Vitamin A and D Deficiencies Associated with Incident Tuberculosis in HIV-Infected Patients Initiating Antiretroviral Therapy in Multinational Case-Cohort Study

Journal of Acquired Immune Deficiency Syndromes

Volumn 75, Issue 3, 2017, Pages e71-e79

  Tenforde, Mark W ^a   Yadav, Ashish ^b   Dowdy, David W ^b   Gupte, Nikhil ^c   Shivakoti, Rupak ^c   Yang, Wei Teng ^d   Mwelase, Noluthando ^e   Kanyama, Cecilia ^f   Pillay, Sandy ^g   Samaneka, Wadzanai ^h   Santos, Breno ⁱ   Poongulali, Selvamuthu ^j   Tripathy, Srikanth ^k   Riviere, Cynthia ^l   Berendes, Sima ^c,m   Lama, Javier R ⁿ   Cardoso, Sandra W ^o   Sugandhavesa, Patcharaphan ^p   Christian, Parul ^b   Semba, Richard D ^c   Campbell, Thomas B ^q   Gupta, Amita ^b,c   more..

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d BRIDGEPORT HOSPITAL   (United States)

^e UNIVERSITY OF THE WITWATERSRAND   (South Africa)

^f Baylor College of Medicine Abbott Fund Children's Clinical Center of Excellence   (Malawi)

^g DURBAN UNIVERSITY OF TECHNOLOGY   (South Africa)

^h UNIVERSITY OF ZIMBABWE   (Zimbabwe)

ⁱ Neonatal Unit   (Brazil)

^j YRG CENTRE FOR AIDS RESEARCH AND EDUCATION   (India)

^k NATIONAL AIDS RESEARCH INSTITUTE   (India)

^l Centers Institute of Infectious Diseases and Reproductive Health   (Haïti)

^m LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

ⁿ ASOCIACIÓN CIVIL IMPACTA SALUD Y EDUCACIÓN   (Peru)

^o Funda??o Oswaldo Cruz   (Brazil)

^p Research Institute for Health Sciences   (Thailand)

^q UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

more..

Author keywords

antiretroviral treatment; case cohort study; HIV; micronutrients; resource limited settings; tuberculosis

Indexed keywords

ALPHA CAROTENE; ALPHA TOCOPHEROL; ATAZANAVIR; BETA CAROTENE; BETA CRYPTOXANTHIN; C REACTIVE PROTEIN; CYANOCOBALAMIN; DIDANOSINE; EFAVIRENZ; EMTRICITABINE; EMTRICITABINE PLUS TENOFOVIR DISOPROXIL; LAMIVUDINE PLUS ZIDOVUDINE; LYCOPENE; PYRIDOXINE; RETINOL; SELENIUM; VIRUS RNA; VITAMIN D; XANTHOPHYLL; ZEAXANTHIN; ANTIRETROVIRUS AGENT; TRACE ELEMENT;

ANTIRETROVIRAL THERAPY; ARTICLE; BLACK PERSON; BODY MASS; CD4 LYMPHOCYTE COUNT; COHORT ANALYSIS; COMBINATION DRUG THERAPY; CONTROLLED STUDY; DISEASE ASSOCIATION; DRUG DOSE COMPARISON; FEMALE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MAJOR CLINICAL STUDY; MALE; OPEN STUDY; PRIORITY JOURNAL; PROSPECTIVE STUDY; RANDOMIZED CONTROLLED TRIAL; RETINOL DEFICIENCY; SELENIUM BLOOD LEVEL; TREATMENT DURATION; TUBERCULOSIS; VIRUS LOAD; VITAMIN BLOOD LEVEL; VITAMIN D DEFICIENCY; ADULT; ADVERSE EFFECTS; BLOOD; CD4+ T LYMPHOCYTE; CLINICAL TRIAL; COMPLICATION; DEFICIENCY; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HIV INFECTIONS; IMMUNOLOGY; MALNUTRITION; MIXED INFECTION; MULTICENTER STUDY; PREVALENCE;

