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Maternal pregnancy C-reactive protein predicts offspring birth size and body composition in metropolitan Cebu, Philippines

Published online by Cambridge University Press:  19 July 2017

C. W. Kuzawa ,
R. L. Fried ,
J. B. Borja  and
T. W. McDade
C. W. Kuzawa*
Affiliation:
Department of Anthropology, Northwestern University, Evanston, IL, USA Institute for Policy Research, Northwestern University, Evanston, IL, USA
R. L. Fried
Affiliation:
Department of Anthropology, Northwestern University, Evanston, IL, USA
J. B. Borja
Affiliation:
Office of Population Studies Foundation, University of San Carlos, Cebu City, Philippines
T. W. McDade
Affiliation:
Department of Anthropology, Northwestern University, Evanston, IL, USA Institute for Policy Research, Northwestern University, Evanston, IL, USA
*
*Address for correspondence: C. W. Kuzawa, Department of Anthropology, Northwestern University, 1810 Hinman, Evanston, IL 60208, USA. (Email [email protected])
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Abstract

The gestational milieu is an important influence on fetal development and long-term disease risk. Here we assess relationships between maternal pregnancy inflammation, indicated by C-reactive protein (CRP), and offspring anthropometric outcomes measured soon after birth. Data come from female participants (n=327, age 24.4–30.2 years) in a longitudinal study located in Metropolitan Cebu, Philippines. Between 2009 and 2014, pregnancy interviews (n=429) were conducted during which questionnaire and anthropometric data were obtained along with dried blood spot cards for CRP measurement. Offspring body weight, length, head circumference and five skinfold thickness measures were obtained soon after birth. Maternal pregnancy CRP was borderline (−1.11±0.64 days/log-mg/l; P<0.1) inversely related to gestational age at delivery, but did not increase the likelihood of preterm delivery. After adjusting for maternal pre-pregnancy body mass index, height, pregnancy adiposity, age, parity and other covariates, CRP was significantly, inversely related to offspring body weight (−0.047±0.017 kg/log-mg/l), length (−0.259±0.092 cm/log-mg/l) and sum of skinfolds (−0.520±0.190 mm/log-mg/l) (all P<0.05), and borderline inversely related to offspring head circumference (−0.102±0.068 cm/log-mg/l; P<0.1). Notably, relationships were continuous across the full CRP range, and not limited to unusually high levels of inflammation. These findings point to an important role of maternal non-specific immune activation as a predictor of offspring birth outcomes. In light of evidence that early life microbial, nutritional and stress experiences influence adult inflammatory regulation, these findings point to inflammation as a potential pathway for the intergenerational transmission of maternal experience to offspring health.

Keywords

body fatgrowthinflammationintergenerationalnewborn
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 8 , Issue 6 , December 2017 , pp. 674 - 681
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Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2017 

