J Clin Periodontol 2015; 42 (Suppl. 16): S202S213 doi: 10.1111/jcpe.

12349

Efficacy of professionally
administered plaque removal with
or without adjunctive measures
for the treatment of peri-implant
mucositis. A systematic review
and meta-analysis

Frank Schwarz1, Kathrin Becker1 and

Martin Sager2
1

Department of Oral Surgery, Heinrich Heine

sseldorf, Germany; 2Animal
University, Du
Research Institute, Heinrich Heine University,
sseldorf, Germany
Du

Schwarz F, Becker K, Sager M. Efficacy of professionally administered plaque

removal with or without adjunctive measures for the treatment of peri-implant
mucositis. A systematic review and meta-analysis. J Clin Periodontol; 2015; 42
(Suppl. 16): S202S213. doi: 10.1111/jcpe.12349.

Abstract
Focused Question: In patients with peri-implant mucositis, what is the efficacy of
professionally administered plaque removal (PAPR) with adjunctive measures on
changing signs of inflammation compared with PARP alone?
Materials and Methods: After electronic database and hand search, 19 full-text
articles were independently screened by two reviewers. Finally, a total of seven
studies fulfilled the inclusion criteria. The weighted mean difference (WMD) in
bleeding on probing- (BOP) (primary outcome), gingival index- (GI) and probing
pocket depth- (PD) reductions was estimated (random effect model).
Results: WMD in BOP reduction between test and control groups amounted to
8.16% [SD = 4.61; p = 0.07; 95% CI ( 17.20, 0.88)] not favouring adjunctive
antiseptic or antibiotic (local, systemic) therapy over PAPR alone. WMD in GI
and PD reductions amounted to 0.12 [SD = 0.13; p = 0.34; 95% CI ( 0.38,
0.13)] and 0.056 mm [SD = 0.10; p = 0.60; 95% CI ( 0.27, 0.16)] not favouring
adjunctive (antiseptics, systemic antibiotics, air abrasive device) over control measures respectively. Most studies evaluated reported on residual BOP and GI
scores after therapy.
Conclusions: Adjunctive therapy may not improve the efficacy of PAPR in reducing BOP, GI and PD scores at mucositis sites. Despite clinically important
improvements, a complete disease resolution may not be expected by any of the
treatment protocols investigated.

Conflict of interest and source of funding

The authors declare that they have no conflict of interests related to this systematic
review. This systematic review was self- funded by the authors and their institutions.

S202

Key words: animal studies; clinical studies;

peri-implant mucositis; systematic review
Accepted for publication 27 November 2014

Peri-implant mucositis describes an

inflammatory lesion that is restricted
to the soft tissues surrounding an osseointegrated implant in function. At

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

Management of peri-implant mucositis

peri-implantitis sites, this lesion has
extended in apical direction and also
affects the implant supporting bone
(Lang & Berglundh 2011). Experimental studies performed in humans
provide clear evidence that periimplant mucositis may be induced
by a discontinuation of oral hygiene
procedures over a period of 3 weeks
(Pontoriero et al. 1994, Zitzmann
et al. 2001). These plaque-induced
lesions were associated with changes
in clinical (e.g. redness, oedema formation, bleeding on probing), histological (e.g. inflammatory cell
infiltrate, CD68 antigen reactivity,
pocket formation) and immunological (e.g. increases of interleukin
(IL)-1b, IL-8, matrixmetalloproteinase-8) parameters (Berglundh et al.
1992, Ericsson et al. 1995, Abrahamsson et al. 1998, Schwarz et al.
2014).
It has been reported that experimentally induced mucositis was
reversible at the clinical and biomarker level once the biofilm was disrupted and oral hygiene procedures
were reinforced (Pontoriero et al.
1994, Salvi et al. 2012). While nonsurgical therapy was effective in the
treatment of mucositis lesions, for
peri-implantitis, mechanical debridement alone has shown limited efficacy (Renvert et al. 2008, Klinge
et al. 2012). Adjunctive measures
(e.g. local antibiotics/antiseptics,
laser application) may be effective in
arresting disease progression at initial sites, however, moderate to
advanced peri-implantitis lesions
commonly require a more demanding surgical intervention or even
removal of the implant (Klinge et al.
2012, Heitz-Mayfield & Mombelli
2014). The treatment of early clinical
signs of peri-implant mucositis may
be considered a key strategy for the
primary prevention of peri-implantitis (Salvi & Zitzmann 2014). Accordingly, there is a need to identify the
most effective interventions for the
treatment of mucositis lesions. The
aim of this systematic review was
therefore to address the following
focused question: In patients with
peri-implant mucositis, what is the
efficacy of professionally administered plaque removal (PAPR) with
adjunctive measures on changing
signs of inflammation compared with
PARP alone?

