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Treatment of peri-implantitis
using multiple applications of
chlorhexidine chips: a
double-blind, randomized
multi-centre clinical trial
Machtei EE, Frankenthal S, Levi G, Elimelech R, Shoshani E, Rosenfeld O,
Tagger-Green N, Shlomi B. Treatment of peri-implantitis using multiple
applications of chlorhexidine chips: a double-blind, randomized multi-centre clinical
trial. J Clin Periodontol 2012. 39: 1198–1205. doi: 10.1111/jcpe.12006.
Abstract
Background: Universal strategies for managing peri-implantitis are yet to be
adopted. The aim of this study is to examine a protocol of intensive application
of chlorhexidine containing chips in sites with peri-implantitis.
Materials and Methods: This multi-centre, randomized, double-blind, parallel,
two-arm clinical trial included 60 patients (77 implants) with probing depth (PD)
6–10 mm and bone loss ! 2 mm around 1–2 implants. One to two weeks follow-
ing SRP, baseline measurements were made followed by implants’ debridement.
Patients were randomized to receive matrix chips (MatrixC) or chlorhexidine
Chips (PerioC). Measurements and chips placement were repeated at weeks 2, 4,
6, 8, 12 and 18. At 6 months, patients returned for final examination.
Results: Probing depth reduction was greater in the PerioC (2.19 ± 0.24 mm)
compared with MatrixC (1.59 ± 0.23 mm), p = 0.07. Seventy percentage of the
implants in the PerioC and 54% in the MatrixC had PD reduction ! 2 mm.
Likewise, 40% of the sites (PerioC) and 24% (MatrixC) had PD reduc-
tion ! 3 mm. Clinical attachment level gains for both groups were significant;
however, the changes in the PerioC group were significantly greater than in
MatrixC [2.21 ± 0.23 mm. and 1.56 ± 0.25 mm respectively, p = 0.05]. Bleeding
on probing was reduced by half in both groups.
Conclusion: Frequent placement of PerioC and MatrixC together with implants
debridement resulted in a substantial improvement in sites with peri-implantitis.
Further studies will be required to fully appreciate the mechanism of this treat-
ment.
Eli E. Machtei1
, Shai Frankenthal1
,
Guy Levi1
, Rina Elimelech1
, Eyal
Shoshani2
, Olivia Rosenfeld3
, Nirit
Tagger-Green3
and Benjamin Shlomi3
1
Department of Periodontology, School of
Graduate Dentistry, Rambam HCC and
Faculty of Medicine, Technion – Israeli
Institute of Technology, Haifa, Israel; 2
Dexcel
Pharma, Or-Akiva, Israel; 3
Department of
Oral and Maxillofacial Surgery, Tel Aviv
Sourasky Medical Center, Tel-Aviv, Israel
Key words: anti-Inflammatory agents;
antimicrobial agents; clinical trial; delayed-
action preparations; dental implants;
peri-implantitis; therapy
Accepted for publication 11 August 2012
Peri-implantitis is rapidly becoming
a major oral disease entity that is
frequently encountered in the dental
office. With approximately ten mil-
lion new implants placed annually
worldwide (Markets for Dental
Conflict of interest and source of funding statement
This study was supported by a research grant from Dexcel Pharma, Or-Akiva, Israel.
The authors declare no conflict of interest except for Mr. Eyal Shoshani who was on
the R&D team of Dexcel Pharma at the time of the study. Prof. Eli E. Machtei also
served as a consultant for Dexcel Pharma.
© 2012 John Wiley & Sons A/S1198
J Clin Periodontol 2012; 39: 1198–1205 doi: 10.1111/jcpe.12006
Implants and Final Abutments
2009), and tens of millions of
implants that are currently function-
ing, the magnitude of this problem is
ever growing.
In their systematic review, Zitz-
mann & Berglundh (2008) have
reported that 50% of the implants
and 80% of the patients had mucosi-
tis, while peri-implantitis was
reported in 12–43% of the implants
and 28–56% of the patients.
Conversely, Jung et al. (2008) in a
systematic review and meta-analysis
on the 5 years survival and complica-
tions of dental implants supporting
single crowns reported lower frequen-
cies of peri-implantitis (~ 10%).
These differences in the reported
prevalence might be associated with
the threshold used to define disease.
Koldsland et al. (2010) studied 164
subjects treated with dental implants
and followed for over 8 years; he was
able to show that depending on the
different clinical and radiographic
threshold that was used, disease prev-
alence varied considerably between
11.3% and 47.1%. Another possible
variable that might affect the preva-
lence of peri-implantitis is patient’s
periodontal status. Roccuzzo et al.
(2012) reported their results of a
10-year prospective cohort study on
implants in periodontally healthy and
compromised patients treated with
scaling and root planing (SRP):
10.7% of the implants in the peri-
odontally healthy cases required
some kind of adjunctive (surgical or
non-surgical) treatment through these
years compared with 15.9% and
27.2% for patients with initial diag-
nosis of moderate and severe chronic
periodontitis. Similar findings were
recently reported by Cho-Yan Lee
et al. (2012).
Optimal treatment strategies for
the treatment of peri-implantitis are
yet to be commonly agreed upon.
Renvert et al. (2008a) in a literature
review have reported that non-surgi-
cal therapy was not found to be
effective in these lesions. These
authors, in a subsequent double-
blind study (2009) of debridement
of dental implants affected by peri-
implantitis, using hand and ultra-
sonic instruments, have reported
only minimal (0.2 mm.) and statisti-
cally insignificant change in probing
depth (PD) 6-month post-operative
for both treatment groups. Like-
wise, Lindhe & Meyle (2008) on
behalf
of the European workshop on
Periodontology have concluded that
non-surgical mechanical therapy
causes the reduction of inflamma-
tion as evident in the decrease in
bleeding on probing (BOP); how-
ever, the overall improvement in
clinical parameters is at best unpre-
dictable. Furthermore, Tonetti &
Palmer (2012) on behalf of the 8th
European workshop on Periodontol-
ogy referred to the relatively small
number of well-designed randomized
clinical trials in implant dentistry as
an impairment for our progress in
this field.
To further improve treatment
outcome, several adjunctive treat-
ment modalities were employed.
Renvert et al. (2011) reported similar
and only modest improvement in
PD, when using air abrasive or Er:
YAG laser therapy in patients with
peri-implantitis. Sahm et al. (2011)
reported that 6 months after treat-
ment of peri-implantitis with either
air abrasive of mechanical cleaning
and subgingival application of
chlorhexidine solution and gel, mean
pocket reduction and clinical attach-
ment level (CAL) gain were both
approximately 0.5 mm, which was
similar in both groups. The use of
local delivery of minocycline to
enhance treatment response in these
cases was reported by Salvi et al.
(2007). Despite some pocket reduc-
tion, six patients (25% of the entire
study population) were removed
from the study as the implants were
either explanted or required addi-
tional therapy due to ! 2 mm.
increase in PD during the observa-
tion period. Similarly, Bu¨ chter et al.
(2004) have utilized doxycyline
gel for the treatment of peri-implan-
titis. PD reduction and CAL gain
were greater (0.6 mm) in sites
with the adjunctive treatment com-
pared with subgingival debridement
only.
Recently (Machtei et al. 2011),
we have been able to demonstrate
that frequent application of biode-
gradable matrix containing chlorhex-
idine (PerioChip®
; Dexcel Pharma,
Or-Akiva, Israel) in patients with
chronic periodontitis with
PD ! 5 mm resulted in a sizeable
improvement in mean PD (2.1 mm)
and gain in CAL (1.7 mm).
Several in vitro investigations have
demonstrated that chlorhexidine
(CHX) is adsorbed to the oxide layer
of titanium surfaces. Recent data
indicate that the type of oxide may
influence the amount of CHX
absorbed (Morra et al. 2004, Barbour
et al. 2009). It has also been shown
that the absorption kinetics is directly
related to implants’ surface roughness
and was also positively correlated
with the concentration of the CHX
solution. A desorption occurs within
24 hours and inhibits bacterial
growth (Kozlovsky et al. 2006).
Therefore, the aim of this study is
to examine a novel protocol of
intensive application of chlorhexi-
dine chips on peri-implant health in
sites with peri-implantitis.
Materials and Methods
This study was designed as a multi-
centre, randomized, double-blind,
parallel, two-arm clinical trial. The
study was initially approved by the
institutional ethic committees (IECs)
of both medical centres and posted
on the NIH website.
Patients seeking treatment for
peri-implant disease at either Ram-
bam health care campus in Haifa or
at the Sourasky Medical Center in
Tel-Aviv were initially screened for
this study (with first patient in
17.3.2010 and last patient out
27.10.2011).
Inclusion criteria
Patients 21 years or older with peri-
implantitis characterized by the pres-
ence of at least one implant with PD
of 6–10 mm in depth (potential target
implant), with BOP and radiographic
evidence of bone loss. Patients were
required to read and if satisfied with
it, sign a written consent form that
was previously approved by the IECs.
Also, patients needed to affirm their
availability for the 6-month duration
of the study. At screening, all patients
had a periodontal examination and
when necessary periodontal treatment
for the existing teeth was rendered
first and the study commencement
was postponed.
