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New Bacterial Species Associated with Chronic Periodontitis
P.S. Kumar1,
A.L. Griffen2,*,
J.A. Barton3,
B.J. Paster4,5,
M.L. Moeschberger6 and
E.J. Leys7
1 Department of Periodontology,
2 Department of Pediatric Dentistry,
3 College of Dentistry,
7 Department of Oral Biology, College of Dentistry, and
6 Division of Epidemiology and Biometrics, School of Public Health, College of Medicine and Public Health, The Ohio State University, 305 W. 12th Ave., PO Box 182357, Columbus, OH 43218-2357;
4 Department of Molecular Genetics, The Forsyth Institute, and
5 Department of Oral and Developmental Biology, Harvard School of Dental Medicine, Boston, MA;
Correspondence: * corresponding author, griffen.1{at}osu.edu
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ABSTRACT
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Recent investigations of the human subgingival oral flora based on ribosomal 16S cloning and sequencing have shown many of the bacterial species present to be novel species or phylotypes. The purpose of the present investigation was to identify potential periodontal pathogens among these newly identified species and phylotypes. Species-specific ribosomal 16S primers for PCR amplification were developed for detection of new species. Associations with chronic periodontitis were observed for several new species or phylotypes, including uncultivated clones D084 and BH017 from the Deferribacteres phylum, AU126 from the Bacteroidetes phylum, Megasphaera clone BB166, clone X112 from the OP11 phylum, and clone I025 from the TM7 phylum, and the named species Eubacterium saphenum, Porphyromonas endodontalis, Prevotella denticola, and Cryptobacterium curtum. Species or phylotypes more prevalent in periodontal health included two uncultivated phylotypes, clone W090 from the Deferribacteres phylum and clone BU063 from the Bacteroidetes, and named species Atopobium rimae and Atopobium parvulum.
Key Words: 16S ribosomal identification • periodontal microbiology • periodontitis • human epidemiology • uncultivated bacteria
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INTRODUCTION
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Chronic periodontitis is characterized by a bacterially induced progressive loss of clinical attachment, including destruction of periodontal ligament and adjacent supporting bone. For the identification of the bacterial pathogens responsible for periodontitis, many investigations targeting known species have been conducted with the use of both cultivation and molecular identification methods. Tannerella forsythensis (Bacteroides forsythus) and Porphyromonas gingivalis are widely regarded as major periodontal pathogens, and evidence has implicated several other species in disease etiology. However, no single pathogen or group of pathogens has been clearly identified as the cause of periodontitis. A recent comprehensive investigation of the human subgingival oral flora based on ribosomal 16S cloning and sequencing showed 40% of the bacterial species present to be novel species or phylotypes (Paster et al., 2001). Several other recent investigations with similar methodologies have also shown the presence of high numbers of novel species in the oral cavity (Dymock et al., 1996; Kroes et al., 1999; Sakamoto et al., 2000). Therefore, it seems likely that unrecognized periodontal pathogens remain to be identified.
The purpose of the present study was to evaluate the association of newly identified bacterial species or phylotypes with periodontitis. Targets for investigation included both uncultivated phylotypes and characterized species that were not previously thought to be associated with periodontitis. In addition, species previously strongly linked to periodontitis were included for comparison.
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MATERIALS & METHODS
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Study Population
Samples collected and stored from a previous study were available for re-analysis for this study. As previously described (Griffen et al., 1998), subjects for this institutionally approved study were recruited from the dental clinics of the Ohio State University, and informed consent was obtained. Exclusionary criteria were set to select the most and least periodontally healthy segments of the population on the basis of probing depths and attachment levels, as previously described (Griffen et al., 1998). For each subject, the mesial sulci of all teeth present were sampled with endodontic paper points, and samples from each individual were pooled. A set of samples from 66 subjects with chronic periodontitis and 66 age-matched controls was randomly selected for the present study. The same set of samples was used for all 39 species or phylotypes examined.