Materials and Methods

This systematic review was structured and conducted according to

the preferred reporting items of the
PRISMA statement (Moher et al.
2009).
Focused question

The focused question serving for literature search was structured

according to the PICO format
(Miller & Forrest 2001): In patients
with peri-implant mucositis, what is
the efficacy of professionally administered plaque removal (PAPR) with
adjunctive measures on changing
signs of inflammation compared with
PARP alone?.
Population: patients with periimplant mucositis,
Intervention: PAPR with adjunctive measures,
Comparison:
PAPR
without
adjunctive measures,
Outcome: changes of signs of
inflammation.

Search strategy

The PubMed database of the U.S.

National Library of Medicine and
the Web of Knowledge of Thomson
Reuters were used as electronic databases to perform a systematic
search for relevant articles published in the dental literature
between 1992 up to May 31, 2014.
A commercially available software
program (Endnote X7, Thomson,
London, UK) was used for electronic title management. Screening
was performed independently by
two authors (F.S. and K.B.). Disagreement regarding inclusion during the first and second stage of
study selection was resolved by
discussion.
The combination of key words
(i.e. Medical Subject Headings
MeSH) and free text terms included:
treatment OR nonsurgical
treatment OR non-surgical
treatment OR therapy OR
nonsurgical therapy OR nonsurgical therapy OR antiseptic
treatment OR antibiotic treatment OR adjunctive treatment OR antiseptic therapy
OR antibiotic therapy OR

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

S203

adjunctive therapy OR management OR care management, patient (MeSH) OR

dental prophylaxis (MeSH)
OR maintenance (MeSH) OR
implant maintenance OR
maintenance care OR recall
OR supportive care OR supportive therapy
AND
peri-implant
disease
OR
periimplant disease OR periimplant infection OR periimplant infection OR mucositis
(MeSH) OR peri-implant mucositis OR periimplant mucositis
Electronic search was complemented by a hand search of the following journals:
Clinical Implant Dentistry and
Related Research; Clinical Oral
Implants Research; International
Journal of Oral and Maxillofacial
Implants; Journal of Clinical Periodontology; Journal of Periodontology. Finally, the references of
all selected full-text articles and
related reviews were scanned. If
required,
the
corresponding
authors were contacted and
requested to provide missing data
or information.

Study inclusion and exclusion criteria

During the first stage of study

selection, the titles and abstracts
were screened and evaluated according to the following inclusion criteria:
1 English language.
2 Prospective randomized controlled
(RCT), or non-randomized controlled (CCT) studies (split-mouth
or parallel group designs) in
humans comparing PAPR (i.e. any
type of mechanical debridement)
with or without adjunctive measures for biofilm removal, or
adjunctive
antiseptic/antibiotic
therapy in the treatment of periimplant mucositis.
3 Data on the clinical changes in
mucosal inflammation (i.e. bleeding scores) of PARP with or without adjunctive measures.

Management of peri-implant mucositis

S211

(a)

(b)

Fig. 3. Publication bias assessment: Funnel plot of precision by difference in means. Eggers linear regression method revealed symmetrical plots (p > 0.05) for changes in (a) BOP (p = 0.51) and (b) PD (p = 0.69) thus suggesting the absence of publication bias.

Similarly, WMD in GI- [SD = 0.13;

p = 0.34; 95% CI ( 0.38, 0.13)]
(Strooker et al. 1998, Thone-Muhling et al. 2010) and PD [SD = 0.10;
p = 0.60; 95% CI ( 0.27, 0.16)]
(Strooker et al. 1998, Porras et al.
2002, Thone-Muhling et al. 2010,
Hallstr
om et al. 2012, Ji et al. 2014)
reductions also failed to reach statistical significance between respective
test and control groups. In this context, it must be emphasized that
BOP is the key parameter for the
clinical diagnosis of peri-implant mu-

cositis, while a concomitant deepening of the pocket refers to periimplantitis (Lang & Berglundh
2011). However, the assessment of
both BOP and PD scores at healthy
implant sites is strongly influenced
by the probing pressure, and therefore bears a higher risk for false
positive outcomes when compared
with natural teeth (Gerber et al.
2009). Since the probing pressure
has only been reported in a very few
of the included studies (Strooker
et al. 1998, Hallstr
om et al. 2012), it

