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Bacteriology

Changes in Periodontal Health Status Are Associated with Bacterial Community Shifts as Assessed by Quantitative 16S Cloning and Sequencing

Purnima S. Kumar, Eugene J. Leys, Jennifer M. Bryk, Francisco J. Martinez, Melvin L. Moeschberger, Ann L. Griffen
Purnima S. Kumar
1Section of Periodontology
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Eugene J. Leys
2Section of Oral Biology
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Jennifer M. Bryk
3Section of Pediatric Dentistry, College of Dentistry
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Francisco J. Martinez
2Section of Oral Biology
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Melvin L. Moeschberger
4Division of Biostatistics, School of Public Health, The Ohio State University, Columbus, Ohio 43218
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Ann L. Griffen
3Section of Pediatric Dentistry, College of Dentistry
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  • For correspondence: griffen.1@osu.edu
DOI: 10.1128/JCM.00317-06
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  • FIG. 1.
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    FIG. 1.

    Clinical stability of 24 subjects over 2 years. For the improved group, the shaded and open bars taken together indicate the number of sites with probe depths of >4 mm (deep sites) at baseline. Open bars represent decreases in the number of deep sites that occurred between the baseline and final sampling times. For the worse group, the shaded bars indicate initial clinical status and the solid bars represent increases in the number of deep sites that occurred between the baseline and final sampling times.

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    FIG. 2.

    Relationship between periodontal status and microbial stability and diversity for 24 subjects over 2 years. (Top) Relationship between clinical status and microbial conservation. (Center) Relationship between the number of species lost or gained over 2 years and clinical status. (Bottom) Relationship between mean microbial diversity (number of species present in each subject over 2 years) and clinical status. The standard deviation (small lines), group mean (central line in diamond), and 95% confidence intervals (height of diamond) are shown for each group.

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    FIG. 3.

    Mean levels at 2 years (top) and change in levels (mean level at 2 years minus mean level at baseline) (bottom) for species significantly associated with improvement or worsening of periodontitis. (Top) Percentage of total clones accounted for by each species for the stable healthy, improved, and worse groups at the final sampling time. (Bottom) Percentage of change between the initial and final sampling times for the same species and clinical groups. Species showing significant differences (P < 0.05) among the three clinical groups are indicated by an asterisk.

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  • TABLE 1.

    Species and phylotypes for each clinical group, arranged in order of decreasing frequencya