Detection of Bacterial Species and Phylotypes
We use the term "phylotype" rather than "species" to refer to novel clone sequences that differ by at least 2% from known species in the ribosomal 16S gene. Bacterial species and phylotypes were detected by PCR amplification of the 16S rDNA and the downstream intergenic spacer region (ISR). Inclusion of the ISR provided an additional check on the specificity of primers, since the length of this region varies among species. DNA isolated from the plaque samples was first amplified with prokaryotic universal ribosomal 16S and 23S primers, as described previously (McClellan et al., 1996). Individual species were then identified by a second, nested amplification with species-specific 16S primers paired with a universal primer located in the 23S gene. Primer sequences are shown in Table 1 . DNA fragments were separated by 1% agarose gel electrophoresis, stained with ethidium bromide, and viewed under UV transillumination. A positive or negative score was assigned based on the presence of clear bands of the expected molecular size. All assays were repeated, and if the results were not in agreement, they were repeated again.
Primer Specificity
Species-specific primers in the 16S rRNA coding region were selected based on sequences available in GenBank (Table 1 ). We confirmed species specificity by sequencing at least one PCR product from a clinical sample for each primer in an ABI Prism 310 automated sequencer as described previously (Rumpf et al., 1999), and comparing the sequence generated with those available in GenBank.
Data Analysis
Chi-square analysis was used to compare the prevalence of various species in healthy individuals and in individuals with chronic periodontitis. The alpha level was adjusted from 0.05 to 0.002 based on the Bonferroni correction for multiple comparisons. Prevalence ratios and 95% confidence intervals were calculated for the presence of each species in the periodontally healthy group vs. the group with chronic periodontitis. Prevalence ratios and confidence intervals were calculated in the same manner as a relative risk (Fleiss, 1981).
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RESULTS
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The clinical status of the study population has been previously described (Griffen et al., 1998). In the subgroup examined for this study, the mean for the deepest PD was 3.8 mm (SD 0.8) in the periodontally healthy group, and 7.7 mm (SD 1.3) in the periodontitis group. The mean age was 47.9 yrs (SD 13.1) for the healthy group and 50.6 yrs (SD 16.2) for the group with periodontitis. This difference was not significant by t test. The healthy group was 79% white, 15% African-American, 5% Asian-American, and 2% other racial groups. The group with periodontitis was 68% white, 21% African-American, 3% Asian-American, and 8% other racial groups. The racial distribution of the two groups was not significantly different by chi-square analysis. The periodontally healthy group was 68% female and 32% male, and the group with periodontitis was 41% female and 59% male. This difference was statistically significant by chi-square analysis (P = 0.002). However, no statistically significant differences were seen in the presence of any species by sex or race by chi-square analysis, or by age by t test.
Comparisons of the presence or absence of 39 species or phylotypes in periodontal health and in chronic periodontitis are shown in Table 2 and in Fig. 1, which is arranged with the species most commonly found in healthy subjects shown at the top, and those most common in disease at the bottom. Fig. 2 and Table 2 show the prevalence ratio for the distribution between subjects with and without periodontitis for each species or phylotype. Prevalence ratios greater than 1 indicate association with disease, and those less than 1 show association with health. Data for P. gingivalis (Griffen et al., 1998), T. forsythensis (B. forsythus), and clone BU063 (Leys et al., 2002) have been previously reported, and are included here for comparison.
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Figure 1. Prevalence of 39 bacterial species or phylotypes in 66 subjects with periodontitis and 66 healthy control subjects. Differences significant by chi-square analysis with P < 0.05 are marked "*" after the species name; differences significant with P < 0.002 are marked "**".
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Figure 2. Prevalence ratios (calculated like a relative risk) for 39 bacterial species or phylotypes for 66 subjects with periodontitis and 66 healthy control subjects. Ninety-five percent confidence intervals are shown as bars. The values to the left of 1 show species more common in health than in disease, and those to the right of 1 show species more common in disease than in health. Confidence intervals could not be calculated for F. nucleatum or G. morbillorum, since there were 0 subjects without the bacteria in the disease group.
