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

American Journal of Tropical Medicine and Hygiene

Volumn 95, Issue 4, 2016, Pages 928-937

  Kosek, Margaret N ^a   Mduma, Estomih ^b   Kosek, Peter S ^c   Lee, Gwenyth O ^d   Svensen, Erling ^e   Pan, William K Y ^f   Olortegui, Maribel Paredes ^g   Bream, Jay H ^a   Patil, Crystal ^h   Asayag, Cesar Ramal ⁱ   Sanchez, Graciela Meza ^j   Caulfield, Laura E ^a   Gratz, Jean ^k   Yori, Pablo Peñataro ^a  

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

^b HAYDOM LUTHERAN HOSPITAL   (Tanzania)

^c Pain Consultants of Oregon   (United States)

^d TULANE UNIVERSITY   (United States)

^e HAUKELAND UNIVERSITY HOSPITAL   (Norway)

^f DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g ASOCIACIÓN BENÉFICA PRISMA   (Peru)

^h UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

ⁱ Programa Académico de Ingeniería Ambiental   (Peru)

^j UNIVERSIDAD NACIONAL DE LA AMAZONÍA PERUANA   (Peru)

^k UNIVERSITY OF VIRGINIA   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CITRULLINE; INDOLEAMINE 2,3 DIOXYGENASE; INDOLEAMINE 2,3 DIOXYGENASE 1; INTERLEUKIN 10; KYNURENINE; ORAL POLIOMYELITIS VACCINE; PENTAVALENT VACCINE; TETANUS TOXOID; TRYPTOPHAN; UNCLASSIFIED DRUG; ANTIBODY; CYTOKINE; VIRUS ANTIBODY;

ANTHROPOMETRY; ARTICLE; BLOOD LEVEL; BODY BUILD; CHILD; CLINICAL EVALUATION; COHORT ANALYSIS; CONFIDENCE INTERVAL; CORRELATION ANALYSIS; ENTEROPATHY; ENVIRONMENTAL ENTEROPATHY; ENZYME ACTIVITY; FEMALE; HIGH RISK PATIENT; HUMAN; HUMAN POLIOVIRUS 1; IMMUNE RESPONSE; INFANT; INFLAMMATION; LENGTH FOR AGE Z SCORE; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; MULTICENTER STUDY; OUTCOME ASSESSMENT; PATHOPHYSIOLOGY; PERU; RURAL AREA; SENSITIVITY AND SPECIFICITY; STUNTING; TANZANIA; TREATMENT RESPONSE; VACCINE FAILURE; WEIGHT FOR AGE Z SCORE; BLOOD; CHILD DEVELOPMENT; ENTERITIS; GROWTH DISORDER; IMMUNOLOGY; PRESCHOOL CHILD; STATISTICAL MODEL;

ANTHROPOMETRY; ANTIBODIES; ANTIBODIES, VIRAL; CHILD DEVELOPMENT; CHILD, PRESCHOOL; CITRULLINE; COHORT STUDIES; CYTOKINES; ENTERITIS; FEMALE; GROWTH DISORDERS; HUMANS; INFANT; INFLAMMATION; KYNURENINE; LINEAR MODELS; MALE; PERU; POLIOVIRUS VACCINE, ORAL; TANZANIA; TETANUS TOXOID; TRYPTOPHAN;

EID: 84990246470     PISSN: 00029637     EISSN: None     Source Type: Journal    
DOI: 10.4269/ajtmh.16-0037     Document Type: Article

References (45)