Exclusion criteria
(i) History of allergy to CHX
or regular use of it (ii) horizontal
© 2012 John Wiley & Sons A/S
Protocol for the treatment of peri-implantitis 1199
inter-implant distance <2 mm (if an
adjacent implant existed); (iii) Tita-
nium Plasma-sprayed or hydroxylap-
atite coated implants; (iv) systemic
conditions that might affect inflam-
mation and bleeding; (v) Any local
irritation that could not be negoti-
ated (i.e. orthodontic appliances; ill-
fitted restorations; apical pathology);
(vi) systemic antibiotic therapy or
periodontal/mechanical/local delivery
therapy within 6 weeks prior to
study entry and throughout the
study duration; (vii) continuous use
of non-steroidal anti-inflammatory
drugs or drugs known to cause gin-
gival overgrowth; (viii) pregnancy or
intention to become pregnant in the
next 6 months.
At Screening visit (Week 1),
patients came to establish eligibility.
At this time, the following informa-
tion was recorded: Demographic
data and smoking habits, relevant
past medical history and concomi-
tant diseases and medications (mea-
surements were performed by a
periodontist or oral surgeon).
Oral examination was performed
and the following parameters were
recorded: plaque index, gingival
index and BOP. In addition, the fol-
lowing site measurements were per-
formed for the target implants using
a manual 15 mm. University of
North Carolina probe (Hu-Friedy,
Chicago, IL, USA): BOP using a
dichotomized 0/1 scale; PD, gingival
recession (GR) measured from the
crown/restoration margins. CAL was
calculated as the sum of PD+GR.
Periapical radiographs were further
used to confirm bone loss ( ! 2 mm)
and screen for any exclusion condi-
tions.
Each qualified patient then
underwent supragingival scaling of
all the teeth and implants (if not
done in the 6 weeks prior the
Screening visit) using ultrasonic
instruments (OEM; Electeo Medical
System, Nyon, Switzerland) with
standard periodontal tips (performed
by a well experienced dental hygien-
ists). Following oral hygiene instruc-
tion, patients were given a sodium
fluoride toothpaste (Colgate cavity
protection; Colgate–Palmolive, NJ,
USA) and soft toothbrush to be
used throughout the study. One to
two weeks later, patients were
invited to return for the baseline visit
(week 0), at which time final eligibil-
ity was determined. Periodontal
assessments and measurements were
repeated for all potential target
implants. For each patient, at least
one and no more than two implants
(if available) with PD 6–10 mm were
selected. In cases where more than
two eligible implants were present,
the following selection grid was
employed: implants with the deepest
pocket/s (primary); different arch
(secondary); furthest away from each
other (tertiary).
Next, surface debridement was
performed for the chosen target
implant/s and the two adjacent teeth
using ultrasonic instruments.
Randomization, allocation concealment
and blinding
Patients were then randomized to
receive either a biodegradable cross-
linked gelatin matrix chip (matrix
chip group, MatrixC) or matrix con-
taining 2.5-mg chlorhexidine-gluco-
nate chips (PerioC; Dexcel Pharma).
Eligible patients at baseline visit were
assigned a randomization number
starting from 601. Each randomiza-
tion number was randomly assigned
to one of the two letters A or B; each
letter assigned randomly to one of the
two treatments MatrixC or PerioC.
Randomization was performed using
a computer-generated sequence of
Random binomial numbers by SAS
9.2 RANBIN CALL. The blinding of
the study could only be broken upon
completion of the clinical phase of the
study including adverse effects (AE)
and database queries all being
resolved. One set of sealed envelopes
was provided to the investigator con-
taining individual randomization
codes which was kept at the investiga-
tional site in case of a severe adverse
effect (SAE); however, none have
occu-rred.
To ensure examiner’s blindness,
two separate investigators attended to
each patient: one that placed
the chips and another one making the
clinical measurements. Also, the chips
were identical in size, shape and col-
our so that even the examiner that
placed them was unaware of the iden-
tity of the chips that were placed.
Upto four chips were inserted for
each implant’s sites which PD was
6–10, and patients were discharged
with instruction to refrain from
using toothpicks and other proximal
hygiene aids for 10 days. To ensure
blindness, chips were inserted by a
different investigator than that per-
forming the clinical measurements.
Patients were also asked to notify
the investigator of any adverse reac-
tion. At each visit, they were also
actively approached to inquire of
any adverse reaction that they might
have failed to report.
Patients returned at weeks 2, 4, 6,
8, 12 and 18 and clinical measure-
ments were repeated. For target sites
with PD still ! 6 mm new chips
were re-inserted. At 12 weeks, supra-
gingival debridement was also per-
formed. At each of these visits,
patients were asked to report of any
AE that they might have encoun-
tered and this was recorded. In cases
where the target pockets depths
increased during the study in more
than 2 mm (confirmed on a subse-
quent visit), the patient was with-
drawn from the study and referred
for surgical therapy. At 6 months,
patients returned for the final clinical
examination and determination of
any further treatment needs.
Statistical analysis
Power calculation was initially per-
formed to determine sample size.
Assuming normal distribution, nomi-
nal power of 80%, a 0.05, a stan-
dard deviation of the difference
between treatments of 1.18 mm
(based on previous study), we need
28 volunteers in each treatment
group (using Two sample t-test for
mean difference) to achieve a mean
difference between treatments of
À0.9 mm (SAS 9.2 POWER PRO-
CEDURE, SAS Institute, Cary, NC,
USA). Thus, we chose to allocate 30
volunteers to each study treatment.
The statistical procedure used
was SAS procedure GENMODE.
The modelization method: General-
ized mixed linear model with gener-
alized estimating equations method
for repeated measures. This method
was used for linear models (ΔPPD,
CAL) and for binary models (ΔBOP,
success to achieve 1,2,3,4 mm PPD
reduction) with different links and
distribution functions for each
variable.
Continuous variables were analy-
sed and compared using t-test when
appropriate. Discrete variables were
compared using two-sided fisher’s
© 2012 John Wiley & Sons A/S
1200 Machtei et al.
exact test. PD reduction, baseline to
6 months served as the primary out-
come variable. Secondary outcome
variables included changes in CAL,
GR, BOP and PD at weeks 2, 4, 6,
8, 12 and 18. Change in PD and
CAL was modelled using a linear-
mixed model (SAS 9.2 Mixed Proce-
dure) with treatment, and centre as
fixed factors. Patient and pocket
were entered as random effects.
Analysis was done for subjects that
completed the study and again for
all patients that were enrolled [inten-
tion to treat (ITT)] subjects, with
data missing being complemented
using last observation carried
forward (LOCF) method.
Contrasts with 95% confidence
intervals for the difference or ratio
between the changes were computed.
Analysis for the number of pock-
ets with at least 1/2/3/4 mm reduc-
tion in PD, and analysis for BOP for
the target implant/s measured at
each visit were analysed by a Coch-
ran–Mantel–Haenszel (CMH) test.
All treatment comparisons were
two-sided at the 0.05 level of signifi-
cance. Similar mixed model with a
binary distribution and Logit link
was used for BOP changes during
the trial.
Similar mixed models for PD and
CAL with time as a fixed repeated
covariate were used to reveal the
changes over time of these parameters.
Results
Sixty patients, 35 females and 25
males, age 27–77 years (mean ± SD
59.18 ± 9.2) with a total of 77 den-
tal implants were initially accepted
into the study. Thirty-six patients
(44 implants) were in Centre A and
24 patients (33 implants) in Centre
B (Table 1). Thirty patients with 40
implants were randomly assigned
into the chlorhexidine group (Pe-
rioC), whereas an equal numbers of
patients with 37 implants were
included in the matrix chip group
(MatrixC). Of the original 60
patients that were enrolled, 56
patients (93.3%) were available and
eligible for the final examination
6 months later (the corresponding
implant level retention rate was
94.8%, 73/77). Four patients, all
from the MatrixC were exited from
the study. One required extended
antibiotic use (non-related to the
study), one had total hip replace-
ment and could not come for the
follow-up and the other two were
withdrawn, due to emergency dental
treatment which interfered with the
study endpoints.
Five patients in each group were
current smokers, whereas the rest
were former smokers or never
smoked. Both groups and both cen-
tres were similar in their baseline
demographic and smoking habits.
Baseline PDs (7.60 and 7.21 mm
for the PerioC and MatrixC groups
respectively) have shown continuous
improvement throughout the study
(Fig. 1). Greater reduction was
noticeable in the first 8 weeks with
continuous improvement, although
at slower rate thereafter. Mean
pocket depth at 6 months were 5.47
and 5.48 mm PerioC and MatrixC
respectively, which were significantly
different from baseline (p = 0.0001).
PD improvement in the PerioC
(2.13 mm.) was greater than that
for the MatrixC (1.73 mm.),
p = 0.17 (Table 2a). When data
were analysed with LOCF, these
changes (2.19 and 1.59 mm respec-
tively, Table 2b) were borderline
significant (p = 0.07, mixed model).
Probing depth reduction was further
dichotomized into sites with PD
reduction that was equal to/or
greater than a threshold (Table 3).
