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DOHaD at the intersection of maternal immune activation and maternal metabolic stress: a scoping review

Published online by Cambridge University Press:  15 February 2017

J. A. Goldstein Open the ORCID record for J. A. Goldstein [Opens in a new window] ,
S. A. Norris  and
D. M. Aronoff
J. A. Goldstein
Affiliation:
Department of Pathology, Microbiology, and Immunology, Vanderbilt UniversityMedical Center, Nashville, Tennessee, United States of America
S. A. Norris
Affiliation:
Medical Research Council Developmental Pathways for Health Research Unit, University of the Witwatersrand, Johannesburg, South Africa
D. M. Aronoff*
Affiliation:
Department of Pathology, Microbiology, and Immunology, Vanderbilt UniversityMedical Center, Nashville, Tennessee, United States of America Department of Medicine, Vanderbilt UniversityMedical Center, Nashville, Tennessee, United States of America
*
*Address for correspondence: D. M. Aronoff, MD, 1161 21st Avenue South, A-2200 Medical Center North, Nashville, TN 37232-2582, USA. (Email: d.aronoff@vanderbilt.edu)
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Abstract

The prenatal environment is now recognized as a key driver of non-communicable disease risk later in life. Within the developmental origins of health and disease (DOHaD) paradigm, studies are increasingly identifying links between maternal morbidity during pregnancy and disease later in life for offspring. Nutrient restriction, metabolic disorders during gestation, such as diabetes or obesity, and maternal immune activation provoked by infection have been linked to adverse health outcomes for offspring later in life. These factors frequently co-occur, but the potential for compounding effects of multiple morbidities on DOHaD-related outcomes has not received adequate attention. This is of particular importance in low- or middle-income countries (LMICs), which have ongoing high rates of infectious diseases and are now experiencing transitions from undernutrition to excess adiposity. The purpose of this scoping review is to summarize studies examining the effect and interaction of co-occurring metabolic or nutritional stressors and infectious diseases during gestation on DOHaD-related health outcomes. We identified nine studies in humans – four performed in the United States and five in LMICs. The most common outcome, also in seven of nine studies, was premature birth or low birth weight. We identified nine animal studies, six in mice, two in rats and one in sheep. The interaction between metabolic/nutritional exposures and infectious exposures had varying effects including synergism, inhibition and independent actions. No human studies were specifically designed to assess the interaction of metabolic/nutritional exposures and infectious diseases. Future studies of neonatal outcomes should measure these exposures and explicitly examine their concerted effect.

