Clinical Parameters, Subgingival Microbiota, and MMP-8 Expression in Dental Implants and Homologous Teeth: Insights into Peri-Implant and Periodontal HealthEste estudo teve como objetivo avaliar e comparar parâmetros clínicos, a composição da microbiota subgengival e a expressão da metaloproteinase de matriz-8 (MMP-8) entre implantes dentários e dentes homólogos, em condições de saúde e considerando distintos designs de plataforma de implantes. Materiais e Métodos: Um total de 47 pacientes contribuiu com 79 implantes e 79 dentes homólogos. Parâmetros clínicos, incluindo profundidade de sondagem (PS) e dimensões da mucosa ceratinizada (HKM, TKM, e WKM), foram avaliados. Amostras de biofilme subgengival foram submetidas à análise por hibridização DNA-DNA em checkerboard. O fluido crevicular peri-implantar e gengival foi coletado para quantificação de MMP-8. Resultados: Os implantes apresentaram um aumento significativo na PS e redução nas dimensões da mucosa ceratinizada em comparação com os dentes. Embora as cargas microbianas totais fossem comparáveis, os perfis microbiológicos diferiram: Actinomyces naeslundii I, Actinomyces oris, Prevotella intermedia e Treponema denticola foram detectados em níveis mais altos nos dentes. Inversamente, Prevotella nigrescens, Aggregatibacter actinomycetemcomitans A + B e Selenomonas noxia foram mais prevalentes nos implantes. Altos níveis de Aggregatibacter actinomycetemcomitans A + B e Selenomonas noxia foram observados no grupo de Hexágono Externo (HE). É importante ressaltar que a expressão de MMP-8 foi aproximadamente 29% mais alta em implantes do que em dentes (p<0.05), independentemente do design da plataforma do implante. Os níveis de MMP-8 correlacionaram-se exclusivamente com o volume do fluido crevicular, mas não com outros parâmetros clínicos. Conclusões: Implantes dentários diferem dos dentes homólogos, apresentando maior PS, menor altura da mucosa ceratinizada (HKM) e distintas composições microbianas. Embora os níveis totais de bactérias tenham sido semelhantes, os implantes apresentaram níveis elevados de MMP-8 em comparação com os dentes, independentemente da plataforma do implante, sugerindo uma atividade bioquímica distinta mesmo em sítios clinicamente saudáveis
Autoria
person Carla Dias Matos
schoolDental Implant Program, Department of Dentistry, Pontific Catholic University of Minas Gerais (PUC Minas), 30535-901, Belo Horizonte, Brazil Pontific Catholic University of Minas GeraisBrazilBelo Horizonte, BrazilDental Implant Program, Department of Dentistry, Pontific Catholic University of Minas Gerais (PUC Minas), 30535-901, Belo Horizonte, Brazil
person Maria Cândida Dourado Pacheco
schoolDental Implant Program, Department of Dentistry, Pontific Catholic University of Minas Gerais (PUC Minas), 30535-901, Belo Horizonte, Brazil Pontific Catholic University of Minas GeraisBrazilBelo Horizonte, BrazilDental Implant Program, Department of Dentistry, Pontific Catholic University of Minas Gerais (PUC Minas), 30535-901, Belo Horizonte, Brazil
person Marcílio Alves Ferraz
schoolDental Implant Program, Department of Dentistry, Pontific Catholic University of Minas Gerais (PUC Minas), 30535-901, Belo Horizonte, Brazil Pontific Catholic University of Minas GeraisBrazilBelo Horizonte, BrazilDental Implant Program, Department of Dentistry, Pontific Catholic University of Minas Gerais (PUC Minas), 30535-901, Belo Horizonte, Brazil