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

is impossible to estimate to what

extend variations in probing forces
may have contributed either to false
positive case definitions at baseline
or false-negative outcomes after therapy. For instance, Strooker et al.
(1998) used a pressure of 0.65N,
which is markedly higher than the
threshold level (0.25N) recommended for probing at implant sites
Lang & Berglundh (2011).
Despite the lack of a significant
difference in the calculated WMD in
BOP, GI and PD reductions between

Identification

Management of peri-implant mucositis

11488 of records identified through

database searching

S205

24 of additional records identified through

other sources

Eligibility

Screening

8135 of records after duplicates removed

312 of records screened

295 of records excluded

19 of full-text articles
assessed for eligibility

12 of full-text articles
excluded

Included

7 of studies included in
qualitative synthesis

6 of studies included in
quantitative synthesis

Fig. 1. Flow diagram of literature search and inclusion.

Table 2. Risk of bias (+ low/

studies

high/? unclear) summary for finally selected randomized

Random
sequence
generation
Schenk et al. (1997)
Strooker et al. (1998)
Porras et al. (2002)
Thone-Muhling
et al. (2010)
Hallstr
om et al. (2012)
McKenna et al. (2013)
Ji et al. (2014)

Allocation
concealment

Blinding of
participants
and
personnel

?
?
?

Blinding of
outcome
assessment

+
?

+
+
+

?
+
?

between group differences at both

subject and implant level failed to
reach statistical significance (Ji et al.
2014) (Table 3a).
PAPR with or without adjunctive
antiseptic therapy

Four RCTs reported on the clinical

outcomes when antiseptic therapy
was used as an adjunct to OHI and
mechanical debridement (Strooker
et al. 1998, Porras et al. 2002, ThoneMuhling et al. 2010, McKenna et al.
2013) (Table 3b).
In one RCT, 16 patients each
exhibiting four mandibular implants

+
+

Incomplete
outcome
data
+
+
+
+
+

(implant system not reported) with a

bar retained overdenture and clinical
signs of peri-implants mucositis were
included (Strooker et al. 1998). A
case definition was not reported and
it remains unclear whether all
implants revealed clinical signs of
peri-implant mucositis. Test (carbon
curets + rubber cup polishing) and
control (adjunctive application of
phosphoric acid gel) treatments were
provided every month. At 5 months,
mean BOP (proportion of bleeding
sites) scores were significantly
reduced in both groups, while test
sites revealed a significantly higher
reduction in mean GI (L
oe & Silness

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

1963) (modified, but not specified)

scores and colony-forming unites
when compared with control sites
respectively (Strooker et al. 1998).
Porras et al. (2002) compared
OHI + mechanical debridement with
and without local pocket irrigation
using
chlorhexidine
digluconate
(CHX) + topical CHX gel application + CHX mouthwash (twice for
10 days). At 3 months, statistical
analysis failed to identify any significant differences in mean mucosal
bleeding following probing (mBI), or
mean BOP (bleeding within 30 s of
probing) scores between test and
control groups. However, the test
group revealed a significantly higher
change in mean PD values when
compared with the control group.
Both groups revealed marked
improvements at the microbiological
level (Porras et al. 2002).
In another RCT, adjunctive antiseptic therapy consisting of topical
CHX gel application + full-mouth
disinfection + CHX mouthrinse (29/
day) and tonsil spraying (19/day)
for 14 days was compared with OHI
+ mechanical debridement (plastic
scaler + polyetheretherketone-coated
ultrasonic instruments) + full-mouth
scaling alone (Thone-Muhling et al.

S206

Schwarz et al.

