Diet Influences the Oral Microbiota of Infants during the First Six Months of Life

Nutrients - Tập 12 Số 11 - Trang 3400
Patrícia M Oba1, Hannah D. Holscher2,3, Rose Ann Mathai4, Juhee Kim5, Kelly S. Swanson1,3
1Department of Animal Sciences, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA,
2Department of Food Science and Human Nutrition, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA
3Division of Nutritional Sciences, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA
4Department of Nutrition, Dominican University, River Forest, IL 60305, USA
5Department of Nutrition, East Carolina State University, Greenville, NC 27834, USA

Tóm tắt

Background: Oral microorganisms contribute to oral health and disease, but few have studied how infant feeding methods affect their establishment. Methods: Infant (n = 12) feeding records and tongue and cheek swabs were collected within 48 h of birth, and after 2, 4, and 6 mo. DNA was extracted from samples, bacterial and fungal amplicons were generated and sequenced using Illumina MiSeq, and sequences were analyzed using Quantitative Insights Into Microbial Ecology (QIIME) and Statistical Analysis System (SAS) to evaluate differences over time and among breast-fed, formula-fed, mixed-fed, and solid food-fed infants. Results: Considering all time points, breast milk- and mixed-fed infants had lower oral species richness than solid food-fed infants (p = 0.006). Regardless of feeding mode, species richness was lower at birth than at other time points (p = 0.006). Principal coordinates analysis (PCoA) of unique fraction metric (UniFrac) distances indicated that bacterial communities were impacted by feeding method (p < 0.005). Considering all time points, breast-fed infants had higher Streptococcus, while formula-fed infants had higher Actinomyces and Prevotella. Regardless of feeding mode, Propionibacterium, Porphyromonas, Prevotella, Gemella, Granulicatella, Veillonella, Fusobacterium, Leptotrichia, Neisseria, and Haemophilus increased with age, while Cloacibacterium and Dechloromonas decreased with age. Oral fungi were detected in infants but were not impacted by diet. Conclusions: These findings demonstrate that the establishment of oral bacteria depends on dietary composition and age. More research is necessary to determine whether this affects risk of oral caries and other health outcomes later in life.

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Tài liệu tham khảo

Ballard, 2013, Human milk composition: Nutrients and bioactive factors, Pediatr. Clin. N. Am., 60, 49, 10.1016/j.pcl.2012.10.002

Jeurink, 2013, Human milk: A source of more life than we imagine, Benef. Microbes, 4, 17, 10.3920/BM2012.0040

Hunt, K.M., Foster, J.A., Forney, L.J., Schütte, U.M.E., Beck, D.L., Abdo, Z., Fox, L.K., Williams, J.E., Mcguire, M.K., and Mcguire, M.A. (2011). Characterization of the diversity and temporal stability of bacterial communities in human milk. PLoS ONE, 6.

Street, 2016, Bacterial microbiome of breast milk and child saliva from low-income Mexican-American women and children, Pediatr. Res., 79, 846, 10.1038/pr.2016.9

Cephas, K.D., Kim, J., Mathai, R.A., Barry, K.A., Dowd, S.E., Meline, B.S., and Swanson, K.S. (2011). Comparative analysis of salivary bacterial microbiome diversity in edentulous infants and their mothers or primary care givers using pyrosequencing. PLoS ONE, 6.

Aagaard, 2014, The placenta harbors a unique microbiome, Sci. Transl. Med., 6, 237ra65

Bearfield, 2002, Possible association between amniotic fluid micro-organism infection and microflora in the mouth, BJOG, 109, 527

Odriozola, 2005, Isolation of commensal bacteria from umbilical cord blood of healthy neonates born by cesarean section, Curr. Microbiol., 51, 270, 10.1007/s00284-005-0020-3

Stout, 2013, Identification of intracellular bacteria in the basal plate of the human placenta in term and preterm gestations, Am. J. Obstet. Gynecol., 208, 226.e1, 10.1016/j.ajog.2013.01.018