person João Gabriel Silva Souza
schoolDepartment of Periodontology, Dental Research Division, Guarulhos University, 07043-070, Guarulhos, SP, Brazil Guarulhos UniversityBrazilGuarulhos, SP, BrazilDepartment of Periodontology, Dental Research Division, Guarulhos University, 07043-070, Guarulhos, SP, Brazil school Faculdade Israelita de Ciências da Saúde Albert Einstein, Hospital Israelita Albert Einstein, São Paulo, BrazilHospital Israelita Albert EinsteinBrazilSão Paulo, Brazil Faculdade Israelita de Ciências da Saúde Albert Einstein, Hospital Israelita Albert Einstein, São Paulo, Brazil
person Fernanda Faot
schoolDental Implant Program, Department of Dentistry, Pontific Catholic University of Minas Gerais (PUC Minas), 30535-901, Belo Horizonte, Brazil Pontific Catholic University of Minas GeraisBrazilBelo Horizonte, BrazilDental Implant Program, Department of Dentistry, Pontific Catholic University of Minas Gerais (PUC Minas), 30535-901, Belo Horizonte, Brazil schoolDepartment of Restorative Dentistry - School of Dentistry, Federal University of Pelotas, Pelotas, RS, Brazil Federal University of PelotasBrazilPelotas, RS, BrazilDepartment of Restorative Dentistry - School of Dentistry, Federal University of Pelotas, Pelotas, RS, Brazil
person Karolina Ladeira Felisberto
person Jamil Awad Shibli
schoolDepartment of Periodontology, Dental Research Division, Guarulhos University, 07043-070, Guarulhos, SP, Brazil Guarulhos UniversityBrazilGuarulhos, SP, BrazilDepartment of Periodontology, Dental Research Division, Guarulhos University, 07043-070, Guarulhos, SP, Brazil school Faculdade Israelita de Ciências da Saúde Albert Einstein, Hospital Israelita Albert Einstein, São Paulo, BrazilHospital Israelita Albert EinsteinBrazilSão Paulo, Brazil Faculdade Israelita de Ciências da Saúde Albert Einstein, Hospital Israelita Albert Einstein, São Paulo, Brazilschool Department of Oral Medicine, Infection, and Immunity, Harvard School of Dental Medicine, Boston, Massachusetts, USAHarvard School of Dental MedicineUSABoston, Massachusetts, USA Department of Oral Medicine, Infection, and Immunity, Harvard School of Dental Medicine, Boston, Massachusetts, USAschoolDepartment of Oral Health Sciences, Periodontology, KU Leuven & Dentistry, University Hospitals Leuven, Leuven, BelgiumUniversity Hospitals LeuvenBelgiumLeuven, BelgiumDepartment of Oral Health Sciences, Periodontology, KU Leuven & Dentistry, University Hospitals Leuven, Leuven, Belgium
person Rodrigo Villamarim Soares
schoolDental Implant Program, Department of Dentistry, Pontific Catholic University of Minas Gerais (PUC Minas), 30535-901, Belo Horizonte, Brazil Pontific Catholic University of Minas GeraisBrazilBelo Horizonte, BrazilDental Implant Program, Department of Dentistry, Pontific Catholic University of Minas Gerais (PUC Minas), 30535-901, Belo Horizonte, Brazil
person Elton Gonçalves Zenóbio
schoolDental Implant Program, Department of Dentistry, Pontific Catholic University of Minas Gerais (PUC Minas), 30535-901, Belo Horizonte, Brazil Pontific Catholic University of Minas GeraisBrazilBelo Horizonte, BrazilDental Implant Program, Department of Dentistry, Pontific Catholic University of Minas Gerais (PUC Minas), 30535-901, Belo Horizonte, Brazil
