Subgingival Microbial Profiles of Smokers with Periodontitis
25 Aug 2010-Journal of Dental Research (International Association for Dental Research)-Vol. 89, Iss: 11, pp 1247-1253
TL;DR: The hypothesis that the subgingival biofilm is compositionally different in current and never-smokers is tested by using an open-ended molecular approach for bacterial identification, with significant differences in the prevalence and abundance of disease-associated and health-compatible organisms.
Abstract: The subgingival microbiome is largely uncultivated, and therefore, cultivation-based and targeted molecular approaches have limited value in examining the effect of smoking on this community. We tested the hypothesis that the subgingival biofilm is compositionally different in current and never-smokers by using an open-ended molecular approach for bacterial identification. Subgingival plaque from deep sites of current and never-smokers matched for disease was analyzed by 16S sequencing. Smokers demonstrated greater abundance of Parvimonas, Fusobacterium, Campylobacter, Bacteroides, and Treponema and lower levels of Veillonella, Neisseria, and Streptococcus. Several uncultivated Peptostreptococci, Parvimonas micra, Campylobacter gracilis, Treponema socranskii, Dialister pneumosintes, and Tannerella forsythia were elevated in this group, while Veillonella sp. oral clone B2, Neisseria sp. oral clone 2.24, Streptococcus sanguinis, and Capnocytophaga sp. clone AH015 were at lower levels. The microbial profile of smoking-associated periodontitis is distinct from that of non-smokers, with significant differences in the prevalence and abundance of disease-associated and health-compatible organisms.
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TL;DR: This study provides a global-scale framework for the ecological events in subgingival communities that underline the development of periodontitis and elucidate the relationship between inflammation and the subgesival microbiome.
Abstract: The goals of this study were to better understand the ecology of oral subgingival communities in health and periodontitis and elucidate the relationship between inflammation and the subgingival microbiome. Accordingly, we used 454-pyrosequencing of 16S rRNA gene libraries and quantitative PCR to characterize the subgingival microbiome of 22 subjects with chronic periodontitis. Each subject was sampled at two sites with similar periodontal destruction but differing in the presence of bleeding, a clinical indicator of increased inflammation. Communities in periodontitis were also compared with those from 10 healthy individuals. In periodontitis, presence of bleeding was not associated with different α-diversity or with a distinct microbiome, however, bleeding sites showed higher total bacterial load. In contrast, communities in health and periodontitis largely differed, with higher diversity and biomass in periodontitis. Shifts in community structure from health to periodontitis resembled ecological succession, with emergence of newly dominant taxa in periodontitis without replacement of primary health-associated species. That is, periodontitis communities had higher proportions of Spirochetes, Synergistetes, Firmicutes and Chloroflexi, among other taxa, while the proportions of Actinobacteria, particularly Actinomyces, were higher in health. Total Actinomyces load, however, remained constant from health to periodontitis. Moreover, an association existed between biomass and community structure in periodontitis, with the proportion of specific taxa correlating with bacterial load. Our study provides a global-scale framework for the ecological events in subgingival communities that underline the development of periodontitis. The association, in periodontitis, between inflammation, community biomass and community structure and their role in disease progression warrant further investigation.
759 citations
Cites background from "Subgingival Microbial Profiles of S..."
...As smoking has been shown to influence microbiome composition (Shchipkova et al., 2010), further investigation of differences in health and periodontitis is necessary in a homogeneous population....
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University of Pittsburgh1, University of Colorado Denver2, University of Michigan3, University of Washington4, Veterans Health Administration5, University of California, San Francisco6, George Washington University7, University of California, Los Angeles8, Washington University in St. Louis9, Indiana University10, Michigan State University11
TL;DR: This study is the largest to examine composition of the lower respiratory tract microbiome in healthy individuals and the first to use the neutral model to compare the lung to the mouth, demonstrating that the lung microbiome does not derive entirely from the mouth.
