Long-Term Results of Peri-implant Conditions

in Periodontally Compromised Patients Following

Lateral Bone Augmentation
Philip L. Keeve, DMD, MSc1/Fouad Khoury, DMD, PhD2

Purpose: The aim of this retrospective study was to compare long-term (≥ 5 years) outcomes of implants
placed in patients treated for chronic periodontitis versus those placed in periodontally healthy patients. In
both groups, the implants were placed in alveolar ridges that were laterally augmented with autogenous bone
block grafts using a split bone block technique. Materials and Methods: Two hundred ninety-two patients
were screened in the course of supportive periodontal treatment examinations. Nonsmoking patients without
any severe systemic diseases who had adhered to regular supportive periodontal treatment for a minimum of
5 years after undergoing autogenous lateral grafting (using the split bone block technique), implant placement,
and prosthetic reconstructions were classified into two groups based on their presurgical status: periodontally
healthy patients (PHP) and periodontally compromised patients (PCP). Results: Clinical outcomes for 77
patients, 38 PHP and 39 PCP, were examined. All had been successfully treated for severe lateral atrophy
and received a total of 241 endosseous implants between 2002 and 2008. At the final examination, mean
bleeding on probing was 7.08% ± 7.27% in PHP and 14.49% ± 18.14% in PCP, a statistically significant
difference. Significantly higher Plaque Index and more recession were associated with a narrow (< 2 mm) width
of keratinized mucosa. Conclusion: Implants in alveolar ridges laterally augmented using a split bone block
technique revealed similar clinical peri-implant conditions in both PHP and PCP. Using autogenous bone block
grafts without biomaterials resulted in long-term peri-implant tissue stability. Int J Oral Maxillofac Implants
2017;32:137–146. doi: 10.11607/jomi.4880

Keywords: autogenous bone augmentation, CIST, lateral augmentation, peri-implant disease, periodontally
compromised patients, split bone block grafting

D uring the past decades, the use of dental implants in

partially or totally edentulous patients has become a
common practice for stomatognathic rehabilitation, re-
periodontally healthy patients (PHP). More peri-implant
bone loss in PCP compared with PHP has also been re-
ported in other studies.11–15 A recent meta-analysis, based
sulting in reliable long-term results. Although replacing on 16 studies, suggests that there is evidence of more im-
missing teeth with implants to rehabilitate periodontally plant loss and complications around implants in patients
compromised patients (PCP) is a realistic option,1–5 several with periodontitis.8,16 A study by Roccuzzo et al shows
studies have identified a high prevalence of peri-implant that the survival rate for solid screw implants is lower,
disease.6–9 Karoussis et al10 first provided evidence that and there are more peri-implant sites with bone loss in
hollow-screw dental implants placed in patients treat- patients with a history of periodontitis.3 To control rein-
ed for periodontal disease had a higher failure rate and fection and limit biologic complications, the value of sup-
more biologic complications than what was found in portive periodontal treatment is stressed in enhancing
the long-term outcomes of implant therapy. Higher im-
plant failure rates are found particularly in patients who
1Head, Department of Periodontology, Private Dental Clinic are affected by periodontitis and did not completely ad-
Schloss Schellenstein, Olsberg, Germany.
2Head and Medical Director, Private Dental Clinic Schloss here to supportive periodontal treatment.17–19
Schellenstein, Olsberg, Germany; Clinical Professor, Periodontally treated subjects may have insufficient
Department of Oral-Maxillo-Facial-Surgery, University Münster, bone volume due to atrophy, periodontal disease, and
Münster, Germany. trauma sequelae. Bone augmentation of the alveolar
ridge may be necessary to place an implant correctly
Correspondence to: Dr Philip Leander Keeve, Private Dental
Clinic Schloss Schellenstein, Am Schellenstein 1, 59939 in a sufficient quality and quantity of bone. Horizontal
Olsberg, Germany. Fax: +49 02962 9719 22. resorption of the alveolar ridge and subsequent lack of
Email: [email protected] adequate width for optimal implant placement are fre-
quent conditions following teeth removal.20 A number
©2017 by Quintessence Publishing Co Inc. of surgical procedures have been utilized to reconstruct

The International Journal of Oral & Maxillofacial Implants 137

© 2017 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.
NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
Keeve/Khoury

the alveolar crest. These procedures include “split-ridge” Helsinki and the Good Clinical Practice Guidelines. This
osteotomy for lateral expansion, osteodistraction, bone article was written following the STROBE (Strengthen-
grafting with different grafting materials (autogenous ing the Reporting of Observational Studies in Epidemi-
bone, allograft, xenograft, and alloplastic materials), ology, http://www.strobe-statement.org) guidelines.26
and guided bone regeneration (GBR) alone or in com-
bination with grafting materials.21,22 In the present Pretreatment Examination
study, a modification of autogenous block augmenta- Date of birth, medical history, and sex at the time of first
tion was used to improve healing and bone stability.23 visit to the clinic, and treatment planning records were
This concept of mandibular bone block grafting com- obtained. Subjects were clinically and radiographically
bines use of a thin block graft as a biologic membrane monitored at the first examination in the clinic. Full-
that gives form to particulated bone graft material. The mouth plaque scores and full-mouth bleeding scores
particulated bone has an increased surface area that were obtained, and probing depth (PD) was measured
gives it a high regenerative potential to improve mainly at four sites per tooth for all teeth using a periodontal
osteoconduction.23,24 probe (XP23/UNC 15; Hu-Friedy) and rounding off to the
The aim of the present study was to assess long- nearest millimeter. At the time of initial presentation and
term results of implant therapy using this approach treatment planning, two groups were formed based on
in two groups of patients who had been followed for the community periodontal index of treatment needs
a minimum of 5 years: periodontally healthy patients (CPITN).27 The groups consisted of periodontally com-
and periodontally compromised ones. Peri-implant promised patients (PCP), who showed a code 3 and/or
inflammation, number of peri-implant sites with bone 4 in CPITN at the first visit, and periodontally healthy
loss > 3 mm, and width of keratinized mucosa were patients (PHP), who showed codes between 0 and 2 in
recorded in both groups. CPITN at the first visit.