ADULT; ANTI-RETROVIRAL AGENTS; ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; CD4-POSITIVE T-LYMPHOCYTES; COINFECTION; FEMALE; HIV INFECTIONS; HUMANS; MALE; MALNUTRITION; MICRONUTRIENTS; PREVALENCE; PROSPECTIVE STUDIES; TUBERCULOSIS; VITAMIN A DEFICIENCY; VITAMIN D DEFICIENCY;

EID: 85011890563     PISSN: 15254135     EISSN: 10779450     Source Type: Journal    
DOI: 10.1097/QAI.0000000000001308     Document Type: Article

References (70)

1. World Health Organization. Global Tuberculosis Report. Geneva, Switzerland: WHO Press; 2015.
2. Kyeyune R, den Boon S, Cattamanchi A, et al. Causes of early mortality in HIV-infected TB suspects in an East African referral hospital. J Acquir Immune Defic Syndr. 2010;55:446-450.
3. Lawn SD, Harries AD, Anglaret X, et al. Early mortality among adults accessing antiretroviral treatment programmes in sub-Saharan Africa. AIDS. 2008;22:1897-1908.
4. Lawn SD, Badri M, Wood R. Tuberculosis among HIV-infected patients receiving HAART: long term incidence and risk factors in a South African cohort. AIDS. 2005;19:2109-2116.
5. Dembélé M, Saleri N, Carvalho AC, et al. Incidence of tuberculosis after HAART initiation in a cohort of HIV-positive patients in Burkina Faso. Int J Tuberc Lung Dis. 2010;14:318-323.
6. Van Rie A, Westreich D, Sanne I. Tuberculosis in patients receiving antiretroviral treatment: incidence, risk factors, and prevention strategies. J Acquir Immune Defic Syndr. 2011;56:349-355.
7. Nicholas S, Sabapathy K, Ferreyra C, et al. Incidence of tuberculosis in HIV-infected patients before and after starting combined antiretroviral therapy in 8 sub-Saharan African HIV programs. J Acquir Immune Defic Syndr. 2011;57:311-318.
8. Kassa A, Teka A, Shewaamare A, et al. Incidence of tuberculosis and early mortality in a large cohort of HIV infected patients receiving antiretroviral therapy in a tertiary hospital in Addis Ababa, Ethiopia. Trans R Soc Trop Med Hyg. 2012;106:363-370.
9. Isanaka S, Aboud S, Mugusi F, et al. Iron status predicts treatment failure and mortality in tuberculosis patients: A prospective cohort study from Dar es Salaam, Tanzania. PLoS One. 2012;7:e37350.
10. Cegielski JP, Arab L, Cornoni-Huntley J. Nutritional risk factors for tuberculosis among adults in the United States, 1971-1992. Am J Epidemiol. 2012;176:409-422.
11. Shivakoti R, Yang WT, Gupte N, et al. Concurrent anemia and elevated C-Reactive protein predicts HIV clinical treatment failure, including tuberculosis, after antiretroviral therapy initiation. Clin Infect Dis. 2015; 61:102-110.
12. Boulle A, Schomaker M, May MT, et al. Mortality in patients with HIV-1 infection starting antiretroviral therapy in South Africa, Europe, orNorth America: A collaborative analysis of prospective studies. PLoS Med. 2014;11:e1001718.
13. Moore DM, Yiannoutsos CT, Musick BS, et al. Determinants of early and late mortality among HIV-infected individuals receiving home-based antiretroviral therapy in rural Uganda. J Acquir Immune Defic Syndr. 2011;58:289-296.
14. Wheelwright M, Kim EW, Inkeles MS, et al. All-trans retinoic acidtriggered antimicrobial activity against Mycobacterium tuberculosis is dependent on NPC2. J Immunol. 2014;192:2280-2290.
15. Webb AL, Villamor E. Update: effects of antioxidant and nonantioxidant vitamin supplementation on immune function. Nutr Rev. 2007;65:181-217.
