Characterization of the Subgingival Cultivable Microbiota in Patients with Different Stages of Periodontitis in Spain and Colombia. A Cross-Sectional Study
Abstract
:1. Introduction
2. Materials and Methods
2.1. Subjects
2.1.1. Inclusion Criteria
- Health and gingivitis subjects, as controls. No clinical attachment loss (CAL) nor radiographical bone loss (RBL) and probing depths (PD) ≤ 3 mm, assuming no pseudo pockets [25].
- Periodontitis in stages I or II. Following the criteria for severity, interdental CAL of 1–2 mm (stage I) or 3–4 mm (stage II) and RBL affecting only the coronal third of the root (<15 % for stage I and 15–33% for stage II) [2].
- Periodontitis in stages III or IV. Following the criteria for severity, interdental CAL ≥5 mm and RBL extending to middle or apical third of the root. There should be evidence of tooth loss ≤ 4 teeth due to periodontal reasons in stage III, and ≥5 teeth in stage IV [2]. If needed, and using the criteria for complexity, furcation involvement class II or III.
2.1.2. Exclusion Criteria
- Periodontal treatment in the previous year.
- Acute periodontal conditions such as periodontal abscesses or necrotizing periodontal diseases, at the time of the screening.
- Having taken antibiotics in the previous 3 months.
- Systemic diseases or conditions (diabetes, quantitative and/or qualitative polymorphonuclear neutrophil defects, other immune system disorders).
- Pregnant women.
- Chronic use of anti-inflammatories, anticonvulsants, immunosuppressants, calcium channel blockers, upon sample collection for the study, or 6 months prior to the study.
2.2. Study Visit
2.3. Clinical Variables
- Gingival recession (REC), measured as the distance from the cementoenamel junction (CEJ) to the gingival margin and recorded to the nearest millimetre.
- PD, measured from the gingival margin to the bottom of the sulcus/pocket and recorded to the nearest millimetre.
- CAL, measured as the distance from the bottom of the pocket to the CEJ.
- Bleeding on probing (BoP), measured after probing to the base of the pocket and expressed as a percentage [26].
- Plaque index (PlI), evaluated by the presence of visible dental plaque, disclosed by erythrosine staining (Plac-Control®, Dentaid, Barcelona, Spain) and expressed as a percentage [27].
2.4. Microbiological Variables
2.4.1. Microbiological Sampling
- In healthy/gingivitis subjects, subgingival samples were taken from the mesio-buccal sites of the first molars and, when absent, from the adjacent second molars (the next alternative was the second premolars and from there, any teeth present mesially).
