Malnutrition and vaccination in developing countries

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 370, Issue 1671, 2015, Pages

  Prendergast, Andrew J ^a,b,c  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^c Zvitambo Institute for Maternal and Child Health Research   (Zimbabwe)

Author keywords

Children; Developing countries; Immunology; Malnutrition; Vaccination

Indexed keywords

CHILD HEALTH; DEVELOPING WORLD; GLOBAL PERSPECTIVE; IMMUNE RESPONSE; MALNUTRITION; VACCINATION;

HUMAN; IMMUNOLOGY; INFANT; MALNUTRITION; PRESCHOOL CHILD; VACCINATION;

CHILD, PRESCHOOL; HUMANS; INFANT; MALNUTRITION; VACCINATION;

EID: 84929247359     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2014.0141     Document Type: Review

References (81)

1. Black RE et al. 2013 Maternal and child undernutrition and overweight in low-income and middle-income countries. Lancet 382, 427–451. (doi:10.1016/S0140-6736(13)60937-X)
2. Katona P, Katona-Apte J. 2008 The interaction between nutrition and infection. Clin. Infect. Dis. 46, 1582–1588. (doi:10.1086/587658)
3. Christian P et al. 2013 Risk of childhood undernutrition related to small-for-gestational age and preterm birth in low- and middle-income countries. Int. J. Epidemiol. 42, 1340–1355. (doi:10.1093/ije/dyt109)
4. Emergency Nutrition Network. 2014 Review of the links between wasting and stunting. ENN. See http://www.ennonline.net/ourwork/reviews/wastingstunting (accessed 25 August 2014).
5. Black RE, Allen LH, Bhutta ZA, Caulfield LE, de Onis M, Ezzati M, Mathers C, Rivera J. 2008 Maternal and child undernutrition: global and regional exposures and health consequences. Lancet 371, 243–260. (doi:10.1016/S0140-6736(07)61690-0)
6. Kossmann J, Nestel P, Herrera MG, El Amin A, Fawzi WW. 2000 Undernutrition in relation to childhood infections: a prospective study in the Sudan. Eur. J. Clin. Nutr. 54, 463–472. (doi:10.1038/sj.ejcn.1600998)
7. Olofin I, McDonald CM, Ezzati M, Flaxman S, Black RE, Fawzi WW, Caulfield LE, Danaei G. 2013 Associations of suboptimal growth with all-cause and cause-specific mortality in children under five years: a pooled analysis of ten prospective studies. PLoS ONE 8, e64636. (doi:10.1371/journal.pone.0064636)
8. Pelletier DL, Frongillo Jr EA, Schroeder DG, Habicht JP. 1995 The effects of malnutrition on child mortality in developing countries. Bull. World Health Organ. 73, 443–448.
9. Scrimshaw NS, Taylor CE, Gordon AJE. 1968 Interactions of nutrition and infection. Geneva, Switzerland: WHO; Monograph series no. 57.
10. Jones KD, Thitiri J, Ngari M, Berkley JA. 2014 Childhood malnutrition: toward an understanding of infections, inflammation, and antimicrobials. Food Nutr. Bull. 35, S64–S70.
11. Prendergast A, Kelly P. 2012 Enteropathies in the developing world: neglected effects on global health. Am. J. Trop. Med. Hyg. 86, 756–763. (doi:10.4269/ajtmh.2012.11-0743)
12. Rytter MJ, Kolte L, Briend A, Friis H, Christensen VB. 2014 The immune system in children with malnutrition: a systematic review. PLoS ONE 9, e105017. (doi:10.1371/journal.pone.0105017)
13. Cox JA, Beachkofsky T, Dominguez A. 2014 Flaky paint dermatosis. Kwashiorkor. JAMA Dermatol. 150, 85–86. (doi:10.1001/jamadermatol.2013.5520)
14. Freyre EA, Chabes A, Poemape O. 1973 Abnormal Rebuck skin window response in kwashiorkor. J. Pediatr. 82, 523–526. (doi:10.1016/S0022-3476(73)80137-4)
15. Sims RT. 1968 The ultrastructure of depigmented skin in kwashiorkor. Br. J. Dermatol. 80, 822–832. (doi:10.1111/j.1365-2133.1968.tb11952.x)
16. Thavaraj V, Sesikeran B. 1989 Histopathological changes in skin of children with clinical protein energy malnutrition before and after recovery. J. Trop. Pediatr. 35, 105–108. (doi:10.1093/tropej/35.3.105)
17. Burman D. 1965 The jejunal mucosa in kwashiorkor. Arch. Dis. Child. 40, 526–531. (doi:10.1136/adc.40.213.526)
18. Desai HG, Borkar AV, Pathare SM, Dighe PK, Jeejeebhoy KN. 1969 ‘Flat’ jejunal mucosa in the tropics. Indian J. Med. Sci. 23, 1–5.
