Maturation of the infant microbiome community structure and function across multiple body sites and in relation to mode of delivery
Open accessAbstract
Human microbial communities are characterized by their taxonomic, metagenomic and metabolic diversity, which varies by distinct body sites and influences human physiology. However, when and how microbial communities within each body niche acquire unique taxonomical and functional signatures in early life remains underexplored. We thus sought to determine the taxonomic composition and potential metabolic function of the neonatal and early infant microbiota across multiple body sites and assess the effect of the mode of delivery and its potential confounders or modifiers. A cohort of pregnant women in their early third trimester (n = 81) were prospectively enrolled for longitudinal sampling through 6 weeks after delivery, and a second matched cross-sectional cohort (n = 81) was additionally recruited for sampling once at the time of delivery. Samples across multiple body sites, including stool, oral gingiva, nares, skin and vagina were collected for each maternal-infant dyad. Whole-genome shotgun sequencing and sequencing analysis of the gene encoding the 16S rRNA were performed to interrogate the composition and function of the neonatal and maternal microbiota. We found that the neonatal microbiota and its associated functional pathways were relatively homogeneous across all body sites at delivery, with the notable exception of the neonatal meconium. However, by 6 weeks after delivery, the infant microbiota structure and function had substantially expanded and diversified, with the body site serving as the primary determinant of the composition of the bacterial community and its functional capacity. Although minor variations in the neonatal (immediately at birth) microbiota community structure were associated with the cesarean mode of delivery in some body sites (oral gingiva, nares and skin; R 2 = 0.038), this was not true for neonatal stool (meconium; Mann-Whitney P > 0.05), and there was no observable difference in community function regardless of delivery mode. For infants at 6 weeks of age, the microbiota structure and function had expanded and diversified with demonstrable body site specificity (P < 0.001, R 2 = 0.189) but without discernable differences in community structure or function between infants delivered vaginally or by cesarean surgery (P = 0.057, R 2 = 0.007). We conclude that within the first 6 weeks of life, the infant microbiota undergoes substantial reorganization, which is primarily driven by body site and not by mode of delivery.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Although differences can dissipate a few weeks or months after birth, it has been suggested that some microbes acquired during the first years of life will be important residents of the adult microbiota.
“Although these differences can dissipate a few weeks or months after birth (248), it has been suggested that some microbes acquired during the first years of life will be important residents of the adult microbiota (249).”
From Diet and the Microbiota–Gut–Brain Axis: Sowing the Seeds of Good Mental Health (2021) · cites this paper as [248]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
QIIME allows analysis of high-throughput community sequencing data
Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Peña, A. G., Goodrich, J. K., Gordon, J. I., et al. (2010) · Nature Methods · doi:10.1038/nmeth.f.303 · Cited by 34,887 · see citing works
Search and clustering orders of magnitude faster than BLAST
Edgar, R. C. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq461 · Cited by 20,617 · see citing works
Metagenomic biomarker discovery and explanation
Segata, N., Izard, J., Waldron, L., Gevers, D., Miropolsky, L., Garrett, W. S., & Huttenhower, C. (2011) · Genome Biology · doi:10.1186/gb-2011-12-6-r60 · Cited by 16,192 · see citing works
An obesity-associated gut microbiome with increased capacity for energy harvest
Turnbaugh, P. J., Ley, R. E., Mahowald, M. A., Magrini, V., Mardis, E. R., & Gordon, J. I. (2006) · Nature · doi:10.1038/nature05414 · Cited by 12,444 · see citing works
Structure, function and diversity of the healthy human microbiome
The Human Microbiome Project Consortium (2012) · Nature · doi:10.1038/nature11234 · Cited by 11,726 · see citing works
Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB
DeSantis, T. Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E. L., Keller, K., Huber, T., Dalevi, D., Hu, P., & Andersen, G. L. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.03006-05 · Cited by 10,891 · see citing works
Diet rapidly and reproducibly alters the human gut microbiome
David, L. A., Maurice, C. F., Carmody, R. N., Gootenberg, D. B., Button, J. E., Wolfe, B. E., Ling, A. V., Devlin, A. S., Varma, Y., Fischbach, M. A., et al. (2014) · Nature · doi:10.1038/nature12820 · Cited by 10,100 · see citing works
SPECIES ASSEMBLAGES AND INDICATOR SPECIES:THE NEED FOR A FLEXIBLE ASYMMETRICAL APPROACH
