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Zotero
EndNote
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Stunting Is Preceded by Intestinal Mucosal Damage and Microbiome Changes and Is Associated with Systemic Inflammation in a Cohort of Peruvian Infants
Mara Zambruni
Mara Zambruni
Department of Pediatrics, The University of Texas Health Science Center at Houston Medical School, Houston, Texas;
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Theresa J. Ochoa
Theresa J. Ochoa
Department of Pediatrics, The University of Texas Health Science Center at Houston Medical School, Houston, Texas;
Department of Pediatrics, The University of Texas Health Science Center at Houston Medical School, Houston, Texas;
Instituto de Medicina Tropical “Alexander von Humboldt,” Universidad Peruana Cayetano Heredia, Lima, Peru;
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Department of Pediatrics, The University of Texas Health Science Center at Houston Medical School, Houston, Texas;
Instituto de Medicina Tropical “Alexander von Humboldt,” Universidad Peruana Cayetano Heredia, Lima, Peru;
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Anoma Somasunderam
Anoma Somasunderam
Division of Infectious Diseases, The University of Texas Health Science Center at Houston Medical School, Houston, Texas;
Division of Infectious Diseases, The University of Texas Health Science Center at Houston Medical School, Houston, Texas;
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Division of Infectious Diseases, The University of Texas Health Science Center at Houston Medical School, Houston, Texas;
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Miguel M. Cabada
Miguel M. Cabada
Universidad Peruana Cayetano Heredia–University of Texas Medical Branch Collaborative Research Center Cusco, Universidad Peruana Cayetano Heredia, Cusco, Peru;
Universidad Peruana Cayetano Heredia–University of Texas Medical Branch Collaborative Research Center Cusco, Universidad Peruana Cayetano Heredia, Cusco, Peru;
Infectious Diseases Division, Department of Internal Medicine, University of Texas Medical Branch, Galveston, Texas;
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Universidad Peruana Cayetano Heredia–University of Texas Medical Branch Collaborative Research Center Cusco, Universidad Peruana Cayetano Heredia, Cusco, Peru;
Infectious Diseases Division, Department of Internal Medicine, University of Texas Medical Branch, Galveston, Texas;
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Maria L. Morales
Maria L. Morales
Universidad Peruana Cayetano Heredia–University of Texas Medical Branch Collaborative Research Center Cusco, Universidad Peruana Cayetano Heredia, Cusco, Peru;
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Makedonka Mitreva
Makedonka Mitreva
The McDonnell Genome Institute, Washington University in St. Louis, St. Louis, Missouri;
Division of Infectious Diseases, Department of Medicine, Washington University School of Medicine, St. Louis, Missouri
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Division of Infectious Diseases, Department of Medicine, Washington University School of Medicine, St. Louis, Missouri
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Bruce A. Rosa
Bruce A. Rosa
The McDonnell Genome Institute, Washington University in St. Louis, St. Louis, Missouri;
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Gonzalo J. Acosta
Gonzalo J. Acosta
Instituto de Medicina Tropical “Alexander von Humboldt,” Universidad Peruana Cayetano Heredia, Lima, Peru;
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Natalia I. Vigo
Natalia I. Vigo
Instituto de Medicina Tropical “Alexander von Humboldt,” Universidad Peruana Cayetano Heredia, Lima, Peru;
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Maribel Riveros
Maribel Riveros
Instituto de Medicina Tropical “Alexander von Humboldt,” Universidad Peruana Cayetano Heredia, Lima, Peru;
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Sara Arango
Sara Arango
Instituto de Medicina Tropical “Alexander von Humboldt,” Universidad Peruana Cayetano Heredia, Lima, Peru;
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David Durand
David Durand
Instituto de Medicina Tropical “Alexander von Humboldt,” Universidad Peruana Cayetano Heredia, Lima, Peru;
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Maitreyee N. Berends
Maitreyee N. Berends
