaam, Tanzania. Am J Trop Med Hyg 2: 384–392.
Noor RA, Abioye AI, Hertzmark E, Darling AM, Aboud S, Mugusi FM, Sudfeld CR, Spiegelman D, Fawzi WW, 2020. Impaired hematological status increases the risk of mortality among HIV-infected adults initiating antiretroviral therapy in Tanzania. J Nutr 9: 2375–2382.
Clark TD, Semba RD, 2001. Iron supplementation during human immunodeficiency virus infection: A double-edged sword? Med Hypotheses 4: 476–479.
Drakesmith H, Prentice AM, 2012. Hepcidin and the iron-infection axis. Science 6108: 768–772.
Kupka R, Msamanga GI, Mugusi F, Petraro P, Hunter DJ, Fawzi WW, 2007. Iron status is an important cause of anemia in HIV-infected Tanzanian women but is not related to accelerated HIV disease progression. J Nutr 10: 2317–2323.
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Anemia is common among people living with HIV (PLWH), particularly in Africa. Outcomes for PLWH on modern antiretroviral therapy (ART) regimens are not well documented. We conducted an observational study to determine the outcomes and predictors of anemia after ART initiation in Tanzania. We enrolled and followed ART-naïve PLWH and HIV-uninfected individuals at three clinics in Tanzania. We grouped participants into four longitudinal categories based on hemoglobin concentration measured at baseline and 6 months after ART initiation (normal, resolved anemia, incident anemia, and persistent anemia) and followed them for 24 months. There were 991 study participants (494 PLWH, 497 HIV uninfected). After 6 months of ART, 33.9% of PLWH had persistent anemia and 9.9% had incident anemia compared with 12.6% and 9.6% for HIV-uninfected controls. Female sex (adjusted odds ratio [aOR]: 2.62; 95% CI: 1.91–6.75) and low income (aOR: 3.10; 95% CI: 1.36–7.20) were strong predictors of persistent anemia for both PLWH and HIV-uninfected individuals. For PLWH, having a CD4+ T cell count of less than 350 cells/mm3 (aOR: 0.34; 95% Cl: 0.15–0.73) was significantly associated with anemia resolution. Mortality was higher for PLWH who had persistent anemia or incident anemia than for PLWH who had normal hemoglobin or improved anemia (hazard ratio: 4.0, 95% Cl 1.3–12.2). One-third of adults in Tanzania had persistent anemia after 6 months on ART, and persistent anemia was associated with increased mortality. PLWH with persistent or incident anemia after 6 months on modern ART deserve close follow-up, particularly women and low-income adults.
Financial support: This study was supported by R. N. Peck’s
Disclosures: This study protocol was reviewed and approved by the institutional review boards of Weill Cornell Medicine (1506016328), the Tanzanian National Institute of Medical Research (NIMR/HQ/R.8c/Vol.1/1399), and Bugando Medical Center (CREC/074/2015). All study procedures were performed in accordance with the World Medical Association Declaration of Helsinki. All participants provided written informed consent.
Current contact information: Duncan K. Hau, Department of Pediatrics, Weill Cornell Medical College, New York, NY, E-mail: dkh2001@med.cornell.edu. Salama Fadhil, Mwanza Intervention Trials Unit, Mwanza, Tanzania, E-mail: salama.fadhil@mitu.or.tz. Myung Hee Lee, Megan Willkens, and Robert N. Peck, Center for Global Health, Weill Cornell Medical College, New York, NY, E-mails: myl2003@med.cornell.edu, maw4016@med.cornell.edu, and rnp2002@med.cornell.edu. Bernard Desderius and Samuel E. Kalluvya, Department of Medicine, Catholic University of Health and Allied Sciences, Mwanza, Tanzania, E-mails: bm.desderius@gmail.com and samuelkalluvya@yahoo.com. Erius Tebuka, Department of Pathology, Catholic University of Health and Allied Sciences, Mwanza, Tanzania, E-mail: eriust@yahoo.com. Luke R. Smart, Department of Pediatrics, College of Medicine, University of Cincinnati, Cincinnati, OH, E-mail: luke.smart@cchmc.org.
UNAIDS, 2023. Global HIV and AIDS Statistics – Fact Sheet 2023. Available at: https://www.unaids.org/sites/default/files/media_asset/UNAIDS_FactSheet_en.pdf. Accessed September 5, 2023.
Cao G, Wang Y, Wu Y, Jing W, Liu J, Liu M, 2022. Prevalence of anemia among people living with HIV: A systematic review and meta-analysis. EClinicalMedicine 44: 101283.
Abioye AI, Andersen CT, Sudfeld CR, Fawzi WW, 2020. Anemia, iron status, and HIV: A systematic review of the evidence. Adv Nutr 5: 1334–1363.
Groopman JE, 1990. Zidovudine intolerance. Rev Infect Dis 12 (Suppl 5 ):S500–S506.