16. Campbell GR, Spector SA. Vitamin D inhibits human immunodeficiency virus type 1 and Mycobacterium tuberculosis infection in macrophages through the induction of autophagy. PLoS Pathog. 2012;8:e1002689.
17. Cegielski JP, McMurray DN. The relationship between malnutrition and tuberculosis: evidence from studies in humans and experimental animals. Int J Tuberc Lung Dis. 2004;8:286-298.
18. McMurray DN, Bartow RA, Mintzer CL, et al. Micronutrient status and immune function in tuberculosis. Ann N Y Acad Sci. 1990;587:59-69.
19. Pakasi TA, Karyadi E, Wibowo Y, et al. Vitamin A deficiency and other factors associated with severe tuberculosis in timor and rote islands, east nusa tenggara province, Indonesia. Eur J Clin Nutr. 2009;63:1130-1135.
20. Mugusi FM, Rusizoka O, Habib N, et al. Vitamin A status of patients presenting with pulmonary tuberculosis and asymptomatic HIV-infected individuals, Dar es Salaam, Tanzania. Int J Tuberc Lung Dis. 2003;7: 804-807.
21. Ramachandran G, Santha T, Garg R, et al. Vitamin A levels in sputumpositive pulmonary tuberculosis patients in comparison with household contacts and healthy "normals". Int J Tuberc Lung Dis. 2004;8:1130-1133.
22. van Lettow M, Harries AD, Kumwenda JJ, et al. Micronutrient malnutrition and wasting in adults with pulmonary tuberculosis with and without HIV co-infection in Malawi. BMC Infect Dis. 2004;4:61.
23. Gibney KB, MacGregor L, Leder K, et al. Vitamin D deficiency is associated with tuberculosis and latent tuberculosis infection in immigrants from sub-Saharan Africa. Clin Infect Dis. 2008;46:443-446.
24. Nnoaham KE, Clarke A. Low serum vitamin D levels and tuberculosis: A systematic review and meta-analysis. Int J Epidemiol. 2008; 37:113-119.
25. Talat N, Perry S, Parsonnet J, et al. Vitamin d deficiency and tuberculosis progression. Emerg Infect Dis. 2010;16:853-855.
26. Banda R, Mhemedi B, Allain TJ. Prevalence of vitamin D deficiency in adult tuberculosis patients at a central hospital in Malawi. Int J Tuberc Lung Dis. 2011;15:408-410.
27. Zeng J, Wu G, Yang W, et al. A serum vitamin D level, 25 nmol/L pose high tuberculosis risk: A meta-analysis. PLoS One. 2015;10:e0126014.
28. Desai NS, Tukvadze N, Frediani JK, et al. Effects of sunlight and diet on vitamin D status of pulmonary tuberculosis patients in Tbilisi, Georgia. Nutrition. 2012;28:362-366.
29. Ho-Pham LT, Nguyen ND, Nguyen TT, et al. Association between vitamin D insufficiency and tuberculosis in a Vietnamese population. BMC Infect Dis. 2010;10:306.
30. Vijayamalini M, Manoharan S. Lipid peroxidation, vitamins C, E and reduced glutathione levels in patients with pulmonary tuberculosis. Cell Biochem Funct. 2004;22:19-22.
31. Madebo T, Lindtjørn B, Aukrust P, et al. Circulating antioxidants and lipid peroxidation products in untreated tuberculosis patients in Ethiopia. Am J Clin Nutr. 2003;78:117-122.
32. van Lettow M, West CE, van der Meer JW, et al. Low plasma selenium concentrations, high plasma human immunodeficiency virus load and high interleukin-6 concentrations are risk factors associated with anemia in adults presenting with pulmonary tuberculosis in Zomba district, Malawi. Eur J Clin Nutr. 2005;59:526-532.
33. Shivakoti R, Gupte N, Yang WT, et al. Pre-antiretroviral therapy serum selenium concentrations predict WHO stages 3, 4 or death but not virologic failure post-antiretroviral therapy. Nutrients. 2014;6:5061-5078.