2014, Acquisition and maturation of oral microbiome throughout childhood: An update, Dent. Res. J., 11, 291

Costello, 2010, Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns, Proc. Natl. Acad. Sci. USA, 107, 11971, 10.1073/pnas.1002601107

Harnevik, 2011, Mode of birth delivery affects oral microbiota in infants, J. Dent. Res., 90, 1183, 10.1177/0022034511418973

Roswall, 2015, Dynamics and stabilization of the human gut microbiome during the first year of life resource dynamics and stabilization of the human gut microbiome during the first year of life, Cell Host Microbe, 17, 690, 10.1016/j.chom.2015.04.004

Filippidi, 2014, The effect of maternal flora on Candida colonisation in the neonate, Mycoses, 57, 43, 10.1111/myc.12100

Holgerson, 2013, Oral microbial profile discriminates breast-fed from formula-fed infants, J. Pediatr. Gastroenterol. Nutr., 56, 127, 10.1097/MPG.0b013e31826f2bc6

Moossavi, 2019, Composition and variation of the human milk microbiota are influenced by maternal and early-life factors, Cell Host Microbe, 25, 324, 10.1016/j.chom.2019.01.011

Araujo, 2014, Interindividual variability and intraindividual stability of oral fungal microbiota over time, Med. Mycol., 52, 498, 10.1093/mmy/myu027

Araujo, 2013, Characterization of the oral fungal microbiota in smokers and non-smokers, Eur. J. Oral Sci., 121, 132, 10.1111/eos.12030

Ghannoum, M.A., Jurevic, R.J., Mukherjee, P.K., Cui, F., Sikaroodi, M., Naqvi, A., and Gillevet, P.M. (2010). Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. Plos Pathog., 6.

Payne, 2016, Detection of Candida spp. in the vagina of a cohort of nulliparous pregnant women by culture and molecular methods: Is there an association between maternal vaginal and infant oral colonisation ?, Aust. N. Z. J. Obstet. Gynaecol., 56, 179, 10.1111/ajo.12409

Kraneveld, E.A., Buijs, M.J., Bonder, M.J., Visser, M., Keijser, B.J., Crielaard, W., and Zaura, E. (2012). The relation between oral candida load and bacterial microbiome profiles in Dutch older adults. PLoS ONE, 7.

Socransky, 2002, Dental biofilms: Difficult therapeutic targets, Periodontol. 2000, 28, 12, 10.1034/j.1600-0757.2002.280102.x

Segata, N., Haake, S., Mannon, P., Lemon, K.P., Waldron, L., Gevers, D., Huttenhower, C., and Izard, J. (2012). Composition of the adult digestive tract bacterial microbiome based on seven mouth surfaces, tonsils, throat and stool samples. Genome Biol., 13.

Klimesova, K., Jiraskova Zakostelska, Z., and Tlaskalova-Hogenova, H. (2018). Oral bacterial and fungal microbiome impacts colorectal carcinogenesis. Front. Microbiol., 9.

Trojanowska, 2010, The role of Candida in inflammatory bowel disease. Estimation of transmission of C. albicans fungi in gastrointestinal tract based on genetic affinity between strains, Med. Sci. Monit., 16, CR451

Walther-António, M.R.S., Jeraldo, P., Berg Miller, M.E., Yeoman, C.J., Nelson, K.E., Wilson, B.A., White, B.A., Chia, N., and Creedon, D.J. (2014). Pregnancy’s stronghold on the vaginal microbiome. PLoS ONE, 9.