Periodontal Therapy
MATERIALS AND METHODS Depending on the cases, appropriate initial therapy
consisting of motivation (PHP and PCP), oral hygiene
Study Population instruction (PHP and PCP), extraction of hopeless teeth
Between April and June 2014, 292 recall patients who (PHP and PCP) and scaling and root planing (PCP) was
were receiving supportive periodontal treatment at performed to reduce periodontal pathogens in the
Private Dental Clinic Schloss Schellenstein, Germany, long term. Patients received periodontal surgery as
were screened by one external examiner for possible needed. Depending on patients’ needs and desires, an
inclusion in the study. All patients had been treated individual treatment was established. After reevalua-
at the clinic between 2002 and 2008 and afterward tion of the periodontal treatment, questionable teeth
adhered to regular supportive periodontal treatment were extracted and not included in prosthetic recon-
there. The study inclusion criteria were: struction.28 End-points of active periodontal treatment
were defined as no residual PDs of > 6 mm. Implant
• Lateral bone block augmentation accomplished us- surgery was only performed if full-mouth plaque
ing the split bone block technique scores and full-mouth bleeding scores were recorded
• Prosthetic reconstruction in function for more than as less than 30% at reevaluation.
5 years
• Xive implants (Xive S plus, Dentsply) Surgical Procedure
• Regular adherence to supportive periodontal treat- All grafting procedures were performed using the split
ment based on individual risk profiles determined bone block technique.23,29 Antibiotics, usually penicil-
with periodontal risk assessment25 lin G 1.2 g or in the case of allergy, clindamycin 600 mg,
were given intravenously before administration of local
The study exclusion criteria were: anesthesia. Surgeries were done under local anesthesia
and conscious sedation or general anesthesia. After har-
• Severe systemic diseases and uncontrolled meta- vesting an autogenous bone block using a MicroSaw
bolic disorders (Dentsply) from the retromolar area or chin (Fig 1b), the
• Smoking bone block was split into two blocks using a thin diamond
• Aggressive periodontitis disc of the MicroSaw (Fig 1c) and separated completely
• No interest in participating in the study with a larger diamond disc (Komet). The harvested ma-
terial was then scraped with a safescraper (Safescraper
The retrospective study was performed in accor- Twist curved, Meta) to obtain two 1-mm-thick blocks and
dance with the principles stated in the Declaration of particulated bone. After releasing a mucoperiosteal flap,

138 Volume 32, Number 1, 2017

© 2017 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.
NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
 Keeve/Khoury

a b c d

e f g

h i j
Fig 1   The split bone block technique: a representative case. (a) Baseline radiograph of a 52-year-old patient shows a dentition with
untreated chronic periodontitis and bony atrophy in horizontal and vertical dimensions in the maxilla and mandible. (b) Autogenous
bone block is harvested from the retromolar area using the MicroSaw. (c) The bone block is split in two blocks with a diamant disc
and separated completely. (d) Thin blocks were fixed on distance from the crest using MicroScrews. (e) The space between the block
and alveolar ridge is filled with particulated bone. (f) Postoperative radiograph of bone augmentation. (g) Three months later, implant
placement and removal of osteosynthesis material was performed. (h) Nine-year radiograph after inserting prosthetic reconstruction.
(i, j) Clinical images 9 years after prosthetic reconstruction.

implants were inserted in a one- or two-stage procedure, Soft tissue management32 and prosthetic recon-
according to the bone situation. In edentulous arches, struction with implant-supported fixed and removable
provisional implants (Tempion) were placed in the local screwed restorations were performed 3 months after im-
atrophied crest before the grafting procedure to support a plant placement.33 All restorations were individualized to
fixed provisional restoration while avoiding uncontrolled facilitate both the oral hygiene procedures and probing
loading in the grafted area.30 The thin bone blocks were along their circumferences. To establish a baseline, prob-
fixed with gap between the crest and block using medi- ing measurements were recorded around the implants,
cal stainless steel screws (MicroScrews, Stoma; Fig 1d).31 and radiographic data were collected after prosthesis
The space between the block and the recipient site was insertion.
filled with particulated bone (Fig 1e).24 Particles were well
packed in the space to avoid fibroblast migration and ob- Follow-up
tain greater contact between the host bed and the graft. Continuous evaluation, including reinstruction, cleaning,
No membrane or biomaterials were used. treatment of reinfected sites as needed, and motivation,
The periosteum was incised to obtain a primary was performed on patients’ individual supportive peri-
and tension-free wound closure. Antibiotics were giv- odontal treatment programs. Recall intervals were chosen
en for an additional 12 days (Isocillin 1.2 Mega, 1-1-1 on the basis of the periodontal risk assessment.25 Further-
or Clindamycin 600 mg, 1-1-1). In the two-stage ap- more, the following parameters were recorded:
proaches, implant placement (Xive S plus, Dentsply)
and removal of the osteosynthesis material followed • Probing depth (PD): measured at six sites (mesiobuc-
3 months later (Fig 1g). The number and position of cal, buccal, distobuccal, mesiolingual, lingual, and dis-
implants for each patient were chosen in accordance tolingual) by means of a periodontal probe (XP23/UNC
with the needs of the planned prosthesis. 15, Hu-Friedy) rounded off to the nearest millimeter.

