You are on page 1of 11

334 PERI-IMPLANT DISEASE • FERREIRA JR et al

Clinical, Histological, and Microbiological


Findings in Peri-Implant Disease:
A Pilot Study
Samuel Barros Ferreira, Jr., DDS,* Caio Márcio Figueiredo, DDS, MSc,†
Ana Lúcia Pompéia Fraga Almeida, DDS, MSc, PhD,‡ Gerson Francisco Assis, MSc, PhD,§ Thiago José Dionísio,储
and Carlos Ferreira Santos, DDS, MSc, PhD¶

eri-implant disease is defined as Objectives: This study is intended and the HI, except for the mPI on the

P an inflammatory process on the


soft tissues around implants.1
Dental implants do not have a periodon-
to verify the correlation among clini-
cal indices of the peri-implant soft tis-
sues, the histological condition and
central area of lingual aspects (r ⫽
0.85, P ⫽ 0.0029). There was a ten-
dency for a positive correlation
tal ligament2 and the connective tissue the presence of 3 pathogens commonly between the mPI on the central area of
around dental implants is differently ar-
associated with peri-implant diseases buccal aspects and the HI (r ⫽ 0.63,
ranged when compared with natural
teeth.3 Despite these differences, similar (Aggregatibacter actinomycetem- P ⫽ 0.0544). The counting of lympho-
characteristics between periodontal and comitans, Porphyromonas gingivalis, cytes and plasmocytes correlated pos-
peri-implant diseases exist.4 Thus, clin- and Tannerella forsythia). itively with HI, thus suggesting the
ical indices used to assess periodontal Materials: Four clinical indices, index reliability. The prevalence of A.
disease can also be used to monitor tis- Gingival Index (GI), Sulcus Bleeding In- actinomycetemcomitans, P. gingivalis,
sues around dental implants.5 Although dex, GI modified by Mombelli, and and T. forsythia did not present a sig-
some modifications in periodontal indices Plaque Index modified by Mombelli nificant relationship with the HI.
may be necessary to allow a more accurate (mPI) were evaluated around 1 dental Conclusion: Despite the small
evaluation of peri-implant disease,4,6 it is implant of each subject (n ⫽ 10). Sub- number of samples and the poor sta-
important to assess the reliability of the gingival plaque was collected for tistical significance, the mPI seems to
correlation between such clinical indices bacterial analysis (polymerase chain re- be useful for evaluation of inflamma-
and the real inflammatory condition as
revealed by histological findings.7–10
action) and a biopsy of peri-implant soft tory severity on soft tissue around den-
tissues for histological analysis was har- tal implants as demonstrated by its
vested. The clinical indices and detected relationship with the HI. Further stud-
*Specialization Student, Section of Periodontology, Hospital for
Rehabilitation of Craniofacial Anomalies, University of São pathogens correlated with a developed ies are necessary to elucidate this sub-
Paulo, Bauru, Brazil.
†Instructor, Section of Implantodontology, Hospital for histological index (HI). ject. (Implant Dent 2009;18:334 –344)
Rehabilitation of Craniofacial Anomalies, University of São
Paulo, Bauru, Brazil. Results: There was no statistically Key Words: periodontal index, gingi-
‡Instructor, Section of Periodontology, Hospital for
Rehabilitation of Craniofacial Anomalies, University of São significant relationship between the val index, plaque index, bleeding
Paulo, Bauru, Brazil.
§Associate Professor, Department of Biological Sciences, clinical indices (GI, Sulcus Bleeding index, peri-implant disease
Discipline of Histology, Bauru School of Dentistry, University of
São Paulo, Bauru, Brazil. Index, and GI modified by Mombelli)
储Laboratory Technician, Department of Biological Sciences,
Bauru School of Dentistry, University of São Paulo, Bauru,
Brazil.
¶Associate Professor, Department of Biological Sciences,
Discipline of Pharmacology, Bauru School of Dentistry,
University of São Paulo, Bauru, Brazil.
Visual inspection of the peri- Several studies have been con-
implant soft tissues may indicate ducted with the purpose of demon-
Reprint requests and correspondence to: Carlos signs of disease as color alteration, strating the correlation between the
Ferreira Santos, DDS, MSc, PhD, Bauru School of
Dentistry, University of São Paulo, Alameda Dr.
swelling, thickness,11 and bleeding clinical indices and the real histologi-
Octávio Pinheiro Brisolla, 9-75, Discipline of on probing by indices widely used cal changes in the periodontal tissues.
Pharmacology, Bauru/São Paulo 17012-901, Brazil, for evaluating the gingival dis- The results are controversial since
Phone: ⴙ55 14 32358282, Fax: ⴙ55 14 32234679,
E-mail: cebola@usp.br ease.12,13 Inflammatory lesions may some of these works demonstrated that
exist in the absence of visual signs of there is a positive correlation,18,19
ISSN 1056-6163/09/01804-334
Implant Dentistry inflammation.14 Despite the healthy whereas others did not.16,17,20
Volume 18 • Number 4
Copyright © 2009 by Lippincott Williams & Wilkins aspect, an inflammatory infiltrate Furthermore, probing around
DOI: 10.1097/ID.0b013e3181a44fd8 may be present.11,15–17 teeth has been demonstrated to be an
IMPLANT DENTISTRY / VOLUME 18, NUMBER 4 2009 335