Infectious Diseases Division, Department of Internal Medicine, University of Texas Medical Branch, Galveston, Texas;
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Peter Melby
Peter Melby
Infectious Diseases Division, Department of Internal Medicine, University of Texas Medical Branch, Galveston, Texas;
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Netanya S. Utay
Netanya S. Utay
Division of Infectious Diseases, The University of Texas Health Science Center at Houston Medical School, Houston, Texas;
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Stunting, defined as height-for-age Z score equal to or lower than −2, is associated with increased childhood mortality, cognitive impairment, and chronic diseases. The aim of the study was to investigate the relationship between linear growth, intestinal damage, and systemic inflammation in infants at risk of stunting. We followed up 78 infants aged 5–12 months living in rural areas of Peru for 6 months. Blood samples for biomarkers of intestinal damage (intestinal fatty-acid–binding protein [I-FABP] and zonulin) and systemic inflammation (interleukin-1β, interleukin-6, tumor necrosis factor α [TNF-α], soluble CD14, and lipopolysaccharide-binding protein [LBP]) and fecal samples for microbiome analysis were collected at baseline and closure of the study. The children’s growth and health status were monitored through biweekly home visits by trained staff. Twenty-one percent of the children became stunted: compared with non-stunted children, they had worse nutritional parameters and higher levels of serum I-FABP at baseline. The likelihood of becoming stunted was strongly associated with an increase in sCD14 over time; LBP and TNF-α showed a trend toward increase in stunted children but not in controls. The fecal microbiota composition of stunted children had an increased beta diversity compared with that of healthy controls throughout the study. The relative abundance of Ruminococcus 1 and 2, Clostridium sensu stricto, and Collinsella increased in children becoming stunted but not in controls, whereas Providencia abundance decreased. In conclusion, stunting in our population was preceded by an increase in markers of enterocyte turnover and differences in the fecal microbiota and was associated with increasing levels of systemic inflammation markers.
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Author Notes
Financial support: This study was supported by the Thrasher Research fund.
Authors’ addresses: Mara Zambruni, Department of Pediatrics, The University of Texas Health Science Center at Houston Medical School, Houston, TX, E-mail: mara.zambruni@uth.tmc.edu. Theresa J. Ochoa, Gonzalo J. Acosta, Natalia I. Vigo, Maribel Riveros, Sara Arango, and David Durand, Instituto de Medicina Tropical “Alexander von Humboldt,” Universidad Peruana Cayetano Heredia, Lima, Peru, E-mails: theresa.j.ochoa@uth.tmc.edu, gjacostagarcia@houstonmethodist.org, natalia.vigo@outlook.com, maribel.riveros@upch.pe, sara.arango29@gmail.com, and david.durand@upch.pe. Anoma Somasunderam and Netanya S. Utay, Division of Infectious Diseases, The University of Texas Health Science Center at Houston Medical School, Houston, TX, E-mails: anoma.somasunderam@uth.tmc.edu and netanya.s.utay@uth.tmc.edu. Miguel M. Cabada, Maitreyee N. Berends, and Peter Melby, Infectious Diseases Division, Department of Internal Medicine, University of Texas Medical Branch, Galveston, TX, E-mails: micabada@utmb.edu, maitreyee.n.berends@ttuhsc.edu, and pcmelby@utmb.edu. Maria L. Morales, Universidad Peruana Cayetano Heredia–University of Texas Medical Branch Collaborative Research Center Cusco, Universidad Peruana Cayetano Heredia, Cusco, Peru, E-mail: maria.morales.f@upch.pe. Makedonka Mitreva, Division of Infectious Diseases, Department of Medicine, Washington University School of Medicine, St. Louis, MO, E-mail: mmitreva@wustl.edu. Bruce A. Rosa, The McDonnell Genome Institute, Washington University in St. Louis, MO, E-mail: barosa@wustl.edu.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
WHO, World Bank, UNICEF, 2017. Joint Child Malnutrition Estimates New York, NY: United Nations Children’s Fund, the World Health Organization, the World Bank Group.
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2.
Prendergast AJ, Humphrey JH, 2014. The stunting syndrome in developing countries. Paediatr Int Child Health 34: 250–265.
-
3.