2010). Mean BOP scores were significantly reduced in the test group at
1, 2 and 4 months, while these
changes did not reach statistical significance in the control group. However, at 8 months, mean BOP scores
were not significantly different to
baseline in both groups. A significant reduction in mean GI values
was merely observed in the control
group at 2 months. Both treatment
procedures resulted in a significant
reduction in mean PD values at
8 months. Between-group comparisons did not reveal any significant
differences for any of the clinical
and
microbiological
parameters
investigated (Thone-Muhling et al.
2010).
In a double blind RCT, mucositis lesions were experimentally
induced in 20 patients with four
root form implants each (total of
80 implants) (McKenna et al. 2013).
In parallel with the induction of
mucositis lesions (case definition
was not reported), the four
implants in each patient were randomly allocated to the following
treatment (60 s) procedures: ozone
therapy (about 2100 ppm delivered
by a fine plastic cannula) + 0.9%
NaCl (test 1), 3.0% H2O2 + air
(test 2), ozone + 3.0% H2O2 (test
3), or air + 0.9% NaCl (control).
Treatment was repeated at days 7
and 14. At 21 days, mean bleeding
index (grades 04) was significantly
higher in the control when compared with the test groups respectively. Similar results were also
noted for mean GI values, with the
significantly lowest values noted in
the test groups (McKenna et al.
2013) (Table 3b).
PAPR with or without adjunctive antibiotic
therapy

Two RCTs reported on the clinical

outcomes following local or systemic
antibiotic therapy used as an adjunct
to OHI and mechanical debridement
(Schenk et al. 1997, Hallstr
om et al.
2012) (Table 3c).
In one RCT, eight patients with a
total of 24 implants and clinical
signs of peri-implant mucositis
(PD > 4 mm, BOP+, no radiographic bone loss) were randomly
allocated in a split-mouth design to
either mechanical debridement (steel
curets + rubber cup polishing) +

local delivery of tetracycline HCl

(25%) fibres for 10 days (test) or
mechanical debridement alone (control). All patients were instructed to
use a 0.2% CHX mouthrinse twice
for 10 days. At three test implants,
the fibre was completely or partially
lost between 7 and 10 days. While
test sites revealed BOP improvements, control sites were characterized by a further increase in bleeding
scores at 3 months (Schenk et al.
1997).
In another RCT, 45 patients each
exhibiting one implant with clinical
signs of mucositis (PD 4 mm,
BOP and/or Pus +, radiographic
bone loss 2 mm) underwent basic
periodontal therapy at remaining
teeth (Hallstr
om et al. 2012). Two
groups were randomly allocated to
either OHI + mechanical debridement (titanium curets + rubber polishing)
+
systemic
antibiotic
medication (Azithromycin 500 mg
day 1 and 250 mg days 24) (test),
or OHI + mechanical debridement
alone (control). Clinical and microbiological parameters were assessed
after 1, 3 and 6 months, without
providing any further professional
plaque control. The per-protocol
analysis (subject level) at 6 months
did not reveal any significant differences between both groups for all
clinical and microbiological parameters investigated (Hallstr
om et al.
2012) (Table 3c).
Meta-analysis

Meta-analysis was conducted on

studies reporting on similar assessments of either BOP, GI or PD
scores. Since the clinical outcomes
noted by McKenna et al. (2013)
mainly reflect disease prevention
rather than therapy of established
lesions, this study was not considered for the quantitative analysis.
Based on four studies (Schenk
et al. 1997, Strooker et al. 1998,
Thone-Muhling et al. 2010, Hallstr
om
et al. 2012), the weighted mean
difference (WMD) [SD; p; 95% CI]
in BOP reduction between test and
control groups amounted to 8.16%
[SD = 4.61; p = 0.07; 95% CI
( 17.20, 0.88)] not favouring adjunctive antiseptic or antibiotic (local
and systemic) measures over PAPR
alone (p value for heterogeneity:
0.42, I2 = 0% = low heterogeneity)

(Fig. 2a). Based on two studies

(Strooker et al. 1998, Thone-Muhling
et al. 2010), WMD in GI reduction
between test and control groups
amounted to
0.12 [SD = 0.13;
p = 0.34; 95% CI ( 0.38, 0.13)]
not favouring adjunctive antiseptic
therapy (p value for heterogeneity:
0.35, I2 = 0% = low heterogeneity)
(Fig. 2b).
Based on five studies (Strooker
et al. 1998, Porras et al. 2002, ThoneMuhling et al. 2010, Hallstr
om et al.
2012, Ji et al. 2014), WMD in PD
reduction between test and control
groups amounted to
0.056 mm
[SD = 0.10; p = 0.60; 95% CI ( 0.27,
0.16)] not favouring adjunctive
(antiseptics, systemic antibiotics, air
abrasive device) measures over
PAPR alone (p value for heterogeneity: 0.42, I2 = 0% = low heterogeneity) (Fig. 2c).
Funnel plots of precision by difference in means are presented in
Figures 3a and b. Eggers linear
regression method revealed symmetrical plots for changes in BOP
(p = 0.51) and PD (p = 0.69) thus
suggesting the absence of publication
bias.
Discussion