Marchionatti A, Parisi MM, 2021. Anemia and thrombocytopenia in people living with HIV/AIDS: A narrative literature review. Int Health 2: 98–109.
Volberding PA, Levine AM, Dieterich D, Mildvan D, Mitsuyasu R, Saag M, 2004. Anemia in HIV Working Group. Anemia in HIV infection: Clinical impact and evidence-based management strategies. Clin Infect Dis 10: 1454–1463.
Albrecht S, et al., 2019. Age-related comorbidities and mortality in people living with HIV in rural Tanzania. AIDS 6: 1031–1041.
Belperio PS, Rhew DC, 2004. Prevalence and outcomes of anemia in individuals with human immunodeficiency virus: A systematic review of the literature. Am J Med 116 (Suppl 7A ):27S–43S.
Ezeamama AE, Guwatudde D, Sikorskii A, Kabagambe EK, Spelts R, Vahey G, Fenton JI, Fawzi WW, 2018. Impaired hematologic status in relation to clinical outcomes among HIV-infected adults from Uganda: A prospective cohort study. Nutrients 4: 475.
Gunda DW, Kilonzo SB, Mpondo BC, 2016. Magnitude and correlates of moderate to severe anemia among adult HIV patients receiving first line HAART in Northwestern Tanzania: A cross sectional clinic based study. Pan Afr Med J 23: 26.
Haider BA, Spiegelman D, Hertzmark E, Sando D, Duggan C, Makubi A, Sudfeld C, Aris E, Chalamilla GE, Fawzi WW, 2019. Anemia, iron deficiency, and iron supplementation in relation to mortality among HIV-infected patients receiving highly active antiretroviral therapy in Tanzania. Am J Trop Med Hyg 6: 1512–1520.
Berhane K, Karim R, Cohen MH, Masri-Lavine L, Young M, Anastos K, Augenbraun M, Watts DH, Levine AM, 2004. Impact of highly active antiretroviral therapy on anemia and relationship between anemia and survival in a large cohort of HIV-infected women: Women’s Interagency HIV Study. J Acquir Immune Defic Syndr 2: 1245–1252.
Kiragga AN, Castelnuovo B, Nakanjako D, Manabe YC, 2010. Baseline severe anaemia should not preclude use of zidovudine in antiretroviral-eligible patients in resource-limited settings. J Int AIDS Soc 13: 42.
Johannessen A, Naman E, Gundersen SG, Bruun JN, 2011. Antiretroviral treatment reverses HIV-associated anemia in rural Tanzania. BMC Infect Dis 11: 190.
Takuva S, Maskew M, Brennan AT, Sanne I, Macphail AP, Fox MP, 2013. Anemia among HIV-infected patients initiating antiretroviral therapy in South Africa: Improvement in hemoglobin regardless of degree of immunosuppression and the initiating ART regimen. J Trop Med 2013: 162950.
Akilimali PZ, Kashala-Abotnes E, Musumari PM, Kayembe PK, Tylleskar T, Mapatano MA, 2015. Predictors of persistent anaemia in the first year of antiretroviral therapy: A retrospective cohort study from Goma, the Democratic Republic of Congo. PLoS One 10: e0140240.
Getaneh Z, Wale W, Chanie B, Temesgen E, Abebe M, Walie M, Lemma M, 2021. Magnitude and associated factors of anemia among AZT based HAART experienced adult HIV patients at University of Gondar Comprehensive Specialized Referral Hospital, Northwest, Ethiopia, 2019: A retrospective cohort study. BMC Infect Dis 1: 1016.
Harris RJ, et al., 2008. Prognostic importance of anaemia in HIV type-1-infected patients starting antiretroviral therapy: Collaborative analysis of prospective cohort studies. Antivir Ther 8: 959–967.
Kerkhoff AD, Wood R, Cobelens FG, Gupta-Wright A, Bekker LG, Lawn SD, 2014. Resolution of anaemia in a cohort of HIV-infected patients with a high prevalence and incidence of tuberculosis receiving antiretroviral therapy in South Africa. BMC Infect Dis 14: 3860.
Jaganath D, Walker AS, Ssali F, Musiime V, Kiweewa F, Kityo C, Salata R, Mugyenyi P; DART Trial; ARROW Trial, 2014. HIV-associated anemia after 96 weeks on therapy: Determinants across age ranges in Uganda and Zimbabwe. AIDS Res Hum Retroviruses 6: 523–530.
Moh R, et al., 2005. Haematological changes in adults receiving a zidovudine-containing HAART regimen in combination with cotrimoxazole in Côte d’Ivoire. Antivir Ther 5: 615–624.
Tamir Z, Alemu J, Tsegaye A, 2018. Anemia among HIV infected individuals taking ART with and without zidovudine at Addis Ababa, Ethiopia. Ethiop J Health Sci 1: 73–82.