At 6 months, 93% of the implants
in the PerioC and 88% in the Ma-
trixC achieved at least 1-mm pocket
reduction. For pocket reduction
! 2 mm, 70% of the sites in the
PerioC and 54% in the MatrixC
reached this threshold (p = 0.077).
Likewise, 40% of the sites in the
PerioC and 24% of the sites in the
MatrixC have had pocket reduction
that was equal to or greater than
3 mm (p = 0.073). Chips were
inserted until PD was reduced to
5mm. To this end, 11 of the 40
implants in the PerioC (28%) and 5
of the 33 implants (15%) in the
MatrixC group reached this goal at
6 months. At baseline, 60 implants
(78%) required one or two chips,
whereas three implants required
four chips each. At the last treat-
ment visit, 43 implants (56%) did
not require any chip placement, 30
required 1–2 chips (Table 4).
Both treatment modalities have
shown significant improvement in
CAL (Fig. 2). Sites in the PerioC had
a mean baseline CAL of 7.88 ± 0.2
mm (SE) with an ultimate 6 months
CAL level of 5.70 ± 0.3 mm
(p = 0.001, mixed model). Similarly,
Sites in the MatrixC had a mean base-
line CAL of 7.63 ± 0.3 mm (SE) with
a final 6 months CAL level of
5.94 ± 0.3 mm (p = 0.001, mixed
model). These differences in CAL
gain amounted to 2.18 mm in the
PerioC and 1.69 mm in the MatrixC
(p = 0.12, mixed model), while when
using all IIT patients, CAL gain (2.21
and 1.56 mm respectively) were sig-
nificantly different (p = 0.05, mixed
model).
At baseline, 100% of the sites in
both groups had shown BOP in the
peri-implantitis site (Fig. 3). As early
as week 6, these percentiles were
already declining (65.8% and 71.4%
for the PerioC and MatrixC respec-
tively); by 6 months, more than half
of these sites had had no signs of
BOP. Yet, sites with BOP were
observed post-operatively more often
in the MatrixC (59.0%) compared
with 42.5% in the PerioC (p = 0.17,
Mixed models)
Table 1. Patients and groups’ baseline demographic data
Variable
Centre Group
Patients
(implants)
Mean age
(±SD)
Gender (F:M)
distribution
Smoking
habits
Current/
former/
Never
BMI
Mean
(±SD)
Both centres PerioC 30 (40) 57.42 ± 10.5 20:10 5/7/18 27.2 ± 4.5
Both centres MatrixC 30 (37) 60.95 ± 7.9 15:15 5/6/19 26 ± 3.5
Centre A PerioC 17 (20) 54.88 ± 12.1 12:5 2/3/12 26.9 ± 4.3
Centre A MatrixC 19 (24) 61.83 ± 7.6 9:10 2/4/13 26.0 ± 2.3
Centre B PerioC 13 (20) 60.75 ± 7.0 8:5 3/4/6 27.4 ± 4.8
Centre B MatrixC 11 (13) 59.43 ± 8.4 6:5 3/2/6 25.9 ± 5.1
MatrixC, Matrix Chip Group; PerioC, Periochip Group.
© 2012 John Wiley & Sons A/S
Protocol for the treatment of peri-implantitis 1201
Adverse effects were minimal and
generally included toothache and
gingival tenderness; all of these have
spontaneously resolved after several
days. Additional remedy or interven-
tion was not required.
Discussion
Intensive placement of chips in the
gingival pockets around implants
with peri-implantitis resulted in a
significant improvement of their
periodontal parameters as evident in
mean PD reduction of 1.59 mm.
(MatrixC) to 2.19 mm. (PerioC),
CAL gain of 1.56 mm. (MatrixC) to
2.21 mm (PerioC) and BOP reduction
of 41.0% (MatrixC) to 57.5%
(PerioC) at 6-month post-operative.
These results are much superior com-
pared with previously reported results
for non-surgical treatment for peri-
implantitis: Persson et al. (2011) have
recently published the clinical and
microbiological results of non-surgi-
cal treatment of peri-implantitis using
air abrasive or laser; PD reductions in
both groups were 0.8 and 0.9 mm
respectively. Similarly, Sahm et al.
(2011) using manual debridement or
air-abrasive device reported approxi-
mately half a millimetre pocket reduc-
tion and CAL gain in both groups.
Faggion et al. (2011) in a network
meta-analysis comparing different
treatment modalities for peri-implan-
titis have calculated an overall
weighted mean PD reduction of
0.77 mm. and CAL gain of 0.79 mm
4 months after non-surgical treat-
ment. Finally, Lindhe & Meyle (2008)
in their consensus report have there-
fore concluded that non-surgical ther-
apy in peri-implantitis is as of yet
unpredictable.
The sizeable response that was
achieved in this study was not previ-
ously reported even with the adjunc-
tive local application of antimicrobial
Table 2a. Changes in clinical parameters baseline to six months: comparison between treat-
ment
Variable
Group
Implants
(patients) ΔPD (±SE) (mm) ΔCAL (±SE) (mm.) ΔBOP (±SE) (%)
PerioC 40 (30) 2.13 ± 0.22 2.18 ± 0.22 57.5 ± 7.92
MatrixC 33 (26) 1.73 ± 0.19 1.69 ± 0.21 45.5 ± 8.8
Differences – 0.40 ± 0.31 0.48 ± 0.32 12.1 ± 6.7
p-value – 0.1780 0.1216 0.3125
PerioC, Chlorhexidine Group; MatrixC Matrix Chip Group.
5.0
Screening
Baseline
2
4
6
8
12
18
24
6.0
PD(mm)
Weeks
7.0
7.06
7.50 7.60
7.13
6.73
6.45
6.08
6.05
5.75
5.48
7.21
6.58
6.06 6.06
5.84
5.79
5.65
5.48
8.0
Matrix Chip (MtrixC) group
PerioChip (PerioC) group
Fig. 1. Probing depth exhibited continues reduction throughout the study. In the first 8 weeks, the rate of this improvement seems
greater.
Table 2b. Changes in clinical parameters baseline to 6 months (intention to treat subjects): comparison between treatment groups*
Variable
Group
Implants
(patients) ΔPD (±SE) (mm) ΔCAL (±SE) (mm) Δ%BOP ± SE
PerioChip 40 (30) 2.19 ± 0.24 2.21 ± 0.23 57.5 ± 7.92
Matrix Chip 37 (30) 1.59 ± 0.23 1.56 ± 0.25 41.0 ± 8.1
Differences – 0.59 ± 0.331 0.65 ± 0.34 17.0 ± 10.9 (1.83 odd ratio)
p-value (95% CI) – 0.07 (À0.05 to 1.24) 0.05 (À0.01 to 1.31) 0.17 (0.65–5.12)
*Model derived last square means (generalized mixed model – SAS GenMod procedure), model controlled for centre.
© 2012 John Wiley & Sons A/S
1202 Machtei et al.
agents. Sahm et al. (2011) reported
PD reduction of 0.8 mm and CAL
gain of 0.8 mm using mechanical
debridement and adjunctive subgin-
gival irrigation with CHX solution
and gel application into the pockets.
Salvi et al. (2007) using adjunctive
minocycline microspheres (Arestin®
,
Orapharma, Horsham, PA, USA)
reported similar clinical response (PD
reduction of 1.0 mm. and CAL gain
of 1.1 mm.) 1-year post-operative;
Renvert et al. (2008b) in a similar
study reported even less favour-
able results (mean PD reduction of
0.5 mm). Bu¨ chter et al. (2004) using
adjunctive doxycycline gel reported
slightly better results (PD reduction
and CAL gain of 1.15 and 1.17 mm
respectively) 4-month post-operative.
Yet, the response in this study with
the intensive use of CHX chips
(2.13 mm.) was twice as big, thus
highlighting the persistent nature of
the peri-implant infection.
Patients in the PerioC have had
greater PD reduction (2.19 mm.),
CAL gain (2.21 mm) and reduction
of BOP (57.5%) compared with the
MatrixC (1.59, 1.56 mm and 41.0%
respectively), these differences were
only statistically significant for the
CAL changes. The considerable
response in the MatrixC would tend
to suggest that matrix degradation
by itself might have exerted some
antibacterial effect. The hydrolysed
gelatin matrix (cross-linked with
Glutaraldehyde) is undergoing an
initial rapid degradation with con-
comitant slower continuous resorp-
tion for 7–10 days via collagenolytic
Table 3. Proportions of changes in probing depth greater than a threshold
Reduction number (%)
2 weeks
77 implants
4 weeks
76 implants
6 weeks
73 implants
8 weeks
73 implants
12 weeks
75 implants
18 weeks
71 implants
6 months
73 implants
MatrixC
37 implants 36 implants 35 implants 34 implants 35 implants 31 implants 33 implants
1 mm 18(49%) 26 (72%) 24 (69%) 27 (79%) 29 (83%) 25 (81%) 29 (88%)
2 mm 3 (8%) 13(36%) 11 (31%) 14 (41%) 16 (46%) 17 (55%) 19 (54%)
3 mm 1 (3%) 2 (6%) 4 (11%) 4 (12%) 4 (11%) 7 (23%) 8 (24%)
4 mm 0 0 2 (6%) 0 0 0 2 (6%)
PerioC¶,
*
40 implants 40 implants 38 implants 39 implants 40 implants 40 implants 40 implants
1 mm 23 (58%) 26 (65%) 28 (74%) 31 (79%) 31 (78%) 36 (90%) 37 (93%)
2 mm 1 (3%) 10 (25%) 18 (47%) 22 (56%) 22 (55%) 27 (68%) 28 (70%)
3 mm 0 2 (5%) 5 (13%) 5 (13%) 8 (20%) 10 (25%) 16 (40%)
4 mm 0 1 (3%) 0 2 (5%) 3 (8%) 3 (8%) 6 (15%)
*p = 0.077.