excellent way to access the health of consent during the pretreatment with sterile cotton rolls, and the su-
natural teeth by measuring the probing screening period. pragingival plaque was removed with
depth, tissue consistency, bleeding, Ten systemically healthy patients sterile cotton. After 15 seconds, the
and the presence of exudate. On the of both genders aging from 33 to 73 paper points were removed from the
other hand, probing around dental im- years, wearing implant-supported pockets and submersed in 0.5 mL of
plants has been of little value because prostheses, and with indication of sur- sterile water in a microcentrifuge
of the structural differences between gical treatment of peri-implant pockets tube,32 which was immediately stored
natural teeth and dental implants, as caused by mucositis were selected at at ⫺20°C for further analysis.33
well as the lack of scientific criteria.21 our institution. Biopsy in the measured area was
Thus, it is important to investigate the All patients included in this study performed under local anesthesia by in-
correlation of clinical indices and the were nonsmokers, with the absence of cisions with conformity to excisional
real histological conditions. acute infection or hormonal alter- new attachment procedure,34 1 mm dis-
The amount of plaque can be mea- ations, were not taking antibiotics, tant of buccal and lingual edges. Peri-
sured by different indices.12,22 Many anti-inflammatory medicines, or other implant tissues were gently removed
studies demonstrated the correlation of drugs during the previous 6 months, from the abutments and stored in 10%
gingivitis and mucositis with the and were not subjected to any situation buffered formaldehyde (pH 7.3) for 1
plaque index.12,23,24 Plaque is also con- that could interfere with the clinical, week. On completion of surgeries, the
sidered the most important etiological histological, or bacteriological results. surgical sites were thoroughly irrigated,
factor in peri-implant disease.6,25 suctioned, and sutured.
The diagnosis of peri-implant dis- Clinical Procedures Postoperative instructions and
ease also uses bacteriological examina- Anamnesis, radiographic exami- medication were given to all patients,
tions, and nowadays techniques of DNA nation, peri-implant probing, determi- who returned 1 week later for postop-
identification, such as the polymerase nation of the adopted clinical indices, erative control.
chain reaction (PCR) represent an im- subgingival plaque collection, and an
portant auxiliary instrument for the de- incisional biopsy of the peri-implant Histological Procedures
tection of periodontal pathogens.26 –29 soft tissues were performed for each Samples were properly treated
The microbiota commonly associated patient. One trained examiner con- according to standard histological pro-
with peri-implant diseases comprises the ducted all these procedures. To carry cedures. Each buccal and lingual sam-
following: Prevotella intermedia, Porphy- out the biopsies, only 1 area with 1 ples were included in separate paraffin
romonas gingivalis, Aggregatibacter implant per patient was selected, tak- blocks (total of 20 blocks—2 per pa-
actinomycetemcomitans (formerly Acti- ing into account the amount of kera- tient). Serial sections (5 ␮m) parallel
nobacillus actinomycetemcomitans), Tan- tinized mucosa. to the longitudinal axis were obtained
nerella forsythia (formerly Bacteroides Four indices were determined to from each sample and stained with
forsythus), Treponema denticola, Pre- measure the degree of soft tissue in- hematoxylin and eosin.
votella nigrescens, and Fusobacte- flammation (Gingival Index [GI],12 GI For each buccal (n ⫽ 10) and lin-
rium nucleatum.25,27,30,31 modified by Mombelli [mGI],22 and gual fragments (n ⫽ 10) of peri-
This study was carried out due to Sulcus Bleeding Index [SBI]13) and 1 implant tissues, duplicates for the
the paucity of data in the literature measuring the presence of supragingi- mesial, central, and distal areas of the
correlating clinical parameters and the val plaque (Plaque Index modified by fragments were prepared, thus com-
histological inflammatory findings on Mombelli [mPI] 22 ). These indices prising a total of 120 slides (60 slides
soft tissues affected by peri-implant were adopted because they are widely in duplicates).
disease. Therefore, the aims were to used to determine gingivitis severity.
evaluate (i) the correlation of gingival mGI and mPI were adopted since they Histological Analysis
and plaque indices with the histologi- are modifications from Löe GI and PI A developed HI was used for
cal changes of peri-implant soft tissues used for dental implants. comparison with the clinical parame-
measured by a developed histological in- The clinical indices and probing ters determined. The HI is expressed
dex (HI) and (ii) the correlation between depth were determined at 6 sites by scores ranging from 0 to 3 (Table
the prevalence of 3 periodontopathic bac- around the implant: mesiobuccal, buc- 1) based on the inflammatory condition
teria (A. actinomycetemcomitans, P. gin- cal, distobuccal, mesiolingual, lingual, of both the connective and epithelial tis-
givalis, and T. forsythia) and HI. and distolingual aspects (mb, b, db, sues. These scores were established in
ml, l, and dl, respectively). accordance with qualitative character-
Subgingival plaque samples sur- istics of the inflammatory infiltrate
PATIENTS AND METHODS rounding the implants were collected (extension, density, and predominant
Patient Selection twice with sterile paper points (No. cells), which corresponded to the in-
The institutional Ethics Commit- 40) that were inserted into the deeper flammatory degree in the evolution of
tee approved the protocol of this study site at the buccal and lingual aspects. gingivitis according to the classifica-
(No 253/2006-SVAPEPE-CEP). All To avoid contamination, before plaque tion of Page and Schroeder35 and
patients provided written informed collection the implants were isolated Kinane and Lindhe.36
336 PERI-IMPLANT DISEASE • FERREIRA JR et al

Table 1. Histological Index


Score Histological Features
0 Gingiva with normal Connective tissue: slight lymphocyte infiltrated, slightly near the epithelial areas, isolated cells,
appearance or rare or in small groups subjacent to connective or sulcus epithelium; normal vessels; absence of
and insignificant edema.
inflammatory infiltrate Epithelial tissue: cellular disjunction is rare or absent at the basal layer; vacuolization of
cytoplasm is rare or absent; absence of hyperplasia.
1 Gingiva with slight Connective tissue: slight infiltration of lymphocytes/plasmocytes with obvious predominance of
inflammation lymphocytes near the epithelial tissue, in a continuous thin layer under the sulcus or pocket
epithelium; accumulation of cells in connective papillae areas between the epithelial
projections, but may be involving all of areas “a” and “c” of Figure 1; possible presence of
hyperemic vessels and edema; slight collagen degradation.
Epithelial tissue: slight disjunctions at the basal layer; slight cytoplasm vacuolization, possible
epithelial hyperplasia.
2 Gingiva with moderate Connective tissue: diffuse infiltration of lymphocytes/plasmocytes, more evident that in the
inflammation condition described above, with predominance of lymphocytes, collagen degradation in
areas “a” and “c” of Figure 1, proliferation of infiltrated cells towards the oral epithelium with
large involvement of areas “b” and “d” of Figure 1; hyperemia of vessels with possible
capillary proliferation; increase of neutrophil migration toward the sulcus (and junctional
epithelium) or pocket epithelium; moderate edema; increase of collagen degradation.
Epithelial tissue: cellular disjunctions at the basal layer; cytoplasm vacuolization, hyperplastic
epithelium with some prominent crests; migration of leucocytes to epithelial tissues.
3 Gingiva with intense Connective tissue: Intense and diffuse infiltration of lymphocytes/plasmocytes, with
inflammation considerable number of plasmocytes, replacing the most part of collagen fibers, with large
degradation in areas “a,” “b,” “c,” and “d” of Figure 1; hyperemia of vessels more frequently
observed; edema; neutrophil migration to pocket epithelium and the remaining junctional
epithelium.
Epithelial tissue: cellular disjunctions at the basal layer and cytoplasm vacuolization more
frequently observed; acanthotic epithelium with prominent epithelial crests.