Schoch, 2012, Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi, Proc. Natl. Acad. Sci. USA, 109, 6241, 10.1073/pnas.1117018109

Caporaso, 2010, QIIME allows analysis of high-throughput community sequencing data, Nat. Methods, 7, 335, 10.1038/nmeth.f.303

Edgar, 2010, Search and clustering orders of magnitude faster than BLAST, Bioinformatics, 26, 2460, 10.1093/bioinformatics/btq461

DeSantis, 2006, Greengenes, a Chimera-Checked 16S rRNA gene database and workbench compatible with ARB, Appl. Environ. Microbiol., 72, 5069, 10.1128/AEM.03006-05

Lozupone, 2005, UniFrac: A new phylogenetic method for comparing microbial communities, Appl. Environ. Microbiol., 71, 8228, 10.1128/AEM.71.12.8228-8235.2005

Bender, 2001, Adjusting for multiple testing—when and how?, J. Clin. Epidemiol., 54, 343, 10.1016/S0895-4356(00)00314-0

Sweeney, 2016, Deep sequencing of the 16S ribosomal RNA of the neonatal oral microbiome: A comparison of breast-fed and formula-fed infants, Sci. Rep., 6, 38309, 10.1038/srep38309

Costello, E.K., Carlisle, E.M., Bik, E.M., Morowitz, M.J., and Relman, D.A. (2013). Microbiome assembly across multiple body sites in low-birthweight infants. mBio, 4.

Ling, 2010, Analysis of oral microbiota in children with dental caries by PCR-DGGE and barcoded pyrosequencing, Microb. Ecol., 60, 677, 10.1007/s00248-010-9712-8

Lazarevic, 2009, Metagenomic study of the oral microbiota by Illumina high-throughput sequencing, J. Microbiol. Methods, 79, 266, 10.1016/j.mimet.2009.09.012

Keijser, 2008, Pyrosequencing analysis of the oral microflora of healthy adults, J. Dent. Res., 87, 1016, 10.1177/154405910808701104

Bryk, 2002, Establishment of streptococci in the upper respiratory tract: Longitudinal changes in the mouth and nasopharynx up to 2 years of age, J. Med. Microbiol., 51, 723, 10.1099/0022-1317-51-9-723

Asikainen, 1992, The early colonization of gram-negative anaerobic bacteria in edentulous infants, Oral Microbiol. Immunol., 7, 28, 10.1111/j.1399-302X.1992.tb00016.x

Asikainen, 1994, The oral gram-negative anaerobic microflora in young children: Longitudinal changes from edentulous to dentate mouth, Oral Microbiol. Immunol., 9, 136, 10.1111/j.1399-302X.1994.tb00049.x

Kolenbrander, 2010, Oral multispecies biofilm development and the key role of cell–cell distance, Nat. Rev. Microbiol., 8, 471, 10.1038/nrmicro2381

Collado, 2009, Assessment of the bacterial diversity of breast milk of healthy women by quantitative real-time PCR, Lett. Appl. Microbiol., 48, 523, 10.1111/j.1472-765X.2009.02567.x

Aas, 2008, Bacteria of dental caries in primary and permanent teeth in children and young adults, J. Clin. Microbiol., 46, 1407, 10.1128/JCM.01410-07

Mantzourani, 2009, The isolation of bifidobacteria from occlusal carious lesions in children and adults, Caries Res., 43, 308, 10.1159/000222659

Kanasi, 2010, Clonal analysis of the microbiota of severe early childhood caries, Caries Res., 44, 485, 10.1159/000320158

Tanner, 2011, Cultivable Anaerobic microbiota of severe early childhood caries, J. Clin. Microbiol., 49, 1464, 10.1128/JCM.02427-10

Tham, 2015, Breastfeeding and the risk of dental caries: A systematic review and meta-analysis, Acta Paediatr., 104, 62, 10.1111/apa.13118

Hegde, 1998, Influence of the maternal vaginal microbiota on the oral microbiota of the newborn, J. Clin. Pediatr. Dent., 22, 317

Bagg, J., MacFarlane, T.W., Poxton, I.R., and Smith, A.J. (2006). Essentials of Microbiology for Dental Students, Oxford University Press.

Peters, B.A., Wu, J., Hayes, R.B., and Ahn, J. (2017). The oral fungal mycobiome: Characteristics and relation to periodontitis in a pilot study. BMC Microbiol.

Dinleyici, 2020, Human milk mycobiota composition: Relationship with gestational age, delivery mode, and birth weight, Benef. Microbes, 11, 151, 10.3920/BM2019.0158