Effects of antenatal and postnatal environments on CD4 T-cell responses to Mycobacterium bovis BCG in healthy infants in the Gambia

Clinical and Vaccine Immunology

Volumn 15, Issue 6, 2008, Pages 995-1002

  Miles, David J C ^a,e   Van Der Sande, Marianne ^b   Crozier, Sarah ^a   Ojuola, Olubukola ^c   Palmero, Melba S ^a   Sanneh, Mariama ^a   Touray, Ebrima S ^a   Rowland Jones, Sarah ^a   Whittle, Hilton ^a   Ota, Martin ^a   Marchant, Arnaud ^d  

^a MEDICAL RESEARCH COUNCIL LABORATORIES   (Gambia)

^b NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^c BRONX LEBANON HOSPITAL CENTER   (United States)

^d UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^e MALAWI LIVERPOOL WELLCOME TRUST CLINICAL RESEARCH PROGRAMME   (Malawi)

Author keywords

[No Author keywords available]

Indexed keywords

BCG VACCINE; CD40 LIGAND; GAMMA INTERFERON; INTERLEUKIN 2; MYCOBACTERIUM ANTIGEN;

ADULT; ARTICLE; BCG VACCINATION; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DRUG EFFECT; DRUG EFFICACY; FEMALE; GAMBIA; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; IMMUNE RESPONSE; INFANT; LOWEST INCOME GROUP; MALE; MYCOBACTERIUM BOVIS; NORMAL HUMAN; PERINATAL PERIOD; PRENATAL PERIOD; PRESCHOOL CHILD; PRIORITY JOURNAL; TUBERCULOSIS;

ADULT; BCG VACCINE; BODY MASS INDEX; CD4-POSITIVE T-LYMPHOCYTES; CD40 LIGAND; CHILD; CHILD, PRESCHOOL; ETHNIC GROUPS; FEMALE; GAMBIA; HUMANS; INFANT; INFANT, NEWBORN; INTERFERON TYPE II; INTERLEUKIN-2; MALE; MATERNAL WELFARE; MYCOBACTERIUM BOVIS; SEASONS; SOCIAL CLASS; TUBERCULOSIS;

EID: 47049130254     PISSN: 15566811     EISSN: 1556679X     Source Type: Journal    
DOI: 10.1128/CVI.00037-08     Document Type: Article

References (49)