Each section evaluated was di-


vided into 4 areas (Fig. 1, a– d). This
division is part of the classification
criteria (Table 1), with the objective to
better analyze the different degrees of
histological changes based on quanti-
tative attributions of descriptive histo-
logical analysis adopted in this study.
The slides were evaluated in an
optical microscope, under magnifica-
tion of 40, 100, and 400⫻. The HI
score was determined for each mesial,
central, and distal areas of buccal and
lingual aspects through analyses of 2
slides of each area (in duplicates).
To offer additional support data to
allow a better understanding of the
inflammatory changes and to help the
classification of the slides with the HI
scores, a counting of inflammatory
cells considered in the index (lympho-
cytes and plasmocytes) was conducted
using a 40⫻ objective and a Zeiss kpl
8⫻ eyepiece containing a Zeiss II
Fig. 1. Localization of areas a, b, c, and d used as reference regions for histological analysis.
This division is part of the classification criteria (Table 1), with the objective to better visualize
integration grid (Carl Zeiss Jena
and analyze the histological changes. Areas (a) and (c) represent the region next to the GmbH, Jena, Germany) resulting in an
peri-implant sulcus or pocket. Areas (b) and (d) represent the region next the oral epithelium. area of 102,400 ␮m2. The grid image
was superimposed on 1 representative
IMPLANT DENTISTRY / VOLUME 18, NUMBER 4 2009 337

Table 2. Clinical and Histological Indices


GI mGI SBI mPI HI
Buccal Lingual Buccal Lingual Buccal Lingual Buccal Lingual Buccal Lingual
Patient M C D M C D M C D M C D M C D M C D M C D M C D M C D M C D
1 2 2 2 2 2 2 2 2 2 2 2 2 1 1 1 1 1 1 1 1 1 1 1 1 2 2 2 1 1 2
2 2 2 2 2 2 2 2 2 2 2 2 2 4 4 4 4 4 4 1 1 1 1 1 1 1 2 2 1 1 1
3 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 1 1 1 1 1 1 1 1 1 0 1 1
4 2 2 2 2 2 2 2 2 2 2 2 2 1 1 1 3 3 3 0 0 0 1 0 0 1 1 1 1 1 1
5 1 1 1 2 2 2 0 0 0 2 2 2 0 0 0 3 3 3 0 0 0 0 0 0 1 1 2 1 1 1
6 2 2 2 2 2 2 2 2 2 2 2 2 3 3 3 3 3 3 0 0 0 0 0 0 1 1 1 1 1 1
7 2 2 2 1 1 1 1 1 1 0 0 0 4 4 4 0 0 0 0 0 0 0 0 0 2 1 1 1 0 2
8 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 2 2 2 2 2 2 2 2 2 2 1
9 2 2 2 2 2 2 1 1 1 2 2 2 4 4 4 4 4 4 1 1 1 2 2 1 1 1 1 1 2 2
10 2 2 2 2 2 2 2 2 2 2 2 2 4 4 4 4 4 4 1 1 1 2 2 2 2 1 1 1 2 1
M indicates mesial; C, central; D, distal; GI, gingival index (1967); mGI, gingival Index modified by mombelli (1987); SBI, sulcus bleeding index (1971); mPI, plaque index modified by mombelli (1987); HI,
histological index.

Table 3. Statistical Correlation Between Clinical Indices and HI


GI mGI SBI mPI
r P r P r P r P
Buccal
M 0.000 1.000 0.03858 0.9184 0.1118 0.7589 0.3536 0.3129
C ⫺0.1409 0.7072 0.1237 0.7330 ⫺0.1195 0.7330 0.6299 0.0544
D ⫺0.3953 0.2632 ⫺0.1543 0.6821 ⫺0.3727 0.2957 0.3536 0.3129
Lingual
M ⫺0.1443 0.6821 0.0000 1.0000 0.0000 1.0000 0.2887 0.4069
C 0.0643 0.8651 0.1739 0.6321 0.4033 0.2475 0.8487 0.0029*
D 0.0000 1.0000 ⫺0.04762 0.8916 ⫺0.1183 0.7330 ⫺0.08133 0.8382
*Statistically significant correlation (Spearman’s correlation test).

M indicates mesial; C, central; D, distal; GI, Löe gingival index (1967); mGI, mombelli gingival index (1987); SBI, Mühlemann and Son sulcus bleeding index (1971); mPI, mombelli plaque index (1987); HI,
histological index.

area of each 4 sections represented in sample, 5 ␮L of 10⫻ PCR buffer, 2.5 pairs. The sequences of the primers
Figure 1. unit of Taq DNA polymerase, 0.2 ␮M and the temperature profiles were pre-
of each deoxyribonucleotides, 1.0 ␮M viously described.40,41
DNA Extraction of each primer, and 1.5 ␮M of MgCl2. PCR amplification products (9
The subgingival plaque samples As positive controls, isolated DNA from ␮L) were analyzed by 2% agarose
were diluted 1:2 in sterile water and A. actinomycetemcomitans ATCC 29522, gel electrophoresis. The agarose gels
collected by centrifugation at 10,000g P. gingivalis ATCC 33277, and T. for- were stained with 0.5 ␮ g/mL
for 5 minutes in a microcentrifuge at sythia ATCC 43037 were tested with the ethidium bromide and photographed
4°C. The supernatant was discarded species-specific primers. Ubiquitous prim- under ultraviolet light. A 100 bp
and the resulting pellet was washed 2 ers were also used as a positive control for DNA ladder served as a molecular
more times with 1 mL sterile water.
the PCR amplification. For each set of weight marker.37
The pellet was reconstituted with 100
primers, PCR was performed on sterile
␮L of water and 100 ␮L of InstaGene
Matrix (Bio-Rad Laboratories, Inc., water to check for DNA contamination Data Analysis
Hercules, CA) and incubated at 56°C (negative controls). The values for each of the 4 clin-
for 30 minutes. The samples were then Specificities of all primers were ical indices and the presence of 3
vortexed and boiled for 10 minutes. previously investigated38,39 and primer periodontopathic bacteria were cor-
After centrifugation to remove unbroken sequences were compared with similar related with the HI. The correlations
cells (10,000g for 3 minutes), the super- sequences of the reference organisms were performed using the values of
natant was used for PCR analysis.37 by BLAST search (http://ncbi.nlm. mesial, central and distal area of
nih.gov/blast/). To further test the buccal, and lingual aspects. The re-
PCR Conditions specificity of the primers, total DNA sults of the counting of inflamma-
A total of 50 ␮L of PCR reaction from all bacterial strains cited above tory cells were correlated with the
mixture contained 10 ␮L of DNA was used with each of the primer attributed scores of HI. Spearman’s cor-
338 PERI-IMPLANT DISEASE • FERREIRA JR et al

