Journal of Hospital Infection (2009) 72, 104e110

Available online at www.sciencedirect.com

www.elsevierhealth.com/journals/jhin

REVIEW

A review of dental implants and infection

A.D. Pye a, D.E.A. Lockhart b, M.P. Dawson a, C.A. Murray b, A.J. Smith b,*

a Glasgow Dental Hospital and School, Faculty of Medicine, Glasgow University, Glasgow, UKb Infection Research Group, Glasgow Dental Hospital and School,Faculty of Medicine, Glasgow University, Glasgow, UK

Available online 28 March 2009

KEYWORDSDental implants;Failure; Infections;Peri-implantitis

* Corresponding author. Address: InLevel 9, Glasgow Dental Hospital andStreet, Glasgow G2 3JZ, UK. Tel.: þþ44 0141 353 1593.

E-mail address: a.smith@dental.gl

0195-6701/$ - see front matter ª 200doi:10.1016/j.jhin.2009.02.010

Summary Dental implants have become increasingly common for themanagement of tooth loss. Despite their placement in a contaminated sur-gical field, success rates are relatively high. This article reviews dental im-plants and highlights factors leading to infection and potential implantfailure. A literature search identified studies analysing the microbial com-position of peri-implant infections. The microflora of dental peri-implanti-tis resembles that found in chronic periodontitis, featuring predominantlyanaerobic Gram-negative bacilli, in particular Porphyromonas gingivalisand Prevotella intermedia, anaerobic Gram-negative cocci such as Veillo-nella spp. and spirochaetes including Treponema denticola. The role ofStaphylococcus aureus and coagulase-negative staphylococci that are typ-ically encountered in orthopaedic infections is debatable, although theyundoubtedly play a role when isolated from clinically infected sites. Like-wise, the aetiological involvement of coliforms and Candida spp. requiresfurther longitudinal studies. Currently, there are neither standardised an-tibiotic prophylactic regimens for dental implant placement nor universallyaccepted treatment for peri-implantitis. The treatment of infected im-plants is difficult and usually requires removal. In the UK there is no sys-tematic post-surgical implant surveillance programme. Therefore, thedevelopment of such a project would be advisable and provide valuableepidemiological data.ª 2009 The Hospital Infection Society. Published by Elsevier Ltd. All rightsreserved.

fection Research Group,School, 378 Sauchiehall44 0141 211 9747; fax:

a.ac.uk

9 The Hospital Infection Socie

Introduction

Dental implants are inert, alloplastic materialsembedded in the maxilla and/or mandible for themanagement of tooth loss and to aid replacementof lost orofacial structures as a result of trauma,

ty. Published by Elsevier Ltd. All rights reserved.

Dental implants and infection 105

neoplasia and congenital defects. The most com-mon type of dental implant is endosseous compris-ing a discrete, single implant unit (screw- orcylinder-shaped are the most typical forms) placedwithin a drilled space within dentoalveolar or basalbone. Commercially pure titanium or titanium al-loy are the common constituents of dental im-plants. However, alternative materials includeceramics such as aluminium oxide and other alloys(gold and nickelechromeevanadium). Generally,endosseous implants have a coating which maycomprise plasma-sprayed titanium or a layer of hy-droxyapatite to enhance early osseointegration.1

‘Osseointegration’ was discovered by P.-I. Bra-nemark in 1969 when he observed that a piece oftitanium embedded in rabbit bone became firmlyanchored and difficult to remove.2 Following oneyear of observation, no inflammation was detectedin the peri-implant bone, meanwhile soft tissuehad formed an attachment to the metal andbone to the titanium.3

The Branemark system of dental implants wasintroduced in 1971.4 Subsequently, an estimatedone million endosseous dental implants are placedannually worldwide and w80 different manufac-turers produce 220 implant brands.5,6

Dental implants are predominantly placed inprimary care settings, commonly in general dentalpractice under local anaesthesia. There are, how-ever, no controls legislated over the operatingenvironment. Despite this and the contaminatedoral surgical field through which they are placed,success rates are reported as being as high as90e95%.7e9 This paper reviews endosseous dentalimplants and infections associated with theirfailure.

