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Nutrition and Diarrheal Disease and Enteric Pathogens

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Nutrition and Infectious Diseases

Part of the book series: Nutrition and Health ((NH))

Abstract

Malnutrition, a public health problem for the low- and middle-income countries, mainly affects young children. It contributes significantly to their morbidity and mortality and makes them vulnerable to diarrheal diseases and enteric infections through various mechanisms. Protein calorie and micronutrient deficiencies increase the risk of exposure to diarrhea causing pathogens through placing affected persons in high-risk environments, e.g., hospitals. It also disrupts immune mechanisms at various levels leading to diminished ability to prevent pathogens from entering the body and mounting a sufficiently strong and appropriate response when required. For example, malnutrition reduces the capacity to maintain a robust gut mucosal barrier needed to prevent intrusion of microbes deeper into the body, and it diminishes the production of inflammatory response hormones, cells, and antibodies that are needed to eliminate the invading organisms. Therefore, enteric infections progress faster, have greater severity, and worse outcomes. Even when timely treatments are provided, they are less effective in malnourished compared with well-nourished individuals. Antimicrobial interventions are frequently required, which though lifesaving in most instances, are known to deteriorate the already stressed gut microbiome, worsening the gut’s resistance capabilities. Greater harm inflicted by the infections in the presence of malnutrition further aggravates existing malnutrition initiating a vicious cycle. It is important to note, however, that some deficiencies reduce the risk of disease. For example, the risk of amebic infection is lower in the presence of iron deficiency and that some components of immunity are retained despite lack of energy. Further research into specific areas is required to identify new intervention targets.

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Abbreviations

AhR:

Aryl Hydrocarbon Receptor

APP:

Acute phase protein

C:

Complement

CD2:

Cluster of Differentiation 2

CD69:

Cluster of Differentiation 69

CRP:

C-reactive protein

DALY:

Disability Adjusted Life Year

DC:

Dendritic cell

DNA:

Deoxyribonucleic acid

EED:

Environment Enteric Dysfunction

EPEC:

Enteropathogenic Escherichia coli

ETEC:

Enterotoxigenic Escherichia coli

GALT:

Gut Associated Lymphoid Tissue

IFN-γ:

Interferon gamma

IgA:

Immunoglobulin A

IL:

Interleukin

ILC :

Innate Lymphoid Cell

IMCI:

Integrated management of childhood illnesses

LPS:

Lipopolysaccharide

MAM:

Moderate acute malnutrition

MHC:

Major histocompatibility complex molecules

NK:

Natural Killer cell

NO:

Nitric oxide

PEM:

Protein-energy malnutrition

PGE2:

Prostaglandin E2

RUTF:

Ready to use therapeutic food

SAM:

Severe acute malnutrition

SDG:

Sustainable development goal

SDI:

Sociodemographic Index

SIgA:

Serum Immunoglobulin A

Th1:

Helper T cell (Type 1)

WHO:

World Health Organization

References

  1. WHO. Diarrhoeal disease 2017. Available from: https://www.who.int/news-room/fact-sheets/detail/diarrhoeal-disease.

  2. Berkley JA. Bacterial infections and nutrition - a primer. In: Humphries DL, Scott ME, Vermund SH, editors. Nutrition and infectious disease: shifting the clinical paradigm: Humana Press; 2020.

    Google Scholar 

  3. Green WD, Karlsson EA, Beck MA. Viral infections and nutrition: influenza virus as a case study. In: Humphries DL, Scott ME, Vermund SH, editors. Nutrition and infectious disease: shifting the clinical paradigm: Humana Press; 2020.

    Google Scholar 

  4. Wiser MF. Nutrition and protozoan pathogens of humans -- a primer. In: Humphries DL, Scott ME, Vermund SH, editors. Nutrition and infectious diseases: shifting the clinical Paradigm2020.

    Google Scholar 

  5. Geary TG, Haque M. Human helminth infections. In: Humphries DL, Scott ME, Vermund SH, editors. Nutrition and infectious disease: shifting the clinical paradigm: Humana Press; 2020.

    Google Scholar 

  6. Defeat DD. Diarrhea and enteric illnesses 2017. Available from: https://www.defeatdd.org/article/diarrhea-and-enteric-illnesses.

  7. Emory Institute of Drug Development. What is Diarrheal Diseases 2019. Available from: http://www.globalhealthprimer.emory.edu/diseases/diarrheal-diseases.html.

  8. Institute for Health Metrics and Evaluation. Findings from the Global Burden of Disease Study 2017. Seattle: IHME, 2018.

    Google Scholar 

  9. Collaborators GBDDD. Estimates of global, regional, and national morbidity, mortality, and aetiologies of diarrhoeal diseases: a systematic analysis for the global burden of disease study 2015. Lancet Infect Dis. 2017;17(9):909–48.

    Article  Google Scholar 

  10. Checkley W, Buckley G, Gilman RH, Assis AM, Guerrant RL, Morris SS, et al. Multi-country analysis of the effects of diarrhoea on childhood stunting. Int J Epidemiol. 2008;37(4):816–30.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Global burden of disease collaborative network. Global burden of disease study 2017 (GBD 2017) results. In: Institute for Health Metrics and Evaluation (IHME). Seattle; 2018.