Dufrêne, M., & Legendre, P. (1997) · Ecological Monographs · doi:10.1890/0012-9615(1997)067[0345:saaist]2.0.co;2 · Cited by 8,346 · see citing works
Enterotypes of the human gut microbiome
MetaHIT Consortium (additional members), Arumugam, M., Raes, J., Pelletier, E., Le Paslier, D., Yamada, T., Mende, D. R., Fernandes, G. R., Tap, J., Bruls, T., et al. (2011) · Nature · doi:10.1038/nature09944 · Cited by 7,548 · see citing works
A metagenome-wide association study of gut microbiota in type 2 diabetes
Qin, J., Li, Y., Cai, Z., Li, S., Zhu, J., Zhang, F., Liang, S., Zhang, W., Guan, Y., Shen, D., et al. (2012) · Nature · doi:10.1038/nature11450 · Cited by 6,762 · see citing works
Smith, P. M., Howitt, M. R., Panikov, N., Michaud, M., Gallini, C. A., Bohlooly-Y, M., Glickman, J. N., & Garrett, W. S. (2013) · Science · doi:10.1126/science.1241165 · Cited by 5,413 · see citing works
The Ribosomal Database Project: improved alignments and new tools for rRNA analysis
Cole, J., Wang, Q., Cardenas, E., Fish, J., Chai, B., Farris, R. J., Kulam-Syed-Mohideen, A., Mcgarrell, D., Marsh, T., Garrity, G., et al. (2008) · Nucleic Acids Res. · doi:10.1093/nar/gkn879 · Cited by 4,940 · see citing works
Dominguez-Bello, M. G., Costello, E. K., Contreras, M., Magris, M., Hidalgo, G., Fierer, N., & Knight, R. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002601107 · Cited by 4,774 · see citing works
Richness of human gut microbiome correlates with metabolic markers
Le Chatelier, E., Nielsen, T., Qin, J., Prifti, E., Hildebrand, F., Falony, G., Almeida, M., Arumugam, M., Batto, J.-M., Kennedy, S., et al. (2013) · Nature · doi:10.1038/nature12506 · Cited by 4,662 · see citing works
Induction of Intestinal Th17 Cells by Segmented Filamentous Bacteria
Ivanov, I. I., Atarashi, K., Manel, N., Brodie, E. L., Shima, T., Karaoz, U., Wei, D., Goldfarb, K. C., Santee, C. A., Lynch, S. V., et al. (2009) · Cell · doi:10.1016/j.cell.2009.09.033 · Cited by 4,554 · see citing works
Vaginal microbiome of reproductive-age women
Ravel, J., Gajer, P., Abdo, Z., Schneider, G. M., Koenig, S. S. K., McCulle, S. L., Karlebach, S., Gorle, R., Russell, J., Tacket, C. O., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002611107 · Cited by 4,254 · see citing works
Gut Microbiota from Twins Discordant for Obesity Modulate Metabolism in Mice
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., et al. (2013) · Science · doi:10.1126/science.1241214 · Cited by 3,788 · see citing works
Induction of Colonic Regulatory T Cells by Indigenous <i>Clostridium</i> Species
Atarashi, K., Tanoue, T., Shima, T., Imaoka, A., Kuwahara, T., Momose, Y., Cheng, G., Yamasaki, S., Saito, T., Ohba, Y., et al. (2011) · Science · doi:10.1126/science.1198469 · Cited by 3,752 · see citing works
Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR ampliconsPreprint
Haas, B. J., Gevers, D., Earl, A. M., Feldgarden, M., Ward, D. V., Giannoukos, G., Ciulla, D., Tabbaa, D., Highlander, S. K., Sodergren, E. J., et al. (2011) · Genome Research · doi:10.1101/gr.112730.110 · Cited by 3,480 · see citing works
Dynamics and Stabilization of the Human Gut Microbiome during the First Year of Life
Bäckhed, F., Roswall, J., Peng, Y., Feng, Q., Jia, H., Kovatcheva-Datchary, P., Li, Y., Xia, Y., Xie, H., Zhong, H., et al. (2015) · Cell Host & Microbe · doi:10.1016/j.chom.2015.04.004 · Cited by 3,315 · see citing works
Bacterial Community Variation in Human Body Habitats Across Space and Time
Costello, E. K., Lauber, C. L., Hamady, M., Fierer, N., Gordon, J. I., & Knight, R. (2009) · Science · doi:10.1126/science.1177486 · Cited by 3,231 · see citing works
Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment
Morgan, X. C., Tickle, T. L., Sokol, H., Gevers, D., Devaney, K. L., Ward, D. V., Reyes, J. A., Shah, S. A., LeLeiko, N., Snapper, S. B., et al. (2012) · Genome Biology · doi:10.1186/gb-2012-13-9-r79 · Cited by 2,713 · see citing works
Succession of microbial consortia in the developing infant gut microbiome
Koenig, J. E., Spor, A., Scalfone, N., Fricker, A. D., Stombaugh, J., Knight, R., Angenent, L. T., & Ley, R. E. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1000081107 · Cited by 2,540 · see citing works
The Placenta Harbors a Unique Microbiome
Aagaard, K., Ma, J., Antony, K. M., Ganu, R., Petrosino, J., & Versalovic, J. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3008599 · Cited by 2,494 · see citing works
Self-citationFactors influencing the composition of the intestinal microbiota in early infancy
Penders, J., Thijs, C., Vink, C., Stelma, F. F., Snijders, B., Kummeling, I., van den Brandt, P. A., & Stobberingh, E. E. (2006) · PEDIATRICS · doi:10.1542/peds.2005-2824 · Cited by 2,232 · see citing works
Host Remodeling of the Gut Microbiome and Metabolic Changes during Pregnancy
Koren, O., Goodrich, J. K., Cullender, T. C., Spor, A., Laitinen, K., Kling Bäckhed, H., Gonzalez, A., Werner, J. J., Angenent, L. T., Knight, R., et al. (2012) · Cell · doi:10.1016/j.cell.2012.07.008 · Cited by 2,165 · see citing works
