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Birth weight and postnatal microbial exposures predict the distribution of peripheral blood leukocyte subsets in young adults in the Philippines

Published online by Cambridge University Press:  11 October 2017

T. W. McDade*
Affiliation:
Department of Anthropology, Northwestern University, Evanston, IL, USA Institute for Policy Research, Northwestern University, Evanston, IL, USA Child and Brain Development Program, Canadian Institute for Advanced Research, Toronto, ON, Canada
M. J. Jones
Affiliation:
BC Children’s Hospital Research Institute, University of British Columbia, Vancouver, BC, Canada
G. Miller
Affiliation:
Institute for Policy Research, Northwestern University, Evanston, IL, USA Department of Psychology, Northwestern University, Evanston, IL, USA
J. Borja
Affiliation:
USC-Office of Population Studies Foundation Inc., University of San Carlos, Cebu City, the Philippines Department of Nutrition and Dietetics, University of San Carlos, Cebu City, the Philippines
M. S. Kobor
Affiliation:
Child and Brain Development Program, Canadian Institute for Advanced Research, Toronto, ON, Canada BC Children’s Hospital Research Institute, University of British Columbia, Vancouver, BC, Canada
C. W. Kuzawa
Affiliation:
Department of Anthropology, Northwestern University, Evanston, IL, USA Institute for Policy Research, Northwestern University, Evanston, IL, USA
*
*Address for correspondence: T. W. McDade, Department of Anthropology, Northwestern University, Evanston, IL 60208, USA. (Email [email protected])

Abstract

The immune system not only provides protection against infectious disease but also contributes to the etiology of neoplastic, atopic, and cardiovascular and metabolic diseases. Prenatal and postnatal nutritional and microbial environments have lasting effects on multiple aspects of immunity, indicating that immune processes may play important roles in the developmental origins of disease. The objective of this study is to evaluate the association between birth weight and the distribution of leukocyte (white blood cell) subsets in peripheral blood in young adulthood. Postnatal microbial exposures were also considered as predictors of leukocyte distribution. Participants (n=486; mean age=20.9 years) were drawn from a prospective birth cohort study in the Philippines, and analyses focused on the following cell types: CD4 T lymphocytes, CD8 T lymphocytes, B lymphocytes, natural killer cells, monocytes, granulocytes. Higher birth weight was a strong predictor of higher proportion of CD4 T lymphocytes (B=0.12, s.e.=0.041, P=0.003), lower proportion of CD8 T lymphocytes (B=−0.874, s.e.=0.364, P=0.016), higher CD4:CD8 ratio (B=1.964, s.e.=0.658, P=0.003), and higher B lymphocytes (B=0.062, s.e.=0.031, P=0.047). Measures of microbial exposure in infancy were negatively associated with proportions of B lymphocytes and granulocytes, and lower CD4:CD8 ratio. Leukocytes are the key regulators and effectors of innate and specific immunity, but the origins of variation in the distribution of cell type across individuals are not known. Our findings point toward nutritional and microbial exposures in infancy as potentially important determinants of immune-phenotypes in adulthood, and they suggest that leukocyte distribution is a plausible mechanism through which developmental environments have lasting effects on disease risk in adulthood.

