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Decontamination of Titanium Implant Surface and Re-Osseointegration To Treat Peri-Implantitis: A Literature Review
Decontamination of Titanium Implant Surface and Re-Osseointegration To Treat Peri-Implantitis: A Literature Review
Purpose: To review the literature on decontamination of titanium implant surfaces following peri-implantitis
and the effect of various cleaning methods on re-osseointegration. Materials and Methods: An electronic
search of the literature at PubMed was conducted on the studies published between 1966 and October
2010. In vitro, animal, and clinical studies were included. Results: Of 597 studies retrieved, 74 manuscripts
were selected for the review. Various implant surface decontamination methods using various chemical
and mechanical agents have been suggested for treatment and re-osseointegration following peri-
implantitis. It has been shown that re-osseointegration of contaminated implant surfaces is possible; this
largely depends upon the surface of the implant and the types of decontamination techniques and bone
regenerative materials used. Complete re-osseointegration cannot be achieved by surface decontamination
alone. Titanium implants with titanium plasma-sprayed or sandblasted and acid-etched surfaces may be
effectively decontaminated by applying chlorhexidine and saline-soaked gauze or by repeated rinsing with
these solutions. Conclusions: Both mechanical and chemical decontamination techniques should be applied
alongside regenerative surgical procedures to obtain optimum re-osseointegration and successfully treat
peri-implantitis. In recent years, lasers and photodynamic therapy have shown minor beneficial results,
which need to be confirmed by long-term clinical studies with comparable groups. Int J Oral Maxillofac
Implants 2012;27:1043–1054
Key words: biofilm removal, chemical and mechanical cleaning, laser, peri-implantitis, photodynamic therapy,
re-osseointegration
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chemistry, roughness, and design features of the im- Topical application of minocycline microspheres has
plant-abutment complex play significant roles in biofilm also been shown to be effective in reducing microbial
formation.21 The microorganisms and their by-products count and bleeding scores.40,41 Citric acid was effective
lead to infection of the peri-implant tissues and subse- in reducing bacterial growth when applied at a pH of 1.2
quent destruction of the alveolar bone surrounding the It was also shown that contaminated hydroxyapatite-
implant.22–26 Therefore, the removal of biofilm from the coated titanium surfaces could be treated equally well
implant surface is a priority. For such purposes, the im- with airborne-particle abrasion or citric acid.43,45 Pre-
plant should be cleaned by instruments that are softer clinical studies on the re-osseointegration of rough im-
than titanium to avoid surface roughening (which may plant surfaces previously coated with bacterial biofilm,
encourage bacterial colonization). Mechanical cleans- following cleaning with citric acid and hydrogen perox-
ing using different prophylaxis procedures (ultrasonic ide, showed favorable results in terms of osseointegra-
scalers, plastic tip ultrasonic scalers, stainless steel cu- tion.42,44 Preclinical study findings are summarized in
rettes, titanium curettes, expanded polytetrafluoroeth- Table 2.10,30,42,44,57–63
ylene [e-PTFE] curettes, air-powered systems, abrasive Clinical studies of decontamination treatments are
rubber cups, polishing rubber cups, and brushes) summarized in Table 3.12,29,31,32,46,64–67 One study con-
have been studied in vitro to evaluate surface altera- cluded that hydrogen peroxide treatment of titanium
tions on titanium implant necks.27 Abrasive pumices,10 implants (from advanced peri-implantitis lesions) was
airborne particle–abrasion units (sodium bicarbo successful for 58% of the treated implants in terms of
nate),28 plastic scalers,29,30 and ultrasonic carbon fiber surgical and antimicrobial treatment aspects during a
curettes31,32 have also been evaluated. 5-year follow-up period.46 In a 5-month clinical trial,
the cleaning efficacy of 35% phosphoric acid etching
Investigations of Chemical Decontamination gel (pH 1) was evaluated and compared with mechani-
Chemical decontamination techniques via local appli- cal cleaning methods using carbon fiber curettes and
cation of antimicrobial solutions such as chlorhexidine a rubber cup.32 Both treatment modalities instantly
solution or gel,8,33–36 stannous fluoride,37 tetracy- reduced the number of colony-forming units, but the
cline,38,39 minocycline,40,41 citric acid,9,42–45 hydrogen reduction following the application of phosphoric acid
peroxide,2,42,44,46 and 35% phosphoric acid etching was greater.