Abstract: Rationale: Results from 16S rDNA-encoding gene sequence–based, culture-independent techniques have led to conflicting conclusions about the composition of the lower respiratory tract microbiome. Objectives: To compare the microbiome of the upper and lower respiratory tract in healthy HIV-uninfected nonsmokers and smokers in a multicenter cohort. Methods: Participants were nonsmokers and smokers without significantcomorbidities.Oralwashesandbronchoscopicalveolarlavages were collected in a standardized manner. Sequence analysis of bacterial 16S rRNA-encoding genes was performed, and the neutral modelincommunityecologywasusedtoidentifybacteriathatwere the most plausible members of a lung microbiome. Measurements and Main Results: Sixty-four participants were enrolled. Mostbacteriaidentifiedinthelungwerealsointhemouth,butspecific bacteria such as Enterobacteriaceae, Haemophilus, Methylobacterium, and Ralstonia species were disproportionally represented in the lungs compared with values predicted by the neutral model. Tropheryma was
648 citations
Cites background from "Subgingival Microbial Profiles of S..."
...In addition, other groups have reported enrichment of certain organisms in smokers as well as depletion of organisms, particularly of normal community members (14, 25, 26)....
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TL;DR: Different regions of the human upper respiratory tract contain characteristic microbial communities that exhibit disordered patterns in cigarette smokers, both in individual components and global structure, which may contribute to the prevalence of respiratory tract complications in this population.
Abstract: Cigarette smokers have an increased risk of infectious diseases involving the respiratory tract. Some effects of smoking on specific respiratory tract bacteria have been described, but the consequences for global airway microbial community composition have not been determined. Here, we used culture-independent high-density sequencing to analyze the microbiota from the right and left nasopharynx and oropharynx of 29 smoking and 33 nonsmoking healthy asymptomatic adults to assess microbial composition and effects of cigarette smoking. Bacterial communities were profiled using 454 pyrosequencing of 16S sequence tags (803,391 total reads), aligned to 16S rRNA databases, and communities compared using the UniFrac distance metric. A Random Forest machine-learning algorithm was used to predict smoking status and identify taxa that best distinguished between smokers and nonsmokers. Community composition was primarily determined by airway site, with individuals exhibiting minimal side-of-body or temporal variation. Within airway habitats, microbiota from smokers were significantly more diverse than nonsmokers and clustered separately. The distributions of several genera were systematically altered by smoking in both the oro- and nasopharynx, and there was an enrichment of anaerobic lineages associated with periodontal disease in the oropharynx. These results indicate that distinct regions of the human upper respiratory tract contain characteristic microbial communities that exhibit disordered patterns in cigarette smokers, both in individual components and global structure, which may contribute to the prevalence of respiratory tract complications in this population.
356 citations
Cites background from "Subgingival Microbial Profiles of S..."
...To date, the effects of cigarette smoke on altering microbial colonization have been characterized in greatest detail in the subgingival environment, especially as it relates to periodontitis [14,15,17,43]....
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...and a decrease in potential healthpromoting taxa from the Veillonella, Neisseria, Streptococcus, and Capnocytophaga genera [43]....
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TL;DR: Peri-implantitis is a microbially heterogeneous infection with predominantly gram-negative species, and is less complex than periodontitis, whereas the periodontal community in both health and disease differs significantly.
Abstract: Aim
Although it is established that peri-implantitis is a bacterially induced disease, little is known about the bacterial profile of peri-implant communities in health and disease. The purpose of the present investigation was to examine the microbial signatures of the peri-implant microbiome in health and disease.
286 citations
Cites methods from "Subgingival Microbial Profiles of S..."
...A variance stabilizing transformation was used to create normal distribution of the data(Shchipkova et al., 2010)....
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TL;DR: It is important to understand the etiological factors and the pathogenesis of periodontal disease to recognize and appreciate the associated risk factors, and effective disease management requires a clear understanding of all the associatedrisk factors.