Bayesian community-wide culture-independent microbial source tracking
Knights, D., Kuczynski, J., Charlson, E. S., Zaneveld, J., Mozer, M. C., Collman, R. G., Bushman, F. D., Knight, R. D., & Kelley, S. T. (2011) · Nature Methods · doi:10.1038/nmeth.1650 · Cited by 1,839 · see citing works
Metagenomic microbial community profiling using unique clade-specific marker genes
Segata, N., Waldron, L., Ballarini, A., Narasimhan, V., Jousson, O., & Huttenhower, C. (2012) · Nature Methods · doi:10.1038/nmeth.2066 · Cited by 1,776 · see citing works
Microbial Exposure During Early Life Has Persistent Effects on Natural Killer T Cell Function
Olszak, T., An, D., Zeissig, S., Vera, M. P., Richter, J., Franke, A., Glickman, J. N., Siebert, R., Baron, R. M., Kasper, D. L., et al. (2012) · Science · doi:10.1126/science.1219328 · Cited by 1,661 · see citing works
Antibiotics, birth mode, and diet shape microbiome maturation during early life
Bokulich, N. A., Chung, J., Battaglia, T., Henderson, N., Jay, M., Li, H., D. Lieber, A., Wu, F., Perez-Perez, G. I., Chen, Y., et al. (2016) · Science Translational Medicine · doi:10.1126/scitranslmed.aad7121 · Cited by 1,469 · see citing works
Safe prevention of the primary cesarean delivery
Caughey, A. B., Cahill, A. G., Guise, J., & Rouse, D. J. (2014) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2014.01.026 · Cited by 1,380 · see citing works
Bile acids and the gut microbiome
Ridlon, J. M., Kang, D. J., Hylemon, P. B., & Bajaj, J. S. (2014) · Current Opinion in Gastroenterology · doi:10.1097/mog.0000000000000057 · Cited by 1,329 · see citing works
Variation in Microbiome LPS Immunogenicity Contributes to Autoimmunity in Humans
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., et al. (2016) · Cell · doi:10.1016/j.cell.2016.04.007 · Cited by 1,289 · see citing works
The maternal microbiota drives early postnatal innate immune development
Gomez de Agüero, M., Ganal-Vonarburg, S. C., Fuhrer, T., Rupp, S., Uchimura, Y., Li, H., Steinert, A., Heikenwalder, M., Hapfelmeier, S., Sauer, U., et al. (2016) · Science · doi:10.1126/science.aad2571 · Cited by 1,231 · see citing works
Collado, M. C., Rautava, S., Aakko, J., Isolauri, E., & Salminen, S. (2016) · Scientific Reports · doi:10.1038/srep23129 · Cited by 1,098 · see citing works
B Vitamins and the Brain: Mechanisms, Dose and Efficacy—A Review
Kennedy, D. (2016) · Nutrients · doi:10.3390/nu8020068 · Cited by 1,055 · see citing works
Metabolic Reconstruction for Metagenomic Data and Its Application to the Human Microbiome
Abubucker, S., Segata, N., Goll, J. B., Schubert, A. M., Izard, J., Cantarel, B. L., Rodriguez-Mueller, B., Zucker, J., Thiagarajan, M., Henrissat, B., et al. (2012) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002358 · Cited by 1,050 · see citing works
Yassour, M., Vatanen, T., Siljander, H., Hämäläinen, A.-M., Härkönen, T., Ryhänen, S. J., Franzosa, E. A., Vlamakis, H., Huttenhower, C., Gevers, D., et al. (2016) · Science Translational Medicine · doi:10.1126/scitranslmed.aad0917 · Cited by 1,043 · see citing works
Partial restoration of the microbiota of cesarean-born infants via vaginal microbial transfer
Dominguez-Bello, M. G., De Jesus-Laboy, K. M., Shen, N., Cox, L. M., Amir, A., Gonzalez, A., Bokulich, N. A., Song, S. J., Hoashi, M., Rivera-Vinas, J. I., et al. (2016) · Nature Medicine · doi:10.1038/nm.4039 · Cited by 1,014 · see citing works
Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months
Azad, M. B., Konya, T., Maughan, H., Guttman, D. S., Field, C. J., Chari, R. S., Sears, M. R., Becker, A. B., Scott, J. A., & Kozyrskyj, A. L. (2013) · Canadian Medical Association Journal · doi:10.1503/cmaj.121189 · Cited by 953 · see citing works
Is meconium from healthy newborns actually sterile?
Jiménez, E., Marín, M. L., Martı́n, R., Odriozola, J. M., Olivares, M. M., Xaus, J., Fernández, L., & Rodríguez, J. M. (2008) · Research in Microbiology · doi:10.1016/j.resmic.2007.12.007 · Cited by 944 · see citing works
DiGiulio, D. B., Romero, R. J., Amogan, H., Kusanovic, J. P., Bik, E. M., Gotsch, F., Kim, C. J., Erez, O., Edwin, S. S., & Relman, D. A. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003056 · Cited by 798 · see citing works
Fast Identification and Removal of Sequence Contamination from Genomic and Metagenomic Datasets
Schmieder, R., & Edwards, R. A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017288 · Cited by 740 · see citing works
Dynamics and stabilization of the human gut microbiome during the first year of life
Bäckhed, F., Roswall, J., Peng, Y., Feng, Q., Jia, H., Kovatcheva-Datchary, P., Li, Y., Xia, Y., Xie, H., Zhong, H., et al. (2015) · Cell Host & Microbe · doi:10.1016/j.chom.2015.05.012 · Cited by 738 · cited 8× · see citing works
“These include: Cesarean delivery 40,43,52 , exclusive breastfeeding 26,42,59 , maternal high fat diet 47 , maternal obesity 46 , transition to solid foods 30 , and other yet unknown factors 52 .”