19. Schenk EA, Samloff IM, Klipstein FA. 1968 Morphology of small bowel biopsies. Am. J. Clin. Nutr. 21, 944–961.
20. Campbell DI, Elia M, Lunn PG. 2003 Growth faltering in rural Gambian infants is associated with impaired small intestinal barrier function, leading to endotoxemia and systemic inflammation. J. Nutr. 133, 1332–1338.
21. Lunn PG, Northrop-Clewes CA, Downes RM. 1991 Intestinal permeability, mucosal injury, and growth faltering in Gambian infants. Lancet 338, 907–910. (doi:10.1016/0140-6736(91)91772-M)
22. Kosek M et al. 2013 Fecal markers of intestinal inflammation and permeability associated with the subsequent acquisition of linear growth deficits in infants. Am. J. Trop. Med. Hyg. 88, 390–396. (doi:10.4269/ajtmh.2012.12-0549)
23. Lin A et al. 2013 Household environmental conditions are associated with enteropathy and impaired growth in rural Bangladesh. Am. J. Trop. Med. Hyg. 89, 130–137. (doi:10.4269/ajtmh.12-0629)
24. Prendergast AJ et al. 2014 Stunting is characterized by chronic inflammation in Zimbabwean infants. PLoS ONE 9, e86928. (doi:10.1371/journal.pone.0086928)
25. Keusch GT et al. 2013 Implications of acquired environmental enteric dysfunction for growth and stunting in infants and children living in low- and middle-income countries. Food Nutr. Bull. 34, 357–364.
26. Gilmartin JA, Petri Jr WA. 2015 Exploring the role of environmental enteropathy in malnutrition, infant development and oral vaccine response. Phil. Trans. R. Soc. B 370, 20140143. (doi:10.1098/rstb.2014.0143)
27. Berkley JA et al. 2005 Bacteremia among children admitted to a rural hospital in Kenya. N. Engl. J. Med. 352, 39–47. (doi:10.1056/NEJMoa040275)
28. Hughes SM, Amadi B, Mwiya M, Nkamba H, Tomkins A, Goldblatt D. 2009 Dendritic cell anergy results from endotoxemia in severe malnutrition. J. Immunol. 183, 2818–2826. (doi:10.4049/jimmunol.0803518)
29. Chatraw JH, Wherry EJ, Ahmed R, Kapasi ZF. 2008 Diminished primary CD8 T cell response to viral infection during protein energy malnutrition in mice is due to changes in microenvironment and low numbers of viral-specific CD8 T cell precursors. J. Nutr. 138, 806–812.
30. Iyer SS, Chatraw JH, Tan WG, Wherry EJ, Becker TC, Ahmed R, Kapasi ZF. 2012 Protein energy malnutrition impairs homeostatic proliferation of memory CD8 T cells. J. Immunol. 188, 77–84. (doi:10.4049/jimmunol.1004027)
31. Taylor AK et al. 2013 Protein energy malnutrition decreases immunity and increases susceptibility to influenza infection in mice. J. Infect. Dis. 207, 501–510. (doi:10.1093/infdis/jis527)
32. 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. (doi:10.3945/jn.109.105312)
33. 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.
34. Greenwood BM, Bradley-Moore AM, Bradley AK, Kirkwood BR, Gilles HM. 1986 The immune response to vaccination in undernourished and wellnourished Nigerian children. Ann. Trop. Med. Parasitol. 80, 537–544.
35. Kielmann AA, Uberoi IS, Chandra RK, Mehra VL. 1976 The effect of nutritional status on immune capacity and immune responses in preschool children in a rural community in India. Bull. World Health Organ. 54, 477–483.
36. Salimonu LS, Johnson AO, Williams AI, Adeleye GI, Osunkoya BO. 1982 Lymphocyte subpopulations and antibody levels in immunized malnourished children. Br. J. Nutr. 48, 7–14. (doi:10.1079/BJN19820082)
37. Gaayeb L et al. 2014 Immune response to Bordetella pertussis is associated with season and undernutrition in Senegalese children. Vaccine 32, 3431–3437. (doi:10.1016/j.vaccine.2014.03.086)
38. el-Gamal Y, Aly RH, Hossny E, Afify E, el-Taliawy D. 1996 Response of Egyptian infants with protein calorie malnutrition to hepatitis B vaccination. J. Trop. Pediatr. 42, 144–145. (doi:10.1093/tropej/42.3.144)
39. Asturias EJ et al. 2009 Differences in the immune response to hepatitis B and Haemophilus influenzae type b vaccines in Guatemalan infants by ethnic group and nutritional status. Vaccine 27, 3650–3654. (doi:10.1016/j.vaccine.2009.03.035)
