Chronic consequences on human health induced by microbial pathogens: Growth faltering among children in developing countries

Vaccine

Volumn 35, Issue 49, 2017, Pages 6807-6812

  Nataro, James P ^a   Guerrant, Richard L ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Child health; Diarrhea; Environmental enteric dysfunction; Growth faltering

Indexed keywords

BIOLOGICAL MARKER; IMMUNOGLOBULIN A;

ANIMAL MODEL; ARTICLE; BODY GROWTH; CHILD HEALTH; CHILDHOOD DISEASE; DEVELOPING COUNTRY; ENTEROPATHY; ENVIRONMENTAL ENTERIC DYSFUNCTION; GROWTH DISORDER; HUMAN; INFECTIOUS DIARRHEA; INTESTINE FLORA; INTESTINE INFECTION; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; ANIMAL; BACTERIUM; CHILD; COMPLICATION; COST OF ILLNESS; DIARRHEA; DISEASE MODEL; ENVIRONMENT; FEMALE; INFANT; INJURIES; INTESTINE; INTESTINE MUCOSA; MALE; MICROBIOLOGY; ORGANIZATION; PATHOGENICITY; PATHOPHYSIOLOGY; PRESCHOOL CHILD; STATISTICS AND NUMERICAL DATA;

ANIMALS; BACTERIA; CHILD; CHILD HEALTH; CHILD, PRESCHOOL; CONGRESSES AS TOPIC; COST OF ILLNESS; DEVELOPING COUNTRIES; DIARRHEA; DISEASE MODELS, ANIMAL; ENVIRONMENT; FEMALE; GASTROINTESTINAL MICROBIOME; GROWTH DISORDERS; HUMANS; INFANT; INTESTINAL MUCOSA; INTESTINES; MALE;

EID: 85019888457     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2017.05.035     Document Type: Article

References (71)

