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IMPLANT DENTISTRY / VOLUME 24, NUMBER 1 2015 13

Treatment of Periimplant Mucositis:


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A Systematic Review of Randomized


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Controlled Trials
Javier Ata-Ali, DDS, MS, MPH, PhD,* Fadi Ata-Ali, DDS, MS,† and Pablo Galindo-Moreno, DDS, PhD‡

n the same way as in the case of Objective: To determine the most are not effective for the treatment of

I peri-implantitis,1 the definitions of


periimplant mucositis vary in the
literature, and no clear criteria have
effective treatment for periimplant
mucositis in patients with dental im-
plants compared with a control group.
periimplant mucositis. The only effec-
tive treatment seems to be the use of
toothpaste with 0.3% triclosan.
been established regarding the diag- Materials and Methods: A Conclusion: Definitions of peri-
nosis and treatment of this disorder.
PubMed (MEDLINE) literature implant mucositis vary in the liter-
The Sixth European Workshop in
Periodontology2 held in 2008 in search was made of articles published ature, and no clear criteria have
Göteborg (Sweden) defined periim- up until October 2013. Randomized been established regarding the
plant mucositis as inflammation of controlled trials (RCTs) were strati- diagnosis and treatment of this
the periimplant mucosa, without signs fied according to their level of quality disorder. It highlights our lack of
of supporting bone loss. Later, the using the Jadad scale and levels of uniform treatment and need to
Seventh European Workshop in Peri- evidence (University of Oxford). establish additional research to
odontology3 held in Segovia (Spain) Results: The combinations of fully provide effective treatments
established the presence of bleeding search terms resulted in a list of 371 for this common condition. More,
on probing (BOP) as the key parameter titles. Of these, 114 references were larger, and longer-term RCTs are
for diagnosing periimplant mucositis. finally reviewed. Finally, 7 RCTs needed in this periimplant disease.
According to the latest definition of fulfilled the inclusion criteria and (Implant Dent 2015;24:13–18)
the American Academy of Periodontol-
were thus selected for inclusion in Key Words: dental implant, periim-
ogy,4 periimplant mucositis is a disease
in which the presence of inflammation the systematic review. Chlorhexidine, plant mucositis, periimplant dis-
is confined to the soft tissues surround- the administration of azithromycin, eases, inflammation, mechanical
ing a dental implant, with no signs of and glycine powder air polishing debridement, chlorhexidine
loss of supporting bone after initial
bone remodeling during healing.
Experimental studies in humans
have shown that the accumulation of teeth (gingivitis) and dental implants periimplant mucositis to affect 63.4%
bacterial plaque during a period of 3 (periimplant mucositis).5,6 Accord- of the patients and 30.7% of the implants.
weeks exhibits a similar effect in both ingly, periimplant mucositis appears The protocols used to treat gingivitis
as a host response to bacterial invasion, and periimplant mucositis are similar.
*Master in Oral Surgery and Medicine, Master in Oral Surgery
and Implantology, Public Dental Health Service, Arnau de in the same way as gingivitis in relation However, very few studies have ad-
Vilanova Hospital, Valencia University Medical and Dental
School, Valencia, Spain. to natural teeth.7 Histological studies of dressed the treatment of periimplant
†Valencia University Medical and Dental School, Valencia, Spain.
‡Department of Oral Surgery and Implant Dentistry, School of soft tissues have shown that inflamma- mucositis.12–17 A number of therapies
Dentistry, University of Granada, Granada, Spain.
tory infiltrations in the mucosa around have been used in application to periim-
Reprint requests and correspondence to: Javier Ata-Ali,
implants and the gingiva around natural plant mucositis, including antiseptic
DDS, MS, MPH, PhD, Public Dental Health Service, teeth have many features in common.8–10 agents,15,16,18–20 the administration of anti-
Arnau de Vilanova Hospital, San Clemente Street 12,
46015 Valencia, Spain, Phone: +0034963868501, Fax:
However, if bacterial plaque accumu- biotics,17 the use of glycine powder air
00963868197, E-mail: javiataali@hotmail.com lates for more than 3 months, the polishing (GPAP),21 or sodium carbonate
inflammatory infiltrate of the periimplant abrasive air powdering.14,22
ISSN 1056-6163/15/02401-013
Implant Dentistry mucosa is almost 3 times as great as in the The purpose of this study was to
Volume 24  Number 1
Copyright © 2014 by Lippincott Williams & Wilkins case of natural teeth.7,9 A meta-analysis systematically review the current liter-
DOI: 10.1097/ID.0000000000000190 conducted by Atieh et al11 found ature and determine the most effective
14 PERIIMPLANT MUCOSITIS  ATA-ALI ET AL