Osseointegration

After endosseous implant fixtures are surgicallyinserted into bone, the process of osseointegrationbegins. Osseointegration is considered ‘a direct,structural and functional connection betweenorganised vital bone and the surface of a titaniumimplant, capable of bearing the functional load’.10

This is possible as the titanium surface oxide layer(mainly titanium dioxide) is biocompatible, reac-tive and spontaneously forms calcium-phosphate-apatite.11

Furthermore, the titanium oxide surface ofimplants achieves a union with the superficialgingivae restricting the ingress of oral micro-organisms. Consequently, the implant/soft tissueinterface is similar to the union between tooth andgingivae.12

Success and failure

Criteria for successful integration of dental im-plants have been proposed.13 Of these, a lack ofmobility is of prime importance as ‘loosening’ isthe most often cited reason for implant fixture re-moval.14 Adell reported the success rate of 895 im-plant fixtures over an observational period of 5e9years after placement.7 Eighty-one percent ofmaxillary and 91% of mandibular implants re-mained stable.

Despite high success rates, implant fixture failuremay occur and is defined as ‘the inadequacy of thehost tissue to establish or maintain osseointegra-tion’.8 One review suggested that w2% of implantsfailed to achieve osseointegration following place-ment.9 Using a meta-analysis, failure rates forBranemark dental implants were 7.7% (excludingbone grafts) over five years.8 Interestingly, failurerates within edentulous patients were almost dou-ble those for partially dentate patients (7.6% versus3.8%). In addition, failure in the edentulous maxillawas approximately three times higher compared tothe edentulous mandible.8

Peri-implantitis is considered ‘an inflammatoryprocess affecting the tissues around an osseointe-grated implant in function, resulting in loss ofsupporting bone’.15 Signs of a failing dental implantare detected both clinically and radiographicallywith the diagnosis made in a similar way toperiodontitis.16 This involves measuring clinicalparameters including peri-implant loss of gingivalattachment, bleeding on probing, plaque/gingivitisindices, suppuration and mobility. Other relevantassessments include a peri-implant radiographicexamination and microbiological sampling. Peri-implantitis has been reported in 5e8% of caseswithin selected implant systems.17

Classification of failures

Implants can be described as failing or failed. Afailing implant demonstrates a progressive loss ofsupporting bone but is clinically immobile,whereas a failed implant is clinically mobile.18

When an implant has failed, removal is recommen-ded while a failing implant may be salvaged if it isdiagnosed early and treated appropriately.19,20

Implant failures may also be categorised as earlyor late. Early failures occur before osseointegrationand prosthetic rehabilitation has taken place withlate failures occurring afterwards.13 Factors affect-ing early failure of dental implants may be broadlyclassified as: implant-, patient- and surgical tech-nique/environment-related (Table I). Late failures

Table I Factors related to the failure of dentalimplants21e27

Factor Comment

Implant Previous failureSurface roughnessSurface purity and sterilityFit discrepanciesIntra-oral exposure timePremature loading

Mechanicaloverloading

Traumatic occlusion due to inadequaterestorationsOral hygiene

Patient (localfactors)

GingivitisBone quantity/qualityAdjacent infection/inflammationPresence of natural teethPeriodontal status of natural teethImpaction of foreign bodies (includingdebris from surgical procedure) in theimplant pocketSoft tissue viabilityVascular integrity

Patient(systemicfactors)

SmokingAlcoholismPredisposition to infection, e.g. age,obesity, steroid therapy, malnutrition,metabolic disease (diabetes)Systemic illnessChemotherapy/radiotherapyHypersensitivity to implantcomponents

Surgicaltechnique/environment

Surgical traumaOverheating (use of handpiece)Perioperative bacterialcontamination, e.g. via saliva, perioralskin, instruments, gloves, operatingroom air or air expired by patient

106 A.D. Pye et al.

usually concern a small number of patients with theiraetiology less well understood.21 Late failures maybe subclassified into lateeearly or lateedelayed de-pending on whether they occur during or after thefirst year of loading. Late-delayed failures are likelydue to changes in loading conditions in relation tothe quality/volume of bone and peri-implantitis.22