1. Liu, L., Oza, S., Hogan, D., et al. Global, regional, and national causes of child mortality in 2000–13, with projections to inform post-2015 priorities: an updated systematic analysis. Lancet 385:9966 (2015 Jan 31), 430–440.
2. Kosek, M., Bern, C., Guerrant, R.L., The global burden of diarrhoeal disease, as estimated from studies published between 1992 and 2000. Bull World Health Organ 81:3 (2003), 197–204.
3. Guerrant, R.L., DeBoer, M.D., Moore, S.R., Scharf, R.J., Lima, A.A., The impoverished gut–a triple burden of diarrhoea, stunting and chronic disease. Nat Rev Gastroenterol Hepatol 10:4 (2013 Apr), 220–229.
4. Mata, L.J., The children of Santa Maria Cauque: a prospective field study of health and growth. 1978, MIT Press, Cambridge, Mass.
5. Victora, C.G., de, O.M., Hallal, P.C., Blossner, M., Shrimpton, R., Worldwide timing of growth faltering: revisiting implications for interventions. Pediatrics 125:3 (2010), e473–e480.
6. Schorling, J.B., Guerrant, R.L., Diarrhoea and catch-up growth. Lancet 335:8689 (1990), 599–600.
7. Moore, S.R., Lima, A.A., Conaway, M.R., Schorling, J.B., Soares, A.M., Guerrant, R.L., Early childhood diarrhoea and helminthiases associate with long-term linear growth faltering. Int J Epidemiol 30:6 (2001), 1457–1464.
8. Checkley, W., Buckley, G., Gilman, R.H., et al. Multi-country analysis of the effects of diarrhoea on childhood stunting. Int J Epidemiol 37:4 (2008), 816–830.
9. Moore, S.R., Lima, N.L., Soares, A.M., et al. Prolonged episodes of acute diarrhea reduce growth and increase risk of persistent diarrhea in children. Gastroenterology 139:4 (2010), 1156–1164.
10. Guerrant, D.I., Moore, S.R., Lima, A.A., Patrick, P.D., Schorling, J.B., Guerrant, R.L., Association of early childhood diarrhea and cryptosporidiosis with impaired physical fitness and cognitive function four-seven years later in a poor urban community in northeast Brazil. Am J Trop Med Hyg 61:5 (1999), 707–713.
11. Niehaus, M.D., Moore, S.R., Patrick, P.D., et al. Early childhood diarrhea is associated with diminished cognitive function 4 to 7 years later in children in a northeast Brazilian shantytown. Am J Trop Med Hyg 66:5 (2002), 590–593.
12. Pinkerton, R., Oria, R.B., Lima, A.A., et al. Early Childhood Diarrhea Predicts Cognitive Delays in Later Childhood Independently of Malnutrition. Am J Trop Med Hyg 95:5 (2016), 1004–1010.
13. Nokes, C., Grantham-McGregor, S.M., Sawyer, A.W., Cooper, E.S., Bundy, D.A., Parasitic helminth infection and cognitive function in school children. Proc Biol Sci 247:1319 (1992), 77–81.
14. Mendez, M.A., Adair, L.S., Severity and timing of stunting in the first two years of life affect performance on cognitive tests in late childhood. J Nutr 129:8 (1999), 1555–1562.
15. Berkman, D.S., Lescano, A.G., Gilman, R.H., Lopez, S.L., Black, M.M., Effects of stunting, diarrhoeal disease, and parasitic infection during infancy on cognition in late childhood: a follow-up study. Lancet 359:9306 (2002), 564–571.
16. Tarleton, J.L., Haque, R., Mondal, D., Shu, J., Farr, B.M., Petri, W.A. Jr., Cognitive effects of diarrhea, malnutrition, and Entamoeba histolytica infection on school age children in Dhaka. Bangladesh. Am J Trop Med Hyg 74:3 (2006), 475–481.
17. Stein, A.D., Wang, M., DiGirolamo, A., et al. Nutritional supplementation in early childhood, schooling, and intellectual functioning in adulthood: a prospective study in Guatemala. Arch Pediatr Adolesc Med 162:7 (2008), 612–618.
18. Ajjampur, S.S., Koshy, B., Venkataramani, M., et al. Effect of cryptosporidial and giardial diarrhoea on social maturity, intelligence and physical growth in children in a semi-urban slum in south India. Ann Trop Paediatr 31:3 (2011), 205–212.
19. Pongcharoen, T., Ramakrishnan, U., DiGirolamo, A.M., et al. Influence of prenatal and postnatal growth on intellectual functioning in school-aged children. Arch Pediatr Adolesc Med 166:5 (2012), 411–416.
20. Barker, D.J., Osmond, C., Forsen, T.J., Kajantie, E., Eriksson, J.G., Trajectories of growth among children who have coronary events as adults. N Engl J Med 353:17 (2005), 1802–1809.
21. Eppig, C., Fincher, C.L., Thornhill, R., Parasite prevalence and the worldwide distribution of cognitive ability. Proc Biol Sci 277:1701 (2010), 3801–3808.
22. Ferreira, H.S., Moura, F.A., Cabral, C.R. Jr., Florencio, T.M., Vieira, R.C., de Assuncao, M.L., Short stature of mothers from an area endemic for undernutrition is associated with obesity, hypertension and stunted children: a population-based study in the semi-arid region of Alagoas Northeast Brazil. Br J Nutr 101:8 (2009), 1239–1245.
23. van Abeelen, A.F., Elias, S.G., Bossuyt, P.M., et al. Famine exposure in the young and the risk of type 2 diabetes in adulthood. Diabetes 61:9 (2012), 2255–2260.
