Maternal HIV infection influences the microbiome of HIV-uninfected infants

Science Translational Medicine

Volumn 8, Issue 349, 2016, Pages

  Bender, Jeffrey M ^a,b   Li, Fan ^a   Martelly, Shoria ^c   Byrt, Erin ^d,e   Rouzier, Vanessa ^c   Leo, Marguerite ^c   Tobin, Nicole ^a   Pannaraj, Pia S ^a,b   Adisetiyo, Helty ^a   Rollie, Adrienne ^a   Santiskulvong, Chintda ^a   Wang, Shaun ^d   Autran, Chloe ^f   Bode, Lars ^f   Fitzgerald, Daniel ^e   Kuhn, Louise ^d   Aldrovandi, Grace M ^a,b  

^a CHILDREN S HOSPITAL LOS ANGELES   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

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

^d Columbia University ^*  (United States)

^e WEILL CORNELL MEDICAL COLLEGE   (United States)

^f UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; ANTIRETROVIRUS AGENT; COTRIMOXAZOLE; OLIGOSACCHARIDE;

AGED; ARTICLE; BACTERIAL STRAIN; BREAST MILK; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INFANT; INFANT DISEASE; INFANT MORTALITY; MALE; MATERNAL DISEASE; MICROBIOME; MORBIDITY; NONHUMAN; ORGANISMAL INTERACTION; PRIORITY JOURNAL; RISK FACTOR; BREAST FEEDING; CHEMISTRY; CROSS-SECTIONAL STUDY; METABOLISM; MICROBIOLOGY; MICROFLORA; MOTHER; NEWBORN; PHYSIOLOGY; PREGNANCY; PREGNANCY COMPLICATION; PROSPECTIVE STUDY; TRANSMISSION; VERTICAL TRANSMISSION;

BREAST FEEDING; CROSS-SECTIONAL STUDIES; FEMALE; HIV INFECTIONS; HUMANS; INFANT, NEWBORN; INFECTIOUS DISEASE TRANSMISSION, VERTICAL; MICROBIOTA; MILK, HUMAN; MOTHERS; OLIGOSACCHARIDES; PREGNANCY; PREGNANCY COMPLICATIONS, INFECTIOUS; PROSPECTIVE STUDIES; RISK FACTORS;

EID: 84980002150     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aaf5103     Document Type: Article

References (48)