Keywords

child growth and healthobesityoutcome/systempregnancy
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 8 , Issue 3 , June 2017 , pp. 273 - 283
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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. Eriksson, JG. Developmental Origins of Health and Disease – from a small body size at birth to epigenetics. Ann Med. 2016; 48, 1–12. https://doi.org/10.1080/07853890.2016.2016.1193786.CrossRefGoogle ScholarPubMed
2. Chavatte-Palmer, P, Tarrade, A, Rousseau-Ralliard, D. Diet before and during pregnancy and offspring health: the importance of animal models and what can be learned from them. Int J Environ Res Public Health. 2016; 13, 586.Google Scholar
3. Tarrade, A, Panchenko, P, Junien, C, Gabory, A. Placental contribution to nutritional programming of health and diseases: epigenetics and sexual dimorphism. J Exp Biol. 2015; 218, 50–58.CrossRefGoogle ScholarPubMed
4. Brenseke, B, Prater, MR, Bahamonde, J, Gutierrez, JC. Current thoughts on maternal nutrition and fetal programming of the metabolic syndrome. J Pregnancy. 2013; 2013, 368461.Google Scholar
5. Xiang, AH, Wang, X, Martinez, MP, et al. Association of maternal diabetes with autism in offspring. JAMA. 2015; 313, 1425–1434.Google Scholar
6. Tomar, AS, Tallapragada, DS, Nongmaithem, SS, et al. Intrauterine programming of diabetes and adiposity. Curr Obes Rep. 2015; 4, 418–428.CrossRefGoogle ScholarPubMed
7. Yan, J, Yang, H. Gestational diabetes mellitus, programing and epigenetics. J Matern Fetal Neonatal Med. 2014; 27, 1266–1269.CrossRefGoogle ScholarPubMed
8. Bezek, S, Ujhazy, E, Mach, M, Navarova, J, Dubovicky, M. Developmental origin of chronic diseases: toxicological implication. Interdiscip Toxicol. 2008; 1, 29–31.Google Scholar
9. Howerton, CL, Bale, TL. Prenatal programing: at the intersection of maternal stress and immune activation. Horm Behav. 2012; 62, 237–242.Google Scholar
10. Monk, C, Georgieff, MK, Osterholm, EA. Research review: maternal prenatal distress and poor nutrition – mutually influencing risk factors affecting infant neurocognitive development. J Child Psychol Psychiatry. 2013; 54, 115–130.Google Scholar
11. Sutton, EF, Gilmore, LA, Dunger, DB, et al. Developmental programming: state-of-the-science and future directions – summary from a Pennington Biomedical symposium. Obesity (Silver Spring). 2016; 24, 1018–1026.Google Scholar
12. Bobetsis, YA, Barros, SP, Lin, DM, et al. Bacterial infection promotes DNA hypermethylation. J Dental Res. 2007; 86, 169–174.Google Scholar
13. Adams Waldorf, KM, McAdams, RM. Influence of infection during pregnancy on fetal development. Reproduction. 2013; 146, R151–R162.CrossRefGoogle ScholarPubMed
14. Zager, A, Peron, JP, Mennecier, G, et al. Maternal immune activation in late gestation increases neuroinflammation and aggravates experimental autoimmune encephalomyelitis in the offspring. Brain Behav Immun. 2015; 43, 159–171.Google Scholar
15. Popkin, BM, Adair, LS, Ng, SW. Global nutrition transition and the pandemic of obesity in developing countries. Nutr Rev. 2012; 70, 3–21.CrossRefGoogle ScholarPubMed
16. Guariguata, L, Linnenkamp, U, Beagley, J, Whiting, DR, Cho, NH. Global estimates of the prevalence of hyperglycaemia in pregnancy. Diabetes Res Clin Pract. 2014; 103, 176–185.Google Scholar
17. Arksey, H, O’Malley, L. Scoping studies: towards a methodological framework. Int J Soc Res Methodol. 2005; 8, 19–32.Google Scholar
18. Baer, RJ, Chambers, CD, Jones, KL, et al. Maternal factors associated with the occurrence of gastroschisis. Am J Med Genet A. 2015; 167, 1534–1541.CrossRefGoogle ScholarPubMed
19. Botto, LD, Lynberg, MC, Erickson, JD. Congenital heart defects, maternal febrile illness, and multivitamin use: a population-based study. Epidemiology. 2001; 12, 485–490.CrossRefGoogle ScholarPubMed
20. Doyle, TJ, Goodin, K, Hamilton, JJ. Maternal and neonatal outcomes among pregnant women with 2009 pandemic influenza A(H1N1) illness in Florida, 2009–2010: a population-based cohort study. PLoS One. 2013; 8, e79040.CrossRefGoogle ScholarPubMed
21. Friis, H, Gomo, E, Nyazema, N, et al. Effect of multimicronutrient supplementation on gestational length and birth size: a randomized, placebo-controlled, double-blind effectiveness trial in Zimbabwe. Am J Clin Nutr. 2004; 80, 178–184.Google Scholar
