Deming MS, Linkins RW, Jaiteh KO, Hull HF, 1997. The clinical efficacy of trivalent oral polio vaccine in The Gambia by season of vaccine administration. J Infect Dis 175 (Suppl 1): S254–S257.
Moore SE, Collinson AC, Fulford AJ, Jalil F, Siegrist CA, Goldblatt D, Hanson LA, Prentice AM, 2006. Effect of month of vaccine administration on antibody responses in The Gambia and Pakistan. Trop Med Int Health 11: 1529–1541.
Miles DJ, van der Sande M, Crozier S, Ojuola O, Palmero MS, Sanneh M, Touray ES, Rowland-Jones S, Whittle H, Ota M, Marchant A, 2008. Effects of antenatal and postnatal environments on CD4 T-cell responses to Mycobacterium bovis BCG in healthy infants in the Gambia. Clin Vaccine Immunol 15: 995–1002.
Lalor MK, Ben-Smith A, Gorak-Stolinska P, Weir RE, Floyd S, Blitz R, Mvula H, Newport MJ, Branson K, McGrath N, Crampin AC, Fine PE, Dockrell HM, 2009. Population differences in immune responses to Bacille Calmette-Guerin vaccination in infancy. J Infect Dis 199: 795–800.
Marchant A, Pihlgren M, Goetghebuer T, Weiss HA, Ota MO, Schlegel-Hauter SE, Whittle H, Lambert PH, Newport MJ, Siegrist CA, 2006. Predominant influence of environmental determinants on the persistence and avidity maturation of antibody responses to vaccines in infants. J Infect Dis 193: 1598–1605.
Collinson AC, Ngom PT, Moore SE, Morgan G, Prentice AM, 2008. Birth season and environmental influences on blood leucocyte and lymphocyte subpopulations in rural Gambian infants. BMC Immunol 9: 18.
Schaible UE, Kaufmann SH, 2007. Malnutrition and infection: complex mechanisms and global impacts. PLoS Med 4: e115.
Haque R, Mondal D, Shu J, Roy S, Kabir M, Davis AN, Duggal P, Petri WA Jr, 2007. Correlation of interferon-gamma production by peripheral blood mononuclear cells with childhood malnutrition and susceptibility to amebiasis. Am J Trop Med Hyg 76: 340–344.
Fillol F, Sarr JB, Boulanger D, Cisse B, Sokhna C, Riveau G, Simondon KB, Remoue F, 2009. Impact of child malnutrition on the specific anti-Plasmodium falciparum antibody response. Malar J 8: 116.
Savy M, Edmond K, Fine PE, Hall A, Hennig BJ, Moore SE, Mulholland K, Schaible U, Prentice AM, 2009. Landscape analysis of interactions between nutrition and vaccine responses in children. J Nutr 139: 2154S–2218S.
Borkow G, Bentwich Z, 2008. Chronic parasite infections cause immune changes that could affect successful vaccination. Trends Parasitol 24: 243–245.
Dauby N, Alonso-Vega C, Suarez E, Flores A, Hermann E, Cordova M, Tellez T, Torrico F, Truyens C, Carlier Y, 2009. Maternal infection with Trypanosoma cruzi and congenital Chagas disease induce a trend to a type 1 polarization of infant immune responses to vaccines. PLoS Negl Trop Dis 3: e571.
McDade TW, Beck MA, Kuzawa C, Adair LS, 2001. Prenatal undernutrition, postnatal environments, and antibody response to vaccination in adolescence. Am J Clin Nutr 74: 543–548.
Moore SE, Jalil F, Ashraf R, Szu SC, Prentice AM, Hanson LA, 2004. Birth weight predicts response to vaccination in adults born in an urban slum in Lahore, Pakistan. Am J Clin Nutr 80: 453–459.
Gaayeb L, Sarr JB, Ndiath MO, Hanon JB, Debrie AS, Seck M, Schacht AM, Remoue F, Hermann E, Riveau G, 2012. Seroprevalence of pertussis in Senegal: a prospective study. PLoS One 7: e48684.
WHO, 1995. Physical Status: The Use and Interpretation of Anthropometry. WHO Technical Report Series. WHO Technical Report Series 854. Geneva: World Health Organization, 1–452.