gel32 have been reported. Findings of in vitro studies are
summarized in Table 1.28,43,45,47–55 The decontamination Examinations of PDT and Laser Treatment
of titanium cylinders with machined, plasma-sprayed, PDT has been employed for decontamination of im-
and hydroxyapatite-coated surfaces contaminated plant surfaces in the treatment of peri-implantitis for
with radioactive endotoxin from Porphyromonas microbial reduction and biofilm control.29,55 PDT is a
gingivalis was evaluated with cotton pellets soaked technique that uses a photosensitizer drug that is ca-
with water, citric acid, 0.12% chlorhexidine, and an pable of binding to the microbes in biofilm and, when
airborne particle–abrasion system.43 The study con- excited with high-energy laser light, cytotoxic singlet
cluded that citric acid treatment was equally effective oxygen molecules are produced, which can destroy
on both surfaces in the removal of the bacterial endo- bacterial cells. PDT using photosensitizer solutions
toxin, while machined and plasma-sprayed implants such as toluidine blue55 and chlorine e6 with BLC1010
were decontaminated effectively by all types of treat- (a water-soluble derivative of chlorine e6)68 in combi-
ment (Table 1). nation with a diode laser and azulene photosensitizer
Clinical studies have shown that chlorhexidine, solution with gallium-aluminum-arsenide (GaAlAs)
which is an effective bactericidal, can be used to de- laser69 have been reported.
stroy bacteria and prevent biofilm formation for Along with the use of PDT over the past few years,
treatment of peri-implantitis.33–35 The 12-week use of lasers have garnered great interest for their potential
stannous fluoride mouthrinse was shown to be effec- in implant decontamination for treatment of peri-
tive in controlling the amount of supragingival plaque implantitis. Different lasers, including erbium-doped
deposits in patients with generalized aggressive perio- yttrium-aluminum-garnet (Er:YAG) lasers,30,52,54,70
dontitis.56 A recent study has suggested that the use erbium,chromium–doped yttrium-scandium-gallium-
of stannous fluoride could decrease the production garnet (Er,Cr:YSGG) lasers,50 neodymium:yttrium-
of proinflammatory molecules like interleukin-1 beta, aluminum-garnet (Nd:YAG) lasers,71 and carbon
prostaglandin E2, and vascular endothelial growth dioxide (CO2) lasers,51,72–74 have been studied in vitro
factor, which aid in peri-implantitis–induced bone re- and in animal and human trials.
sorption.37 Local delivery of tetracycline via polymeric
fibers significantly reduced the numbers of microbes
causing peri-implantitis.39
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Table 1 In Vitro Studies of Various Decontamination Methods to Remove Biofilm from Implant Surfaces
Study Substrate Decontamination methods
Duarte et al Titanium disks with smooth machined 1. Er:YAG laser
(2009)28 surfaces and SAE surfaces 2. Metal curette
3. Plastic curette
4. Airborne particle–abrasion system (sodium bicarbonate)
Goncalves et al Titanium implants with machined 1. 980-nm GaAlAs laser
(2009)47 surfaces, surfaces sandblasted with 2. 1,064-nm Nd:YAG laser
titanium oxide (TiO2), and SAE surfaces
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Efficiently removed all bacterial cells from all surfaces tested. S sanguis
Nonsurgical instrumentation with Er:YAG laser resulted in effective removal of subgingival Not reported
calculus without any thermal damage.
Combined dye/laser treatment resulted in the destruction of bacterial cells in all the A actinomycetemcomitans,
surfaces studied. P gingivalis, and P intermedia
Machined implants were decontaminated more effectively by all treatments than the other Radioactive endotoxin from
surfaces, with the exception of citric acid treatment, which was equally effective on either P gingivalis
machined or hydroxyapatite surfaces.