1. Black, G., R. Weir, S. Floyd, L. Bliss, D. Warndorff, A. Crampin, B. Ngwira, L. Sichali, B. Nazareth, J. Blackwell, K. Branson, S. Chaguluka, L. Donovan, E. Jarman, E. King, E. Fine, and H. Dockrell. 2002. BCG-induced increase in interferon-gamma response to mycobacterial antigens and efficacy of BCG vaccination in Malawi and the UK: two randomised controlled studies. Lancet 359:1393-1401.
2. Brosch, R., S. Gordon, T. Garnier, K. Eiglmeier, W. Frigui, P. Valenti, S. Dos Santos, S. Duthoy, C. Lacroix, C. Garcia-Pelayo, J. Inwald, P. Golby, J. Garcia, R. Hewinson, M. Behr, M. Quail, C. Churcher, B. Barrell, J. Parkhill, and S. Cole. 2007. Genome plasticity of BCG and impact on vaccine efficacy. Proc. Natl. Acad. Sci. USA 104:5596-5601.
3. + T lymphocytes with cellular maturation. J. Exp. Med. 203:2865-2877.
4. Chattopadhyay, P., J. Yu, and M. Roederer. 2005. A live-cell assay to detect antigen-specific CD4+ T cells with diverse cytokine profiles. Nat. Med. 11:1113-1117.
5. Colditz, G., C. Berkey, F. Mosteller, T. Brewer, M. Wilson, E. Burdick, and H. Fineberg. 1995. The efficacy of bacillus Calmette-Guérin vaccination of newborns and infants in the prevention of tuberculosis: meta-analyses of the published literature. Pediatrics 96:29-35.
6. Collinson, A., S. Moore, T. Cole, and A. Prentice. 2003. Birth season and environmental influences on patterns of thymic growth in rural Gambian infants. Acta Paediatr. 92:1014-1020.
7. Dorman, S., and S. Holland. 1998. Mutation in the signal-transducing chain of the interferon-γ receptor and susceptibility to mycobacterial infection. J. Clin. Investig. 101:2364-2369.
8. Durandy, A., G. De Saint Basile, B. Lisowska-Grospierre, J. Gauchat, M. Forveille, R. Kroczek, J. Bonnefoy, and A. Fischer. 1995. Undetectable CD40 ligand expression on T cells and low B cell responses to CD40 binding agonists in human newborns. J. Immunol. 154:1560-1568.
9. Dye, C., S. Scheele, P. Dolin, V. Pathania, M. Raviglione, et al. 1999. Consensus statement. Global burden of tuberculosis: estimated incidence, prevalence, and mortality by country. JAMA 282:677-686.
10. Ellner, J. 1997. The immune response in human tuberculosis - implications for tuberculosis control. J. Infect. Dis. 176:1351-1359.
11. Frentsch, M., O. Arbach, D. Kirchhoff, B. Moewes, M. Worm, M. Rothe, A. Scheffold, and A. Thiel. 2005. Direct access to CD4+ T cells specific for defined antigens according to CD154 expression. Nat. Med. 11:1118-1124.
12. Hayashi, T., S. Rao, P. Meylan, R. Kornbluth, and A. Catanzaro. 1999. Role of CD40 ligand in Mycobacterium avium infection. Infect. Immun. 67:3558-3565.
13. Hill, P., D. Jackson-Sillah, S. Donkor, J. Otu, R. Adegbola, and C. Lienhardt. 2006. Risk factors for pulmonary tuberculosis: a clinic-based case control study in The Gambia. BMC Public Health 6:156.
14. Hogan, L., W. Markofski, A. Bock, B. Barger, J. Morrissey, and M. Sandor. 2001. Mycobacterium bovis BCG-induced granuloma formation depends on gamma interferon and CD40 ligand but does not require CD28. Infect. Immun. 69:2596-2603.
15. Hughes, A., P. Hutchinson, T. Gooding, N. Freezer, S. Holdsworth, and P. Johnson. 2005. Diagnosis of Mycobacterium tuberculosis infection using ESAT-6 and intracellular cytokine cytometry. Clin. Exp. Immunol. 142:132-139.
16. Johnson, B., L.-G. Bekker, R. Rickman, S. Brown, M. Lesser, S. Ress, P. Willcox, L. Steyn, and G. Kaplan. 1997. rhuIL-2 adjunctive therapy in multidrug resistant tuberculosis: a comparison of two treatment regimens and placebo. Tuber. Lung Dis. 78:195-203.
