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

Available online 28 March 2009

KEYWORDS
Dental implants;
Failure; Infections;
Peri-implantitis

Summary Dental implants have become increasingly common for the


management of tooth loss. Despite their placement in a contaminated surgical field, success rates are relatively high. This article reviews dental implants and highlights factors leading to infection and potential implant
failure. A literature search identified studies analysing the microbial composition of peri-implant infections. The microflora of dental peri-implantitis resembles that found in chronic periodontitis, featuring predominantly
anaerobic Gram-negative bacilli, in particular Porphyromonas gingivalis
and Prevotella intermedia, anaerobic Gram-negative cocci such as Veillonella spp. and spirochaetes including Treponema denticola. The role of
Staphylococcus aureus and coagulase-negative staphylococci that are typically encountered in orthopaedic infections is debatable, although they
undoubtedly play a role when isolated from clinically infected sites. Likewise, the aetiological involvement of coliforms and Candida spp. requires
further longitudinal studies. Currently, there are neither standardised antibiotic prophylactic regimens for dental implant placement nor universally
accepted treatment for peri-implantitis. The treatment of infected implants is difficult and usually requires removal. In the UK there is no systematic post-surgical implant surveillance programme. Therefore, the
development of such a project would be advisable and provide valuable
epidemiological data.
2009 The Hospital Infection Society. Published by Elsevier Ltd. All rights
reserved.

Introduction
* Corresponding author. Address: Infection Research Group,
Level 9, Glasgow Dental Hospital and School, 378 Sauchiehall
Street, Glasgow G2 3JZ, UK. Tel.: 44 0141 211 9747; fax:
44 0141 353 1593.
E-mail address: a.smith@dental.gla.ac.uk

Dental implants are inert, alloplastic materials


embedded in the maxilla and/or mandible for the
management of tooth loss and to aid replacement
of lost orofacial structures as a result of trauma,

0195-6701/$ - see front matter 2009 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.jhin.2009.02.010

Dental implants and infection


neoplasia and congenital defects. The most common type of dental implant is endosseous comprising a discrete, single implant unit (screw- or
cylinder-shaped are the most typical forms) placed
within a drilled space within dentoalveolar or basal
bone. Commercially pure titanium or titanium alloy are the common constituents of dental implants. However, alternative materials include
ceramics such as aluminium oxide and other alloys
(gold and nickelechromeevanadium). Generally,
endosseous implants have a coating which may
comprise plasma-sprayed titanium or a layer of hydroxyapatite to enhance early osseointegration.1
Osseointegration was discovered by P.-I. Bra
nemark in 1969 when he observed that a piece of
titanium embedded in rabbit bone became firmly
anchored and difficult to remove.2 Following one
year of observation, no inflammation was detected
in the peri-implant bone, meanwhile soft tissue
had formed an attachment to the metal and
bone to the titanium.3
The Bra
nemark system of dental implants was
introduced in 1971.4 Subsequently, an estimated
one million endosseous dental implants are placed
annually worldwide and w80 different manufacturers produce 220 implant brands.5,6
Dental implants are predominantly placed in
primary care settings, commonly in general dental
practice under local anaesthesia. There are, however, no controls legislated over the operating
environment. Despite this and the contaminated
oral surgical field through which they are placed,
success rates are reported as being as high as
90e95%.7e9 This paper reviews endosseous dental
implants and infections associated with their
failure.

Osseointegration
After endosseous implant fixtures are surgically
inserted into bone, the process of osseointegration
begins. Osseointegration is considered a direct,
structural and functional connection between
organised vital bone and the surface of a titanium
implant, capable of bearing the functional load.10
This is possible as the titanium surface oxide layer
(mainly titanium dioxide) is biocompatible, reactive and spontaneously forms calcium-phosphateapatite.11
Furthermore, the titanium oxide surface of
implants achieves a union with the superficial
gingivae restricting the ingress of oral microorganisms. Consequently, the implant/soft tissue
interface is similar to the union between tooth and
gingivae.12

105

Success and failure


Criteria for successful integration of dental implants have been proposed.13 Of these, a lack of
mobility is of prime importance as loosening is
the most often cited reason for implant fixture removal.14 Adell reported the success rate of 895 implant fixtures over an observational period of 5e9
years after placement.7 Eighty-one percent of
maxillary and 91% of mandibular implants remained stable.
Despite high success rates, implant fixture failure
may occur and is defined as the inadequacy of the
host tissue to establish or maintain osseointegration.8 One review suggested that w2% of implants
failed to achieve osseointegration following placement.9 Using a meta-analysis, failure rates for
Bra
nemark dental implants were 7.7% (excluding
bone grafts) over five years.8 Interestingly, failure
rates within edentulous patients were almost double those for partially dentate patients (7.6% versus
3.8%). In addition, failure in the edentulous maxilla
was approximately three times higher compared to
the edentulous mandible.8
Peri-implantitis is considered an inflammatory
process affecting the tissues around an osseointegrated implant in function, resulting in loss of
supporting bone.15 Signs of a failing dental implant
are detected both clinically and radiographically
with the diagnosis made in a similar way to
periodontitis.16 This involves measuring clinical
parameters including peri-implant loss of gingival
attachment, bleeding on probing, plaque/gingivitis
indices, suppuration and mobility. Other relevant
assessments include a peri-implant radiographic
examination and microbiological sampling. Periimplantitis has been reported in 5e8% of cases
within selected implant systems.17

Classification of failures
Implants can be described as failing or failed. A
failing implant demonstrates a progressive loss of
supporting bone but is clinically immobile,
whereas a failed implant is clinically mobile.18
When an implant has failed, removal is recommended while a failing implant may be salvaged if it is
diagnosed early and treated appropriately.19,20
Implant failures may also be categorised as early
or late. Early failures occur before osseointegration
and prosthetic rehabilitation has taken place with
late failures occurring afterwards.13 Factors affecting early failure of dental implants may be broadly
classified as: implant-, patient- and surgical technique/environment-related (Table I). Late failures

106

A.D. Pye et al.