¶
p = 0.073.
Table 4. Changes in the number of chips placed baseline to 18 weeks
Baseline 18 weeks
No. used Frequency Per cent
Cumulative
frequency
Cumulative
per cent Frequency Per cent
Cumulative
frequency
Cumulative
per cent
0 0 0 0 0 43 55.84 43 55.84
1 35 45.45 35 45.45 15 19.48 58 75.32
2 25 32.47 60 77.92 15 19.48 73 94.81
3 14 18.18 74 96.10 4 5.19 77 100.00
4 3 3.90 77 100.00 0 0 77 100.00
Screening
Baseline
2
4
6
8
12
18
24
Weeks
5.0
6.0
CAL(mm)
7.0
8.0
9.0
7.58
7.64
7.06
6.61 6.60
6.32
6.24
6.13
5.94
7.78
7.88
7.35
7.03
6.71
6.28
6.28
5.95
5.70
Matrix Chip (MatrixC) group
PerioChip (PerioC) group
Fig. 2. Gain in CAL is also more rapid in the first 8 weeks; however, this improve-
ment continues for the duration of the study.
© 2012 John Wiley & Sons A/S
Protocol for the treatment of peri-implantitis 1203
activity (Soskolne et al. 1998). This
native collagenase once released
might have an antimicrobial effect
on the pathogenic flora around these
implants, thus reducing inflamma-
tion and improving peri-implant gin-
gival indices (Spitznagel & Shafer
1985, McGarry-Houghton et al.
2009). Also, such degradation is real-
izing Glutaraldehyde which is
embedded in the matrix. This latter
material is well known for its antibac-
terial properties, thus probably con-
tributing to the overall improvement
(Gorman et al. 1980, Russell 1994).
The sizeable response in the
MatrixC group might also be attrib-
uted to the overwhelming effect of
implant debridement that was per-
formed in both groups. Similarly,
Jeffcoat et al. (1998) in a periodonti-
tis treatment study reported that the
SRP+matrix chip were not signifi-
cantly different from the SRO+CHX
chips in the first 3 months. Even at
9 months, these differences, though
statistically significant, were only
0.26 mm compared with 0.59 mm in
this study. Consequently, this study
might be under power due to the
major effect of the SRP together
with the MatrixC. Also, the repeated
application protocol might be acting
to disrupt the biofilm thus exerting a
beneficial mechanical effect. Simi-
larly, Varela et al. (2011) using
repeated mechanical therapy have
reported no difference between pla-
cebo and systemic antibiotics in sites
with initial PPD and CAL ! 7 mm.
Bleeding on probing, initially
100% at baseline was completely
eliminated in 57.5% (PerioC) and
41.0% (MatrixC) of these sites at
6 months. Heitz-Mayfield et al.
(2011) in a randomized control
multi-centre study reported a some-
what lower percentile (38%). Ren-
vert et al. (2009) reported that only
15% of the sites treated with hand
instrument or ultrasonic were free of
BOP 6 months later. In contrary,
Bu¨ chter et al. (2004) reported similar
results in sites treated with doxycy-
cline (from 54% to 27% at
4 months). The relatively consider-
able proportions of sites with persis-
tent BOP even post-operatively,
further emphasize the aggressive nat-
ure of the inflammatory process in
peri-implantitis. Thus, sites with
residual BOP would require constant
monitoring and in time further ther-
apy in the unlikely event of further
attachment loss.
Of particular interest is the lack
of GR in most of these sights
(mean change of 0.04 and
À0.05 mm for the MatrixC and Pe-
rioC respectively). This observation
tends to suggest that pocket reduc-
tion resulted primarily from re-
attachment/adherence or increased
resistance to probe penetration of
the peri-implant mucosa. Similar
results were previously reported;
however, these have received limited
attention (Bu¨ chter et al. 2004, Fag-
gion et al. 2011, Sahm et al. 2011).
In comparison, the overall mean
GR reported in a meta-analysis of
non-surgical periodontal therapy for
pockets that were initially moderate
to deep was 0.5 mm. (Hung &
Douglass 2002). More recently, we
have reported (Machtei et al. 2011)
on the clinical response to a similar
intensive protocol of chlorhexidine
chips placement around teeth: Mean
PD reduction was incredibly similar
(2.09 mm) compared with that
around implants in this study
(2.13 mm); In contrary, CAL gain
in this study (2.18 mm) was much
greater than what we have achieved
around teeth (1.66 mm). This phe-
nomenon would require further
research as it may lend some clues
to the less favourable response to
therapy often reported with dental
implants (Lang & Berglundh 2011).
In conclusion, A protocol that
included an intensive programme for
placement of PerioC and MatrixC
resulted in a substantial reduction in
PD, gain in CAL and reduction in
BOP in sites with peri-implantitis.
Further studies will be required to
fully appreciate the mechanism by
which these chips reduce the peri-
implant inflammation.
Acknowledgement
The authors acknowledge Mrs. Liron
Eliezer (research coordinator, Ram-
bam HCC School of graduate den-
tistry, Haifa) for her skilful assistance
in the management of this study.
The authors also thank Dr. Arie
Laor for the statistical analysis and
advice.
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Address:
Eli E. Machtei
Department of Periodontology
School of Graduate Dentistry
Rambam Health Care Center, Haifa
Israel
E-mail: machtei@rambam.health.gov.il
Clinical Relevance
Scientific rational for the study:
Peri-implantitis is becoming an ever
growing health issue for dental
practitioners. Yet, current treatment
protocols for the treatment of this
condition are unpredictable. The
purpose of this study was to explore
the use of repeated application of
CHX chips on peri-implantitis.
Principal findings: Both treatment
groups had PD reduction > 2 mm.
and BOP reduction of approximately
50%, which was maintained at
6 months. This response is greater
that what was previously reported
with non-surgical therapy of peri-
implantitis.
Practical implications: If these find-
ings will be further substantiated in
future research, this protocol of fre-
quent chips placement together with
mechanical debridement might prove
useful in negotiating peri-implantitis.