The International Journal of Oral & Maxillofacial Implants 139

© 2017 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.
NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
Keeve/Khoury

Table 1  Patient Characteristics and Diagnostic The diagnosis of peri-implantitis was defined in com-
Parameters for PHP and PCP Groups parison to baseline clinical measurements and baseline
at Baseline, Post–Periodontal Therapy radiographs: presence of BOP and/or suppuration, in-
and Final Examination crease of more than 3 mm in PD compared with baseline
Variable PHP PCP P value
probing depth at prosthetic insertion,37 and progressive
crestal bone loss > 3 mm compared with baseline radio­
No. subjects 38 39 –
graphs.38 Treatment of peri-implant biologic compli-
Age (y) 42.9 ± 11.2 51.1 ± 14.9 .049*
cations was performed on the basis of the cumulative
Sex (% females) 52.63 46.15 .435 interceptive supportive therapy.39,40 The maintenance
Follow-up period 96.8 ± 30.4 98 ± 30.28 .172 care program included removal of hard deposits with soft
(mo) scalers, polishing with a rubber cup and paste, and in-
CPITN – baseline 1.26 ± 0.69 3.55 ± 0.5 .031* struction in effective oral hygiene practices. Treatment of
FMPS (%) peri-implant mucositis and peri-implantitis first included
Baseline 47 ± 6 56 ± 9 .369 a combination of antiseptic therapy with chlorhexidine
Post–periodontal 21 ± 4 19 ± 3 .267
digluconate and application of a local antibiotic delivery
therapy
Final examination 17 ± 2 18 ± 3 .184 device (Ligosan Slow Release, Heraeus Kulzer; Arestin,
FMBS (%)
OraPharma Europe). In cases of peri-implantitis, either
Baseline 13 ± 2 69 ± 14 .001* resective surgery with implantoplasty and an apical re-
Post–periodontal 11 ± 1 21 ± 4 .029* positioning flap or guided tissue regeneration with au-
therapy togenous bone and a nonresorbable membrane41 was
Final examination 12 ± 2 23 ± 4 .027*
performed depending on the vertical dimension of the
PD (mm) intraosseous defects. Implants with more than 70% bone
Baseline 2.54 ± 0.47 5.89 ± 1.32 .021*
Post–periodontal 2.61 ± 0.32
loss were removed. The number of sites treated according
2.89 ± 1.12 .411
therapy to therapy modalities with antibiotics and/or surgery in
Final examination 2.68 ± 0.35 2.98 ± 1.17 .585 the observation period was recorded.
*Statistically significant.
CPITN = community periodontal index of treatment needs; FMPS = full-
mouth plaque score; FMBS = full-mouth bleeding score; PD = probing
Statistical Analysis
depth. Data were expressed as median with interquartile
range and mean ± SD or counts and percentages. Non-
Gaussian distribution (tested by the Shapiro-Wilk test)
was found in all quantitative parameters, except age.
Between-group differences of the skewed quantitative
• Plaque score: total score (full-mouth plaque score) measures were tested for significance by the unpaired t
and for implants alone (Plaque Index [PI]34 and ap- test or two-way analysis of variance (ANOVA). Standard
proximal PI), measured at four sites per implant. PI errors were all estimated considering the correlation
and approximal PI were expressed as a percentage of observations, because several patients were treated
of the examined sites.35 with more than one implant. All tests were two-tailed,
• Bleeding on probing (BOP) score: total full-mouth and the statistical significance level was set at .05.
score (full-mouth bleeding score) and implant sites
(BOP), measured at six sites per implant. BOP was
expressed as a percentage of the examined sites.36 RESULTS
• Peri-implant inflammation: the Gingival Index (GI)34
was recorded for each implant to estimate the de- Patient Population
gree of peri-implant inflammation. Of the 292 patients in supportive periodontal treatment
• Peri-implant recession: the vestibular distance (me- who were initially screened, 77 met the inclusion criteria. Of
siobuccal, buccal, distobuccal) between the abut- the 77, 38 PHP received 136 implants, and 39 PCP received
ment connector and the peri-implant mucosal 105 implants. PCP had a statistically significantly higher
margin was measured to the nearest millimeter. mean age than PHP (51.1 ± 14.9 versus 42.9 ± 11.2 years).
• Keratinized mucosa around each implant at the facial The PHP group included 18 males (47.4%) and 20 females
and lingual site was identified with Schiller’s iodine (52.6%), while the PCP group consisted of 21 males (53.8%)
test and evaluated as the distance between the peri- and 18 females (46.2%; Table 1).The follow-up period, mea-
implant margin and the lining mucosa to the nearest sured from date of prosthetic insertion, was 97.8 months
0.1 mm. on average, with a range from 60 to 155 months.