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DISCUSSION
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Chronic periodontitis appears to have a complex bacterial etiology. More than 400 species have been commonly detected in the gingival sulcus (Paster et al., 2001), and several different species have been previously associated by some measure with human periodontitis. Before the availability of DNA-based detection methods, investigations were limited to those species that could be cultivated on an artificial medium. The first molecular investigations of the microbiology of periodontitis were limited to molecular detection of species that had been previously identified by cultivation. Recently, ribosomal 16S cloning and sequencing have been used to identify uncultivated bacteria in the oral cavity, and investigation of the disease association of these new species is now possible. The purpose of the present investigation was to evaluate the association of newly identified bacterial species with chronic periodontitis. Newly identified targets for investigation included both uncultivated phylotypes and previously characterized species that were not thought to be common inhabitants of the gingival sulcus. Species and phylotypes were selected for testing based on their detection in a previous large-scale investigation of oral bacterial diversity by cloning and sequencing of bacterial 16S genes (Paster et al., 2001). Samples from subjects with chronic periodontitis were compared with those from age-matched periodontally healthy subjects to identify species of bacteria that may play a role in determining periodontal health. The study was designed to determine the presence or absence of each species in the subgingival environment of the entire dentition for each subject by sampling every tooth. We used this strategy to avoid the bias introduced by sampling only selected sites, and to identify qualitative differences in the flora of periodontal health and disease. If periodontitis is caused by pathogens rather than commensal species that overgrow in the absence of oral hygiene, this strategy will allow them to be identified.
Five species or phylotypes more prevalent in periodontally healthy subjects than in subjects with periodontitis were identified: Atopobium rimae, Atopobium parvulum, Corynebacterium matruchotii, and two uncultivated phylotypes, clone W090 from the Deferribacteres phylum, and clone BU063 from the Bacteroidetes phylum. Data shown here for clone BU063 have been previously reported (Leys et al., 2002). To our knowledge, association with periodontal health has not been previously reported for the other 3 species/phylotypes. Both clone BU063 and W090 are very closely related to species or phylotypes (T. forsythensis and Deferribacteres clone D084/ BH017, respectively) (Paster et al., 2001) that are strongly associated with periodontitis (Fig. 2), suggesting that phylogeny is not necessarily a good predictor of disease association. The demonstration of a higher prevalence of certain bacterial species in the mouths of healthy subjects suggests that replacement of a pathogenic flora with a benign one may be therapeutically important, and deserves further study.
Several uncultivated phylotypes showed a very strong relationship to disease, suggesting that there may be previously unrecognized organisms that play an important role in the pathogenesis of periodontitis. Clones D084 and BH017 from the Deferribacteres group (indistinguishable by our assay) and clone AU126 from the Bacteroidetes were among the most strongly associated with disease of any species tested, with strength of association comparable with or greater than that of the organisms widely regarded as the major pathogens in chronic periodontitis, P. gingivalis and T. forsythensis (Fig. 2). In addition, clone X112 from the OP11 phylum was strongly associated with periodontitis, and Megasphaera clone BB166 and clone I025 from the TM7 group were associated with periodontitis at the P = 0.05 level.
Named species more commonly found in subjects with chronic periodontitis than in healthy subjects, when a stringent threshold of P < 0.002 was applied, included Treponema denticola, Eubacterium saphenum, Porphyromonas endodontalis, P. gingivalis, T. forsythensis, Filifactor alocis, Prevotella denticola, Cryptobacterium curtum, Treponema medium, Treponema socranskii, and Actinomyces naeslundii. Most of these species have been previously associated with periodontitis. Of these, P. gingivalis, T. forsythensis, and T. denticola have consistently been associated with periodontitis (Socransky et al., 1998). Associations with chronic periodontitis for several species were newly demonstrated in the present study, including P. endodontalis, E. saphenum, P. denticola, T. medium, and C. curtum. P. endodontalis has primarily been reported in symptomatic infections originating in the pulp chamber (Haapasalo, 1993), but it has been detected in periodontal pockets and other oral sites (Petit et al., 1993). Eubacterium saphenum has been isolated from periodontal pockets (Uematsu et al., 1993) and detected in infected root canal systems (Hashimura et al., 2001). P. denticola (Teanpaisan et al., 1995; Fosse et al., 1999) and T. medium (Willis et al., 1999; Asai et al., 2002) have been previously identified in deep periodontal pockets, although an association with disease has not been demonstrated. Cryptobacterium curtum is a recently characterized species isolated from the gingival sulcus of a patient with periodontitis (Nakazawa et al., 1999). Limited evidence has demonstrated more frequent detection of T. socranskii in subjects with periodontitis, although the observed differences were not statistically significant (Riviere et al., 1997; Takeuchi et al., 2001), and the bacterium has been seen more frequently in deeper pockets (Ximenez-Fyvie et al., 2000b). Filifactor alocis has been seen more commonly in sites with periodontitis than in healthy sites (Tanner et al., 1998). The strong association between the presence of A. naeslundii II and periodontitis is somewhat surprising, since A. naeslundii II and other Actinomyces species are more commonly found in the supragingival plaque than in the gingival sulcus (Ximenez-Fyvie et al., 2000b). However, both A. naeslundii I and II have previously been seen in higher numbers in the gingival sulcus of subjects with periodontitis as compared with healthy subjects (Ximenez-Fyvie et al., 2000a).