InfluentialA Metagenomic Approach to Characterization of the Vaginal Microbiome Signature in Pregnancy
Aagaard, K. M., Riehle, K. P., Ma, J., Segata, N., Mistretta, T., Coarfa, C., Raza, S., Rosenbaum, S., den Veyver, I. B. V., Milosavljevic, A., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036466 · Cited by 714 · see citing works
Self-citationIndications Contributing to the Increasing Cesarean Delivery Rate
Barber, E. L., Lundsberg, L. S., Belanger, K. D., Pettker, C. M., Funai, E. F., & Illuzzi, J. L. (2011) · Obstetrics and Gynecology · doi:10.1097/aog.0b013e31821e5f65 · Cited by 694 · see citing works
Jiménez, E., Fernández, L., Marín, M. L., Martı́n, R., Odriozola, J. M., Nueno‐Palop, C., Narbad, A., Olivares, M. M., Xaus, J., & Rodríguez, J. M. (2005) · Current Microbiology · doi:10.1007/s00284-005-0020-3 · Cited by 681 · see citing works
Azad, M. B., Konya, T., Persaud, R. R., Guttman, D. S., Chari, R., Field, C. J., Sears, M., Mandhane, P., Turvey, S., Subbarao, P., et al. (2015) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/1471-0528.13601 · Cited by 619 · see citing works
Vertical mother–neonate transfer of maternal gut bacteria via breastfeeding
Jost, T., Lacroix, C., Braegger, C., Rochat, F., & Chassard, C. (2013) · Environmental Microbiology · doi:10.1111/1462-2920.12238 · Cited by 577 · see citing works
Patterned progression of bacterial populations in the premature infant gut
Rosa, P. S. L., Warner, B. B., Zhou, Y., Weinstock, G. M., Sodergren, E. J., Hall-Moore, C. M., Stevens, H. J., Bennett, W. E., Shaikh, N., Linneman, L. A., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1409497111 · Cited by 573 · see citing works
Fallani, M., Young, D., Scott, J. A., Norin, E. L., Amarri, S., Adam, R., Aguilera, J., Khanna, S., Gil, Á., Edwards, C. A., et al. (2010) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0b013e3181d1b11e · Cited by 559 · see citing works
Mode of delivery affects the bacterial community in the newborn gut
Biasucci, G., Rubini, M., Riboni, S., Morelli, L., Bessi, E., & Retetangos, C. (2010) · Early Human Development · doi:10.1016/j.earlhumdev.2010.01.004 · Cited by 507 · see citing works
Meconium Microbiome Analysis Identifies Bacteria Correlated with Premature Birth
Ardissone, A. N., de la Cruz, D., Davis‐Richardson, A. G., Rechcigl, K. T., Li, N., Drew, J. C., Torrazza, R. J. M., Sharma, R. R., Hudak, M. L., Triplett, E. W., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0090784 · Cited by 460 · see citing works
Developmental dynamics of the preterm infant gut microbiota and antibiotic resistome
Gibson, M. K., Wang, B., Ahmadi, S., Burnham, C.-A. D., Tarr, P. I., Warner, B. B., & Dantas, G. (2016) · Nature Microbiology · doi:10.1038/nmicrobiol.2016.24 · Cited by 457 · see citing works
High-fat-diet-mediated dysbiosis promotes intestinal carcinogenesis independently of obesity
Schulz, M. D., Atay, Ç., Heringer, J., Romrig, F., Schwitalla, S., Aydın, B., Ziegler, P. K., Varga, J., Reindl, W., Pommerenke, C., et al. (2014) · Nature · doi:10.1038/nature13398 · Cited by 452 · see citing works
The gnotobiotic animal as a tool in the study of host microbial relationships
Gordon, H. A., & Pesti, L. (1971) · Bacteriological Reviews · doi:10.1128/br.35.4.390-429.1971 · Cited by 393 · see citing works
Fallani, M., Amarri, S., Uusijärvi, A., Adam, R., Khanna, S., Aguilera, J., Gil, Á., Vieites, J. M., Norin, E. L., Young, D., et al. (2011) · Microbiology · doi:10.1099/mic.0.042143-0 · Cited by 393 · see citing works
Aagaard, K., Petrosino, J., Keitel, W., Watson, M., Katancik, J., Garcia, N., Patel, S., Cutting, M., Madden, T., Hamilton, H., et al. (2013) · The FASEB Journal · doi:10.1096/fj.12-220806 · Cited by 383 · see citing works
Self-citationThe early infant gut microbiome varies in association with a maternal high-fat diet
Chu, D. M., Antony, K. M., Ma, J., Prince, A., Showalter, L., Moller, M., & Aagaard, K. M. (2016) · Genome Medicine · doi:10.1186/s13073-016-0330-z · Cited by 376 · see citing works
Self-citationHypothesis Testing and Power Calculations for Taxonomic-Based Human Microbiome Data
Rosa, P. S. L., Brooks, J. P., Deych, E., Boone, E. L., Edwards, D., Wang, Q., Sodergren, E. J., Weinstock, G. M., & Shannon, W. D. (2012) · PLoS ONE · doi:10.1371/journal.pone.0052078 · Cited by 325 · see citing works
Bacteria and inflammatory cells in fetal membranes do not always cause preterm labor
Steel, J. H., Malatos, S., Kennea, N., Edwards, A. D., Miles, L., Duggan, P., Reynolds, P. R., Feldman, R. G., & Sullivan, M. H. F. (2005) · Pediatric Research · doi:10.1203/01.pdr.0000153869.96337.90 · Cited by 317 · see citing works