140 Volume 32, Number 1, 2017

© 2017 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.
NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
 Keeve/Khoury

ns
*
20  80 

BOP mean per subject (%)

15  60 
Plaque (%)

10  40 

5  20

0  0 
a PHP PCP b PHP PCP

ns ns ns ns ns ns
0.8  8 

0.6  6 
PI mean (subjects)

PD mean (mm)
0.4 4

0.2 2

0.0  0 
l

al
l

al

l
l
ca

ra

ra

ia

ia
ca

ca

ra

ra
ca
ist

ist
es

es
-o

-o

-o

-o
uc

uc

uc

uc
-d

-d
-m

-m
-b

-b

-b

-b
P

P
PH

PC

PH

PC
P
P

P
P

P
PH

PC
PH

PC

PC
PH

PH

PC
c d

ns ns
1.0  *
1.0 
0.8 
Recessions mean (mm)

0.8 
0.6 
GI (mean)

0.6 
0.4
0.4 
0.2
0.2
0.0 
l

l
l

0.0 
ca

ra

ra
ca

-o

-o
uc

uc

PHP PCP
-b

-b

P
PH

PC
P

P
PH

PC

e f
Fig 2   Clinical parameters around the implants at follow-up examination in two groups: (a) plaque score [mean], (b) bleeding on prob-
ing (BOP) score [mean], (c) localized Plaque Index (PI) [mean], (d) probing depth (PD) [mean of vestibular and oral measurements], (e)
recessions [mean of vestibular or oral measurements], (f) Gingival Index (GI) [mean]; ns = not statistically significant; * = intergroup
statistical difference, P < .05.

Clinical Parameters at Final Examination group (Figs 2c and 2e). The mean Gingival Index was
At the final examination, the mean plaque score was significantly different between groups with 0.36 ±
5.81% ± 12.78% for the PHP group and 4.08% ± 7.01% 0.47 for PCP and 0.12 ± 0.28 for PHP (P < .05) (Fig 2f ).
for the PCP group. The BOP scores were 7.08% ± 7.27% In the subject-based analysis, 11.69% ± 0.33% of
(PHP) and 14.49% ± 18.14% (PCP) (Figs 2a and 2b), a cases of peri-implant mucositis and 6.49% ± 0.24%
significant difference (P < .01) (Fig 2b). Subdivided for of cases of peri-implantitis were diagnosed during
buccal and lingual sites, plaque, pocket depth, and re- the minimum follow-up period of 5 years. There were
cession depth were not significantly higher in the PCP statistical differences in the frequency of peri-implant

The International Journal of Oral & Maxillofacial Implants 141

© 2017 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.
NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
Keeve/Khoury

Fig 3   Number of (a) patients

Mucositis Peri-implantitis Mucositis Peri-implantitis and (b) implants with peri-im-
plant biologic complications
* * subdivided into two groups
25 25 during the follow-up period;
* *
*P < .05.
20  20 

Implants (%)
Subjects (%)

15 15

10 10

5 5

0  0 
a PCP PHP All patients b PCP PHP All patients

mucositis and peri-implantitis (P < .01) between the was done for two implants in two patients (PCP group).
PHP and PCP groups (Fig 3a). Peri-implant mucositis Two implants had to be removed, each 138 months af-
was diagnosed in 2.63% ± 0.16% of the PHP subjects ter prosthetic insertion. These two implants in one PCP
and 20.51% ± 0.41% of the PCP subjects, while peri- subject were lost due to peri-implantitis. When remov-
implantitis was diagnosed in 5.26% ± 0.22% of the ing those implants, vertical bone loss around the im-
PHP and 7.69% ± 0.27% of the PCP subjects. plants was 71% and 79%, respectively. Implant-based
Implant-based analysis showed 14.71% ± 0.5% of im- analysis revealed that implant loss was 0.9%, 0%, and
plants with peri-implant mucositis and 13.73% ± 0.43% 1.9% for all implants inserted in the PHP group and
with peri-implantitis (Fig 3b). In the PCP group, there the PCP group, respectively. Subject-based analysis
were 18% ± 0.53% of implants with peri-implantitis showed implant loss to be 1.2% for all subjects, 0%
in 7.69% ± 0.27% of the subjects, whereas in the PHP for the PHP group, and 2.5% for the PCP group. There
group, 9.62% ± 0.29% of implants with peri-implantitis were no statistical differences between the PHP and
were seen in 5.26% ± 0.22% of the subjects (Figs 3a and PCP groups. Statistical analysis revealed a significant
3b). Two implants in the PCP group were lost. difference in local antibiotic and surgical interventions
The mean width of keratinized mucosa around between the PHP and PCP groups (P < .01).
the implants was 4.3 ± 1.9 mm in the PCP group and
3.8 ± 1.6 mm in the PHP group, which was not a sig-
nificant difference (Fig 4a). Implants with more than DISCUSSION
2 mm width of keratinized mucosa42 showed statisti-
cally significant differences in mucosal recession (P < Long-term results of implant therapy in patients with
.01), plaque, and Gingival Index (P < .05) independent a history of periodontitis have received great attention
of PHP and PCP grouping (Figs 4b, 4d, and 4f ). There in the past years. Levin et al43 published a prospec-
were no differences in PD or BOP (both for buccal sites) tive cohort study consisting of 736 patients (2,336
between implants surrounded by more than 2 mm of implants) with a follow-up of 144 months (mean: 54.4
keratinized mucosa and those with less than 2 mm of months). The cumulative survival rate was 0.96 for
keratinized mucosa (Figs 4c and 4e). implants inserted in PHP, 0.95 for implants inserted
in moderate PCP, and 0.88 for implants inserted in se-
Interventions During Supportive Periodontal vere PCP at 108 months. The extended Cox model re-
Treatment vealed that until around 50 months, periodontal status
During the minimum 5-year follow-up period, local was not a significant factor, but after 50 months, the
antibiotics were applied for the treatment of biologic hazard for implant failure was eight times greater for
complications in 5.2% of the PHP cases (Fig 5). The cor- severe PCP. These results are in accordance with previ-
responding value for PCP was 10.26%. Surgical therapy ous publications,2,3 but they could not be confirmed
was undertaken in four subjects (2.63% in PHP, 7.69% in in more recent research.4 A minimum follow-up period
PCP). Implantoplasty was performed for nine implants of 60 months was chosen for the present study, and a
in four subjects (seven implants/three subjects in PCP stricter selection criteria was established regarding the
group, two implants/one subject in PHP group). GBR presence of inflammation and the need for additional