Airborne-particle abrasion removed significantly greater amounts of lipopolysaccharide Radioactive endotoxin from E coli
than all other treatment modalities on titanium. Citric acid was superior in the removal of
lipopolysaccharide from HA-coated surfaces.
acute clinical reaction characterized by pain, submu- surfaces in the cited study. A considerable amount of
cosal emphysema, and breakdown of marginal bone re-osseointegration (39.4%) was reported in an animal
surrounding the implants was reported. The use of study when implant surfaces were decontaminated
metal curettes and airborne particle–abrasion sys- using plastic scalers and saline irrigation,30 and a sig-
tems on smooth and rough (sandblasted/acid-etched nificant reduction in counts of Actinobacillus actinomy-
[SAE]) surfaces showed that these surfaces were less cetemcomitans, P gingivalis, and Prevotella intermedia
susceptible to bacterial adhesion, probably because of species was achieved in a clinical study when a soft di-
the texture modification and the presence of abrasive ode laser (PDT) was added to the treatment regimen.29
deposits.28 Moreover, the use of metal curettes can In a clinical and radiographic study, decontamination
alter the surface roughness, encouraging additional with mechanical debridement using ultrasonic carbon
bacterial colonization. Plastic curette instrumenta- fiber curettes did not consistently result in healing of
tion caused no or minimal changes on the titanium peri-implant lesions.31
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Table 2 Animal Studies of Various Decontamination Methods for Peri-implantitis Treatment and
Animal
Study model Implant surface Decontamination and treatment protocol
Parlar et al Dogs Machined; SAE and TPS 1. Exchanging for a pristine implant cylinder
(2009)57 titanium implant cylinders 2. Spraying in situ with saline
3. Removal, cleansing outside the mouth by spraying with saline,
steam-sterilization, and remounting
Alhag et al Dogs Ti-Unite, Nobel Biocare 1. Swabbing with citric acid for 30 s followed by rinsing with
(2008)42 physiologic saline
2. Cleaning with a toothbrush and physiologic saline for 1 min
3. Swabbing with 10% hydrogen peroxide for 1 min followed by
rinsing with physiologic saline
Takasaki et al Dogs SAE surface 1. Er:YAG laser + saline irrigation
(2007)30 2. Plastic scaler + saline irrigation
Persson et al Dogs Machined Ti surface, SAE 1. CO2 laser + hydrogen peroxide
(2004)58 surface 2. Saline soaked in cotton pellets
Schou et al Monkeys TPS surface (Straumann) 1. Airborne-particle abrasion (sodium bicarbonate) + citric acid on
(2003)59 cotton pellet 2 min + saline irrigation 20 times
2. Airborne-particle abrasion
3. Five min of cleaning with gauze soaked in saline + citric acid
applied for 2 min followed by 20 times irrigation with saline
4. Gauze soaked alternately in chlorhexidine (0.1% aqueous) and
saline and irrigated repeatedly 20 times with both solutions
Schou et al Monkeys TPS surface (Straumann) Treatment with gauze soaked alternatively in chlorhexidine and saline,
(2003)60 followed by irrigation plus:
1. Flap surgery with autogenous bone, e-PTFE membrane for 3 months
2. Flap surgery and autogenous bone
3. Flap surgery and e-PTFE membrane for 3 months
4. Flap surgery alone
Kolonidis et al Dogs Commercially pure Ti 1. Citric acid (30 s) on cotton pellet and rinsing with saline
(2003)44 (Brånemark) implant 2. Toothbrush and saline rinsing for 1 min
3. Hydrogen peroxide (10%) on cotton pellet
Persson et al Dogs 1. Turned surface Saline-soaked cotton pellets and systemic antibiotic therapy with
(2001)61 2. SAE surface amoxicillin and metronidazole
(ITI implants)
Persson et al Dogs Commercially pure Ti 1. Abrasive pumice with rotating brush
(1999)10 (Brånemark) implants 2. Cotton pellets soaked with saline
Ericsson et al Dogs Ti (Brånemark) implants 1. Curettage + 1% delmopinol detergent and abutments autoclaved
(1996)62 2. No decontamination
Hurzeler et al Dogs Ti (Brånemark) implants Airborne-particle abrasion debridement (control group) along with
(1997)63 GBR (test groups)
CO2 = carbon dioxide; e-PTFE = expanded polytetrafluoroethylene; Er:YAG = erbium-doped yttrium-aluminum-garnet; SAE = sandblasted/acid-etched;
Ti = titanium; TPS = titanium plasma sprayed.