Microbial colonization influences early B-lineage development in the gut lamina propria
Wesemann, D. R., Portuguese, A. J., Meyers, R. M., Gallagher, M. P., Cluff-Jones, K., Magee, J. M., Panchakshari, R. A., Rodig, S. J., Kepler, T. B., & Alt, F. W. (2013) · Nature · doi:10.1038/nature12496 · Cited by 286 · see citing works
Diversified Microbiota of Meconium Is Affected by Maternal Diabetes Status
Hu, J., Nomura, Y., Bashir, A., Fernandez-Hernandez, H., Itzkowitz, S. H., Pei, Z., Stone, J. L., Loudon, H., & Peter, I. (2013) · PLoS ONE · doi:10.1371/journal.pone.0078257 · Cited by 257 · see citing works
Factors influencing rising caesarean section rates in China between 1988 and 2008
Feng, X. L., Xu, L., Guo, Y. J., & Ronsmans, C. (2012) · Bulletin of the World Health Organization · doi:10.2471/blt.11.090399 · Cited by 254 · see citing works
The preterm placental microbiome varies in association with excess maternal gestational weight gain
Antony, K. M., Ma, J., Mitchell, K. B., Racusin, D., Versalovic, J. A., & Aagaard, K. M. (2015) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2014.12.041 · Cited by 212 · see citing works
Self-citationThe gnotobiotic animal as a tool in the study of host microbial relationships.
Gordon, H. A., & Pesti, L. (1971) · Bacteriological Reviews · doi:10.1128/mmbr.35.4.390-429.1971 · Cited by 205 · see citing works
Hansen, R., Scott, K. P., Khan, S., Martin, J. C., Berry, S. H., Stevenson, M. D., Augusta, O., Munro, M. J., & Hold, G. L. (2015) · PLoS ONE · doi:10.1371/journal.pone.0133320 · Cited by 183 · see citing works
Maternal Obesity Is Associated with Alterations in the Gut Microbiome in Toddlers
Galley, J. D., Bailey, M. T., Dush, C. M. K., Schoppe‐Sullivan, S. J., & Christian, L. M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0113026 · Cited by 180 · see citing works
Microbiome Assembly across Multiple Body Sites in Low-Birthweight Infants
Costello, E. K., Carlisle, E. M., Bik, E. M., Morowitz, M. J., & Relman, D. A. (2013) · mBio · doi:10.1128/mbio.00782-13 · Cited by 172 · see citing works
Mueller, N. T., Shin, H., Pizoni, A., Werlang, I. C. R., Matte, Ú. D. S., Goldani, M. Z., Goldani, H. A. S., & Domínguez-Bello, M. G. (2016) · Scientific Reports · doi:10.1038/srep23133 · Cited by 141 · see citing works
Trends in low-risk cesarean delivery in the United States, 1990-2013.
Osterman, M. J. K., & Martin, J. A. (2014) · PubMed · Cited by 137 · see citing works
Breast-fed and bottle-fed infant rhesus macaques develop distinct gut microbiotas and immune systems
Ardeshir, A., Narayan, N. R., Méndez-Lagares, G., Lu, D., Rauch, M., Huang, Y., Van Rompay, K. K. A., Lynch, S. V., & Hartigan-O’Connor, D. J. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3008791 · Cited by 134 · see citing works
The impact of birth mode of delivery on childhood asthma and allergic diseases–a sibling study
Almqvist, C., Cnattingius, S., Lichtenstein, P., & Lundholm, C. (2012) · Clinical & Experimental Allergy · doi:10.1111/j.1365-2222.2012.04021.x · Cited by 117 · see citing works
Black, M. E., Bhattacharya, S., Philip, S., Norman, J. E., & McLernon, D. J. (2016) · PLoS Medicine · doi:10.1371/journal.pmed.1001973 · Cited by 69 · see citing works
Preventing the First Cesarean Delivery
Benson, J. (2013) · Obstetrics and Gynecology · doi:10.1097/aog.0b013e31828a82b5 · Cited by 13 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Cryan, J. F., O'Riordan, K. J., Cowan, C. S. M., Sandhu, K. V., Bastiaanssen, T. F. S., Boehme, M., Codagnone, M. G., Cussotto, S., Fulling, C., Golubeva, A. V., et al. (2019) · Physiological Reviews · doi:10.1152/physrev.00018.2018 · Cited by 5,286 · see citing works
Milani, C., Duranti, S., Bottacini, F., Casey, E., Turroni, F., Mahony, J., Belzer, C., Delgado Palacio, S., Arboleya Montes, S., Mancabelli, L., et al. (2017) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00036-17 · Cited by 1,950 · see citing works
Stunted microbiota and opportunistic pathogen colonization in caesarean-section birth
Shao, Y., Forster, S. C., Tsaliki, E., Vervier, K., Strang, A., Simpson, N., Kumar, N., Stares, M. D., Rodger, A., Brocklehurst, P., et al. (2019) · Nature · doi:10.1038/s41586-019-1560-1 · Cited by 1,088 · see citing works
The Human Gut Microbiome: From Association to Modulation
Schmidt, T. S. B., Raes, J., & Bork, P. (2018) · Cell · doi:10.1016/j.cell.2018.02.044 · Cited by 845 · see citing works
The Human Microbiome and Child Growth – First 1000 Days and Beyond
Robertson, R. C., Manges, A. R., Finlay, B. B., & Prendergast, A. J. (2019) · Trends in Microbiology · doi:10.1016/j.tim.2018.09.008 · Cited by 793 · see citing works