The present systematic review was

conducted to address the following
focused question: In patients with
peri-implant mucositis, what is the
efficacy of professionally administered plaque removal (PAPR) with
adjunctive measures on changing
signs of inflammation compared with
PARP alone?
Basically, the literature search
revealed that the efficacy of PAPR
with or without adjunctive measures
for the therapy of mucositis lesions
around
osseointegrated
dental
implants has merely been evaluated
in a total of seven RCTs. The
majority of these studies reported on
the application of adjunctive antiseptics (Strooker et al. 1998, Porras
et al. 2002, Thone-Muhling et al.
2010, McKenna et al. 2013), while
only one RCT each compared PAPR
either with adjunctive mechanical
measures (i.e. air abrasive device) (Ji
et al. 2014), local- (Schenk et al.
1997), or systemic (Hallstr
om et al.
2012) antibiotics. Furthermore, one
RCT aimed at assessing the efficacy
of subgingival ozone application on

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

(b)
Strooker
et al. (1998)

(a)
Ji et al. (2014)

Publication

RCT
Split-mouth
Design

RCT, parallel

Design

16 patients
each with 4
mandibular
implants and bar
retained
overdenture

24 patients
33 implants
1 Implant System

Population

Not reported

PD 4 mm, BOP +
No radiographic
bone loss

Case definition

5 months

3 months

Period

Supra-/subgingival scaling
(carbon curets) + polishing
(rubber cup)
+
Phosphoric acid gel
(35%) in sulcus for 1 min
Once every month

OHI + Mechanical
debridement
(ultrasonic scaler with
carbon fibre tips) + air
abrasive device (sites
with PD 4 mm)

Test

Supra-/subgingival
scaling (carbon curets) +
polishing (rubber cup)
Once every month

OHI + Mechanical
debridement
(ultrasonic
scaler with carbon
fibre tips)

Control

Test (Subject Level)

BOP: 30.5 (27.5) (BL) to
9.7 (10.97) % (5 months)
(sign.)
GI: 0.92 (0.75) (BL) to
0.34 (0.38) (5 months)
(sign.)
PD: 2.97 (0.68) (BL) to
2.34 (0.54) mm (5 months)
(sign.)
Control (Subject Level)
BOP: 29.2 (29.44) (BL) to
14.3 (22.47) % (5 months)
(sign.)
GI: 0.82 (0.8) (BL) to 0.57
(0.6) (5 months) (sign.)
PD: 2.83 (0.57) (BL) to
2.48 (0.49) mm (5 months)
(sign.)
Sign. between group
difference in mean GI values
and colony-forming units at
5 months

Test
BI: 1.4  0.57 (BL) to
1.1  0.58 (3 months,
Subject Level)
BI: 1.7  0.93 (BL) to
1.1  0.98 (3 months,
Implant Level) (sign.)
Sites without bleeding: 29.3%
PD: 3.6  0.47 (BL) to
3.2  0.48 mm (3 months,
Subject Level) (sign.)
Control
BI: 1.5  0.65 (BL) to
1.0  0.85 (3 months,
Subject Level)
BI: 1.7  1.0 (BL) to
0.9  1.1 (3 months,
Implant Level) (sign.)
Sites without bleeding:
42.1%
PD: 3.5  0.5 (BL) to
3.1  0.38 mm (3 months,
Subject Level) (sign.)

Mean (SD) outcome

Table 3. Included studies: (a) with or without adjunctive measures for biofilm removal; (b) with or without adjunctive antiseptic therapy; and (c) with or without adjunctive antibiotic
therapy

Management of peri-implant mucositis

S207

RCT, parallel

Thone-Muhling
et al. (2010)

RCT

RCT, parallel

Porras
et al. (2002)

McKenna
et al. (2013)

Design

Publication

Table 3. (continued)

20 patients
80 root form
implants

11 patients
36 implants
2 implant types

16 patients
28 implants
3 implant types
(plasma sprayed
Ti/cp Ti (HA
coated Ti)