- In subjects with periodontitis, subgingival samples were taken from the most accessible site with the deepest PD and BoP, per quadrant.
2.4.2. Microbiological Processing
2.5. Statistical Analysis
2.5.1. Calibration
2.5.2. Sample Size Calculation
2.5.3. Statistical Analysis
3. Results
3.1. Study Population
3.2. Clinical Outcome Variables
3.3. Subgingival Cultivable Microbiota-Total Anaerobic Counts
3.4. Subgingival Cultivable Microbiota-Periodontal Pathogens
3.5. Impact of Periodontal Status, Country, Smoking and Age
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Periodontal Status | Age | Spain (n) | Colombia (n) | |
---|---|---|---|---|
Selected subjects by country | 90 | 77 | ||
Selected subjects by periodontal status group and country | Health and Gingivitis | 30 | 18 | |
Periodontitis I-II | 30 | 23 | ||
Periodontitis III-IV | 30 | 36 | ||
Selected subjects by periodontal status group, age and country | Health and Gingivitis | 30–40 | 10 | 7 |
41–50 | 10 | 5 | ||
51–60 | 10 | 6 | ||
Periodontitis I-II | 30–40 | 10 | 11 | |
41–50 | 10 | 6 | ||
51–60 | 10 | 6 | ||
Periodontitis III-IV | 30–40 | 10 | 11 | |
41–50 | 10 | 16 | ||
51–60 | 10 | 9 |
Age a | Gender b | Smoking b | |||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Comparison | First Comparison | Second Comparison | n | Mean (SD) | p Value | n | Female % | n | Male % | p Value | n | Non Smokers % | n | Smokers % | p Value |
Periodontal status group | Health and Gingivitis | 48 | 45.13 (9.71) | 0.170 | 26 | 54.2 | 22 | 45.8 | 0.409 | 43 | 89.6 | 5 | 10.4 | 0.064 | |
Periodontitis I-II | 53 | 43.72 (8.77) | 30 | 56.6 | 23 | 43.4 | 43 | 81.1 | 10 | 18.9 | |||||
Periodontitis III-IV | 66 | 45.32 (8.00) | 31 | 47.0 | 35 | 53.0 | 50 | 75.8 | 16 | 24.2 | |||||
Periodontal status by country | Health and Gingivitis | Spain | 30 | 44.97 (8.28) | 0.588 | 16 | 53.3 | 14 | 46.7 | 1.000 | 27 | 90.0 | 3 | 10.0 | 0.045, Periodontitis I-II (Colombia) versus Periodontitis III-IV (Spain) |
Colombia | 18 | 45.39 (11.99) | 10 | 55.6 | 8 | 44.4 | 16 | 88.9 | 2 | 11.1 | |||||
Periodontitis I-II | Spain | 30 | 45.17 (8.04) | 16 | 53.3 | 14 | 46.7 | 21 | 70.0 | 9 | 30.0 | ||||
Colombia | 23 | 41.83 (9.49) | 14 | 60.9 | 9 | 39.1 | 22 | 95.7 | 1 | 4.3 | |||||
Periodontitis III-IV | Spain | 30 | 46.33 (8.25) | 15 | 50.0 | 15 | 50.0 | 18 | 60.0 | 12 | 40.0 | ||||
Colombia | 36 | 44.47 (7.81) | 16 | 44.4 | 20 | 55.6 | 32 | 88.9 | 4 | 11.1 |
Health and Gingivitis a | Periodontitis I-II a | Periodontitis III-IV a | Second Comparison (among Periodontal Status b) | ||||||||
---|---|---|---|---|---|---|---|---|---|---|---|
First Comparison | n | Mean (SD) | p Value | n | Mean (SD) | p Value | n | Mean (SD) | p Value | p Value | |