1. Joint United Nations Programme on HIV/AIDS, The Gap Report (UNAIDS, Geneva, Switzerland, 2014); http://www.unaids.org/en/resources/documents/2014/20140716-UNAIDS-gap-report.
2. C. von Mollendorf, A. von Gottberg, S. Tempia, S. Meiring, L. de Gouveia, V. Quan, S. Lengana, T. Avenant, N. du Plessis, B. Eley, H. Finlayson, G. Reubenson, M. Moshe, K. L. O'Brien, K. P. Klugman, C. G. Whitney, C. Cohen, Increased risk for and mortality from invasive pneumococcal disease in HIV-exposed but uninfected infants aged. Clin. Infect. Dis.60,1346-1356 (2015).
3. A. Slogrove, B. Reikie, S. Naidoo, C. De Beer, K. Ho, M. Cotton, J. Bettinger, D. Speert, M. Esser, T. Kollmann, HIV-exposed uninfected infants are at increased risk for severe infections in the first year of life. J. Trop. Pediatr. 58, 505-508 (2012).
4. D. Chilongozi, L. Wang, L. Brown, T. Taha, M. Valentine, L. Emel, M. Sinkala, G. Kafulafula, R. A. Noor, J. S. Read, E. R. Brown, R. L. Goldenberg, I. Hoffman; HIVNET 024 Study Team, Morbidity and mortality among a cohort of human immunodeficiency virus type 1-infected and uninfected pregnant women and their infants from Malawi, Zambia, and Tanzania. Pediatr. Infect. Dis. J. 27, 808-814 (2008).
5. C. Taron-Brocard, J. Le Chenadec, A. Faye, C. Dollfus, T. Goetghebuer, V. Gajdos, J.-M. Labaune, A. Perilhou, L. Mandelbrot, S. Blanche, J. Warszawski; France REcherche Nord&Sud Sida-HIV Hepatites - Enquete Perinatale Francaise - CO1/CO11 Study Group, Increased risk of serious bacterial infections due to maternal immunosuppression in HIV-exposed uninfected infants in a European country. Clin. Infect. Dis. 59, 1332-1345 (2014).
6. E.Marinda, J. H. Humphrey, P. J. Iliff, K. Mutasa, K. J. Nathoo, E. G. Piwoz, L. H. Moulton, P. Salama, B. J. Ward, Child mortality according to maternal and infant HIV status in Zimbabwe. Pediatr. Infect. Dis. J. 26, 519-526 (2007).
7. S. Filteau, The HIV-exposed, uninfected African child. Trop. Med. Int. Health 14, 276-287 (2009).
8. L. Kuhn, P. Kasonde, M. Sinkala, C. Kankasa, K. Semrau, N. Scott, W.-Y. Tsai, S. H. Vermund, G. M. Aldrovandi, D. M. Thea, Does severity of HIV disease in HIV-infected mothers affect mortality and morbidity among their uninfected infants? Clin. Infect. Dis. 41, 1654-1661 (2005).
9. L. Kuhn, G. M. Aldrovandi, M. Sinkala, C. Kankasa, M. Mwiya, D. M. Thea, Potential impact of new WHO criteria for antiretroviral treatment for prevention of mother-to-child HIV transmission. AIDS 24, 1374-1377 (2010).
10. M. Clerici, M. Saresella, F. Colombo, S. Fossati, N. Sala, D. Bricalli, M. L. Villa, P. Ferrante, L. Dally, A. Vigano, T-lymphocyte maturation abnormalities in uninfected newborns and children with vertical exposure to HIV. Blood 96, 3866-3871 (2000).
11. M. Schanche, E. Avershina, C. Dotterud, T. Oien, O. Storr, R. Johnsen, K. Rudi, High-resolution analyses of overlap in the microbiota between mothers and their children. Curr. Microbiol. 71, 283-290 (2015).
12. T. Jost, C. Lacroix, C. P. Braegger, F. Rochat, C. Chassard, Vertical mother-neonate transfer of maternal gut bacteria via breastfeeding. Environ. Microbiol. 16, 2891-2904 (2014).
13. V. Martín, A. Maldonado-Barragán, L. Moles, M. Rodriguez-Baños, R. del Campo, L. Fernández, J. M. Rodríguez, E. Jiménez, Sharing of bacterial strains between breast milk and infant feces. J. Hum. Lact. 28, 36-44 (2012).
14. C.A. Lozupone, M. Li, T. B. Campbell, S. C. Flores, D. Linderman, M. J. Gebert, R. Knight, A. P. Fontenot, B. E. Palmer, Alterations in the gut microbiota associated with HIV-1 infection. Cell Host Microbe 14, 329-339 (2013).
15. C. A. Lozupone, M. E. Rhodes, C. P. Neff, A. P. Fontenot, T. B. Campbell, B. E. Palmer, HIV-induced alteration in gut microbiota: Driving factors, consequences, and effects of antiretroviral therapy. Gut Microbes 5, 562-570 (2014).
16. I. Vujkovic-Cvijin, R. M. Dunham, S. Iwai, M. C. Maher, R. G. Albright, M. J. Broadhurst, R. D. Hernandez, M.M. Lederman, Y.Huang, M. Somsouk, S.G. Deeks, P. W.Hunt, S. V. Lynch, J.M. McCune, Dysbiosis of the gut microbiota is associated with HIV disease progression and tryptophan catabolism. Sci. Transl. Med. 5, 193ra91 (2013).