Table 4. Inflammatory Cells by Area* of Histological Index


A-L A-P B-L B-P C-L C-P D-L D-P
Score 0
Mean 6.00 0.00 0.00 0.00 4.0 0.00 0.00 0.00
Std. error 0.58 0.00 0.00 0.00 0.58 0.00 0.00 0.00
Score 1
Mean 176.3 6.75 73.75 5.13 73.38 2.88 48.50 3.88
Std. error 39.54 1.05 16.84 0.74 14.72 0.64 14.84 3.31
Score 2
Mean 237.60 8.50 121.40 5.63 150.40 6.13 90.88 3.75
Std. error 37.76 1.04 18.25 1.21 28.51 1.32 19.58 0.65
Spearman’s correlation test. A, B, C, and D are the correspondent areas of Figure 1.

*Number of cells/102,400 ␮m2.

L indicates lymphocytes; P, plasmocytes.

Table 5. Correlation Between Inflammatory Cells and HI Scores


A-L A-P B-L B-P C-L C-P D-L D-P
r 0.5943 0.6295 0.7095 0.4332 0.7386 0.6849 0.6194 0.4463
P 0.0073* 0.0039* 0.0007* 0.0639 0.0003* 0.0012* 0.0047* 0.0554
*Statistically significant correlation (Spearman’s correlation test). A, B, C, and D are the areas of Figure 1.

L indicates lymphocytes; P, plasmocytes.

relation test (P ⬍ 0.05), through the P. gingivalis was detected in 4 patients tion of the counting of lymphocytes
software Statistica (version 5.1, Stat (40%) and in 6 surfaces (30%). The and plasmocytes and HI found in this
Soft Inc., Tulsa, OK), was used for most prevalent bacterium was T. for- study strongly suggest the reliability
data analysis. sythia, which was detected in 5 pa- of the HI.
tients (50%) and in 6 faces (30%). In 3 The results found in this study for
RESULTS patients, none of the bacteria was de- the clinical indices based on visual and
tected. The presence of the 3 peri- bleeding conditions (GI, mGI, and
A total of 120 slides (duplicates of odontopathic bacteria studied did not
60 slides) were evaluated and used as SBI), despite the nonstatistically sig-
correlate with the HI. nificant correlation, suggest that these
gold standard for comparison with the
other parameters in this study. indices do not reflect the real inflam-
The results of clinical and histo- DISCUSSION matory degree (HI) of the evaluated
logical indices and their statistical cor- This study evaluated the correla- tissues. Probably, the parameters of
relations can be observed in Tables 2 tion of 3 clinical indices of gingival GI, mGI, and SBI used in this study
and 3, respectively. The mPI showed a inflammation, based on bleeding and are not exactly applicable to evaluate
statistically significant correlation visual aspects (GI, mGI, and SBI), and the inflammation status in the peri-
with the HI in the central area of lin- 1 index of plaque accumulation (mPI) implant tissues.
gual aspect. No statistically significant with the histological condition, As far as the use of bleeding as a
correlation was found for areas of the through a developed HI. Such correla- diagnostic tool of peri-implant inflam-
buccal aspects and the other areas of tion was analyzed to test the ability of mation is considered, some studies in-
lingual aspect. No statistically signifi- the clinical indices to show the real dicate the use of bleeding indices
cant correlation was detected for the inflammatory changes on the tissues as a signal of inflammation,23,26,43,44
other indices either. clinically evaluated. The aim of deter- whereas others do not corroborate
The counting of lymphocytes and mining bacterial detection was to cor- these findings since a correlation with
plasmocytes in Figure 1, a– d is relate the presence of 3 common species the real inflammatory changes in the
depicted in Table 4. The positive cor- in peri-implant disease with the in- tissues was not observed.23,45
relation between the counting of in- flammatory degree of the tissues. Structural differences between
flammatory cells and HI can be There are controversial findings in peri-implant and periodontal tissues
obtained from Table 5. the literature regarding the ability of are mainly represented by the parallel
For each patient, samples of sub- clinical indices to show the histologi- disposition of collagen fibers to the
gingival plaque were collected both in cal condition of gingival tissues. Some implant surface and the absence of
buccal and lingual aspects, with a total authors found positive results,18,19,42 connective tissue insertion.3 There-
of 20 samples. A. actinomycetemcomi- whereas others do not agree since they fore, when probing the peri-implant
tans was detected in only 1 patient did not find positive association in sulcus, the probe goes beyond the ep-
(10%) and in 1 surface (5%), whereas their studies.17,20 The positive correla- ithelial seal and causes injury to sub-
IMPLANT DENTISTRY / VOLUME 18, NUMBER 4 2009 339