© 2012 John Wiley & Sons A/S
Protocol for the treatment of peri-implantitis 1205

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Dental implants and periochip

  • 1. Treatment of peri-implantitis using multiple applications of chlorhexidine chips: a double-blind, randomized multi-centre clinical trial Machtei EE, Frankenthal S, Levi G, Elimelech R, Shoshani E, Rosenfeld O, Tagger-Green N, Shlomi B. Treatment of peri-implantitis using multiple applications of chlorhexidine chips: a double-blind, randomized multi-centre clinical trial. J Clin Periodontol 2012. 39: 1198–1205. doi: 10.1111/jcpe.12006. Abstract Background: Universal strategies for managing peri-implantitis are yet to be adopted. The aim of this study is to examine a protocol of intensive application of chlorhexidine containing chips in sites with peri-implantitis. Materials and Methods: This multi-centre, randomized, double-blind, parallel, two-arm clinical trial included 60 patients (77 implants) with probing depth (PD) 6–10 mm and bone loss ! 2 mm around 1–2 implants. One to two weeks follow- ing SRP, baseline measurements were made followed by implants’ debridement. Patients were randomized to receive matrix chips (MatrixC) or chlorhexidine Chips (PerioC). Measurements and chips placement were repeated at weeks 2, 4, 6, 8, 12 and 18. At 6 months, patients returned for final examination. Results: Probing depth reduction was greater in the PerioC (2.19 ± 0.24 mm) compared with MatrixC (1.59 ± 0.23 mm), p = 0.07. Seventy percentage of the implants in the PerioC and 54% in the MatrixC had PD reduction ! 2 mm. Likewise, 40% of the sites (PerioC) and 24% (MatrixC) had PD reduc- tion ! 3 mm. Clinical attachment level gains for both groups were significant; however, the changes in the PerioC group were significantly greater than in MatrixC [2.21 ± 0.23 mm. and 1.56 ± 0.25 mm respectively, p = 0.05]. Bleeding on probing was reduced by half in both groups. Conclusion: Frequent placement of PerioC and MatrixC together with implants debridement resulted in a substantial improvement in sites with peri-implantitis. Further studies will be required to fully appreciate the mechanism of this treat- ment. Eli E. Machtei1 , Shai Frankenthal1 , Guy Levi1 , Rina Elimelech1 , Eyal Shoshani2 , Olivia Rosenfeld3 , Nirit Tagger-Green3 and Benjamin Shlomi3 1 Department of Periodontology, School of Graduate Dentistry, Rambam HCC and Faculty of Medicine, Technion – Israeli Institute of Technology, Haifa, Israel; 2 Dexcel Pharma, Or-Akiva, Israel; 3 Department of Oral and Maxillofacial Surgery, Tel Aviv Sourasky Medical Center, Tel-Aviv, Israel Key words: anti-Inflammatory agents; antimicrobial agents; clinical trial; delayed- action preparations; dental implants; peri-implantitis; therapy Accepted for publication 11 August 2012 Peri-implantitis is rapidly becoming a major oral disease entity that is frequently encountered in the dental office. With approximately ten mil- lion new implants placed annually worldwide (Markets for Dental Conflict of interest and source of funding statement This study was supported by a research grant from Dexcel Pharma, Or-Akiva, Israel. The authors declare no conflict of interest except for Mr. Eyal Shoshani who was on the R&D team of Dexcel Pharma at the time of the study. Prof. Eli E. Machtei also served as a consultant for Dexcel Pharma. © 2012 John Wiley & Sons A/S1198 J Clin Periodontol 2012; 39: 1198–1205 doi: 10.1111/jcpe.12006
  • 2. Implants and Final Abutments 2009), and tens of millions of implants that are currently function- ing, the magnitude of this problem is ever growing. In their systematic review, Zitz- mann & Berglundh (2008) have reported that 50% of the implants and 80% of the patients had mucosi- tis, while peri-implantitis was reported in 12–43% of the implants and 28–56% of the patients. Conversely, Jung et al. (2008) in a systematic review and meta-analysis on the 5 years survival and complica- tions of dental implants supporting single crowns reported lower frequen- cies of peri-implantitis (~ 10%). These differences in the reported prevalence might be associated with the threshold used to define disease. Koldsland et al. (2010) studied 164 subjects treated with dental implants and followed for over 8 years; he was able to show that depending on the different clinical and radiographic threshold that was used, disease prev- alence varied considerably between 11.3% and 47.1%. Another possible variable that might affect the preva- lence of peri-implantitis is patient’s periodontal status. Roccuzzo et al. (2012) reported their results of a 10-year prospective cohort study on implants in periodontally healthy and compromised patients treated with scaling and root planing (SRP): 10.7% of the implants in the peri- odontally healthy cases required some kind of adjunctive (surgical or non-surgical) treatment through these years compared with 15.9% and 27.2% for patients with initial diag- nosis of moderate and severe chronic periodontitis. Similar findings were recently reported by Cho-Yan Lee et al. (2012). Optimal treatment strategies for the treatment of peri-implantitis are yet to be commonly agreed upon. Renvert et al. (2008a) in a literature review have reported that non-surgi- cal therapy was not found to be effective in these lesions. These authors, in a subsequent double- blind study (2009) of debridement of dental implants affected by peri- implantitis, using hand and ultra- sonic instruments, have reported only minimal (0.2 mm.) and statisti- cally insignificant change in probing depth (PD) 6-month post-operative for both treatment groups. Like- wise, Lindhe & Meyle (2008) on behalf of the European workshop on Periodontology have concluded that non-surgical mechanical therapy causes the reduction of inflamma- tion as evident in the decrease in bleeding on probing (BOP); how- ever, the overall improvement in clinical parameters is at best unpre- dictable. Furthermore, Tonetti & Palmer (2012) on behalf of the 8th European workshop on Periodontol- ogy referred to the relatively small number of well-designed randomized clinical trials in implant dentistry as an impairment for our progress in this field. To further improve treatment outcome, several adjunctive treat- ment modalities were employed. Renvert et al. (2011) reported similar and only modest improvement in PD, when using air abrasive or Er: YAG laser therapy in patients with peri-implantitis. Sahm et al. (2011) reported that 6 months after treat- ment of peri-implantitis with either air abrasive of mechanical cleaning and subgingival application of chlorhexidine solution and gel, mean pocket reduction and clinical attach- ment level (CAL) gain were both approximately 0.5 mm, which was similar in both groups. The use of local delivery of minocycline to enhance treatment response in these cases was reported by Salvi et al. (2007). Despite some pocket reduc- tion, six patients (25% of the entire study population) were removed from the study as the implants were either explanted or required addi- tional therapy due to ! 2 mm. increase in PD during the observa- tion period. Similarly, Bu¨ chter et al. (2004) have utilized doxycyline gel for the treatment of peri-implan- titis. PD reduction and CAL gain were greater (0.6 mm) in sites with the adjunctive treatment com- pared with subgingival debridement only. Recently (Machtei et al. 2011), we have been able to demonstrate that frequent application of biode- gradable matrix containing chlorhex- idine (PerioChip® ; Dexcel Pharma, Or-Akiva, Israel) in patients with chronic periodontitis with PD ! 5 mm resulted in a sizeable improvement in mean PD (2.1 mm) and gain in CAL (1.7 mm). Several in vitro investigations have demonstrated that chlorhexidine (CHX) is adsorbed to the oxide layer of titanium surfaces. Recent data indicate that the type of oxide may influence the amount of CHX absorbed (Morra et al. 2004, Barbour et al. 2009). It has also been shown that the absorption kinetics is directly related to implants’ surface roughness and was also positively correlated with the concentration of the CHX solution. A desorption occurs within 24 hours and inhibits bacterial growth (Kozlovsky et al. 2006). Therefore, the aim of this study is to examine a novel protocol of intensive application of chlorhexi- dine chips on peri-implant health in sites with peri-implantitis. Materials and Methods This study was designed as a multi- centre, randomized, double-blind, parallel, two-arm clinical trial. The study was initially approved by the institutional ethic committees (IECs) of both medical centres and posted on the NIH website. Patients seeking treatment for peri-implant disease at either Ram- bam health care campus in Haifa or at the Sourasky Medical Center in Tel-Aviv were initially screened for this study (with first patient in 17.3.2010 and last patient out 27.10.2011). Inclusion criteria Patients 21 years or older with peri- implantitis characterized by the pres- ence of at least one implant with PD of 6–10 mm in depth (potential target implant), with BOP and radiographic evidence of bone loss. Patients were required to read and if satisfied with it, sign a written consent form that was previously approved by the IECs. Also, patients needed to affirm their availability for the 6-month duration of the study. At screening, all patients had a periodontal examination and when necessary periodontal treatment for the existing teeth was rendered first and the study commencement was postponed. Exclusion criteria (i) History of allergy to CHX or regular use of it (ii) horizontal © 2012 John Wiley & Sons A/S Protocol for the treatment of peri-implantitis 1199
  • 3. inter-implant distance <2 mm (if an adjacent implant existed); (iii) Tita- nium Plasma-sprayed or hydroxylap- atite coated implants; (iv) systemic conditions that might affect inflam- mation and bleeding; (v) Any local irritation that could not be negoti- ated (i.e. orthodontic appliances; ill- fitted restorations; apical pathology); (vi) systemic antibiotic therapy or periodontal/mechanical/local delivery therapy within 6 weeks prior to study entry and throughout the study duration; (vii) continuous use of non-steroidal anti-inflammatory drugs or drugs known to cause gin- gival overgrowth; (viii) pregnancy or intention to become pregnant in the next 6 months. At Screening visit (Week 1), patients came to establish eligibility. At this time, the following informa- tion was recorded: Demographic data and smoking habits, relevant past medical history and concomi- tant diseases and medications (mea- surements were performed by a periodontist or oral surgeon). Oral examination was performed and the following parameters were recorded: plaque index, gingival index and BOP. In addition, the fol- lowing site measurements were per- formed for the target implants using a manual 15 mm. University of North Carolina probe (Hu-Friedy, Chicago, IL, USA): BOP using a dichotomized 0/1 scale; PD, gingival recession (GR) measured from the crown/restoration margins. CAL was calculated as the sum of PD+GR. Periapical radiographs were further used to confirm bone loss ( ! 2 mm) and screen for any exclusion condi- tions. Each qualified patient then underwent supragingival scaling of all the teeth and implants (if not done in the 6 weeks prior the Screening visit) using ultrasonic instruments (OEM; Electeo Medical System, Nyon, Switzerland) with standard periodontal tips (performed by a well experienced dental hygien- ists). Following oral hygiene instruc- tion, patients were given a sodium fluoride toothpaste (Colgate cavity protection; Colgate–Palmolive, NJ, USA) and soft toothbrush to be used throughout the study. One to two weeks later, patients were invited to return for the baseline visit (week 0), at which time final eligibil- ity was determined. Periodontal assessments and measurements were repeated for all potential target implants. For each patient, at least one and no more than two implants (if available) with PD 6–10 mm were selected. In cases where more than two eligible implants were present, the following selection grid was employed: implants with the deepest pocket/s (primary); different arch (secondary); furthest away from each other (tertiary). Next, surface debridement was performed for the chosen target implant/s and the two adjacent teeth using ultrasonic instruments. Randomization, allocation concealment and blinding Patients were then randomized to receive either a biodegradable cross- linked gelatin matrix chip (matrix chip group, MatrixC) or matrix con- taining 2.5-mg chlorhexidine-gluco- nate chips (PerioC; Dexcel Pharma). Eligible patients at baseline visit were assigned a randomization number starting from 601. Each randomiza- tion number was randomly assigned to one of the two letters A or B; each letter assigned randomly to one of the two treatments MatrixC or PerioC. Randomization was performed using a computer-generated sequence of Random binomial numbers by SAS 9.2 RANBIN CALL. The blinding of the study could only be broken upon completion of the clinical phase of the study including adverse effects (AE) and database queries all being resolved. One set of sealed envelopes was provided to the investigator con- taining individual randomization codes which was kept at the investiga- tional site in case of a severe adverse effect (SAE); however, none have occu-rred. To ensure examiner’s blindness, two separate investigators attended to each patient: one that placed the chips and another one making the clinical measurements. Also, the chips were identical in size, shape and col- our so that even the examiner that placed them was unaware of the iden- tity of the chips that were placed. Upto four chips were inserted for each implant’s sites which PD was 6–10, and patients were discharged with instruction to refrain from using toothpicks and other proximal hygiene aids for 10 days. To ensure blindness, chips were inserted by a different investigator than that per- forming the clinical measurements. Patients were also asked to notify the investigator of any adverse reac- tion. At each visit, they were also actively approached to inquire of any adverse reaction that they might have failed to report. Patients returned at weeks 2, 4, 6, 8, 12 and 18 and clinical measure- ments were repeated. For target sites with PD still ! 6 mm new chips were re-inserted. At 12 weeks, supra- gingival debridement was also per- formed. At each of these visits, patients were asked to report of any AE that they might have encoun- tered and this was recorded. In cases where the target pockets depths increased during the study in more than 2 mm (confirmed on a subse- quent visit), the patient was with- drawn from the study and referred for surgical therapy. At 6 months, patients returned for the final clinical examination and determination of any further treatment needs. Statistical analysis Power calculation was initially per- formed to determine sample size. Assuming normal distribution, nomi- nal power of 80%, a 0.05, a stan- dard deviation of the difference between treatments of 1.18 mm (based on previous study), we need 28 volunteers in each treatment group (using Two sample t-test for mean difference) to achieve a mean difference between treatments of À0.9 mm (SAS 9.2 POWER PRO- CEDURE, SAS Institute, Cary, NC, USA). Thus, we chose to allocate 30 volunteers to each study treatment. The statistical procedure used was SAS procedure GENMODE. The modelization method: General- ized mixed linear model with gener- alized estimating equations method for repeated measures. This method was used for linear models (ΔPPD, CAL) and for binary models (ΔBOP, success to achieve 1,2,3,4 mm PPD reduction) with different links and distribution functions for each variable. Continuous variables were analy- sed and compared using t-test when appropriate. Discrete variables were compared using two-sided fisher’s © 2012 John Wiley & Sons A/S 1200 Machtei et al.