Correspondence: Rodrigo Villamarim Soares Dental Implant Program, Department of Dentistry, Pontific Catholic University of Minas Gerais (PUC Minas), 30535-901, Belo Horizonte, Brazil; e-mail :
soaresrv@pucminas.br
soaresrv@pucminas.br
Responsible Editor
Manoel Damião de Sousa-Neto
SCIMAGO INSTITUTIONS RANKINGS
Dental Implant Program, Department of Dentistry, Pontific Catholic University of Minas Gerais (PUC Minas), 30535-901, Belo Horizonte, Brazil Pontific Catholic University of Minas GeraisBrazilBelo Horizonte, BrazilDental Implant Program, Department of Dentistry, Pontific Catholic University of Minas Gerais (PUC Minas), 30535-901, Belo Horizonte, Brazil
Department of Periodontology, Dental Research Division, Guarulhos University, 07043-070, Guarulhos, SP, Brazil Guarulhos UniversityBrazilGuarulhos, SP, BrazilDepartment of Periodontology, Dental Research Division, Guarulhos University, 07043-070, Guarulhos, SP, Brazil
Faculdade Israelita de Ciências da Saúde Albert Einstein, Hospital Israelita Albert Einstein, São Paulo, BrazilHospital Israelita Albert EinsteinBrazilSão Paulo, Brazil Faculdade Israelita de Ciências da Saúde Albert Einstein, Hospital Israelita Albert Einstein, São Paulo, Brazil
Department of Restorative Dentistry - School of Dentistry, Federal University of Pelotas, Pelotas, RS, Brazil Federal University of PelotasBrazilPelotas, RS, BrazilDepartment of Restorative Dentistry - School of Dentistry, Federal University of Pelotas, Pelotas, RS, Brazil
Figuras | Tabelas
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imageopen_in_new
imageBox 1 Sample Characterization open_in_new
SD - standard deviation; EH: external hexagon implant; IH: internal hexagon
imageFigure 1 MMP-8 levels (pg/uL) in the peri-implant and periodontal crevicular fluid. MMP-8: Matrix Metalloproteinase-8.* Wilcoxon test. Values are expressed as median ± IIQ. open_in_new
imageFigure 2 MMP-8 levels(pg/uL) in the peri-implant crevicular fluid. MMP-8: Matrix Metalloproteinase-8; EH: external hexagon implant; IH: internal hexagon implant. Values are expressed as median ± IIQ.* Wilcoxon test. open_in_new
table_chartTable 1
Peri-implant and periodontal clinical parameters
| Variable | Implants X Homologous teeth | Implant platforms (EH X IH) | ||||||
|---|---|---|---|---|---|---|---|---|
| Dental Implants | Teeth | p | EH | IH | p | |||
| PD (mm)* | 2.00 ± 1.50 | 1.50 ± 1.00 | < 0.001† | 2.00 ± 0.50 | 2.00 ± 1.50 | 0.939 | ||
| WKM (mm)* | 2.00 ± 3.00 | 3.00 ± 3.00 | < 0.001† | 2.00 ± 3.00 | 2.00 ± 3.00 | 0.918 | ||
| TKM (mm)** | 0.88 ± 0.33 | 0.89 ± 0.30 | 0.817‡ | 0.86 ± 0.33 | 0.88 ± 0.52 | 0.721 | ||
| VCF (µL)* | 0.26 ± 0.24 | 0.25 ± 0.00 | 0.079† | 0.26 ± 0.33 | 0.30 ± 0.23 | 0.965 | ||
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PD - probing depth; WKM - width of keratinized mucosa; TKM - thickness of keratinized mucosa; VCF - volume of crevicular fluid; EH: external hexagon implant; IH: internal hexagon implant.
-
*
Values expressed in median ± IIQ; ** Values expressed in average ± SD; † Wilcoxon test; ‡ Paired sample Student t test.
table_chartTable 2
Determination of microorganism levels (x105) in the biofilm samples from implant, tooth, EH implants, and IH implants (Mean±SD).