24. Schroeder, D.G., Martorell, R., Flores, R., Infant and child growth and fatness and fat distribution in Guatemalan adults. Am J Epidemiol 149:2 (1999), 177–185.
25. Bhargava, S.K., Sachdev, H.S., Fall, C.H., et al. Relation of serial changes in childhood body-mass index to impaired glucose tolerance in young adulthood. N Engl J Med 350:9 (2004), 865–875.
26. Fall, C.H., Sachdev, H.S., Osmond, C., et al. Adult metabolic syndrome and impaired glucose tolerance are associated with different patterns of BMI gain during infancy: Data from the New Delhi Birth Cohort. Diabetes Care 31:12 (2008), 2349–2356.
27. Victora, C.G., Adair, L., Fall, C., et al. Maternal and child undernutrition: consequences for adult health and human capital. Lancet 371:9609 (2008), 340–357.
28. Margolis R. The effects of early childhood diseases on young adult health in guatemala. University of Pennsylvania Scholarly Commons Population Aging Research Center (PARC) working paper series; 9-3-2008. University of Pennsylvania.
29. Margolis, R., Childhood Morbidity and Health in Early Adulthood: Life course linkages in a high morbidity context. Adv Life Course Res 15:4 (2010), 132–146.
30. DeBoer, M.D., Chen, D., Burt, D.R., et al. Early childhood diarrhea and cardiometabolic risk factors in adulthood: the Institute of Nutrition of Central America and Panama Nutritional Supplementation Longitudinal Study. Ann Epidemiol 23:6 (2013), 314–320.
31. Kvestad, I., Taneja, S., Hysing, M., Kumar, T., Bhandari, N., Strand, T.A., Diarrhea, stimulation and growth predict neurodevelopment in young North Indian children. PLoS One, 10(3), 2015, e0121743.
32. Steiner, T.S., Lima, A.A., Nataro, J.P., Guerrant, R.L., Enteroaggregative Escherichia coli produce intestinal inflammation and growth impairment and cause interleukin-8 release from intestinal epithelial cells. J Infect Dis 177:1 (1998), 88–96.
33. Checkley, W., Gilman, R.H., Epstein, L.D., et al. Asymptomatic and symptomatic cryptosporidiosis: their acute effect on weight gain in Peruvian children. Am J Epidemiol 145:2 (1997), 156–163.
34. Checkley, W., Epstein, L.D., Gilman, R.H., Black, R.E., Cabrera, L., Sterling, C.R., Effects of Cryptosporidium parvum infection in Peruvian children: growth faltering and subsequent catch-up growth. Am J Epidemiol 148:5 (1998), 497–506.
35. Amour, C., Gratz, J., Mduma, E., et al. Epidemiology and Impact of Campylobacter Infection in Children in 8 Low-Resource Settings: Results From the MAL-ED Study. Clin Infect Dis 63:9 (2016), 1171–1179.
36. Rogawski, E., Bartelt, L., Platts-Mills, J.A., et al. Determinants and Impact of Giardia Infection in the First 2 Years of Life in the MAL-ED Birth Cohort. J Pediatr Inf Dis Soc., 2017 in press.
37. Patrick, P.D., Oria, R.B., Madhavan, V., et al. Limitations in verbal fluency following heavy burdens of early childhood diarrhea in Brazilian shantytown children. Child Neuropsychol 11:3 (2005), 233–244.
38. Oria, R.B., Patrick, P.D., Zhang, H., et al. APOE4 protects the cognitive development in children with heavy diarrhea burdens in Northeast Brazil. Pediatr Res 57:2 (2005), 310–316.
39. Oria, R.B., Murray-Kolb, L.E., Scharf, R.J., et al. Early-life enteric infections: relation between chronic systemic inflammation and poor cognition in children. Nutr Rev 74:6 (2016), 374–386.
40. Filiano, A.J., Xu, Y., Tustison, N.J., et al. Unexpected role of interferon-gamma in regulating neuronal connectivity and social behaviour. Nature 535:7612 (2016), 425–429.
41. DeBoer, M.D., Scharf, R.J., Leite, A.M., et al. Systemic inflammation, growth factors, and linear growth in the setting of infection and malnutrition. Nutrition 33 (2017), 248–253.
42. Lee, G.O., Olortegui, M.P., Salas, M.S., et al. Environmental enteropathy is associated with cardiometabolic risk factors in Peruvian children. J Dev Orig Health Dis 7 (2017), 1–12.
43. Kosek, M., Haque, R., Lima, A., 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 88:2 (2013), 390–396.
44. Guerrant, R.L., Leite, A.M., Pinkerton, R., et al. Biomarkers of Environmental Enteropathy, Inflammation, Stunting, and Impaired Growth in Children in Northeast Brazil. PLoS One, 11(9), 2016, e0158772.
45. Prata, M.M., Havt, A., Bolick, D.T., Pinkerton, R., Lima, A., Guerrant, R.L., Comparisons between myeloperoxidase, lactoferrin, calprotectin and lipocalin-2, as fecal biomarkers of intestinal inflammation in malnourished children. J Transl Sci 2:2 (2016), 134–139.
46. Arndt, M.B., Richardson, B.A., Ahmed, T., et al. Fecal Markers of Environmental Enteropathy and Subsequent Growth in Bangladeshi Children. Am J Trop Med Hyg 95:3 (2016), 694–701.