jacent connective tissue.21 This causes Additional studies are necessary to better sual signs of interdental gingival inflamma-
bleeding even if the inflammation is elucidate these points. tion. J Periodontol. 1988;59:722-727.
absent,46 thus affecting the results of 15. Bernier JL. The histologic changes
of the gingival tissues in health and peri-
clinical examinations of inflammation, ACKNOWLEDGMENTS odontal disease: A preliminary report. Oral
as those used in this study. Surg Oral Med Oral Pathol. 1950;3:1194-
There is evidence that the incom- The authors thank Daniele Santi Ceolin
1199.
patibility of bleeding signal with the and Tânia Mary Cestari for the excellent 16. Seymour GJ, Powell RN, Aitken JF.
histological inflammatory condition in technical assistance. This research was Experimental gingivitis in humans. A clini-
peri-implant tissues may result from partially supported by FAPESP (Process cal and histologic investigation. J Peri-
the small number of blood vessels in No 02/09380-6). odontol. 1983;54:522-528.
17. Zachrisson BU. A histological
these tissues when compared with the study of experimental gingivitis in man.
periodontal tissues. 3,47 Because of REFERENCES J Periodontal Res. 1968;3:293-302.
these differences, the clinical indices 1. Albrektsson T, Isidor F. Consensus 18. Brecx MC, Schlegel K, Gehr P, et
that evaluate bleeding and visual as- Report of Sessions IV. In: Lang NP, Karring al. Comparison between histological and
pects, which sometimes successfully T, eds. Proceedings of the 1st European clinical parameters during human experi-
reflect the real inflammatory degree in Workshop on Periodontology; London: mental gingivitis. J Periodontal Res. 1987;
Quintessence; 1994. 22:50-57.
periodontal tissues, may not be appli- 19. Oliver RC, Holm-Pederen P, Löe H.
2. Nishimura K, Itoh T, Takaki K, et al.
cable to peri-implant tissues. This Periodontal parameters of osseointe- The correlation between clinical scoring,
could explain our divergent results for grated dental implants. A 4-year controlled exudate measurements and microscopic
the lack of correlation of GI, mGI, and follow-up study. Clin Oral Implants Res. evaluation of inflammation in the gingiva.
SBI with the HI. 1997;8:272-278. J Periodontol. 1969;40:201-209.
The significant correlation be- 3. Berglundh T, Lindhe J, Ericsson I, et 20. Fourel J. [Longitudinal study in 8
tween mPI and HI found in this study al. The soft tissue barrier at implants and human subjects having various gingival in-
teeth. Clin Oral Implants Res. 1991;2:81-90. flammation indices]. J Parodontol. 1985;4:
suggests that plaque accumulation 197-210.
4. Mombelli A. Etiology, diagnosis, and
may be a good parameter to monitor treatment considerations in peri-implantitis. 21. Misch CE, Perel ML, Wang HL, et
peri-implant healthy. This was the only Curr Opin Periodontol. 1997;4:127-136. al. Implant success, survival, and failure:
index that positively correlated with the 5. Salvi GE, Lang NP. Diagnostic pa- The International Congress of Oral Implan-
histological changes (Table 3). These rameters for monitoring peri-implant con- tologists (ICOI) Pisa Consensus Confer-
results agree with others that found a ditions. Int J Oral Maxillofac Implants. ence. Implant Dent. 2008;17:5-15.
positive correlation between the plaque 2004;19(suppl):116-127. 22. Mombelli A, van Oosten MA,
6. Mombelli A, Lang NP. Clinical pa- Schurch E Jr, et al. The microbiota associ-
index and inflammation.16,23,24 ated with successful or failing osseointe-
rameters for the evaluation of dental im-
Despite the positive correlation plants. Periodontol 2000. 1994;4:81-86. grated titanium implants. Oral Microbiol
between mPI and HI, the bacterial 7. Bollmer BW, Sturzenberger OP, Immunol. 1987;2:145-151.
analysis in this work did not demon- Lehnhoff RW, et al. A comparison of 3 clin- 23. Lekholm U, Adell R, Lindhe J, et al.
strate statistically significant correla- ical indices for measuring gingivitis. J Clin Marginal tissue reactions at osseointe-
tion between the 3 studied species Periodontol. 1986;13:392-395. grated titanium fixtures. II. A cross-
with the inflammatory degree, in con- 8. Chaves ES, Wood RC, Jones AA, et sectional retrospective study. Int J Oral
al. Relationship of “bleeding on probing” Maxillofac Surg. 1986;15:53-61.
trast with studies that documented and “gingival index bleeding” as clinical pa- 24. Sanz M, Alandez J, Lazaro P, et al.
these bacteria as key pathogens in rameters of gingival inflammation. J Clin Histo-pathologic characteristics of peri-
periodontal and peri-implant dis- Periodontol. 1993;20:139-143. implant soft tissues in Branemark implants
ease.27,48 –50 The bacterial composition 9. Dababneh RH, Khouri AT, Smith RG, with 2 distinct clinical and radiological pat-
of plaque is accepted as its pathogenic et al. A new method of plaque scoring: A terns. Clin Oral Implants Res. 1991;2:128-
factor.51 In this study, the lack of cor- laboratory comparison with other plaque in- 134.
relation between the prevalence of the dices. J Clin Periodontol. 2002;29:832-837. 25. Sanchez-Garces MA, Gay-Escoda
10. McCracken GI, Preshaw PM, C. Periimplantitis. Med Oral Patol Oral Cir
bacterial species in the subgingival Steen IN, et al. Measuring plaque in clinical Bucal. 2004;9(suppl):69-74; 63-69.
plaque with the HI (Table 5) may be trials: Index or weight? J Clin Periodontol. 26. Greenstein G. The role of bleeding
explained by the sample size. 2006;33:172-176. upon probing in the diagnosis of periodon-
11. Bauman GR, Mills M, Rapley JW, tal disease. A literature review. J Periodon-
et al. Clinical parameters of evaluation dur- tol. 1984;55:684-688.
CONCLUSION ing implant maintenance. Int J Oral Maxil- 27. Hultin M, Gustafsson A, Hallström
lofac Implants. 1992;7:220-227. H, et al. Microbiological findings and host
In conclusion, within the limita- 12. Loe H. The gingival index, the plaque response in patients with peri-implantitis.
tions of a pilot study, our results suggest index and the retention index systems. J Clin Oral Implants Res. 2002;13:349-358.
that mPI may be used as an indicator Periodontol. 1967;38(suppl):610-616. 28. Perea EJ. Oral flora in the age of
of the real inflammatory status in peri- 13. Muhlemann HR, Son S. Gingival molecular biology. Med Oral Patol Oral Cir
sulcus bleeding—A leading symptom in Bucal. 2004;9(suppl):6–10; 11-15.
implant disease. Other indices, such as GI, initial gingivitis. Helv Odontol Acta. 1971; 29. Sanz M, Lau L, Herrera D, et al.
mGI, and SBI, which depend on probing 15:107-113. Methods of detection of Actinobacillus
of the implant sulcus, did not show statis- 14. Caton J, Polson A, Bouwsma O, et actinomycetemcomitans, Porphyromonas
tically significant correlations with the HI. al. Associations between bleeding and vi- gingivalis and Tannerella forsythensis in
340 PERI-IMPLANT DISEASE • FERREIRA JR et al

