Causal Pathways from Enteropathogens to Environmental Enteropathy: Findings from the MAL-ED Birth Cohort Study

EBioMedicine

Volumn 18, Issue , 2017, Pages 109-117

  Kosek, Margaret N ^j   Ahmed, Tahmeed ^h   Bhutta, Zulfiqar A ^b   Caulfield, Laura ^j   Guerrant, Richard L ^q   Houpt, Eric ^q   Kang, Gagandeep ^d   Lee, Gwenyth ^j   Lima, Aldo A M ^m,t   McCormick, Benjamin J J ^f   Platts Mills, James ^q   Seidman, Jessica C ^f   Blank, Rebecca R ^f   Gottlieb, Michael ^f   Knobler, Stacey L ^f   Lang, Dennis R ^f   Miller, Mark A ^f   Tountas, Karen H ^f   Checkley, William ^f,j   Mason, Carl J ^c   Murray Kolb, Laura E ^k   Petri, William A ^q   Bessong, Pascal ^p   Haque, Rashidul ^h   John, Sushil ^d   Mduma, Estomih R ^g   Oriá, Reinaldo B ^m   Shrestha, Prakash Sunder ⁱ   Shrestha, Sanjaya Kumar ^r   Svensen, Erling ^g,s   Zaidi, Anita K M ^b   Abreu, Cláudia B ^m   Acosta, Angel Mendez ^a   Ahmed, Imran ^b   Shamsir Ahmed, A M ^h   Ali, Asad ^b   Ambikapathi, Ramya ^f   Barrett, Leah ^q   Bauck, Aubrey ^j   Bayyo, Eliwaza ^g   Bodhidatta, Ladaporn ^c   Bose, Anuradha ^d   Daniel Carreon, J ^f   Chandyo, Ram Krishna ⁱ   Charu, Vivek ^f   Costa, Hilda ^m   Dillingham, Rebecca ^q   Di Moura, Alessandra ^m   Doan, Viyada ^f   Filho, Jose Quirino ^f,m   Graham, Jhanelle ^f   Hoest, Christel ^f   Hossain, Iqbal ^h   Islam, Munirul ^h   Steffi Jennifer, M ^d   Kaki, Shiny ^d   Koshy, Beena ^d   Leite, Álvaro M ^m   Lima, Noélia L ^m   Maciel, Bruna L L ^m   Mahfuz, Mustafa ^h   Mahopo, Cloupas ^p   Maphula, Angelina ^p   McGrath, Monica ^f   Mohale, Archana ^f   Moraes, Milena ^m   Mota, Francisco S ^m   Muliyil, Jayaprakash ^d   Mvungi, Regisiana ^g   Nayyar, Gaurvika ^f   Nyathi, Emanuel ^p   Olortegui, Maribel Paredes ^a   Vasquez, Angel Orbe ^a   Pan, William K ^e,f   Pascal, John ^g   Patil, Crystal L ^o   Pendergast, Laura ^l   Pinedo, Silvia Rengifo ^a   Psaki, Stephanie ^f   Raghava, Mohan Venkata ^d   Ramanujam, Karthikeyan ^d   Rasheed, Muneera ^b   Rasmussen, Zeba A ^f   Richard, Stephanie A ^f   Rose, Anuradha ^d   Roshan, Reeba ^d   Schaefer, Barbara ^f,k   Scharf, Rebecca ^q   Sharma, Srujan L ^d   Shrestha, Binob ^r   Shrestha, Rita ⁱ   Simons, Suzanne ^k   Soares, Alberto M ^m   Mota, Rosa M S ^m   Soofi, Sajid ^b   Strand, Tor ^n,r   Tofail, Fahmida ^h   Thomas, Rahul J ^d   Turab, Ali ^b   Ulak, Manjeswori ⁱ   Wang, Vivian ^f   Yarrot, Ladislaus ^g   Yori, Pablo Peñataro ^j   Alam, Didar ^b   Amour, Caroline ^g   Chavez, Cesar Banda ^a   Babji, Sudhir ^d   de Burga, Rosa Rios ^a   Flores, Julian Torres ^a   Gratz, Jean ^q   George, Ajila T ^d   Hariraju, Dinesh ^d   Havt, Alexandre ^m   Karunakaran, Priyadarshani ^d   Lazarus, Robin P ^d   Lima, Ila F ^m   Mondal, Dinesh ^h   Medeiros, Pedro H Q S ^m   Nshama, Rosemary ^g   Quetz, Josiane ^m   Qureshi, Shahida ^b   Raju, Sophy ^d   Ramachandran, Anup ^d   Ramadas, Rakhi ^d   Catharine Ross, A ^k   Salas, Mery Siguas ^a   Samie, Amidou ^p   Schulze, Kerry ^j   Shanmuga Sundaram, E ^d   Swema, Buliga Mujaga ^g   Trigoso, Dixner Rengifo ^a   more..