142 Volume 32, Number 1, 2017

© 2017 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.
NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
 Keeve/Khoury

15  *
ns 2.0

PI buccal/approximate
1.5 
10 
KT (mm)

1.0 

5 
0.5

0  0.0 
PHP PCP KT ≥ 2 mm KT < 2 mm
a b

10  ns *
3
PD buccal mean (mm)

Recessions mean (mm)

8 

6  2 

4 
1 
2 

0 
0 
KT ≥ 2 mm KT < 2 mm
KT ≥ 2 mm KT < 2 mm
c d

1.5 3 *
ns
BOP sites (%)

1.0  2 
GI

0.5  1 

0.0  0 
KT ≥ 2 mm KT < 2 mm KT ≥ 2 mm KT < 2 mm
e f
Fig 4   Differences between implants with wide and narrow keratinized mucosa: (a) distribution of width of keratinized tissue (KT)
between the two groups, (b) Plaque Index score [mean of buccal and proximal measurements], (c) probing depth (PD) [mean of buccal
measurements], (d) recessions [mean], (e) bleeding on probing [mean for buccal measurements], (f) Gingival Index [mean]; ns = not
statistically significant; * = intergroup statistical difference, P < .05.

15 PHP PCP

10 *
Subjects (%)

0 
Local Surgery
Fig 5   Number of patients treated with cumulative interceptive antibiotics needed
supportive therapy; ns = not statistically significant; * = inter- needed
group statistical difference, P < .05.

The International Journal of Oral & Maxillofacial Implants 143

© 2017 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.
NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
Keeve/Khoury