    Google Scholar 

  12. Liu J, Platts-Mills JA, Juma J, Kabir F, Nkeze J, Okoi C, et al. Use of quantitative molecular diagnostic methods to identify causes of diarrhoea in children: a reanalysis of the GEMS case-control study. Lancet. 2016;388(10051):1291–301.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Walker CLF, Rudan I, Liu L, Nair H, Theodoratou E, Bhutta ZA, et al. Global burden of childhood pneumonia and diarrhoea. Lancet. 2013;381(9875):1405–16.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Glass RI, Guttmacher AE, Black RE. Ending preventable child death in a generation. JAMA. 2012;308(2):141–2.

    Article  CAS  PubMed  Google Scholar 

  15. Rudan I, El Arifeen S, Black RE, Campbell H. Childhood pneumonia and diarrhoea: setting our priorities right. Lancet Infect Dis. 2007;7(1):56–61.

    Article  PubMed  Google Scholar 

  16. Ganguly E, Sharma PK, Bunker CH. Prevalence and risk factors of diarrhea morbidity among under-five children in India: a systematic review and meta-analysis. Indian J Child Health (Bhopal). 2015;2(4):152–60.

    Article  Google Scholar 

  17. Rice AL, Sacco L, Hyder A, Black RE. Malnutrition as an underlying cause of childhood deaths associated with infectious diseases in developing countries. Bull World Health Organ. 2000;78(10):1207–21.

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Initiatives D. Global nutrition report: shining a light to spur action on nutrition. Bristoal; 2018. p. 2018.

    Google Scholar 

  19. Stephensen CB. Primer on immune response and Interface with malnutrition. In: Humphries DL, Scott ME, Vermund SH, editors. Nutrition and infectious disease: shifting the clinical paradigm: Humana Press; 2020.

    Google Scholar 

  20. DALYs GBD, Collaborators H. Global, regional, and national disability-adjusted life-years (DALYs) for 359 diseases and injuries and healthy life expectancy (HALE) for 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet. 2018;392(10159):1859–922.

    Article  Google Scholar 

  21. WHO. Global Health Risks: Mortality and burden of disease attributable to selected major risks. Geneva, Switzerland: WHO, 2009 Contract No.: ISBN 978 92 4 156387 1.

    Google Scholar 

  22. Barffour MA, Humphries DL. Core principles: infectious disease risk in relation to macro and micronutrient status. In: Humphries DL, Scott ME, Vermund SH, editors. Nutrition and infectious disease: shifting the clinical paradigm: Humana Press; 2020.

    Google Scholar 

  23. Brown KH. Diarrhea and malnutrition. J Nutr. 2003;133(1):328S–32S.

    Article  PubMed  Google Scholar 

  24. Bailey RL, West KP Jr, Black RE. The epidemiology of global micronutrient deficiencies. Ann Nutr Metab. 2015;66(Suppl 2):22–33.

    Article  CAS  PubMed  Google Scholar 

  25. Paganini D, Uyoga MA, Zimmermann MB. Iron fortification of foods for infants and children in low-income countries: effects on the gut microbiome, gut inflammation, and diarrhea. Nutrients. 2016;8(8):494.

    Article  PubMed Central  CAS  Google Scholar 

  26. Imdad A, Mayo-Wilson E, Herzer K, Bhutta ZA. Vitamin a supplementation for preventing morbidity and mortality in children from six months to five years of age. Cochrane Database Syst Rev. 2017;3(3):CD008524.

    PubMed  Google Scholar 

  27. Levy A, Fraser D, Rosen SD, Dagan R, Deckelbaum RJ, Coles C, et al. Anemia as a risk factor for infectious diseases in infants and toddlers: results from a prospective study. Eur J Epidemiol. 2005;20(3):277–84.

    Article  PubMed  Google Scholar 

  28. Rytter MJ, Kolte L, Briend A, Friis H, Christensen VB. The immune system in children with malnutrition--a systematic review. PLoS One. 2014;9(8):e105017.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Schneider SM, Hebuterne X. Is malnutrition a risk factor for nosocomial infections? Rev Med Interne. 2006;27(7):515–8.

    Article  PubMed  Google Scholar 

  30. Woerther PL, Angebault C, Jacquier H, Hugede HC, Janssens AC, Sayadi S, et al. Massive increase, spread, and exchange of extended spectrum beta-lactamase-encoding genes among intestinal Enterobacteriaceae in hospitalized children with severe acute malnutrition in Niger. Clin Infect Dis. 2011;53(7):677–85.

    Article  CAS  PubMed  Google Scholar 

  31. Manary MJ. Local production and provision of ready-to-use therapeutic food for the treatment of severe childhood malnutrition. 2005.

    Google Scholar 

  32. World Health O. Complementary feeding: family foods for breastfed children. 2000.

    Google Scholar 

  33. Boatbil C, Guure C, Ayoung A. Impact of belief systems on the management of child malnutrition: the case of talensis of northern ghana 2014.

    Google Scholar 

  34. Verkerke H, Sobuz S, Ma JZ, Petri SE, Reichman D, Qadri F, et al. Malnutrition is associated with protection from rotavirus diarrhea: evidence from a longitudinal birth cohort study in Bangladesh. J Clin Microbiol. 2016;54(10):2568–74.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Tickell KD, Pavlinac PB, John-Stewart GC, Denno DM, Richardson BA, Naulikha JM, et al. Impact of childhood nutritional status on pathogen prevalence and severity of acute diarrhea. Am J Trop Med Hyg. 2017;97(5):1337–44.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Ezenwa VO. Co-infection and nutrition: integrating ecological and epidemiological perspectives. In: Humphries DL, Scott ME, Vermund SH, editors. Nutrition and infectious disease: shifting the clinical paradigm: Springer; 2020.

