Plasma micronutrient concentrations are altered by antiretroviral therapy and lipid-based nutrient supplements in lactating HIV-infected Malawian women

Journal of Nutrition

Volumn 145, Issue 8, 2015, Pages 1950-1957

  Flax, Valerie L ^a,b,i   Adair, Linda S ^a,b,i   Allen, Lindsay H ^e   Shahab Ferdows, Setarah ^e   Hampel, Daniela ^e   Chasela, Charles S ^f,g,i   Tegha, Gerald ^f   Daza, Eric J ^b   Corbett, Amanda ^c   Davis, Nicole L ^b   Kamwendo, Deborah ^f   Kourtis, Athena P ^h   van der Horst, Charles M ^d   Jamieson, Denise J ^h   Bentley, Margaret E ^a,b,i   Ahmed, Yusuf ⁱ   Ait Khaled, Mounir ⁱ   Albrecht, Sandra ⁱ   Bangdiwala, Shrikant ⁱ   Bayer, Ronald ⁱ   Bramson, Brian ⁱ   Bobrow, Emily ⁱ   Boyle, Nicola ⁱ   Butera, Sal ⁱ   Chavula, Charity ⁱ   Chimerang'ambe, Joseph ⁱ   Chigwenembe, Maggie ⁱ   Chikasema, Maria ⁱ   Chikhungu, Norah ⁱ   Chilongozi, David ⁱ   Chiudzu, Grace ⁱ   Chome, Lenesi ⁱ   Cole, Anne ⁱ   Corneli, Amy ⁱ   Dow, Anna ⁱ   Duerr, Ann ⁱ   Eliya, Henry ⁱ   Ellington, Sascha ⁱ   Eron, Joseph ⁱ   Farr, Sherry ⁱ   Ferguson, Yvonne Owens ⁱ   Fiscus, Susan ⁱ   Fokar, Ali ⁱ   Galvin, Shannon ⁱ   Guay, Laura ⁱ   Heilig, Chad ⁱ   Hoffman, Irving ⁱ   Hooten, Elizabeth ⁱ   Hosseinipour, Mina ⁱ   Hudgens, Michael ⁱ   Hurst, Stacy ⁱ   Hyde, Lisa ⁱ   Jamieson, Denise ⁱ   Joaki, George ⁱ   Jones, David ⁱ   Jordan Bell, Elizabeth ⁱ   Kacheche, Zebrone ⁱ   Kamanga, Esmie ⁱ   Kamanga, Gift ⁱ   Kampani, Coxcilly ⁱ   Kamthunzi, Portia ⁱ   Kanyama, Cecilia ⁱ   Kashuba, Angela ⁱ   Kathyola, Damson ⁱ   Kayira, Dumbani ⁱ   Kazembe, Peter ⁱ   King, Caroline C ⁱ   Knight, Rodney ⁱ   Krysiak, Robert ⁱ   Kumwenda, Jacob ⁱ   Lee, Hana ⁱ   Loeliger, Edde ⁱ   Long, Dustin ⁱ   Luhanga, Misheck ⁱ   Madhlopa, Victor ⁱ   Majawa, Maganizo ⁱ   Maida, Alice ⁱ   Marcus, Cheryl ⁱ   Martinson, Francis ⁱ   Thoofer, Navdeep ⁱ   Matiki, Chrissie ⁱ   Mayers, Douglas ⁱ   Mayuni, Isabel ⁱ   McDonough, Marita ⁱ   Meme, Joyce ⁱ   Merry, Ceppie ⁱ   Mita, Khama ⁱ   Mkomawanthu, Chimwemwe ⁱ   Mndala, Gertrude ⁱ   Mndala, Ibrahim ⁱ   Moses, Agnes ⁱ   Msika, Albans ⁱ   Msungama, Wezi ⁱ   Mtimuni, Beatrice ⁱ   Muita, Jane ⁱ   Mumba, Noel ⁱ   Musis, Bonface ⁱ   Mwansambo, Charles ⁱ   Mwapasa, Gerald ⁱ   Nkhoma, Jacqueline ⁱ   Parker, Megan ⁱ   Pendame, Richard ⁱ   Piwoz, Ellen ⁱ   Raines, Byron ⁱ   Ramdas, Zane ⁱ   Rublein, John ⁱ   Ryan, Mairin ⁱ   Sanne, Ian ⁱ   Sellers, Christopher ⁱ   Shugars, Diane ⁱ   Sichali, Dorothy ⁱ   Snowden, Wendy ⁱ   Soko, Alice ⁱ   Spensley, Allison ⁱ   Steens, Jean Marc ⁱ   Tembo, Martin ⁱ   Thomas, Roshan ⁱ   Tien, Hsiao Chuan ⁱ   Tohill, Beth ⁱ   van der Horst, Charles ⁱ   Waalberg, Esther ⁱ   Widen, Elizabeth ⁱ   Wiener, Jeffrey ⁱ   Wilfert, Cathy ⁱ   Wiyo, Patricia ⁱ   Zgambo, Innocent ⁱ   Zimba, Chifundo ⁱ   more..