treatment during supportive periodontal treatment other grafting techniques, the disadvantages of the
to reduce the number of implants lost. The aim was split bone block technique are that the surgical proce-
to make it easier to determine the influence of bone dure is longer and more extensive, which may lead to
quality and initial periodontal diagnosis on peri-im- more swelling and postoperative morbidity in patients
plant conditions and implant survival.4 In comparison 7 days after surgery.
to the present 5-year results for the PHP group, Buser Although previous reviews47 have failed to sup-
et al published a retrospective analysis with a 10-year port the concept that a lack of keratinized mucosa
implant survival rate of 98.8%.44 In this large cohort of could jeopardize the maintenance of soft tissue health
PHPs with one implant type, the prevalence of peri-im- around dental implants, the results of current reviews
plantitis was small (1.8%) and comparable to the pres- and meta-analyses, derived mainly from cross-section-
ent study’s 5-year results. al studies, suggest that the presence of at least 1 to 2
However, the quality and quantity of the surround- mm of keratinized mucosa might be beneficial in mu-
ing bone can influence the progression of peri-implant cosal recession decreasing plaque accumulation, loss
inflammation processes. In cases requiring lateral of clinical attachment, and tissue inflammation.48 The
bone augmentation procedures, many bone graft op- results of the present study showed that peri-implant
tions are available, including autografts, xenografts, inflammations are found less frequently, if the minimal
allografts, and either cortical or cancellous structures, amount of keratinized mucosa is present. Moreover,
each of which has specific biologic and mechanical current results in other studies and reviews48,49 dem-
properties.21 Vascularized autografts are capable of in- onstrate that PI and GI were statistically significantly
tegrating to the host bone, even under adverse physi- lower in the wide keratinized mucosa group, suggest-
ologic conditions, while successful incorporation of ing a positive effect of keratinized mucosa on de-
allografts and xenografts depends more on the host creasing plaque accumulation. The current results are
bed.24 The biologic activity of a bone graft is a result also in accordance with several studies50,51 that have
of two functions: osteoinduction and mechanical sup- shown less mucosal recession and attachment loss
port. The survival of the grafted cellular element di- with wide keratinized mucosa. The mean PD, however,
rectly influences the osteogenic potential of a graft. was not significantly different in the wide versus nar-
This survival depends on the quality of the surgical row keratinized mucosa groups. This relationship was
procedure (trauma, short ex vivo exposure time, etc), also reported and conforms with previous studies.48,52
revascularization, grafted site preparation, the graft More recession was observed in the narrow keratinized
origin, and graft immobilization.31 mucosa group. There is a non–statistically significant
In the present study, the split bone block technique trend to have more bone loss in the narrow keratinized
was used to create a three-dimensional configuration mucosa group.52,53
for the in-growth of host capillaries, perivascular tis- Smoking can negatively influence the effects of
sue, and osteoprogenitor cells from the recipient into periodontal therapy.54 In a recent long-term study,
the graft. This technique results in an exponentially in- the authors concluded that important risk factors for
creased surface area of transplanted cancellous bone peri-implant inflammation were smoking and com-
and optimal recruitment of mesenchymal cells. It was pliance.55 Because of past recommendations based
chosen because it leads to the replacement of the graft on long-term data from well-defined patient popula-
material, which becomes host bone in a predictable tions,1 smokers and patients with systemic diseases
pattern under influences of load bearing. Therefore, it were excluded from the present study.
can be an optimal way to create immunologically po- The current data support the need for strict sup-
tent bone quality with long-term stability. portive periodontal treatment with reassessment of
When an autogenous bone block is used as graft- clinical and, when indicated, radiographic parameters
ing material to increase bone volume, the factor of at every follow-up visit to detect peri-implant infec-
time has a major influence on the ability to obtain tions and intervene as early as possible.39 The results
high-quality bone for osseointegration.29 The heal- from Roccuzzo et al2–4 demonstrated that PCP with ir-
ing time for autogenous bone is increased by at least regular supportive periodontal treatment tend to have
3 more months.23,24 Regarding peri-implant condi- more complications both around implants and teeth.
tions, the split bone block technique for lateral alveo- The results of the present study relate to patients in a
lar ridge augmentation leads to similar peri-implant private office who were compliant overall. Mir-Mari et
results around implants placed in native bone over a al estimated the prevalence of peri-implantitis in pa-
mean follow-up period of 8.15 years for both PHP and tients who were in supportive periodontal treatment
PCP.45,46 Autogenous bone block grafts used with- in private practice to be between 12% and 22%,56 re-
out biomaterials have shown a long-term stability sults that are similar to those of the present study and
in terms of peri-implant conditions. Compared with in university environment samples. The overall quality

144 Volume 32, Number 1, 2017

© 2017 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.
NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
 Keeve/Khoury