| Complex | Species | Implants X Homologous | P value* | Implant platforms (EH X IH) | P value* | ||
|---|---|---|---|---|---|---|---|
| Implants | Teeth | EH | IH | ||||
| Actinomyces | A. gerencseriae | 0.55±1.34 | 1.49±2.96 | 0.117 | 0.75±1.59 | 0.32±0.95 | 0.511 |
| A. israelii | 3.82±12.45 | 4.72±12.50 | 0.117 | 2.56±3.11 | 5.30±18.07 | 0.935 | |
| A. naeslundii I | 0.13±0.64 | 1.50±2.96 | 0.001* | 0.17±0.84 | 0.09±0.25 | 0.636 | |
| A. oris | 0.71±1.86 | 1.89±3.42 | 0.012* | 0.91±2.25 | 0.49±1.27 | 0.904 | |
| Purple | A. odontolyticus | 0.25±0.89 | 0.76±1.72 | 0.103 | 0.42±1.19 | 0.06±0.18 | 0.477 |
| V. parvula | 3.76±17.43 | 3.84±17.42 | 0.580 | 3.87±16.98 | 3.62±18.23 | 0.456 | |
| Yellow | S. gordonii | 0.20±0.88 | 0.37±1.50 | 0.618 | 0.22±0.86 | 0.18±0.91 | 0.363 |
| S. intermedius | 0.42±1.83 | 0.22±0.89 | 0.692 | 0.48±1.86 | 0.35±1.82 | 0.583 | |
| S. mitis | 0.46±1.61 | 0.37±1.50 | 0.696 | 0.81±2.14 | 0.05±0.18 | 0.288 | |
| S. oralis | 0.27±0.90 | 0.28±1.38 | 0.385 | 0.41±1.19 | 0.11±0.30 | 0.242 | |
| S. sanguinis | 0.37±1.21 | 0.51±1.70 | 0.744 | 0.39±1.19 | 0.35±1.27 | 0.412 | |
| Green | A. actinomycetemcomitans A + B | 0.01±0.03 | 0.01±0.03 | 1.000 | 0.01±0.04 | 0.00±0.00 | 0.033 |
| C. gingivalis | 0.32±1.07 | 0.70±1.87 | 0.194 | 0.41±1.19 | 0.22±0.92 | 0.865 | |
| C. ochracea | 0.01±0.03 | 0.25±1.38 | 0.235 | 0.01±0.04 | 0.01±0.03 | 0.603 | |
| C. sputigena | 1.23±2.54 | 1.24±2.82 | 0.652 | 1.43±2.47 | 0.98±2.63 | 0.530 | |
| E. corrodens | 0.08±0.27 | 0.30±1.39 | 0.449 | 0.09±0.28 | 0.07±0.25 | 0.430 | |
| Orange | C. gracilis | 0.67±1.65 | 0.51±1.61 | 0.827 | 0.89±1.90 | 0.42±1.27 | 0.882 |
| C. rectus | 0.08±0.62 | 0.04±0.17 | 0.564 | 0.01±0.02 | 0.17±0.91 | 0.503 | |
| C. showae | 0.08±0.62 | 0.06±0.24 | 0.567 | 0.01±0.03 | 0.17±0.91 | 0.546 | |
| E. nodatum | 2.78±12.50 | 4.87±17.35 | 0.145 | 1.42±3.01 | 4.36±18.16 | 0.261 | |
| F. nuc ss nucleatum | 1.00±2.56 | 1.45±2.64 | 0.306 | 0.81±2.13 | 1.22±3.00 | 0.317 | |
| F. nuc ss polymorphum | 0.42±1.22 | 0.56±1.46 | 0.809 | 0.43±1.19 | 0.41±1.27 | 0.973 | |
| F. nuc ss vincentii | 6.80±24.12 | 5.72±21.07 | 0.717 | 6.44±23.47 | 7.22±25.25 | 0.177 | |
| F. periodonticum | 0.21±1.25 | 0.32±1.07 | 0.179 | 0.10±0.28 | 0.35±1.82 | 0.940 | |
| M. micra | 3.68±17.41 | 3.69±17.41 | 0.959 | 3.73±16.95 | 3.61±18.23 | 0.688 | |
| P. intermédia | 0.96±2.63 | 1.57±12.40 | 0.014* | 0.91±2.56 | 1.02±2.75 | 0.313 | |
| P. nigrescens | 1.44±2.98 | 0.48±1.92 | 0.024* | 1.75±3.18 | 1.08±2.74 | 0.861 | |
| S. constellatus | 0.32±1.07 | 0.14±0.65 | 0.351 | 0.38±1.19 | 0.25±0.93 | 0.950 | |