47. Mayneris-Perxachs, J., Lima, A.A., Guerrant, R.L., et al. Urinary N-methylnicotinamide and beta-aminoisobutyric acid predict catch-up growth in undernourished Brazilian children. Sci Rep, 27(6), 2016, 19780.
48. Mayneris-Perxachs, J., Bolick, D.T., Leng, J., et al. Protein- and zinc-deficient diets modulate the murine microbiome and metabolic phenotype. Am J Clin Nutr 104:5 (2016), 1253–1262.
49. Coutinho, B.P., Oria, R.B., Vieira, C.M., et al. Cryptosporidium infection causes undernutrition and conversely, weanling undernutrition intensifies infection. J Parasitol 94:6 (2008), 1225–1232.
50. Costa, L.B., Noronha, F.J., Roche, J.K., et al. Novel in vitro and in vivo models and potential new therapeutics to break the vicious cycle of Cryptosporidium infection and malnutrition. J Infect Dis 205:9 (2012), 1464–1471.
51. Roche, J.K., Cabel, A., Sevilleja, J., Nataro, J., Guerrant, R.L., Enteroaggregative Escherichia coli (EAEC) impairs growth while malnutrition worsens EAEC infection: a novel murine model of the infection malnutrition cycle. J Infect Dis 202:4 (2010), 506–514.
52. Bolick, D.T., Roche, J.K., Hontecillas, R., Bassaganya-Riera, J., Nataro, J.P., Guerrant, R.L., Enteroaggregative Escherichia coli strain in a novel weaned mouse model: exacerbation by malnutrition, biofilm as a virulence factor and treatment by nitazoxanide. J Med Microbiol 62:Pt 6 (2013), 896–905.
53. Bolick, D.T., Kolling, G.L., Moore, J.H., et al. Zinc deficiency alters host response and pathogen virulence in a mouse model of enteroaggregative Escherichia coli-induced diarrhea. Gut Microbes 5:5 (2014), 618–627.
54. Bartelt, L.A., Roche, J., Kolling, G., et al. Persistent G. lamblia impairs growth in a murine malnutrition model. J Clin Invest 123:6 (2013), 2672–2684.
55. Azevedo, O.G., Bolick, D.T., Roche, J.K., et al. Apolipoprotein E plays a key role against cryptosporidial infection in transgenic undernourished mice. PLoS One, 9(2), 2014, e89562.
56. Castro, I.C., Oliveira, B.B., Slowikowski, J.J., et al. Arginine decreases Cryptosporidium parvum infection in undernourished suckling mice involving nitric oxide synthase and arginase. Nutrition 28:6 (2012), 678–685.
57. Liu, J., Bolick, D.T., Kolling, G.L., Fu, Z., Guerrant, R.L., Protein Malnutrition Impairs Intestinal Epithelial Cell Turnover, a Potential Mechanism of Increased Cryptosporidiosis in a Murine Model. Infect Immun 84:12 (2016), 3542–3549.
58. Subramanian, S., Huq, S., Yatsunenko, T., et al. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature 510:7505 (2014), 417–421.
59. Smith, M.I., Yatsunenko, T., Manary, M.J., et al. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science 339:6119 (2013), 548–554.
60. Blanton LV, Charbonneau MR, Salih T, et al. Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science 2016 Feb 19;351(6275).
61. Planer, J.D., Peng, Y., Kau, A.L., Blanton, L.V., Ndao, I.M., Tarr, P.I., Warner, B.B., Gordon, J.I., Development of the gut microbiota and mucosal IgA responses in twins and gnotobiotic mice. Nature 534:7606 (2016), 263–266.
62. Kau, A.L., Planer, J.D., Liu, J., et al. Functional characterization of IgA-targeted bacterial taxa from undernourished Malawian children that produce diet-dependent enteropathy. Sci Transl Med, 7(276), 2015, 276ra24.
63. Pop, M., Walker, A.W., Paulson, J., et al. Diarrhea in young children from low-income countries leads to large-scale alterations in intestinal microbiota composition. Genome Biol, 15(6), 2014, R76.
64. Lindsay, B., Oundo, J., Hossain, M.A., et al. Microbiota that affect risk for shigellosis in children in low-income countries. Emerg Infect Dis 21:2 (2015), 242–250.
65. Guandalini, S., Probiotics for prevention and treatment of diarrhea. J Clin Gastroenterol 45:Suppl (2011), S149–S153.
66. Muhsen, K., Ornoy, A., Akawi, A., Alpert, G., Cohen, D., An association between Helicobacter pylori infection and cognitive function in children at early school age: a community-based study. BMC Pediatr, 25(11), 2011, 43.
67. Windle, H.J., Kelleher, D., Crabtree, J.E., Childhood Helicobacter pylori infection and growth impairment in developing countries: a vicious cycle?. Pediatrics 119:3 (2007), e754–e759.
68. Beatty, J.K., Akierman, S.V., Motta, J.P., et al. Giardia duodenalis induces pathogenic dysbiosis of human intestinal microbiota biofilms. Int J Parasitol 47:6 (2017), 311–326.
69. Ochieng, J.B., Boisen, N., Lindsay, B., et al. Serratia marcescens is injurious to intestinal epithelial cells. Gut Microbes 5:6 (2014), 729–736.
70. Bartelt, L.A., Guerrant, R.L., Antibiotics help control rotavirus infections and enhance antirotaviral immunity: are you serious?. J Infect Dis 210:2 (2014), 167–170.
71. Wu, H.J., Wu, E., The role of gut microbiota in immune homeostasis and autoimmunity. Gut Microbes 3:1 (2012), 4–14.