    Google Scholar 

  37. Murray MJ, Murray A, Murray CJ. The salutary effect of milk on amoebiasis and its reversal by iron. Br Med J. 1980;280(6228):1351–2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Lee J, Park SJ, Yong TS. Effect of iron on adherence and cytotoxicity of Entamoeba histolytica to CHO cell monolayers. Korean J Parasitol. 2008;46(1):37–40.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Bourke CD, Berkley JA, Prendergast AJ. Immune dysfunction as a cause and consequence of malnutrition. Trends Immunol. 2016;37(6):386–98.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Turner JR. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol. 2009;9(11):799–809.

    Article  CAS  PubMed  Google Scholar 

  41. Murch S. Gastrointestinal Mucosal Immunology and Mechanisms of Inflammation. In: Wyllie Robert, Jeffery S. Hyams, Kay M, editors. Pediatric gastrointestinal and liver disease. 4th ed: Saint Louis: W.B. Saunders; 2011. p. 50.

    Google Scholar 

  42. Genton L, Cani PD, Schrenzel J. Alterations of gut barrier and gut microbiota in food restriction, food deprivation and protein-energy wasting. Clin Nutr. 2015;34(3):341–9.

    Article  CAS  PubMed  Google Scholar 

  43. Omoike I, Lindquist B, Abud R, Merrick J, Lebenthal E. The effect of protein-energy malnutrition and refeeding on the adherence of Salmonella typhimurium to small intestinal mucosa and isolated enterocytes in rats. J Nutr. 1990;120(4):404–11.

    Article  CAS  PubMed  Google Scholar 

  44. Bansal D, Ave P, Kerneis S, Frileux P, Boche O, Baglin AC, et al. An ex-vivo human intestinal model to study Entamoeba histolytica pathogenesis. PLoS Negl Trop Dis. 2009;3(11):e551.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Cornick S, Tawiah A, Chadee K. Roles and regulation of the mucus barrier in the gut. Tissue Barriers. 2015;3(1–2):e982426.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Mondal D, Minak J, Alam M, Liu Y, Dai J, Korpe P, et al. Contribution of enteric infection, altered intestinal barrier function, and maternal malnutrition to infant malnutrition in Bangladesh. Clin Infect Dis. 2012;54(2):185–92.

    Article  PubMed  Google Scholar 

  47. Campbell DI, Elia M, Lunn PG. Growth faltering in rural Gambian infants is associated with impaired small intestinal barrier function, leading to endotoxemia and systemic inflammation. J Nutr. 2003;133(5):1332–8.

    Article  CAS  PubMed  Google Scholar 

  48. Rho S, Kim H, Shim SH, Lee SY, Kim MJ, Yang BG, et al. Protein energy malnutrition alters mucosal IgA responses and reduces mucosal vaccine efficacy in mice. Immunol Lett. 2017;190:247–56.

    Article  CAS  PubMed  Google Scholar 

  49. Martens EC, Neumann M, Desai MS. Interactions of commensal and pathogenic microorganisms with the intestinal mucosal barrier. Nat Rev Microbiol. 2018;16(8):457–70.

    Article  CAS  PubMed  Google Scholar 

  50. Rodriguez L, Cervantes E, Ortiz R. Malnutrition and gastrointestinal and respiratory infections in children: a public health problem. Int J Environ Res Public Health. 2011;8(4):1174–205.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Ibrahim MK, Zambruni M, Melby CL, Melby PC. Impact of childhood malnutrition on host defense and infection. Clin Microbiol Rev. 2017;30(4):919–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Semba RD. The role of vitamin A and related retinoids in immune function. 1998.

    Google Scholar 

  53. Maciel AA, Oria RB, Braga-Neto MB, Braga AB, Carvalho EB, Lucena HB, et al. Role of retinol in protecting epithelial cell damage induced by Clostridium difficile toxin a. Toxicon. 2007;50(8):1027–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Lazzerini M, Wanzira H. Oral zinc for treating diarrhoea in children. Cochrane Database Syst Rev. 2016;(12, 12):CD005436.

    Google Scholar 

  55. Tuerk MJ, Fazel N. Zinc deficiency. Curr Opin Gastroenterol. 2009;25(2):136–43.

    Article  CAS  PubMed  Google Scholar 

  56. Podany AB, Wright J, Lamendella R, Soybel DI, Kelleher SL. ZnT2-mediated zinc import into Paneth cell granules is necessary for coordinated secretion and Paneth cell function in mice. Cell Mol Gastroenterol Hepatol. 2016;2(3):369–83.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Hughes S, Kelly P. Interactions of malnutrition and immune impairment, with specific reference to immunity against parasites. Parasite Immunol. 2006;28(11):577–88.