  • 4. exact test. PD reduction, baseline to 6 months served as the primary out- come variable. Secondary outcome variables included changes in CAL, GR, BOP and PD at weeks 2, 4, 6, 8, 12 and 18. Change in PD and CAL was modelled using a linear- mixed model (SAS 9.2 Mixed Proce- dure) with treatment, and centre as fixed factors. Patient and pocket were entered as random effects. Analysis was done for subjects that completed the study and again for all patients that were enrolled [inten- tion to treat (ITT)] subjects, with data missing being complemented using last observation carried forward (LOCF) method. Contrasts with 95% confidence intervals for the difference or ratio between the changes were computed. Analysis for the number of pock- ets with at least 1/2/3/4 mm reduc- tion in PD, and analysis for BOP for the target implant/s measured at each visit were analysed by a Coch- ran–Mantel–Haenszel (CMH) test. All treatment comparisons were two-sided at the 0.05 level of signifi- cance. Similar mixed model with a binary distribution and Logit link was used for BOP changes during the trial. Similar mixed models for PD and CAL with time as a fixed repeated covariate were used to reveal the changes over time of these parameters. Results Sixty patients, 35 females and 25 males, age 27–77 years (mean ± SD 59.18 ± 9.2) with a total of 77 den- tal implants were initially accepted into the study. Thirty-six patients (44 implants) were in Centre A and 24 patients (33 implants) in Centre B (Table 1). Thirty patients with 40 implants were randomly assigned into the chlorhexidine group (Pe- rioC), whereas an equal numbers of patients with 37 implants were included in the matrix chip group (MatrixC). Of the original 60 patients that were enrolled, 56 patients (93.3%) were available and eligible for the final examination 6 months later (the corresponding implant level retention rate was 94.8%, 73/77). Four patients, all from the MatrixC were exited from the study. One required extended antibiotic use (non-related to the study), one had total hip replace- ment and could not come for the follow-up and the other two were withdrawn, due to emergency dental treatment which interfered with the study endpoints. Five patients in each group were current smokers, whereas the rest were former smokers or never smoked. Both groups and both cen- tres were similar in their baseline demographic and smoking habits. Baseline PDs (7.60 and 7.21 mm for the PerioC and MatrixC groups respectively) have shown continuous improvement throughout the study (Fig. 1). Greater reduction was noticeable in the first 8 weeks with continuous improvement, although at slower rate thereafter. Mean pocket depth at 6 months were 5.47 and 5.48 mm PerioC and MatrixC respectively, which were significantly different from baseline (p = 0.0001). PD improvement in the PerioC (2.13 mm.) was greater than that for the MatrixC (1.73 mm.), p = 0.17 (Table 2a). When data were analysed with LOCF, these changes (2.19 and 1.59 mm respec- tively, Table 2b) were borderline significant (p = 0.07, mixed model). Probing depth reduction was further dichotomized into sites with PD reduction that was equal to/or greater than a threshold (Table 3). At 6 months, 93% of the implants in the PerioC and 88% in the Ma- trixC achieved at least 1-mm pocket reduction. For pocket reduction ! 2 mm, 70% of the sites in the PerioC and 54% in the MatrixC reached this threshold (p = 0.077). Likewise, 40% of the sites in the PerioC and 24% of the sites in the MatrixC have had pocket reduction that was equal to or greater than 3 mm (p = 0.073). Chips were inserted until PD was reduced to 5mm. To this end, 11 of the 40 implants in the PerioC (28%) and 5 of the 33 implants (15%) in the MatrixC group reached this goal at 6 months. At baseline, 60 implants (78%) required one or two chips, whereas three implants required four chips each. At the last treat- ment visit, 43 implants (56%) did not require any chip placement, 30 required 1–2 chips (Table 4). Both treatment modalities have shown significant improvement in CAL (Fig. 2). Sites in the PerioC had a mean baseline CAL of 7.88 ± 0.2 mm (SE) with an ultimate 6 months CAL level of 5.70 ± 0.3 mm (p = 0.001, mixed model). Similarly, Sites in the MatrixC had a mean base- line CAL of 7.63 ± 0.3 mm (SE) with a final 6 months CAL level of 5.94 ± 0.3 mm (p = 0.001, mixed model). These differences in CAL gain amounted to 2.18 mm in the PerioC and 1.69 mm in the MatrixC (p = 0.12, mixed model), while when using all IIT patients, CAL gain (2.21 and 1.56 mm respectively) were sig- nificantly different (p = 0.05, mixed model). At baseline, 100% of the sites in both groups had shown BOP in the peri-implantitis site (Fig. 3). As early as week 6, these percentiles were already declining (65.8% and 71.4% for the PerioC and MatrixC respec- tively); by 6 months, more than half of these sites had had no signs of BOP. Yet, sites with BOP were observed post-operatively more often in the MatrixC (59.0%) compared with 42.5% in the PerioC (p = 0.17, Mixed models) Table 1. Patients and groups’ baseline demographic data Variable Centre Group Patients (implants) Mean age (±SD) Gender (F:M) distribution Smoking habits Current/ former/ Never BMI Mean (±SD) Both centres PerioC 30 (40) 57.42 ± 10.5 20:10 5/7/18 27.2 ± 4.5 Both centres MatrixC 30 (37) 60.95 ± 7.9 15:15 5/6/19 26 ± 3.5 Centre A PerioC 17 (20) 54.88 ± 12.1 12:5 2/3/12 26.9 ± 4.3 Centre A MatrixC 19 (24) 61.83 ± 7.6 9:10 2/4/13 26.0 ± 2.3 Centre B PerioC 13 (20) 60.75 ± 7.0 8:5 3/4/6 27.4 ± 4.8 Centre B MatrixC 11 (13) 59.43 ± 8.4 6:5 3/2/6 25.9 ± 5.1 MatrixC, Matrix Chip Group; PerioC, Periochip Group. © 2012 John Wiley & Sons A/S Protocol for the treatment of peri-implantitis 1201
  • 5. Adverse effects were minimal and generally included toothache and gingival tenderness; all of these have spontaneously resolved after several days. Additional remedy or interven- tion was not required. Discussion Intensive placement of chips in the gingival pockets around implants with peri-implantitis resulted in a significant improvement of their periodontal parameters as evident in mean PD reduction of 1.59 mm. (MatrixC) to 2.19 mm. (PerioC), CAL gain of 1.56 mm. (MatrixC) to 2.21 mm (PerioC) and BOP reduction of 41.0% (MatrixC) to 57.5% (PerioC) at 6-month post-operative. These results are much superior com- pared with previously reported results for non-surgical treatment for peri- implantitis: Persson et al. (2011) have recently published the clinical and microbiological results of non-surgi- cal treatment of peri-implantitis using air abrasive or laser; PD reductions in both groups were 0.8 and 0.9 mm respectively. Similarly, Sahm et al. (2011) using manual debridement or air-abrasive device reported approxi- mately half a millimetre pocket reduc- tion and CAL gain in both groups. Faggion et al. (2011) in a network meta-analysis comparing different treatment modalities for peri-implan- titis have calculated an overall weighted mean PD reduction of 0.77 mm. and CAL gain of 0.79 mm 4 months after non-surgical treat- ment. Finally, Lindhe & Meyle (2008) in their consensus report have there- fore concluded that non-surgical ther- apy in peri-implantitis is as of yet unpredictable. The sizeable response that was achieved in this study was not previ- ously reported even with the adjunc- tive local application of antimicrobial Table 2a. Changes in clinical parameters baseline to six months: comparison between treat- ment Variable Group Implants (patients) ΔPD (±SE) (mm) ΔCAL (±SE) (mm.) ΔBOP (±SE) (%) PerioC 40 (30) 2.13 ± 0.22 2.18 ± 0.22 57.5 ± 7.92 MatrixC 33 (26) 1.73 ± 0.19 1.69 ± 0.21 45.5 ± 8.8 Differences – 0.40 ± 0.31 0.48 ± 0.32 12.1 ± 6.7 p-value – 0.1780 0.1216 0.3125 PerioC, Chlorhexidine Group; MatrixC Matrix Chip Group. 5.0 Screening Baseline 2 4 6 8 12 18 24 6.0 PD(mm) Weeks 7.0 7.06 7.50 7.60 7.13 6.73 6.45 6.08 6.05 5.75 5.48 7.21 6.58 6.06 6.06 5.84 5.79 5.65 5.48 8.0 Matrix Chip (MtrixC) group PerioChip (PerioC) group Fig. 1. Probing depth exhibited continues reduction throughout the study. In the first 8 weeks, the rate of this improvement seems greater. Table 2b. Changes in clinical parameters baseline to 6 months (intention to treat subjects): comparison between treatment groups* Variable Group Implants (patients) ΔPD (±SE) (mm) ΔCAL (±SE) (mm) Δ%BOP ± SE PerioChip 40 (30) 2.19 ± 0.24 2.21 ± 0.23 57.5 ± 7.92 Matrix Chip 37 (30) 1.59 ± 0.23 1.56 ± 0.25 41.0 ± 8.1 Differences – 0.59 ± 0.331 0.65 ± 0.34 17.0 ± 10.9 (1.83 odd ratio) p-value (95% CI) – 0.07 (À0.05 to 1.24) 0.05 (À0.01 to 1.31) 0.17 (0.65–5.12) *Model derived last square means (generalized mixed model – SAS GenMod procedure), model controlled for centre. © 2012 John Wiley & Sons A/S 1202 Machtei et al.