    Overall rankSpecies/phylotype(s)% of total clonesbMean % of total clones ± SD for individuals with the following clinical status:
    StableBetterWorse
    1 Veillonella sp. oral clone X0429.5210.3 ± 4.08.1 ± 7.59.8 ± 8.1
    2 Campylobacter gracilis 3.654.5 ± 4.34.2 ± 4.71.9 ± 2.6
    3 Streptococcus mitis 3.483.4 ± 3.23.4 ± 3.23.5 ± 2.2
    4 Streptococcus gordonii 3.214.5 ± 5.73.1 ± 1.81.5 ± 1.7
    5 Streptococcus oralis 2.752.7 ± 2.33.4 ± 2.92.1 ± 1.9
    6 Streptococcus sanguinis 2.423.2 ± 3.91.9 ± 2.41.9 ± 2.0
    7 Streptococcus sp. oral strain 12F2.422.7 ± 2.03.5 ± 3.91.0 ± 1.7
    8 Peptostreptococcus sp. oral clone FG0142.172.1 ± 2.12.3 ± 2.62.1 ± 5.1
    9 Selenomonas infelix 2.132.0 ± 1.91.8 ± 1.42.7 ± 2.4
    10 Campylobacter showae 1.921.9 ± 2.12.0 ± 2.91.9 ± 2.8
    11 Peptostreptococcus sp. oral clone AJ0621.900.9 ± 2.30.5 ± 1.44.8 ± 17.0
    12 Streptococcus genomospecies C81.882.3 ± 4.01.7 ± 2.81.5 ± 4.0
    13 Streptococcus intermedius 1.811.9 ± 1.71.6 ± 2.31.9 ± 3.2
    14 Gemella morbillorum 1.731.5 ± 1.72.4 ± 3.51.4 ± 1.7
    15 Gemella haemolysans 1.631.9 ± 1.61.5 ± 1.71.4 ± 1.8
    16 Streptococcus pneumoniae 1.631.8 ± 2.11.4 ± 2.21.6 ± 1.8
    17 Filifactor alocis 1.480.2 ± 0.41.4 ± 2.93.4 ± 3.8
    18 Granulicatella elegans 1.461.6 ± 1.61.6 ± 1.41.2 ± 1.4
    19 Peptostreptococcus sp. oral clone BS0441.461.3 ± 1.81.7 ± 1.91.4 ± 1.6
    20 Veillonella atypica 1.421.6 ± 2.11.2 ± 2.21.4 ± 1.9
    21 Streptococcus sp. oral clone 2056B1.231.0 ± 1.41.6 ± 2.31.3 ± 2.0
    22 Peptostreptococcus micros 1.191.9 ± 2.80.7 ± 1.70.7 ± 1.5
    23 Neisseria elongata 1.171.4 ± 3.71.3 ± 1.90.6 ± 2.8
    24 Streptococcus sp. oral strain 7A1.080.9 ± 1.51.4 ± 1.71.4 ± 1.8
    25 Selenomonas sputigena 0.980.8 ± 1.41.1 ± 2.21.1 ± 1.9
    26 Streptococcus sp. oral clone FN0510.960.7 ± 1.51.7 ± 2.20.7 ± 1.5
    27 Capnocytophaga gingivalis 0.940.7 ± 0.90.9 ± 1.21.3 ± 1.5
    28 Campylobacter concisus 0.901.3 ± 2.00.6 ± 1.00.6 ± 1.2
    29 Selenomonas sp. oral clone EW051a0.881.0 ± 1.40.1 ± 0.51.5 ± 2.2
    30 Streptococcus anginosus 0.810.5 ± 0.90.6 ± 1.01.4 ± 1.3
    31 Megasphaera sp. oral clone BB1660.790.8 ± 1.20.9 ± 1.50.6 ± 1.0
    32 Eikenella corrodens 0.730.8 ± 1.00.9 ± 1.00.6 ± 1.2
    33 Dialister sp. oral clone E2_200.710.5 ± 1.01.1 ± 1.60.7 ± 1.1
    34 Streptococcus genomospecies C70.670.6 ± 1.21.3 ± 2.30.2 ± 0.6
    35 Neisseria sp. oral clone AP0600.670.9 ± 1.70.9 ± 1.50.2 ± 0.8
    36 Streptococcus salivarius 0.630.8 ± 1.80.3 ± 0.60.7 ± 1.4
    37 Selenomonas sp. oral clone AA0240.631.1 ± 2.50.3 ± 0.70.2 ± 0.8
    38 Selenomonas sp. oral clone AJ0360.630.6 ± 0.80.6 ± 1.00.6 ± 1.2
    39 Streptococcus infantis 0.580.6 ± 1.00.5 ± 1.30.6 ± 1.0
    40 Dialister sp. oral clone BS0950.580.7 ± 1.00.4 ± 0.90.7 ± 0.8
    41 Selenomonas noxia 0.560.7 ± 1.20.7 ± 0.90.3 ± 0.6
    42 Gemella sanguinis 0.500.6 ± 1.90.6 ± 1.30.2 ± 0.4
    43 Dialister pneumosintes 0.500.4 ± 0.80.4 ± 0.80.8 ± 1.1
    44 Dialister invisus 0.500.7 ± 1.30.5 ± 0.90.2 ± 0.4
    45 Selenomonas sp. oral clone DY0270.480.5 ± 1.00.4 ± 0.90.5 ± 1.1
    46 Selenomonas sp. oral clone DS0510.480.4 ± 0.71.0 ± 1.70.1 ± 0.4