The likelihood of bacteria producing infection de-pends on their virulence and host factors.28

While the above factors relate to the failure ofimplants with regard to their anchorage in bone,occasionally the infectious process is limited to thesoft tissues overlying the healing implant site causingperi-implant mucositis.20 An implant compromisedby soft-tissue problems has a more favourable prog-nosis than one undergoing bone loss.29 Nevertheless,infection originating in the soft tissues may poten-tially progress deeper into the bone and undermine

the osseointegration process. Some of the most fre-quent causes of soft tissue infection during the heal-ing period involve residual suture material, poorlyseatedcover screws,protruding implantsandtraumafrom inadequately relieved dentures or occlusaltrauma from opposing teeth.19

Microbiology of failing dental implants

Infection represents one of many factors contrib-uting to the failure of dental implants. Presently,no single micro-organism has been closely associ-ated with colonisation or infection of any implantsystem.30

Failing dental implants are associated witha microbial flora traditionally associated withperiodontitis. Thus, a transition is observed froma predominately Gram-positive non-motile, aero-bic and facultative anaerobic composition towardsa flora with a greater proportion of Gram-negative,motile, anaerobic bacteria.31e34 If this predomi-nates for significant time periods then peri-implan-titis and eventual implant failure may result.35

Table II highlights studies investigating the micro-biology of failing implants.

Interestingly, micro-organisms not usually asso-ciated with periodontitis or dental abscesses such asstaphylococci, coliforms and Candida spp. are com-monly isolated from peri-implant lesions in somestudies.31,32,41 Staphylococci are present withinthe oral cavity and their isolation from peri-implantinfection is significant as both Staphylococcusaureus and coagulase-negative staphylococci arefrequently responsible for infections associatedwith metallic biomaterials and indwelling medicalinfections in general.42,43 More recently, Staphylo-coccus aureus has been demonstrated to have theability to adhere to titanium surfaces. This may besignificant in the colonisation of dental implantsand subsequent infections.44

Guidelines for the placement of dentalimplants

There are few published guidelines on infectioncontrol during the placement of dental implants.Those available advocate that the surgical fieldshould be isolated and free of contamination.45,46

This is clearly not readily achievable within the oralcavity. However, it has been elucidated that contam-ination of the operative site by patient’s saliva doesnot preclude success.47 Additionally, no significantdifferences were found in osseointegration successrates for implants placed under controlled operating

Table II Summary of studies investigating microbiology of failing implants

Type of implant(no. of patients/implants)

Method of detection Most prevalent microbes detected(% sites infected with bacteria)

Branemark(37/1e4 per patient)32

Culture Prevotella intermedia/P. nigrescens 60%Actinobacillus actinomycetemcomitans 60%Staphylococci, coliforms, Candida spp. 55%

Not stated(41/not stated)33

Culture/indirectimmunofluorescence

Bacteroides forsythus 59%Spirochetes 54%Fusobacterium spp. 41%Peptostreptococcus micros 39%Porphyromonas gingivalis 27%

Titanium hollow cylinderimplants (7/not stated)34

Culture/dark fieldmicroscopy

Bacteroides spp., Fusobacterium spp., spirochetes,fusiform bacilli, motile and curved rods (% not stated)

Not stated (13/20)36 Culture Staphylococcus spp. 55%Not stated (21/28)37 Checkerboard DNAeDNA

hybridization techniqueP. nicrescens, P. micros, Fusobacteriumnucleatum (% not stated)

IMZ (12/18)38 Culture Bacteroides spp. 89%Actinobacillus actinomycetemcomitans 89%Fusobacterium nucleatum 22%Capnocytophaga spp.27.8% Eikenella corrodens 17%

Various (10/12)39 PCR Porphyromonas gingivalis 67%Campylobacter rectus 42%Eikonella corrodens 42%Treponema denticola 42%Prevotella intermedia 33%Tannerella forsythia 33%Actinobacillus actinomycetemcomitans 17%

9 Astra16 Branemark5 ITI

Staumann (17/30)40

Culture Actinomyces spp. 83% F. nucleatum 70%P. intermedia/nigrescens group 60%Steptococcus anginosus (milleri) group 70%P. micros 63%Enterococcus spp. 30% Yeast spp. 30%

PCR, polymerase chain reaction.

