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Evidence for maternal diet-mediated effects on the offspring microbiome and immunity: implications for public health initiatives

Abstract

Diets rich in saturated fats have become a staple globally. Fifty percent of women of childbearing age in the United States are obese or overweight, with diet being a significant contributor. There is increasing evidence of the impact of maternal high-fat diet on the offspring microbiome. Alterations of the neonatal microbiome have been shown to be associated with multiple morbidities, including the development of necrotizing enterocolitis, atopy, asthma, metabolic dysfunction, and hypertension among others. This review provides an overview of the recent studies and mechanisms being examined on how maternal diet can alter the immune response and microbiome in offspring and the implications for directed public health initiatives for women of childbearing age.

Impact

  • Maternal diet is important in shaping the offspring microbiome and neonatal immune system.

  • Reviews the current literature in the field and suggests potential mechanisms and areas of research to be targeted.

  • Highlights the current scope of our knowledge of ideal nutrition during pregnancy and consideration for enhanced public health initiatives to promote well-being of the future generation.

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Fig. 1: Potential mechanisms for maternal diet-mediated effects on the fetus affecting postnatal colonization and immunity.
Fig. 2: Macronutrient consumption in women of child bearing age and recommended ranges in USA.

References

  1. 1.

    Obanewa, O. & Newell, M. L. Maternal nutritional status during pregnancy and infant immune response to routine childhood vaccinations. Future Virol. 12, 525–536 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  2. 2.

    Belkaid, Y. & Hand, T. W. Role of the microbiota in immunity and inflammation. Cell 157, 121–141 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  3. 3.

    Milani, C. et al. The first microbial colonizers of the human gut: composition, activities, and health implications of the infant gut microbiota. Microbiol. Mol. Biol. Rev. 81, https://doi.org/10.1128/MMBR.00036-17 (2017).

  4. 4.

    Kominiarek, M. A. & Rajan, P. Nutrition recommendations in pregnancy and lactation. Med. Clin. North Am. 100, 1199–1215 (2016).

    PubMed  PubMed Central  Google Scholar 

  5. 5.

    Chu, D. M. et al. The early infant gut microbiome varies in association with a maternal high-fat diet. Genome Med. 8, 77 (2016).

    PubMed  PubMed Central  Google Scholar 

  6. 6.

    Lundgren, S. N. et al. Maternal diet during pregnancy is related with the infant stool microbiome in a delivery mode-dependent manner. Microbiome 6, 109 (2018).

    PubMed  PubMed Central  Google Scholar 

  7. 7.

    Maher, S. E. et al. The association between the maternal diet and the maternal and infant gut microbiome: a systematic review. Br. J. Nutr. 1–29, https://doi.org/10.1017/S0007114520000847 (2020).

  8. 8.

    Dominguez-Bello, M. G. et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc. Natl Acad. Sci. USA 107, 11971–11975 (2010).

    PubMed  Google Scholar 

  9. 9.

    Backhed, F. et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17, 690–703 (2015).

    PubMed  Google Scholar 

  10. 10.

    Bokulich, N. A. et al. Antibiotics, birth mode, and diet shape microbiome maturation during early life. Sci. Transl. Med. 8, 343ra382 (2016).

    Google Scholar 

  11. 11.

    Ferretti, P. et al. Mother-to-infant microbial transmission from different body sites shapes the developing infant gut microbiome. Cell Host Microbe 24, 133–145.e135 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. 12.

    Korpela, K. et al. Selective maternal seeding and environment shape the human gut microbiome. Genome Res. 28, 561–568 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. 13.

    Iwasaki, A. & Medzhitov, R. Control of adaptive immunity by the innate immune system. Nat. Immunol. 16, 343–353 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. 14.

    Torres, J. et al. Infants born to mothers with IBD present with altered gut microbiome that transfers abnormalities of the adaptive immune system to germ-free mice. Gut 69, 42–51 (2020).

    CAS  PubMed  Google Scholar 

  15. 15.

    Sausenthaler, S. et al. Maternal diet during pregnancy in relation to eczema and allergic sensitization in the offspring at 2 y of age. Am. J. Clin. Nutr. 85, 530–537 (2007).

    CAS  PubMed  Google Scholar 

  16. 16.

    Calvani, M. et al. Consumption of fish, butter and margarine during pregnancy and development of allergic sensitizations in the offspring: role of maternal atopy. Pediatr. Allergy Immunol. 17, 94–102 (2006).

    PubMed  Google Scholar 

  17. 17.

    Romieu, I. et al. Maternal fish intake during pregnancy and atopy and asthma in infancy. Clin. Exp. Allergy. 37, 518–525 (2007).