PD (mm) | Spain | 30 | 2.26 (0.31) | 0.359 | 30 | 2.90 (0.39) | 0.037 | 30 | 4.04 (0.76) | 0.069 | <0.001 |
Colombia | 18 | 2.17 (0.27) | 23 | 3.19 (0.57) | 36 | 3.72 (0.65) | |||||
PD 1–3 mm (%) | Spain | 30 | 98.37 (3.14) | 0.148 | 30 | 77.38 (14.17) | 0.073 | 30 | 43.08 (21.77) | 0.083 | <0.001 |
Colombia | 18 | 94.83 (12.62) | 23 | 68.42 (21.38) | 36 | 50.19 (9.73) | |||||
PD 4–5 mm (%) | Spain | 30 | 1.60 (3.12) | 0.145 | 30 | 20.78 (12.71) | 0.110 | 30 | 38.04 (14.06) | 0.170 | <0.001 |
Colombia | 18 | 5.16 (12.62) | 23 | 24.07 (17.07) | 36 | 33.41 (13.00) | |||||
PD ≥ 6 mm (%) | Spain | 30 | 0.01 (0.10) | 0.445 | 30 | 1.82 (2.06) | 0.174 | 30 | 18.86 (14.52) | 0.424 | <0.001, Health and Gingivitis versus Periodontitis III-IV <0.001, Periodontitis I-II versus Periodontitis III-IV |
Colombia | 18 | 0 | 23 | 3.19 (4.91) | 36 | 16.36 (10.66) | |||||
CAL (mm) | Spain | 30 | 0.33 (0.24) | 0.521 | 30 | 3.07 (0.39) | 0.660 | 30 | 4.78 (0.85) | 0.237 | <0.001 |
Colombia | 18 | 0.28 (0.26) | 23 | 3.16 (0.96) | 36 | 4.52 (0.93) | |||||
BoP (%) | Spain | 30 | 15.53 (15.01) | 0.251 | 30 | 32.71 (17.01) | <0.001 | 30 | 63.87 (26.33) | 0.024 | <0.001 |
Colombia | 18 | 10.94 (9.45) | 23 | 68.82 (38.93) | 36 | 79.69 (28.65) | |||||
PlI (%) | Spain | 30 | 50.97 (25.07) | <0.001 | 30 | 62.69 (25.59) | 0.736 | 30 | 76.00 (24.20) | 0.465 | <0.001, Health and Gingivitis versus Periodontitis I-II <0.001, Health and Gingivitis versus Periodontitis III-IV |
Colombia | 18 | 22.77 (13.78) | 23 | 65.86 (38.77) | 36 | 70.27 (36.49) |
Comparison | First Comparison | Second Comparison | n | Mean (SD) | Mean Difference | 95% CI | p Value a | |
---|---|---|---|---|---|---|---|---|
Lower Bound | Upper Bound | |||||||
Periodontal status group | Health and Gingivitis | 48 | 6.29 (0.73) | −0.31 * | −0.60 | −0.02 | 0.029 | |
Periodontitis I-II | 53 | 6.60 (0.55) | −0.02 † | −0.29 | 0.24 | 1.000 | ||
Periodontitis III-IV | 66 | 6.63 (0.53) | −0.34 ‡ | −0.61 | −0.60 | 0.010 | ||
Country | Spain | 90 | 6.43 (0.64) | −0.20 § | −0.38 | −0.01 | 0.036 | |
Colombia | 77 | 6.63 (0.56) | ||||||
Periodontal status by country | Health and Gingivitis | Spain | 30 | 5.99 (0.67) | −0.80 § | −1.18 | −0.43 | <0.001 |
Colombia | 18 | 6.79 (0.51) | ||||||
Periodontitis I-II | Spain | 30 | 6.57 (0.46) | −0.09 § | −0.40 | 0.22 | 0.565 | |
Colombia | 23 | 6.66 (0.67) | ||||||
Periodontitis III-IV | Spain | 30 | 6.74 (0.53) | 0.20 § | −0.05 | 0.46 | 0.115 | |
Colombia | 36 | 6.54 (0.51) |
Periodontal Status (Group) | Country | Counts a | Proportions a | Frequency b | ||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