Dental implants and infection 107

theatre conditions compared to a less environmen-tally controlled dental school clinic.48 Thismay implythat the operative environment is not as critical tothe success of dental implants compared to implantplacementwithinotherbody sites. Several strategiesto reduce contamination from the oral flora duringsurgery have been postulated.49,50 One such strategyinvolves rinsing preoperatively with chlorhexidine asthis may reduce microbial complications followingimplant placement.51 An in-vivo study showed thatchlorhexidine in suspension form is more effectivein inhibiting Porphyromonas gingivalis than the useof antibiotics.52 Others, however, failed to reachthese conclusions.53

During the surgical procedure, the implantshould be stored in the manufacturer’s sterilepackaging and only used in conjunction with therecommended instruments. Previously, the drillsused for bone preparation were not designatedsingle use and were decontaminated according to

local protocols. Manufacturers are graduallyintroducing single-use drills for use with theirimplant systems.

The role of antibiotics

The use of prophylactic antibiotics during im-plant placement remains controversial. A Co-chrane review found insufficient evidenceadvocating or dissuading their use.54 An updateof the review, however, determined there wassome evidence that 2 g of amoxicillin givenorally 1 h preoperatively significantly reducedearly failures of dental implants.55 The reviewconcluded by recommending the routine use ofone dose of 2 g of prophylactic amoxicillin imme-diately prior to placing dental implants. How-ever, it also stated that further research wasrequired to confirm the findings.

Table III Suggested treatments for infected dentalimplants20,29,57

Mechanical debridement

Pharmaceutical treatment e irrigation withchlorhexidine, local antibiotics (e.g. tetracyclinefibre) and systemic antibiotics

Surgical procedures e open flap debridement (todecontaminate and smooth the implant surface)

Correct anatomical conditions that impair plaquecontrol and encourage the formation of an anaerobicenvironment (includes both resective procedures andregenerative techniques such as guided tissueregeneration)

108 A.D. Pye et al.

At present, there is no reliable evidence for themost successful method of treating peri-implanti-tis.56 Despite a variety of therapeutic options(Table III), infected implants are difficult to treatand usually require removal.21 Some cliniciansadvise systemic antibiotics for the treatment offailing implants and a variety of drug regimensare described.58 Oral agents such as doxycycline,clindamycin, co-amoxiclav, penicillin V, amoxicil-lin and a combination of amoxicillin and metroni-dazole have been recommended. Nevertheless,no double-blind, randomised, placebo-controlledtrial has been undertaken.

Monitoring of success/failure

In the UK there are no surveillance programmes inplace providing epidemiological data on the micro-biology, success and failure rates of dental implants.Conversely, in Finland an Implant Register providescomprehensive data on the number of implantsinserted and removed together with any complica-tions related to the treatment.14 The programmestrives to ensure safe treatment for patients andhas been operational for nearly 20 years.

Conclusion

Dental implants are an increasingly common form ofprosthetic device implanted into patients. Theapparent high success rate for the placement ofendosseous dental implants under uncontrolled en-vironmental conditions and through a heavily colon-ised oral environment appears counterintuitive. Ifdental implants become infected the causativemicro-organisms are usually those implicated inperiodontal disease and include a range of Gram-negative anaerobes and spirochaetes. SinceS. aureus and coliforms are infrequently detected

in oral infection, their presence at implant infectionsites may represent cross-infection episodesalthough further data are required to support this.As occurs withorthopaedic implants, infecteddentalimplants are difficult to treat and removal is fre-quently required.

Data on failure and complications of dentalimplants should be collected and reported ina systematic fashion. This would enable a moredetailed analysis of the microbiology, treatmentoutcomes and assist in the formulation of clinicalguidelines in implant placement and treatment ofimplant-associated infections. Concerns have beenraised over the efficacy of dental instrument de-contamination, and this, coupled with the highlyinvasive nature of the insertion of dental implants,suggests that the introduction of a generic surveil-lance programme with appropriate microbiologicalmonitoring should be urgently considered.

Conflict of interest statementNone declared.

Funding sourcesNone.

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