The Microbial Ecology of the Large Bowel of Breastfed and Formula-fed Infants During the First Year of Life
Abstract
The succession of bacterial populations in the large bowel of seven breast-fed and seven formula-fed infants was examined during the first year of life. The composition of the intestinal microflora varied according to the infant's diet. During the first week of life breast-fed and formula-fed infants were colonised by enterobacteria and enterococci followed by bifidobacteria, Bacteroides spp., clostridia and anaerobic streptococci. From week 4 until solid foods were given, breast-fed babies had a simple flora consisting of bifidobacteria and relatively few enterobacteria and enterococci. Formula-fed babies during the corresponding period were more often colonised by other anaerobes in addition to bifidobacteria and had higher counts of facultatively anaerobic bacteria. The introduction of solid food to the breast-fed infants caused a major disturbance in the microbial ecology of the large bowel as counts of enterobacteria and enterococci rose sharply and colonisation by Bacteroides spp., clostridia and anaerobic streptococci occurred. This was not observed when formula-fed infants began to take solids; instead, counts of facultative anaerobes remained high while colonisation by anaerobes other than bifidobacteria continued. At 12 months, the anaerobic bacterial populations of the large bowel of breast-fed and formula-fed infants were beginning to resemble those of adults in number and composition and there was a corresponding decrease in the number of facultative anaerobes. These changes are discussed in relation to changes in susceptibility to gastro-intestinal infection.
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Breast-fed and formula-fed infants differ in the composition of their intestinal microbiota.
“Multiple studies have established differences in the composition of the intestinal microbiota based on whether infants are breast- or formula-fed5-7.”
From Diet and the Intestinal Microbiome: Associations, Functions, and Implications for Health and Disease (2014) · cites this paper as [6]
Many studies show a higher proportion of Bifidobacteria in breast-fed infants than in formula-fed infants, and this difference is thought to be secondary to human milk oligosaccharide effects.
“Some of the differences in the composition of the intestinal microbiota in breast-fed vs formula-fed infants are thought to be secondary to the effects of MOS on these bacteria—many studies have shown an increased proportion of Bifidobacteria in breast-fed infants 6, 7, 11 compared to formula-fed infants.”
From Diet and the Intestinal Microbiome: Associations, Functions, and Implications for Health and Disease (2014) · cites this paper as [6]
Aerobic organisms appear more prevalent in feces of breast-fed infants, while anaerobic and facultatively anaerobic organisms are more common in feces of formula-fed infants.
“aerobic organisms seem to be more prevalent in the feces of breast-fed infants, whereas anaerobic and facultatively anaerobic organisms, which preferentially use anerobic glycolysis, are more commonly found in the feces of formula-fed infants6.”
From Diet and the Intestinal Microbiome: Associations, Functions, and Implications for Health and Disease (2014) · cites this paper as [6]
Cites
The estimation of the bactericidal power of the blood
Miles, A. A., Misra, S. S., & Irwin, J. O. (1938) · Epidemiology and Infection · doi:10.1017/s002217240001158x · Cited by 3,619 · see citing works
Iron-binding Proteins in Milk and Resistance to Escherichia coli Infection in Infants
Bullen, J. J., Rogers, H. J., & Leigh, L. C. (1972) · BMJ · doi:10.1136/bmj.1.5792.69 · Cited by 651 · see citing works
Some current concepts in intestinal bacteriology
Moore, W., Cato, E., & Holdeman, L. V. (1978) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/31.10.s33 · Cited by 256 · see citing works
INTESTINAL COLONIZATION OF BREAST‐FED CHILDREN IN A RURAL AREA OF LOW SOCIOECONOMIC LEVEL*
Mata, L. J., & Urrutia, J. J. (1971) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1971.tb34996.x · Cited by 251 · see citing works
MITSUOKA, T., & Kaneuchi, C. (1977) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/30.11.1799 · Cited by 220 · see citing works
Bifidobacteria in the intestinal tract of infants: an in-vivo study
Bullen, C. L., TEARLE, P. V., & Willis, A. T. (1976) · Journal of Medical Microbiology · doi:10.1099/00222615-9-3-325 · Cited by 164 · see citing works
The Effect of "Humanised" Milks and Supplemented Breast Feeding on The Faecal Flora of Infants
Bullen, C. L., TEARLE, P. V., & STEWART, M. G. (1977) · Journal of Medical Microbiology · doi:10.1099/00222615-10-4-403 · Cited by 159 · see citing works
The normal colonic bacterial flora.
