Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-22T14:36:43.506Z Has data issue: false hasContentIssue false

Chapter 8 - Developmental Programming and the Microbiome

How the Maternal Environment and Early Life Shape the Infant Gut Microbiome Pathway(s) and Risk of Disease

from Section II - Exposures Driving Long-Term DOHaD Effects

Published online by Cambridge University Press:  01 December 2022

By
Kameron Y. Sugino  and
Jacob E. Friedman
Edited by
Lucilla Poston ,
Keith M. Godfrey ,
Peter D. Gluckman  and
Mark A. Hanson
Lucilla Poston
Affiliation:
King's College London
Keith M. Godfrey
Affiliation:
University of Southampton
Peter D. Gluckman
Affiliation:
University of Auckland
Mark A. Hanson
Affiliation:
University of Southampton
Get access

Summary

Maternal and infant microbiota are an emerging target of investigation and have particular relevance to disease, ranging from obesity and diabetes to many immunological disorders. Infant gut microbiome colonization and growth are influenced by environmental stimuli such as mode of delivery, infant diet (breastmilk), antibiotic exposure and maternal characteristics including obesity, diet and gestational diabetes. Alterations to the normal bacterial colonization and maturation of the infant gut microbiota – notably short chain fatty acid producers in the phylum Firmicutes and lipopolysaccharide-producers of the family Gammaproteobacteria – can lead to substantial differences in host-microbe interactions and altered neonatal immune system memory/development. Remodelling these pathways during early life may hold promise for correcting developmental programming of both innate and adaptive immunity associated with insulin resistance, pre-diabetes, obesity, non-alcoholic fatty liver disease and diseases linked to dysregulated immunity in youth, including Type I diabetes, asthma and allergies.

Type
Chapter
Information
Developmental Origins of Health and Disease , pp. 66 - 74
Publisher: Cambridge University Press
Print publication year: 2022