Viana PO, Ono E, Miyamoto M, Salomao R, Costa-Carvalho BT, Weckx LY, de Moraes-Pinto MI, 2010. Humoral and cellular immune responses to measles and tetanus: the importance of elapsed time since last exposure and the nature of the antigen. J Clin Immunol 30: 574–582.
Finan C, Ota MO, Marchant A, Newport MJ, 2008. Natural variation in immune responses to neonatal Mycobacterium bovis Bacillus Calmette-Guerin (BCG) vaccination in a cohort of Gambian infants. PLoS One 3: e3485.
Black GF, Dockrell HM, Crampin AC, Floyd S, Weir RE, Bliss L, Sichali L, Mwaungulu L, Kanyongoloka H, Ngwira B, Warndorff DK, Fine PE, 2001. Patterns and implications of naturally acquired immune responses to environmental and tuberculous mycobacterial antigens in northern Malawi. J Infect Dis 184: 322–329.
Brussow H, Sidoti J, Dirren H, Freire WB, 1995. Effect of malnutrition in Ecuadorian children on titers of serum antibodies to various microbial antigens. Clin Diagn Lab Immunol 2: 62–68.
Monjour L, Bourdillon F, Korinek AM, Aubonnet-Laignel A, Brousse G, Gentilini M, Bayard P, Ballet JJ, 1988. Humoral immunity, 5 years after anti-tetanus vaccination, in a group of malaria-infected and malnourished African children. Pathol Biol (Paris) 36: 235–239.
Siekmann JH, Allen LH, Watnik MR, Nestel P, Neumann CG, Shoenfeld Y, Peter JB, Patnik M, Ansari AA, Coppel RL, Gershwin ME, 2003. Titers of antibody to common pathogens: relation to food-based interventions in rural Kenyan schoolchildren. Am J Clin Nutr 77: 242–249.
Simondon KB, Ndiaye T, Dia M, Yam A, Ndiaye M, Marra A, Diallo A, Simondon F, 2008. Seasonal variations and trends in weight and arm circumference of non-pregnant rural Senegalese women, 1990–1997. Eur J Clin Nutr 62: 997–1004.
Ceesay SM, Prentice AM, Cole TJ, Foord F, Weaver LT, Poskitt EM, Whitehead RG, 1997. Effects on birth weight and perinatal mortality of maternal dietary supplements in rural Gambia: 5 year randomised controlled trial. BMJ 315: 786–790.
Simondon KB, Simondon F, 1998. Mothers prolong breastfeeding of undernourished children in rural Senegal. Int J Epidemiol 27: 490–494.
Moore SE, Prentice AM, Wagatsuma Y, Fulford AJ, Collinson AC, Raqib R, Vahter M, Persson LA, Arifeen SE, 2009. Early-life nutritional and environmental determinants of thymic size in infants born in rural Bangladesh. Acta Paediatr 98: 1168–1175.
Moore SE, Richards AA, Goldblatt D, Ashton L, Szu SC, Prentice AM, 2012. Early-life and contemporaneous nutritional and environmental predictors of antibody response to vaccination in young Gambian adults. Vaccine 30: 4842–4848.
Thomas TA, Mondal D, Noor Z, Liu L, Alam M, Haque R, Banu S, Sun H, Peterson KM, 2010. Malnutrition and helminth infection affect performance of an interferon gamma-release assay. Pediatrics 126: e1522–e1529.
McMurray DN, Loomis SA, Casazza LJ, Rey H, Miranda R, 1981. Development of impaired cell-mediated immunity in mild and moderate malnutrition. Am J Clin Nutr 34: 68–77.
Semba RD, Muhilal SAL, Natadisastra G, Wirasasmita S, Mele L, Ridwan E, West KP Jr, Sommer A, 1992. Depressed immune response to tetanus in children with vitamin A deficiency. J Nutr 122: 101–107.
de Onis M, Onyango AW, Borghi E, Siyam A, Nishida C, Siekmann J, 2007. Development of a WHO growth reference for school-aged children and adolescents. Bull World Health Organ 85: 660–667.
Ndiath MO, Sarr JB, Gaayeb L, Mazenot C, Sougoufara S, Konate L, Remoue F, Hermann E, Trape JF, Riveau G, Sokhna C, 2012. Low and seasonal malaria transmission in the middle Senegal River basin: identification and characteristics of Anopheles vectors. Parasit Vectors 5: 21.