Woldeamanuel GG, Wondimu DH, 2018. Prevalence of anemia before and after initiation of antiretroviral therapy among HIV infected patients at Black Lion Specialized Hospital, Addis Ababa, Ethiopia: A cross sectional study. BMC Hematol 18: 7.
Gelmon K, et al., 1989. Nature, time course and dose dependence of zidovudine-related side effects: Results from the Multicenter Canadian Azidothymidine Trial. AIDS 9: 555–561.
World Health Organization, 2021. Consolidated Guidelines on HIV Prevention, Testing, Treatment, Service Delivery and Monitoring: Recommendations for a Public Health Approach, 2021 Update. Available at: https://apps.who.int/iris/handle/10665/342899. Accessed September 5, 2023.
Tanzania Ministry of Health National AIDS Control Programme, 2019. National Guidelines for the Management of HIV and AIDS, 7th edition. Available from: https://nacp.go.tz/download/national-guidelines-for-the-management-of-hiv-and-aids-april-2019. Accessed September 5, 2023.
Peck RN, Shedafa R, Kalluvya S, Downs JA, Todd J, Suthanthiran M, Fitzgerald DW, Kataraihya JB, 2014. Hypertension, kidney disease, HIV and antiretroviral therapy among Tanzanian adults: A cross-sectional study. BMC Med 12: 125.
Reis KG, Desderius B, Kingery J, Kirabo A, Makubi A, Myalla C, Lee MH, Kapiga S, Peck RN, 2020. Blood pressure, T cells, and mortality in people with HIV in Tanzania during the first 2 years of antiretroviral therapy. J Clin Hypertens (Greenwich) 9: 1554–1562.
World Health Organization, 2012. WHO Steps Instrument. Available at: https://www.who.int/teams/noncommunicable-diseases/surveillance/systems-tools/steps. Accessed June 1, 2015.
Kavishe B, et al., 2015. High prevalence of hypertension and of risk factors for non-communicable diseases (NCDs): A population based cross-sectional survey of NCDS and HIV infection in Northwestern Tanzania and Southern Uganda. BMC Med 13: 126.
Wyatt CM, et al., 2013. Estimating kidney function in HIV-infected adults in Kenya: Comparison to a direct measure of glomerular filtration rate by iohexol clearance. PLoS One 8: e69601.
World Health Organization, 2011. Haemoglobin Concentrations for the Diagnosis of Anaemia and Assessment of Severity. Available at: https://apps.who.int/iris/handle/10665/85839. Accessed June 1, 2016.
Tigabu A, et al., 2022. Incidence and predictors of anemia among adults on HIV care at South Gondar Zone Public General Hospital Northwest Ethiopia, 2020; retrospective cohort study. PLoS One 1: e0259944.
Harding BN, et al., 2020. Antiretroviral drug class and anaemia risk in the current treatment era among people living with HIV in the USA: A clinical cohort study. BMJ Open 3: e031487.
Levine AM, et al., 2001. Prevalence and correlates of anemia in a large cohort of HIV-infected women: Women’s Interagency HIV Study. J Acquir Immune Defic Syndr 1: 28–35.
Semba RD, Shah N, Klein RS, Mayer KH, Schuman P, Vlahov D; Human Immunodeficiency Virus Epidemiology Research Study Group, 2002. Prevalence and cumulative incidence of and risk factors for anemia in a multicenter cohort study of human immunodeficiency virus-infected and -uninfected women. Clin Infect Dis 2: 260–266.
Petraro P, Duggan C, Spiegelman D, Hertzmark E, Makubi A, Chalamilla G, Siril H, Sando D, Aboud S, Fawzi WW, 2016. Determinants of anemia among human immunodeficiency virus-positive adults at care and treatment clinics in Dar es Salaam, Tanzania. Am J Trop Med Hyg 2: 384–392.
Noor RA, Abioye AI, Hertzmark E, Darling AM, Aboud S, Mugusi FM, Sudfeld CR, Spiegelman D, Fawzi WW, 2020. Impaired hematological status increases the risk of mortality among HIV-infected adults initiating antiretroviral therapy in Tanzania. J Nutr 9: 2375–2382.
Clark TD, Semba RD, 2001. Iron supplementation during human immunodeficiency virus infection: A double-edged sword? Med Hypotheses 4: 476–479.
Drakesmith H, Prentice AM, 2012. Hepcidin and the iron-infection axis. Science 6108: 768–772.
Kupka R, Msamanga GI, Mugusi F, Petraro P, Hunter DJ, Fawzi WW, 2007. Iron status is an important cause of anemia in HIV-infected Tanzanian women but is not related to accelerated HIV disease progression. J Nutr 10: 2317–2323.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 426 | 426 | 148 |
Full Text Views | 22 | 22 | 2 |
PDF Downloads | 34 | 34 | 3 |