| Red | T. forsythia | 0.28±1.39 | 0.44±1.61 | 0.163 | 0.21±0.87 | 0.37±1.83 | 0.304 |
| P. gingivalis | 0.32±1.39 | 0.15±0.66 | 0.448 | 0.41±1.70 | 0.21±0.92 | 0.220 | |
| T. denticola | 2.01±2.33 | 3.18±3.38 | 0.008* | 2.03±2.34 | 1.98±2.36 | 0.939 | |
| Other species | E. saburreum | 0.10±0.63 | 0.17±0.67 | 0.307 | 0.18±0.86 | <0.01±0.02 | 0.072 |
| G. morbillorum | 0.38±1.22 | 0.54±1.45 | 0.330 | 0.64±1.61 | 0.09±0.25 | 0.639 | |
| L. buccalis | 0.46±1.34 | 0.83±2.20 | 0.303 | 0.53±1.42 | 0.37±1.27 | 0.276 | |
| N. mucosa | 0.98±2.24 | 1.78±3.18 | 0.059 | 1.01±2.23 | 0.95±2.28 | 0.905 | |
| P. melaninogenica | 1.01±2.12 | 0.99±2.23 | 0.954 | 1.27±2.41 | 0.70±1.72 | 0.760 | |
| P. acnes I + II | <0.01±0.02 | 0.01±0.02 | 0.317 | 0.01±0.02 | 0.00±0.00 | 0.187 | |
| S. noxia | 0.12±0.64 | 0.14±0.65 | 0.606 | 0.21±0.87 | <0.01±0.02 | 0.023* | |
| S. anginosus | 0.56±2.18 | 0.34±1.50 | 0.714 | 0.59±2.35 | 0.52±2.01 | 0.964 | |
| T. socranskii | 1.88±2.68 | 5.56±17.29 | 0.807 | 2.28±2.86 | 1.43 ± 2.43 | 0.151 | |
-
SD: Standard deviation; * Wilcoxon test.
table_chartTable 3
Correlations between microorganism levels and clinical parameters in implant and homologous teeth samples
| Implant variables | PD | HKM | TKM | |||
|---|---|---|---|---|---|---|
| rspearman | p-value | rspearman | p-value | rspearman | p-value | |
| A. naeslundii I | 0.02 | NS | - 0.36 | 0.003 | - 0.16 | NS |
| C. gingivalis | 0.19 | NS | - 0.25 | 0.045 | - 0.12 | NS |
| F. nuc ss polymorphum | 0.26 | 0.039 | - 0.26 | 0.035 | - 0.14 | NS |
| F. nuc ss vincentii | 0.28 | 0.022 | - 0.20 | NS | 0.02 | NS |
| F. periodonticum | 0.04 | NS | - 0. 23 | NS | - 0.25 | 0.042 |
| M. micra | 0.25 | 0.048 | - 0.17 | NS | - 0.20 | NS |
| P. nigrescens | 0.23 | NS | - 0.28 | 0.022 | - 0.26 | 0.040 |
| T. forsythia | 0.08 | NS | - 0.26 | 0.039 | - 0.13 | NS |
| T. denticola | - 0.02 | NS | - 0.33 | 0.008 | - 0.08 | NS |
| G. morbillorum | 0.09 | NS | - 0.41 | 0.001 | - 0.18 | NS |
| N. mucosa | 0.06 | NS | - 0.19 | NS | - 0.43 | <0.001 |
| Actinomyces group | - 0.11 | NS | - 0.26 | 0.036 | - 0.16 | NS |
| Yellow complex | 0.17 | NS | - 0.27 | 0.027 | - 0.06 | NS |
| Red complex | 0.03 | NS | - 0.33 | 0.008 | - 0.09 | NS |
| Other species | 0.06 | NS | - 0.27 | 0.032 | - 0.28 | 0.026 |
| Total | 0.10 | NS | - 0.26 | 0.038 | - 0.22 | NS |
| Homologous teeth variables | ||||||
| S. intermedius | - 0.03 | 0.033 | - 0.26 | 0.040 | 0.01 | NS |
| F. nuc ss nucleatum | 0.06 | NS | - 0.32 | 0.010 | 0.10 | NS |
| M. micra | 0.08 | NS | - 0.26 | 0.037 | 0.02 | NS |
| P. nigrescens | 0.02 | NS | - 0.27 | 0.030 | - 0.07 | NS |