^a UNIVERSITY OF NORTH CAROLINA AT CHAPEL HILL   (United States)

^b University of North Carolina at Chapel Hill   (United States)

^c UNC Hamner Institute for Drug Safety Sciences   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^e AGRICULTURAL RESEARCH SERVICE   (United States)

^f UNIVERSITY OF NORTH CAROLINA PROJECT   (Malawi)

^g UNIVERSITY OF THE WITWATERSRAND   (South Africa)

^h CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

ⁱ NONE

Author keywords

Highly active antiretroviral therapy; HIV mothers; Lipid based nutrient supplements; Micronutrient

Indexed keywords

CYANOCOBALAMIN; FERRITIN; FOLIC ACID; HEMOGLOBIN; RETINOL BINDING PROTEIN; SELENIUM; TRACE ELEMENT; TRANSFERRIN RECEPTOR; ANTIRETROVIRUS AGENT; LIPID;

ADULT; ARTICLE; BLOOD SAMPLING; BODY MASS; CD4 LYMPHOCYTE COUNT; COMPARATIVE STUDY; CONTROLLED STUDY; FEMALE; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LABORATORY TEST; LACTATION; MAJOR CLINICAL STUDY; MALAWIAN; MEDICATION COMPLIANCE; NUTRIENT; PREGNANT WOMAN; RANDOMIZED CONTROLLED TRIAL; VIRUS LOAD; VITAMIN SUPPLEMENTATION; BLOOD; CHEMISTRY; DIET SUPPLEMENTATION; HIV INFECTIONS; MALAWI; MALE; YOUNG ADULT;

ADULT; ANTI-RETROVIRAL AGENTS; ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; DIETARY SUPPLEMENTS; FEMALE; HIV INFECTIONS; HUMANS; LIPIDS; MALAWI; MALE; MICRONUTRIENTS; YOUNG ADULT;

EID: 84938906963     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.115.212290     Document Type: Article

References (63)