  • 6. agents. Sahm et al. (2011) reported PD reduction of 0.8 mm and CAL gain of 0.8 mm using mechanical debridement and adjunctive subgin- gival irrigation with CHX solution and gel application into the pockets. Salvi et al. (2007) using adjunctive minocycline microspheres (Arestin® , Orapharma, Horsham, PA, USA) reported similar clinical response (PD reduction of 1.0 mm. and CAL gain of 1.1 mm.) 1-year post-operative; Renvert et al. (2008b) in a similar study reported even less favour- able results (mean PD reduction of 0.5 mm). Bu¨ chter et al. (2004) using adjunctive doxycycline gel reported slightly better results (PD reduction and CAL gain of 1.15 and 1.17 mm respectively) 4-month post-operative. Yet, the response in this study with the intensive use of CHX chips (2.13 mm.) was twice as big, thus highlighting the persistent nature of the peri-implant infection. Patients in the PerioC have had greater PD reduction (2.19 mm.), CAL gain (2.21 mm) and reduction of BOP (57.5%) compared with the MatrixC (1.59, 1.56 mm and 41.0% respectively), these differences were only statistically significant for the CAL changes. The considerable response in the MatrixC would tend to suggest that matrix degradation by itself might have exerted some antibacterial effect. The hydrolysed gelatin matrix (cross-linked with Glutaraldehyde) is undergoing an initial rapid degradation with con- comitant slower continuous resorp- tion for 7–10 days via collagenolytic Table 3. Proportions of changes in probing depth greater than a threshold Reduction number (%) 2 weeks 77 implants 4 weeks 76 implants 6 weeks 73 implants 8 weeks 73 implants 12 weeks 75 implants 18 weeks 71 implants 6 months 73 implants MatrixC 37 implants 36 implants 35 implants 34 implants 35 implants 31 implants 33 implants 1 mm 18(49%) 26 (72%) 24 (69%) 27 (79%) 29 (83%) 25 (81%) 29 (88%) 2 mm 3 (8%) 13(36%) 11 (31%) 14 (41%) 16 (46%) 17 (55%) 19 (54%) 3 mm 1 (3%) 2 (6%) 4 (11%) 4 (12%) 4 (11%) 7 (23%) 8 (24%) 4 mm 0 0 2 (6%) 0 0 0 2 (6%) PerioC¶, * 40 implants 40 implants 38 implants 39 implants 40 implants 40 implants 40 implants 1 mm 23 (58%) 26 (65%) 28 (74%) 31 (79%) 31 (78%) 36 (90%) 37 (93%) 2 mm 1 (3%) 10 (25%) 18 (47%) 22 (56%) 22 (55%) 27 (68%) 28 (70%) 3 mm 0 2 (5%) 5 (13%) 5 (13%) 8 (20%) 10 (25%) 16 (40%) 4 mm 0 1 (3%) 0 2 (5%) 3 (8%) 3 (8%) 6 (15%) *p = 0.077. ¶ p = 0.073. Table 4. Changes in the number of chips placed baseline to 18 weeks Baseline 18 weeks No. used Frequency Per cent Cumulative frequency Cumulative per cent Frequency Per cent Cumulative frequency Cumulative per cent 0 0 0 0 0 43 55.84 43 55.84 1 35 45.45 35 45.45 15 19.48 58 75.32 2 25 32.47 60 77.92 15 19.48 73 94.81 3 14 18.18 74 96.10 4 5.19 77 100.00 4 3 3.90 77 100.00 0 0 77 100.00 Screening Baseline 2 4 6 8 12 18 24 Weeks 5.0 6.0 CAL(mm) 7.0 8.0 9.0 7.58 7.64 7.06 6.61 6.60 6.32 6.24 6.13 5.94 7.78 7.88 7.35 7.03 6.71 6.28 6.28 5.95 5.70 Matrix Chip (MatrixC) group PerioChip (PerioC) group Fig. 2. Gain in CAL is also more rapid in the first 8 weeks; however, this improve- ment continues for the duration of the study. © 2012 John Wiley & Sons A/S Protocol for the treatment of peri-implantitis 1203
  • 7. activity (Soskolne et al. 1998). This native collagenase once released might have an antimicrobial effect on the pathogenic flora around these implants, thus reducing inflamma- tion and improving peri-implant gin- gival indices (Spitznagel & Shafer 1985, McGarry-Houghton et al. 2009). Also, such degradation is real- izing Glutaraldehyde which is embedded in the matrix. This latter material is well known for its antibac- terial properties, thus probably con- tributing to the overall improvement (Gorman et al. 1980, Russell 1994). The sizeable response in the MatrixC group might also be attrib- uted to the overwhelming effect of implant debridement that was per- formed in both groups. Similarly, Jeffcoat et al. (1998) in a periodonti- tis treatment study reported that the SRP+matrix chip were not signifi- cantly different from the SRO+CHX chips in the first 3 months. Even at 9 months, these differences, though statistically significant, were only 0.26 mm compared with 0.59 mm in this study. Consequently, this study might be under power due to the major effect of the SRP together with the MatrixC. Also, the repeated application protocol might be acting to disrupt the biofilm thus exerting a beneficial mechanical effect. Simi- larly, Varela et al. (2011) using repeated mechanical therapy have reported no difference between pla- cebo and systemic antibiotics in sites with initial PPD and CAL ! 7 mm. Bleeding on probing, initially 100% at baseline was completely eliminated in 57.5% (PerioC) and 41.0% (MatrixC) of these sites at 6 months. Heitz-Mayfield et al. (2011) in a randomized control multi-centre study reported a some- what lower percentile (38%). Ren- vert et al. (2009) reported that only 15% of the sites treated with hand instrument or ultrasonic were free of BOP 6 months later. In contrary, Bu¨ chter et al. (2004) reported similar results in sites treated with doxycy- cline (from 54% to 27% at 4 months). The relatively consider- able proportions of sites with persis- tent BOP even post-operatively, further emphasize the aggressive nat- ure of the inflammatory process in peri-implantitis. Thus, sites with residual BOP would require constant monitoring and in time further ther- apy in the unlikely event of further attachment loss. Of particular interest is the lack of GR in most of these sights (mean change of 0.04 and À0.05 mm for the MatrixC and Pe- rioC respectively). This observation tends to suggest that pocket reduc- tion resulted primarily from re- attachment/adherence or increased resistance to probe penetration of the peri-implant mucosa. Similar results were previously reported; however, these have received limited attention (Bu¨ chter et al. 2004, Fag- gion et al. 2011, Sahm et al. 2011). In comparison, the overall mean GR reported in a meta-analysis of non-surgical periodontal therapy for pockets that were initially moderate to deep was 0.5 mm. (Hung & Douglass 2002). More recently, we have reported (Machtei et al. 2011) on the clinical response to a similar intensive protocol of chlorhexidine chips placement around teeth: Mean PD reduction was incredibly similar (2.09 mm) compared with that around implants in this study (2.13 mm); In contrary, CAL gain in this study (2.18 mm) was much greater than what we have achieved around teeth (1.66 mm). This phe- nomenon would require further research as it may lend some clues to the less favourable response to therapy