| T. denticola | - 0.21 | NS | - 0.26 | 0.034 | - 0.12 | NS |
| E. saburreum | 0.09 | NS | - 0.31 | 0.013 | 0.07 | NS |
| S. anginosus | 0.03 | NS | - 0.28 | 0.025 | 0.03 | NS |
| Red complex | - 0.17 | NS | - 0.25 | 0.044 | - 0.13 | NS |
| EH Implants variables | ||||||
| A. naeslundii I | 0.03 | NS | - 0.38 | 0.024* | - 0.20 | NS |
| P. nigrescens | 0.23 | NS | - 0.41 | 0.015* | - 0.02 | NS |
| T. denticola | 0.00 | NS | - 0.38 | 0.026* | - 0.16 | NS |
| G. morbillorum | 0.17 | NS | - 0.37 | 0.027* | 0.05 | NS |
| Actinomyces | 0.07 | NS | - 0.34 | 0.045* | - 0.15 | NS |
| Red complex | 0.07 | NS | - 0.36 | 0.034* | - 0.16 | NS |
| IH Implant variables | ||||||
| A. israelii | - 0.44 | 0.015* | - 0.02 | NS | - 0.22 | NS |
| C. gingivalis | 0.09 | NS | - 0.42 | 0.021* | - 0.18 | NS |
| F. periodonticum | - 0.08 | NS | - 0.11 | NS | - 0.40 | 0.028* |
| P. nigrescens | 0.24 | NS | - 0.10 | NS | - 0.50 | 0.005* |
| G. morbillorum | 0.02 | NS | - 0.46 | 0.011* | - 0.46 | 0.010* |
| N. mucosa | - 0.16 | NS | - 0.02 | NS | - 0.65 | < 0.001* |
| Other species | 0.05 | NS | - 0.23 | NS | - 0.37 | 0.044* |
-
PD: probing depth; HKM: height of keratinized mucosa; TKM: thickness of keratinized mucosa; NS: not significant.
table_chartTable 4
Correlation between MMP-8 expression levels and clinical parameters
| Variables | Dental Implants | p-value | Teeth | p-value | EH | p-value | IH | p-value |
|---|---|---|---|---|---|---|---|---|
| PD | 0.05 | p = 0.700 | -0.04 | p = 0.741 | 0.08 | p = 0.642 | 0.07 | p = 0.742 |
| WKM | -0.16 | p = 0.232 | 0.17 | p = 0.199 | -0.18 | p = 0.277 | -0.04 | p = 0.864 |
| TKM | -0.05 | p = 0.733 | 0.01 | p = 0.968 | 0.07 | p = 0.674 | -0.24 | p = 0.280 |
| VCF | -0.59 | p < 0.001 | -0.71 | p < 0.001 | -0.62 | p < 0.001 | -0.50 | p = 0.017 |
-
Spearman rank correlation coefficient; MMP-8: Matrix Metalloproteinase-8; PD - probing depth; WKM - width of keratinized mucosa; TKM - thickness of keratinized mucosa; VCF -the volume of crevicular fluid; EH: external hexagon implant; IH: internal hexagon implant.
table_chartTable 5
MMP-8 concentration according to the categories of WKM and TKM
| Variable | Dental Implants | p-value* | Teeth | p* |
|---|---|---|---|---|
| WKM | ||||
| < 2 mm | 15515 ± 23971 | 0.466 | 9725 ± 6892 | 0.256 |
| ≥ 2 mm | 14268 ± 24924 | 12637 ± 9495 | ||
| TKM | ||||
| < 1 mm | 14294 ± 24228 | 0.674 | 9725 ± 8594 | .381 |
| ≥ 1 mm | 13796 ± 29291 | 12754 ± 13968 |
-
MMP-8: Matrix Metalloproteinase-8; Median ± IIQ; WKM - width of keratinized mucosa; TKM - thickness of keratinized mucosa. * Mann-Whitney U test.
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