Additional named species more commonly found in subjects with chronic periodontitis than in healthy subjects, when a less stringent threshold of P < 0.05 was applied, included Treponema lecithinolyticum, Peptostreptococcus micros, Selenomonas sputigena, Rothia dentocariosa, Eikenella corrodens, and Dialister isolate GBA27. T. lecithinolyicum is a recently characterized species that has been associated with both chronic and aggressive periodontitis (Wyss et al., 1999). R. dentocariosa has been associated with gingival recession (Tanner et al., 1998) and with pericoronitis (Peltroche-Llacsahuanga et al., 2000). E. corrodens has been associated with chronic periodontitis (Ximenez-Fyvie et al., 2000a) and aggressive forms of periodontitis (Suda et al., 2002), and has been found in close association with other bacteria often found in this form of periodontitis (Muller et al., 1997; Socransky et al., 1998). The presence of P. micros has been positively associated with periodontitis (Socransky et al., 1998; Choi et al., 2000; Papapanou et al., 2000; Ximenez-Fyvie et al., 2000a). Both Dialister isolate GBA27 and S. sputigena have been detected in subjects with periodontitis (Paster et al., 2001).
Several species were nearly universally present in both health and disease states, including Fusobacterium naviforme, Fusobacterium nucleatum, Gemella haemolysans, Gemella morbillorum, and Campylobacter rectus. Little previous information is available about F. naviforme or G. haemolysans in the oral cavity. F. nucleatum has been frequently associated with periodontitis (Colombo et al., 2002; Van Winkelhoff et al., 2002; Ximenez-Fyvie et al., 2000a), and G. morbillorum and C. rectus have been found in higher numbers in the subgingival plaque of subjects with periodontitis as compared with healthy subjects (Ximenez-Fyvie et al., 2000a). These findings suggest that these ubiquitous species may be commensals that overgrow in periodontitis, in contrast to true pathogens that usually produce disease when present. Evidence suggests that F. nucleatum may play a role in disease by providing the anaerobic environment necessary for the growth of pathogens (Diaz et al., 2002). Several species—A. naeslundii, S. sputigena, R. dentocariosa, E. corrodens, and clone I025 from the TM7 phylum—were more prevalent in periodontitis than in health in the present study, but the prevalence in health was so high (Table 2 and Fig. 1) that they may also be regarded as commensal species.
The microbial etiology of chronic periodontitis appears to be complex, with a large number of species showing association with disease. The present investigation has expanded this list to include several uncultivated species recently identified by ribosomal sequence analysis. Multiple factors probably account for the observed complexity, including interdependence among bacterial species within the bacterial community, and inter-individual variation in microbial etiology and host susceptibility. In addition to functional studies to elucidate mechanisms of pathogenesis, future studies that provide quantitative information on proportions of these newly identified species at sites of disease activity, as well as longitudinal studies elucidating the natural history of this chronic disease, are needed. In addition, the bacterial species that are found in a healthy subgingival environment deserve further study.
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ACKNOWLEDGMENTS
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This work was supported by Public Health Service grant DE10467 from the National Institute of Dental and Craniofacial Research.
Received for publication January 27, 2003.
Revision received February 17, 2003.
Accepted for publication February 19, 2003.
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Journal of Dental Research, Vol. 82, No. 5,
338-344 (2003)
DOI: 10.1177/154405910308200503
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TOP
ABSTRACT
INTRODUCTION