Hill, M. J., & Drašar, B. S. (1975) · Gut · doi:10.1136/gut.16.4.318 · Cited by 139 · see citing works
Infant feeding and infant mortality in rural Chile.
Plank, S. J., & Ml, M. (1973) · PubMed · Cited by 134 · see citing works
Longitudinal study of the morbidity of diarrheal and respiratory infections in malnourished children
James, J. (1972) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/25.7.690 · Cited by 126 · see citing works
BACTERIAL IRON METABOLISM IN INFECTION AND IMMUNITY
Bullen, J. J., Rogers, H. J., & Griffiths, E. (1974) · Elsevier eBooks · doi:10.1016/b978-0-12-515250-1.50025-4 · Cited by 104 · see citing works
Bacteria and the etiology of colonic cancer
Hill, M. J. (1974) · Cancer · doi:10.1002/1097-0142(197409)34:3+ · Cited by 104 · see citing works
Transport and Storage of Faeces for Bacteriological Examination
Crowther, J. S. (1971) · Journal of Applied Bacteriology · doi:10.1111/j.1365-2672.1971.tb02307.x · Cited by 103 · see citing works
The faecal flora of children in the United Kingdom
Ellis-Pegler, R. B., Crabtree, C. G., & LAMBERT, H. P. (1975) · Journal of Hygiene · doi:10.1017/s002217240004715x · Cited by 90 · see citing works
Some new media for the isolation and identification of clostridia
Willis, A. T., & Hobbs, G. (1959) · The Journal of Pathology and Bacteriology · doi:10.1002/path.1700770223 · Cited by 88 · see citing works
Breast-feeding and Salmonella Infection
France, G. L. (1980) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/archpedi.1980.02130140021007 · Cited by 78 · see citing works
THE MOUSE INTESTINAL MICROFLORA WITH EMPHASIS ON THE STRICT ANAEROBES
Lee, A., Gordon, J. H., Lee, C., & Dubos, R. J. (1971) · The Journal of Experimental Medicine · doi:10.1084/jem.133.2.339 · Cited by 74 · see citing works
Self-citationBifidobacteria in the intestinal tract of infants: an in-vitro study
Bullen, C. L., & TEARLE, P. V. (1976) · Journal of Medical Microbiology · doi:10.1099/00222615-9-3-335 · Cited by 46 · see citing works
Faecal flora of south indian infants and young children in health and with acute gastroenteritis
ALBERT, M. J., BHAT, P., RAJAN, D., MAIYA, P. P., PEREIRA, S. M., & BAKER, S. J. (1978) · Journal of Medical Microbiology · doi:10.1099/00222615-11-2-137 · Cited by 37 · see citing works
Hewitt, J. H., & Rigby, J. (1976) · Journal of Hygiene · doi:10.1017/s0022172400055601 · Cited by 36 · see citing works
The Relationship of Bottle Feeding to Malnutrition and Gastroenteritis in a Pre-Industrial Setting
Kanaaneh, H. (1972) · Journal of Tropical Pediatrics · doi:10.1093/tropej/18.4.302 · Cited by 35 · see citing works
DIARRHEAL DISEASE OF EARLY CHILDHOOD—WORLDWIDE SCOPE OF THE PROBLEM
Gordon, J. E. (1971) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1971.tb34988.x · Cited by 30 · see citing works
The Size, pH, and Redox Potential of the Cecum in Mice Associated with Various Microbial Floras
Celesk, R. A., Asano, T., & Wagner, M. (1976) · Experimental Biology and Medicine · doi:10.3181/00379727-151-39187 · Cited by 25 · see citing works
Incidence and treatment of infantile gastro-entritis in general practice.