of supportive periodontal treatment in this study can 3. Roccuzzo M, De Angelis N, Bonino L, Aglietta M. Ten-year results of
a three-arm prospective cohort study on implants in periodontally
be confirmed by the significant reduction in the full- compromised patients. Part 1: Implant loss and radiographic bone
mouth plaque score and full-mouth bleeding score loss. Clin Oral Implants Res 2010;21:490–496.
values throughout at least 5 years of follow-up. Pa- 4. Roccuzzo M, Bonino L, Dalmasso P, Aglietta M. Long-term results of
a three arms prospective cohort study on implants in periodontally
tients undergoing successful supportive periodontal compromised patients: 10-year data around sandblasted and acid-
treatment had similarly low plaque scores regardless etched (SLA) surface. Clin Oral Implants Res 2014;25:1105–1112.
of their history of periodontitis. 5. Khoury F. Chirurgische Aspekte und Ergebnisse zur Verbesserung
des Knochenlagers vor implantologischen Maßnahmen. Implanto-
Patients treated for chronic periodontitis often suf- logie 1994;3:237–247.
fer from decreased minimal residual bone volume. 6. Costa FO, Takenaka-Martinez S, Cota LO, Ferreira SD, Silva GL, Costa
The present investigation indicates that endosseous JE. Peri-implant disease in subjects with and without preventive
maintenance: A 5-year follow-up. J Clin Periodontol 2012;39:173–
implant placement with horizontal alveolar ridge aug- 181.
mentation using a split bone block technique may 7. Marrone A, Lasserre J, Bercy P, Brecx MC. Prevalence and risk factors
lead to peri-implant conditions comparable to implant for peri-implant disease in Belgian adults. Clin Oral Implants Res
2013;24:934–940.
placement in periodontally healthy patients for up to 8. Sgolastra F, Petrucci A, Severino M, Gatto R, Monaco A. Periodon-
5 years posttherapy. It must be emphasized that these titis, implant loss and peri-implantitis. A meta-analysis. Clin Oral
results can only be obtained in conjunction with a reg- Implants Res 2015;26:e8–e16.
9. Aguirre-Zorzano LA, Estefanía-Fresco R, Telletxea O, Bravo M.
ular periodontal and implant prosthetic maintenance Prevalence of peri-implant inflammatory disease in patients with a
program. history of periodontal disease who receive supportive periodontal
therapy. Clin Oral Implants Res 2015;26:1338–1344.
10. Karoussis IK, Salvi GE, Heitz-Mayfield LJ, Brägger U, Hämmerle CH,
Lang NP. Long-term implant prognosis in patients with and without
CONCLUSIONS a history of chronic periodontitis: A 10-year prospective cohort
study of the ITI Dental Implant System. Clin Oral Implants Res
2003;14:329–339.
Overall, implant placement along with horizontal al- 11. Mengel R, Behle M, Flores-de-Jacoby L. Osseointegrated implants
veolar ridge augmentation using a split bone block in subjects treated for generalized aggressive periodontitis: 10-year
technique offers predictable long-term results. In results of a prospective, long-term cohort study. J Periodontol
2007;78:2229–2237.
particular, healthy patients who take part in a proper 12. Mengel R, Flores-de-Jacoby L. Implants in patients treated for gen-
maintenance program appear to have a very low in- eralized aggressive and chronic periodontitis: A 3-year prospective
cidence of biologic complications. Patients with a his- longitudinal study. J Periodontol 2005;76:534–543.
13. Mengel R, Schröder T, Flores-de-Jacoby L. Osseointegrated
tory of periodontitis show similar results in regular implants in patients treated for generalized chronic periodontitis
supportive periodontal treatment. Excellent values for and generalized aggressive periodontitis: 3- and 5-year results of a
long-term peri-implant conditions can be obtained in prospective long-term study. J Periodontol 2001;72:977–989.
14. Roos-Jansåker AM, Lindahl C, Renvert H, Renvert S. Nine- to four-
PHP and PCP who have experienced a previous loss of teen-year follow-up of implant treatment. Part I: Implant loss and
horizontal alveolar ridge dimensions but are following associations to various factors. J Clin Periodontol 2006;33:283–289.
an individual maintenance care program. Keratinized 15. Roos-Jansåker AM, Lindahl C, Renvert H, Renvert S. Nine- to
fourteen-year follow-up of implant treatment. Part II: Presence of
mucosa width may be important for healthy peri-im- peri-implant lesions. J Clin Periodontol 2006;33:290–295.
plant conditions around implants and appears to in- 16. Lee DW. Periodontitis and dental implant loss. Evid Based Dent
fluence the width of mucosal recession, plaque, and 2014;15:59–60.
17. De Boever AL, Quirynen M, Coucke W, Theuniers G, De Boever JA.
Gingival Index. Clinical and radiographic study of implant treatment outcome in
periodontally susceptible and non-susceptible patients: A prospec-
tive long-term study. Clin Oral Implants Res 2009;20:1341–1350.
18. Schmidlin K, Schnell N, Steiner S, et al. Complication and failure
ACKNOWLEDGMENTS rates in patients treated for chronic periodontitis and restored with
single crowns on teeth and/or implants. Clin Oral Implants Res
The authors reported no conflicts of interest related to this 2010;21:550–557.
study. 19. Buchmann R, Khoury F, Faust C, Lange DE. Peri-implant conditions
in periodontally compromised patients following maxillary sinus
augmentation. A long-term post-therapy trial. Clin Oral Implants
Res 1999;10:103–110.
20. Araújo MG, Sukekava F, Wennström JL, Lindhe J. Ridge alterations
REFERENCES following implant placement in fresh extraction sockets: An experi-
mental study in the dog. J Clin Periodontol 2005;32:645–652.
1. Renvert S, Persson GR. Periodontitis as a potential risk factor for 21. Jensen SS, Terheyden H. Bone augmentation procedures in local-
peri-implantitis. J Clin Periodontol 2009;36:9–14. ized defects in the alveolar ridge: Clinical results with different
2. Roccuzzo M, Bonino F, Aglietta M, Dalmasso P. Ten-year results of a bone grafts and bone-substitute materials. Int J Oral Maxillofac
three arms prospective cohort study on implants in periodontally Implants 2009;24(suppl):s218–s236.
compromised patients. Part 2: Clinical results. Clin Oral Implants Res 22. Chiapasco M, Casentini P, Zaniboni M. Bone augmentation
2012;23:389–395. procedures in implant dentistry. Int J Oral Maxillofac Implants
2009;24(suppl):s237–s259.

The International Journal of Oral & Maxillofacial Implants 145

© 2017 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.
NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
Keeve/Khoury