Population

Experimentally induced
mucositis
Case definition
not reported
Treatment was initiated
with developing
mucositis lesions (day 0)

Test 1:
Ozone + 0.9% NaCl
Test 2:
3.0% H2O2+ air
Test 3:
Ozone + 3.0% H2O2
Repeated treatments
(60 s each) at days
7 and 14

21 days

Air + 0.9% NaCl

Repeated treatments
(60 s each) at days
7 and 14

OHI + Mechanical
cleansing
(plastic scaler and
polyetheretherketone
-coated
ultrasonic instruments)
+
full mouth scaling
in one session

BOP +
and/or GI 1
absence of radiographic
bone loss during
the last 2 years

OHI + Mechanical cleansing

(plastic scaler and
polyetheretherketone-coated
ultrasonic instruments)
+
topical CHX gel application
once + full-mouth disinfection
(deep scaling in one session +
CHX disinfection of tongue
and tonsils)
+
0.2% CHX mouthrinse
29/day and tonsil spraying
19/day for 14 days

3 months

8 months

Control
OHI + Mechanical
cleansing (plastic scaler,
rubber cups, polishing
paste)

Test
OHI + Mechanical
cleansing (plastic scaler,
rubber cups, polishing
paste)
+
local irrigation CHX
(0.12%) and topical
CHX gel application
+
0.12% CHX mouthrinse
twice for 10 day

Period

Supra- and
subgingival plaque
PD 5 mm
BOP +
incipient
radiographic lesion

Case definition

mBI and BOP (%) scores:

no sign. differences between
groups at 1 and 3 months
PD values:
Test: 3.27 (0.81) (BL) to 2.71
(0.70) mm (3 months)
Control: 3.48 (0.61) (BL) to
2.55 (0.72) mm (3 months)
Changes in mean PD between
test and control groups at 3
months were statistically
significant (0.56 versus
0.93 mm)
Microbiological improvements
in both groups
Test
BOP: 0.22 (0.11) (BL) to 0.16
(0.09) (8 months)
GI: 0.6 (0.24) (BL) to 0.44
(0.23) (8 months)
PD: 3.4 (0.68) (BL) to 2.82
(0.59) (8 months) (sign.)
Control
BOP: 0.17 (0.19) (BL) to 0.17
(0.11) (8 months)
GI: 0.62 (0.36) (BL) to 0.43
(0.37) (8 months)
PD: 3.49 (0.78) (BL) to 2.84
(0.64) (8 months) (sign.)
Bacterial recolonization over
time
BI (21 days)
Control: 0.56 > Test 2: 0.18 =
Test 1: 0.05 = Test 3: 0.05
GI (21 days)
Control: 0.99 > Test 1: 0.50 =
Test 2: 0.49 = Test 3: 0.44

Mean (SD) outcome

S208
Schwarz et al.

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

RCT, parallel

RCT
Split-mouth
Design

Design

45 Patients
3 Implant
Systems

8 Patients
24 implants
1 implant type
(endosseous part:
titanium and
zirconoxide/
transmucosal
part: titanium
oxynitride)

Population
3 months

6 months

PD 4 mm BOP +
and/or Pus
Radiographic bone
loss 2 mm

Period

PD > 4 mm
BOP on at least 1 site
per implant
+/ mucosal hyperplasia
no radiographic bone loss

Case definition

OHI + Mechanical cleansing

(titanium curets + rubber
cups + polishing paste)
+
Azithromycin 500 mg day
1 and 250 mg days 24

Supra-/subgingival scaling
(Steel curets) + polishing
(rubber cup)
+
locally delivered tetracycline
HCl (25%) fibre for 10 days
+0.2% CHX mouthrinse
twice for 10 day

Test

OHI + Mechanical
cleansing (titanium
curets + rubber
cups + polishing paste)

Supra-/subgingival scaling
(Steel curets) + polishing
(rubber cup)
+
+0.2% CHX mouthrinse
twice for 10 day

Control

DBOP (3 months, Subject

Level)
Test: 17  25%
Control: 15  37%
PD/CAL values without
significant changes in both
groups
No adverse events
Partial/complete fibre loss
at 3 sites
Test
BOP: 82.6 (24.4) (BL) to
27.3 (18.8) (6 months,
Subject Level) (sign.)
PD at worst site: 5.5 (0.8)
(BL) to 4.1 (1.2) (6 months,
Subject Level)
Control
BOP: 80.0 (25.0) (BL) to
47.5 (32.3) (6 months, Subject
Level) (sign.)
PD at worst site: 5.7 (0.8)
(BL) to 4.9 (1.1) (6 months,
Subject Level)
odds ratio of a positive
treatment outcome (PD
4.0 mm and BOP 1) was
4.5:1 (test versus control)
Comparable reductions in
bacterial counts

