The effects of a lipid-based nutrient supplement and antiretroviral therapy in a randomized controlled trial on iron, copper, and zinc in milk from HIV-infected Malawian mothers and associations with maternal and infant biomarkers

Maternal and Child Nutrition

Volumn 14, Issue 2, 2018, Pages

  Hampel, Daniela ^a,b   Shahab Ferdows, Setareh ^a   Gertz, Erik ^a   Flax, Valerie L ^c   Adair, Linda S ^c   Bentley, Margaret E ^c   Jamieson, Denise J ^d   Tegha, Gerald ^e   Chasela, Charles S ^e,f   Kamwendo, Debbie ^e   van der Horst, Charles M ^g   Allen, Lindsay H ^a,b  

^a U S DEPARTMENT OF AGRICULTURE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c IL   (United States)

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

^e UNIVERSITY OF NORTH CAROLINA PROJECT   (Malawi)

^f UNIVERSITY OF THE WITWATERSRAND   (South Africa)

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

Author keywords

copper; haemoglobin status; HIV; human milk; iron; zinc

Indexed keywords

ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; BIOLOGICAL MARKER; COPPER; HEMOGLOBIN; IRON; LIPID; ZINC;

ADULT; BLOOD; BREAST FEEDING; BREAST MILK; CONTROLLED STUDY; DIETARY SUPPLEMENT; DRUG EFFECT; FEMALE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INFANT; INFLAMMATION; MALAWI; MALE; METABOLISM; MOTHER; NEWBORN; RANDOMIZED CONTROLLED TRIAL; YOUNG ADULT;

ADULT; ANTI-HIV AGENTS; BIOMARKERS; BREAST FEEDING; COPPER; DIETARY SUPPLEMENTS; FEMALE; HEMOGLOBINS; HIV INFECTIONS; HUMANS; INFANT; INFANT, NEWBORN; INFLAMMATION; IRON; LIPIDS; MALAWI; MALE; MILK, HUMAN; MOTHERS; YOUNG ADULT; ZINC;

EID: 85044251413     PISSN: 17408695     EISSN: 17408709     Source Type: Journal    
DOI: 10.1111/mcn.12503     Document Type: Article

References (66)