Type
Original Article
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2017 

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References

1. Wadhwa, PD, Buss, C, Entringer, S, Swanson, JM. Developmental origins of health and disease: brief history of the approach and current focus on epigenetic mechanisms. Semin Reprod Med. 2009; 27, 358368.CrossRefGoogle ScholarPubMed
2. Gluckman, PD, Hanson, MA, Cooper, C, Thornburg, KL. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med. 2008; 359, 6173.Google Scholar
3. Smith, CJ, Ryckman, KK. Epigenetic and developmental influences on the risk of obesity, diabetes, and metabolic syndrome. Diabetes Metab Syndr Obes. 2015; 8, 295302.Google ScholarPubMed
4. Hansson, GK, Hermansson, A. The immune system in atherosclerosis. Nat Immunol. 2011; 12, 204212.CrossRefGoogle ScholarPubMed
5. de Visser, KE, Eichten, A, Coussens, LM. Paradoxical roles of the immune system during cancer development. Nat Rev Cancer. 2006; 6, 2437.Google Scholar
6. Chandra, RK. Reduced secretory antibody response to live attenuated measles and poliovirus vaccines in malnourished children. BMJ. 1975; 2, 583585.Google Scholar
7. Chandra, RK. Serum thymic hormone activity and cell-mediated immunity in healthy neonates, preterm infants, and small-for-gestational age infants. Pediatrics. 1981; 67, 407411.Google Scholar
8. Moore, SE, Prentice, AM, Wagatsuma, Y, et al. Early-life nutritional and environmental determinants of thymic size in infants born in rural bangladesh. Acta Paediatr. 2009; 98, 11681175.Google Scholar
9. Ferguson, AC. Prolonged impairment of cellular immunity in children with intrauterine growth retardation. J Pediatr. 1978; 93, 5256.CrossRefGoogle ScholarPubMed
10. Sattar, N, McConnachie, A, O’Reilly, D, et al. Inverse association between birth weight and c-reactive protein concentrations in the midspan family study. Arterioscler Thromb Vasc Biol. 2004; 24, 583587.Google Scholar
11. McDade, TW, Rutherford, J, Adair, L, Kuzawa, CW. Early origins of inflammation: microbial exposures in infancy predict lower levels of c-reactive protein in adulthood. Proc Biol Sci. 2010; 277, 11291137.Google Scholar
12. McDade, TW, Metzger, MW, Chyu, L, et al. Long-term effects of birth weight and breastfeeding duration on inflammation in early adulthood. P R Soc B. 2014; 281, 20133116.Google Scholar
13. Chen, W, Srinivasan, SR, Berenson, GS. Influence of birth weight on white blood cell count in biracial (black-white) children, adolescents, and young adults: the Bogalusa Heart Study. Am J Epidemiol. 2009; 169, 214218.CrossRefGoogle Scholar
14. Moore, SE, Jalil, F, Ashraf, R, et al. Birth weight predicts response to vaccination in adults born in an urban slum in lahore, pakistan. Am J Clin Nutr. 2004; 80, 453459.CrossRefGoogle Scholar
15. Godfrey, KM, Barker, DJP, Osmond, C. Disproportionate fetal growth and raised ige concentration in adult life. Clin Exp Allergy. 1994; 24, 641648.Google Scholar
16. Barker, DJ, Eriksson, JG, Forsen, T, Osmond, C. Fetal origins of adult disease: strength of effects and biological basis. Int J Epidemiol. 2002; 31, 12351239.Google Scholar
17. Rook, GA, Lowry, CA, Raison, CL. Hygiene and other early childhood influences on the subsequent function of the immune system. Brain Res. 2015; 1617, 4762.CrossRefGoogle ScholarPubMed
18. Stein, MM, Hrusch, CL, Gozdz, J, et al. Innate immunity and asthma risk in amish and hutterite farm children. N Engl J Med. 2016; 375, 411421.Google Scholar
19. Yazdanbakhsh, M, Dremsner, PG, van Ree, R. Allergy, parasites, and the hygiene hypothesis. Science. 2002; 296, 490494.Google Scholar