Abstract: Objectives. This paper aims to review the evidence on the potential roles of modifiable and nonmodifiable risk factors associated with periodontal disease. Data. Original articles that reported on the risk factors for periodontal disease were included. Sources. MEDLINE (1980 to Jan 2014), PubMed (using medical subject headings), and Google Scholar were searched using the following terms in different combinations: “periodontal disease,” “periodontitis,” “risk factors,” and “causal.” This was supplemented by hand-searching in peer-reviewed journals and cross-referenced with the articles accessed. Conclusions. It is important to understand the etiological factors and the pathogenesis of periodontal disease to recognize and appreciate the associated risk factors. As periodontal disease is multifactorial, effective disease management requires a clear understanding of all the associated risk factors.
249 citations
References
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01 Jan 1969
10,262 citations
TL;DR: The purpose of the present investigation was to attempt to define communities using data from large numbers of plaque samples and different clustering and ordination techniques, which related strikingly to clinical measures of periodontal disease particularly pocket depth and bleeding on probing.
Abstract: It has been recognized for some time that bacterial species exist in complexes in subgingival plaque. The purpose of the present investigation was to attempt to define such communities using data from large numbers of plaque samples and different clustering and ordination techniques. Subgingival plaque samples were taken from the mesial aspect of each tooth in 185 subjects (mean age 51 +/- 16 years) with (n = 160) or without (n = 25) periodontitis. The presence and levels of 40 subgingival taxa were determined in 13,261 plaque samples using whole genomic DNA probes and checkerboard DNA-DNA hybridization. Clinical assessments were made at 6 sites per tooth at each visit. Similarities between pairs of species were computed using phi coefficients and species clustered using an averaged unweighted linkage sort. Community ordination was performed using principal components analysis and correspondence analysis. 5 major complexes were consistently observed using any of the analytical methods. One complex consisted of the tightly related group: Bacteroides forsythus, Porphyromonas gingivalis and Treponema denticola. The 2nd complex consisted of a tightly related core group including members of the Fusobacterium nucleatum/periodonticum subspecies, Prevotella intermedia, Prevotella nigrescens and Peptostreptococcus micros. Species associated with this group included: Eubacterium nodatum, Campylobacter rectus, Campylobacter showae, Streptococcus constellatus and Campylobacter gracilis. The 3rd complex consisted of Streptococcus sanguis, S. oralis, S. mitis, S. gordonii and S. intermedius. The 4th complex was comprised of 3 Capnocytophaga species, Campylobacter concisus, Eikenella corrodens and Actinobacillus actinomycetemcomitans serotype a. The 5th complex consisted of Veillonella parvula and Actinomyces odontolyticus. A. actinomycetemcomitans serotype b, Selenomonas noxia and Actinomyces naeslundii genospecies 2 (A. viscosus) were outliers with little relation to each other and the 5 major complexes. The 1st complex related strikingly to clinical measures of periodontal disease particularly pocket depth and bleeding on probing.
4,143 citations
"Subgingival Microbial Profiles of S..." refers background in this paper
...Smokers also demonstrated a greater abundance of Parvimonas, Campylobacter, Treponema, Bacteroides, and Fusobacterium—genera that are consistently associated with disease (Socransky et al., 1998; Kumar et al., 2005)....
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TL;DR: The purposes were to utilize culture-independent molecular techniques to extend the knowledge on the breadth of bacterial diversity in the healthy human oral cavity, including not-yet-cultivated bacteria species, and to determine the site and subject specificity of bacterial colonization.
Abstract: More than 700 bacterial species or phylotypes, of which over 50% have not been cultivated, have been detected in the oral cavity. Our purposes were (i) to utilize culture-independent molecular techniques to extend our knowledge on the breadth of bacterial diversity in the healthy human oral cavity, including not-yet-cultivated bacteria species, and (ii) to determine the site and subject specificity of bacterial colonization. Nine sites from five clinically healthy subjects were analyzed. Sites included tongue dorsum, lateral sides of tongue, buccal epithelium, hard palate, soft palate, supragingival plaque of tooth surfaces, subgingival plaque, maxillary anterior vestibule, and tonsils. 16S rRNA genes from sample DNA were amplified, cloned, and transformed into Escherichia coli. Sequences of 16S rRNA genes were used to determine species identity or closest relatives. In 2,589 clones, 141 predominant species were detected, of which over 60% have not been cultivated. Thirteen new phylotypes were identified. Species common to all sites belonged to the genera Gemella, Granulicatella, Streptococcus, and Veillonella. While some species were subject specific and detected in most sites, other species were site specific. Most sites possessed 20 to 30 different predominant species, and the number of predominant species from all nine sites per individual ranged from 34 to 72. Species typically associated with periodontitis and caries were not detected. There is a distinctive predominant bacterial flora of the healthy oral cavity that is highly diverse and site and subject specific. It is important to fully define the human microflora of the healthy oral cavity before we can understand the role of bacteria in oral disease.