34. Ramakrishnan K, Shenbagarathai R, Kavitha K, et al. Selenium levels in persons with HIV/tuberculosis in India, Madurai City. Clin Lab. 2012; 58:165-168.
35. Kassu A, Yabutani T, Mahmud ZH, et al. Alterations in serum levels of trace elements in tuberculosis and HIV infections. Eur J Clin Nutr. 2006; 60:580-586.
36. Shor-Posner G, Miguez MJ, Pineda LM, et al. Impact of selenium status on the pathogenesis of mycobacterial disease in HIV-1-infected drug users during the era of highly active antiretroviral therapy. J Acquir Immune Defic Syndr. 2002;29:169-173.
37. Campbell TB, Smeaton LM, Kumarasamy N, et al. Efficacy and safety of three antiretroviral regimens for initial treatment of HIV-1: A randomized clinical trial in diverse multinational settings. PLoS Med. 2012;9: e1001290.
38. Barlow WE, Ichikawa L, Rosner D, et al. Analysis of case-cohort designs. J Clin Epidemiol. 1999;52:1165-1172.
39. Onland-Moret NC, van der ADL, van der Schouw YT, et al. Analysis of case-cohort data: A comparison of different methods. J Clin Epidemiol. 2007;60:350-355.
40. Cai J, Zeng D. Sample size/power calculation for case-cohort studies. Biometrics. 2004;60:1015-1024.
41. Tenforde MW, Gupte N, Dowdy DW, et al. C-reactive protein (CRP), interferon gamma-inducible protein 10 (IP-10), and lipopolysaccharide (LPS) are associated with risk of tuberculosis after initiation of antiretroviral therapy in resource-limited settings. PLoS One. 2015;10: e0117424.
42. Semba RD, Graham NM, Caiaffa WT, et al. Increased mortality associated with vitamin A deficiency during human immunodeficiency virus type 1 infection. Arch Intern Med. 1993;153:2149-2154.
43. Baeten JM, Mostad SB, Hughes MP, et al. Selenium deficiency is associated with shedding of HIV-1-infected cells in the female genital tract. J Acquir Immune Defic Syndr. 2001;26:360-364.
44. Baum MK, Shor-Posner G, Lai S, et al. High risk of HIV-related mortality is associated with selenium deficiency. J Acquir Immune Defic Syndr Hum Retrovirol. 1997;15:370-374.
45. Jiang T, Christian P, Khatry SK, et al. Micronutrient deficiencies in early pregnancy are common, concurrent, and vary by season among rural Nepali pregnant women. J Nutr. 2005;135:1106-1112.
46. Thurnham DI, McCabe GP, Northrop-Clewes CA, et al. Effects of subclinical infection on plasma retinol concentrations and assessment of prevalence of vitamin A deficiency: meta-analysis. Lancet. 2003;362: 2052-2058.
47. Schulze KJ, Christian P, Wu LS, et al. Micronutrient deficiencies are common in 6-to 8-year-old children of rural Nepal, with prevalence estimates modestly affected by inflammation. J Nutr. 2014;144:979-987.
48. Thurnham DI, Mburu AS, Mwaniki DL, et al. Using plasma acute-phase protein concentrations to interpret nutritional biomarkers in apparently healthy HIV-1-seropositive Kenyan adults. Br J Nutr. 2008;100:174-182.
49. Shivakoti R, Christian P, Yang WT, et al. Prevalence and risk factors of micronutrient deficiencies pre-and post-antiretroviral therapy (ART) among a diverse multicountry cohort of HIV-infected adults. Clin Nutr. 2016;35:183-189.
50. Grobler L, Nagpal S, Sudarsanam TD, et al. Nutritional supplements for people being treated for active tuberculosis. Cochrane Database Syst Rev. 2016;CD006086.
51. Martineau AR. Old wine in new bottles: vitamin D in the treatment and prevention of tuberculosis. Proc Nutr Soc. 2012;71:84-89.