20. McDade, T, Beck, MA, Kuzawa, C, Adair, L. Prenatal undernutrition, postnatal environments, and antibody response to vaccination in adolescence. Am J Clin Nutr. 2001; 74, 543548.Google Scholar
21. McDade, TW. Life history theory and the immune system: steps toward a human ecological immunology. Am J Phys Anthropol. 2003; 37(Suppl.), 100125.Google Scholar
22. Male, DK. Immunology, 8th edn, (ed. Male DK, Brostoff J, Roth DB, Roitt IM), 2013. Elsevier/Saunders: Philadelphia, USA.Google Scholar
23. Adair, LS, Popkin, BM, Akin, JS, et al. Cohort profile: the Cebu longitudinal health and nutrition survey. Int J Epidemiol. 2011; 40, 619625.CrossRefGoogle ScholarPubMed
24. McDade, TW, Beck, MA, Kuzawa, CW, Adair, LS. Prenatal undernutrition and postnatal growth are associated with adolescent thymic function. J Nutr. 2001; 131, 12251231.CrossRefGoogle ScholarPubMed
25. Ziegler-Heitbrock, L. The cd14+ cd16+ blood monocytes: their role in infection and inflammation. J Leukoc Biol. 2007; 81, 584592.Google Scholar
26. McDade, TW, Georgiev, AV, Kuzawa, CW. Trade-offs between acquired and innate immune defenses in humans. Evol Med Public Health. 2016; 2016, 116.Google Scholar
27. Perez, TL. Attrition in the Cebu longitudinal health and nutrition survey. Report Series No. 1, USC-Office of Population Studies Foundation Inc., 2015.Google Scholar
28. McDade, TW, Borja, JB, Largado, F, Adair, LS, Kuzawa, CW. Adiposity and chronic inflammation in young women predict inflammation during normal pregnancy in the philippines. J Nutr. 2016; 146, 353357.CrossRefGoogle ScholarPubMed
29. McDade, TW, Ryan, C, Jones, MJ, et al. Social and physical environments early in development predict DNA methylation of inflammatory genes in young adulthood. Proc Natl Acad Sci USA. 2017; 114, 76117616.Google Scholar
30. Ji, H, Ehrlich, LI, Seita, J, et al. Comprehensive methylome map of lineage commitment from haematopoietic progenitors. Nature. 2010; 467, 338342.CrossRefGoogle ScholarPubMed
31. Houseman, EA, Accomando, WP, Koestler, DC, et al. DNA methylation arrays as surrogate measures of cell mixture distribution. BMC Bioinformatics. 2012; 13, 86.Google Scholar
32. Koestler, DC, Christensen, B, Karagas, MR, et al. Blood-based profiles of DNA methylation predict the underlying distribution of cell types: a validation analysis. Epigenetics. 2013; 8, 816826.Google Scholar
33. Aryee, MJ, Jaffe, AE, Corrada-Bravo, H, et al. Minfi: a flexible and comprehensive bioconductor package for the analysis of infinium DNA methylation microarrays. Bioinformatics. 2014; 30, 13631369.Google Scholar
34. Lohman, TG, Roche, AF, Martorell, R. Anthropometric Standardization Reference Manual. 1988. Human Kinetics Books: Champaign, IL.Google Scholar
35. Nurgalieva, ZZ, Malaty, HM, Graham, DY, et al. Helicobacter pylori infection in Kazakhstan: effect of water source and household hygiene. Am J Trop Med Hyg. 2002; 67, 201206.Google Scholar
36. VanDerslice, J, Popkin, B, Briscoe, J. Drinking-water quality, sanitation, and breast-feeding: their interactive effects on infant health. Bull World Health Organ. 1994; 72, 589601.Google Scholar
37. Moe, CL, Sobsey, MD, Samsa, GP, Mesolo, V. Bacterial indicators of risk of diarrhoeal disease from drinking water in the philippines. Bull World Health Organ. 1991; 9, 305317.Google Scholar
38. Vyas, S, Kumaranayake, L. Constructing socio-economic status indices: how to use principal components analysis. Health Policy Plan. 2006; 21, 459468.Google Scholar