22. Ndirangu, J, Newell, ML, Bland, RM, Thorne, C. Maternal HIV infection associated with small-for-gestational age infants but not preterm births: evidence from rural South Africa. Hum Reprod. 2012; 27, 1846–1856.Google Scholar
23. Njim, T, Atashili, J, Mbu, R, Choukem, SP. Low birth weight in a sub-urban area of Cameroon: an analysis of the clinical cut-off, incidence, predictors and complications. BMC Pregnancy Childbirth. 2015; 15, 288.Google Scholar
24. Scholl, TO, Sowers, M, Chen, X, Lenders, C. Maternal glucose concentration influences fetal growth, gestation, and pregnancy complications. Am J Epidemiol. 2001; 154, 514–520.CrossRefGoogle ScholarPubMed
25. Tellapragada, C, Eshwara, VK, Bhat, P, et al. Risk factors for preterm birth and low birth weight among pregnant indian women: a hospital-based prospective study. J Prev Med Public Health. 2016; 49, 165–175.Google Scholar
26. Vogel, JP, Lee, AC, Souza, JP. Maternal morbidity and preterm birth in 22 low- and middle-income countries: a secondary analysis of the WHO Global Survey dataset. BMC Pregnancy Childbirth. 2014; 14, 56.Google Scholar
27. Batty, GD, Shipley, MJ, Gunnell, D, et al. Height, wealth, and health: an overview with new data from three longitudinal studies. Econ Hum Biol. 2009; 7, 137–152.Google Scholar
28. Chen, YH, Zhao, M, Chen, X, et al. Zinc supplementation during pregnancy protects against lipopolysaccharide-induced fetal growth restriction and demise through its anti-inflammatory effect. J Immunol. 2012; 189, 454–463.Google Scholar
29. Punareewattana, K, Sharova, LV, Li, W, Ward, DL, Holladay, SD. Reduced birth defects caused by maternal immune stimulation may involve increased expression of growth promoting genes and cytokine GM-CSF in the spleen of diabetic ICR mice. Int Immunopharmacol. 2003; 3, 1639–1655.Google Scholar
30. Odiere, MR, Scott, ME, Weiler, HA, Koski, KG. Protein deficiency and nematode infection during pregnancy and lactation reduce maternal bone mineralization and neonatal linear growth in mice. J Nutr. 2010; 140, 1638–1645.Google Scholar
31. Starr, LM, Koski, KG, Scott, ME. Expression of growth-related genes in the mouse placenta is influenced by interactions between intestinal nematode (Heligmosomoides bakeri) infection and dietary protein deficiency. Int J Parasitol. 2016; 46, 97–104.Google Scholar
32. Starr, LM, Scott, ME, Koski, KG. Protein deficiency and intestinal nematode infection in pregnant mice differentially impact fetal growth through specific stress hormones, growth factors, and cytokines. J Nutr. 2015; 145, 41–50.Google Scholar
33. Coyle, P, Tran, N, Fung, JN, Summers, BL, Rofe, AM. Maternal dietary zinc supplementation prevents aberrant behaviour in an object recognition task in mice offspring exposed to LPS in early pregnancy. Behav Brain Res. 2009; 197, 210–218.Google Scholar
34. Harvey, L, Boksa, P. Do prenatal immune activation and maternal iron deficiency interact to affect neurodevelopment and early behavior in rat offspring? Brain Behav Immun. 2014; 35, 144–154.Google Scholar
35. Harvey, L, Boksa, P. Additive effects of maternal iron deficiency and prenatal immune activation on adult behaviors in rat offspring. Brain Behav Immun. 2014; 40, 27–37.Google Scholar
36. Fisher, RE, Or’Rashid, M, Quinton, M, et al. Maternal supplementation with fishmeal protects against late gestation endotoxin-induced fetal programming of the ovine hypothalamic-pituitary-adrenal axis. J Dev Orig Health Dis. 2014; 5, 206–213.Google Scholar
37. Anderson, EK, Gutierrez, DA, Kennedy, A, Hasty, AH. Weight cycling increases T-cell accumulation in adipose tissue and impairs systemic glucose tolerance. Diabetes. 2013; 62, 3180–3188.Google Scholar
38. Graves, DT, Kayal, RA. Diabetic complications and dysregulated innate immunity. Front Biosci. 2008; 13, 1227–1239.Google Scholar
39. Benjamin, B, Wilson, GN. Registry analysis supports different mechanisms for gastroschisis and omphalocele within shared developmental fields. Am J Med Genet A. 2015; 167a, 2568–2581.Google Scholar
40. Lubinsky, M. Hypothesis: estrogen related thrombosis explains the pathogenesis and epidemiology of gastroschisis. Am J Med Genet A. 2012; 158a, 808–811.Google Scholar
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