    47 Selenomonas sp. oral clone IK0040.460.3 ± 0.70.6 ± 1.70.5 ± 1.3
    48 Veillonella sp. oral clone BU0830.460.4 ± 0.90.2 ± 0.40.9 ± 1.9
    49 Capnocytophaga granulosa 0.440.9 ± 1.40.1 ± 0.50.1 ± 0.3
    50 Streptococcus sp. oral clone EK0480.440.3 ± 0.80.6 ± 1.40.5 ± 0.8
    51 Abiotrophia para-adiacens 0.420.6 ± 1.10.4 ± 0.80.2 ± 0.6
    52 Abiotrophia sp. oral clone P4PA_1550.420.5 ± 0.90.4 ± 0.80.5 ± 0.9
    53 Streptococcus parasanguinis 0.420.4 ± 1.20.7 ± 1.90.2 ± 0.6
    54 Selenomonas sp. oral clone DS0710.420.1 ± 0.20.6 ± 1.20.8 ± 1.3
    55 Selenomonas sp. oral clone EQ0540.420.5 ± 1.20.4 ± 0.80.3 ± 0.6
    56 Neisseria meningitidis 0.420.5 ± 0.80.2 ± 0.60.5 ± 0.8
    57 Campylobacter rectus 0.420.1 ± 0.50.6 ± 1.00.7 ± 1.1
    58 Rothia dentocariosa 0.400.6 ± 1.10.4 ± 0.90.1 ± 0.3
    59 Streptococcus cristatus 0.400.3 ± 0.60.5 ± 0.90.4 ± 0.9
    60 Selenomonas dianae 0.400.6 ± 0.90.1 ± 0.30.4 ± 0.8
    61 Capnocytophaga sp. oral clone AH0150.380.3 ± 0.40.6 ± 1.30.4 ± 0.8
    62 Streptococcus sinensis 0.380.3 ± 0.60.3 ± 0.50.6 ± 0.8
    63 Kingella oralis 0.380.3 ± 0.70.9 ± 1.20.0 ± 0.0
    64 Neisseria denitrificans 0.380.4 ± 0.70.7 ± 1.30.1 ± 0.3
    65 Enterococcus faecalis 0.350.6 ± 0.90.2 ± 0.60.1 ± 0.4
    66 Eubacterium brachy 0.350.3 ± 0.70.6 ± 1.00.2 ± 0.6
    67 Capnocytophaga sputigena 0.330.3 ± 0.70.5 ± 0.80.2 ± 0.6
    68 Eubacterium sp. oral clone EW0530.330.3 ± 1.00.4 ± 0.80.2 ± 0.6
    69 Selenomonas sp. oral clone EW0840.330.5 ± 0.10.2 ± 0.60.2 ± 0.6
    70 Eubacterium saphenum 0.310.3 ± 0.80.1 ± 0.30.6 ± 1.0
    71 Porphyromonas gingivalis 0.290.0 ± 0.00.2 ± 0.60.8 ± 2.4
    72 Streptococcus agalactiae 0.290.3 ± 1.10.3 ± 0.80.2 ± 0.6
    73 Selenomonas sp. oral clone DO0420.290.2 ± 0.40.5 ± 0.90.3 ± 0.8
    74 Streptococcus bovis 0.270.2 ± 0.40.5 ± 1.10.2 ± 0.4
    75 Streptococcus suis 0.270.3 ± 0.50.1 ± 0.30.4 ± 0.8
    76 Peptostreptococcus sp. oral clone CK0350.270.4 ± 0.90.1 ± 0.30.3 ± 0.8
    77 Selenomonas-like sp. oral clone CS0150.270.1 ± 0.20.3 ± 0.70.5 ± 0.8
    78 Selenomonas sp. oral clone CS0020.270.1 ± 0.20.6 ± 1.30.2 ± 0.6
    79 Corynebacterium matruchotii 0.250.2 ± 0.40.4 ± 0.90.1 ± 0.5
    80 Streptococcus sp. oral clone 4093B0.250.2 ± 0.70.3 ± 0.80.3 ± 0.5
    81 Streptococcus sp. oral clone FX0030.250.3 ± 0.60.1 ± 0.50.4 ± 0.9
    82 Eubacterium sp. oral clone E1-K170.250.3 ± 0.70.2 ± 0.40.2 ± 0.6
    83 Treponema sp. strain Smibert-50.250.2 ± 0.40.2 ± 0.80.4 ± 0.9
    84 Atopobium rimae 0.230.4 ± 0.90.0 ± 0.00.2 ± 0.6
    85 Streptococcus pyogenes 0.230.3 ± 0.80.3 ± 0.60.1 ± 0.4
    86 Desulfobulbus sp. oral clone CH0310.230.3 ± 0.80.0 ± 0.00.4 ± 1.2
    87 Peptostreptococcus sp. oral clone MDA2346-20.230.0 ± 0.00.3 ± 0.60.5 ± 1.2
    88 Selenomonas sp. oral clone CS0240.230.4 ± 0.80.3 ± 0.00.3 ± 0.6
    89 Selenomonas sp. oral clone GT0100.230.5 ± 1.40.1 ± 0.00.1 ± 0.5
    90 Selenomonas lacticifex 0.230.6 ± 1.60.0 ± 0.00.0 ± 0.0
    91 Alysiella filiformis 0.230.0 ± 0.00.8 ± 1.90.0 ± 0.0
    92 Lautropia sp. oral clone AP0090.230.1 ± 0.20.7 ± 1.30.0 ± 0.0
    93 Granulicatella adiacens 0.210.3 ± 0.60.2 ± 0.60.1 ± 0.5