40. Moore SE, Goldblatt D, Bates CJ, Prentice AM. 2003 Impact of nutritional status on antibody responses to different vaccines in undernourished Gambian children. Acta Paediatr. 92, 170–176. (doi:10.1111/j.1651-2227.2003.tb00522.x)
41. Coovadia HM et al. 1974 An evaluation of factors associated with the depression of immunity in malnutrition and in measles. Am. J. Clin. Nutr. 27, 665–669.
42. Dossetor J, Whittle HC, Greenwood BM. 1977 Persistent measles infection in malnourished children. Br. Med. J. 1, 1633–1635. (doi:10.1136/bmj.1.6077.1633)
43. Suskind R et al. 1976 Immunoglobulins and antibody response in children with protein-calorie malnutrition. Am. J. Clin. Nutr. 29, 836–841.
44. Reddy V, Srikantia SG. 1964 Antibody response in Kwashiorkor. Indian J. Med. Res. 52, j1154–j1158.
45. Mathews JD, Mackay IR, Whittingham S, Malcolm LA. 1972 Protein supplementation and enhanced antibody-producing capacity in New Guinean school-children. Lancet 2, 675–677. (doi:10.1016/S0140-6736(72)92086-7)
46. Neumann CG et al. 1975 Immunologic responses in malnourished children. Am. J. Clin. Nutr. 28, 89–104.
47. Mohammed I, Damisah MM. 1982 The immunological response to polyvalent meningococcal vaccine in Bauchi State, Nigeria. Trans. R. Soc. Trop. Med. Hyg. 76, 351–353. (doi:10.1016/0035-9203(82)90188-2)
48. Greenwood BM, Bradley AK, Blakebrough IS, Whittle HC, Marshall TF, Gilles HM. 1980 The immune response to a meningococcal polysaccharide vaccine in an African village. Trans. R. Soc. Trop. Med. Hyg. 74, 340–346. (doi:10.1016/0035-9203(80)90095-4)
49. Abbassy AS et al. 1974 Studies of cell-mediated immunity and allergy in protein energy malnutrition. I. Cell-mediated delayed hypersensitivity. J. Trop. Med. Hyg. 77, 13–17.
50. Harland PS. 1965 Tuberculin reactions in malnourished children. Lancet 2, 719–721. (doi:10.1016/S0140-6736(65)90457-5)
51. McMurray DN, Loomis SA, Casazza LJ, Rey H, Miranda R. 1981 Development of impaired cellmediated immunity in mild and moderate malnutrition. Am. J. Clin. Nutr. 34, 68–77.
52. McMurray DN, Watson RR, Reyes MA. 1981 Effect of renutrition on humoral and cell-mediated immunity in severely malnourished children. Am. J. Clin. Nutr. 34, 2117–2126.
53. Seth V, Kukreja N, Sundaram KR, Malaviya AN. 1981 Delayed hypersensitivity after BCG in preschool children in relation to their nutritional status. Indian J. Med. Res. 74, 392–398.
54. Ekunwe EO. 1985 Malnutrition and seroconversion following measles immunization. J. Trop. Pediatr. 31, 290–291. (doi:10.1093/tropej/31.6.290)
55. Halsey NA, Boulos R, Mode F, Andre J, Bowman L, Yaeger RG, Toureau S, Rohde J, Boulos C. 1985 Response to measles vaccine in Haitian infants 6 to 12 months old. Influence of maternal antibodies, malnutrition, and concurrent illnesses. N. Engl. J. Med. 313, 544–549. (doi:10.1056/NEJM198508293130904)
56. Idris S, El Seed AM. 1983 Measles vaccination in severely malnourished Sudanese children. Ann. Trop. Paediatr. 3, 63–67.
57. Ifekwunigwe AE, Grasset N, Glass R, Foster S. 1980 Immune responses to measles and smallpox vaccinations in malnourished children. Am. J. Clin. Nutr. 33, 621–624.
58. Marshall R, Habicht JP, Landrigan PJ, Foege WH, Delgado H. 1974 Effectiveness of measles vaccine given simultaneously with DTP. J. Trop. Pediatr. Environ. Child Health 20, 126–129. (doi:10.1093/tropej/20.3.126)
59. McMurray DN, Loomis SA, Casazza LJ, Rey H. 1979 Influence of moderate malnutrition on morbidity and antibody response following vaccination with live, attenuated measles virus vaccine. Bull. Pan. Am. Health Organ. 13, 52–57.
60. Powell GM. 1982 Response to live attenuated measles vaccine in children with severe kwashiorkor. Ann. Trop. Paediatr. 2, 143–145.
61. Wesley A, Coovadia HM, Watson AR. 1979 Immunization against measles in children at risk for severe disease. Trans. R. Soc. Trop. Med. Hyg. 73, 710–715. (doi:10.1016/0035-9203(79)90026-9)