1. Adu-Afarwuah, S., Lartey, A., Okronipa, H., Ashorn, P., Zeilani, M., Peerson, J. M., … Dewey, K. G. (2015). Lipid-based nutrient supplement increases the birth size of infants of primiparous women in Ghana. American Journal of Clinical Nutrition, 101, 835–846.
2. Aggett, P. J., & Harries, J. T. (1979). Current status of zinc in health and disease states. Archives of Disease in Childhood, 54, 909–917.
3. Allen, L. H., Hampel, D., Shahab-Ferdows, S., York, E. R., Adair, L. S., Flax, V. L., … Benltey, M. E. (2015). Antiretroviral therapy provided to HIV-infected Malawian women in a randomized trial diminishes the positive effects of lipid-based nutrient supplements on breast-milk B vitamins. American Journal of Clinical Nutrition, 102, 1468–1476.
4. Beshgetoor, D., & Hambidge, M. (1998). Clinical conditions altering copper metabolism in humans. American Journal of Clinical Nutrition, 67(suppl.). 1017S-1021S
5. Black, R. E., Allen, L. H., Bhutta, Z. A., Caufield, L. E., de Onis, M., Ezzati, M., … Rivera, J. (2008). Maternal and child undernutrition: Global and regional exposures and health consequences. The Lancet, 371, 243–260.
6. Brown, K. H., Engle-Stone, R., Krebs, N. F., & Peerson, J. M. (2009). Dietary intervention strategies to enhance zinc nutrition: Promotion and support of breastfeeding for infants and young children. Food and Nutrition Bulletin, 30, S144–S171.
7. Chasela, C. S., Hudgens, M. G., Jamieson, D. J., Kayira, D., Hosseinipour, M. C., Kourtis, A. P., … Ahmed, Y. I. (2010). Maternal or infant antiretroviral drugs to reduce HIV-1 transmission. New England Journal of Medicine, 362, 2271–2281.
8. Childs, K., Welz, T., Samarawickrama, A., & Post, F. A. (2012). Effects of vitamin D deficiency and combination antiretroviral therapy on bone in HIV-positive patients. AIDS, 26, 253–262.
9. Corbett, A. H., Kayira, D., White, N. R., Davis, N. L., Kourtis, A. P., Chasela, C., … Kamwendo, D. (2014). Antiretroviral pharmacokinetics in mothers and breastfeeding infants from 6 to 24 weeks post partum: Results of the BAN Study. Antiviral Therapy, 19, 587–595.
10. Dauncy, M. J., Shaw, J. C. L., & Urman, J. (1977). The absorption and retention of magnesium, zinc, and copper by low birth weight infants fed pasteurized human breast milk. Pediatric Research, 11, 991–997.
11. de Pee, S., & Semba, R. D. (2010). Role of nutrition in HIV infection: Review of evidence for more effective programming in resource-limited settings. Food and Nutrition Bulletin, 31, 313S–344S.
12. Domellöf, M., Lönnerdal, B., Dewey, K. G., Cohen, R. J., & Hernell, O. (2004). Iron, zinc, and copper concentrations in breast milk are independent of maternal mineral status. American Journal of Clinical Nutrition, 79, 111–115.
13. Donangelo, C., Trugo, N., Koury, J., Barreto, S. M. I., Freitas, L., Feldheim, W., & Barth, C. (1989). Iron, zinc, folate and vitamin B12 nutritional status and milk composition of low-income Brazilian mothers. European Journal of Clinical Nutrtition, 43, 253–266.
14. Dorea, J. G. (2000). Iron and copper in human milk. Nutrition, 16, 209–220.
15. Duggan, C., Srinivasan, K., Thomas, T., Samuel, T., Rajendran, R., Muthayya, S., … Allen, L. H. (2014). Vitamin B-12 supplementation during pregnancy and early lactation increases maternal, breast milk, and infant measures of vitamin B-12 status. Journal of Nutrition, 144, 758–764.
16. Feeley, R. M., Eitenmiller, R., Jones, J., & Barnhart, H. (1983). Copper, iron, and zinc contents of human milk at early stages of lactation. American Journal of Clinical Nutrition, 37, 443–448.
17. Ferguson, Y. O., Eng, E., Bentley, M., Sandelowski, M., Steckler, A., Randall-David, E., … Soko, A. (2009). Evaluating nurses' implementation of an infant-feeding counseling protocol for HIV-infected mothers: The BAN study in Lilongwe, Malawi. AIDS Education and Prevention, 21, 141–155.