    94 Gemella sp. strain 1754-940.210.1 ± 0.30.0 ± 0.00.6 ± 0.9
    95 Streptococcus intestinalis 0.210.3 ± 0.80.2 ± 0.60.1 ± 0.3
    96 Streptococcus mutans 0.210.2 ± 0.70.1 ± 0.40.3 ± 0.6
    97 Streptococcus peroris 0.210.2 ± 0.40.1 ± 0.50.4 ± 0.7
    98 Catonella sp. oral clone FL0370.210.3 ± 0.80.0 ± 0.00.4 ± 0.9
    99 Catonella morbi 0.210.1 ± 0.30.4 ± 0.60.2 ± 0.6
    100 Selenomonas noxia-like sp. oral clone CI0020.210.5 ± 1.10.0 ± 0.00.1 ± 0.3
    101 Selenomonas sp. oral clone GI0640.210.0 ± 0.00.7 ± 0.20.0 ± 0.0
    102 Neisseria flava 0.210.3 ± 0.80.1 ± 0.40.2 ± 0.8
    103 Campylobacter hominis 0.210.2 ± 0.50.4 ± 0.90.0 ± 0.0
    104 Corynebacterium sp. oral clone AK1530.190.2 ± 0.50.4 ± 0.90.0 ± 0.0
    105 Streptococcus hyointestinalis 0.190.0 ± 0.00.2 ± 0.60.4 ± 0.9
    106 Streptococcus sp. oral clone CH0160.190.1 ± 0.20.5 ± 0.80.1 ± 0.3
    107 Streptococcus sp. oral clone BM0350.190.4 ± 0.80.0 ± 0.00.1 ± 0.5
    108 Eubacterium saburreum 0.190.4 ± 0.80.1 ± 0.30.0 ± 0.0
    109 Megasphaera micronuciformis 0.190.1 ± 0.50.2 ± 0.60.3 ± 0.8
    110 Selenomonas sp. oral clone EW0760.190.3 ± 0.60.1 ± 0.30.2 ± 0.4
    111 Selenomonas sp. oral clone DD0200.190.3 ± 0.60.1 ± 0.50.1 ± 0.5
    112 Veillonella parvula 0.190.1 ± 0.30.2 ± 0.60.3 ± 0.6
    113 Neisseria genomospecies P1 clone P4PC_200.190.4 ± 1.10.0 ± 0.00.1 ± 0.4
    114 Neisseria pharyngis 0.190.3 ± 0.60.0 ± 0.00.2 ± 0.4
    115 Deferribacteres sp. oral clone BH0070.170.0 ± 0.00.4 ± 0.90.1 ± 0.4
    116 Streptococcus didelphis 0.170.4 ± 0.90.1 ± 0.30.1 ± 0.3
    117 Streptococcus oligofermentans 0.170.1 ± 0.20.4 ± 0.60.1 ± 0.4
    118 Streptococcus sp. oral clone 3097C0.170.1 ± 0.20.1 ± 0.50.4 ± 0.6
    119 Streptococcus sp. oral clone AY0200.170.3 ± 0.60.1 ± 0.40.1 ± 0.3
    120 Streptococcus sp. oral clone BW0090.170.4 ± 0.80.0 ± 0.00.0 ± 0.0
    121 Catonella sp. oral clone EZ0060.170.1 ± 0.20.2 ± 0.80.3 ± 0.8
    122 Johnsonella ignava 0.170.2 ± 0.70.3 ± 0.80.0 ± 0.0
    123 Selenomonas sp. oral clone EW0790.170.2 ± 0.50.1 ± 0.40.2 ± 0.6
    124 Veillonella dispar 0.170.2 ± 0.40.1 ± 0.50.2 ± 0.4
    125 Treponema sp. strain VI:G:G470.170.0 ± 0.00.1 ± 0.50.4 ± 0.9
    126 Treponema sp. strain V:19:D360.170.0 ± 0.00.3 ± 0.70.3 ± 0.8
    127 Deferribacteres sp. oral clone BA1210.150.2 ± 0.70.2 ± 1.00.0 ± 0.0
    128 Gemella sp. oral strain C24KA0.150.1 ± 0.30.2 ± 0.60.1 ± 0.4
    129 Streptococcus sp. oral clone 2061A0.150.1 ± 0.20.1 ± 0.30.4 ± 0.9
    130 Streptococcus uberis 0.150.1 ± 0.20.3 ± 0.60.1 ± 0.4
    131 Dialister sp. oral strain GBA270.150.2 ± 0.40.2 ± 0.40.1 ± 0.3
    132 Eubacterium sp. oral clone EI0740.150.1 ± 0.30.3 ± 0.60.1 ± 0.5
    133 Eubacterium sp. oral clone DO0080.150.1 ± 0.30.0 ± 0.00.4 ± 1.2
    134 Eubacterium sp. oral clone IR0090.150.2 ± 0.70.1 ± 0.30.1 ± 0.5
    135 Megasphaera sp. oral clone BU0570.150.2 ± 0.50.1 ± 0.50.1 ± 0.4
    136 Selenomonas-like sp. oral strain FNA30.150.3 ± 0.70.0 ± 0.00.1 ± 0.3
    • ↵ a The 136 most common species are listed here. For a complete listing of all 260 species detected, see Table S1A in the supplemental material.

