Oral microbiome and obesity in a large study of low-income and African-American populations

ABSTRACT Few studies have evaluated the relationship of oral microbiome with obesity. We investigated the oral microbiome among 647 obese and 969 non-obese individuals from the Southern Community Cohort Study, through 16S rRNA gene sequencing in mouth rinse samples. We first investigated 16 taxa in two probiotic genera, Bifidobacterium and Lactobacillus. Among them, eight showed nominal associations with obesity (P < 0.05). Especially, Bifidobacterium (odds ratio [OR] = 0.67, 95% confidence interval [CI]:0.54, 0.83) and Bifidobacterium longum (OR = 0.57, 95% CI: 0.45, 0.73) were significantly associated with decreased obesity prevalence with false-discovery rate (FDR)-corrected P of 0.01 and 5.41 × 10−4, respectively. Multiple other bacterial taxa were also significantly associated with obesity prevalence at FDR-corrected P < 0.05. Among them, five in Firmicutes and two respectively in Actinobacteria and Proteobacteria were significantly associated with increased obesity prevalence. Significant associations with decreased obesity prevalence were observed for two taxa respectively in Actinobacteria and Firmicutes. Most of these taxa were associated with body mass index at study enrollment and weight gain during adulthood. Also, most of these associations were observed in both European- and African-Americans. Our findings indicate that multiple oral bacterial taxa, including several probiotic taxa, were significantly associated with obesity.

[1]  Sergey I. Nikolenko,et al.  BayesHammer: Bayesian clustering for error correction in single-cell sequencing , 2012, BMC Genomics.

[2]  W. Wade,et al.  The oral microbiome in health and disease. , 2013, Pharmacological research.

[3]  F. Matsuda,et al.  Evaluation of a probiotics, Bifidobacterium breve BBG-01, for enhancement of immunogenicity of an oral inactivated cholera vaccine and safety: a randomized, double-blind, placebo-controlled trial in Bangladeshi children under 5 years of age. , 2011, Vaccine.

[4]  C. Genco,et al.  Immune dysregulation mediated by the oral microbiome: potential link to chronic inflammation and atherosclerosis , 2016, Journal of internal medicine.

[5]  R. Burne,et al.  Fueling the caries process: carbohydrate metabolism and gene regulation by Streptococcus mutans , 2014, Journal of oral microbiology.

[6]  Tadashi Sato,et al.  Effect of Probiotics, Bifidobacterium breve and Lactobacillus casei, on Bisphenol A Exposure in Rats , 2008, Bioscience, biotechnology, and biochemistry.

[7]  Kunyan Zhang,et al.  Gemella bergeriae Endocarditis Diagnosed by Sequencing of rRNA Genes in Heart Valve Tissue , 2004, Journal of Clinical Microbiology.

[8]  A. B. Cinar,et al.  Interrelation between obesity, oral health and life-style factors among Turkish school children , 2011, Clinical Oral Investigations.

[9]  M. Zarrati,et al.  Relationship between probiotic consumption and IL-10 and IL-17 secreted by PBMCs in overweight and obese people. , 2013, Iranian journal of allergy, asthma, and immunology.

[10]  M. Bernardeau,et al.  Safety and efficacy of probiotic lactobacilli in promoting growth in post-weaning Swiss mice. , 2002, International journal of food microbiology.

[11]  William A. Walters,et al.  Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms , 2012, The ISME Journal.

[12]  T. Sobko,et al.  Microbiota in the Oral Subgingival Biofilm Is Associated With Obesity in Adolescence , 2012, Obesity.

[13]  Hongzhe Li,et al.  Testing in Microbiome-Profiling Studies with MiRKAT, the Microbiome Regression-Based Kernel Association Test. , 2015, American journal of human genetics.

[14]  A. Ogawa,et al.  Anti-obesity effect of Lactobacillus gasseri SBT2055 accompanied by inhibition of pro-inflammatory gene expression in the visceral adipose tissue in diet-induced obese mice , 2013, European Journal of Nutrition.

[15]  S. Prakash,et al.  Lactobacillus fermentum and Lactobacillus amylovorus as probiotics alter body adiposity and gut microflora in healthy persons , 2013 .

[16]  William A. Walters,et al.  Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample , 2010, Proceedings of the National Academy of Sciences.

[17]  C. Perronne,et al.  Actinomyces graevenitzii pulmonary abscess mimicking tuberculosis in a healthy young man. , 2014, Canadian respiratory journal.

[18]  Hui-Young Lee,et al.  Human originated bacteria, Lactobacillus rhamnosus PL60, produce conjugated linoleic acid and show anti-obesity effects in diet-induced obese mice. , 2006, Biochimica et biophysica acta.

[19]  Jonathan Friedman,et al.  Inferring Correlation Networks from Genomic Survey Data , 2012, PLoS Comput. Biol..

[20]  S. Rane,et al.  Beneficial Metabolic Effects of a Probiotic via Butyrate-induced GLP-1 Hormone Secretion* , 2013, The Journal of Biological Chemistry.

[21]  William A. Walters,et al.  QIIME allows analysis of high-throughput community sequencing data , 2010, Nature Methods.

[22]  K. Flegal,et al.  Prevalence of Childhood and Adult Obesity in the United States, 2011–2012 , 2014 .