periodontal microbiology, with special em- odontopathic bacteria in saliva of a group sue conditions during supportive peri-
phasis on advanced molecular of Brazilian children with mixed dentition: odontal therapy (SPT). Clin Oral Implants
techniques:A review. J Clin Periodontol. 1-year longitudinal study. Int J Paediatr Res. 2000;11:521-529.
2004;31:1034-1047. Dent. 2007;17:192-199. 45. Stallard RE, Orban JE, Hove KA.
30. Heydenrijk K, Meijer HJ, van der 38. Kimura S, Ooshima T, Takiguchi M, et Clinical significance of the inflammatory
Reijden WA, et al. Microbiota around root- al. Periodontopathic bacterial infection in child- process. J Periodontol. 1970;41:620-624.
form endosseous implants: A review of the hood. J Periodontol. 2002;73: 46. Atassi F. Periimplant probing: Pos-
literature. Int J Oral Maxillofac Implants. 20-26. itives and negatives. Implant Dent. 2002;
2002;17:829-838. 39. Ooshima T, Nishiyama N, Hou B, et 11:356-362.
31. Leonhardt A, Renvert S, Dahlén G. al. Occurrence of periodontal bacteria in 47. Berglundh T, Lindhe J, Jonsson K,
Microbial findings at failing implants. Clin healthy children: A 2-year longitudinal et al. The topography of the vascular sys-
Oral Implants Res. 1999;10:339-345. study. Community Dent Oral Epidemiol. tems in the periodontal and peri-implant
32. Nociti FH Jr, Cesco De Toledo R, 2003;31:417-425. tissues in the dog. J Clin Periodontol.
Machado MA, et al. Clinical and microbio- 40. Ashimoto A, Chen C, Bakker I, et 1994;21:189-193.
logical evaluation of ligature-induced peri- al. Polymerase chain reaction detection of 48. Consensus report. Periodontal
implantitis and periodontitis in dogs. Clin 8 putative periodontal pathogens in sub- diseases: Pathogenesis and microbial fac-
Oral Implants Res. 2001;12:295-300. gingival plaque of gingivitis and advanced
tors. Ann Periodontol. 1996;1:926-932.
33. Mayanagi G, Sato T, Shimauchi H, et periodontitis lesions. Oral Microbiol Immu-
49. Agerbaek MR, Lang NP, Persson
al. Detection frequency of periodontitis- nol. 1996;11:266-273.
GR. Comparisons of bacterial patterns
associated bacteria by polymerase chain re- 41. Umeda M, Contreras A, Chen C, et
action in subgingival and supragingival al. The utility of whole saliva to detect the present at implant and tooth sites in sub-
plaque of periodontitis and healthy subjects. oral presence of periodontopathic bacte- jects on supportive periodontal therapy. I.
Oral Microbiol Immunol. 2004;19:379-385. ria. J Periodontol. 1998;69:828-833. Impact of clinical variables, gender and
34. Carranza FA, Takei HH. Carranza Pe- 42. Hancock EB, Cray RJ, O’Leary TJ. smoking. Clin Oral Implants Res. 2006;17:
riodontia Clínica. 9th ed. Rio de Janeiro, Brazil: The relationship between gingival cervicular 18-24.
Guanabara-Koogan; 2004:662-625. fluid and gingival inflammation. A clinical and 50. Quirynen M, Alsaadi G, Pauwels M,
35. Page RC, Schroeder HE. Patho- histologic study. J Periodontol. 1979;50:13- et al. Microbiological and clinical outcomes
genesis of inflammatory periodontal dis- 19. and patient satisfaction for two treatment
ease. A summary of current work. Lab 43. Lang NP, Joss A, Orsanic T, et al. options in the edentulous lower jaw after
Invest. 1976;34:235-249. Bleeding on probing. A predictor for the 10 years of function. Clin Oral Implants
36. Kinane DF, Lindhe J. Tratado de progression of periodontal disease? J Clin Res. 2005;16:277-287.
Periodontia Clínica e Implantologia Oral. Periodontol. 1986;13:590-596. 51. Loesche WJ. Clinical and microbi-
3rd ed. Rio de Janeiro, Brazil: Guanabara- 44. Luterbacher S, Mayfield L, Brägger ological aspects of chemotherapeutic
Koogan; 1997:127-152. U, et al. Diagnostic characteristics of clini- agents used according to the specific
37. Sakai VT, Campos MR, Machado cal and microbiological tests for monitoring plaque hypothesis. J Dent Res. 1979;58:
MA, et al. Prevalence of four putative peri- periodontal and peri-implant mucosal tis- 2404-2412.

Abstract Translations
romonas gingivalis sowie Tannerella forsythia]. Materialien
GERMAN / DEUTSCH und Methoden: Vier klinische Kennziffern, der Zahn-
AUTOR(EN): Samuel Barros Ferreira, Jr., DDS, Caio Már- fleischindex (GI), der Sulcus-Blutungs-Index (SBI), der
cio Figueiredo, DDS, MSc, Ana Lúcia Pompéia Fraga Mombelli-Zahnfleischindex (mGI) und der Mombelli-
Almeida, DDS, MSc, PhD, Gerson Francisco Assis, MSc, Plaque-Index (mPI), wurden bei jedem Patienten um ein
PhD, Thiago José Dionísio, Carlos Ferreira Santos, DDS, Zahnimplantat herum bewertet (n ⫽ 10). Unter dem Zahn-
MSc, PhD. fleisch liegende Plaque wurde zum Zweck der bakteriellen
Klinische, histologische und mikrobiologische Untersu- Analyse (PCR) gesammelt. Außerdem wurde eine Biopsie
chungsergebnisse bei Erkrankungen im das Implantat um- der Weichgewebsteile um das Implantat herum für eine his-
lagernden Gewebe: Eine Pilotstudie tologische Analyse erhoben. Die klinischen Kennziffern
sowie entdeckten Pathogene wurden mit einem eigens en-
ZUSAMMENFASSUNG: Zielsetzungen: Diese Studie hebt twickelten histologischen Index (HI) in Verbindung gebracht.
darauf ab, den Zusammenhang zwischen den klinischen Ken- Ergebnisse: Außer beim mPI im zentralen Bereich der lin-
nzahlen in Bezug auf das Weichgewebe im das Implantat gualen Seiten ergab sich keinerlei statistisch maßgebliche
umlagernden Bereich, der histologischen Grundvorausset- Verbindung zwischen den klinischen Kennzahlen (GI, SBI
zung und dem Vorhandensein von 3 unterschiedlichen Patho- and mGI) und dem HI (r ⫽ 0.85, P ⫽ 0.0029). Allerdings war
genen zu bestätigen, die Allgemeinhin mit Erkrankungen im eine Tendenz hinsichtlich einer Positivverbindung zwischen
Bereich um das Implantat herum in Verbindung gebracht dem mPI im zentralen Bereich der bukkalen Seiten und dem
werden [Aggregatibacter actinomycetemcomitans, Porphy- HI (r ⫽ 0.63, P ⫽ 0.0544) zu beobachten. Eine Zählung der
IMPLANT DENTISTRY / VOLUME 18, NUMBER 4 2009 341