17. Johnson, B., I. Estrada, Z. Shen, S. Ress, P. Willcox, M. Colston, and G. Kaplan. 1998. Differential gene expression in response to adjunctive recombinant human interleukin-2 immunotherapy in multidrug-resistant tuberculosis patients. Infect. Immun. 66:2426-2433.
18. Johnson, J., E. Ssekasanvu, A. Okwera, H. Mayanja, C. Hirsch, J. Nakibali, D. Jankus, K. Eisenach, W. Boom, J. Ellner, and R. Mugerwa. 2003. Randomized trial of adjunctive interleukin-2 in adults with pulmonary tuberculosis. Am. J. Respir. Crit. Care Med. 168:185-191.
19. Kampmann, B., P. Gaora, V. Snewin, M. Gares, D. Young, and M. Levin. 2000. Evaluation of human antimycobacterial immunity using recombinant reporter mycobacteria. J. Infect. Dis. 182:895-901.
20. Kampmann, B., C. Hemingway, A. Stephens, R. Davidson, A. Goodsall, S. Anderson, M. Nicol, E. Schölvinck, D. Relman, S. Waddell, P. Langford, B. Sheehan, L. Semple, K. Wilkinson, R. Wilkinson, S. Ress, M. Hibberd, and M. Levin. 2005. Acquired predisposition to mycobacterial disease due to autoantibodies to IFN-γ. J. Clin. Investig. 115:2480-2488.
21. Malhotra, I., P. Mungai, A. Wamachi, J. Kioko, J. Ouma, J. Kazura, and C. King. 1999. Helminth- and bacillus Calmette-Guérin-induced immunity in children sensitized in utero to filariasis and schistosomiasis. J. Immunol. 162:6843-6848.
22. Marchant, A., T. Goetghebuer, M. Ota, I. Wolfe, S. Ceesay, G. De, D. T. Corrak, S. Bennett, J. Wheeler, K. Huygen, P. Aaby, K. McAdam, and M. Newport. 1999. Newborns develop a Th1-type immune response to Mycobacterium bovis bacillus Calmette-Guerin vaccination. J. Immunol. 2249-2255.
23. McDade, T., M. Beck, C. Kuzawa, and L. Adair. 2001. Prenatal undernutrition and postnatal growth are associated with adolescent thymic function. J. Nutr. 131:1225-1231.
24. McDade, T., M. Beck, C. Kuzawa, and L. Adair. 2001. Prenatal undernutrition, postnatal environments, and antibody response to vaccination in adolescence. Am. J. Clin. Nutr. 74:543-548.
25. Miles, D., M. van der Sande, D. Jeffries, S. Kaye, J. Ismaili, O. Ojuola, M. Sanneh, E. Touray, P. Waight, S. Rowland-Jones, H. Whittle, and A. Marchant. 2007. Cytomegalovirus infection in Gambian infants leads to profound CD8 T-cell differentiation. J. Virol. 81:5766-5776.
26. + T cell responses to cytomegalovirus in early life: a prospective birth cohort study. J. Infect. Dis. 197:658-662.
27. Moore, S., T. Cole, A. Collinson, E. Poskitt, I. McGregor, and A. Prentice. 1999. Prenatal or early postnatal events predict infectious deaths in young adulthood in rural Africa. Int. J. Epidemiol. 28:1088-1095.
28. Moore, S., T. Cole, E. Poskitt, B. Sonko, R. Whitehead, I. McGregor, and A. Prentice. 1997. Season of birth predicts mortality in rural Gambia. Nature 388:434.
29. Moore, S., A. Collinson, A. Fulford, F. Jalil, C.-A. Siegrist, D. Goldblatt, L. Hanson, and A. Prentice. 2006. Effect of month of vaccine administration on antibody responses in The Gambia and Pakistan. Trop. Med. Int. Health 11:1529-1541.
30. Moore, S., F. Jalil, R. Ashraf, S. Szu, A. Prentice, and L. Hanson. 2004. Birth weight predicts response to vaccination in adults born in an urban slum in Lahore, Pakistan. Am. J. Clin. Nutr. 80:453-459.
31. Narayanan, P. 2006. Influence of sex, age & nontuberculous infection at intake on the efficacy of BCG: re-analysis of 15-year data from a doubleblind randomized control trial in South India. Indian J. Med. Res. 123:119-124.
32. Newport, M., T. Goetghebuer, H. Weiss, H. Whittle, C.-A. Siegrist, and A. Marchant. 2004. Genetic regulation of immune responses to vaccines in early life. Genes Immun. 5:122-129.