18. Finley, D. A., Lönnerdal, B., Dewey, K. G., & Grivetti, L. E. (1985). Inorganic constituents of breast milk from vegetarian and nonvegetarian women: Relationships with each other and with organic constituents. Journal of Nutrition, 115, 772–781.
19. Flax, V. L., Adair, L. S., Allen, L. H., Shahab-Ferdows, S., Hampel, D., Chasela, C. S., … Davis, N. L. (2015). Plasma micronutrient concentrations are altered by antiretroviral therapy and lipid-based nutrient supplements in lactating HIV-infected Malawian women. Journal of Nutrition, 145, 1950–1957.
20. Fransson, G. B., & Lönnerdal, B. (1980). Iron in human milk. Journal of Paediatrics, 96, 380–384.
21. Fransson, G. B., & Lönnerdal, B. (1982). Zinc, copper, calcium, and magnesium in human milk. Journal of Paediatrics, 101, 504–508.
22. Fransson, G. B., & Lönnerdal, B. (1984). Iron, copper, zinc, calcium, and magnesium in human milk fat. American Journal of Clinical Nutrition, 39, 185–189.
23. Gambling, L., Andersen, H. S., & McArdle, H. J. (2008). Iron and copper, and their interactions during development. Biochemical Society Transactions, 36, 1258–1261.
24. Gambling, L., Danzeisen, R., Gair, S., Lea, R. G., Charania, Z., Solanky, N., … McArdle, H. J. (2001). Effect of iron deficiency on placental transfer of iron and expression of iron transport proteins in vivo and in vitro. Biochemical Journal, 356, 883–889.
25. Gibson, R. S., & Huddle, J. M. (1998). Suboptimal zinc status in pregnant Malawian women: Its association with low intakes of poorly available zinc, frequent reproductive cycling, and malaria. American Journal of Clinical Nutrition, 67, 702–709.
26. Hirai, Y., Kawakata, N., Satoh, K., Ikeda, Y., Hisayasu, S., Orimo, H., & Yoshino, Y. (1990). Concentrations of lactoferrin and iron in human milk at different stages of lactation. Journal of Nutritional Science Vitaminology, 36, 531–544.
27. Institute of Medicine. (2001). Dietary reference intakes for vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium, and zinc. Washington DC. Free on-line book: National Academies Press.
28. Jobarteh, M. L., McArdle, H. J., Holtrop, G., Sise, E. A., Prentice, A. M., & Moore, S. E. (2017). mRNA levels of placental iron and zinc transporter genes are upregulated in Gambian women with low iron and zinc status. Journal of Nutrition. https://doi.org/10.3945/jn.116.244780
29. Kayira, D., Bentley, M. E., Wiener, J., Mkhomawanthu, C., King, C. C., Chitsulo, P., … Kourtis, A. P. (2012). A lipid-based nutrient supplement mitigates weight loss among HIV-infected women in a factorial randomized trial to prevent mother-to-child transmission during exclusive breastfeeding. American Journal of Clinical Nutrition, 95, 759–765.
30. Krebs, N. F., Hambidge, K., Jacobs, M., & Rasbach, J. O. (1985). The effects of a dietary zinc supplement during lactation on longitudinal changes in maternal zinc status and milk zinc concentrations. American Journal of Clinical Nutrition, 41, 560–570.
31. Kumar, A., Rai, A. K., Basu, S., Dash, D., & Singh, J. S. (2008). Cord blood and breast milk iron status in maternal anemia. Pediatrics, 121, e673–e677.
32. Linder, M. C., Wooten, L., Cerveza, P., Cotton, S., Shulze, R., & Lomeli, N. (1998). Copper transport. American Journal of Clinical Nutrition, 67, 965S–971S.
33. Lönnerdal, B., Hoffman, B., & &Hurley L. (1982). Zinc and copper binding proteins in human milk. American Journal of Clinical Nutrition, 36, 1170–1176.
34. Lönnerdal, B., Keen, C. L., & Hurley, L. S. (1981a). Iron, copper, zinc, and manganese in milk. Annual Review of Nutrition, 1, 149–174.
35. Lönnerdal, B., Keen, C., & Hurley, L. (1981b). Trace elements in milk from various species. In C. T. T. Howel Mc, J. M. Gawthorne, & C. L. White (Eds.), Trace element metabolism in man and animals (TEMA-4) (pp. 249–252). Canberra: Australian Academy of Science.