62. Kizito D et al. 2013 Factors affecting the infant antibody response to measles immunisation in Entebbe-Uganda. BMC Public Health 13, 619. (doi:10.1186/1471-2458-13-619)
63. Pretorius PJ, De Villiers LS. 1962 Antibody response in children with protein malnutrition. Am. J. Clin. Nutr. 10, 379–383.
64. WHO Publication 2012 Pneumococcal vaccines WHO position paper–recommendations. Vaccine 30, 4717–4718. (doi:10.1016/j.vaccine.2012.04.093)
65. von Gottberg A et al. 2014 Effects of vaccination on invasive pneumococcal disease in South Africa. N. Engl. J. Med. 371, 1889–1899. (doi:10.1056/NEJMoa1401914)
66. Cohen C et al. 2014 Effectiveness of 7-valent pneumococcal conjugate vaccine against invasive pneumococcal disease in HIV-infected and -uninfected children in South Africa: a matched case-control study. Clin. Infect. Dis. 59, 808–818. (doi:10.1093/cid/ciu431)
67. Satyanarayana K, Bhaskaram P, Seshu VC, Reddy V. 1980 Influence of nutrition on postvaccinial tuberculin sensitivity. Am. J. Clin. Nutr. 33, 2334–2337.
68. Heyworth B. 1977 Delayed hypersensitivity to PPD-S following BCG vaccination in African children: an 18-month field study. Trans. R. Soc. Trop. Med. Hyg. 71, 251–253. (doi:10.1016/0035-9203(77)90019-0)
69. Azzopardi P, Bennett CM, Graham SM, Duke T. 2009 Bacille Calmette-Guerin vaccine-related disease in HIV-infected children: a systematic review. Int. J. Tuberc. Lung Dis. 13, 1331–1344.
70. Patel SY, Doffinger R, Barcenas-Morales G, Kumararatne DS. 2008 Genetically determined susceptibility to mycobacterial infection. J. Clin. Pathol. 61, 1006–1012. (doi:10.1136/jcp.2007.051201)
71. Ishikawa LL et al. 2012 Is the BCG vaccine safe for undernourished individuals? Clin. Dev. Immunol. 2012, 673186. (doi:10.1155/2012/673186)
72. Nobrega C, Roque S, Nunes-Alves C, Coelho A, Medeiros I, Castro AG, Appelberg R, Correia-Neves M. 2010 Dissemination of mycobacteria to the thymus renders newly generated T cells tolerant to the invading pathogen. J. Immunol. 184, 351–358. (doi:10.4049/jimmunol.0902152)
73. World Health Organization. 1999 Management of severe malnutrition: a manual for physicians and other senior health workers. Geneva, Switzerland: WHO.
74. Prendergast AJ, Humphrey JH. 2014 The stunting syndrome in developing countries. Paediatr. Int. Child Health 34, 250–265. (doi:10.1179/2046905514Y.0000000158)
75. Bhutta ZA, Das JK, Rizvi A, Gaffey MF, Walker N, Horton S, Webb P, Lartey A, Black RE. 2013 Evidence-based interventions for improvement of maternal and child nutrition: what can be done and at what cost? Lancet 382, 452–477. (doi:10.1016/S0140-6736(13)60996-4)
76. Pronyk PM et al. 2012 The effect of an integrated multisector model for achieving the millennium development goals and improving child survival in rural sub-Saharan Africa: a non-randomised controlled assessment. Lancet 379, 2179–2188. (doi:10.1016/S0140-6736(12)60207-4)
77. Victora CG, Aquino EM, do Carmo Leal M, Monteiro CA, Barros FC, Szwarcwald CL. 2011 Maternal and child health in Brazil: progress and challenges. Lancet 377, 1863–1876. (doi:10.1016/S0140-6736(11)60138-4)
78. Feller AJ, Zaman K, Lewis KD, Hossain I, Yunus M, Sack DA. 2012 Malnutrition levels among vaccinated and unvaccinated children between 2 and 3 years of age following enrollment in a randomized clinical trial with the pentavalent rotavirus vaccine (PRV) in Bangladesh. Vaccine 30, A101–A105. (doi:10.1016/j.vaccine.2011.09.065)
79. Frongillo Jr EA, de Onis M, Hanson KM. 1997 Socioeconomic and demographic factors are associated with worldwide patterns of stunting and wasting of children. J. Nutr. 127, 2302–2309.
80. Milman A, Frongillo EA, de Onis M, Hwang JY. 2005 Differential improvement among countries in child stunting is associated with long-term development and specific interventions. J. Nutr. 135, 1415–1422.
81. Anekwe TD, Kumar S. 2012 The effect of a vaccination program on child anthropometry: evidence from India’s Universal Immunization Program. J. Public Health 34, 489–497. (doi:10.1093/pubmed/fds032)