Efficacy of Chemical Decontamination animal studies swabbed sites with citric acid for 30 sec-
Mechanical debridement can be combined with chem- onds and followed this with physiologic saline rinse to
ical agents to remove hard (calculus, bone debris) and remove peri-implant biofilm.42,44 Hydrogen peroxide
soft deposits (tissue remnants and bacterial biofilm) swabbing for 1 minute followed by rinsing with physi-
from the infected implant surface. Citric acid has been ologic saline was another treatment protocol used in
shown to be effective in reducing bacterial growth at a these studies. Direct BIC and re-osseointegration were
pH of 1.2 However, clinical application of citric acid at a reported. It should be taken into consideration that
highly acidic pH may affect peri-implant tissues. A few these studies involved the removal of contaminated
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Subramani/Wismeijer
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Table 3 Human Studies of Various Decontamination Methods for Peri-implant Mucositis and Peri-
No. of patients
Study and implants Implant surface Decontamination and treatment protocol
Schwarz et al 12 patients, SAE implants (ITI) Nonsurgical treatment with Er:YAG laser
(2006)64 12 implants
Karring et al 11 patients, ITI, Brånemark, and Astra Oral hygiene instruction plus:
(2005)31 22 implants implants 1. Vector system (carbon fiber tip with HA aerosol spray)
2. Carbon fiber curette
Leonhardt et 9 patients, Branemark implants 10% hydrogen peroxide + rinsing with saline followed by
al (2003)46 26 implants 0.2% CHX mouthrinse twice daily and systemic antibiotics
(amoxicillin and metronidazole )
Dortbudak et 15 patients; no Plasma-spray-coated IMZ Plastic scalers, curettage, toluidine blue (100 µg/mL)–soft diode
al (2001)29 details about no. (Friatec) implants laser irradiation (905 nm for 60 seconds)
of implants used
Behneke et al 17 patients, ITI screw-type implants Airborne-particle abrasion with powder + saline irrigation on test
(2000)12 25 implants groups filled with autogenous bone grafts (bone chips and bone
blocks)
Haas et al 17 patients, TPS cylindric implants Toluidine blue (100 µg/mL) and laser irradiation at a wavelength
(2000)65 24 implants of 906 nm, followed by grafting with autogenous bone supported
with e-PTFE membranes
Strooker et al 16 patients, Implant-supported 1. Mechanical therapy + monthly 35% phosphoric acid gel (pH 1)
(1998)32 64 implants overdentures; no details for 1 minute. 2. Monthly mechanical debridement (with carbon
about the implant surface fiber curettes and rubber cup)
Hammerle et 2 patients, ITI implants (TPS surface) Wound debridement, rinsing with saline and 0.2% CHX, followed
al (1995)66 2 implants by e-PTFE membranes placed around the implants to aid GBR
Ten-day systemic antibiotic regimen (metronidazole and
amoxicillin) and 0.12% CHX mouthrinse twice daily
Lehmann et al 1 patient, Mandibular hollow-screw 0.1% CHX and saline rinsing, e-PTFE membrane for GBR, 10-day
(1992)67 1 implant implant (Bonefit, ITI) systemic antibiotic regimen (amoxicillin and ornidazole)
A actinomycetemcomitans = Actinobacillus actinomycetemcomitans; CHX = chlorhexidine digluconate; e-PTFE = expanded polytetrafluoroethylene;
Er:YAG = erbium-doped yttrium-aluminum-garnet; HA = hydroxyapatite; P intermedia = Prevotella intermedia; SAE = sandblasted/acid etched;
TPS = titanium plasma sprayed.
influence on the reduction of microbial counts.32 There study confirmed that the use of toluidine blue solution
are no long-term follow-up studies to confirm the re- and soft laser irradiation resulted in a significant re-
sults. The use of acids for decontaminating implant duction of A actinomycetemcomitans, P gingivalis, and
surfaces also must be evaluated further through in vi- P intermedia on a TPS surface.29 However, there have
tro and in human studies with more patients. been no long-term clinical studies on the use of PDT.