33. Newport, M., C. Huxley, S. Huston, C. Hawrylowicz, B. Oostra, R. Williamson, and M. Levin. 1996. A mutation in the interferon-gamma-receptor gene and susceptibility to mycobacterial infection. N. Engl. J. Med. 335:1941-1949.
34. Nonoyama, S., L. Penix, C. Edwards, D. Lewis, S. Ito, A. Aruffo, C. Wilson, and H. Ochs. 1995. Diminished expression of CD40 ligand by activated neonatal T cells. J. Clin. Investig. 95:66-75.
35. Olerup, O., M. Troye-Blomberg, G. Schreuder, and E. Riley. 1991. HLA-DR and -DQ gene polymorphism in West Africans is twice as extensive as in north European Caucasians: evolutionary implications. Proc. Natl. Acad. Sci. USA 88:8480-8484.
36. Pathan, A., K. Wilkinson, P. Klenerman, H. McShane, R. Davidson, G. Pasvol, A. Hill, and A. Lalvani. 2001. Direct ex vivo analysis of antigen-specific IFN-γ-secreting CD4 T cells in Mycobacterium tuberculosis-infected individuals: associations with clinical disease state and effect of treatment. J. Immunol. 167:5217-5225.
37. Pönnighaus, J., P. Fine, J. Sterne, R. Wilson, E. Msosa, P. Gruer, P. Jenkins, S. Lucas, N. Liomba, and L. Bliss. 1992. Efficacy of BCG vaccine against leprosy and tuberculosis in northern Malawi. Lancet 339:636-639.
38. Prentice, A., R. Whitehead, S. Roberts, and A. Paul. 1981. Long-term energy balance in child-bearing Gambian women. Am. J. Clin. Nutr. 34:2790-2799.
39. Rayco-Solon, P., A. Fulford, and A. Prentice. 2005. Differential effects of seasonality on preterm birth and intrauterine growth restriction in rural Africans. Am. J. Clin. Nutr. 81:134-139.
40. Rodrigues, L., V. Diwan, and J. Wheeler. 1993. Protective effect of BCG against tuberculous meningitis and miliary tuberculosis: a meta-analysis. Int. J. Epidemiol. 22:1154-1158.
41. Roth, A., M. Sodemann, H. Jensen, A. Poulsen, P. Gustafson, J. Gomes, Q. Djana, M. Jakobsen, M.-L. Garly, A. Rodrigues, and P. Aaby. 2005. Vaccination technique, PPD reaction and BCG scarring in a cohort of children born in Guinea-Bissau 2000-2002. Vaccine 23:3991-3998.
42. Samten, B., E. Thomas, J. Gong, and P. Barnes. 2000. Depressed CD40 ligand expression contributes to reduced gamma interferon production in human tuberculosis. Infect. Immun. 68:3002-3006.
43. + T lymphocytes produce multiple cytokines and proliferate in vivo in humans. J. Immunol. 177:8185-8190.
44. Tena, G., D. Young, B. Eley, H. Henderson, M. Nicol, M. Levin, and B. Kampmann. 2003. Failure to control growth of mycobacteria in blood from children infected with human immunodeficiency virus and its relationship to T cell function. J. Infect. Dis. 187:1544-1551.
45. Vekemans, J., M. Ota, J. Sillah, K. Fielding, M. Alderson, Y. Skeiky, W. Dalemans, K. McAdam, C. Lienhardt, and A. Marchant. 2004. Immune responses to mycobacterial antigens in the Gambian population: implications for vaccines and immunodiagnostic test design. Infect. Immun. 72:381-388.
46. Vincenti, D., S. Carrara, P. de Mori, P. L. Pucillo, N. Petrosillo, F. Palmieri, O. Armignacco, G. Ippolito, E. Girardi, M. Amicosante, and D. Goletti. 2003. Identification of early secretory antigen target-6 epitopes for the immunodiagnosis of active tuberculosis. Mol. Med. 9:105-111.
47. Wallis, R. 2005. Reconsidering adjuvant immunotherapy for tuberculosis. Clin. Infect. Dis. 41:201-208.
48. WHO. 2007. World health statistics 2007. World Health Organization, Geneva, Switzerland.
49. WHO/UNICEF. 2004. Review of national immunization coverage 1980-2003: Gambia. WHO/UNICEF, Geneva, Switzerland.