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Vandenplas, Y., Carnielli, V. P., Ksiazyk, J., Luna, M. S., Migacheva, N., Mosselmans, J. M., Picaud, J. C., Possner, M., Singhal, A., & Wabitsch, M., Factors affecting early-life intestinal microbiota development. Nutrition, 78 (2020) 110812. https://doi.org/10.1016/j.nut.2020.110812.Google Scholar
Moles, L. & Otaegui, D., The impact of diet on microbiota evolution and human health. Is diet an adequate tool for microbiota modulation? Nutrients, 12 (2020) 1654. https://doi.org/10.3390/nu12061654.Google Scholar
Eggesbø, M., Moen, B., Peddada, S., Baird, D., Rugtveit, J., Midtvedt, T., Bushel, P. R., Sekelja, M., & Rudi, K., Development of gut microbiota in infants not exposed to medical interventions. APMIS, 119 (2011) 17–35. https://doi.org/10.1111/j.1600-0463.2010.02688.x.Google Scholar
Kimura, I., Miyamoto, J., Ohue-Kitano, R., Watanabe, K., Yamada, T., Onuki, M., Aoki, R., Isobe, Y., Kashihara, D., Inoue, D., Inaba, A., Takamura, Y., Taira, S., Kumaki, S., Watanabe, M., Ito, M., Nakagawa, F., Irie, J., Kakuta, H., Shinohara, M., Iwatsuki, K., Tsujimoto, G., Ohno, H., Arita, M., Itoh, H., & Hase, K., Maternal gut microbiota in pregnancy influences offspring metabolic phenotype in mice. Science, 367 (2020). https://doi.org/10.1126/science.aaw8429.CrossRefGoogle Scholar
Louis, P. & Flint, H. J., Formation of propionate and butyrate by the human colonic microbiota. Environmental Microbiology, 19 (2017) 29–41. https://doi.org/10.1111/1462-2920.13589.Google Scholar
Ma, J., Prince, A. L., Bader, D., Hu, M., Ganu, R., Baquero, K., Blundell, P., Alan Harris, R., Frias, A. E., Grove, K. L., & Aagaard, K. M., High-fat maternal diet during pregnancy persistently alters the offspring microbiome in a primate model. Nature Communications, 5 (2014) 1–11. https://doi.org/10.1038/ncomms4889.CrossRefGoogle Scholar
Grech, A., C. E. Collins, A. Holmes, R. Lal, K. Duncanson, R. Taylor, & A. Gordon, Maternal exposures and the infant gut microbiome: a systematic review with meta-analysis. Gut Microbes, 13 (2021) 1–30. https://doi.org/10.1080/19490976.2021.1897210.CrossRefGoogle Scholar
de Goffau, M. C., Lager, S., Sovio, U., Gaccioli, F., Cook, E., Peacock, S. J., Parkhill, J., Charnock-Jones, D. S., & Smith, G. C. S., Human placenta has no microbiome but can contain potential pathogens. Nature, (2019). https://doi.org/10.1038/s41586-019-1451-5.Google Scholar
Palmer, C., Bik, E. M., DiGiulio, D. B., Relman, D. A., & Brown, P. O., Development of the human infant intestinal microbiota. PLoS Biology, 5 (2007) 1556–1573. https://doi.org/10.1371/journal.pbio.0050177.Google Scholar
Daele, E. Van, Knol, J., & Belzer, C., Microbial transmission from mother to child: Improving infant intestinal microbiota development by identifying the obstacles. Critical Reviews in Microbiology, 45 (2019) 613–648. https://doi.org/10.1080/1040841X.2019.1680601.Google Scholar
Stewart, C. J., Ajami, N. J., O’Brien, J. L., Hutchinson, D. S., Smith, D. P., Wong, M. C., Ross, M. C., Lloyd, R. E., Doddapaneni, H. V., Metcalf, G. A., Muzny, D., Gibbs, R. A., Vatanen, T., Huttenhower, C., Xavier, R. J., Rewers, M., Hagopian, W., Toppari, J., Ziegler, A. G., She, J. X., Akolkar, B., Lernmark, A., Hyoty, H., Vehik, K., Krischer, J. P., & Petrosino, J. F., Temporal development of the gut microbiome in early childhood from the TEDDY study (Nature Publishing Group, 2018). https://doi.org/10.1038/s41586-018-0617-x.Google Scholar
Mitchell, C., Hogstrom, L., Bryant, A. M., Bergerat, A., Cher, A., Pochan, S., Herman, P., Carrigan, M., Sharp, K., Huttenhower, C., Lander, E. S., Vlamakis, H., Xavier, R. J., & Yassour, M., Delivery mode impacts newborn gut colonization efficiency. bioRxiv, (2020) 2020.01.29.919993. https://doi.org/10.1101/2020.01.29.919993.Google Scholar