    CAS  PubMed  Google Scholar 

  18. 18.

    Vuillermin, P. J. et al. The maternal microbiome during pregnancy and allergic disease in the offspring. Semin. Immunopathol. 39, 669–675 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. 19.

    Bianchi, M. et al. Maternal intake of n-3 polyunsaturated fatty acids during pregnancy is associated with differential methylation profiles in cord blood white cells. Front. Genet. 10, 1050 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Miyake, Y., Sasaki, S., Tanaka, K., Ohfuji, S. & Hirota, Y. Maternal fat consumption during pregnancy and risk of wheeze and eczema in Japanese infants aged 16-24 months: the Osaka Maternal and Child Health Study. Thorax 64, 815–821 (2009).

    CAS  PubMed  Google Scholar 

  21. 21.

    Ma, J. et al. High-fat maternal diet during pregnancy persistently alters the offspring microbiome in a primate model. Nat. Commun. 5, 3889 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Babu, S. T. et al. Maternal high-fat diet results in microbiota-dependent expansion of ILC3s in mice offspring. JCI insight 3, https://doi.org/10.1172/jci.insight.99223 (2018).

  23. 23.

    Myles, I. A. et al. Parental dietary fat intake alters offspring microbiome and immunity. J. Immunol. 191, 3200–3209 (2013).

    CAS  PubMed  Google Scholar 

  24. 24.

    Bhagavata Srinivasan, S. P., Raipuria, M., Bahari, H., Kaakoush, N. O. & Morris, M. J. Impacts of diet and exercise on maternal gut microbiota are transferred to offspring. Front. Endocrinol. 9, 716 (2018).

    Google Scholar 

  25. 25.

    Xie, R. et al. Maternal high fat diet alters gut microbiota of offspring and exacerbates DSS-induced colitis in adulthood. Front. Immunol. 9, 2608 (2018).

    PubMed  PubMed Central  Google Scholar 

  26. 26.

    Li, Y. et al. Maternal dietary fiber composition during gestation induces changes in offspring antioxidative capacity, inflammatory response, and gut microbiota in a sow model. Int. J. Mol. Sci. 21, https://doi.org/10.3390/ijms21010031 (2019).

  27. 27.

    Cheng, C. et al. Maternal soluble fiber diet during pregnancy changes the intestinal microbiota, improves growth performance, and reduces intestinal permeability in piglets. Appl. Environ. Microbiol. 84, https://doi.org/10.1128/AEM.01047-18 (2018).

  28. 28.

    Goncalves, P., Araujo, J. R. & Di Santo, J. P. A cross-talk between microbiota-derived short-chain fatty acids and the host mucosal immune system regulates intestinal homeostasis and inflammatory bowel disease. Inflamm. Bowel Dis. 24, 558–572 (2018).

    PubMed  Google Scholar 

  29. 29.

    Needell, J. C. et al. Maternal treatment with short-chain fatty acids modulates the intestinal microbiota and immunity and ameliorates type 1 diabetes in the offspring. PLoS ONE 12, e0183786 (2017).

    PubMed  PubMed Central  Google Scholar 

  30. 30.

    Round, J. L. & Mazmanian, S. K. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9, 313–323 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. 31.

    Gomez de Aguero, M. et al. The maternal microbiota drives early postnatal innate immune development. Science 351, 1296–1302 (2016).

    PubMed  Google Scholar 

  32. 32.

    David, L. A. et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559–563 (2014).

    CAS  PubMed  Google Scholar 

  33. 33.

    Singh, R. K. et al. Influence of diet on the gut microbiome and implications for human health. J. Transl. Med. 15, 73 (2017).

    PubMed  PubMed Central  Google Scholar 

  34. 34.

    Srugo, S. A., Bloise, E., Nguyen, T. T. N. & Connor, K. L. Impact of maternal malnutrition on gut barrier defense: implications for pregnancy health and fetal development. Nutrients 11, https://doi.org/10.3390/nu11061375 (2019).

  35. 35.

    Keleher, M. R. et al. Maternal high-fat diet associated with altered gene expression, DNA methylation, and obesity risk in mouse offspring. PLoS ONE 13, e0192606 (2018).

    PubMed  PubMed Central  Google Scholar 

  36. 36.

    Thorburn, A. N. et al. Evidence that asthma is a developmental origin disease influenced by maternal diet and bacterial metabolites. Nat. Commun. 6, 7320 (2015).

    CAS  PubMed  Google Scholar 

  37. 37.