1. WHO. Consolidated guidelines on the use of antiretroviral drugs for treating and preventing HIV infection: recommendations for a public health approach June 2013. Geneva (Switzerland): WHO; 2013.
2. WHO. Use of antiretroviral drugs for treating pregnant women and preventing HIV infections in infants: executive summary. Geneva (Switzerland): WHO; 2012.
3. UNAIDS. Global report: UNAIDS report on the global AIDS epidemic 2013. Geneva (Switzerland): Joint United Nations Programme on HIV/AIDS (UNAIDS); 2013.
4. Baum MK, Shor-Posner G, Zhang G, Lai H, Quesada JA, Campa A, Jose-Burbano M, Fletcher MA, Sauberlich H, Page JB. HIV-1 infection in women is associated with severe nutritional deficiencies. J Acquir Immune Defic Syndr Hum Retrovirol 1997;16:272-8.
5. Tang AM, Graham NM, Semba RD, Saah AJ. Association between serum vitamin A and E levels and HIV-1 disease progression. AIDS 1997;11:613-20.
6. Friis H. Micronutrient interventions and HIV infection: a review of current evidence. Trop Med Int Health 2006;11:1849-57.
7. Campa A, Baum MK. Micronutrients and HIV infection. HIV Ther 2010;4:437-69.
8. Semba RD, Shah N, Vlahov D. Improvement of anemia among HIVinfected injection drug users receiving highly active antiretroviral therapy. J Acquir Immune Defic Syndr 2001;26:315-9.
9. Semba RD, Shah N, Klein RS, Mayer KH, Schuman P, Gardner LI, Vlahov D. Highly active antiretroviral therapy associated with improved anemia among HIV-infected women. AIDS Patient Care STDS 2001;15:473-80.
10. Moore RD, Forney D. Anemia in HIV-infected patients receiving highly active antiretroviral therapy. J Acquir Immune Defic Syndr 2002; 29:54-7.
11. Jones CY, Tang AM, Forrester JE, Huang J, Hendricks KM, Knox TA, Spiegelman D, Semba RD, Woods MN. Micronutrient levels and HIV disease status in HIV-infected patients on highly active antiretroviral therapy in the Nutrition for Healthy Living cohort. J Acquir Immune Defic Syndr 2006;43:475-82.
12. Rousseau MC, Molines C, Moreau J, Delmont J. Influence of highly active antiretroviral therapy on micronutrient profiles in HIV-infected patients. Ann Nutr Metab 2000;44:212-6.
13. Allavena C, Delpierre C, Cuzin L, Rey D, Viget N, Bernard J, Guillot P, Duvivier C, Billaud E, Raffi F. High frequency of vitamin D deficiency in HIV-infect patients: effects of HIV-related factors and antiretroviral drugs. J Antimicrob Chemother 2012;67:2222-30.
14. Havers FP, Detrick B, Cardoso SW, Berendes S, Lama JR, Sungandhavesa P, Mwelase NH, Campbell TB, Gupta A; ACTG A5175 PEARLS and NWCS319 Study Teams. Change in vitamin D levels occurs early after antiretroviral therapy initation and depends on treatment regimen in resource-limited settings. PLoS ONE 2014;9:e95164.
15. Paltiel O, Falutz J, Veilleux M, Rosenblatt DS, Gordon K. Clinical correlates of subnormal vitamin B12 concentrations in patients infected with the human immunodeficiency virus. Am J Hematol 1995;49:318-22.
16. Woods MN, Tang AM, Forester J, Jones C, Hendricks K, Ding B, Knox TA. Effect of dietary intake and protease inhibitors on serum vitamin B12 levels in a cohort of human immunodeficiency virus-positive patients. Clin Infect Dis 2003;37(Suppl 2):S124-31.
17. Fawzi WW, Msamanga GI, Kupka R, Spiegelman D, Villamor E, Mugusi F, Wei R, Hunter D. Multivitamin supplementation improves hematologic status in HIV-infected women and their children in Tanzania. Am J Clin Nutr 2007;85:1335-43.