Wheatley, D. (1968) · Archives of Disease in Childhood · doi:10.1136/adc.43.227.53 · Cited by 16 · see citing works
Gastroenteritis in London and Jamaica: a clinical and bacteriological study
Ellis-Pegler, R. B., Higgs, R. H., & LAMBERT, H. P. (1979) · Journal of Hygiene · doi:10.1017/s0022172400025523 · Cited by 6 · see citing works
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Diversity, stability and resilience of the human gut microbiota
Lozupone, C. A., Stombaugh, J. I., Gordon, J. I., Jansson, J. K., & Knight, R. (2012) · Nature · doi:10.1038/nature11550 · Cited by 5,533 · see citing works
Development of the Human Infant Intestinal Microbiota
Palmer, C., Bik, E. M., DiGiulio, D. B., Relman, D. A., & Brown, P. O. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050177 · Cited by 2,877 · see citing works
Factors 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
The role of gut microbiota in immune homeostasis and autoimmunity
Wu, H.-J., & Wu, E. (2012) · Gut Microbes · doi:10.4161/gmic.19320 · Cited by 1,426 · see citing works
Developmental microbial ecology of the neonatal gastrointestinal tract
Mackie, R. I., Sghir, A., & Gaskins, H. R. (1999) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/69.5.1035s · Cited by 1,360 · see citing works
Harmsen, H. J. M., Wildeboer-Veloo, A. C. M., Raangs, G. C., Wagendorp, A. A., Klijn, N., BINDELS, J. G., & Welling, G. W. (2000) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/00005176-200001000-00019 · Cited by 1,326 · see citing works
Early differences in fecal microbiota composition in children may predict overweight
Kalliomäki, M. A., Collado, M. C., Salminen, S., & Isolauri, E. (2008) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/87.3.534 · Cited by 1,056 · see citing works
Intestinal microbiota in functional bowel disorders: a Rome foundation report
Simrén, M., Barbara, G., Flint, H. J., Spiegel, B. M. R., Spiller, R. C., Vanner, S., Verdu, E. F., Whorwell, P. J., & Zoetendal, E. G. (2013) · Gut · doi:10.1136/gutjnl-2012-302167 · Cited by 939 · see citing works
Probiotics, prebiotics, and synbiotics: approaches for modulating the microbial ecology of the gut
COLLINS, M. D., & Gibson, G. R. (1999) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/69.5.1052s · Cited by 899 · see citing works
Grölund, M., Lehtonen, O. ‐., Eerola, E., & Kero, P. O. (1999) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/00005176-199901000-00007 · Cited by 873 · see citing works
Molecular Monitoring of Succession of Bacterial Communities in Human Neonates
Favier, C. F., Vaughan, E. E., de Vos, W. M., & Akkermans, A. D. L. (2002) · Applied and Environmental Microbiology · doi:10.1128/aem.68.1.219-226.2002 · Cited by 859 · see citing works
Dietary prebiotics: current status and new definition
Gibson, G. R., Scott, K. P., Rastall, R. A., Tuohy, K. M., Hotchkiss, A. T., Dubert‐Ferrandon, A., Gareau, M. G., Murphy, E. F., Saulnier, D. M. A., Loh, G., et al. (2010) · Food Science & Technology Bulletin Functional Foods · doi:10.1616/1476-2137.15880 · Cited by 784 · see citing works
Intestinal microflora in early infancy: composition and development
Fanaro, S., Chierici, R., Guerrini, P., & Vigi, V. (2003) · Acta Paediatrica · doi:10.1111/j.1651-2227.2003.tb00646.x · Cited by 738 · see citing works
Probiotic Spectra of Lactic Acid Bacteria (LAB)
Naidu, A. S., Bidlack, W. R., & Clemens, R. (1999) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408699991279187 · Cited by 690 · see citing works
Establishment of the gut microbiota in Western infants