Diallo TO, Remoue F, Gaayeb L, Schacht AM, Charrier N, De Clerck D, Dompnier JP, Pillet S, Garraud O, N'Diaye AA, Riveau G, 2010. Schistosomiasis coinfection in children influences acquired immune response against Plasmodium falciparum malaria antigens. PLoS One 5: e12764.
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To evaluate immunity to vaccine-preventable diseases according to nutritional status, a longitudinal study was conducted in Senegalese children ages 1–9 years old. A linear regression analysis predicted that weight for age was positively associated with immunoglobulin G (IgG) response to tetanus toxoid in children born during the rainy season or at the beginning of the dry season. A relationship between village, time of visits, and levels of antibodies to tetanus showed that environmental factors played a role in modulating humoral immunity to tetanus vaccine over time. Moreover, a whole-blood stimulation assay highlighted that the production of interferon-γ (IFN-γ) in response to tetanus toxoid was compromised in stunted children. However, the absence of cytokine modulation in response to Mycobacterium tuberculosis-purified protein derivatives and phytohemagglutinin suggests that the overall ability to produce IFN-γ was preserved in stunted children. Therefore, these results show that nutritional status can specifically alter the efficacy of long-lasting immunity to tetanus.
Financial support: L.G. received support from the Region Nord-Pas de Calais and the Pasteur Institute of Lille. Centre de Recherche Biomédicale Espoir Pour la Santé supported field investigation, and the Center for Infection and Immunity of Lille provided support for the achievement of the immunological assays.
Authors' addresses: Lobna Gaayeb and Gilles Riveau, Center for Infection and Immunity of Lille (CIIL)—U1019 Inserm, UMR8204 CNRS, Université Lille Nord de France, Institut Pasteur de Lille, Lille, France and Centre de Recherche Biomédicale Espoir Pour la Santé (EPLS), Saint-Louis, Senegal, E-mails: lobna.gaayeb@gmail.com and gilles.riveau@gmail.com. Jean B. Sarr, Modou Seck, and Andre B. Sagna, Centre de Recherche Biomédicale Espoir Pour la Santé (EPLS), Saint-Louis, Senegal, E-mails: sarrjeanbirame@yahoo.fr, modou.seck@espoir-sante.org, and sagna.ab@gmail.com. Cécile Cames, Institut de Recherche pour le Développement UMI233 TransVIHmi, Centre Régional de Recherche et de Formation à la prise en charge Clinique, Centre Hospitalier Universitaire de Fann, Dakar, Senegal, E-mail: Cecile.Cames@ird.fr. Claire Pincon, Department of Biostatistics, Faculté de Pharmacie, Université Lille Nord de France, Lille, France, E-mail: claire.pincon@univ-lille2.fr. Jean-Baptiste Hanon, Fabien Herbert, Anne-Marie Schacht, and Emmanuel Hermann, Center for Infection and Immunity of Lille (CIIL)—U1019 Inserm, UMR8204 CNRS, Université Lille Nord de France, Institut Pasteur de Lille, Lille, France, E-mails: jb.hanon@yahoo.fr, fabien.herbert@pasteur-lille.fr, am.schacht@gmail.com, and emmanuel.hermann@univ-lille2.fr. Mamadou O. Ndiath, UMR198 URMITE, Campus International, Institut de Recherche pour le Développement, UCAD, Institut de Recherche pour le Développement Hann, Dakar, Senegal, E-mail: ousmane.ndiatt@ird.fr. Franck Remoue, UMR MIVEGEC, Institut de Recherche pour le Développement 224, CNRS5290, Université de Montpellier 1 et 2, Institut de Recherche pour le Développement, Centre de Recherche Entomologique de Cotonou (CREC), Cotonou, Benin, E-mail: franck.remoue@ird.fr.
Deming MS, Linkins RW, Jaiteh KO, Hull HF, 1997. The clinical efficacy of trivalent oral polio vaccine in The Gambia by season of vaccine administration. J Infect Dis 175 (Suppl 1): S254–S257.
Moore SE, Collinson AC, Fulford AJ, Jalil F, Siegrist CA, Goldblatt D, Hanson LA, Prentice AM, 2006. Effect of month of vaccine administration on antibody responses in The Gambia and Pakistan. Trop Med Int Health 11: 1529–1541.