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References

1. Barker, D. Mothers, Babies, and Health in Later Life (2nd edn) 1998. Churchill Livingstone: Edinburgh, UK.Google Scholar
2. Gluckman, PD, Hanson, MA, Cooper, C, Thornburg, KL. Effect of in utero and early-life conditions on adult health and disease. New Engl J Med. 2009; 359, 61–73.Google Scholar
3. Guven, MA, Coskun, A, Ertas, IE, et al. Association of maternal serum CRP, IL-6, TNF-alpha, homocysteine, folic acid and vitamin B12 levels with the severity of preeclampsia and fetal birth weight. Hypertens Pregnancy. 2009; 28, 190–200.Google Scholar
4. Tjoa, ML, van Vugt, JMG, Go, ATJJ, et al. Elevated C-reactive protein levels during first trimester of pregnancy are indicative of preeclampsia and intrauterine growth restriction. J Reprod Immunol. 2003; 59, 29–37.Google Scholar
5. Akum, A, Kuoh, AJ, Minang, JT, et al. The effect of maternal, umbilical cord and placental malaria parasitaemia on the birthweight of newborns from South‐western Cameroon. Acta Paediatr. 2005; 94, 917–923.Google Scholar
6. Blas, MM, Canchihuaman, FA, Alva, IE, Hawes, SE. Pregnancy outcomes in women infected with Chlamydia trachomatis: a population-based cohort study in Washington State. Sex Trans Infect. 2007; 83, 314–318.CrossRefGoogle ScholarPubMed
7. R, Romero, Moshe, M. Infection and preterm labor. Clin Obstetr Gynecol. 1988; 31, 553–584.Google Scholar
8. Bullen, BL, Jones, NM, Holzman, CB, et al. C-reactive protein and preterm delivery: clues from placental findings and maternal weight. Reprod Sci. 2013; 20, 715–722.CrossRefGoogle ScholarPubMed
9. Pitiphat, W, Gillman, MW, Joshipura, KJ, et al. Plasma C-reactive protein in early pregnancy and preterm delivery. Am J Epidemiol. 2005; 162, 1108–1113.Google Scholar
10. Hwang, HS, Kwon, JY, Kim, MA, Park, YW, Kim, YH. Maternal serum highly sensitive C-reactive protein in normal pregnancy and pre-eclampsia. Int J Gynaecol Obstet. 2007; 98, 105–109.Google Scholar
11. Sacks, GP, Seyani, L, Lavery, S, Trew, G. Maternal C-reactive protein levels are raised at 4 weeks gestation. Human Reprod. 2004; 19, 1025–1030.Google Scholar
12. Teran, E, Escudero, C, Calle, A. C-reactive protein during normal pregnancy and preeclampsia. Int J Gynaecol Obstet. 2005; 89, 299–300.CrossRefGoogle ScholarPubMed
13. Kuzawa, CW, Adair, LS, Borja, J, McDade, TW. C-reactive protein by pregnancy and lactational status among Filipino young adult women. Am J Human Biol. 2013; 25, 131–134.Google Scholar
14. 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, 353–357.CrossRefGoogle ScholarPubMed
15. Redman, C, Sacks, GP, Sargeant, IL. Pregnancy: an excessive maternal inflammatory response to pregnancy. Am J Obstet Gynecol. 1999; 180, 499–506.CrossRefGoogle ScholarPubMed
16. Han, YS, Ha, EH, Park, HS, Kim, YJ, Lee, SS. Relationships between pregnancy outcomes, biochemical markers and pre-pregnancy body mass index. Int J Obes. 2011; 35, 570–577.Google Scholar
17. Lowe, LP, Metzger, BE, Lowe, WL Jr., et al. Inflammatory mediators and glucose in pregnancy: results from a subset of the Hyperglycemia and Adverse Pregnancy Outcome (HAPO) Study. J Clin Endocrinol Metabol. 2010; 95, 5427–5434.Google Scholar
18. Sen, S, Rifas-Shiman, SL, Shivappa, N, et al. Dietary inflammatory potential during pregnancy is associated with lower fetal growth and breastfeeding failure: results from project viva. J Nutr. 2016; 146, 728–736.Google Scholar
19. Gershov, D, Kim, S, Brot, N, Elkon, KB. C-reactive protein binds to apoptotic cells, protects the cells from assembly of the terminal complement components, and sustains an antiinflammatory innate immune response: implications for systemic autoimmunity. J Exp Med. 2000; 192, 1353–1364.CrossRefGoogle ScholarPubMed
20. Lam, C, Lim, KH, Karumanchi, SA. Circulating angiogenic factors in the pathogenesis and prediction of preeclampsia. Hypertension. 2005; 46, 1077–1085.CrossRefGoogle ScholarPubMed
21. Ernst, GD, de Jonge, LL, Hofman, A, et al. C-reactive protein levels in early pregnancy, fetal growth patterns, and the risk for neonatal complications: the Generation R Study. Am J Obstet Gynecol. 2011; 205, 132.e1–132.e12.CrossRefGoogle ScholarPubMed
22. Ali, Z, Bokhari, FA, Zaki, S, et al. Correlation of CRP levels in third trimester with fetal birth weight in preeclamptic and normotensive pregnant women. J Coll Phys Surg Pak. 2015; 25, 111–114.Google Scholar
23. Redman, CWG. Preeclampsia and the systemic inflammatory response. Sem Nephrol. 2004; 24, 565–570.CrossRefGoogle ScholarPubMed