^a ASOCIACIÓN BENÉFICA PRISMA   (Peru)

^b AGA KHAN UNIVERSITY   (Pakistan)

^c ARMED FORCES RESEARCH INSTITUTE OF MEDICAL SCIENCES   (Thailand)

^d CHRISTIAN MEDICAL COLLEGE   (India)

^e DUKE UNIVERSITY   (United States)

^f NATIONAL INSTITUTES OF HEALTH   (United States)

^g HAYDOM LUTHERAN HOSPITAL   (Tanzania)

^h INTERNATIONAL CENTRE FOR DIARRHOEAL DISEASE RESEARCH   (Bangladesh)

ⁱ TRIBHUVAN UNIVERSITY   (Nepal)

^j JOHNS HOPKINS UNIVERSITY   (United States)

^k PENNSYLVANIA STATE UNIVERSITY   (United States)

^l TEMPLE UNIVERSITY   (United States)

^m FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

ⁿ UNIVERSITY OF BERGEN   (Norway)

^o UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^p UNIVERSITY OF VENDA   (South Africa)

^q UNIVERSITY OF VIRGINIA   (United States)

^r Walter Reed/AFRIMS Research Unit   (Nepal)

^s HAUKELAND UNIVERSITY HOSPITAL   (Norway)

^t Haukeland University Hospital ^*

more..

Author keywords

Child growth; Child health; Enteropathogen; Enteropathy; Stunting; Undernutrition

Indexed keywords

ALPHA 1 ANTITRYPSIN; LACTULOSE; MANNITOL; MYELOPEROXIDASE; NEOPTERIN; OROSOMUCOID; BIOLOGICAL MARKER; PEROXIDASE;

ARTICLE; CHILD; CHILD GROWTH; CHILD HEALTH; COHORT ANALYSIS; CRYPTOSPORIDIUM; ENTEROPATHY; ENVIRONMENTAL ENTEROPATHY; FECES ANALYSIS; GIARDIA; HUMAN; INFANT; INFLAMMATION; INTESTINE INFECTION; MALNUTRITION; NEWBORN; NONHUMAN; PRESCHOOL CHILD; PRIORITY JOURNAL; STUNTING; URINALYSIS; CHEMISTRY; FECES; METABOLISM; MICROBIOLOGY; PATHOLOGY; THEORETICAL MODEL; URINE; VIROLOGY;

ALPHA 1-ANTITRYPSIN; BIOMARKERS; COHORT STUDIES; FECES; HUMANS; INFANT; INTESTINAL DISEASES; LACTULOSE; MALNUTRITION; MANNITOL; MODELS, THEORETICAL; NEOPTERIN; OROSOMUCOID; PEROXIDASE;

EID: 85018513442     PISSN: None     EISSN: 23523964     Source Type: Journal    
DOI: 10.1016/j.ebiom.2017.02.024     Document Type: Article