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Castro IC, Oliveira BB, Slowikowski JJ, Coutinho BP, Siqueira FJ, Costa LB, et al. Arginine decreases Cryptosporidium parvum infection in undernourished suckling mice involving nitric oxide synthase and arginase. Nutrition. 2012;28(6):678–85.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Lima NL, Soares AM, Mota RM, Monteiro HS, Guerrant RL, Lima AA. Wasting and intestinal barrier function in children taking alanyl-glutamine-supplemented enteral formula. J Pediatr Gastroenterol Nutr. 2007;44(3):365–74.

    Article  CAS  PubMed  Google Scholar 

  60. Denno DM, Tarr PI, Nataro JP. Environmental enteric dysfunction: a case definition for intervention trials. Am J Trop Med Hyg. 2017;97(6):1643–6.

    Article  PubMed  PubMed Central  Google Scholar 

  61. Keusch GT, Denno DM, Black RE, Duggan C, Guerrant RL, Lavery JV, et al. Environmental enteric dysfunction: pathogenesis, diagnosis, and clinical consequences. Clin Infect Dis. 2014;59(Suppl 4):S207–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Bartelt LA, Bolick DT, Guerrant RL. Disentangling microbial mediators of malnutrition: modeling environmental enteric dysfunction. Cell Mol Gastroenterol Hepatol. 2019;7(3):692–707.

    Article  PubMed  PubMed Central  Google Scholar 

  63. Crane RJ, Jones KD, Berkley JA. Environmental enteric dysfunction: an overview. Food Nutr Bull. 2015;36(1 Suppl):S76–87.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Goto R, Panter-Brick C, Northrop-Clewes CA, Manahdhar R, Tuladhar NR. Poor intestinal permeability in mildly stunted Nepali children: associations with weaning practices and Giardia lamblia infection. Br J Nutr. 2002;88(2):141–9.

    Article  CAS  PubMed  Google Scholar 

  65. Weisz AJ, Manary MJ, Stephenson K, Agapova S, Manary FG, Thakwalakwa C, et al. Abnormal gut integrity is associated with reduced linear growth in rural Malawian children. J Pediatr Gastroenterol Nutr. 2012;55(6):747–50.

    Article  PubMed  Google Scholar 

  66. Ballinger A, El-Haj T, Perrett D, Turvill J, Obeid O, Dryden S, et al. The role of medial hypothalamic serotonin in the suppression of feeding in a rat model of colitis. Gastroenterology. 2000;118(3):544–53.

    Article  CAS  PubMed  Google Scholar 

  67. Garcia SE, Kaiser LL, Dewey KG. Self-regulation of food intake among rural Mexican preschool children. Eur J Clin Nutr. 1990;44(5):371–80.

    CAS  PubMed  Google Scholar 

  68. Prendergast AJ, Rukobo S, Chasekwa B, Mutasa K, Ntozini R, Mbuya MN, et al. Stunting is characterized by chronic inflammation in Zimbabwean infants. PLoS One. 2014;9(2):e86928.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  69. Kosek M, Haque R, Lima A, Babji S, Shrestha S, Qureshi S, et al. Fecal markers of intestinal inflammation and permeability associated with the subsequent acquisition of linear growth deficits in infants. Am J Trop Med Hyg. 2013;88(2):390–6.

    Article  PubMed  PubMed Central  Google Scholar 

  70. Korpe PS, Petri WA Jr. Environmental enteropathy: critical implications of a poorly understood condition. Trends Mol Med. 2012;18(6):328–36.

    Article  PubMed  PubMed Central  Google Scholar 

  71. Guerrant RL, Oria RB, Moore SR, Oria MO, Lima AA. Malnutrition as an enteric infectious disease with long-term effects on child development. Nutr Rev. 2008;66(9):487–505.

    Article  PubMed  Google Scholar 

  72. Patriarca PA, Wright PF, John TJ. Factors affecting the immunogenicity of oral poliovirus vaccine in developing countries: review. Rev Infect Dis. 1991;13(5):926–39.

    Article  CAS  PubMed  Google Scholar 

  73. Soares-Weiser K, Maclehose H, Bergman H, Ben-Aharon I, Nagpal S, Goldberg E, et al. Vaccines for preventing rotavirus diarrhoea: vaccines in use. Cochrane Database Syst Rev. 2012;11:CD008521.

    PubMed  Google Scholar 

  74. Murphy K, Travers P, Walport M, Janeway C. Janeway's immunobiology. New York: Garland Science; 2008.

    Google Scholar 

  75. Bhutta ZA, Das JK, Walker N, Rizvi A, Campbell H, Rudan I, et al. Interventions to address deaths from childhood pneumonia and diarrhoea equitably: what works and at what cost? Lancet. 2013;381(9875):1417–29.

    Article  PubMed  Google Scholar 

  76. Gilman RH, Partanen R, Brown KH, Spira WM, Khanam S, Greenberg B, et al. Decreased gastric acid secretion and bacterial colonization of the stomach in severely malnourished Bangladeshi children. Gastroenterology. 1988;94(6):1308–14.

    Article  CAS  PubMed  Google Scholar 

  77. Shashidhar S, Shah SB, Acharya PT. Gastric acid, pH and pepsin in healthy and protein calorie malnourished children. Indian J Pediatr. 1976;43(341):145–51.

    Article  CAS  PubMed  Google Scholar 

  78. Adesola AO. The influence of severe protein deficiency (kwashiorkor) on gastric acid secretion in Nigerian children. Br J Surg. 1968;55(11):866.