17. S.M. Dillon, E. J. Lee, C. V. Kotter, G. L. Austin, Z. Dong, D. K. Hecht, S. Gianella, B. Siewe, D. M. Smith, A. L. Landay, C. E. Robertson, D. N. Frank, C. C. Wilson, An altered intestinal mucosal microbiome in HIV-1 infection is associated with mucosal and systemic immune activation and endotoxemia. Mucosal Immunol. 7, 983-994 (2014).
18. J. M. Brenchley, T. W. Schacker, L. E. Ruff, D. A. Price, J. H. Taylor, G. J. Beilman, P. L. Nguyen, A. Khoruts, M. Larson, A. T. Haase, D. C. Douek, CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J. Exp. Med. 200, 749-759 (2004).
19. R. González, A. Maldonado, V. Martán, I. Mandomando, V. Fumadó, K. J. Metzner, C. Sacoor, L. Fernndez, E. Macete, P. L. Alonso, J. M. Rodrguez, C. Menendez, Breast milk and gut microbiota in African mothers and infants from an area of high HIV prevalence. PLOS One 8, e80299 (2013).
20. L. Kuhn, H.-Y. Kim, L. Hsiao, C. Nissan, C. Kankasa, M. Mwiya, D. M. Thea, G. M. Aldrovandi, L. Bode, Oligosaccharide composition of breast milk influences survival of uninfected children born to HIV-infected mothers in Lusaka, Zambia. J. Nutr. 145, 66-72 (2015).
21. S. Arpadi, A. Fawzy, G. M. Aldrovandi, C. Kankasa, M. Sinkala, M. Mwiya, D. M. Thea, L. Kuhn, Growth faltering due to breastfeeding cessation in uninfected children born to HIVinfected mothers in Zambia. Am. J. Clin. Nutr. 90, 344-353 (2009).
22. L. Kuhn, G. M. Aldrovandi, M. Sinkala, C. Kankasa, K. Semrau, M. Mwiya, P. Kasonde, N. Scott, C. Vwalika, J. Walter, M. Bulterys, W.-Y. Tsai, D. M. Thea, Effects of early, abrupt weaning on HIV-free survival of children in Zambia. N. Engl. J. Med. 359, 130-141 (2008).
23. L. Bode, L. Kuhn, H.-Y. Kim, L. Hsiao, C. Nissan, M. Sinkala, C. Kankasa, M. Mwiya, D. M. Thea, G. M. Aldrovandi, Human milk oligosaccharide concentration and risk of postnatal transmission of HIV through breastfeeding. Am. J. Clin. Nutr. 96, 831-839 (2012).
24. L. Kuhn, M. Sinkala, K. Semrau, C. Kankasa, P. Kasonde, M. Mwiya, C.-C. Hu, W.-Y. Tsai, D. M. Thea, G. M. Aldrovandi, Elevations in mortality associated with weaning persist into the second year of life among uninfected children born to HIV-infected mothers. Clin. Infect. Dis. 50, 437-444 (2010).
25. World Health Organization, Guidelines on HIV and Infant Feeding 2010: Principles and Recommendations for Infant Feeding in the Context of HIV and a Summary of Evidence (World Health Organization, Geneva, Switzerland, 2010).
26. L. Bode, Human milk oligosaccharides: Every baby needs a sugar mama. Glycobiology 22, 1147-1162 (2012).
27. M. W. Groer, A. A. Luciano, L. J. Dishaw, T. L. Ashmeade, E. Miller, J. A. Gilbert, Development of the preterm infant gut microbiome: A research priority. Microbiome 2, 38 (2014).
28. N. H. Tobin, G. M. Aldrovandi, Immunology of pediatric HIV infection. Immunol. Rev. 254, 143-169 (2013).
29. J. G. Caporaso, J. Kuczynski, J. Stombaugh, K. Bittinger, F. D. Bushman, E. K. Costello, N. Fierer, A. G. Pea, J. K. Goodrich, J. I. Gordon, G. A. Huttley, S. T. Kelley, D. Knights, J. E. Koenig, R. E. Ley, C. A. Lozupone, D. McDonald, B. D. Muegge, M. Pirrung, J. Reeder, J. R. Sevinsky, P. J. Turnbaugh, W. A. Walters, J. Widmann, T. Yatsunenko, J. Zaneveld, R. Knight, QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335-336 (2010).
30. D. McDonald, M. N. Price, J. Goodrich, E. P. Nawrocki, T. Z. DeSantis, A. Probst, G. L. Andersen, R. Knight, P. Hugenholtz, An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 6, 610-618 (2012).
31. D. Knights, J. Kuczynski, E. S. Charlson, J. Zaneveld, M. C. Mozer, R. G. Collman, F. D. Bushman, R. Knight, S. T. Kelley, Bayesian community-wide culture-independent microbial source tracking. Nat. Methods 8, 761-763 (2011).
32. S. Subramanian, S. Huq, T. Yatsunenko, R. Haque, M. Mahfuz, M. A. Alam, A. Benezra, J. DeStefano, M. F. Meier, B. D. Muegge, M. J. Barratt, L. G. VanArendonk, Q. Zhang, M. A. Province, W. A. Petri Jr., T. Ahmed, J. I. Gordon, Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature 510, 417-421 (2014).
33. M. G. I. Langille, J. Zaneveld, J. G. Caporaso, D. McDonald, D. Knights, J. A. Reyes, J. C. Clemente, D. E. Burkepile, R. L. Vega Thurber, R. Knight, R. G. Beiko, C. Huttenhower, Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 31, 814-821 (2013).