treatment for periimplant mucositis in Search Strategy for the Identification mucositis,” “peri-implant mucositis
patients with dental implants compared of Studies treatment,” “humans,” “mechanical
with a control group. The PubMed (MEDLINE) data- debridement,” “non-surgical treat-
base of the United States National ment,” “RCT,” and “controlled clinical
Library of Medicine was used to con- study”. Two examiners read the titles
MATERIAL AND METHODS duct a literature search of articles pub- and abstracts of all studies, and no
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The Preferred Reporting Items for lished up until October 2013. The blinding was carried out regarding the
Systematic Reviews and Meta-Analysis following search terms were used in names of the authors, journals and pub-
different combinations: “peri-implant lication date. The search was completed
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statement was used in this report.


Idenficaon
Screening
Eligibility
Included

Fig. 1. Prisma flow diagram of the searching processes and results. Seven RCTs were seen to meet the inclusion criteria and were thus
selected for inclusion in the systematic review.
IMPLANT DENTISTRY / VOLUME 24, NUMBER 1 2015 15

with a review of the references of the Oral y Cirugía Bucal, and Oral Surgery, retrospective studies, and articles pub-
selected articles to identify additional Oral Medicine, Oral Pathology, Oral lished as abstracts only; (3) studies on
studies not found in the initial literature Radiology, and Endodontology. peri-implantitis; (4) studies failing to
search. specify the diagnostic criteria of periim-
In addition, a manual search (up Study Screening Criteria plant mucositis or the duration of
until October 2013) was made of the Before starting the study, a series of follow-up. No restrictions were placed
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following journals: Clinical Implant inclusion and exclusion criteria were on the year or language of publication.
Dentistry and Related Research, Clini- established. Full-text articles chosen Authors were contacted for clarification
cal Oral Investigations, Clinical Oral were assessed for the following inclu- of missing information when necessary.
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Implants Research, European Journal sion criteria: (1) patients with at least 1
of Oral Implantology, Implant Den- dental implant presenting signs of peri- Quality Assessment
tistry, International Journal of Oral implant mucositis; (2) follow-up for at The methodological quality of the
and Maxillofacial Implants, Journal of least 3 months; and (3) randomized studies was assessed according to the
Clinical Periodontology, Journal of controlled trials (RCTs). The following levels of evidence (University of
Oral Implantology, Journal of Peri- exclusion criteria were applied: (1) non- Oxford Centre for Evidence Based
odontology, Medicina Oral, Patología randomized studies; (2) case series, Medicine)23 and the Jadad scale,