    CAS  PubMed  Google Scholar 

  79. Maffei H, Nobrega F. Gastric pH and microflora of normal and diarrhoeic infants. Gut. 1975;16(9):719–26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Peters-Golden M, Canetti C, Mancuso P, Coffey MJ. Leukotrienes: underappreciated mediators of innate immune responses. J Immunol. 2005;174(2):589–94.

    Article  CAS  PubMed  Google Scholar 

  81. Jahoor F, Badaloo A, Reid M, Forrester T. Protein metabolism in severe childhood malnutrition. Ann Trop Paediatr. 2008;28(2):87–101.

    Article  PubMed  Google Scholar 

  82. Haller L, Zubler RH, Lambert PH. Plasma levels of complement components and complement haemolytic activity in protein-energy malnutrition. Clin Exp Immunol. 1978;34(2):248–52.

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Haque R, Mondal D, Shu J, Roy S, Kabir M, Davis AN, et al. Correlation of interferon-gamma production by peripheral blood mononuclear cells with childhood malnutrition and susceptibility to amebiasis. Am J Trop Med Hyg. 2007;76(2):340–4.

    Article  CAS  PubMed  Google Scholar 

  84. Hamano S, Asgharpour A, Stroup SE, Wynn TA, Leiter EH, Houpt E. Resistance of C57BL/6 mice to amoebiasis is mediated by nonhemopoietic cells but requires hemopoietic IL-10 production. J Immunol. 2006;177(2):1208–13.

    Article  CAS  PubMed  Google Scholar 

  85. Schonland M. Depression of immunity in protein-calorie malnutrition: a post-mortem study. J Trop Pediatr Environ Child Health. 1972;18(3):217–24.

    CAS  PubMed  Google Scholar 

  86. Pretorius PJ, De Villiers LS. Antibody response in children with protein malnutrition. Am J Clin Nutr. 1962;10:379–83.

    Article  CAS  PubMed  Google Scholar 

  87. Salimonu LS, Johnson AO, Williams AI, Adeleye GI, Osunkoya BO. Lymphocyte subpopulations and antibody levels in immunized malnourished children. Br J Nutr. 1982;48(1):7–14.

    Article  CAS  PubMed  Google Scholar 

  88. Awdeh ZL, Kanawati AK, Alami SY. Antibody response in marasmic children during recovery. Acta Paediatr Scand. 1977;66(6):689–92.

    Article  CAS  PubMed  Google Scholar 

  89. el-Gamal Y, Aly RH, Hossny E, Afify E, el-Taliawy D. Response of Egyptian infants with protein calorie malnutrition to hepatitis B vaccination. J Trop Pediatr. 1996;42(3):144–5.

    Article  CAS  PubMed  Google Scholar 

  90. Hafez M, Aref GH, Mehareb SW, Kassem AS, El-Tahhan H, Rizk Z, et al. Antibody production and complement system in protein energy malnutrition. J Trop Med Hyg. 1977;80(2):36–9.

    CAS  PubMed  Google Scholar 

  91. Powell GM. Response to live attenuated measles vaccine in children with severe kwashiorkor. Ann Trop Paediatr. 1982;2(3):143–5.

    Article  CAS  PubMed  Google Scholar 

  92. Brown RE, Katz M. Failure of antibody production to yellow fever vaccine in children with kwashiorkor. Trop Geogr Med. 1966;18(2):125–8.

    CAS  PubMed  Google Scholar 

  93. Brown RE, Katz M. Antigenic stimulation in undernourished children. East Afr Med J. 1965;42:221–32.

    CAS  PubMed  Google Scholar 

  94. Wesley A, Coovadia HM, Watson AR. Immunization against measles in children at risk for severe disease. Trans R Soc Trop Med Hyg. 1979;73(6):710–5.

    Article  CAS  PubMed  Google Scholar 

  95. Idris S, El Seed AM. Measles vaccination in severely malnourished Sudanese children. Ann Trop Paediatr. 1983;3(2):63–7.

    Article  CAS  PubMed  Google Scholar 

  96. Suskind R, Sirishinha S, Vithayasai V, Edelman R, Damrongsak D, Charupatana C, et al. Immunoglobulins and antibody response in children with protein-calorie malnutrition. Am J Clin Nutr. 1976;29(8):836–41.

    Article  CAS  PubMed  Google Scholar 

  97. el-Molla A, el-Ghoroury A, Hussein M, Badr-el-Din MK, Hassen AH, Aref GH, et al. Antibody production in protein calorie malnutrition. J Trop Med Hyg. 1973;76(9):248–50.

    CAS  PubMed  Google Scholar 

  98. Taylor PE, Tejada C, Sanchez M. The effect of malnutrition on the inflammatory response as exhibited by the granuloma pouch of the rat. J Exp Med. 1967;126(4):539–56.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Zijlstra RT, McCracken BA, Odle J, Donovan SM, Gelberg HB, Petschow BW, et al. Malnutrition modifies pig small intestinal inflammatory responses to rotavirus. J Nutr. 1999;129(4):838–43.