36. Mahdavi, R., Nikniaz, L., & Gayemmagami, S. J. (2010). Association between zinc, copper, and iron concentrations in breast milk and growth of healthy infants in Tabriz, Iran. Biological Trace Element Research, 135, 174–181.
37. McCormick, N. H., Hennigar, S. R., Kiselyov, K., & Kelleher, S. L. (2014). The biology of zinc transport in mammary epithelial cells: Implications for mammary gland development, lactation, and involution. Journal of Mammary Gland Biology and Neoplasia, 19, 59–71.
38. Mello-Neto, J., Rondó, P. H. C., Oshiiwa, M., Morgano, M. A., Zacari, C. Z., & dos Santos, M. L. (2013). Iron supplementation in pregnancy and breastfeeding and iron, copper and zinc status of lactating women from a human milk bank. Journal of Tropical Pediatrics, 59, 140–144.
39. Montalbetti, N., Dalghi, M. G., Albrecht, C., & Hediger, M. A. (2014). Nutrient transport in the mammary gland: Calcium, trace minerals and water soluble vitamins. Journal of Mammary Gland Biology and Neoplasia, 19, 73–90.
40. Moser, P. B., Reynolds, R. D., Acharya, S., Howard, M. P., Andon, M., & Lewis, S. (1988). Copper, iron, zinc, and selenium dietary intake and status of Nepalese lactating women and their breast-fed infants. American Journal of Clinical Nutrition, 47, 729–734.
41. Murray, M., Murray, A. B., Murray, N., & Murray, M. B. (1978). The effect of iron status of Nigerien mothers on that of their infants at birth and 6 months, and on the concentration of Fe in breast milk. British Journal of Nutrition, 39, 627–630.
42. Nakamori, M., Ninh, N. X., Isomura, H., Yodshiike, N., Hien, V. T. T., Nhug, B. T., … Yamamoto, S. (2009). Nutritional status of lactating mothers and their breast milk concentration of iron, zinc and copper in rural Vietnam. Journal of Nutritional Science and Vitaminology, 55, 338–345.
43. National Statistical Office (NSO) [Malawi] and ICF. (2017). Malawi demographic and health survey 2015–16. Zomba, Malawi, and Rockville, MD, USA.
44. Paltiel, O., Falutz, J., Veilleux, M., Rosenblatt, D. S., & Gordon, K. (1995). Clinical correlates of subnormal vitamin B12 levels in patients infected with the human immunodeficiency virus. American Journal of Hematology, 49, 318–322.
45. Phuka, J. C., Maleta, K., Thakwalakwa, C., Cheung, Y. B., Briend, A., Manary, M. J., & Ashorn, P. (2009). Postintervention growth of Malawian children who received 12-mo dietary complementation with a lipid-based nutrient supplement or maize-soy flour. American Journal of Clinical Nutrition, 89, 382–390.
46. Picciano, M. F. (2001). Nutrient composition of human milk. Pediatric Clinics of North America, 48, 53–67.
47. Picciano, M. F., & Guthrie, H. A. (1976). Copper, iron, and zinc contents of mature human milk. American Journal of Clinical Nutrition, 29, 242–254.
48. Prado, E. L., Phuka, J., Maleta, K., Ashorn, P., Ashorn, U., Vosti, S. A., & Dewey, K. G. (2016). Provision of lipid-based nutrient supplements from age 6 to 18 months does not affect infant development scores in a randomized trial in Malawi. Maternal and Child Health Journal. https://doi.org/10.1007/s10995-016-2061-6
49. Shahab-Ferdows, S., Engle-Stone, R., Hampel, D., Ndjebayi, A. O., Nankap, M., Brown, K. H., & Allen, L. H. (2015). Regional, socioeconomic, and dietary risk factors for vitamin B-12 deficiency differ from those for folate deficiency in Cameroonian women and children. Journal of Nutrition, 145, 2587–2595.
50. Shapiro, R. L., Holland, D. T., Capparelli, E., Lockman, S., Thior, I., Wester, C., … Connor, J. D. (2005). Antiretroviral concentrations in breast-feeding infants of women in Botswana receiving antiretroviral treatment. Journal of Infectious Diseases, 192, 720–727.