Miles DJ, van der Sande M, Crozier S, Ojuola O, Palmero MS, Sanneh M, Touray ES, Rowland-Jones S, Whittle H, Ota M, Marchant A, 2008. Effects of antenatal and postnatal environments on CD4 T-cell responses to Mycobacterium bovis BCG in healthy infants in the Gambia. Clin Vaccine Immunol 15: 995–1002.
Lalor MK, Ben-Smith A, Gorak-Stolinska P, Weir RE, Floyd S, Blitz R, Mvula H, Newport MJ, Branson K, McGrath N, Crampin AC, Fine PE, Dockrell HM, 2009. Population differences in immune responses to Bacille Calmette-Guerin vaccination in infancy. J Infect Dis 199: 795–800.
Marchant A, Pihlgren M, Goetghebuer T, Weiss HA, Ota MO, Schlegel-Hauter SE, Whittle H, Lambert PH, Newport MJ, Siegrist CA, 2006. Predominant influence of environmental determinants on the persistence and avidity maturation of antibody responses to vaccines in infants. J Infect Dis 193: 1598–1605.
Collinson AC, Ngom PT, Moore SE, Morgan G, Prentice AM, 2008. Birth season and environmental influences on blood leucocyte and lymphocyte subpopulations in rural Gambian infants. BMC Immunol 9: 18.
Schaible UE, Kaufmann SH, 2007. Malnutrition and infection: complex mechanisms and global impacts. PLoS Med 4: e115.
Haque R, Mondal D, Shu J, Roy S, Kabir M, Davis AN, Duggal P, Petri WA Jr, 2007. Correlation of interferon-gamma production by peripheral blood mononuclear cells with childhood malnutrition and susceptibility to amebiasis. Am J Trop Med Hyg 76: 340–344.
Fillol F, Sarr JB, Boulanger D, Cisse B, Sokhna C, Riveau G, Simondon KB, Remoue F, 2009. Impact of child malnutrition on the specific anti-Plasmodium falciparum antibody response. Malar J 8: 116.
Savy M, Edmond K, Fine PE, Hall A, Hennig BJ, Moore SE, Mulholland K, Schaible U, Prentice AM, 2009. Landscape analysis of interactions between nutrition and vaccine responses in children. J Nutr 139: 2154S–2218S.
Borkow G, Bentwich Z, 2008. Chronic parasite infections cause immune changes that could affect successful vaccination. Trends Parasitol 24: 243–245.
Dauby N, Alonso-Vega C, Suarez E, Flores A, Hermann E, Cordova M, Tellez T, Torrico F, Truyens C, Carlier Y, 2009. Maternal infection with Trypanosoma cruzi and congenital Chagas disease induce a trend to a type 1 polarization of infant immune responses to vaccines. PLoS Negl Trop Dis 3: e571.
McDade TW, Beck MA, Kuzawa C, Adair LS, 2001. Prenatal undernutrition, postnatal environments, and antibody response to vaccination in adolescence. Am J Clin Nutr 74: 543–548.
Moore SE, Jalil F, Ashraf R, Szu SC, Prentice AM, Hanson LA, 2004. Birth weight predicts response to vaccination in adults born in an urban slum in Lahore, Pakistan. Am J Clin Nutr 80: 453–459.
Gaayeb L, Sarr JB, Ndiath MO, Hanon JB, Debrie AS, Seck M, Schacht AM, Remoue F, Hermann E, Riveau G, 2012. Seroprevalence of pertussis in Senegal: a prospective study. PLoS One 7: e48684.
WHO, 1995. Physical Status: The Use and Interpretation of Anthropometry. WHO Technical Report Series. WHO Technical Report Series 854. Geneva: World Health Organization, 1–452.
Viana PO, Ono E, Miyamoto M, Salomao R, Costa-Carvalho BT, Weckx LY, de Moraes-Pinto MI, 2010. Humoral and cellular immune responses to measles and tetanus: the importance of elapsed time since last exposure and the nature of the antigen. J Clin Immunol 30: 574–582.
Finan C, Ota MO, Marchant A, Newport MJ, 2008. Natural variation in immune responses to neonatal Mycobacterium bovis Bacillus Calmette-Guerin (BCG) vaccination in a cohort of Gambian infants. PLoS One 3: e3485.