n | Mean (SD) | Median (IR) | p Value | n | Mean (SD) | Median (IR) | p Value | n (%) | p Value | |||
Porphyromonas gingivalis | Health and Gingivitis | 48 | 2.34 (2.66) | 0.00 (5.48) | 0.014 * | 48 | 5.88 (12.22) | 0.00 (6.75) | 0.007 * | 22 (45.8) | 0.006 * | |
Periodontitis I-II | 53 | 4.15 (2.51) | 5.00 (3.77) | 1.000 † | 53 | 14.57 (20.67) | 3.72 (18.50) | 0.512 † | 40 (75.5) | 0.123 † | ||
Periodontitis III-IV | 66 | 3.38 (2.97) | 5.00 (6.07) | 0.062 ‡ | 66 | 10.28 (15.08) | 3.27 (17.29) | 0.195 ‡ | 38 (57.6) | 0.645 ‡ | ||
Spain | 90 | 4.34 (2.33) | 5.12 (1.95) | <0.001 § | 90 | 13.28 (17.52) | 5.83 (18.16) | <0.001 § | 72 (80.0) | <0.001 § | ||
Colombia | 77 | 2.14 (2.88) | 0.00 (5.60) | 77 | 6.99 (14.93) | 0.00 (5.06) | 28 (36.4) | |||||
Prevotella intermedia | Health and Gingivitis | 48 | 3.55 (2.48) | 4.15 (5.78) | 0.294 | 48 | 5.59 (8.59) | 0.92 (5.22) | 0.497 | 35 (72.9) | 0.978 * | |
Periodontitis I-II | 53 | 3.95 (2.11) | 4.69 (2.24) | 53 | 4.97 (8.48) | 0.90 (5.66) | 43 (81.1) | 1.000 † | ||||
Periodontitis III-IV | 66 | 4.17 (2.30) | 5.00 (1.95) | 66 | 7.15 (10.24) | 2.33 (12.11) | 52 (78.8) | 1.000 ‡ | ||||
Spain | 90 | 3.56 (2.14) | 4.00 (2.77) | <0.001§ | 90 | 3.16 (6.39) | 0.66 (3.33) | <0.001§ | 70 (77.8) | 0.982 § | ||
Colombia | 77 | 4.35 (2.41) | 5.43 (1.75) | 77 | 9.35 (10.86) | 5.11 (13.59) | 60 (77.9) | |||||
Tannerella forsythia | Health and Gingivitis | 48 | 2.33 (2.73) | 0.00 (5.58) | 0.335 | 48 | 3.84 (7.10) | 0.00 (5.31) | 0.160 | 21 (43.8) | 0.939 * | |
Periodontitis I-II | 53 | 1.72 (2.45) | 0.00 (4.65) | 53 | 0.89 (1.87) | 0.00 (0.79) | 18 (34.0) | 1.000 † | ||||
Periodontitis III-IV | 66 | 1.83 (2.47) | 0.00 (4.81) | 66 | 0.87 (1.77) | 0.00 (1.02) | 24 (36.4) | 1.000 ‡ | ||||
Spain | 90 | 1.40 (2.18) | 0.00 (4.30) | <0.001 § | 90 | 0.57 (1.63) | 0.00 (0.65) | <0.001 § | 27 (30.0) | 0.026 § | ||
Colombia | 77 | 2.57 (2.78) | 0.00 (5.60) | 77 | 3.09 (5.79) | 0.00 (3.70) | 36 (46.8) | |||||
Parvimonas micra | Health and Gingivitis | 48 | 1.77 (2.57) | 0.00 (5.03) | 0.503 * | 48 | 2.34 (6.27) | 0.00 (2.41) | 0.633 * | 16 (33.3) | 1.000 * | |
Periodontitis I-II | 53 | 1.19 (2.23) | 0.00 (0.00) | 0.275 † | 53 | 1.57 (4.12) | 0.00 (0.00) | 0.271 † | 12 (22.6) | 0.225 † | ||
Periodontitis III-IV | 66 | 0.52 (1.55) | 0.00 (0.00) | 0.006 ‡ | 66 | 0.57 (2.54) | 0.00 (0.00) | 0.009 ‡ | 7 (10.6) | 0.009 ‡ | ||
Spain | 90 | 0.42 (1.36) | 0.00 (0.00) | <0.001 § | 90 | 0.28 (1.59) | 0.00 (0.00) | <0.001 § | 8 (8.9) | <0.001 § | ||
Colombia | 77 | 1.88 (2.61) | 0.00 (5.14) | 77 | 2.70 (6.04) | 0.00 (3.26) | 27 (35.1) | |||||
Fusobacterium nucleatum | Health and Gingivitis | 48 | 4.48 (1.24) | 4.69 (1.13) | 0.111 | 48 | 3.63 (3.37) | 2.58 (4.19) | 0.951 | 46 (95.8) | 0.822 * | |