18. Fawzi WW, Villamor E, Msamanga GI, Antelman G, Aboud S, Urassa W, Hunter D. Trial of zinc supplements in relation to pregnancy outcomes, hematologic indicators, and T cell counts among HIV-1-infected women in Tanzania. Am J Clin Nutr 2005;81:161-7.
19. Hurwitz BE, Klaus JR, Llabre MM, Gonzalez A, Lawrence PJ, Maher KJ, Greeson JM, Baum MK, Shor-Posner G, Skyler JS, et al. Suppression of human immunodeficiency virus type 1 viral load with selenium supplementation: a randomized controlled trial. Arch Intern Med 2007;167:148-54.
20. Allard JP, Aghdassi E, Chau J, Tam C, Kovacs CM, Salit IE, Walmsley SL. Effects of vitamin E and C supplementation on oxidative stress and viral load in HIV-infected subjects. AIDS 1998;12:1653-9.
21. Austin J, Singhal N, Voigt R, Smaill F, Gill MJ, Walmsley S, Salit I, Gilmour J, Schlech WF 3rd, Choudhri S, et al. A community randomized controlled clinical trial of mixed carotenoids and micronutrient supplementation of patients with acquired immunodeficiency syndrome. Eur J Clin Nutr 2006;60:1266-76.
22. Baeten JM, McClelland RS, Overbaugh J, Richardson BA, Emery S, Lavreys L, Mandaliya K, Bankson DD, Ndinya-Achola JO, Bwayo JJ, et al. Vitamin A supplementation and human immunodeficiency virus type 1 shedding in women: results of a randomized clinical trial. J Infect Dis 2002;185:1187-91.
23. Fawzi WW, Msamanga GI, Spiegelman D, Urassa EJ, McGrath N, Mwakagile D, Antelman G, Mbise R, Herrera G, Kapiga S, et al. Randomised trial of effects of vitamin supplements on pregnancy outcomes and T cell counts in HIV-1-infected women in Tanzania. Lancet 1998;351:1477-82.
24. Jiamton S, Pepin J, Suttent R, Filteau S, Mahakkanukrauh B, Hanshaoworakul W, Chaisilwattana P, Suthipinittharm P, Shetty P, Jaffar S. A randomized trial of the impact of multiple micornutrient supplementation on mortality among HIV-infected individuals living in Bangkok. AIDS 2003;17:2461-9.
25. Semba RD, Ricketts EP,Mehta S, Netski D, Thomas D, Kirk G,Wu AW, Vlahov D. Effect of micronutrients and iron supplementation on hemoglobin, iron status, and plasma hepatitis C and HIV RNA levels in female injection drug users: a controlled clinical trial. J Acquir Immune Defic Syndr 2007;45:298-303.
26. van der Horst C, Chasela C, Ahmed Y, Hoffman I, Hosseinipour M, Knight R, Fiscus S, Hudgens M, Kazembe P, Bentley M, et al. Modifications of a large HIV prevention clinical trial to fit changing realities: a case study of the Breastfeeding, Antiretroviral, and Nutrition (BAN) protocol in Lilongwe, Malawi. Contemp Clin Trials 2009;30:24-33.
27. Flax VL, Bentley ME, Chasela CS, Kayira D, Hudgens MG, Knight RJ, Soko A, Jamieson DJ, van der Horst CM, Adair LS. Use of lipid-based nutrient supplements by HIV-infected Malawian women during lactation has no effect on infant growth from 0-24 weeks. J Nutr 2012;142:1350-6.
28. Institute of Medicine. Dietary Reference Intakes for thiamin, riboflavin, niacin, vitamin B6, folate, vitamin B12, pantothenic acid, biotin, and choline. Washington (DC): National Academies Press; 1998.
29. Institute of Medicine. Dietary Reference Intakes for vitamin C, vitamin E, selenium, and carotenoids. Washington (DC): National Academies Press; 2000.
30. Institute of Medicine. Dietary Reference Intakes for vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium, and zinc.Washington (DC): National Academies Press; 2001.
31. Fawzi WW, Msamanga GI, Hunter D, Renjifo B, Antelman G, Bang H, Manji K, Kapiga S, Mwakagile D, Essex M, et al. Randomized trial of vitamin supplements in relation to transmission of HIV-1 through breastfeeding and early child mortality. AIDS 2002;16:1935-44.