Black GF, Dockrell HM, Crampin AC, Floyd S, Weir RE, Bliss L, Sichali L, Mwaungulu L, Kanyongoloka H, Ngwira B, Warndorff DK, Fine PE, 2001. Patterns and implications of naturally acquired immune responses to environmental and tuberculous mycobacterial antigens in northern Malawi. J Infect Dis 184: 322–329.
Brussow H, Sidoti J, Dirren H, Freire WB, 1995. Effect of malnutrition in Ecuadorian children on titers of serum antibodies to various microbial antigens. Clin Diagn Lab Immunol 2: 62–68.
Monjour L, Bourdillon F, Korinek AM, Aubonnet-Laignel A, Brousse G, Gentilini M, Bayard P, Ballet JJ, 1988. Humoral immunity, 5 years after anti-tetanus vaccination, in a group of malaria-infected and malnourished African children. Pathol Biol (Paris) 36: 235–239.
Siekmann JH, Allen LH, Watnik MR, Nestel P, Neumann CG, Shoenfeld Y, Peter JB, Patnik M, Ansari AA, Coppel RL, Gershwin ME, 2003. Titers of antibody to common pathogens: relation to food-based interventions in rural Kenyan schoolchildren. Am J Clin Nutr 77: 242–249.
Simondon KB, Ndiaye T, Dia M, Yam A, Ndiaye M, Marra A, Diallo A, Simondon F, 2008. Seasonal variations and trends in weight and arm circumference of non-pregnant rural Senegalese women, 1990–1997. Eur J Clin Nutr 62: 997–1004.
Ceesay SM, Prentice AM, Cole TJ, Foord F, Weaver LT, Poskitt EM, Whitehead RG, 1997. Effects on birth weight and perinatal mortality of maternal dietary supplements in rural Gambia: 5 year randomised controlled trial. BMJ 315: 786–790.
Simondon KB, Simondon F, 1998. Mothers prolong breastfeeding of undernourished children in rural Senegal. Int J Epidemiol 27: 490–494.
Moore SE, Prentice AM, Wagatsuma Y, Fulford AJ, Collinson AC, Raqib R, Vahter M, Persson LA, Arifeen SE, 2009. Early-life nutritional and environmental determinants of thymic size in infants born in rural Bangladesh. Acta Paediatr 98: 1168–1175.
Moore SE, Richards AA, Goldblatt D, Ashton L, Szu SC, Prentice AM, 2012. Early-life and contemporaneous nutritional and environmental predictors of antibody response to vaccination in young Gambian adults. Vaccine 30: 4842–4848.
Thomas TA, Mondal D, Noor Z, Liu L, Alam M, Haque R, Banu S, Sun H, Peterson KM, 2010. Malnutrition and helminth infection affect performance of an interferon gamma-release assay. Pediatrics 126: e1522–e1529.
McMurray DN, Loomis SA, Casazza LJ, Rey H, Miranda R, 1981. Development of impaired cell-mediated immunity in mild and moderate malnutrition. Am J Clin Nutr 34: 68–77.
Semba RD, Muhilal SAL, Natadisastra G, Wirasasmita S, Mele L, Ridwan E, West KP Jr, Sommer A, 1992. Depressed immune response to tetanus in children with vitamin A deficiency. J Nutr 122: 101–107.
de Onis M, Onyango AW, Borghi E, Siyam A, Nishida C, Siekmann J, 2007. Development of a WHO growth reference for school-aged children and adolescents. Bull World Health Organ 85: 660–667.
Ndiath MO, Sarr JB, Gaayeb L, Mazenot C, Sougoufara S, Konate L, Remoue F, Hermann E, Trape JF, Riveau G, Sokhna C, 2012. Low and seasonal malaria transmission in the middle Senegal River basin: identification and characteristics of Anopheles vectors. Parasit Vectors 5: 21.
Diallo TO, Remoue F, Gaayeb L, Schacht AM, Charrier N, De Clerck D, Dompnier JP, Pillet S, Garraud O, N'Diaye AA, Riveau G, 2010. Schistosomiasis coinfection in children influences acquired immune response against Plasmodium falciparum malaria antigens. PLoS One 5: e12764.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 1755 | 1504 | 23 |
Full Text Views | 549 | 17 | 0 |
PDF Downloads | 194 | 14 | 0 |