Mesa, M. D., Loureiro, B., Iglesia, I., Gonzalez, S. F., Olivé, E. L., Algar, O. G., Solana, M. J., Perez, M. J. C., Sainz, T., Martinez, L., Escuder-Vieco, D., Parra-Llorca, A., Sánchez-Campillo, M., Martinez, G. R., Roig, D. G., Gruz, M. P., Andreu-Fernández, V., Clotet, J., Sailer, S., Iglesias-Platas, I., López-Herce, J., Aras, R., Pallás-Alonso, C., de Pipaon, M. S., Vento, M., Gormaz, M., Daza, E. L., Calvo, C., & Cabañas, F., The evolving microbiome from pregnancy to early infancy: A comprehensive review. Nutrients, 12 (2020). https://doi.org/10.3390/nu12010133.Google Scholar
Enav, H., F. Bäckhed, & R. E. Ley, The developing infant gut microbiome: A strain-level view. Cell Host & Microbe, 30 (2022) 627–638. https://doi.org/10.1016/J.CHOM.2022.04.009.Google Scholar
Ho, N. T., Li, F., Lee-Sarwar, K. A., Tun, H. M., Brown, B. P., Pannaraj, P. S., Bender, J. M., Azad, M. B., Thompson, A. L., Weiss, S. T., Azcarate-Peril, M. A., Litonjua, A. A., Kozyrskyj, A. L., Jaspan, H. B., Aldrovandi, G. M., & Kuhn, L., Meta-analysis of effects of exclusive breastfeeding on infant gut microbiota across populations. Nature Communications, 9 (2018). https://doi.org/10.1038/s41467-018-06473-x.Google Scholar
Lagström, H., Rautava, S., Ollila, H., Kaljonen, A., Turta, O., Mäkelä, J., Yonemitsu, C., Gupta, J., & Bode, L., Associations between human milk oligosaccharides and growth in infancy and early childhood. The American Journal of Clinical Nutrition, (2020). https://doi.org/10.1093/ajcn/nqaa010.CrossRefGoogle Scholar
Korpela, K., Salonen, A., Saxen, H., Nikkonen, A., Peltola, V., Jaakkola, T., de Vos, W., & Kolho, K. L., Antibiotics in early life associate with specific gut microbiota signatures in a prospective longitudinal infant cohort. Pediatric Research, (2020). https://doi.org/10.1038/s41390-020-0761-5.Google Scholar
Zeissig, S. & Blumberg, R. S., Life at the beginning: Perturbation of the microbiota by antibiotics in early life and its role in health and disease. Nature Immunology, 15 (2014) 307–310. https://doi.org/10.1038/ni.2847.Google Scholar
Vitetta, L., Vitetta, G., & Hall, S., Immunological tolerance and function: Associations between intestinal bacteria, probiotics, prebiotics, and phages. Frontiers in Immunology, 9 (2018). https://doi.org/10.3389/fimmu.2018.02240.Google Scholar
Azad, M. B., Konya, T., Persaud, R. R., Guttman, D. S., Chari, R. S., Field, C. J., Sears, M. R., Mandhane, P. J., Turvey, S. E., Subbarao, P., Becker, A. B., Scott, J. A., & Kozyrskyj, A. L., Impact of maternal intrapartum antibiotics, method of birth and breastfeeding on gut microbiota during the first year of life: A prospective cohort study. BJOG: An International Journal of Obstetrics and Gynaecology, 123 (2016) 983–993. https://doi.org/10.1111/1471-0528.13601.Google Scholar
Coker, M. O., Hoen, A. G., Dade, E., Lundgren, S., Li, Z., Wong, A. D., Zens, M. S., Palys, T. J., Morrison, H. G., Sogin, M. L., Baker, E. R., Karagas, M. R., & Madan, J. C., Specific class of intrapartum antibiotics relates to maturation of the infant gut microbiota: A prospective cohort study. BJOG: An International Journal of Obstetrics and Gynaecology, 127 (2020) 217–227. https://doi.org/10.1111/1471-0528.15799.Google Scholar
Ledder, O., Antibiotics in inflammatory bowel diseases: Do we know what we’re doing? Translational Pediatrics, 8 (2019) 42–55. https://doi.org/10.21037/tp.2018.11.02.Google Scholar
Dedrick, S., Sundaresh, B., Huang, Q., Brady, C., Yoo, T., Cronin, C., Rudnicki, C., Flood, M., Momeni, B., Ludvigsson, J., & Altindis, E., The role of gut microbiota and environmental factors in Type 1 diabetes pathogenesis. Frontiers in Endocrinology, 11 (2020). https://doi.org/10.3389/fendo.2020.00078.Google Scholar
Ridaura, V. K., Faith, J. J., Rey, F. E., Cheng, J., Duncan, A. E., Kau, A. L., Griffin, N. W., Lombard, V., Henrissat, B., Bain, J. R., Muehlbauer, M. J., Ilkayeva, O., Semenkovich, C. F., Funai, K., Hayashi, D. K., Lyle, B. J., Martini, M. C., Ursell, L. K., Clemente, J. C., Treuren, W. Van, Walters, W. A., Knight, R., Newgard, C. B., Heath, A. C., & Gordon, J. I., Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science, 341 (2013). https://doi.org/10.1126/science.1241214.Google Scholar