1. Kosek M, Guerrant RL, Kang G, Bhutta Z, Penataro Yori P, Gratz J, Gottlieb M, Lang D, Lee G, Haque R, Mason C, Ahmed T, Lima AA, Petri WA, Houpt E, Paredes Olortegui M, Seidman J, Mduma E, Samie A, Babji S; the MAL-ED Network Investigators, 2014. Assessment of environmental enteropathy in the MAL-ED cohort study: theoretical and analytical framework. Clin Infect Dis 59(Suppl 4):S239-S247.
2. Naylor C, Lu M, Haque R, Mondal D, Buonomo E, Nayak U, Mychlaeckyj JC, Kirkpatrick B, Colgate R, Carmolli M, Dickson D, van der Klis F, Weldon W, Oberste MO; The PROVIDE study teams, Ma JC, Petri WA Jr, 2015. Environmental enteropathy, oral vaccine failure and growth faltering in infants in Bangladesh. EBioMedicine 2:1759-1766.
3. Kelly P, Menzies I, Crane R, Zulu I, Nickols C, Feakins R, Mwansa J, Mudenda V, Katubulushi M, Greenwald S, Farthing M, 2004. Responses of small intestinal architecture and function over time to environmental factors in a tropical population. Am J Trop Med Hyg 70:412-419.
4. Galpin L, Manary MJ, Fleming K, Ou CN, Ashorn P, Shulman RJ, 2005. Effect of Lactobacillus GG on intestinal integrity in Malawian children at risk of tropical enteropathy. Am J Clin Nutr 82:1040-1045.
5. Humphrey JH, 2009. Child undernutrition, tropical enteropathy, toilets, and handwashing. Lancet 374:1032-1035.
6. Platts-Mills JA, Babji S, Bodhidatta L, Gratz J, Haque R, Havt A, McCormick BJ, McGrath M, Olortegui MP, Samie A, Shakoor S, Mondal D, Lima IF, Hariraju D, Rayamajhi BB, Qureshi S, Kabir F, Yori PP, Mufamadi B, Amour C, Carreon JD, Richard SA, Lang D, Bessong P, Mduma E, Ahmed T, Lima AA, Mason CJ, Zaidi AK, Bhutta ZA, Kosek M, Guerrant RL, Gottlieb M, Miller M, Kang G, Houpt ER; MAL-ED Network Investigators, 2015. Pathogen-specific burdens of community diarrhoea in developing countries: a multisite birth cohort study (MAL-ED). Lancet Glob Health 3:e564-e575.
7. Schertzer JD, Steinberg GR, 2014. Immunometabolism: the interface of immune and metabolic responses in disease. Immunol Cell Biol 92:303.
8. Munn DH, Mellor AL, 2013. Indoleamine 2, 3 dioxygenase and metabolic control of immune responses. Trends Immunol 34:137-143.
9. Pena OM, Pistolic J, Raj D, Fjell CD, Hancock RE, 2011. Endotoxin tolerance represents a distinctive state of alternative polarization (M2) in human mononuclear cells. J Immunol 186:7243-7254.
10. Beeson PB, 1946. Development of tolerance to typhoid bacterial pathogen and its abolition by reticulo-endothelial cell blockade. Proc Soc Exp Biol Med 61:248-250.
11. Ertel W, Kremer JP, Kenney J, Steckholzer U, Jarrar D, Trentz O, Schildberg FW, 1995. Downregulation of proinflammatory cytokine release in whole blood from septic patients. Blood 85:1341-1347.
12. Richard SA, Barrett LJ, Guerrant RL, Checkley W, Miller MA; Investigators M-EN, 2014. Disease surveillance methods used in the 8-site MAL-ED cohort study. Clin Infect Dis 59(Suppl 4):S220-S224.
13. Yori PP, Lee G, Olortegui MP, Chávez CB, Flores JT, Vasquez AO, Burga R, Pinedo SR, Asayag CR, Black RE, Caulfield LE, Kosek M, 2014. Santa Clara de Nanay: the MAL-ED cohort in Peru. Clin Infect Dis 59(Suppl 4):S310-S316.
14. Mduma ER, Gratz J, Patil C, Matson K, Dakay M, Liu S, Pascal J, McQuillin L, Mighay E, Hinken E, Ernst A, Amour C, Mvungi R, Bayyo E, Zakaria Y, Kivuyo S, Houpt ER, Svensen E, 2014. The etiology, risk factors, and interactions of enteric infections and malnutrition and the consequences for child health and development study (MAL-ED): description of the Tanzanian site. Clin Infect Dis 59(Suppl 4):S325-S330.
15. WHO Multicentre Growth Reference Study Group, 2006. WHO child growth standards based on length/height, weight and age. Acta Paediatr Suppl 450:76-85.
16. Barboza MS Jr, Silva TM, Guerrant RL, Lima AA, 1999. Measurement of intestinal permeability using mannitol and lactulose in children with diarrheal diseases. Braz J Med Biol Res 32:1499-1504.
17. Lee GO, Kosek P, Lima AA, Singh R, Yori PP, Olortegui MP, Lamsam JL, Oliveira DB, Guerrant RL, Kosek M, 2014. Lactulose: mannitol diagnostic test by HPLC and LC-MSMS platforms: considerations for field studies of intestinal barrier function and environmental enteropathy. J Pediatr Gastroenterol Nutr 59:544-550.
18. Ramakrishnan A, Althoff KN, Lopez JA, Coles CL, Bream JH, 2012. Differential serum cytokine responses to inactivated and live attenuated seasonal influenza vaccines. Cytokine 60:661-666.
19. Rosales FJ, Topping JD, Smith JE, Shankar AH, Ross AC, 2000. Relation of serum retinol to acute phase proteins and malarial morbidity in Papua New Guinea children. Am J Clin Nutr 71:1582-1588.
20. World Health Organization (WHO), 1997. Manual for the Virological Investigation of Poliomyelitis. Geneva, Switzerland: WHO.
21. Borrow R, Balmer P, Roper MH, 2007. The Immunological Basis of Immunization Series: Tetanus Update 2006. Geneva, Switzerland: World Health Organization.