Periodontitis I-II | 53 | 4.52 (1.74) | 5.04 (1.08) | 53 | 4.66 (5.53) | 2.45 (5.15) | 47 (88.7) | 1.000 † | ||||
Periodontitis III-IV | 66 | 4.54 (1.91) | 5.00 (1.14) | 66 | 8.24 (13.55) | 2.65 (9.20) | 58 (87.9) | 0.564 ‡ | ||||
Spain | 90 | 4.16 (1.58) | 4.60 (1.04) | <0.001 § | 90 | 2.58 (2.90) | 1.95 (2.97) | <0.001 § | 81 (90.0) | 0.842 § | ||
Colombia | 77 | 4.94 (1.71) | 5.39 (1.19) | 77 | 9.52 (12.57) | 4.17 (9.06) | 70 (90.9) | |||||
Campylobacter rectus | Health and Gingivitis | 48 | 0.23 (0.91) | 0.00 (0.00) | 0.876 | 48 | 0.18 (0.88) | 0.00 (0.00) | 0.849 | 3 (6.3) | 1.000 * | |
Periodontitis I-II | 53 | 0.20 (1.03) | 0.00 (0.00) | 53 | 0.53 (3.42) | 0.00 (0.00) | 2 (3.8) | 1.000 † | ||||
Periodontitis III-IV | 66 | 0.20 (0.94) | 0.00 (0.00) | 66 | 0.07 (0.37) | 0.00 (0.00) | 3 (4.5) | 1.000 ‡ | ||||
Spain | 90 | 0.39 (1.28) | 0.00 (0.00) | <0.001 § | 90 | 0.46 (2.70) | 0.00 (0.00) | <0.001 § | 8 (8.9) | 0.008 § | ||
Colombia | 77 | 0.00 (0.00) | 0.00 (0.00) | 77 | 0.00 (0.00) | 0.00 (0.00) | 0 (0.0) | |||||
Eikenella corrodens | Health and Gingivitis | 48 | 1.03 (1.89) | 0.00 (2.25) | 0.048 * | 48 | 0.35 (0.91) | 0.00 (0.09) | 0.039 * | 12 (25.0) | 0.051 * | |
Periodontitis I-II | 53 | 0.37 (1.18) | 0.00 (0.00) | 1.000 † | 53 | 0.07 (0.37) | 0.00 (0.00) | 1.000 † | 5 (9.4) | 1.000 † | ||
Periodontitis III-IV | 66 | 0.47 (1.53) | 0.00 (0.00) | 0.074 ‡ | 66 | 0.45 (1.85) | 0.00 (0.00) | 0.066 ‡ | 6 (9.1) | 0.033 ‡ | ||
Spain | 90 | 0.66 (1.53) | 0.00 (0.00) | 0.343 § | 90 | 0.19 (0.75) | 0.00 (0.00) | 0.355 § | 15 (16.7) | 0.241 § | ||
Colombia | 77 | 0.53 (1.60) | 0.00 (0.00) | 77 | 0.43 (1.70) | 0.00 (0.00) | 8 (10.4) | |||||
Capnocytophaga spp. | Health and Gingivitis | 48 | 2.36 (2.74) | 0.00 (5.43) | 0.727 | 48 | 3.30 (6.31) | 0.00 (4.24) | 0.889 | 21 (43.8) | 1.000 * | |
Periodontitis I-II | 53 | 2.55 (2.77) | 0.00 (5.30) | 53 | 4.94 (11.23) | 0.00 (4.47) | 25 (47.2) | 1.000 † | ||||
Periodontitis III-IV | 66 | 2.31 (2.61) | 0.00 (5.12) | 66 | 4.14 (11.22) | 0.00 (3.33) | 30 (45.5) | 1.000 ‡ | ||||
Spain | 90 | 0.74 (1.68) | 0.00 (0.00) | <0.001 § | 90 | 0.15 (0.63) | 0.00 (0.00) | <0.001 § | 15 (16.7) | <0.001 § | ||
Colombia | 77 | 4.34 (2.31) | 5.30 (1.39) | 77 | 8.83 (13.34) | 4.17 (9.34) | 61 (79.2) | |||||
Actinomyces odontolyticus | Health and Gingivitis | 48 | 2.24 (2.94) | 0.00 (5.71) | 0.374 | 48 | 6.95 (10.96) | 0.00 (12.56) | 0.278 | 18 (37.5) | 1.000 * | |
Periodontitis I-II | 53 | 2.14 (2.81) | 0.00 (5.37) | 53 | 5.82 (9.97) | 0.00 (10.62) | 20 (37.7) | 0.399 † | ||||