References (54)

1. Beltinger, J., Del Buono, J., Skelly, M.M., et al. Disruption of colonic barrier function and induction of mediator release by strains of Campylobacter jejuni that invade epithelial cells. World J. Gastroenterol. 14 (2008), 7345–7352.
2. Berkes, J., Viswanathan, V.K., Savkovic, S.D., Hecht, G., Intestinal epithelial responses to enteric pathogens: effects on the tight junction barrier, ion transport, and inflammation. Gut 52 (2003), 439–451.
3. Blanton, L.V., Charbonneau, M.R., Salih, T., et al. Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science, 351, 2016 (aad3311) 10.1126/science.aad3311.
4. Brown, E.M., Wlodarska, M., Willing, B.P., et al. Diet and specific microbial exposure trigger features of environmental enteropathy in a novel murine model. Nat. Commun., 6, 2015, 7806.
5. Campbell, D.I., Lunn, P.G., Elia, M., Age-related association of small intestinal mucosal enteropathy with nutritional status in rural Gambian children. Br. J. Nutr. 88 (2002), 499–505.
6. Campbell, D.I., Murch, S.H., Elia, M., et al. Chronic T cell-mediated enteropathy in rural west African children: relationship with nutritional status and small bowel function. Pediatr. Res. 54 (2003), 306–311.
7. Campbell, D.I., McPhail, G., Lunn, P.G., Elia, M., Jeffries, D.J., Intestinal inflammation measured by fecal neopterin in Gambian children with enteropathy: association with growth failure, Giardia lamblia, and intestinal permeability. J. Pediatr. Gastroenterol. Nutr. 39 (2004), 153–157.
8. Caulfield, L.E., Bose, A., Chandyo, R.K., et al. Infant feeding practices, dietary adequacy, and micronutrient status measures in the MAL-ED study. Clin. Infect. Dis. 59 (2014), S248–S254.
9. Denno, D.M., VanBuskirk, K., Nelson, Z.C., Musser, C.A., Hay Burgess, D.C., Tarr, P.I., Use of the lactulose to mannitol ratio to evaluate childhood environmental enteric dysfunction: a systematic review. Clin. Infect. Dis. 59 (2014), S213–S219.
10. George, C.M., Oldja, L., Biswas, S., et al. Geophagy is associated with environmental enteropathy and stunting in children in Rural Bangladesh. Am. J. Trop. Med. Hyg. 92 (2015), 1117–1124.
11. Goto, R., Mascie-Taylor, C.G.N., Lunn, P.G., Impact of intestinal permeability, inflammation status and parasitic infections on infant growth faltering in rural Bangladesh. Br. J. Nutr. 101 (2009), 1509–1516.
12. Greenland, S., Pearl, J., Robins, J.M., Causal diagrams for epidemiologic research. Epidemiology 10 (1999), 37–48.
13. Guerrant, R.L., Steiner, T.S., Lima, A.A.M., Bobak, D.A., How intestinal bacteria cause disease. J. Infect. Dis. 179 (1999), S331–S337.
14. Hashimoto, T., Perlot, T., Rehman, A., et al. ACE2 links amino acid malnutrition to microbial ecology and intestinal inflammation. Nature 487 (2012), 477–481.
15. Houpt, E., Gratz, J., Kosek, M., et al. Microbiologic methods utilized in the MAL-ED cohort study. Clin. Infect. Dis. 59 (2014), S225–S232.
16. Humphrey, J.H., Child undernutrition, tropical enteropathy, toilets, and handwashing. Lancet 374 (2009), 1032–1035.
17. Kamada, N., Chen, G.Y., Inohara, N., Núñez, G., Control of pathogens and pathobionts by the gut microbiota. Nat. Immunol. 14 (2013), 685–690.
18. 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, 2015 (276ra24) 10.1126/scitranslmed.aaa4877.