Mean (SD) outcome

BI = bleeding index; BL = baseline; BOP = bleeding on probing; CAL = clinical attachment level; GI = modified gingival index; mBI = modified sulcus bleeding index; OHI = oral hygiene
instructions; PD = probing pocket depth; RCT = randomized controlled clinical study.

Hallstr
om
et al. (2012)

(c)
Schenk
et al. (1997)

Publication

Table 3. (continued)

Management of peri-implant mucositis

S209

S210

Schwarz et al.

(a)

(b)

(c)

Fig. 2. Forest plot indicating weighted mean difference (95% CI) in the reduction in primary and secondary outcomes. (a) Bleeding
on probing. (b) Gingival index. (c) Probing pocket depths.

the development of experimentally

induced mucositis (McKenna et al.
2013). Despite beneficial clinical outcomes in test groups 13, these data
mainly reflect disease prevention
rather than therapy of established

lesions. Therefore, the latter RCT

could not be considered in the quantitative analysis.
Data synthesis of respective
RCTs has identified that WMD in
BOP reduction did not favour

adjunctive antiseptic and antibiotic

(local, systemic) therapy over PAPR
alone [SD = 4.61; p = 0.07; 95% CI
( 17.20, 0.88)] (Schenk et al. 1997,
Strooker et al. 1998, Thone-Muhling
et al. 2010, Hallstr
om et al. 2012).

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

Management of peri-implant mucositis

S211

(a)

(b)

Fig. 3. Publication bias assessment: Funnel plot of precision by difference in means. Eggers linear regression method revealed symmetrical plots (p > 0.05) for changes in (a) BOP (p = 0.51) and (b) PD (p = 0.69) thus suggesting the absence of publication bias.

Similarly, WMD in GI- [SD = 0.13;

p = 0.34; 95% CI ( 0.38, 0.13)]
(Strooker et al. 1998, Thone-Muhling et al. 2010) and PD [SD = 0.10;
p = 0.60; 95% CI ( 0.27, 0.16)]
(Strooker et al. 1998, Porras et al.
2002, Thone-Muhling et al. 2010,
Hallstr
om et al. 2012, Ji et al. 2014)
reductions also failed to reach statistical significance between respective
test and control groups. In this context, it must be emphasized that
BOP is the key parameter for the
clinical diagnosis of peri-implant mu-

cositis, while a concomitant deepening of the pocket refers to periimplantitis (Lang & Berglundh
2011). However, the assessment of
both BOP and PD scores at healthy
implant sites is strongly influenced
by the probing pressure, and therefore bears a higher risk for false
positive outcomes when compared
with natural teeth (Gerber et al.
2009). Since the probing pressure
has only been reported in a very few
of the included studies (Strooker
et al. 1998, Hallstr
om et al. 2012), it

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

is impossible to estimate to what

extend variations in probing forces
may have contributed either to false
positive case definitions at baseline
or false-negative outcomes after therapy. For instance, Strooker et al.
(1998) used a pressure of 0.65N,
which is markedly higher than the
threshold level (0.25N) recommended for probing at implant sites
Lang & Berglundh (2011).
Despite the lack of a significant
difference in the calculated WMD in
BOP, GI and PD reductions between

S212

Schwarz et al.