Adlerberth, I., & Wold, A. E. (2009) · Acta Paediatrica · doi:10.1111/j.1651-2227.2008.01060.x · Cited by 665 · see citing works
Falk, P. G., Hooper, L. V., Midtvedt, T., & Gordon, J. I. (1998) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.62.4.1157-1170.1998 · Cited by 643 · see citing works
Burger-van Paassen, N., Vincent, A., Puiman, P. J., van der Sluis, M., Bouma, J., Boehm, G., van Goudoever, J. B., van Seuningen, I., & Renes, I. B. (2009) · Biochemical Journal · doi:10.1042/bj20082222 · Cited by 611 · see citing works
A Model of Host-Microbial Interactions in an Open Mammalian Ecosystem
Bry, L., Falk, P. G., Midtvedt, T., & Gordon, J. I. (1996) · Science · doi:10.1126/science.273.5280.1380 · Cited by 607 · see citing works
Diet and the Intestinal Microbiome: Associations, Functions, and Implications for Health and Disease
Albenberg, L. G., & Wu, G. D. (2014) · Gastroenterology · doi:10.1053/j.gastro.2014.01.058 · Cited by 606 · see citing works
Intestinal Bacteria and the Regulation of Immune Cell Homeostasis
Hill, D. A., & Artis, D. (2010) · Annual Review of Immunology · doi:10.1146/annurev-immunol-030409-101330 · Cited by 586 · see citing works
Hopkins, M. J., Sharp, R., & Macfarlane, G. T. (2001) · Gut · doi:10.1136/gut.48.2.198 · Cited by 577 · 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
The role of microbiota in infectious disease
Stecher, B., & Hardt, W. (2008) · Trends in Microbiology · doi:10.1016/j.tim.2007.12.008 · Cited by 533 · see citing works
Bergström, A., Skov, T. H., Bahl, M. I., Roager, H. M., Christensen, L. B., Ejlerskov, K. T., Mølgaard, C., Michaelsen, K. F., & Licht, T. R. (2014) · Applied and Environmental Microbiology · doi:10.1128/aem.00342-14 · Cited by 532 · see citing works
Modulation of intestinal barrier by intestinal microbiota: Pathological and therapeutic implications
Natividad, J. M. M., & Verdu, E. F. (2013) · Pharmacological Research · doi:10.1016/j.phrs.2012.10.007 · Cited by 525 · see citing works
Ecological control of the gastrointestinal tract. The role of probiotic flora
Bengmark, S. (1998) · Gut · doi:10.1136/gut.42.1.2 · Cited by 505 · see citing works
Metarhizium spp., Cosmopolitan Insect-Pathogenic Fungi: Mycological Aspects
Roberts, D. W., & Leger, R. J. S. (2004) · Advances in applied microbiology · doi:10.1016/s0065-2164(04)54001-7 · Cited by 474 · see citing works
From Structure to Function: the Ecology of Host-Associated Microbial Communities
Robinson, C. J., Bohannan, B. J. M., & Young, V. B. (2010) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00014-10 · Cited by 454 · see citing works
Bezirtzoglou, E., Tsiotsias, A., & Welling, G. W. (2011) · Anaerobe · doi:10.1016/j.anaerobe.2011.03.009 · Cited by 453 · see citing works
Reduced diversity in the early fecal microbiota of infants with atopic eczema
Wang, M., Karlsson, C., Olsson, C., Adlerberth, I., Wold, A. E., Strachan, D. P., Martricardi, P. M., Åberg, N., Perkin, M. R., Tripodi, S., et al. (2007) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2007.09.011 · Cited by 434 · see citing works
Martı́n, R., Jiménez, E., Heilig, H. G. H. J., Fernández, L., Marín, M. L., Zoetendal, E. G., & Rodríguez, J. M. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.02063-08 · Cited by 434 · see citing works
The role of the intestinal microbiota in type 1 diabetes mellitus
Knip, M., & Siljander, H. (2016) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2015.218 · Cited by 434 · see citing works
Benno, Y., Sawada, K., & MITSUOKA, T. (1984) · Microbiology and Immunology · doi:10.1111/j.1348-0421.1984.tb00754.x · Cited by 432 · see citing works