34. S. Iwai, D. Huang, S. Fong, L. G. Jarlsberg, W. Worodria, S. Yoo, A. Cattamanchi, J. L. Davis, S. Kaswabuli, M. Segal, L. Huang, S. V. Lynch, The lung microbiome of Ugandan HIV-infected pneumonia patients is compositionally and functionally distinct from that of San Franciscan patients. PLOS One 9, e95726 (2014).
35. J. U. Scher, A. Sczesnak, R. S. Longman, N. Segata, C. Ubeda, C. Bielski, T. Rostron, V. Cerundolo, E. G. Pamer, S. B. Abramson, C. Huttenhower, D. R. Littman, Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. Elife 2, e01202 (2013).
36. E. Elinav, T. Strowig, A. L. Kau, J. Henao-Mejia, C. A. Thaiss, C. J. Booth, D. R. Peaper, J. Bertin, S. C. Eisenbarth, J. I. Gordon, R. A. Flavell, NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 145, 745-757 (2011).
37. I. A. Zalenskaya, T. Joseph, J. Bavarva, N. Yousefieh, S. S. Jackson, T. Fashemi, H. S. Yamamoto, R. Settlage, R. N. Fichorova, G. F. Doncel, Gene expression profiling of human vaginal cells in vitro discriminates compounds with pro-inflammatory and mucosa-altering properties: Novel biomarkers for preclinical testing of HIV microbicide candidates. PLOS One 10, e0128557 (2015).
38. S. M. Dillon, E. J. Lee, C. V. Kotter, G. L. Austin, S. Gianella, B. Siewe, D. M. Smith, A. L. Landay, M. C. McManus, C. E. Robertson, D. N. Frank, M. D. McCarter, C. C. Wilson, Gut dendritic cell activation links an altered colonic microbiome to mucosal and systemic T-cell activation in untreated HIV-1 infection. Mucosal Immunol. 9, 24-37 (2015).
39. P. McKenna, C. Hoffmann, N. Minkah, P. P. Aye, A. Lackner, Z. Liu, C. A. Lozupone, M. Hamady, R. Knight, F. D. Bushman, The macaque gut microbiome in health, lentiviral infection, and chronic enterocolitis. PLOS Pathog. 4, e20 (2008).
40. M. A. Underwood, S. Gaerlan, M. L. A. De Leoz, L. Dimapasoc, K. M. Kalanetra, D. G. Lemay, J. B. German, D. A. Mills, C. B. Lebrilla, Human milk oligosaccharides in premature infants: Absorption, excretion and influence on the intestinal microbiota. Pediatr. Res. 78, 670-677 (2015).
41. A. Chaplin, P. Parra, F. Serra, A. Palou, Conjugated linoleic acid supplementation under a high-fat diet modulates stomach protein expression and intestinal microbiota in adult mice. PLOS One 10, e0125091 (2015).
42. A. Marcobal, M. Barboza, E. D. Sonnenburg, N. Pudlo, E. C. Martens, P. Desai, C. B. Lebrilla, B. C. Weimer, D. A. Mills, J. B. German, J. L. Sonnenburg, Bacteroides in the infant gut consume milk oligosaccharides via mucus-utilization pathways. Cell Host Microbe 10, 507-514 (2011).
43. N. R. Klatt, L. A. Canary, X. Sun, C. L. Vinton, N. T. Funderburg, D. R. Morcock, M. Quiones, C. B. Deming, M. Perkins, D. J. Hazuda, M. D. Miller, M. M. Lederman, J. A. Segre, J. D. Lifson, E. K. Haddad, J. D. Estes, J. M. Brenchley, Probiotic/prebiotic supplementation of antiretrovirals improves gastrointestinal immunity in SIV-infected macaques. J. Clin. Invest. 123, 903-907 (2013).
44. M. Kerac, J. Bunn, A. Seal, M. Thindwa, A. Tomkins, K. Sadler, P. Bahwere, S. Collins, Probiotics and prebiotics for severe acute malnutrition (PRONUT study): A double-blind efficacy randomised controlled trial in Malawi. Lancet 374, 136-144 (2009).
45. E. Van Niekerk, D. G. Nel, R. Blaauw, G. F. Kirsten, Probiotics reduce necrotizing enterocolitis severity in HIV-exposed premature infants. J. Trop. Pediatr. 61, 155-164 (2015).
46. J. G. Caporaso, C. L. Lauber, W. A. Walters, D. Berg-Lyons, J. Huntley, N. Fierer, S. M. Owens, J. Betley, L. Fraser, M. Bauer, N. Gormley, J. A. Gilbert, G. Smith, R. Knight, Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6, 1621-1624 (2012).
47. J. K. Goodrich, S. C. Di Rienzi, A. C. Poole, O. Koren, W. A. Walters, J. G. Caporaso, R. Knight, R. E. Ley, Conducting a microbiome study. Cell 158, 250-262 (2014).
48. P. D. Schloss, S. L. Westcott, T. Ryabin, J. R. Hall, M. Hartmann, E. B. Hollister, R. A. Lesniewski, B. B. Oakley,D. H. Parks, C. J. Robinson, J.W. Sahl, B. Stres, G. G. Thallinger, D. J. VanHorn, C. F.Weber, Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537-7541 (2009).