Table 1. Description of the 7 Studies Included in the Systematic Review


No. patients/No. Follow-up
implants (Study vs Period
Study Definition of Periimplant Mucositis Treatment (Study vs Control) Control) (mo)
De Siena et al20 BOP with or without swelling and 1% CHX gel twice a day for 10 days 13/d vs 10/d 3
redness. Periimplant bone versus 0.2% CHX rinse twice a day
resorption ,3 mm for 10 days
Ji et al21 PD $4 mm and BOP positive. No Supragingival scaling, root 12/17 vs 12/16 3
detectable loss of supporting bone debridement and polishing versus
as compared with periapical implants in the test group were
radiographs further treated with GPAP*†
Hallström et al17 PD $4 mm combined with bleeding Mechanical debridement with titanium 22/22 vs 21/21 6
and/or pus on probing curettes + polishing using rubber
cups and polishing paste versus
mechanical debridement with
titanium curettes + polishing using
rubber cups and polishing paste +
azithromycin 4 days (500 mg at day
1 and 250 mg at days 2–4)
Heitz-Mayfield Bleeding on light probing with no loss Mechanical treatment + 0.5% CHX 15/15 vs 14/14 3
et al18 of supporting bone gel versus mechanical treatment +
placebo gel
Thöne-Mühling BOP and/or a gingival index $1 at Treatment of remaining teeth (SRP + 6/22 vs 5/14 8
et al16 least at 1 site at baseline, and tartrectomy) versus SRP + 1% CHX
absence of periimplant bone loss gel applied once subgingivally +
during the last 2 years before dorsum of the tongue brushed for
baseline 1 minute with 1% CHX gel + each
tonsil was sprayed 4 times with
0.2% CHX spray + rinse twice for
1 minute with 0.2% CHX solution‡
Ramberg et al15 Bleeding after probing 0.3% triclosan toothpaste versus 30/d vs 29/d 6
sodium fluoride toothpaste
Porras et al19 Presence of supragingival and 0.12% CHX gel + 0.12% CHX rinse 16/16 vs 16/12 3
subgingival plaque; PD #5 mm, versus AT alone
showing evidence of inflammation
as measured with the modified
sulcus bleeding index
*GPAP (AIR-FLOW master and AIR-FLOW Perio; EMS, Nyon, Switzerland).
†All the implants were treated using ultrasonic scalers with carbon fiber tips (Satelec P5 ultrasonic scaling machine and PH2L, PH2R tips; Newtron, France).
‡The implants were cleaned using plastic scalers (Nobel Biocare) and polyetheretherketone-coated ultrasonic instruments (Piezon Master; EMS).
AT indicates antiseptic therapy including mechanical cleaning, using rubber cups and polishing paste, plastic scalers for removing calculus, and the provision of oral hygiene instructions; CHX,
chlorhexidine; SRP, scaling and root planing.
16 PERIIMPLANT MUCOSITIS  ATA-ALI ET AL

referred to the method of randomiza- with Jadad scores of #2. Four stud- plastic scalers and polyetheretherketone-
tion, allocation concealment, blindness ies15–18 were of relatively high quality, coated ultrasonic instruments. The
of examiners, and completeness of with Jadad scores of $3. As regards the control group received the same treat-
follow-up.24 Two authors indepen- level of evidence assessment, 4 stud- ment but without the administration
dently assessed the methodological ies15–18 were ranked as level 1b and 3 of chlorhexidine. Although a decrease
quality of the studies, and discrepancies studies19–21 as level 2b. in bacterial flora was observed in
the first 24 hours in the patients
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were discussed between them to reach