19. Kelly, P., Menzies, I., Crane, R., et al. Responses of small intestinal architecture and function over time to environmental factors in a tropical population. Am.J.Trop. Med. Hyg. 70 (2004), 412–419.
20. Keusch, G.T., Rosenberg, I.H., Denno, D.M., et al. 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 (2013), 357–364.
21. Keusch, G.T., Denno, D.M., Black, R.E., et al. Environmental enteric dysfunction: pathogenesis, diagnosis, and clinical consequences. Clin. Infect. Dis. 59 (2014), S207–S212.
22. Korpe, P.S., Petri, W.A. Jr., Environmental enteropathy: critical implications of a poorly understood condition. Trends Mol. Med. 18 (2012), 328–336.
23. 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 (2013), 390–396.
24. Kosek, M., Guerrant, R.L., Kang, G., et al. Assessment of environmental enteropathy in the MAL-ED cohort study: theoretical and analytic framework. Clin. Infect. Dis. 59 (2014), S239–S247.
25. Kosek, M.N., Mduma, E., Kosek, P.S., et al. Plasma Tryptophan and the Kynurenine-Tryptophan Ratio are Associated with the Acquisition of Statural Growth Deficits and Oral Vaccine Underperformance in Populations with Environmental Enteropathy. Am. J. Trop. Med. Hyg., 2016 (published online Aug 8) 10.4269/ajtmh.16-0037.
26. Kremer, J.M., Wilting, J., Janssen, L.H., Drug binding to human alpha-1-acid glycoprotein in health and disease. Pharmacol. Rev. 40 (1988), 1–47.
27. Lin, A., Arnold, B.F., Afreen, S., et al. Household environmental conditions are associated with enteropathy and impaired growth in rural Bangladesh. Am.J.Trop. Med. Hyg. 89 (2013), 130–137.
28. Lohmann, T.G., Roche, A.F., Martorell, R., Anthropometric Standardization Reference Manual. 1988, Human Kinetics Books, Champaign, IL.
29. Lunn, P.G., The impact of infection and nutrition on gut function and growth in childhood. Proc. Nutr. Soc. 59 (2000), 147–154.
30. Lunn, P.G., Northrop-Clewes, C.A., Downes, R.M., Intestinal permeability, mucosal injury, and growth faltering in Gambian infants. Lancet 338 (1991), 907–910.
31. MAL-ED Network Investigators, The MAL-ED study: a multinational and multidisciplinary approach to understand the relationship between enteric pathogens, malnutrition, gut physiology, physical growth, cognitive development, and immune responses in infants and children up to 2 years of age in resource-poor environments. Clin. Infect. Dis. 59 (2014), S193–S206.
32. MAL-ED Network Investigators, The Malnutrition and Enteric Disease Study (MAL-ED): understanding the consequences for child health and development. Clin. Infect. Dis. 59 (2014), S193–S330.
33. MAL-ED Network Investigators. Growth velocity and attained size at 24 months are affected by enteropathogens and dietary intakes, but not diarrhoea: findings from the MAL-ED birth cohort study. Lancet (submitted).
34. MAL-ED Network Investigators. Prevalence of stunting at 24 months is linked to enteropathogens, diet, socioeconomic status, maternal height, and child weight at enrolment: findings from the MAL-ED birth cohort study. Lancet (submitted).
35. MAL-ED Network Investigators. Oral polio vaccine failure is associated with socio-environmental conditions, enteropathogens, and timing and frequency of vaccination: findings from the MAL-ED birth cohort study. Personal Communication.
36. Mayneris-Perxachs, J., Lima, A.A.M., Guerrant, R.L., et al. Urinary N-methylnicotinamide and β-aminoisobutyric acid predict catch-up growth in undernourished Brazilian children. Sci. Rep., 6, 2016, 19780, 10.1038/srep19780.