    Article  CAS  PubMed  Google Scholar 

  100. Baek O, Fabiansen C, Friis H, Ritz C, Koch J, Willesen JL, et al. Malnutrition predisposes to endotoxin-induced edema and impaired inflammatory response in parenterally fed piglets. JPEN J Parenter Enteral Nutr. 2019;

    Google Scholar 

  101. Wapnir RA. Zinc deficiency, malnutrition and the gastrointestinal tract. J Nutr. 2000;130.(5S Suppl:1388S–92S.

    Article  CAS  PubMed  Google Scholar 

  102. Bolick DT, Kolling GL, Moore JH 2nd, de Oliveira LA, Tung K, Philipson C, et al. Zinc deficiency alters host response and pathogen virulence in a mouse model of enteroaggregative Escherichia coli-induced diarrhea. Gut Microbes. 2014;5(5):618–27.

    Article  PubMed  PubMed Central  Google Scholar 

  103. Ooi JH, Chen J, Cantorna MT. Vitamin D regulation of immune function in the gut: why do T cells have vitamin D receptors? Mol Asp Med. 2012;33(1):77–82.

    Article  CAS  Google Scholar 

  104. Bibbo S, Ianiro G, Giorgio V, Scaldaferri F, Masucci L, Gasbarrini A, et al. The role of diet on gut microbiota composition. Eur Rev Med Pharmacol Sci. 2016;20(22):4742–9.

    CAS  PubMed  Google Scholar 

  105. Reimer RA. Establishing the role of diet in the microbiota-disease axis. Nat Rev Gastroenterol Hepatol. 2019;16(2):86–7.

    Article  PubMed  Google Scholar 

  106. Jain N, Walker WA. Diet and host-microbial crosstalk in postnatal intestinal immune homeostasis. Nat Rev Gastroenterol Hepatol. 2015;12(1):14–25.

    Article  CAS  PubMed  Google Scholar 

  107. Blanton LV, Charbonneau MR, Salih T, Barratt MJ, Venkatesh S, Ilkaveya O, et al. Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science. 2016;351(6275)

    Google Scholar 

  108. Raman AS, Gehrig JL, Venkatesh S, Chang HW, Hibberd MC, Subramanian S, et al. A sparse covarying unit that describes healthy and impaired human gut microbiota development. Science. 2019;365(6449)

    Google Scholar 

  109. Favier CF, Vaughan EE, De Vos WM, Akkermans AD. Molecular monitoring of succession of bacterial communities in human neonates. Appl Environ Microbiol. 2002;68(1):219–26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Kolida S, Tuohy K, Gibson GR. Prebiotic effects of inulin and oligofructose. Br J Nutr. 2002;87(Suppl 2):S193–7.

    Article  CAS  PubMed  Google Scholar 

  111. Hurley BW, Nguyen CC. The spectrum of pseudomembranous enterocolitis and antibiotic-associated diarrhea. Arch Intern Med. 2002;162(19):2177–84.

    Article  PubMed  Google Scholar 

  112. Sullivan A, Edlund C, Nord CE. Effect of antimicrobial agents on the ecological balance of human microflora. Lancet Infect Dis. 2001;1(2):101–14.

    Article  CAS  PubMed  Google Scholar 

  113. Lizko NN. Problems of microbial ecology in man space Mission. Acta Astronaut. 1991;23:163–9.

    Article  CAS  PubMed  Google Scholar 

  114. Alverdy JC, Laughlin RS, Wu L. Influence of the critically ill state on host-pathogen interactions within the intestine: gut-derived sepsis redefined. Crit Care Med. 2003;31(2):598–607.

    Article  PubMed  Google Scholar 

  115. WHO. Updates on the management of severe acute malnutrition in infants and children. Guideline: Updates on the Management of Severe Acute Malnutrition in Infants and Children. WHO Guidelines Approved by the Guidelines Review Committee. Geneva 2013.

    Google Scholar 

  116. Maier L, Pruteanu M, Kuhn M, Zeller G, Telzerow A, Anderson EE, et al. Extensive impact of non-antibiotic drugs on human gut bacteria. Nature. 2018;555(7698):623–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Gibson MK, Crofts TS, Dantas G. Antibiotics and the developing infant gut microbiota and resistome. Curr Opin Microbiol. 2015;27:51–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Silverman MA, Konnikova L, Gerber JS. Impact of antibiotics on necrotizing Enterocolitis and antibiotic-associated diarrhea. Gastroenterol Clin N Am. 2017;46(1):61–76.

    Article  Google Scholar 

  119. Nogueira T, David PHC, Pothier J. Antibiotics as both friends and foes of the human gut microbiome: the microbial community approach. Drug Dev Res. 2019;80(1):86–97.

    Article  CAS  PubMed  Google Scholar 

  120. Guo Q, Goldenberg JZ, Humphrey C, El Dib R, Johnston BC. Probiotics for the prevention of pediatric antibiotic-associated diarrhea. Cochrane Database Syst Rev. 2019;4:CD004827.

    PubMed  Google Scholar 

  121. Gehrig JL, Venkatesh S, Chang HW, Hibberd MC, Kung VL, Cheng J, et al. Effects of microbiota-directed foods in gnotobiotic animals and undernourished children. Science. 2019;365(6449)

    Google Scholar 

  122. Lutgendorff F, Akkermans LM, Soderholm JD. The role of microbiota and probiotics in stress-induced gastro-intestinal damage. Curr Mol Med. 2008;8(4):282–98.

    Article  CAS  PubMed  Google Scholar 

  123. Gupta SS, Mohammed MH, Ghosh TS, Kanungo S, Nair GB, Mande SS. Metagenome of the gut of a malnourished child. Gut Pathog. 2011;3:7.