consensus. Those studies scoring #2 Description of the Studies treated with chlorhexidine, no sta-
points were considered to be of low Porras et al19 placed 28 implants in tistically significant results were
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quality, whereas $3 points were indic- 16 patients; the study group underwent obtained after 8 months of follow-up.
ative of high quality.24 mechanical cleaning, and instructions De Siena et al20 studied the effect of
were provided on oral hygiene, with chlorhexidine in 23 patients, comparing
RESULTS the prescription of 0.12% chlorhexidine 2 forms of presentation: 1% chlorhexi-
as a gel and rinse. The control group dine gel twice a day for 10 days and
Study Screening likewise underwent mechanical clean- 0.2% chlorhexidine rinse twice a day
The combinations of search terms ing, and instructions were provided on for 10 days. After a follow-up period
resulted in a list of 371 titles. Of these, oral hygiene, but without the use of of 3 months, plaque accumulation was
257 were found to be duplicated. To chlorhexidine. After a follow-up period found to differ significantly between the
avoid reviewing duplicate articles, we of 3 months, no statistically significant 2 groups. The bleeding index and prob-
remove any articles that appear more differences were observed between the ing depth (PD) were not significantly
than once. As a result, 114 references 2 groups. Heitz-Mayfield et al18 placed different between the 2 groups. Another
were finally reviewed. All articles 29 implants in 29 patients and studied study15 involving 59 patients analyzed
included in the review were RCTs and the effect of 0.5% chlorhexidine gel the effect of toothpaste with 0.3% tri-
were published in English. One publi- versus the administration of placebo closan (in 30 patients) versus sodium
cation was excluded on applying the gel (control group). After a follow-up fluoride toothpaste (in 29 controls).
defined screening criteria: the study period of 3 months, a decrease in peri- After a follow-up period of 6 months,
published by Corbella et al25 was not implant mucositis was observed in both BOP was seen to have decreased in the
an RCT. Finally, 7 RCTs were seen to groups, with no statistically significant study group from 53.8% to 29.1%,
meet the inclusion criteria and were thus differences associated with the use of whereas in the control group, the values
selected for inclusion in the systematic chlorhexidine. Thöne-Mühling et al16 increased from 52.3% to 58.8%.
review (Fig. 1). The characteristics of in turn placed 36 implants in 13 pa- The changes in BOP and PD were sta-
these 7 studies are summarized in tients. The study group received 1% tistically significant. Plaque accumula-
Table 1. chlorhexidine gel applied once subgin- tion was not significantly different
givally, the dorsum of the tongue was between the 2 groups. The authors
Assessment of Study Quality brushed for 1 minute with 1% chlorhex- concluded that the continuous use of
The assessment of the methodolog- idine gel, each tonsil was sprayed 4 toothpaste with 0.3% triclosan results
ical quality of each article is summa- times with 0.2% chlorhexidine spray, in significant reduction of periimplant
rized in Table 2. Of the 7 RCTs included rinsing was performed twice for 1 min- inflammation.
in the systematic review, 3 studies19–21 ute with 0.2% chlorhexidine solution, In an RCT17 involving 43 patients
were considered to be of low quality, and the implants were cleaned using with periimplant mucositis, the study

Table 2. Assessment of the Methodological Quality of Each Article


Porras Ramberg Thöne-Mühling Heitz-Mayfield Hallström De Siena
Quality Criteria et al19 et al15 et al16 et al18 et al17 Ji et al21 et al20
I Yes Yes Yes Yes Yes Yes No
II No No Yes Yes Yes Yes Yes
III No Yes No Yes No No No
IV No Yes No Yes No No No
V No Yes Yes Yes Yes No Yes
Jadad score 1 4 3 5 3 2 2
Quality of study Low High High High High Low Low
Levels of evidence 2b 1b 1b 1b 1b 2b 2b
(CEMB 2011)
I: Was the study described as random?
II: Was the randomization scheme described and appropriate?
III: Was the study described as double blind?
IV: Was the method of double blinding appropriate?
V: Was there a description of dropouts and withdrawals?
IMPLANT DENTISTRY / VOLUME 24, NUMBER 1 2015 17