The microbiome and gut homeostasis
Lee, J., Tsolis, R. M., & Bäumler, A. J. (2022) · Science · doi:10.1126/science.abp9960 · Cited by 430 · see citing works
Meta-analyses of studies of the human microbiota
Lozupone, C. A., Stombaugh, J., Gonzalez, A., Ackermann, G., Wendel, D., Vázquez-Baeza, Y., Jansson, J. K., Gordon, J. I., & Knight, R. (2013) · Genome Research · doi:10.1101/gr.151803.112 · Cited by 424 · see citing works
Cresci, G., & Bawden, E. (2015) · Nutrition in Clinical Practice · doi:10.1177/0884533615609899 · Cited by 424 · see citing works
Knol, J., Scholtens, P. A. M. J., Kafka, C., Steenbakkers, J., Gro, S., Helm, K., Klarczyk, M., pfer, H. S., ckler, H.-M. B., & Wells, J. (2004) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/00005176-200501000-00007 · Cited by 422 · see citing works
Woodmansey, E. J., McMurdo, M. E. T., Macfarlane, G. T., & Macfarlane, S. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.10.6113-6122.2004 · Cited by 418 · see citing works
Liévin, V, Peiffer, I., Hudault, S., Rochat, F., Brassart, D., Neeser, J.-R., & Servin, A. L. (2000) · Gut · doi:10.1136/gut.47.5.646 · Cited by 397 · 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
Penders, J., Vink, C., Driessen, C., London, N. H. H. J., Thijs, C. T., & Stobberingh, E. E. (2004) · FEMS Microbiology Letters · doi:10.1016/j.femsle.2004.11.052 · Cited by 380 · see citing works
Thomas, S., Izard, J., Walsh, E. K., Batich, K. A., Chongsathidkiet, P., Clarke, G. A., Sela, D. A., Muller, A. J., Mullin, J. M., Albert, K., et al. (2017) · Cancer Research · doi:10.1158/0008-5472.can-16-2929 · Cited by 369 · see citing works
Effect of Breast and Formula Feeding on Gut Microbiota Shaping in Newborns
Guaraldi, F., & Salvatori, G. (2012) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2012.00094 · Cited by 365 · see citing works
Kirjavainen, P. V., Arvola, T., Salminen, S., & Isolauri, E. (2002) · Gut · doi:10.1136/gut.51.1.51 · Cited by 354 · see citing works
Rebuilding the Gut Microbiota Ecosystem
Gagliardi, A., Totino, V., Cacciotti, F., Iebba, V., Neroni, B., Bonfiglio, G., Trancassini, M., Passariello, C., Pantanella, F., & Schippa, S. (2018) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph15081679 · Cited by 340 · see citing works
Prenatal Stress Alters Bacterial Colonization of the Gut in Infant Monkeys
Bailey, M. T., Lubach, G. R., & Coe, C. L. (2004) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/00005176-200404000-00009 · Cited by 339 · see citing works
Murdoch, D. A. (1998) · Clinical Microbiology Reviews · doi:10.1128/cmr.11.1.81 · Cited by 335 · see citing works
New Insights in Gut Microbiota Establishment in Healthy Breast Fed Neonates
Jost, T., Lacroix, C., Braegger, C., & Chassard, C. (2012) · PLoS ONE · doi:10.1371/journal.pone.0044595 · Cited by 331 · see citing works
Intestinal microbiota influence the early postnatal development of the enteric nervous system
Collins, J., Borojevic, R., Verdu, E. F., Huizinga, J. D., & Ratcliffe, E. M. (2014) · Neurogastroenterology & Motility · doi:10.1111/nmo.12236 · Cited by 318 · see citing works
The Prevalence and Control of Bacillus and Related Spore-Forming Bacteria in the Dairy Industry
Gopal, N., Hill, C., Ross, R. P., Beresford, T. P. J., Fenelon, M. A., & Cotter, P. D. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.01418 · Cited by 318 · see citing works
Adlerberth, I., Lindberg, E., Åberg, N., Hesselmar, B., Saalman, R., Strannegård, I., & Wold, A. E. (2005) · Pediatric Research · doi:10.1203/01.pdr.0000191137.12774.b2 · Cited by 317 · see citing works