32. Chasela CS, Hudgens MG, Jamieson DJ, Kayira D, Hosseinipour MC, Kourtis AP, Martinson F, Tegha G, Knight RJ, Ahmed YI, et al. Maternal or infant antiretroviral drugs to reduce HIV-1 transmission. N Engl J Med 2010;362:2271-81.
33. AIDSMAP. Protease inhibitors (PIs). 2014 [cited 2015 Feb 6]. Available from: http://www.aidsmap.com/page/1060148.
34. Thurnham DI, McCabe GP. Influence of infection and inflammation on biomarkers of nutritional status with an emphasis on vitamin A and iron. Geneva (Switzerland): WHO; 2012.
35. Vilaseca MA, Sierra C, Colome C, Artuch R, Valls C, Munos-Almagro C, Vilches M-A, Fortuny C. Hyperhomocysteinaemia and folate deficiency in human immunodeficiency virus-infected children. Eur J Clin Invest 2001;31:992-8.
36. Coria-Ramirez E, Cisneros LN, Trevino-Perez S, Ibarra-Gonzalez I, Casillas-Rodriguez J, Majluf-Cruz A. Effect of highly active antiretroviral therapy on homocysteine plasma concentrations in HIV-1-infected patients. J Acquir Immune Defic Syndr 2010;54:477-81.
37. Wu X, Sun L, Zha W, Studer E, Gurley E, Chen L, Wang X, Hylemon PB, Pandak WM Jr., Sanyal AJ, et al. HIV protease inhibitors induce endoplasmic reticulum stress and disrupt barrier integrity in intestinal epithelial cells. Gastroenterology 2010;138:197-209.
38. Cahn P, Andrade-Villanueva J, Arribas JR, Gatell JM, Lama JR, Norton M, Patterson P, Madero JS, Sued O, Figueroa MI, et al. Dual therapy with lopinavir and ritonavir plus lamivudine versus triple therapy with lopinavir and ritonavir plus two nucleoside reverse transcriptase inhibitors in antiretroviral-therapy-naive adults with HIV-1 infection: 48 week results of the randomised, open label, non-inferiority GARDEL trial. Lancet Infect Dis 2014;14:572-80.
39. Drain PK, Kupka R, Mugusi F, Fawzi WW. Micronutrients in HIVpositive persons receiving highly active antiretroviral therapy. Am J Clin Nutr 2007;85:333-45.
40. Weiss J, Theile D, Ketabi-Kiyanvash N, Lindenmaier H, Haefeli WE. Inhibition of MRP1/ABCC1, MRP2/ABCC2, and MRP3/ABCC3 by nucleoside, nucleotide, and non-nucleoside reverse transcriptase inhibitors. Drug Metab Dispos 2007;35:340-4.
41. Bernasconi E, UhrM, Magenta L, Ranno A, Telenti A. Homocysteinaemia in HIV-infected patients treated with highly active antiretroviral therapy. AIDS 2001;15:1081-2.
42. Deminice R, Vassimon HS, Machado AA, de Paula FJA, Monteiro JP, Jordao AA. Plasma homocysteine levels in HIV-infected men with and without lipodystrophy. Nutrition 2013;29:1326-30.
43. Uccelli MC, Torti C, Lapadula G, Labate L, Cologni G, Tirelli V, Moretti F, Costarelli S, Quiros-Roldan E, Carosi G. Influence of folate serum concentration on plasma homocysteine levels in HIV-positive patients exposed to protease inhibitors undergoing HAART. Ann Nutr Metab 2006;50:247-52.
44. Bongiovanni M, Casana M, Pisacreta M, Tordato F, Cicconi P, Russo U, Ranieri R, Monforte A, Bini T. Predictive factors of hyperhomocysteinemia in HIV-positive patients. J Acquir Immune Defic Syndr 2007;44:117-9.
45. Raiszadeh F, Hoover DR, Lee I, Shi A, Anastos K, Gao W, Kaplan R, Glesby MJ. Plasma homocysteine is not associated with HIV serostatus or antiretroviral therapy in women. J Acquir Immune Defic Syndr 2009;51:175-8.
46. Ndeezi G, Tumwine JK, Ndugwa CM, Bolann BJ, Tylleskar T. Multiple micronutrient supplementation improves vitamin B12 and folate concentrations of HIV infected children in Uganda: a randomized controlled trial. Nutr J 2011;10:56.