Lymphozyten und Plasmozyten korrelierte positiv mit dem edor de implantes dentales tal como lo demuestra su relación con
HI. Man kann daher von einer Zuverlässigkeit des Index el HI. Se necesitan más estudios para aclarar este tema.
ausgehen. Das Vorherrschen von A. actinomycetemcomitans,
P. gingivalis und T. forsythia ergab keine bedeutsame PALABRAS CLAVES: índice periodóntico, índice gingival, índice
Verbindung mit dem HI. Schlussfolgerungen: Trotz der de placa, índice de sangramiento, enfermedad periimplante
geringen Anzahl an Proben und der nur geringfügigen statis-
tischen Bedeutung scheint der mPI in der Bewertung unter-
schiedlicher entzündlicher Tendenzen im Weichgewebe um PORTUGUESE / PORTUGUÊS
das Implantat herum hilfreich zu sein. Dies wird durch dessen AUTOR(ES): Samuel Barros Ferreira, Jr., Cirurgião-
Beziehung zum HI unter Beweis gestellt. Weitere Studien Dentista, Caio Márcio Figueiredo, Cirurgião-Dentista, Mestre
sind zur nötig, um dieses Thema weiter zu verfolgen. em Ciência, Ana Lúcia Pompéia Fraga Almeida, Cirurgiã-
Denista, Mestre em Ciência, PhD, Gerson Francisco Assis,
SCHLÜSSELWÖRTER: Peridontaler Index, Zahnfleischin-
Mestre em Ciência, PhD, Thiago José Dionísio, Carlos
dex, Plaque-Index, Blutungsindex, Erkrankung des das Im- Ferreira Santos, Cirurgião-Dentista, Mestre em Ciência, PhD.
plantat umlagernden Gewebes Achados clı́nicos, histológicos e microbiológicos na periim-
plantite: estudo piloto.

RESUMO: Objetivo: Este estudo teve por objetivo verificar


SPANISH / ESPAÑOL a correlação entre ı́ndices clı́nicos de tecidos moles periim-
AUTOR(ES): Samuel Barros Ferreira, Jr., DDS, Caio Márcio plantares, a condição histológica e a presença de 3 patógenos
Figueiredo, DDS, MSc, Ana Lúcia Pompéia Fraga Almeida, comumente associados a periimplantites (Aggregatibacter
DDS, MSc, PhD, Gerson Francisco Assis, MSc, PhD, Thiago actinomycetemcomitans, Porphyromonas gingivalis, and
José Dionísio, Carlos Ferreira Santos, DDS, MSc, PhD. Tannerella forsythia). Materiais e Métodos: Foram avaliados
Conclusiones clínicas, histológicas y microbiológicas en la quatro ı́ndices clı́nicos, ı́ndice gengival (GI), ı́ndice de san-
enfermedad periimplante: Un estudio piloto gramento do sulco, GI modificado por Mombelli e ı́ndice de
placa modificado por Mombelli (mPI) ao redor de um im-
ABSTRACTO: Propósito: Este estudio tiene por objeto veri- plante dentário de cada indivı́duo (n ⫽ 10). Placa subgengival
ficar la correlación entre índices clínicos de los tejidos suaves foi coletada para realização de análise bacteriana (reação em
periimplante, la condición histológica y la presencia de 3 cadeia da polimerase) e biópsia de tecidos periimplantares foi
patógenos generalmente asociados con las enfermedades per- retirada para análise histológica. Foi realizada análise de
implante [Aggregatibacter actinomycetemcomitans, Porphy- correlação dos ı́ndices e patógenos detectados com um ı́ndice
romonas gingivalis y Tannerella forsythia]. Materiales y histológico desenvolvido (HI). Resultados: Não foi encon-
Métodos: Cuatro índices clínicos, el índice gingival (GI por trada correlação estatisticamente significativa entre os ı́ndices
sus siglas en inglés), el índice de sangramiento gingival (SBI clı́nicos (GI, ı́ndice de sangramento do sulco e GI modificado
por sus siglas en inglés), índice gingival modificado por por Mombelli) e o HI exceto para o mPI na área central das
Mombelli (mGI por sus siglas en inglés) y el índice de placa superfı́cies linguais (r ⫽ 0,85, P ⫽ 0,0029). Houve tendência
modificado por Mombelli (mPI por sus siglas en inglés), de correlação positiva entre o mPI na área central das super-
fueron evaluados alrededor de un implante dental de cada fı́cies vestibulares e o HI (r ⫽ 0,63, P ⫽ 0,0544). A contagem
sujeto (n ⫽ 10). Se recolectó la placa subgingival para el de linfócitos e plasmócitos correlacionou-se positivamente
análisis bacteriano (PCR por sus siglas en inglés) así como com o HI, sugerindo assim a confiabilidade do ı́ndice. A
una biopsia de los tejidos suaves perimplante para el análisis prevalência de A. actinomycetemcomitans, P. gingivalis, e T.
histológico. Los índices clínicos y patógenos detectados se forsythia não apresentou correlação positiva com o HI.
correlacionaron con un índice histológico creado (HI por sus Conclusões: Apesar do pequeno número de amostras e a
siglas en inglés). Resultados: No existió una relación estadís- fraca significância estatı́stica, o mPI parece ser útil para
ticamente significativa entre los índices clínicos (GI, SBI y avaliar a gravidade da inflamação no tecido mole ao redor de
mGI) y el HI, excepto que el mPI en la zona central de los implantes como demonstrado pela correlação com o HI. Es-
aspectos linguales (r ⫽ 0,85, P ⫽ 0,0029). Existió una tudos futuros são necessários para elucidar este assunto.
tendencia a la correlación positiva entre el mPI en la zona
PALAVRAS-CHAVE: ı́ndice periodontal, ı́ndice gengival,
central de los aspectos bucales y el HI (r ⫽ 0,63, P ⫽
ı́ndice de placa, ı́ndice de sangramento, periimplantite.
0,0544). La cantidad de linfocitos y plasmacitos se correla-
cionó positivamente con el HI, sugiriendo la confiabilidad del
índice. La prevalencia de A. actinomycetemcomitans, P. gin-
givalis y T. forsythia no presentó una relación significativa
RUSSIAN /
con el HI. Conclusiones: A pesar de la pequeña cantidad de О: Samuel Barros Ferreira Jr., доко
muestras y el pobre significado estadístico, el mPI parece ser útil уг
ско соолог, Caio Márcio Figueiredo,
para evaluar la severidad inflamatoria en el tejido suave alred- доко уг
ско соолог, гс
342 PERI-IMPLANT DISEASE • FERREIRA JR et al