Soderborg, T. K., Clark, S. E., Mulligan, C. E., Janssen, R. C., Babcock, L., Ir, D., Lemas, D. J., Johnson, L. K., Weir, T., Lenz, L. L., Frank, D. N., Hernandez, T. L., Kuhn, K. A., D’Alessandro, A., Barbour, L. A., Kasmi, K. C. El, & Friedman, J. E., The gut microbiota in infants of obese mothers increases inflammation and susceptibility to NAFLD. Nature Communications, 9 (2018). https://doi.org/10.1038/s41467-018-06929-0.Google Scholar
Castaner, O., Goday, A., Park, Y.-M., Lee, S.-H., Magkos, F., Shiow, S.-A. T. E., & Schröder, H., The gut microbiome profile in obesity: A systematic review. International Journal of Endocrinology, 2018 (2018). https://doi.org/10.1155/2018/4095789.Google Scholar
Barrea, L., Muscogiuri, G., Annunziata, G., Laudisio, D., Pugliese, G., Salzano, C., Colao, A., & Savastano, S., From gut microbiota dysfunction to obesity: Could short-chain fatty acids stop this dangerous course? Hormones, 18 (2019) 245–250. https://doi.org/10.1007/s42000-019-00100-0.Google Scholar
Kim, K. N., Yao, Y., & Ju, S. Y., Short chain fatty acids and fecal microbiota abundance in humans with obesity: A systematic review and meta-analysis. Nutrients, 11 (2019). https://doi.org/10.3390/nu11102512.Google Scholar
Saad, M. J. A., Santos, A., & Prada, P. O., Linking gut microbiota and inflammation to obesity and insulin resistance. Physiology, 31 (2016) 283–293. https://doi.org/10.1152/physiol.00041.2015.Google Scholar
Differding, M. K., Benjamin-Neelon, S. E., Hoyo, C., Østbye, T., & Mueller, N. T., Timing of complementary feeding is associated with gut microbiota diversity and composition and short chain fatty acid concentrations over the first year of life. BMC Microbiology, 20 (2020) 56. https://doi.org/10.1186/s12866-020-01723-9.Google Scholar
Tsukuda, N., K. Yahagi, T. Hara, Y. Watanabe, H. Matsumoto, H. Mori, K. Higashi, H. Tsuji, S. Matsumoto, K. Kurokawa, & T. Matsuki, Key bacterial taxa and metabolic pathways affecting gut short-chain fatty acid profiles in early life. ISME J, 15 (2021) 2574–2590. https://doi.org/10.1038/s41396-021-00937-7.Google Scholar
Bridgman, S. L., Azad, M. B., Field, C. J., Haqq, A. M., Becker, A. B., Mandhane, P. J., Subbarao, P., Turvey, S. E., Sears, M. R., Scott, J. A., Wishart, D. S., & Kozyrskyj, A. L., Fecal short-chain fatty acid variations by breastfeeding status in infants at 4 months: Differences in relative versus absolute concentrations. Frontiers in Nutrition, 4 (2017). https://doi.org/10.3389/fnut.2017.00011.Google Scholar
Tun, H. M., Bridgman, S. L., Chari, R., Field, C. J., Guttman, D. S., Becker, A. B., Mandhane, P. J., Turvey, S. E., Subbarao, P., Sears, M. R., Scott, J. A., & Kozyrskyj, A. L., Roles of birth mode and infant gut microbiota in intergenerational transmission of overweight and obesity from mother to offspring. JAMA Pediatrics, 172 (2018) 368–377. https://doi.org/10.1001/jamapediatrics.2017.5535.CrossRefGoogle Scholar
van der Vossen, E. W. J., M. C. de Goffau, E. Levin, & M. Nieuwdorp, Recent insights into the role of microbiome in the pathogenesis of obesity. Therapeutic Advances in Gastroenterology, 15 (2022). https://doi.org/10.1177/17562848221115320.Google Scholar
Stanislawski, M. A., Dabelea, D., Wagner, B. D., Iszatt, N., Dahl, C., Sontag, M. K., Knight, R., Lozupone, C. A., & Eggesbø, M., Gut microbiota in the first 2 years of life and the association with body mass index at age 12 in a Norwegian Birth Cohort. mBio, 9 (2018). https://doi.org/10.1128/mBio.01751-18.Google Scholar
Netea, M. G., Joosten, L. A. B. B., Latz, E., Mills, K. H. G. G., Natoli, G., Stunnenberg, H. G., O’Neill, L. A. J., Xavier, R. J., ONeill, L. A. J., & Xavier, R. J., Trained immunity: A program of innate immune memory in health and disease (American Association for the Advancement of Science, 2016). https://doi.org/10.1126/science.aaf1098.Google Scholar
Safari, Z. & Gérard, P., The links between the gut microbiome and non-alcoholic fatty liver disease (NAFLD). Cellular and Molecular Life Sciences, 76 (2019) 1541–1558. https://doi.org/10.1007/s00018-019-03011-w.Google Scholar