47. Remacha AF, Cadafalch J. Cobalamin deficiency in patients infected with the human immunodeficiency virus. Semin Hematol 1999;36:75-87.
48. Remacha AF, Cadafalch J, Sarda P, Barcelo M, Fuster M. Vitamin B-12 metabolism in HIV-infected patients in the age of highly active antiretroviral therapy: role of homocysteine in assessing vitamin B-12 status. Am J Clin Nutr 2003;77:420-4.
49. Baeten JM, Richardson BA, Bankson DD, Wener MH, Kriess JK, Lavreys L, Mandaliya K, Bwayo JJ, McClelland RS. Use of serum retinol-binding protein for prediction of vitamin A deficiency: effects of HIV-1 infection, protein malnutrition, and the acute phase response. Am J Clin Nutr 2004;79:218-25.
50. Toma E, Devost D, Chow Lan N, Bhat PV. HIV-protease inhibitors alter retinoic acid synthesis. AIDS 2001;15:1979-84.
51. Tang AM, Smit E, Semba RD, Shah N, Lyles CM, Li D, Vlahov D. Improved antioxidant status among HIV-infected injecting drug users on potent antiretroviral therapy. J Acquir Immune Defic Syndr 2000;23:321-6.
52. Kaio DJ, Rondo PHC, Souza JMP, Firmino AV, Luzia LA, Segurado AA. Vitamin A and beta-carotene concentrations in adults with HIV/AIDS on highly active antiretroviral therapy. J Nutr Sci Vitaminol (Tokyo) 2013;59:496-502.
53. Skikne BS. Serum transferrin receptor. Am J Hematol 2008;83:872-5.
54. Noé G, Augustin J, Hausdorf S, Rich IN, Kubanek B. Serum erythropoietin and transferrin receptor levels in patients with rheumatoid arthritis. Clin Exp Rheumatol 1995;13:445-51.
55. Widen EM, Bentley ME, Chasela CS, Kayira D, Flax VL, Kourtis AP, Ellington SR, Kacheche Z, Tegha G, Jamieson DJ, et al. Antiretroviral treatment is associated with iron deficiency in HIV-infected Malawian women that is mitigated with supplementation, but is not associated with infant iron deficiency during 24 weeks of exclusive breastfeeding. J Acquir Immune Defic Syndr 2015;69:319-28.
56. Berhane K, Karim R, Cohen MH, Masri-Lavine L, Young M, Anastos K, Augenbraun M, Watts DH, Levine AM. 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 2004;37:1245-52.
57. Johannessen A, Naman E, Gundersen SG, Bruun JN. Antiretroviral treatment reverses HIV-associated anemia in rural Tanzania. BMC Infect Dis 2011;11:190.
58. Takuva S, Maskew M, Brennan AT, Sanne I, MacPhail AP, Fox MP. 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;2013:162950.
59. Richman DD, Fischl MA, Grieco MH, Gottlieb MS, Volberding PA, Laskin OL, Leedom JM, Groopman JE,Mildvan D. The toxicity of azidothymidine AZT in the treatment of patients with AIDS and AIDS-related complex: a double-blind placebo-controlled trial. N Engl J Med 1987;317:192-7.
60. Renaud-Thery F, Avila-Figueroa C, Stover J, Thierry S, Vitoria M, Habiyambere V, Souteyrand Y. Utilization patterns and projected demand of antiretroviral drugs in low-and middle-income countries. AIDS Res Treat 2011;2011:749041.
61. Friis H, Gomo E, Koestel P, Ndhlovu P, Nyazema N, Krarup H, Michaelsen KF. HIV and other predictors of serum folate, serum ferritin, and hemoglobin in pregnancy: a cross-sectional study in Zimbabwe. Am J Clin Nutr 2001;73:1066-73.
62. Papathakis PC, Rollins NC, Chantry CJ, Bennish ML, Brown KH. Micronutrient status during lactation in HIV-infected and HIVuninfected South African women during the first 6 mo after delivery. Am J Clin Nutr 2007;85:182-92.
63. Kupka R, Msamanga GI, Mugusi F, Petraro P, Hunter DJ, Fawzi WW. Iron status is an important cause of anemia in HIV-infected Tanzanian women but is not related to accelerated HIV disease progression. J Nutr 2007;137:2317-23.