Dietary metabolism, the gut microbiome, and heart failure
Tang, W. H. W., Li, D. Y., & Hazen, S. L. (2019) · Nature Reviews Cardiology · doi:10.1038/s41569-018-0108-7 · Cited by 789 · see citing works
Maturation of the gut microbiome and risk of asthma in childhood
Stokholm, J., Blaser, M. J., Thorsen, J., Rasmussen, M. A., Waage, J., Vinding, R. K., Schoos, A.-M. M., Kunøe, A., Fink, N. R., Chawes, B. L., et al. (2018) · Nature Communications · doi:10.1038/s41467-017-02573-2 · Cited by 614 · see citing works
MAIT cells are imprinted by the microbiota in early life and promote tissue repair
Constantinides, M. G., Link, V. M., Tamoutounour, S., Wong, A. C., Perez-Chaparro, P. J., Han, S.-J., Chen, Y. E., Li, K., Farhat, S., Weckel, A., et al. (2019) · Science · doi:10.1126/science.aax6624 · Cited by 567 · see citing works
Anxiety, depression, and the microbiome: A role for gut peptides
Lach, G., Schellekens, H., Dinan, T. G., & Cryan, J. F. (2018) · Neurotherapeutics · doi:10.1007/s13311-017-0585-0 · Cited by 573 · see citing works
The microbiome in patients with atopic dermatitis
Paller, A. S., Kong, H. H., Seed, P., Naik, S., Scharschmidt, T. C., Gallo, R. L., Luger, T., & Irvine, A. D. (2019) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2018.11.015 · Cited by 525 · see citing works
Analysis of Gut Microbiota in Patients with Parkinson’s Disease
Petrov, V. A., Saltykova, I. V., Zhukova, I. A., Alifirova, V. M., Zhukova, N. G., Dorofeeva, Y. B., Tyakht, A. V., Kovarsky, B. A., Alekseev, D. G., Kostryukova, E. S., et al. (2017) · Bulletin of Experimental Biology and Medicine · doi:10.1007/s10517-017-3700-7 · Cited by 487 · see citing works
The person-to-person transmission landscape of the gut and oral microbiomes
Valles-Colomer, M., Blanco-Míguez, A., Manghi, P., Asnicar, F., Dubois, L., Golzato, D., Armanini, F., Cumbo, F., Huang, K. D., Manara, S., et al. (2023) · Nature · doi:10.1038/s41586-022-05620-1 · Cited by 449 · see citing works
Dysbiosis of maternal and neonatal microbiota associated with gestational diabetes mellitus
Wang, J., Zheng, J., Shi, W., Du, N., Xu, X., Zhang, Y., Ji, P., Zhang, F., Jia, Z., Wang, Y., et al. (2018) · Gut · doi:10.1136/gutjnl-2018-315988 · Cited by 452 · see citing works
Strain-Level Analysis of Mother-to-Child Bacterial Transmission during the First Few Months of Life
Yassour, M., Jason, E., Hogstrom, L. J., Arthur, T. D., Tripathi, S., Siljander, H., Selvenius, J., Oikarinen, S., Hyöty, H., Virtanen, S. M., et al. (2018) · Cell Host & Microbe · doi:10.1016/j.chom.2018.06.007 · Cited by 455 · see citing works
Diet and the Microbiota–Gut–Brain Axis: Sowing the Seeds of Good Mental Health
Berding, K., Vlckova, K., Marx, W., Schellekens, H., Stanton, C., Clarke, G., Jacka, F., Dinan, T. G., & Cryan, J. F. (2021) · Advances in Nutrition · doi:10.1093/advances/nmaa181 · Cited by 451 · see citing works
Role of priority effects in the early-life assembly of the gut microbiota
Sprockett, D., Fukami, T., & Relman, D. A. (2018) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2017.173 · Cited by 419 · see citing works
RETRACTED ARTICLE: Role of the gut microbiome in chronic diseases: a narrative review
Vijay, A., & Valdes, A. M. (2022) · European Journal of Clinical Nutrition · doi:10.1038/s41430-021-00991-6 · Cited by 361 · see citing works
RetractedPrescott, S. L., Larcombe, D.-L., Logan, A. C., West, C., Burks, W., Caraballo, L., Levin, M., Etten, E. V., Horwitz, P., Kozyrskyj, A., et al. (2017) · World Allergy Organization Journal · doi:10.1186/s40413-017-0160-5 · Cited by 347 · see citing works
Wampach, L., Heintz-Buschart, A., Fritz, J. V., Ramiro-Garcia, J., Habier, J., Herold, M., Narayanasamy, S., Kaysen, A., Hogan, A. H., Bindl, L., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-07631-x · Cited by 292 · see citing works
Microbiota transplantation: Concept, methodology and strategy for its modernization
FMT-standardization Study Group, Zhang, F., Cui, B., He, X., Nie, Y., Wu, K., & Fan, D. (2018) · Protein & Cell · doi:10.1007/s13238-018-0541-8 · Cited by 300 · see citing works
Comprehensive benchmarking and ensemble approaches for metagenomic classifiers
McIntyre, A. B. R., Ounit, R., Afshinnekoo, E., Prill, R. J., Hénaff, E., Alexander, N., Minot, S. S., Danko, D., Foox, J., Ahsanuddin, S., et al. (2017) · Genome Biology · doi:10.1186/s13059-017-1299-7 · Cited by 342 · see citing works
Microbiota succession throughout life from the cradle to the grave
Martino, C., Dilmore, A. H., Burcham, Z. M., Metcalf, J. L., Jeste, D., & Knight, R. (2022) · Nature Reviews Microbiology · doi:10.1038/s41579-022-00768-z · Cited by 275 · see citing works