24. Ertas, IE, Kahyaoglu, S, Yilmaz, B, et al. Association of maternal serum high sensitive C-reactive protein level with body mass index and severity of pre-eclampsia at third trimester. J Obstet Gynaecol Res. 2010; 36, 970–977.Google Scholar
25. Malek, A, Bersinger, NA, Di Santo, S, et al. C-reactive protein production in term human placental tissue. Placenta. 2006; 27, 619–625.Google Scholar
26. 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, 583–587.CrossRefGoogle ScholarPubMed
27. deRosset, L, Strutz, KL. Developmental origins of chronic inflammation: a review of the relationship between birth weight and C-reactive protein. Ann Epidemiol. 2015; 25, 539–543.Google Scholar
28. McDade, TW. Early environments and the ecology of inflammation. Proc Natl Acad Sci. 2012; 109(Suppl. 2), 17281–17288.Google Scholar
29. McDade, TW, Rutherford, JN, Adair, L, Kuzawa, C. Population differences in associations between C-reactive protein concentration and adiposity: comparison of young adults in the Philippines and the United States. Am J Clin Nutr. 2009; 89, 1237–1245.CrossRefGoogle ScholarPubMed
30. Skilton, MR, Viikari, JSA, Juonala, M, et al. Fetal growth and preterm birth influence cardiovascular risk factors and arterial health in young adults. Arterioscler Thromb Vasc Biol. 2011; 31, 2975–2981.CrossRefGoogle ScholarPubMed
31. Tzoulaki, I, Jarvelin, MR, Hartikainen, AL, et al. Size at birth, weight gain over the life course, and low-grade inflammation in young adulthood: northern Finland 1966 Birth Cohort study. Eur Heart J. 2008; 29, 1049–1056.Google Scholar
32. Adair, LS, Popkin, BM, Akin, JS, et al. Cohort profile: The Cebu Longitudinal Health and Nutrition Survey. Int J Epidemiol. 2011; 40, 619–625.Google Scholar
33. Lohman, TG, Roche, AF, Martorell, R. Anthropometric Standardization Reference Manual. 1988. Human Kinetics Books: Champaign, IL.Google Scholar
34. McDade, TW, Burhop, J, Dohnal, J. High-sensitivity enzyme immunoassay for C-reactive protein in dried blood spots. Clin Chem. 2004; 50, 652–654.CrossRefGoogle ScholarPubMed
35. McDade, TW. Development and validation of assay protocols for use with dried blood spot samples. Am J Hum Biol. 2014; 26, 1–9.Google Scholar
36. de Oliveira, LC, Franco-Sena, AB, Farias, DR, Rebelo, F, Kac, G. Maternal C-reactive protein concentrations during pregnancy and birth weight in a prospective cohort in Rio de Janeiro, Brazil. J Matern Fetal Neonatal Med. 2016; 1–8 [epub ahead of print].Google Scholar
37. Widdowson, EM, McCance, RA. A review: new thoughts on growth. Pediatr Res. 1975; 9, 154–156.Google Scholar
38. Kuzawa, CW. Adipose tissue in human infancy and childhood: an evolutionary perspective. Am J Phys Anthropol. 1998; 27, 177–209.Google Scholar
39. Haggarty, P. Fatty acid supply to the human fetus. Annu Rev Nutr. 2010; 30, 237–255.Google Scholar
40. de Onis, M, Onyango, AW, Borghi, E, Garza, C, Yang, H. Comparison of the World Health Organization (WHO) Child Growth Standards and the National Center for Health Statistics/WHO international growth reference: implications for child health programmes. Public Health Nutr. 2006; 9, 942–947.Google Scholar
41. Wladimiroff, JW, Tonge, HM, Stewart, PA, Reuss, A. Severe intrauterine growth retardation; assessment of its origin from fetal arterial flow velocity waveforms. Eur J Obstet Gynecol Reprod Biol. 1986; 22, 23–28.CrossRefGoogle ScholarPubMed
42. Baschat, AA. Fetal responses to placental insufficiency: an update. BJOG. 2004; 111, 1031–1041.CrossRefGoogle ScholarPubMed
43. 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 R Soc B. 2010; 277, 1129–1137.Google Scholar
44. Thayer, ZM, Feranil, AB, Kuzawa, CW. Maternal cortisol disproportionately impacts fetal growth in male offspring: evidence from the Philippines. Am J Human Biol. 2012; 24, 1–4.Google Scholar
45. Lee, J, Fried, R, Thayer, Z, Kuzawa, CW. Preterm delivery as a predictor of diurnal cortisol profiles in adulthood: evidence from Cebu, Philippines. Am J Human Biol. 2014; 26, 598–602.Google Scholar
46. Benyshek, DC. The “early life” origins of obesity-related health disorders: new discoveries regarding the intergenerational transmission of developmentally programmed traits in the global cardiometabolic health crisis. Am J Phys Anthropol. 2013; 31, 79–93.CrossRefGoogle Scholar
47. Kuzawa, CW, Sweet, E. Epigenetics and the embodiment of race: developmental origins of US racial disparities in cardiovascular health. Am J Human Biol. 2008; 21, 2–15.Google Scholar