с с  ук, Ana Lúcia Pompéia Fraga Almeida, к окуг уб ло,
о бло
доко уг
ско соолог, гс од осоо го ос с
с с  ук, доко флософ, Gerson Fran- ок л  HI. Дл об&с  дого фк
cisco Assis, гс с с  ук, доко  обод дл % ссл до.
флософ, Thiago José Dionísio, Carlos Ferreira Santos,
доко уг
ско соолог, гс КЛ $ СЛО:  одол д кс,
с с  ук, доко флософ. д с  д кс, д кс убого к, д кс ко-
ул  клск, гс ологск  оо
ос,  ло бол 
кобологск сслдо  
л  о  бол : д  л о
сслдо 
TURKISH / TÜRKÇE
 !: л. До ссл до    л YAZARLAR: Samuel Barros Ferreira, Jr., DDS, Caio Márcio
од д ко л  ду кл
ск Figueiredo, DDS, MSc, Ana Lúcia Pompéia Fraga Almeida,
ок л  л гк к , DDS, MSc, PhD, Gerson Francisco Assis, MSc, PhD, Thiago
гсолог
ск сосо   л
  3 José Dionísio, Carlos Ferreira Santos, DDS, MSc, PhD.
ог  коого, с с Peri-implant hastalığında klinik, histolojik ve mikrobiy-
 л бол  [Aggregatibacter olojik bulgular: Bir pilot çalışma
actinomycetemcomitans (A.a), Porphyromonas gingivalis
(P.g.)  Tannerella forsythia (T.f.)]. !  л  ÖZET: Bu çalışma, peri-implant yumuşak dokularının klinik
 од.   кл
ск ок л: д с  indeksleri, histolojik durum ve yaygın olarak peri-implant
д кс (GI), д кс кооо
ос д с о hastalıkları ile bağlantılı 3 patojenin [Aggregatibacter actino-
боод (SBI), д с  д кс, одфо mycetemcomitans, Porphyromonas gingivalis and Tannerella
об лл, (mGI)  д кс убого к, одф- forsythia] varlığı arasındaki korrelasyonu araştırmak am-
о об лл, (mPI) о лс окуг acıyla hazırlandı. Gereç ve Yöntem: Her bir hastanın bir
одого убого л у кдого у
ск dental implantı için dört klinik indeks değerlendirildi (n ⫽
ссл до (n ⫽ 10). Бл соб об 10). Bunlar Gingiva İndeksi (Gİ), Sulkus Kanama İndeksi
одд с ого убого к дл бк лого (SKİ), Mombelli tarafından değiştirilen Gingiva İndeksi
л (PCR),  к о д  бос (mGİ) ve Mombelli tarafından değiştirilen Plak İndeksi (mPİ)
 л гк к дл idi. Bakteri analizi (PCR) için subgingivadan plak örneği
гсолог
ского л. Кл
ск ок л alındığı gibi, histolojik analiz için peri-implant yumuşak
 л  ог  коог бл dokularından biyopsi de alındı. Klinik indeksler ve bulunan
соо с  с  д  гсолог
ск patojenlerin arasındaki korrelasyon, geliştirilmiş histolojik
ок л  (HI). ул . " удлос об- bir indeksle (Hİ) incelendi. Bulgular: Klinik indeksler (Gİ,
у сс
ск 
о ос  ду SKİ, ve mGİ) ile Hİ arasında istatistiksel açıdan önemli bir
кл
ск ок л (GI, SBI  mGI)  bağlantı bulunmadı. Buna tek istisna, merkezi lingual alanın
ок л  HI,  скл
  д кс mPI  mPİ değeri idi (r ⫽ 0.85, P ⫽ 0.0029). Merkezi bukkal
 ло облс  
 соо (r ⫽ 0,85; alandaki mPİ ile Hİ arasında olumlu bir korrelasyon eğilimi
p ⫽ 0,0029). Бл л   д  к saptandı (r ⫽ 0.63, P ⫽ 0.0544). Lenfosit ve plazmosit
оло ло ко л  ду д ксо mPI  sayımları, Hİ ile olumlu korrelasyon göstererek indeksin gü-
 ло облс  #
 соо  venilirliğine işaret etti. A. actinomycetemcomitans, P. gingi-
ок л  HI (r ⫽ 0,63; p ⫽ 0,0544). Кол
со valis ve T. forsythia patojenlerinin yaygınlığı Hİ ile önemli
лфоо  лоо оло ло düzeyde bir bağlantı göstermedi. Sonuç: Örnek sayısının ve
ко лолос с ок л  HI,
о оол  istatistiksel açıdan önemin az olmasına rağmen mPİ, dental
 доло д ос ок л. Уо  implantların etrafındaki enflamasyonun düzeyini değer-
сос  ог  коого A.a, lendirmek açısından mPİ’nin Hİ ile ilişkisinden de görüldüğü
P.g.  T.f.  ол 
о ос с gibi yararlı bulundu. Bu konunun açıklığa kavuşturulması
ок л  HI. од. " со   бол%о için daha fazla sayıda çalışmalar gerekmektedir.
кол
со об  ку сс
ску 
-
ос, о-доу, д кс mPI о  окс ANAHTAR KELİMELER: periodontal indeks, gingiva in-
ол  дл о к с  ос осл  гк deksi, plak indeksi, kanama indeksi, peri-implant hastalığı
IMPLANT DENTISTRY / VOLUME 18, NUMBER 4 2009 343

JAPANESE /

CHINESE /
344 PERI-IMPLANT DISEASE • FERREIRA JR et al

KOREAN /

You might also like