37. McCormick, B.J.J., Lee, G.O., Seidman, J.C., et al. Dynamics and trends in fecal biomarkers of gut function in children from 1–24 months in the MAL-ED study. Am.J.Trop. Med. Hyg., 2016 (16–0496).
38. Menzies, I.S., Zuckerman, M.J., Nukajam, W.S., et al. Geography of intestinal permeability and absorption. Gut 44 (1999), 483–489.
39. Meyers, S., Wolke, A., Field, S.P., Feuer, E.J., Johnson, J.W., Janowitz, H.D., Fecal alpha 1-antitrypsin measurement: an indicator of Crohn's disease activity. Gastroenterology 89 (1985), 13–18.
40. Mondal, D., Minak, J., Alam, M., et al. Contribution of enteric infection, altered intestinal barrier function, and maternal malnutrition to infant malnutrition in Bangladesh. Clin. Infect. Dis. 54 (2012), 185–192.
41. Moore, D.F., Rosenfeld, M.R., Gribbon, P.M., Winlove, C.P., Tsai, C.M., Alpha-1-acid (AAG, orosomucoid) glycoprotein: interaction with bacterial lipopolysaccharide and protection from sepsis. Inflammation 21 (1997), 69–82.
42. Naylor, C., Lu, M., Haque, R., et al. Environmental enteropathy, oral vaccine failure and growth faltering in infants in Bangladesh. EBioMedicine 2 (2015), 1759–1766.
43. Pearl, J., Causal diagrams for empirical research. Biometrika 82 (1995), 669–688.
44. Peterson, K.M., Buss, J., Easley, R., et al. REG1B as a predictor of childhood stunting in Bangladesh and Peru. Am. J. Clin. Nutr. 97 (2013), 1129–1133.
45. Platts-Mills, J.A., Babji, S., Bodhidatta, L., et al. Pathogen-specific burdens of community diarrhoea in developing countries: a multisite birth cohort study (MAL-ED). Lancet Glob. Health, 2015 (published online July 17) 10.1016/S2214-109X(15)00151-5.
46. Plummer, M., JAGS: A program for analysis of Bayesian graphical models using Gibbs sampling. Proceedings of the 3rd International Workshop on Distributed Statistical Computing (DSC 2003), March 2003, 20–22.
47. Prendergast, A., Kelly, P., Enteropathies in the developing world: neglected effects on global health. Am.J.Trop. Med. Hyg. 86 (2012), 756–763.
48. Richard, S.A., Barrett, L.J., Guerrant, R.L., Checkley, W., Miller, M.A., Disease surveillance methods used in the 8-site MAL-ED cohort study. Clin. Infect. Dis. 59 (2014), S220–S224.
49. Saiki, T., Myeloperoxidase concentrations in the stool as a new parameter of inflammatory bowel disease. Kurume Med. J. 45 (1998), 69–73.
50. Semba, R.D., Shardell, M., Sakr Ashour, F.A., et al. Child stunting is associated with low circulating essential amino acids. EBioMedicine 6 (2016), 246–252.
51. Subramanian, S., Huq, S., Yatsunenko, T., et al. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature 510 (2014), 417–421.
52. Viswanathan, V.K., Hodges, K., Hecht, G., Enteric infection meets intestinal function: how bacterial pathogens cause diarrhoea. Nat. Rev. Microbiol. 7 (2009), 110–119.
53. Weisz, A.J., Manary, M.J., Stephenson, K., et al. Abnormal gut integrity is associated with reduced linear growth in rural Malawian children. J. Pediatr. Gastroenterol. Nutr. 55 (2012), 747–750.
54. World Health Organization, WHO Child Growth Standards: Methods and development: Length/height-for-age, Weight-for-age, Weight-for-length, Weight-for-height and Body Mass Index-for-age. 2006, World Health Organization, Geneva, Switzerland ( http://www.who.int/childgrowth/publications/technical_report_pub/en/ accessed July 23, 2013).