    Hansen, C. H. et al. A maternal gluten-free diet reduces inflammation and diabetes incidence in the offspring of NOD mice. Diabetes 63, 2821–2832 (2014).

    CAS  PubMed  Google Scholar 

  38. 38.

    Perez-Munoz, M. E., Arrieta, M. C., Ramer-Tait, A. E. & Walter, J. A critical assessment of the “sterile womb” and “in utero colonization” hypotheses: implications for research on the pioneer infant microbiome. Microbiome 5, 48 (2017).

    PubMed  PubMed Central  Google Scholar 

  39. 39.

    de Goffau, M. C. et al. Human placenta has no microbiome but can contain potential pathogens. Nature 572, 329–334 (2019).

    PubMed  PubMed Central  Google Scholar 

  40. 40.

    Aagaard, K. et al. The placenta harbors a unique microbiome. Sci. Transl. Med. 6, 237ra265 (2014).

    Google Scholar 

  41. 41.

    Theis, K. R. et al. No consistent evidence for microbiota in murine placental and fetal tissues. mSphere 5, https://doi.org/10.1128/mSphere.00933-19 (2020).

  42. 42.

    Stinson, L. F., Boyce, M. C., Payne, M. S. & Keelan, J. A. The not-so-sterile womb: evidence that the human fetus is exposed to bacteria prior to birth. Front. Microbiol. 10, 1124 (2019).

    PubMed  PubMed Central  Google Scholar 

  43. 43.

    Rackaityte, E. et al. Viable bacterial colonization is highly limited in the human intestine in utero. Nat. Med. 26, 599–607 (2020).

    CAS  PubMed  Google Scholar 

  44. 44.

    Rautava, S., Collado, M. C., Salminen, S. & Isolauri, E. Probiotics modulate host-microbe interaction in the placenta and fetal gut: a randomized, double-blind, placebo-controlled trial. Neonatology 102, 178–184 (2012).

    PubMed  Google Scholar 

  45. 45.

    Drozdowski, L. & Thomson, A. B. Intestinal hormones and growth factors: effects on the small intestine. World J. Gastroenterol. 15, 385–406 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. 46.

    Dasgupta, S. & Jain, S. K. Protective effects of amniotic fluid in the setting of necrotizing enterocolitis. Pediatr. Res. 82, 584–595 (2017).

    PubMed  Google Scholar 

  47. 47.

    Vidya, M. K. et al. Toll-like receptors: significance, ligands, signaling pathways, and functions in mammals. Int. Rev. Immunol. 37, 20–36 (2018).

    CAS  PubMed  Google Scholar 

  48. 48.

    Hug, H., Mohajeri, M. H. & La Fata, G. Toll-like receptors: regulators of the immune response in the human gut. Nutrients 10, https://doi.org/10.3390/nu10020203 (2018).

  49. 49.

    Shibata, T. et al. Toll-like receptors as a target of food-derived anti-inflammatory compounds. J. Biol. Chem. 289, 32757–32772 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  50. 50.

    Palmas, F. et al. The choice of amniotic fluid in metabolomics for the monitoring of fetus health. Expert Rev. Mol. Diagn. 16, 473–486 (2016).

    CAS  PubMed  Google Scholar 

  51. 51.

    Schwarzer, M. et al. Diet matters: endotoxin in the diet impacts the level of allergic sensitization in germ-free mice. PLoS ONE 12, e0167786 (2017).

    PubMed  PubMed Central  Google Scholar 

  52. 52.

    Nakajima, A. et al. Impact of maternal dietary gut microbial metabolites on an offspring’s systemic immune response in mouse models. Biosci. Microbiota Food Health 39, 33–38 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  53. 53.

    American Society for Reproductive, Medicine, American College of Obstetricians and Gynecologists' Committee on Gynecologic Practice. Prepregnancy counseling: Committee Opinion No. 762. Fertil. Steril. 111, 32–42 (2019).

  54. 54.

    Mousa, A., Naqash, A. & Lim, S. Macronutrient and micronutrient intake during pregnancy: an overview of recent evidence. Nutrients 11, https://doi.org/10.3390/nu11020443 (2019).

  55. 55.

    Wesolowski, S. R. et al. Switching obese mothers to a healthy diet improves fetal hypoxemia, hepatic metabolites, and lipotoxicity in non-human primates. Mol. Metab. 18, 25–41 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by NIH NIDDK R01 DK121975 01A1.

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Correspondence to Julie Mirpuri.

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Mirpuri, J. Evidence for maternal diet-mediated effects on the offspring microbiome and immunity: implications for public health initiatives. Pediatr Res 89, 301–306 (2021). https://doi.org/10.1038/s41390-020-01121-x

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