22. Robberstad B, Evjen-Olsen B, 2010. Preventing mother to child transmission of HIV with highly active antiretroviral treatment in Tanzania: a prospective cost-effectiveness study. J Acquir Immune Defic Syndr 55:397-403.
23. Walker SP, Chang SM, Powell CA, Grantham-McGregor SM, 2005. Effects of early childhood psychosocial stimulation and nutritional supplementation on cognition and education in growth-stunted Jamaican children: prospective cohort study. Lancet 366:1804-1807.
24. Grantham-McGregor S, Cheung YB, Cueto S, Glewwe P, Richter L, Strupp B; International Child Development Steering Group, 2007. Developmental potential in the first 5 years for children in developing countries. Lancet 369:60-70.
25. Glewwe P, Jacoby HG, King EM, 2001. Early childhood nutrition and academic achievement: a longitudinal analysis. J Public Econ 81:345-368.
26. Akachi Y, Canning D, 2015. Inferring the economic standard of living and health from cohort height: evidence from modern populations in developing countries. Econ Hum Biol 19:114-128.
27. Kosek M, Haque R, Lima A, Babji S, Shrestha S, Qureshi S, Amidou S, Mduma E, Lee G, Yori PP, Guerrant RL, Bhutta Z, Mason C, Kang G, Kabir M, Amour C, Bessong P, Turab A, Seidman J, Olortegui MP, Quetz J, Lang D, Gratz J, Miller M, Gottlieb M; Network MAL-ED, 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.
28. Gosselin K, McDonald C, Kellogg M, Manji K, Kisenge R, Aboud S, Maleta K, Benzoni N, Fawzi W, Manary M, Duggan C, 2015. Serum citrulline does not predict stunting or environmental enteric dysfunction in Tanzanian and Malawian infants. FASEB J 29:403-5.
29. Wessells KR, Hess SY, Rouamba N, Ouédraogo ZP, Kellogg M, Goto R, Duggan C, Ouédraogo JB, Brown KH, 2013. Associations between intestinal mucosal function and changes in plasma zinc concentration following zinc supplementation. J Pediatr Gastroenterol Nutr 57:348-355.
30. Previsani N, Tangermann RH, Tallis G, Jafari HS, 2015. World Health Organization guidelines for containment of poliovirus following type-specific polio eradication: worldwide, 2015. Morb Mortal Wkly Rep 64:913-917.
31. Mellor AL, Munn DH, 2004. IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat Rev Immunol 4:762-774.
32. Dai X, Zhu BT, 2010. Indoleamine 2, 3-dioxygenase tissue distribution and cellular localization in mice: implications for its biological functions. J Histochem Cytochem 58:17-28.
33. Gupta NK, Thaker AI, Kanuri N, Riehl TE, Rowley CW, Stenson WF, Ciorba MA, 2012. Serum analysis of tryptophan catabolism pathway: correlation with Crohn's disease activity. Inflamm Bowel Dis 18:1214-1220.
34. Zelante T, Iannitti RG, Cunha C, De Luca A, Giovannini G, Pieraccini G, Zecchi R, D'Angelo C, Massi-Benedetti C, Fallarino F, Carvalho A, Puccetti P, Romani L, 2013. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity 39:372-385.
35. h17 to regulatory T cells in HIV disease. Sci Transl Med 2:32ra36.
36. Braat H, Rottiers P, Hommes DW, Huyghebaert N, Remaut E, Remon JP, van Deventer SJ, Neirynck S, Peppelenbosch MP, Steidler L, 2006. A phase I trial with transgenic bacteria expressing interleukin-10 in Crohn's disease. Clin Gastroenterol Hepatol 4:754-759.
37. Moehn S, Pencharz PB, Ball RO, 2012. Lessons learned regarding symptoms of tryptophan deficiency and excess from animal requirement studies. J Nutr 142:2231S-2235S.
38. Lepage N, McDonald N, Dallaire L, Lambert M, 1997. Agespecific distribution of plasma amino acid concentrations in a healthy pediatric population. Clin Chem 43:2397-2402.
39. Nuss ET, Tanumihardjo SA, 2011. Quality protein maize for Africa: closing the protein inadequacy gap in vulnerable populations. Adv Nutr 2:217-224.
40. Vasal JK, 2000. The quality protein maize story. Food Nutr Bull 21:445-450.
41. Marcobal A, Kashyap PC, Nelson TA, Aronov PA, Donia MS, Spormann A, Fischbach MA, Sonnenburg JL, 2013. A metabolomic view of how the human gut microbiota impacts the host metabolome using humanized and gnotobiotic mice. ISME J 7:1933-1943.
42. Kampman-van de Hoek E, Jansmann AJM, van den Borne JJGC, van der Peet-Schwering CMC, van Beers-Schreurs H, Gerrits WJJ, 2016. Dietary amino acid deficiency reduces the utilization of amino acids for growth in growing pigs after a period of poor health. J Nutr 146:51-58.
43. Le Floc'h N, Matte JJ, Melchior D, van Milgen J, Seve B, 2010. A moderate inflammation caused by the deterioration of housing conditions modifies Trp metabolism but not Trp requirement for growth of post-weaned piglets. Animal 4:1891-1898.
44. de Ridder K, Levesque CL, Htoo JK, de Lange CF, 2012. Immune system stimulation reduces the efficiency of tryptophan utilization for body protein deposition in growing pigs. J Anim Sci 90:3485-3491.
45. Reeds PJ, Fjeld CR, Jahoor F, 1994. Do the differences between the amino acid compositions of acute-phase and muscle proteins have a bearing on nitrogen loss in traumatic states? J Nutr 124:906-910.