51. Siddiqua, T. J., Ahmad, S. M., Ahsan, K. B., Rashid, M., Roy, A., Rahman, S. M., … Allen, L. H. (2016). Vitamin B12 supplementation during pregnancy and postpartum improves B12 status of both mothers and infants but vaccine response in mothers only: A randomized clinical trial in Bangladesh. European Journal of Nutrition, 55, 281–293.
52. Silvestre, D., Martìnez-Costa, C., Lagarda, M. J., Brines, J., Farré, R., & Clemente, G. (2001). Copper, iron, and zinc contents in human milk during the first three months of lactation. Biological Trace Element Research, 80, 1–11.
53. Thakwalakwa, C., Ashorn, P., Phuka, J., Cheung, Y. B., Briend, A., Puumalainen, T., & Maleta, K. (2010). A lipid-based nutrient supplement but not corn-soy blend modestly increases weight gain among 6-to 18-month-old moderately underweight children in rural Malawi. Journal of Nutrition, 140, 2008–2013.
54. Thurnham, D. I., Mburu, A. S., Mwaniki, D. L., Muniu, E. M., Alumasa, F., & de Wagt, A. (2008). Using plasma acute-phase protein concentrations to interpret nutritional biomarkers in apparently healthy HIV-1-seropositive Kenyan adults. British Journal of Nutrition, 100, 174–182.
55. Van den Broek, N. R., & Letsky, E. A. (2000). Etiology of anemia in pregnancy in south Malawi. American Journal of Clinical Nutrition, 72(suppl), 247S–256S.
56. van der Horst, C., Chasela, C., Ahmed, Y., Hoffman, I., Hosseinipour, M., Knight, R., … Bentley, M. (2009). 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. Contemporary Clinical Trials, 30, 24–33.
57. Vuori, E., Mäkinen, S., Kara, R., & Kuitunen, P. (1980). The effects of the dietary intakes of copper, iron, manganese, and zinc on the trace element content of human milk. American Journal of Clinical Nutrition, 33, 227–231.
58. Whitfield, K. C., Karakochuk, C. D., Kroeun, H., Hampel, D., Sokhoing, L., Chan, B. B., … Green, T. J. (2016). Perinatal consumption of thiamine-fortified fish sauce in rural Cambodia. JAMA Pediatrics, 170. e162065. https://doi.org/10.1001/jamapediatrics.2016.2065
59. Widen, E. M., Bentley, M. E., Kayira, D., Chasela, C. S., Daza, E. J., Kacheche, Z. K., … van der Horst, C. M. (2014). Changes in soluble transferrin receptor and hemoglobin concentrations in Malawian mothers are associated with those values in their exclusively breastfed, HIV-exposed infants. Journal of Nutrition, 144, 367–373.
60. Woods, M. N., Tang, A. M., Forrester, J., Jones, C., Hendricks, K., Ding, B., & Knox, T. A. (2003). Effect of dietary intake and protease inhibitors on serum vitamin B12 levels in a cohort of human immunodeficiency virus—Positive patients. Clinical Infectious Diseases, 37, S124–S131.
61. Wooten, L., Shulze, R. A., Lancey, R. W., Lietzow, M., & Linder, M. C. (1996). Ceruloplasmin is found in milk and amniotic fluid and may have a nutritional role. Journal of Nutritional Biochemistry, 7, 632–639.
62. World Health Organization. (2003). HIV and infant feeding: Guidelines for decision-makers. Geneva: World Health Organization.
63. World Health Organization. (2010). Guidelines on HIV and infant feeding 2010: Principles and recommendations for infant feeding in the context of HIV and a summary of evidence. Geneva: WHO.
64. World Health Organization. (2011). Haemoglobin concentrations for the diagnosis of anaemia and assessment of severity. Geneva: World Health Organization.
65. World Health Organization. (2016). Guideline: Updates on HIV and infant feeding: The duration of breastfeeding and support from health services to improve feeding practices among mothers living with HIV. Geneva: WHO.
66. Zeh, C., Weidle, P. J., Nafisa, L., Lwamba, H. M., Okonji, J., Anyango, E., … Nkengasong, J. N. (2011). HIV-1 drug resistance emergence among breastfeeding infants born to HIV-infected mothers during a single-arm trial of triple-antiretroviral prophylaxis for prevention of mother-to-child transmission: A secondary analysis. PLoS Medicine, 8. e1000430