23. Khoury F, Khoury C. Mandibular bone block grafts: Instrumentation, 42. Ericsson I, Lindhe J. Recession in sites with inadequate width of
harvesting technique and application. J Par Impl Orale 2006;25:15– the keratinized gingiva. An experimental study in the dog. J Clin
24. Periodontol 1984;11:95–103.
24. Khoury F, Khoury C, Antoun H, Missika P. Bone Augmentation in 43. Levin L, Ofec R, Grossmann Y, Anner R. Periodontal disease as a risk
Oral Implantology. Chicago: Quintessence, 2007. for dental implant failure over time: A long-term historical cohort
25. Lang NP, Tonetti MS. Periodontal risk assessment (PRA) for patients study. J Clin Periodontol 2011;38:732–737.
in supportive periodontal therapy (SPT). Oral Health Prev Dent 44. Buser D, Janner SF, Wittneben JG, Brägger U, Ramseier CA, Salvi
2003;1:7–16. GE. 10-year survival and success rates of 511 titanium implants
26. Vandenbroucke JP, von Elm E, Altman DG, et al. Strengthening the with a sandblasted and acid-etched surface: A retrospective study
Reporting of Observational Studies in Epidemiology (STROBE): in 303 partially edentulous patients. Clin Implant Dent Relat Res
Explanation and elaboration. Int J Surg 2014;12:1500–1524. 2012;14:839–851.
27. Ainamo J, Barmes D, Beagrie G, Cutress T, Martin J, Sardo-Infirri J. 45. Clementini M, Morlupi A, Canullo L, Agrestini C, Barlattani A.
Development of the World Health Organization (WHO) com- Success rate of dental implants inserted in horizontal and vertical
munity periodontal index of treatment needs (CPITN). Int Dent J guided bone regenerated areas: A systematic review. Int J Oral Max-
1982;32:281–291. illofac Surg 2012;41:847–852.
28. Beikler T, Flemmig T. Implant versus tooth retention from the peri- 46. Donos N, Mardas N, Chadha V. Clinical outcomes of implants follow-
odontal perspective. Quintessence Perio 2006;3:167–176. ing lateral bone augmentation: Systematic assessment of available
29. Khoury F. Augmentation of the sinus floor with mandibular bone options (barrier membranes, bone grafts, split osteotomy). J Clin
block and simultaneous implantation: A 6-year clinical investiga- Periodontol 2008;35:173–202.
tion. Int J Oral Maxillofac Implants 1999;14:557–564. 47. Wennström JL, Derks J. Is there a need for keratinized mucosa
30. Khoury F, Happe A. Interim implants in extensive bone trans- around implants to maintain health and tissue stability? Clin Oral
plantation procedure: Results of a clinical study. Implantologie Implants Res 2012;23:136–146.
2000;9:375–387. 48. Lin GH, Chan HL, Wang HL. The significance of keratinized mucosa
31. Khoury F, Hidajat H. Secure and effective stabilization of different on implant health: A systematic review. J Periodontol 2013;84:1755–
sized autogenous bone grafts. European Journal of Oral Surgery 1767.
2011;2:65–70. 49. Boynueğri D, Nemli SK, Kasko YA. Significance of keratinized mu-
32. Khoury F, Happe A. Soft tissue management in oral implantol- cosa around dental implants: A prospective comparative study. Clin
ogy: A review of surgical techniques for shaping an esthetic and Oral Implants Res 2013;24:928–933.
functional peri-implant soft tissue structure. Quintessence Int 50. Zigdon H, Machtei EE. The dimensions of keratinized mucosa
2000;31:483–499. around implants affect clinical and immunological parameters. Clin
33. Pape F, Khoury C, Khoury F. Treatment protocol for complex Oral Implants Res 2008;19:387–392.
implant-prosthetic rehabilitations: A clinical report. Implantologie 51. Adibrad M, Shahabuei M, Sahabi M. Significance of the width of
2003;11:259–270. keratinized mucosa on the health status of the supporting tis-
34. Loe H, Silness J. Periodontal disease in pregnancy. I. Prevalence and sue around implants supporting overdentures. J Oral Implantol
severity. Acta Odontol Scand 1963;21:533–551. 2009;35:232–237.
35. Saxer UP, Mühlemann HR. [Motivation and education]. SSO Schweiz 52. Roos-Jansåker AM, Renvert H, Lindahl C, Renvert S. Nine- to four-
Monatsschr Zahnheilkd 1975;85:905–919. teen-year follow-up of implant treatment. Part III: Factors associ-
36. Lang NP, Adler R, Joss A, Nyman S. Absence of bleeding on probing. ated with peri-implant lesions. J Clin Periodontol 2006;33:296–301.
An indicator of periodontal stability. J Clin Periodontol 1990;17:714– 53. Kehl M, Swierkot K, Mengel R. Three-dimensional measurement
721. of bone loss at implants in patients with periodontal disease. J
37. Peri-implant mucositis and peri-implantitis: A current understand- Periodontol 2011;82:689–699.
ing of their diagnoses and clinical implications. J Periodontol 54. Sgolastra F, Petrucci A, Severino M, Gatto R, Monaco A. Smoking
2013;84:436–443. and the risk of peri-implantitis. A systematic review and meta-
38. Mombelli A, Müller N, Cionca N. The epidemiology of peri-implanti- analysis. Clin Oral Implants Res 2015;26:e62–e67.
tis. Clin Oral Implants Res 2012;23:67–76. 55. Aglietta M, Siciliano VI, Rasperini G, Cafiero C, Lang NP, Salvi GE.
39. Mombelli A, Lang NP. The diagnosis and treatment of peri-implanti- A 10-year retrospective analysis of marginal bone-level changes
tis. Periodontol 2000 1998;17:63–76. around implants in periodontally healthy and periodontally com-
40. Figuero E, Graziani F, Sanz I, Herrera D, Sanz M. Management of promised tobacco smokers. Clin Oral Implants Res 2011;22:47–53.
peri-implant mucositis and peri-implantitis. Periodontol 2000 56. Mir-Mari J, Mir-Orfila P, Figueiredo R, Valmaseda-Castellón E, Gay-
2014;66:255–273. Escoda C. Prevalence of peri-implant diseases. A cross-sectional
41. Khoury F, Buchmann R. Surgical therapy of peri-implant disease: A study based on a private practice environment. J Clin Periodontol
3-year follow-up study of cases treated with 3 different techniques 2012;39:490–494.
of bone regeneration. J Periodontol 2001;72:1498–1508.

146 Volume 32, Number 1, 2017

© 2017 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.
NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.