often reported with dental implants (Lang & Berglundh 2011). In conclusion, A protocol that included an intensive programme for placement of PerioC and MatrixC resulted in a substantial reduction in PD, gain in CAL and reduction in BOP in sites with peri-implantitis. Further studies will be required to fully appreciate the mechanism by which these chips reduce the peri- implant inflammation. Acknowledgement The authors acknowledge Mrs. Liron Eliezer (research coordinator, Ram- bam HCC School of graduate den- tistry, Haifa) for her skilful assistance in the management of this study. The authors also thank Dr. Arie Laor for the statistical analysis and advice. References Barbour, M. E., Gandhi, N., el-Turki, A., O’Sulli- van, D. J. & Jagger, D. C. (2009) Differential adhesion of Streptococcus gordonii to anatase and rutile titanium dioxide surfaces with and without functionalization with chlorhexidine. Journal of Biomedical Material Research A 90, 993–998. Bu¨ chter, A., Meyer, U., Kruse-Lo¨ sler, B., Joos, U. & Kleinheinz, J. (2004) Sustained release of doxycycline for the treatment of peri-im- plantitis: randomized controlled trial. British Journal of Oral and Maxillofacial Surgery 42, 439–444. Cho-Yan Lee, J., Mattheos, N., Nixon, K. C. & Ivanovski, S. (2012) Residual periodontal pock- ets are a risk indicator for peri-implantitis in patients treated for periodontitis. Clinical Oral Implants Research 23, 325–333. Faggion, C. M. Jr, Chambrone, L., Listl, S. & Tu, Y. K. (2011) Network meta-analysis for evalu- ating interventions in implant dentistry: the case of peri-implantitis treatment. Clinical Implant Dentistry ant Related Research, doi: 10.1111/ j.1708-8208.2011.00384.x. Gorman, S. P., Scott, E. M. & Russell, A. D. (1980) Antimicrobial activity, uses and mecha- nism of action of glutaraldehyde. Journal of Applied Bacteriology 48, 161–190. Heitz-Mayfield, L. J., Salvi, G. E., Botticelli, D., Mombelli, A., Faddy, M. & Lang, N. P. (2011) Anti-infective treatment of peri-implant muco- 0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100% Screening Baseline 2 4 6 8 12 18 24 %SiteswithBOP Weeks MatrixC PerioC 54.5 41.0 Fig. 3. At baseline, 100% of the sites with peri-implantitis exhibited BOP. As early as 4 weeks into the treatment, 25% of these sites ceased to bleed; at the conclusion of the study, less than 50% of these sites had BOP. © 2012 John Wiley & Sons A/S 1204 Machtei et al.
  • 8. sitis: a randomised controlled clinical trial. Clinical Oral Implants Research 22, 237–241. Hung, H. C. & Douglass, C. W. (2002) Meta-anal- ysis of the effect of scaling and root planing, surgical treatment and antibiotic therapies on periodontal probing depth and attachment loss. Journal of Clinical Periodontology 29, 975–986. Jeffcoat, M. K., Bray, K. S., Ciancio, S. G., Den- tino, A. R., Fine, D. H., Gordon, J. M., Gun- solley, J. C., Killoy, W. J., Lowenguth, R. A., Magnusson, N. I., Offenbacher, S., Palcanis, K. G., Proskin, H. M., Finkelman, R. D. & Flashner, M. (1998) Adjunctive use of a sub- gingival controlled-release chlorhexidine chip reduces probing depth and improves attach- ment level compared with scaling and root planing alone. Journal of Periodontology 69, 989–997. Jung, R. E., Pjetursson, B. E., Glauser, R., Zembic, A., Zwahlen, M. & Lang, N. P. (2008) A system- atic review of the 5-year survival and complica- tion rates of implant-supported single crowns. 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(2011) Multiple applications of flurbiprofen and chlorhexidine chips in patients with chronic periodontitis: a randomized, double blind, parallel, 2-arms clin- ical trial. Journal of Clinical Periodontology 38, 1037–1143. Markets for Dental Implants and Final Abut- ments (2009). iDada Research Inc., Vancouver, B.C., Canada. (www.idataresearch.net/idata/ reports_view.php?SubCategoryID=58&Cate- goryId=36) McGarry-Houghton, A., Hartzell, W. O., Robbins, C. S., . Gomis-Ru¨ th, X. & Shapiro, S. D. (2009) Macrophage elastase kills bacteria within mur- ine macrophages. Nature 460, 637–641. Morra, M., Cassinelli, C., Cascardo, G., Carpi, A., Fini, M., Giavaresi, G. & Giardino, R. (2004) Adsorption of cationic antibacterial on collagen-coated titanium implant devices. Bio- medical Pharmacotherapy 58, 418–422. Persson, G. R., Roos-Jansa˚ ker, A. M., Lindahl, C. & Renvert, S. 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(2009) Mechanical non-surgical treatment of peri-implantitis: a double-blind randomized longitudinal clinical study. I: clini- cal results. Journal of Clinical Periodontology 36, 604–609. Roccuzzo, M., Bonino, F., Aglietta, M. & Dalm- asso, P. (2012) Ten-year results of a three arms prospective cohort study on implants in peri- odontally compromised patients. Part 2: clini- cal results. Clinical Oral Implants Research 23, 389–395. Russell, A. D. (1994) Glutaraldehyde: current sta- tus and uses. Infection Control and Hospital Epidemiology 15, 724–733. Sahm, N., Becker, J., Santel, T. & Schwarz, F. (2011) Non-surgical treatment of peri-implantitis using an air-abrasive device or mechanical debridement and local application of chlorhexi- dine: a prospective, randomized, controlled clini- cal study. Journal of Clinical Periodontology 38, 872–878. Salvi, G. E., Persson, G. R., Heitz-Mayfield, L. J., Frei, M. & Lang, N. P. (2007) Adjunctive local antibiotic therapy in the treatment of peri-implantitis II: clinical and radiographic outcomes. Clinical Oral Implants Research 18, 281–285. Soskolne, W. A., Chajek, T., Flashner, M., Landau, I., Stabholtz, A., Kolatch, B. & Ler- ner, E. I. (1998) An in vivo study of the chlorh- exidine release profile of the PerioChip in the gingival crevicular fluid, plasma and urine. Journal of Clinical Periodontology 25, 1017– 1021. Spitznagel, J. K. & Shafer, W. M. (1985) Neutro- phil killing of bacteria by oxygen-independent mechanisms: a historical summary. Review of Infectious Disease 7, 398–403. Tonetti, M. & Palmer, R. (2012) Clinical research in implant dentistry: study design, reporting and outcome measurements: consensus report of Working Group 2 of the VIII European Workshop on Periodontology. Journal of Clini- cal Periodontology 39(Suppl. 12), 73–80. Varela, V. M., Heller, D., Silva-Senem, M. X., Torres, M. C., Colombo, A. P. & Feres-Filho, E. J. (2011) Systemic antimicrobials adjunctive to a repeated mechanical and antiseptic therapy for aggressive periodontitis: a 6-month ran- domized controlled trial. Journal of Periodon- tology 82, 1121–1130. Zitzmann, N. U. & Berglundh, T. (2008) Defini- tion and prevalence of peri-implant diseases. Journal of Clinical Periodontology 35(Suppl. 8), 286–291. Address: Eli E. Machtei Department of Periodontology School of Graduate Dentistry Rambam Health Care Center, Haifa Israel E-mail: machtei@rambam.health.gov.il Clinical Relevance Scientific rational for the study: Peri-implantitis is becoming an ever growing health issue for dental practitioners. Yet, current treatment protocols for the treatment of this condition are unpredictable. The purpose of this study was to explore the use of repeated application of CHX chips on peri-implantitis. Principal findings: Both treatment groups had PD reduction > 2 mm. and BOP reduction of approximately 50%, which was maintained at 6 months. This response is greater that what was previously reported with non-surgical therapy of peri- implantitis. Practical implications: If these find- ings will be further substantiated in future research, this protocol of fre- quent chips placement together with mechanical debridement might prove useful in negotiating peri-implantitis. © 2012 John Wiley & Sons A/S Protocol for the treatment of peri-implantitis 1205