Periodontitis III-IV | 66 | 2.14 (2.81) | 4.15 (5.63) | 66 | 10.48 (17.67) | 0.65 (16.12) | 34 (51.5) | 0.414 ‡ | ||||
Spain | 90 | 0.00 (0.00) | 0.00 (0.00) | <0.001 § | 90 | 0.00 (0.00) | 0.00 (0.00) | <0.001 § | 0 (0.00) | <0.001 § | ||
Colombia | 77 | 5.35 (1.59) | 5.69 (1.24) | 77 | 17.33 (15.95) | 13.87 (20.47) | 72 (93.5) |
Adjusted Model | Coefficient | p Value | OR | 95% CI | ||||
---|---|---|---|---|---|---|---|---|
Whole Cohort | Stratification by Age Ranges | |||||||
Porphyromonas gingivalis | Spain | 2.35 | <0.001 | 10.48 | 4.59 | 23.89 | ||
Periodontitis I-II | 2.13 | <0.001 | 8.43 | 2.93 | 24.19 | |||
Periodontitis III-IV | 1.23 | 0.010 | 3.44 | 1.35 | 8.78 | |||
30–40 years | Spain | 2.02 | 0.001 | 7.60 | 2.34 | 24.67 | ||
41–50 years | Spain | 1.91 | 0.002 | 6.80 | 2.07 | 22.29 | ||
51–60 years | Spain | 2.52 | 0.003 | 12.4 | 2.36 | 65.45 | ||
Periodontitis I-II | 2.69 | 0.010 | 14.7 | 1.90 | 114.05 | |||
Periodontitis III-IV | 2.08 | 0.027 | 8.01 | 1.26 | 50.83 | |||
Parvimonas micra | Colombia | 2.12 | <0.001 | 8.32 | 3.23 | 21.45 | ||
Health and gingivitis | 2.03 | <0.001 | 7.68 | 2.53 | 23.32 | |||
Periodontitis I-II | 1.22 | 0.026 | 3.41 | 1.15 | 10.05 | |||
30–40 years | Colombia | 2.35 | 0.002 | 10.58 | 2.33 | 48.04 | ||
Health and Gingivitis | 2.89 | 0.005 | 18.1 | 2.39 | 137.02 | |||
Periodontitis I-II | 2.06 | 0.027 | 7.91 | 1.25 | 49.71 | |||
Capnocytophagaspp. | Colombia | 2.94 | <0.001 | 19.0 | 8.72 | 41.63 | ||
30–40 years | Colombia | 3.44 | <0.001 | 31.2 | 7.50 | 130.17 | ||
41–50 years | Colombia | 2.07 | 0.001 | 8.00 | 2.40 | 26.56 | ||
51–60 years | Colombia | 3.66 | <0.001 | 39.0 | 7.72 | 195.71 |
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Pianeta, R.; Iniesta, M.; Castillo, D.M.; Lafaurie, G.I.; Sanz, M.; Herrera, D. Characterization of the Subgingival Cultivable Microbiota in Patients with Different Stages of Periodontitis in Spain and Colombia. A Cross-Sectional Study. Microorganisms 2021, 9, 1940. https://doi.org/10.3390/microorganisms9091940
Pianeta R, Iniesta M, Castillo DM, Lafaurie GI, Sanz M, Herrera D. Characterization of the Subgingival Cultivable Microbiota in Patients with Different Stages of Periodontitis in Spain and Colombia. A Cross-Sectional Study. Microorganisms. 2021; 9(9):1940. https://doi.org/10.3390/microorganisms9091940
Chicago/Turabian StylePianeta, Roquelina, Margarita Iniesta, Diana Marcela Castillo, Gloria I. Lafaurie, Mariano Sanz, and David Herrera. 2021. "Characterization of the Subgingival Cultivable Microbiota in Patients with Different Stages of Periodontitis in Spain and Colombia. A Cross-Sectional Study" Microorganisms 9, no. 9: 1940. https://doi.org/10.3390/microorganisms9091940