Cross talk: the microbiota and neurodevelopmental disorders
Kelly, J. R., Minuto, C., Cryan, J. F., Clarke, G., & Dinan, T. G. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00490 · Cited by 271 · see citing works
Problems with the concept of gut microbiota dysbiosis
Brüssow, H. (2020) · Microbial Biotechnology · doi:10.1111/1751-7915.13479 · Cited by 250 · see citing works
Factors affecting early-life intestinal microbiota development
Vandenplas, Y., Carnielli, V. P., Ksiazyk, J., Luna, M. S., Migacheva, N., Mosselmans, J. M., Picaud, J. C., Possner, M., Singhal, A., & Wabitsch, M. (2020) · Nutrition · doi:10.1016/j.nut.2020.110812 · Cited by 247 · see citing works
Maternal vertical transmission affecting early-life microbiota development
Wang, S., Ryan, C. A., Boyaval, P., Dempsey, E. M., Ross, R. P., & Stanton, C. (2020) · Trends in Microbiology · doi:10.1016/j.tim.2019.07.010 · Cited by 243 · see citing works
Bile acids drive the newborn’s gut microbiota maturation
van Best, N., Rolle-Kampczyk, U., Schaap, F. G., Basic, M., Olde Damink, S. W. M., Bleich, A., Savelkoul, P. H. M., von Bergen, M., Penders, J., & Hornef, M. W. (2020) · Nature Communications · doi:10.1038/s41467-020-17183-8 · Cited by 226 · see citing works
Oral microbiome: possible harbinger for children’s health
Xiao, J., Fiscella, K. A., & Gill, S. R. (2020) · International Journal of Oral Science · doi:10.1038/s41368-020-0082-x · Cited by 223 · see citing works
Programming Bugs: Microbiota and the Developmental Origins of Brain Health and Disease
Codagnone, M. G., Spichak, S., O’Mahony, S. M., O’Leary, O. F., Clarke, G., Stanton, C., Dinan, T. G., & Cryan, J. F. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.06.014 · Cited by 198 · see citing works
Early-Life Formation of the Microbial and Immunological Environment of the Human Airways
Pattaroni, C., Watzenboeck, M. L., Schneidegger, S., Kieser, S., Wong, N. C., Bernasconi, E., Pernot, J., Mercier, L., Knapp, S., Nicod, L. P., et al. (2018) · Cell Host & Microbe · doi:10.1016/j.chom.2018.10.019 · Cited by 183 · see citing works
The developing gut microbiota and its consequences for health
Butel, M.-J., Waligora-Dupriet, A.-J., & Wydau-Dematteis, S. (2018) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174418000119 · Cited by 182 · see citing works
Cowan, C. S. M., Dinan, T. G., & Cryan, J. F. (2020) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.13156 · Cited by 176 · see citing works
Intestinal transgene delivery with native E. coli chassis allows persistent physiological changes
Russell, B. J., Brown, S. D., Siguenza, N., Mai, I., Saran, A. R., Lingaraju, A., Maissy, E. S., Dantas Machado, A. C., Pinto, A. F. M., Sanchez, C., et al. (2022) · Cell · doi:10.1016/j.cell.2022.06.050 · Cited by 151 · see citing works
Factors influencing the gut microbiome in children: from infancy to childhood
Kumbhare, S. V., Patangia, D. V., Patil, R. H., Shouche, Y. S., & Patil, N. P. (2019) · Journal of Biosciences · doi:10.1007/s12038-019-9860-z · Cited by 143 · see citing works
Characterizing oral microbial communities across dentition states and colonization niches
Mason, M. R., Chambers, S., Dabdoub, S. M., Thikkurissy, S., & Kumar, P. S. (2018) · Microbiome · doi:10.1186/s40168-018-0443-2 · Cited by 142 · see citing works
The Role of the Microbiome-Brain-Gut Axis in the Pathogenesis of Depressive Disorder
Młynarska, E., Gadzinowska, J., Tokarek, J., Forycka, J., Szuman, A., Franczyk, B., & Rysz, J. (2022) · Nutrients · doi:10.3390/nu14091921 · Cited by 109 · see citing works
The connection between microbiome and schizophrenia
Golofast, B., & Vales, K. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.12.011 · Cited by 92 · see citing works
Of microbes and minds: A narrative review on the second brain aging
Calvani, R., Picca, A., Lo Monaco, M. R., Landi, F., Bernabei, R., & Marzetti, E. (2018) · Frontiers in Medicine · doi:10.3389/fmed.2018.00053 · Cited by 92 · see citing works
Hung, L. Y., & Margolis, K. G. (2024) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-023-00857-1 · Cited by 96 · see citing works
Luk, B., Veeraragavan, S., Engevik, M., Balderas, M., Major, A., Runge, J., Luna, R. A., & Versalovic, J. (2018) · PLOS ONE · doi:10.1371/journal.pone.0196510 · Cited by 90 · see citing works
Andreu-Sánchez, S., Blanco-Míguez, A., Wang, D., Golzato, D., Manghi, P., Heidrich, V., Fackelmann, G., Zhernakova, D. V., Kurilshikov, A., Valles-Colomer, M., et al. (2025) · Cell · doi:10.1016/j.cell.2025.04.014 · Cited by 81 · see citing works
Update on the pathogenesis of atopic dermatitis.