    • ↵ b Values are means of baseline and 24-month samples.

Additional Files

  • Figures
  • Tables
  • Supplemental material

    Files in this Data Supplement:

    • Supplemental file 1 - Table S1A, showing data for all 260 species and phylotypes detected (a partial list of species appears in Table 1 of this study).
      MS Word document, 397K.
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Changes in Periodontal Health Status Are Associated with Bacterial Community Shifts as Assessed by Quantitative 16S Cloning and Sequencing
Purnima S. Kumar, Eugene J. Leys, Jennifer M. Bryk, Francisco J. Martinez, Melvin L. Moeschberger, Ann L. Griffen
Journal of Clinical Microbiology Oct 2006, 44 (10) 3665-3673; DOI: 10.1128/JCM.00317-06

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Changes in Periodontal Health Status Are Associated with Bacterial Community Shifts as Assessed by Quantitative 16S Cloning and Sequencing
Purnima S. Kumar, Eugene J. Leys, Jennifer M. Bryk, Francisco J. Martinez, Melvin L. Moeschberger, Ann L. Griffen
Journal of Clinical Microbiology Oct 2006, 44 (10) 3665-3673; DOI: 10.1128/JCM.00317-06
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  • Article
    • ABSTRACT
    • MATERIALS AND METHODS
    • RESULTS
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    • FOOTNOTES
    • REFERENCES
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KEYWORDS

Gingiva
Health Status
RNA, Ribosomal, 16S

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