Misselhorn A, Hendriks SL, 2017. A systematic review of sub-national food insecurity research in South Africa: missed opportunities for policy insights. PLoS One 12: e0182399.
-
4.
Dewey KG, Adu-Afarwuah S, 2008. Systematic review of the efficacy and effectiveness of complementary feeding interventions in developing countries. Matern Child Nutr 4: 24–85.
-
5.
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.
-
6.
Prendergast AJ, Rukobo S, Chasekwa B, Mutasa K, Ntozini R, Mbuya MN, Jones A, Moulton LH, Stoltzfus RJ, Humphrey JH, 2014. Stunting is characterized by chronic inflammation in Zimbabwean infants. PLoS One 9: e86928.
-
7.
Panter-Brick C, Lunn PG, Langford RM, Maharjan M, Manandhar DS, 2009. Pathways leading to early growth faltering: an investigation into the importance of mucosal damage and immunostimulation in different socio-economic groups in Nepal. Br J Nutr 101: 558–567.
-
8.
Campbell DI, Murch SH, Elia M, Sullivan PB, Sanyang MS, Jobarteh B, Lunn PG, 2003. Chronic T cell-mediated enteropathy in rural west African children: relationship with nutritional status and small bowel function. Pediatr Res 54: 306–311.
-
9.
Chacko CJ, Paulson KA, Mathan VI, Baker SJ, 1969. The villus architecture of the small intestine in the tropics: a necropsy study. J Pathol 98: 146–151.
-
10.
Hossain MI, Nahar B, Hamadani JD, Ahmed T, Roy AK, Brown KH, 2010. Intestinal mucosal permeability of severely underweight and nonmalnourished Bangladeshi children and effects of nutritional rehabilitation. J Pediatr Gastroenterol Nutr 51: 638–644.
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11.
Kelly P et al. 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.
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12.
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.
-
13.
Prendergast A, Kelly P, 2012. Enteropathies in the developing world: neglected effects on global health. Am J Trop Med Hyg 86: 756–763.
-
14.
Weisz AJ, Manary MJ, Stephenson K, Agapova S, Manary FG, Thakwalakwa C, Shulman RJ, Manary MJ, 2012. Abnormal gut integrity is associated with reduced linear growth in rural Malawian children. J Pediatr Gastroenterol Nutr 55: 747–750.
-
15.
Working Group of Infant and Young Child Feeding Indicators, 2007. Developing and Validating Simple Indicators of Dietary Quality of Infants and Young Children in Developing Countries: Food and Nutrition Technical Assistance. Washington, DC: FHI 360.
-
16.
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C, 2011. Metagenomic biomarker discovery and explanation. Genome Biol 12: R60.
-
17.
Levy E, Menard D, Delvin E, Montoudis A, Beaulieu JF, Mailhot G, Dubé N, Sinnett D, Seidman E, Bendayan M, 2009. Localization, function and regulation of the two intestinal fatty acid-binding protein types. Histochem Cell Biol 132: 351–367.
-
18.
Vreugdenhil AC, Wolters VM, Adriaanse MP, Van den Neucker AM, van Bijnen AA, Houwen R, Buurman WA, 2011. Additional value of serum I-FABP levels for evaluating celiac disease activity in children. Scand J Gastroenterol 46: 1435–1441.
-
19.
Fasano A, 2012. Intestinal permeability and its regulation by zonulin: diagnostic and therapeutic implications. Clin Gastroenterol Hepatol 10: 1096–1100.
-
20.
Thayu M, Denson LA, Shults J, Zemel BS, Burnham JM, Baldassano RN, Howard KM, Ryan A, Leonard MB, 2010. Determinants of changes in linear growth and body composition in incident pediatric Crohn’s disease. Gastroenterology 139: 430–438.
-
21.
Sandler NG, Douek DC, 2012. Microbial translocation in HIV infection: causes, consequences and treatment opportunities. Nat Rev Microbiol 10: 655–666.
-
22.
Sandler NG et al. 2011. Plasma levels of soluble CD14 independently predict mortality in HIV infection. J Infect Dis 203: 780–790.
-
23.