PDT has shown to be effective in reducing bleeding on
The Value of PDT probing and inflammation in beagle dogs.68 Preclinical
In recent years, photosensitization using toluidine studies of PDT for the treatment of ligature-induced
blue solution and soft laser irradiation has been shown peri-implantitis conditions and GBR have shown it to
to be effective in eliminating peri-implant pathogens be effective in terms of microbial reduction69 and re-
such as A actinomycetemcomitans, P gingivalis, and osseointegration77,78 in dogs. Re-osseointegration of
P intermedia from different titanium surfaces with- 41.9% for a commercially pure titanium surface and
out modifying the surfaces studied55 (Table 1). This 31.19% for a TPS surface was observed. These results
method was assessed in a clinical study with 24 peri- also need to be validated by human trials.
implantitis–affected implants (TPS surface) grafted
with autogenous bone supported by e-PTFE mem- Effectiveness of Laser Treatment
branes.65 Mean bone regeneration of 2 ± 1.90 mm after Use of the Er:YAG laser has been widely reported in the
a healing period of 9.5 months was observed, but this literature in recent years. Nonsurgical instrumentation
procedure was not compared with other decontami- with the Er:YAG laser effectively removed subgingival
nation methods. A recent clinical and microbiologic calculus without any thermal damage to explanted
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Clinical, microbiologic, and radiologic Despite the loss of seven implants and continuous bone loss around four implants
evaluation during the 5-year follow-up period, the treatment strategy was successful in 58% of
implants treated.
Microbiologic evaluation A actinomycetemcomitans, P gingivalis, and P intermedia were reduced significantly.
Clinical and radiographic evaluation Improved bone fill of 3.9 mm and 4.2 mm.
Radiographic evaluation Peri-implant bone gain was 2 ± 1.90 mm after 9.5 months.
Clinical and microbiologic evaluation Both treatment groups showed reduction in colony-forming units, with greater
reduction in 35% phosphoric acid gel group.
Radiographic analysis Mean bone gain of 1.5 to 3.6 mm, 1 year after membrane removal.
Radiographic analysis Mean bone gain of 4 to 5 mm, 5 months after membrane removal.
titanium SAE implants following peri-implantitis.54 A laser showed a mixed chronic inflammatory cell in-
later in vitro study using the Er:YAG laser showed effec- filtrate in peri-implant biopsy specimens64 (Table 3).
tive removal of supragingival plaque biofilms grown The study concluded that a single course of nonsurgi-
on SAE titanium implants, but the treatment failed to cal treatment of peri-implantitis via the Er:YAG laser
restore the biocompatibility of contaminated titanium may not be sufficient for the maintenance of failing
surfaces.52 A similar study using the Er,Cr:YSGG laser implants. Treatment with the Er:YAG laser followed
showed high efficacy of biofilm removal in an energy- by saline irrigation on infected SAE surfaces in a dog
dependent manner, but this technique also failed to study revealed a higher re-osseointegration value of
reestablish biocompatibility of contaminated titanium 69.7%.30 These studies show that laser therapy should
surfaces.50 A recent in vitro study on the bactericidal be combined with chemical decontaminants like
effect of the Er:YAG laser on titanium implants with chlorhexidine or saline solution to achieve higher re-
machined surfaces, TPS implants, and SAE implants osseointegration.
was reported.48 The results showed no surface altera- In an in vitro study, titanium implants with ma-
tion and decontamination values of 76.2% of total bac- chined surfaces, surfaces sandblasted with titanium
terial count (P gingivalis) for machined test implants, oxide (TiO2), and SAE surfaces contaminated with
90.9% for TPS implants, and 98.3% for SAE implants. Enterococcus faecalis and P gingivalis were treated with
A minimal residual bacterial presence was observed 980-nm GaAlAs laser and 1,064-nm Nd:YAG lasers.47
on all the surfaces evaluated. However, a clinical and Different irradiation outputs were used to explore
histopathologic study in a group of 12 patients with the effect on bacterial killing and surface alterations.
SAE implants using nonsurgical treatment with Er:YAG GaAlAs laser provided 100% bacteria reduction on
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27. Matarasso S, Quaremba G, Coraggio F, Vaia E, Cafiero C, Lang NP. 48. Quaranta A, Maida C, Scrascia A, Campus G, Quaranta M. Er:YAG
Maintenance of implants: An in vitro study of titanium implant laser application on titanium implant surfaces contaminated by
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NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.