Criado, P. R., Miot, H. A., Bueno-Filho, R., Ianhez, M., Criado, R. F. J., & de Castro, C. C. S. (2024) · Anais brasileiros de dermatologia · doi:10.1016/j.abd.2024.06.001 · Cited by 66 · see citing works
The shrinking human gut microbiome
Moeller, A. H. (2017) · Current Opinion in Microbiology · doi:10.1016/j.mib.2017.04.002 · Cited by 50 · see citing works
Between Dysbiosis, Maternal Immune Activation and Autism: Is There a Common Pathway?
Suprunowicz, M., Tomaszek, N., Urbaniak, A., Zackiewicz, K., Modzelewski, S., & Waszkiewicz, N. (2024) · Nutrients · doi:10.3390/nu16040549 · Cited by 44 · see citing works
De Sales-Millán, A., Aguirre-Garrido, J. F., González-Cervantes, R. M., & Velázquez-Aragón, J. A. (2023) · doi:10.20944/preprints202305.1223.v1 · Cited by 44 · see citing works
Composition and maternal origin of the neonatal oral cavity microbiota
Tuominen, H., Collado, M. C., Rautava, J., Syrjänen, S., & Rautava, S. (2019) · Journal of Oral Microbiology · doi:10.1080/20002297.2019.1663084 · Cited by 39 · see citing works
Maternal and food microbial sources shape the infant microbiome of a rural Ethiopian population
Manara, S., Selma-Royo, M., Huang, K. D., Asnicar, F., Armanini, F., Blanco-Miguez, A., Cumbo, F., Golzato, D., Manghi, P., Pinto, F., et al. (2023) · Current Biology · doi:10.1016/j.cub.2023.04.011 · Cited by 30 · see citing works
Kim, K., Jang, H., Kim, E., Kim, H., & Sung, G. Y. (2023) · Experimental Dermatology · doi:10.1111/exd.14940 · Cited by 24 · see citing works
The endocannabinoid system: a bridge between alzheimer’s disease and gut microbiota
Bisogno, T., Lauritano, A., & Piscitelli, F. (2021) · Life · doi:10.3390/life11090934 · Cited by 16 · see citing works
- Authors
- Chu, D. M., Ma, J., Prince, A. L., Antony, K. M., Seferovic, M. D., & Aagaard, K. M.
- Affiliations
- Baylor College of Medicine (US)
- Corresponding author
- Aagaard, Kjersti M
- Venue
- Nature Medicine
- Published
- 2017-01-23
- Volume
- 23
- Issue
- 3
- Pages
- 314-326
- ISSN
- 1078-8956 (ISSN-L)
- 1546-170X
- PMC
- PMC5345907
- OpenAlex
- W2582492205
- Cited by
- 1,063
- References
- 75
- Citations by year
- 2026: 67 · 2025: 87 · 2024: 130 · 2023: 122 · 2022: 118 · 2021: 128 · 2020: 127 · 2019: 116 · 2018: 105 · 2017: 61
- FWCI
- 45.66
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Medicine (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (DP2OD001500)
- National Human Genome Research Institute (U54HG004973)
- National Institute of Nursing Research (R01NR014792)
- National Institute of General Medical Sciences (T32GM007330, T32GM088129)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (F32HD082969, R01HD091731)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Nursing › Nutrition and Dietetics › Infant Nutrition and Health
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Keywords
- infant microbiome, neonatal microbiome, mode of delivery, cesarean section, vaginal delivery, meconium, maternal microbiota, microbial metabolic functions, nares, skin, vaginal microbiota, gut microbiota, early-life microbial colonization, mother-infant dyads, microbial diversity
- MeSH terms
- Gastrointestinal Microbiome, Adult, Cesarean Section, Cross-Sectional Studies, Female, Gingiva, Humans, Infant, Infant, Newborn, Longitudinal Studies, Male, Meconium, Nasal Mucosa, Pregnancy, Pregnancy Trimester, Third, Prospective Studies, RNA, Ribosomal, 16S, Skin, Delivery, Obstetric, Young Adult, Metagenomics
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review