2,683 citations
"Subgingival Microbial Profiles of S..." refers background in this paper
...Streptococci normally form a large fraction of a health-associated microbiome (Aas et al., 2005), and recent evidence suggests that they play a critical role in preventing colonization of this niche by pathogens (Stingu et al....
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...Streptococci normally form a large fraction of a health-associated microbiome (Aas et al., 2005), and recent evidence suggests that they play a critical role in preventing colonization of this niche by pathogens (Stingu et al., 2008; Van Hoogmoed et al., 2008)....
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TL;DR: The purpose of this study was to determine the bacterial diversity in the human subgingival plaque by using culture-independent molecular methods as part of an ongoing effort to obtain full 16S rRNA sequences for all cultivable and not-yet-cultivated species of human oral bacteria.
Abstract: The purpose of this study was to determine the bacterial diversity in the human subgingival plaque by using culture-independent molecular methods as part of an ongoing effort to obtain full 16S rRNA sequences for all cultivable and not-yet-cultivated species of human oral bacteria. Subgingival plaque was analyzed from healthy subjects and subjects with refractory periodontitis, adult periodontitis, human immunodeficiency virus periodontitis, and acute necrotizing ulcerative gingivitis. 16S ribosomal DNA (rDNA) bacterial genes from DNA isolated from subgingival plaque samples were PCR amplified with all-bacterial or selective primers and cloned into Escherichia coli. The sequences of cloned 16S rDNA inserts were used to determine species identity or closest relatives by comparison with sequences of known species. A total of 2,522 clones were analyzed. Nearly complete sequences of approximately 1,500 bases were obtained for putative new species. About 60% of the clones fell into 132 known species, 70 of which were identified from multiple subjects. About 40% of the clones were novel phylotypes. Of the 215 novel phylotypes, 75 were identified from multiple subjects. Known putative periodontal pathogens such as Porphyromonas gingivalis, Bacteroides forsythus, and Treponema denticola were identified from multiple subjects, but typically as a minor component of the plaque as seen in cultivable studies. Several phylotypes fell into two recently described phyla previously associated with extreme natural environments, for which there are no cultivable species. A number of species or phylotypes were found only in subjects with disease, and a few were found only in healthy subjects. The organisms identified only from diseased sites deserve further study as potential pathogens. Based on the sequence data in this study, the predominant subgingival microbial community consisted of 347 species or phylotypes that fall into 9 bacterial phyla. Based on the 347 species seen in our sample of 2,522 clones, we estimate that there are 68 additional unseen species, for a total estimate of 415 species in the subgingival plaque. When organisms found on other oral surfaces such as the cheek, tongue, and teeth are added to this number, the best estimate of the total species diversity in the oral cavity is approximately 500 species, as previously proposed.
1,899 citations
"Subgingival Microbial Profiles of S..." refers background in this paper
...These genera are reported to be abundant in health-associated biofilms, and their levels decrease in disease (Paster et al., 2001; Kumar et al., 2005, 2006), suggesting that in smokers periodontitis is associated with a greater depletion of beneficial bacteria than in nonsmokers....
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...Comparing bacterial profiles of the deep sites from decrease in disease (Paster et al., 2001; Kumar et al., 2005, 2006), suggesting that in smokers periodontitis is associated with a greater depletion of beneficial bacteria than in nonsmokers....
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