The Human Microbiome and Its Potential Importance to Pediatrics
Johnson, C. L., & Versalovic, J. A. (2012) · PEDIATRICS · doi:10.1542/peds.2011-2736 · Cited by 310 · see citing works
Jangi, S., & LaMont, J. T. (2010) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0b013e3181d29767 · Cited by 306 · see citing works
Azad, M. B., Konya, T., Maughan, H., Guttman, D. S., Field, C. J., Sears, M. R., Becker, A. B., Scott, J. A., Kozyrskyj, A. L., & CHILD Study Investigators (2013) · Allergy Asthma and Clinical Immunology · doi:10.1186/1710-1492-9-15 · Cited by 305 · see citing works
Effects of the gut microbiota on obesity and glucose homeostasis
Greiner, T. U., & Bäckhed, F. (2011) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2011.01.002 · Cited by 304 · see citing works
Yang, I. H., Corwin, E. J., Brennan, P. A., Jordan, S., Murphy, J. R., & Dunlop, A. L. (2015) · Nursing Research · doi:10.1097/nnr.0000000000000133 · Cited by 283 · see citing works
Genomic Insights into Bifidobacteria
Lee, J.-H., & O’Sullivan, D. J. (2010) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00004-10 · Cited by 282 · see citing works
Gut microbiota: Changes throughout the lifespan from infancy to elderly
O’Toole, P. W., & Claesson, M. J. (2009) · International Dairy Journal · doi:10.1016/j.idairyj.2009.11.010 · Cited by 279 · see citing works
The Non-O157 Shiga-Toxigenic (Verocytotoxigenic)Escherichia coli; Under-Rated Pathogens
Bettelheim, K. A. (2007) · Critical Reviews in Microbiology · doi:10.1080/10408410601172172 · Cited by 278 · see citing works
Walker, A. W., Martin, J. C., Scott, P., Parkhill, J., Flint, H. J., & Scott, K. P. (2015) · Microbiome · doi:10.1186/s40168-015-0087-4 · Cited by 273 · see citing works
How biological sex of the host shapes its gut microbiota
Valeri, F., & Endres, K. (2021) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2021.100912 · Cited by 267 · see citing works
Nishino, R., Mikami, K., Takahashi, H., Tomonaga, S., Furuse, M., Hiramoto, T., Aiba, Y., Koga, Y., & Sudo, N. (2013) · Neurogastroenterology & Motility · doi:10.1111/nmo.12110 · Cited by 266 · see citing works
Nyangale, E. P., Mottram, D. S., & Gibson, G. R. (2012) · Journal of Proteome Research · doi:10.1021/pr300637d · Cited by 265 · see citing works
Wold, A. E. (1998) · Allergy · doi:10.1111/j.1398-9995.1998.tb04953.x · Cited by 263 · see citing works
Diet and faecal flora in the newborn: breast milk and infant formula
Balmer, S. E., & Wharton, B. A. (1989) · Archives of Disease in Childhood · doi:10.1136/adc.64.12.1672 · Cited by 254 · see citing works
Microbes, immunity, and behavior: psychoneuroimmunology meets the microbiome
Dinan, T. G., & Cryan, J. F. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2016.103 · Cited by 246 · see citing works
Rose, E. C., Odle, J., Blikslager, A. T., & Ziegler, A. L. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22136729 · Cited by 253 · see citing works
Factors Affecting Gastrointestinal Microbiome Development in Neonates
Chong, C. Y. L., Bloomfield, F. H., & O'Sullivan, J. M. (2018) · Nutrients · doi:10.3390/nu10030274 · Cited by 250 · see citing works
Variation in human intestinal microbiota with age
Hopkins, M. J., Sharp, R., & Macfarlane, G. T. (2002) · Digestive and Liver Disease · doi:10.1016/s1590-8658(02)80157-8 · Cited by 249 · see citing works
Devriese, L. A., & Pot, B. (1995) · Springer eBooks · doi:10.1007/978-1-4615-5817-0_10 · Cited by 246 · see citing works
(2006) · Wiley eBooks · doi:10.1002/9780470995785 · Cited by 240 · see citing works