Cani, P. D., Amar, J., Iglesias, M. A., Poggi, M., Knauf, C., Bastelica, D., Neyrinck, A. M., Fava, F., Tuohy, K. M., Chabo, C., Waget, A. Lie, Delmé, E., Cousin, B. Atrice, Sulpice, T., Chamontin, B., Ferriè, J., Tanti, J.-F., Gibson, G. R., Casteilla, L., Delzenne, N. M., Alessi, M. C., & Burcelin, R. My, Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes, 56 (2007) 1761–1772. https://doi.org/10.2337/db06-1491.Google Scholar
Vatanen, T., Kostic, A. D., D’Hennezel, E., Siljander, H., Franzosa, E. A., Yassour, M., Kolde, R., Vlamakis, H., Arthur, T. D., Hämäläinen, A. M., Peet, A., Tillmann, V., Uibo, R., Mokurov, S., Dorshakova, N., Ilonen, J., Virtanen, S. M., Szabo, S. J., Porter, J. A., Lähdesmäki, H., Huttenhower, C., Gevers, D., Cullen, T. W., Knip, M., & Xavier, R. J., Variation in microbiome LPS immunogenicity contributes to autoimmunity in humans. Cell, 165 (2016) 842–853. https://doi.org/10.1016/j.cell.2016.04.007.Google Scholar
Wampach, L., Heintz-Buschart, A., Fritz, J. V., Ramiro-Garcia, J., Habier, J., Herold, M., Narayanasamy, S., Kaysen, A., Hogan, A. H., Bindl, L., Bottu, J., Halder, R., Sjöqvist, C., May, P., Andersson, A. F., de Beaufort, C., & Wilmes, P., Birth mode is associated with earliest strain-conferred gut microbiome functions and immunostimulatory potential. Nature Communications, 9 (2018) 1–14. https://doi.org/10.1038/s41467-018-07631-x.Google Scholar
Kameyama, K. & Itoh, K., Intestinal colonization by a lachnospiraceae bacterium contributes to the development of diabetes in obese mice. Microbes and Environments, 29 (2014) 427–430. https://doi.org/10.1264/jsme2.ME14054.Google Scholar
Loomba, R. & Sanyal, A. J., The global NAFLD epidemic. Nature Reviews Gastroenterology and Hepatology, 10 (2013) 686–690. https://doi.org/10.1038/nrgastro.2013.171.Google Scholar
Goyal, N. P. & Schwimmer, J. B., The progression and natural history of pediatric nonalcoholic fatty liver disease. Clinics in Liver Disease, 20 (2016) 325–338. https://doi.org/10.1016/j.cld.2015.10.003.Google Scholar
Ibrahim, S. H., Jonas, M. M., Taylor, S. A., Sanchez, L. H. Gutierrez, Wolf, J. L., & Sundaram, S. S., Liver diseases in the perinatal period: Interactions between mother and infant. Hepatology, 71 (2020) 1474–1485. https://doi.org/10.1002/hep.31109.Google Scholar
Doycheva, I., Issa, D., Watt, K. D., Lopez, R., Rifai, G., & Alkhouri, N., Nonalcoholic steatohepatitis is the most rapidly increasing indication for liver transplantation in young adults in the United States. Journal of Clinical Gastroenterology, 52 (2018) 339–346. https://doi.org/10.1097/MCG.0000000000000925.Google Scholar
Jayakumar, S. & Loomba, R., Review article: Emerging role of the gut microbiome in the progression of nonalcoholic fatty liver disease and potential therapeutic implications. Alimentary Pharmacology and Therapeutics, 50 (2019) 144–158. https://doi.org/10.1111/apt.15314.Google Scholar
Leatham-Jensen, M. P., Frimodt-Møller, J., Adediran, J., Mokszycki, M. E., Banner, M. E., Caughron, J. E., Krogfelt, K. A., Conway, T., & Cohen, P. S., The streptomycin-treated mouse intestine selects Escherichia coli envZ missense mutants that interact with dense and diverse intestinal microbiota. Infection and Immunity, 80 (2012) 1716–1727. https://doi.org/10.1128/IAI.06193-11.Google Scholar
Koch, M. A., Reiner, G. L., Lugo, K. A., Seher, T. D., Ludington, W. B., & Barton, G. M., Maternal IgG and IgA antibodies Dampen Mucosal T Helper cell responses in early life. Cell, 165 (2016) 827–841. https://doi.org/10.1016/j.cell.2016.04.055.Google Scholar
McCoy, K. D. & Thomson, C. A., The impact of maternal microbes and microbial colonization in early life on hematopoiesis. The Journal of Immunology, 200 (2018) 2519–2526. https://doi.org/10.4049/jimmunol.1701776.Google Scholar
Dogra, S. K., C. K. Chung, D. Wang, O. Sakwinska, S. C. Mottaz, & N. Sprenger, Nurturing the early life gut microbiome and immune maturation for long term health. Microorganisms, 9 (2021) 2110. https://doi.org/10.3390/MICROORGANISMS9102110.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×