group received mechanical debride- clearly different from the pathogenic available for review. A variable to be
ment with titanium curettes, polishing perspective. Both diseases represent taken into account in the interpretation
using rubber cups, polishing paste, a host response to the bacterial chal- of the results is the fact that 4 of the 7
and the administration of azithromycin lenge generated by biofilm formation. RCTs were of high quality, with level of
during 4 days (500 mg the first day, and The infectious etiology of periimplant evidence 1b. The aim was to conduct
250 mg the next 3 days). The control mucositis is well documented.26–28 A a meta-analysis to evaluate the effec-
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group received mechanical debride- study29 involving 34 patients with 77 tiveness of periimplant mucositis treat-
ment with titanium curettes, polishing dental implants (comprising 23 muco- ment. This was not possible mainly due
using rubber cups and polishing paste. sitis and 54 healthy periimplant sites) to the following: (1) Lack of homoge-
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No decrease in bacterial burden was concluded that bacterial plaque induces neity in defining periimplant mucositis.
observed after 3 months of follow-up. an inflammatory response that can lead In effect, each study used a different
After 6 months, BOP and PD were to the development of periimplant mu- definition, and we therefore accepted
seen to have decreased as a result of cositis. Adequate plaque control is the definition used by the authors in
improved oral hygiene. These authors17 therefore able to increase periimplant each publication; (2) The treatments
advised nonsurgical debridement with- health, avoiding the risk of future used in the studies differed in relation
out the administration of systemic anti- complications.29 Because periimplant to the mechanical procedures involved,
biotics as the treatment of choice for mucositis represents the obvious pre- the form of presentation, dosage, the
periimplant mucositis. Finally, Ji cursor of peri-implantitis, in the same treatments of the control groups, and the
et al21 placed 33 implants in 24 patients way that gingivitis is a precursor to pe- duration of follow-up.
and studied the effect of GPAP versus riodontitis, the treatment of mucositis
a control group subjected to supragin- must be the prerequisite for the preven-
gival scaling, root debridement, and tion of peri-implantitis.26 CONCLUSION
polishing. No statistically significant In an experimental study conducted In conclusion, the analysis of the 7
results were observed after a follow- by Trejo et al10 in cynomolgus monkeys RCTs included in the present system-
up period of 3 months. comparing mechanical debridement ver- atic review shows that chlorhexidine,
sus mechanical debridement with 0.12% the administration of azithromycin
chlorhexidine application, no statisti- through the systemic route, and GPAP
DISCUSSION cally significant differences were found are not effective for the treatment of
The purpose of this study was to between the 2 groups. Another study25 periimplant mucositis over the long
determine the most effective treatment demonstrated that a strict implant main- term. The only effective treatment iden-
for periimplant mucositis in patients tenance protocol can prevent the devel- tified was the use of toothpaste with
with dental implants compared with opment of peri-implantitis, and that 0.3% triclosan. An adequate level of
a control group. Four16,18–20 of the 7 periimplant mucositis can be success- oral hygiene is needed. Definitions of
RCTs included in the systematic review fully treated through professional oral periimplant mucositis vary in the liter-
examined the effect of chlorhexidine in hygiene combined with the use of chlo- ature, and no clear criteria have been
the treatment of periimplant mucositis, rhexidine as an antimicrobial agent. established regarding the diagnosis and
and none of them obtained statistically Other authors30,31 consider that GPAP treatment of these disorders. More
significant results. Of the remaining 3 can eliminate bacterial plaque in areas RCTs involving larger sample sizes
RCTs included in the review, signifi- that are scantly accessible to mechanical will be needed to establish the most
cant reduction of the signs of periim- debridement (situations with deep pock- effective treatment option for this
plant inflammation were only recorded ets or narrow defects). Máximo et al14 disease.
after the continuous use during 6 and Duarte et al22 in turn reported sodium
months of toothpaste with 0.3% triclo- carbonate abrasive air powdering to be
san.15 In contrast, no statistically signif- an effective treatment. The mechanical DISCLOSURE
icant results were obtained in the elimination of bacterial plaque improves The authors claim to have no
treatment of periimplant mucositis with but does not fully eliminate inflamma- financial interest, either directly or
either GPAP21 or the administration of tion of the periimplant mucosa.13 For this indirectly, in the products or informa-
azithromycin through the systemic reason, the use of coadjuvant treatments tion listed in the article.
route.17 We contacted the authors of such as chlorhexidine16,18,20 or sodium
the article published by De Siena carbonate abrasive air powdering has
et al,20 who confirmed that the study been proposed.14,22 The meta-analysis REFERENCES
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