Effects of Administration of TOS and Bifidobacterium breve 4006 on the Human Fecal Flora
Tanaka, R., Takayama, H., Morotomi, M., Kuroshima, T., Ueyama, S., Matsumoto, K. T., Kuroda, A., & Mutai, M. (1983) · Bifidobacteria and Microflora · doi:10.12938/bifidus1982.2.1_17 · Cited by 238 · see citing works
Comparative Metagenomics and Population Dynamics of the Gut Microbiota in Mother and Infant
Vaishampayan, P., Kuehl, J. V., Froula, J. L., Morgan, J. L., Ochman, H., & Francino, M. P. (2010) · Genome Biology and Evolution · doi:10.1093/gbe/evp057 · Cited by 236 · see citing works
Composition of the early intestinal microbiota
Fouhy, F., Ross, R. P., Fitzgerald, G. F., Stanton, C., & Cotter, P. D. (2012) · Gut Microbes · doi:10.4161/gmic.20169 · Cited by 234 · see citing works
Hudault, S. (2001) · Gut · doi:10.1136/gut.49.1.47 · Cited by 225 · see citing works
Thompson, C. L., Wang, B., & Holmes, A. J. (2008) · The ISME Journal · doi:10.1038/ismej.2008.29 · Cited by 223 · see citing works
Factors controlling the bacterial colonization of the intestine in breastfed infants
Orrhage, K., & Nord, C. E. (1999) · Acta Paediatrica · doi:10.1111/j.1651-2227.1999.tb01300.x · Cited by 223 · see citing works
The Early Settlers: Intestinal Microbiology in Early Life
Scholtens, P. A. M. J., Oozeer, R., Martı́n, R., Amor, K. B., & Knol, J. (2012) · Annual Review of Food Science and Technology · doi:10.1146/annurev-food-022811-101120 · Cited by 220 · see citing works
Human milk provides peptides highly stimulating the growth of bifidobacteria
Liepke, C., Adermann, K., Raida, M., Mägert, H., Forssmann, W., & Zucht, H. (2002) · European Journal of Biochemistry · doi:10.1046/j.0014-2956.2001.02712.x · Cited by 219 · see citing works
Hekmat, S., & McMahon, D. J. (1992) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(92)77895-3 · Cited by 218 · see citing works
Sasso, J. M., Ammar, R. M., Tenchov, R., Lemmel, S. A., Kelber, O., Grieswelle, M., & Zhou, Q. A. (2023) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.3c00127 · Cited by 218 · see citing works
Munyaka, P. M., Khafipour, E., & Ghia, J. (2014) · Frontiers in Pediatrics · doi:10.3389/fped.2014.00109 · Cited by 215 · see citing works
Oligosaccharides in Human Milk and Bacterial Colonization
Newburg, D. S. (2000) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/00005176-200000002-00003 · Cited by 212 · see citing works
The intestinal microbiota and obesity
Kallus, S. J., & Brandt, L. J. (2012) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0b013e31823711fd · Cited by 210 · see citing works
Intestinal microflora of human infants and current trends for its nutritional modulation
Mountzouris, K. C., McCartney, A. L., & Gibson, G. R. (2002) · British Journal Of Nutrition · doi:10.1079/bjnbjn2002563 · Cited by 207 · see citing works
Perspectives on the role of the human gut microbiota and its modulation by pro- and prebiotics
Steer, T. E., Carpenter, H., Tuohy, K. M., & Gibson, G. R. (2000) · Nutrition Research Reviews · doi:10.1079/095442200108729089 · Cited by 201 · see citing works
Griffiths, E. A., Duffy, L. C., Schanbacher, F. L., Qiao, H., Dryja, D., Leavens, A., Rossman, J., Rich, G. A., DiRienzo, D. B., & Ogra, P. L. O. (2004) · Digestive Diseases and Sciences · doi:10.1023/b:ddas.0000026302.92898.ae · Cited by 197 · see citing works
Microbiological and technological aspects of milks fermented by bifidobacteria
Tamime, A. Y., Marshall, V. M., & Robinson, R. K. (1995) · Journal of Dairy Research · doi:10.1017/s002202990003377x · Cited by 197 · see citing works