39. Kratz, A, Ferraro, M, Sluss, PM, Lewandrowski, KB. Laboratory reference values. N Engl J Med. 2004; 351, 15481563.Google Scholar
40. Valiathan, R, Deeb, K, Diamante, M, et al. Reference ranges of lymphocyte subsets in healthy adults and adolescents with special mention of T cell maturation subsets in adults of South Florida. Immunobiology. 2014; 219, 487496.Google Scholar
41. Wu, X, Zhao, M, Pan, B, Zhang, J, Peng, M, Wang, L, et al. Complete blood count reference intervals for healthy han chinese adults. PLoS One. 2015; 10, e0119669.Google Scholar
42. Lee, BW, Yap, HK, Chew, FT, et al. Age- and sex-related changes in lymphocyte subpopulations of healthy Asian subjects: from birth to adulthood. Cytometry. 1996; 26, 815.Google Scholar
43. Ferrari, SLP, Cribari-Neto, F. Beta regression for modelling rates and proportions. J Appl Stat. 2004; 31, 799815.Google Scholar
44. Brodin, P, Davis, MM. Human immune system variation. Nat Rev Immunol. 2017; 17, 2129.Google Scholar
45. McDade, TW, Kuzawa, CW, Adair, LS, Beck, MA. Prenatal and early postnatal environments are significant predictors of total immunoglobulin E concentration in Filipino adolescents. Clin Exp Allergy. 2004; 34, 4450.Google Scholar
46. Raqib, R, Alam, DS, Sarker, P, et al. Low birth weight is associated with altered immune function in rural Bangladeshi children: a birth cohort study. Am J Clin Nutr. 2007; 85, 845852.Google Scholar
47. Kiss, S, Walcz, E, Revesz, T, Bors, Z, Schuler, D. Lymphocyte subpopulations in peripheral blood of small-for-gestational age and appropriate-for-gestational age preterm neonates. Acta Paediatr Hung. 1984; 25, 291297.Google Scholar
48. Pelkonen, AS, Suomalainen, H, Hallman, M, Turpeinen, M. Peripheral blood lymphocyte subpopulations in schoolchildren born very preterm. Arch Dis Child. 1999; 81, F188F193.CrossRefGoogle ScholarPubMed
49. Montez, JK, Hayward, MD. Cumulative childhood adversity, educational attainment, and active life expectancy among us adults. Demography. 2014; 51, 413435.Google Scholar
50. Miller, GE, Chen, E, Fok, AK, et al. Low early-life social class leaves a biological residue manifested by decreased glucocorticoid and increased proinflammatory signaling. Proc Natl Acad Sci USA. 2009; 106, 1471614721.Google Scholar
51. Taylor, SE, Lehman, BJ, Kiefe, CI, Seeman, TE. Relationship of early life stress and psychological functioning to adult c-reactive protein in the coronary artery risk development in young adults study. Biol Psychiatry. 2006; 60, 819824.Google Scholar
52. Esposito, EA, Jones, MJ, Doom, JR, et al. Differential DNA methylation in peripheral blood mononuclear cells in adolescents exposed to significant early but not later childhood adversity. Dev Psychopathol. 2016; 28, 13851399.Google Scholar
53. Horne, BD, Anderson, JL, John, JM, et al. Which white blood cell subtypes predict increased cardiovascular risk? J Am Coll Cardiol. 2005; 46, 16381643.Google Scholar
54. Ferguson, FG, Wikby, A, Maxson, P, Olsson, J, Johansson, B. Immune parameters in a longitudinal study of a very old population of Swedish people: a comparison between survivors and nonsurvivors. J Gerontol A Biol Sci Med Sci. 1995; 50, B378B382.CrossRefGoogle Scholar
55. Crowe, SM, Carlin, JB, Stewart, KI, Lucas, CR, Hoy, JF. Predictive value of CD4 lymphocyte numbers for the development of opportunistic infections and malignancies in HIV-infected persons. J Acq Immun Def Synd. 1991; 4, 770776.Google Scholar
56. Georgiev, AV, Kuzawa, CW, McDade, TW. Early developmental exposures shape trade-offs between acquired and innate immunity in humans. Evol Med Public Health. 2016; 1, 256269.Google Scholar