test and control groups, one also has

to realize that qualitative analysis of
some of the included comparative
studies also reported on improvements of specific clinical parameters
when PAPR was combined with
adjunctive measures (Schenk et al.
1997, Strooker et al. 1998, McKenna
et al. 1997, Hallstr
om et al. 2012).
Basically, this observation is in
agreement with the clinical results
following non-surgical treatment of
peri-implantitis,
indicating
that
mechanical debridement alone has
limited efficacy, but adjunctive measures may improve the overall outcome of therapy (Lindhe & Meyle
2008, Klinge et al. 2012, Heitz-Mayfield & Mombelli 2014). Similarly, a
casecontrol study also pointed to
an ongoing progression of mucositis
lesions in the absence of any therapeutic intervention, while mean BOP
scores were reduced when OHI +
mechanical plaque removal was provided on a regular basis (Costa et al.
2012).
When further interpreting the
present analysis, it was also noted
that all treatment procedures investigated were associated with varying
residual BOP scores after respective
healing periods. These ranged from
9.7% to 27.3% in the test- and
14.3% to 47.5% in the control
groups. Treatment success has only
been evaluated in two of the
included studies (Hallstr
om et al.
2012, Ji et al. 2014). In particular,
the calculated odds ratio for a positive outcome after therapy (defined
as
PD 4 mm
and
bleeding
scores 1) was 4.5:1 (per-protocolanalysis) and 4.6:1 (intend-to-treat
analysis) favouring adjunctive systemic antibiotic medication over
PAPR alone (Hallstr
om et al. 2012).
The adjunctive use of an air abrasive
device was associated with an
absence of bleeding in 29.3% of the
sites, whereas these values were
42.1% in the control group (Ji et al.
2014). Accordingly, despite clinically
important improvements in mean
BOP scores, the evaluated data
clearly point to a limited efficacy of
various treatment procedures in
achieving disease resolution at mucositis sites. However, in one observational study, experimental mucositis
lesions were reported to be reversible at the biomarker level, since

pre-experimental levels of MMP-8

and IL-1b were obtained at 21 days
after OHI + PAPR. Despite marked
improvements in median GI at
21 days, these values were still significantly elevated when compared to
baseline (Salvi et al. 2012), thus
questioning the sensitivity of commonly used clinical parameters to
evaluate peri-implant health or
disease.
A total of four studies also
reported on microbiological changes
after therapy (Strooker et al. 1998,
Porras et al. 2002, Thone-Muhling
et al. 2010, Hallstr
om et al. 2012).
However, the reported outcomes did
not allow for any robust conclusions
either regarding disease resolution in
specific groups or any superiority of
adjunctive measures over PAPR. In
this context, it must also be emphasized that common periodontopathogenic bacteria could be isolated at
both healthy and diseased implant
sites (Casado et al. 2011), and the
microbiological analysis of 40 species
did no markedly differ by the clinical
implant status (i.e. healthy, mucositis, peri-implantitis) (Renvert et al.
2007). Furthermore, when interpreting the presented results, one has to
realize the short follow-up observation periods, ranging between 3 and
8 months. Accordingly, the longterm effect of various treatment procedures is unknown and needs further investigation. Finally, one has
to realize that all studies investigated
used different protocols for PARP,
and therefore, the potential difference in the clinical efficacy of these
specific control treatments cannot be
estimated. There is a clear need to
properly define a standard control
protocol for the treatment of periimplant mucositis.
Within its limitations, the present
systematic review and meta-analysis
revealed that adjunctive antiseptic,
antibiotic (local and systemic) or
mechanical (i.e. air abrasive device)
therapy may not improve the efficacy of PAPR in reducing BOP, GI
and PD scores at mucositis sites on
the short term. Despite clinically
important improvements, a complete
resolution of clinical signs indicating
peri-implant mucositis may not be
expected by any of the treatment
and maintenance protocols investigated.

Acknowledgements

The authors appreciate the additional

information provided during the
process of contact with the following authors: Giovanni Salvi, Department of Periodontology, School of
Dental Medicine, University of Bern,
Bern, Switzerland; Poliana Duarte,
Department of Periodontology, Dental Research Division, Guarulhos
University, S~
ao Paulo, Brazil; Ali
Farahani, Craniofacial and Special
Care Orthodontics, Childrens Hospital Los Angeles, USC, USA.
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Clinical Relevance

Scientific rationale for the study:

This systematic review and meta
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Principal findings: Adjunctive therapy (i.e. antiseptics, local and systemic antibiotics, air abrasive device)
did not significantly improve the efficacy of PAPR in reducing BOP, GI,
and PD scores at mucositis sites.
Despite
clinically
important
improvements, disease resolution

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

S213

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Address:
Kathrin Becker
Department of Oral Surgery
Westdeutsche Kieferklinik
Heinrich-Heine-University
D-40225 D
usseldorf, Germany
E-mail: Kathrin.Becker@med.uniduesseldorf.de

was not commonly achieved by

any of the treatment protocols
investigated.
Practical implications: PARP with
or without adjunctive measures
may be suitable in controlling perimplant mucositis on the shortterm.