Development of bacterial and bifidobacterial communities in feces of newborn babies
Favier, C. F., de Vos, W. M., & Akkermans, A. D. L. (2003) · Anaerobe · doi:10.1016/j.anaerobe.2003.07.001 · Cited by 194 · see citing works
Rousseau, C., Poilane, I., de Pontual, L., Maherault, A.-C., Monnier, A. L., & Collignon, A. (2012) · Clinical Infectious Diseases · doi:10.1093/cid/cis637 · Cited by 192 · see citing works
Protective Nutrients and Bacterial Colonization in the Immature Human Gut
Dai, D., & Walker, W. A. (1999) · Advances in Pediatrics · doi:10.1016/s0065-3101(24)00035-5 · Cited by 192 · see citing works
Insights into the taxonomy, genetics and physiology of bifidobacteria
Ventura, M., van Sinderen, D., Fitzgerald, G. F., & Zink, R. (2004) · Antonie van Leeuwenhoek · doi:10.1023/b:anto.0000047930.11029.ec · Cited by 190 · see citing works
Nowrouzian, F. L., Wold, A. E., & Adlerberth, I. (2005) · The Journal of Infectious Diseases · doi:10.1086/427996 · Cited by 189 · see citing works
Goldin, B. R., & Gorbach, S. L. (1992) · Springer eBooks · doi:10.1007/978-94-011-2364-8_13 · Cited by 184 · see citing works
Hopkins, M. J., & Macfarlane, G. T. (2003) · Applied and Environmental Microbiology · doi:10.1128/aem.69.4.1920-1927.2003 · Cited by 183 · see citing works
Adaptation of Bacteria to the Intestinal Niche: Probiotics and Gut Disorder
Dunne, C. P. (2001) · Inflammatory Bowel Diseases · doi:10.1097/00054725-200105000-00010 · Cited by 182 · see citing works
Butel, M. J., Roland, N., Hibert, A., Popot, F., Favre, A., Tessèdre, A., Bensaada, M., Rimbault, A., & Szylit, O. (1998) · Journal of Medical Microbiology · doi:10.1099/00222615-47-5-391 · Cited by 181 · see citing works
Kleessen, B., Bunke, H., Tovar, K., Noack, J., & Sawatzki, G. (1995) · Acta Paediatrica · doi:10.1111/j.1651-2227.1995.tb13567.x · Cited by 179 · see citing works
Human gut microbiota: Does diet matter?
Maukonen, J., & Saarela, M. (2015) · Proceedings of The Nutrition Society · doi:10.1017/s0029665114000688 · Cited by 177 · see citing works
Nowrouzian, F., Hesselmar, B., Saalman, R., Strannegård, I.-L., Åberg, N., Wold, A. E., & Adlerberth, I. (2003) · Pediatric Research · doi:10.1203/01.pdr.0000069843.20655.ee · Cited by 176 · see citing works
- Authors
- Stark, P. L., & Lee, A.
- Affiliations
- UNSW Sydney (AU)
- Venue
- Journal of Medical Microbiology
- Publisher
- Microbiology Society
- Published
- 1982-05-01
- Volume
- 15
- Issue
- 2
- Pages
- 189-203
- ISSN
- 0022-2615 (ISSN-L)
- 1473-5644
- OpenAlex
- W2131291912
- Cited by
- 616
- References
- 25
- Citations by year
- 2026: 2 · 2025: 10 · 2024: 7 · 2023: 18 · 2022: 14 · 2021: 16 · 2020: 17 · 2019: 16 · 2018: 21 · 2017: 15 · 2016: 22 · 2015: 22 · 2014: 25 · 2013: 26 · 2012: 36
- FWCI
- 6.91
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Medical Microbiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Nursing › Nutrition and Dietetics › Infant Nutrition and Health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Keywords
- infant gut microbiota, breastfeeding, infant formula, large bowel, bacterial community succession, Bifidobacterium, Enterobacteriaceae, Enterococcus, Bacteroides, Clostridia, anaerobic streptococci, facultative anaerobes, solid food introduction, infant nutrition
- MeSH terms
- Actinomycetaceae, Aerobiosis, Aging, Anaerobiosis, Bacteroides, Bottle Feeding, Breast Feeding, Clostridium, Enterobacteriaceae, Feces, Humans, Infant, Infant, Newborn, Intestine, Large, Prospective Studies
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