    Article  PubMed  PubMed Central  Google Scholar 

  124. Monira S, Nakamura S, Gotoh K, Izutsu K, Watanabe H, Alam NH, et al. Gut microbiota of healthy and malnourished children in Bangladesh. Front Microbiol. 2011;2:228.

    Article  PubMed  PubMed Central  Google Scholar 

  125. Subramanian S, Huq S, Yatsunenko T, Haque R, Mahfuz M, Alam MA, et al. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature. 2014;510(7505):417–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Smith MI, Yatsunenko T, Manary MJ, Trehan I, Mkakosya R, Cheng J, et al. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science. 2013;339(6119):548–54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Lanata CF, Fischer-Walker CL, Olascoaga AC, Torres CX, Aryee MJ, Black RE, et al. Global causes of diarrheal disease mortality in children <5 years of age: a systematic review. PLoS One. 2013;8(9):e72788.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Gracey M, Stone DE, Suharjono S. Isolation of Candida species from the gastrointestinal tract in malnourished children. Am J Clin Nutr. 1974;27(4):345–9.

    Article  CAS  PubMed  Google Scholar 

  129. Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, et al. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the global enteric multicenter study, GEMS): a prospective, case-control study. Lancet. 2013;382(9888):209–22.

    Article  PubMed  Google Scholar 

  130. Rogawski ET, Liu J, Platts-Mills JA, Kabir F, Lertsethtakarn P, Siguas M, et al. Use of quantitative molecular diagnostic methods to investigate the effect of enteropathogen infections on linear growth in children in low-resource settings: longitudinal analysis of results from the MAL-ED cohort study. Lancet Glob Health. 2018;6(12):e1319–e28.

    Article  PubMed  PubMed Central  Google Scholar 

  131. M-EN I. Relationship between growth and illness, enteropathogens and dietary intakes in the first 2 years of life: findings from the MAL-ED birth cohort study. BMJ Glob Health. 2017;2(4):e000370.

    Google Scholar 

  132. Lv Z, Wang Y, Yang T, Zhan X, Li Z, Hu H, et al. Vitamin a deficiency impacts the structural segregation of gut microbiota in children with persistent diarrhea. J Clin Biochem Nutr. 2016;59(2):113–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Blander JM, Longman RS, Iliev ID, Sonnenberg GF, Artis D. Regulation of inflammation by microbiota interactions with the host. Nat Immunol. 2017;18(8):851–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Jaeggi T, Kortman GA, Moretti D, Chassard C, Holding P, Dostal A, et al. Iron fortification adversely affects the gut microbiome, increases pathogen abundance and induces intestinal inflammation in Kenyan infants. Gut. 2015;64(5):731–42.

    Article  CAS  PubMed  Google Scholar 

  135. Marinelli L, Martin-Gallausiaux C, Bourhis JM, Beguet-Crespel F, Blottiere HM, Lapaque N. Identification of the novel role of butyrate as AhR ligand in human intestinal epithelial cells. Sci Rep. 2019;9(1):643.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  136. Offor E, Riepenhoff-Talty M, Ogra PL. Effect of malnutrition on rotavirus infection in suckling mice: kinetics of early infection. Proc Soc Exp Biol Med. 1985;178(1):85–90.

    Article  CAS  PubMed  Google Scholar 

  137. Riepenhoff-Talty M, Uhnoo I, Chegas P, Ogra PL. Effect of nutritional deprivation on mucosal viral infections. Immunol Investig. 1989;18(1–4):127–39.

    Article  CAS  Google Scholar 

  138. Hecht C, Weber M, Grote V, Daskalou E, Dell'Era L, Flynn D, et al. Disease associated malnutrition correlates with length of hospital stay in children. Clin Nutr. 2015;34(1):53–9.

    Article  PubMed  Google Scholar 

  139. Ngari MM, Mwalekwa L, Timbwa M, Hamid F, Ali R, Iversen PO, et al. Changes in susceptibility to life-threatening infections after treatment for complicated severe malnutrition in Kenya. Am J Clin Nutr. 2018;107(4):626–34.

    Article  PubMed  PubMed Central  Google Scholar 

  140. Chevalier P, Sevilla R, Sejas E, Zalles L, Belmonte G, Parent G. Immune recovery of malnourished children takes longer than nutritional recovery: implications for treatment and discharge. J Trop Pediatr. 1998;44(5):304–7.

    Article  CAS  PubMed  Google Scholar 

  141. De Santis S, Cavalcanti E, Mastronardi M, Jirillo E, Chieppa M. Nutritional keys for intestinal barrier modulation. Front Immunol. 2015;6:612.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  142. Countdown Coverage Writing G, Countdown to Core G, Bryce J, Daelmans B, Dwivedi A, Fauveau V, et al. Countdown to 2015 for maternal, newborn, and child survival: the 2008 report on tracking coverage of interventions. Lancet. 2008;371(9620):1247–58.