[23]  N. Boutagy,et al.  Probiotic supplementation attenuates increases in body mass and fat mass during high‐fat diet in healthy young adults , 2015, Obesity.

[24]  D. Savage.  Microbial ecology of the gastrointestinal tract. , 1977, Annual review of microbiology.

[25]  Liping Zhao.  The gut microbiota and obesity: from correlation to causality , 2013, Nature Reviews Microbiology.

[26]  M. Cha,et al.  Antiobesity and lipid-lowering effects of Bifidobacterium spp. in high fat diet-induced obese rats , 2011, Lipids in Health and Disease.

[27]  Jean M. Macklaim,et al.  Microbiome Datasets Are Compositional: And This Is Not Optional , 2017, Front. Microbiol..

[28]  Glenn R. Gibson,et al.  The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic , 2014 .

[29]  K. Yuen,et al.  Granulicatella adiacens and Abiotrophia defectiva bacteraemia characterized by 16S rRNA gene sequencing. , 2003, Journal of medical microbiology.

[30]  J. Plaza-Díaz,et al.  Effects of Probiotics and Synbiotics on Obesity, Insulin Resistance Syndrome, Type 2 Diabetes and Non-Alcoholic Fatty Liver Disease: A Review of Human Clinical Trials , 2016, International journal of molecular sciences.

[31]  Ji Yeun Kim,et al.  Effect of oral probiotics (Bifidobacterium lactis AD011 and Lactobacillus acidophilus AD031) administration on ovalbumin-induced food allergy mouse model. , 2008, Journal of microbiology and biotechnology.

[32]  J. Blanco,et al.  Endocarditis due to Gemella haemolysans in a patient with hemochromatosis. , 2000, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[33]  F. Shanahan,et al.  The oral microbiota in colorectal cancer is distinctive and predictive , 2017, Gut.

[34]  Alan D. Lopez,et al.  Global, regional, and national prevalence of overweight and obesity in children and adults during 1980–2013: a systematic analysis for the Global Burden of Disease Study 2013 , 2014, The Lancet.

[35]  R. Hayes,et al.  Human oral microbiome and prospective risk for pancreatic cancer: a population-based nested case-control study , 2016, Gut.

[36]  L. Lissner,et al.  Oral health and obesity indicators , 2012, BMC oral health.

[37]  A. Ogawa,et al.  Lactobacillus gasseri SBT2055 suppresses fatty acid release through enlargement of fat emulsion size in vitro and promotes fecal fat excretion in healthy Japanese subjects , 2015, Lipids in Health and Disease.

[38]  T. Vicsek,et al.  Uncovering the overlapping community structure of complex networks in nature and society , 2005, Nature.

[39]  K. Smith,et al.  Obesity Statistics. , 2016, Primary care.

[40]  J. Gustafsson,et al.  Decreased Fat Storage by Lactobacillus Paracasei Is Associated with Increased Levels of Angiopoietin-Like 4 Protein (ANGPTL4) , 2010, PloS one.

[41]  Zaid Abdo,et al.  Differences in the composition of vaginal microbial communities found in healthy Caucasian and black women , 2007, The ISME Journal.

[42]  R. Siezen,et al.  Lactic Acid Bacteria: Genetics, Metabolism and Applications , 1999, Springer Netherlands.

[43]  Daniel G. Brown,et al.  PANDAseq: paired-end assembler for illumina sequences , 2012, BMC Bioinformatics.

[44]  K. Flegal,et al.  Prevalence of childhood and adult obesity in the United States, 2011-2012. , 2014, JAMA.

[45]  L. Signorello,et al.  The Southern Community Cohort Study: Investigating Health Disparities , 2010, Journal of health care for the poor and underserved.

[46]  R. Hayes,et al.  Association of Oral Microbiome With Risk for Incident Head and Neck Squamous Cell Cancer , 2018, JAMA oncology.

[47]  S. Halem,et al.  Is Obesity an Oral Bacterial Disease? , 2009, Journal of dental research.

[48]  C. Darimont,et al.  Effect of Lactobacillus rhamnosus CGMCC1.3724 supplementation on weight loss and maintenance in obese men and women , 2013, British Journal of Nutrition.

[49]  W. Zheng,et al.  Southern community cohort study: establishing a cohort to investigate health disparities. , 2005, Journal of the National Medical Association.

[50]  R. Hayes,et al.  Oral Microbiome Composition Reflects Prospective Risk for Esophageal Cancers. , 2017, Cancer research.

[51]  J. Mainardi,et al.  First Case of Streptococcus oligofermentans Endocarditis Determined Based on sodA Gene Sequences after Amplification Directly from Valvular Samples , 2009, Journal of Clinical Microbiology.

[52]  J. Long,et al.  Prospective study of oral microbiome and colorectal cancer risk in low‐income and African American populations , 2018, International journal of cancer.

[53]  K. Michaelsen,et al.  Effect of Lactobacillus salivarius Ls-33 on fecal microbiota in obese adolescents. , 2013, Clinical nutrition.

[54]  C. Quince,et al.  Insight into biases and sequencing errors for amplicon sequencing with the Illumina MiSeq platform , 2015, Nucleic acids research.

[55]  Robert Plomin,et al.  Evidence for a strong genetic influence on childhood adiposity despite the force of the obesogenic environment. , 2008, The American journal of clinical nutrition.