52. Villamor E, Mugusi F, Urassa W, et al. A trial of the effect of micronutrient supplementation on treatment outcome, T cell counts, morbidity, and mortality in adults with pulmonary tuberculosis. J Infect Dis. 2008;197:1499-1505.
53. Lahey T, Mackenzie T, Arbeit RD, et al. Recurrent tuberculosis risk among HIV-infected adults in Tanzania with prior active tuberculosis. Clin Infect Dis. 2013;56:151-158.
54. Golub JE, Durovni B, King BS, et al. Recurrent tuberculosis in HIVinfected patients in Rio de Janeiro, Brazil. AIDS. 2008;22:2527-2533.
55. Middelkoop K, Bekker LG, Shashkina E, et al. Retreatment tuberculosis in a South African community: The role of re-infection, HIV and antiretroviral treatment. Int J Tuberc Lung Dis. 2012;16:1510-1516.
56. Martineau AR, Nhamoyebonde S, Oni T, et al. Reciprocal seasonal variation in vitamin D status and tuberculosis notifications in Cape Town, South Africa. Proc Natl Acad Sci U S A. 2011;108:19013-19017.
57. Sudfeld CR, Giovannucci EL, Isanaka S, et al. Vitamin D status and incidence of pulmonary tuberculosis, opportunistic infections, and wasting among HIV-infected Tanzanian adults initiating antiretroviral therapy. J Infect Dis. 2013;207:378-385.
58. Facchini L, Venturini E, Galli L, et al. Vitamin D and tuberculosis: A review on a hot topic. J Chemother. 2015;27:128-138.
59. Owolabi O, Agbla S, Owiafe P, et al. Elevated serum 25-hydroxy (OH) vitamin D levels are associated with risk of TB progression in Gambian adults. Tuberculosis (Edinb). 2016;98:86-91.
60. Liu PT, Stenger S, Li H, et al. Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science. 2006; 311:1770-1773.
61. Yuk JM, Shin DM, Lee HM, et al. Vitamin D3 induces autophagy in human monocytes/macrophages via cathelicidin. Cell Host Microbe. 2009;6:231-243.
62. Anandaiah A, Sinha S, Bole M, et al. Vitamin D rescues impaired Mycobacterium tuberculosis-mediated tumor necrosis factor release in macrophages of HIV-seropositive individuals through an enhanced Tolllike receptor signaling pathway in vitro. Infect Immun. 2013;81:2-10.
63. Mehta S, Mugusi FM, Bosch RJ, et al. Vitamin D status and TB treatment outcomes in adult patients in Tanzania: A cohort study. BMJ Open. 2013;3:e003703.
64. Crowle AJ, Ross EJ. Inhibition by retinoic acid of multiplication of virulent tubercle bacilli in cultured human macrophages. Infect Immun. 1989;57:840-844.
65. Greenstein RJ, Su L, Brown ST. Vitamins A & D inhibit the growth of mycobacteria in radiometric culture. PLoS One. 2012;7:e29631.
66. Greenstein RJ, Su L, Shahidi A, et al. Unanticipated Mycobacterium tuberculosis complex culture inhibition by immune modulators, immune suppressants, a growth enhancer, and vitamins A and D: clinical implications. Int J Infect Dis. 2014;26:37-43.
67. Forman MR, Borkowf CB, Cantwell MM, et al. Components of variation in serum carotenoid concentrations: The Polyp Prevention Trial. Eur J Clin Nutr. 2009;63:763-770.
68. Shvetsov YB, Hernandez BY, Wong SH, et al. Intraindividual variability in serum micronutrients: effects on reliability of estimated parameters. Epidemiology. 2009;20:36-43.
69. Harvard School of Public Health. Trial of vitamin D in HIV progression (TOV4). Available at: https://clinicaltrials. gov/ct2/show/NCT01798680. Accessed September 7, 2016.
70. Queen Mary University of London. Trial of vitamin D supplementation in Cape Town primary school children (ViDiKids). Available at: https://clinicaltrials. gov/ct2/show/NCT02880982. Accessed September 7, 2016.