    Article  Google Scholar 

  143. de Medeiros P, Pinto DV, de Almeida JZ, Rego JMC, Rodrigues FAP, Lima AAM, et al. Modulation of intestinal immune and barrier functions by vitamin a: implications for current understanding of malnutrition and enteric infections in children. Nutrients. 2018;10(9)

    Google Scholar 

  144. Long KZ, Santos JI, Rosado JL, Estrada-Garcia T, Haas M, Al Mamun A, et al. Vitamin a supplementation modifies the association between mucosal innate and adaptive immune responses and resolution of enteric pathogen infections. Am J Clin Nutr. 2011;93(3):578–85.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Iannotti LL, Trehan I, Clitheroe KL, Manary MJ. Diagnosis and treatment of severely malnourished children with diarrhoea. J Paediatr Child Health. 2015;51(4):387–95.

    PubMed  Google Scholar 

  146. Walker CL, Black RE. Zinc for the treatment of diarrhoea: effect on diarrhoea morbidity, mortality and incidence of future episodes. Int J Epidemiol. 2010.;39 Suppl 1(Supplement 1:i63–9.

    Google Scholar 

  147. Hoque KM, Sarker R, Guggino SE, Tse CM. A new insight into pathophysiological mechanisms of zinc in diarrhea. Ann N Y Acad Sci. 2009;1165:279–84.

    Article  CAS  PubMed  Google Scholar 

  148. Kumar A, Vlasova AN, Deblais L, Huang HC, Wijeratne A, Kandasamy S, et al. Impact of nutrition and rotavirus infection on the infant gut microbiota in a humanized pig model. BMC Gastroenterol. 2018;18(1):93.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  149. Berkley JA, Lowe BS, Mwangi I, Williams T, Bauni E, Mwarumba S, et al. Bacteremia among children admitted to a rural hospital in Kenya. N Engl J Med. 2005;352(1):39–47.

    Article  CAS  PubMed  Google Scholar 

  150. Smythe PM. Changes in intestinal bacterial flora and role of infection in kwashiorkor. Lancet. 1958;2(7049):724–7.

    Article  CAS  PubMed  Google Scholar 

  151. Mogasale V, Desai SN, Mogasale VV, Park JK, Ochiai RL, Wierzba TF. Case fatality rate and length of hospital stay among patients with typhoid intestinal perforation in developing countries: a systematic literature review. PLoS One. 2014;9(4):e93784.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  152. Creek TL, Kim A, Lu L, Bowen A, Masunge J, Arvelo W, et al. Hospitalization and mortality among primarily nonbreastfed children during a large outbreak of diarrhea and malnutrition in Botswana, 2006. J Acquir Immune Defic Syndr. 2010;53(1):14–9.

    Article  PubMed  Google Scholar 

  153. Motarjemi Y, Kaferstein F, Moy G, Quevedo F. Contaminated weaning food: a major risk factor for diarrhoea and associated malnutrition. Bull World Health Organ. 1993;71(1):79–92.

    CAS  PubMed  PubMed Central  Google Scholar 

  154. Schaible UE, Kaufmann SH. Malnutrition and infection: complex mechanisms and global impacts. PLoS Med. 2007;4(5):e115.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  155. Petri WA Jr, Mondal D, Peterson KM, Duggal P, Haque R. Association of malnutrition with amebiasis. Nutr Rev. 2009;67(Suppl 2):S207–15.

    Article  PubMed  Google Scholar 

  156. Coles CL, Levy A, Dagan R, Deckelbaum RJ, Fraser D. Risk factors for the initial symptomatic giardia infection in a cohort of young Arab-Bedouin children. Ann Trop Paediatr. 2009;29(4):291–300.

    Article  CAS  PubMed  Google Scholar 

  157. Mondal D, Petri WA, Sack RB, Kirkpatrick BD, Haque R. Entamoeba histolytica-associated diarrheal illness is negatively associated with the growth of preschool children: evidence from a prospective study. T Roy Soc Trop Med H. 2006;100(11):1032–8.

    Article  Google Scholar 

  158. Scrimshaw NS. Historical concepts of interactions, synergism and antagonism between nutrition and infection. J Nutr. 2003;133(1):316S–21S.

    Article  PubMed  Google Scholar 

  159. Moore SR, Lima NL, Soares AM, Oria RB, Pinkerton RC, Barrett LJ, et al. Prolonged episodes of acute diarrhea reduce growth and increase risk of persistent diarrhea in children. Gastroenterology. 2010;139(4):1156–64.

    Article  PubMed  Google Scholar 

  160. Richard SA, Black RE, Gilman RH, Guerrant RL, Kang G, Lanata CF, et al. Diarrhea in early childhood: short-term association with weight and long-term association with length. Am J Epidemiol. 2013;178(7):1129–38.

    Article  PubMed  PubMed Central  Google Scholar 

  161. World Bank. Repositioning nutrition as central to development: a strategy for large-scale action. Washington, DC; 2006.

    Google Scholar 

  162. Guerrant RL, DeBoer MD, Moore SR, Scharf RJ, Lima AA. The impoverished gut--a triple burden of diarrhoea, stunting and chronic disease. Nat Rev Gastroenterol Hepatol. 2013;10(4):220–9.

    Article  PubMed  Google Scholar 

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Siddiqui, F.J., Belayneh, G., Bhutta, Z.A. (2021). Nutrition and Diarrheal Disease and Enteric Pathogens. In: Humphries, D.L., Scott, M.E., Vermund, S.H. (eds) Nutrition and Infectious Diseases . Nutrition and Health. Humana, Cham. https://doi.org/10.1007/978-3-030-56913-6_8

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