Alvarez P, Mwamzuka M, Marshed F, Kravietz A, Ilmet T, Ahmed A, Borkowsky W, Khaitan A, 2017. Immune activation despite preserved CD4 T cells in perinatally HIV-infected children and adolescents. PLoS One 12: e0190332.
-
24.
Tsalkidou EA, Roilides E, Gardikis S, Trypsianis G, Kortsaris A, Chatzimichael A, Tentes I, 2013. Lipopolysaccharide-binding protein: a potential marker of febrile urinary tract infection in childhood. Pediatr Nephrol 28: 1091–1097.
-
25.
Adriaanse MP et al. 2013. Serum I-FABP as marker for enterocyte damage in coeliac disease and its relation to villous atrophy and circulating autoantibodies. Aliment Pharmacol Ther 37: 482–490.
-
26.
Derikx JP, Vreugdenhil AC, Van den Neucker AM, Grootjans J, van Bijnen AA, Damoiseaux JG, van Heurn LW, Heineman E, Buurman WA, 2009. A pilot study on the noninvasive evaluation of intestinal damage in celiac disease using I-FABP and L-FABP. J Clin Gastroenterol 43: 727–733.
-
27.
Derikx JP, Blijlevens NM, Donnelly JP, Fujii H, Kanda T, van Bijnen AA, Heineman E, Buurman WA, 2009. Loss of enterocyte mass is accompanied by diminished turnover of enterocytes after myeloablative therapy in haematopoietic stem-cell transplant recipients. Ann Oncol 20: 337–342.
-
28.
Kotloff KL et al. 2012. The Global Enteric Multicenter Study (GEMS) of diarrheal disease in infants and young children in developing countries: epidemiologic and clinical methods of the case/control study. Clin Infect Dis 55 (Suppl 4): S232–S245.
-
29.
Zambruni M et al. 2016. High prevalence and increased severity of norovirus mixed infections among children 12–24 months of age living in the suburban areas of Lima, Peru. J Pediatr Infect Dis Soc 5: 337–341.
-
30.
Acosta GJ, Vigo NI, Durand D, Riveros M, Arango S, Zambruni M, Ochoa TJ, 2016. Diarrheagenic Escherichia coli: prevalence and pathotype distribution in children from Peruvian rural communities. Am J Trop Med Hyg 95: 574–579.
-
31.
Lima AAM et al. 2017. Enteroaggregative E. coli subclinical infection and co-infections and impaired child growth in the MAL-ED cohort study. J Pediatr Gastroenterol Nutr 66: 325–333.
-
32.
Olofin I, McDonald CM, Ezzati M, Flaxman S, Black RE, Fawzi WW, Caulfield LE, Danaei G; Nutrition Impact Model Study (Anthropometry Cohort Pooling), 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.
-
33.
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.
-
34.
Morris MC, Gilliam EA, Li L, 2014. Innate immune programing by endotoxin and its pathological consequences. Front Immunol 5: 680.
-
35.
Backhed F et al. 2015. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17: 852.
-
36.
Bokulich NA et al. 2016. Antibiotics, birth mode, and diet shape microbiome maturation during early life. Sci Transl 8: 343ra82.
-
37.
Yatsunenko T et al. 2012. Human gut microbiome viewed across age and geography. Nature 486: 222–227.
-
38.
Tamburini S, Shen N, Wu HC, Clemente JC, 2016. The microbiome in early life: implications for health outcomes. Nat Med 22: 713–722.
-
39.
Johnson CL, Versalovic J, 2012. The human microbiome and its potential importance to pediatrics. Pediatrics 129: 950–960.
-
40.
Backhed F, Fraser CM, Ringel Y, Sanders ME, Sartor RB, Sherman PM, Versalovic J, Young V, Finlay BB, 2012. Defining a healthy human gut microbiome: current concepts, future directions, and clinical applications. Cell Host Microbe 12: 611–622.
-
41.
Yassour M et al. 2016. Natural history of the infant gut microbiome and impact of antibiotic treatment on bacterial strain diversity and stability. Sci Transl Med 8: 343ra81.
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