Table I Factors related to the failure of dental


implants21e27
Factor

Comment

Implant

Previous failure
Surface roughness
Surface purity and sterility
Fit discrepancies
Intra-oral exposure time
Premature loading
Mechanical
Traumatic occlusion due to inadequate
overloading restorations
Oral hygiene
Patient (local Gingivitis
factors)
Bone quantity/quality
Adjacent infection/inflammation
Presence of natural teeth
Periodontal status of natural teeth
Impaction of foreign bodies (including
debris from surgical procedure) in the
implant pocket
Soft tissue viability
Vascular integrity
Smoking
Patient
Alcoholism
(systemic
Predisposition to infection, e.g. age,
factors)
obesity, steroid therapy, malnutrition,
metabolic disease (diabetes)
Systemic illness
Chemotherapy/radiotherapy
Hypersensitivity to implant
components
Surgical trauma
Surgical
Overheating (use of handpiece)
technique/
environment Perioperative bacterial
contamination, e.g. via saliva, perioral
skin, instruments, gloves, operating
room air or air expired by patient

usually concern a small number of patients with their


aetiology less well understood.21 Late failures may
be subclassified into lateeearly or lateedelayed depending on whether they occur during or after the
first year of loading. Late-delayed failures are likely
due to changes in loading conditions in relation to
the quality/volume of bone and peri-implantitis.22
The likelihood of bacteria producing infection depends on their virulence and host factors.28
While the above factors relate to the failure of
implants with regard to their anchorage in bone,
occasionally the infectious process is limited to the
soft tissues overlying the healing implant site causing
peri-implant mucositis.20 An implant compromised
by soft-tissue problems has a more favourable prognosis than one undergoing bone loss.29 Nevertheless,
infection originating in the soft tissues may potentially progress deeper into the bone and undermine

the osseointegration process. Some of the most frequent causes of soft tissue infection during the healing period involve residual suture material, poorly
seated cover screws, protruding implants and trauma
from inadequately relieved dentures or occlusal
trauma from opposing teeth.19

Microbiology of failing dental implants


Infection represents one of many factors contributing to the failure of dental implants. Presently,
no single micro-organism has been closely associated with colonisation or infection of any implant
system.30
Failing dental implants are associated with
a microbial flora traditionally associated with
periodontitis. Thus, a transition is observed from
a predominately Gram-positive non-motile, aerobic and facultative anaerobic composition towards
a flora with a greater proportion of Gram-negative,
motile, anaerobic bacteria.31e34 If this predominates for significant time periods then peri-implantitis and eventual implant failure may result.35
Table II highlights studies investigating the microbiology of failing implants.
Interestingly, micro-organisms not usually associated with periodontitis or dental abscesses such as
staphylococci, coliforms and Candida spp. are commonly isolated from peri-implant lesions in some
studies.31,32,41 Staphylococci are present within
the oral cavity and their isolation from peri-implant
infection is significant as both Staphylococcus
aureus and coagulase-negative staphylococci are
frequently responsible for infections associated
with metallic biomaterials and indwelling medical
infections in general.42,43 More recently, Staphylococcus aureus has been demonstrated to have the
ability to adhere to titanium surfaces. This may be
significant in the colonisation of dental implants
and subsequent infections.44

Guidelines for the placement of dental


implants
There are few published guidelines on infection
control during the placement of dental implants.
Those available advocate that the surgical field
should be isolated and free of contamination.45,46
This is clearly not readily achievable within the oral
cavity. However, it has been elucidated that contamination of the operative site by patients saliva does
not preclude success.47 Additionally, no significant
differences were found in osseointegration success
rates for implants placed under controlled operating

Dental implants and infection


Table II

107

Summary of studies investigating microbiology of failing implants

Type of implant
(no. of patients/implants)

Method of detection

Bra
nemark
(37/1e4 per patient)32

Culture

Not stated
(41/not stated)33

Culture/indirect
immunofluorescence

Titanium hollow cylinder


implants (7/not stated)34
Not stated (13/20)36
Not stated (21/28)37
IMZ (12/18)38

Culture/dark field
microscopy
Culture
Checkerboard DNAeDNA
hybridization technique
Culture

Various (10/12)39

PCR

9 Astra
16 Bra
nemark
5 ITI
Staumann (17/30)40

Culture

Most prevalent microbes detected


(% sites infected with bacteria)
Prevotella intermedia/P. nigrescens 60%
Actinobacillus actinomycetemcomitans 60%
Staphylococci, coliforms, Candida spp. 55%
Bacteroides forsythus 59%
Spirochetes 54%
Fusobacterium spp. 41%
Peptostreptococcus micros 39%
Porphyromonas gingivalis 27%
Bacteroides spp., Fusobacterium spp., spirochetes,
fusiform bacilli, motile and curved rods (% not stated)
Staphylococcus spp. 55%
P. nicrescens, P. micros, Fusobacterium
nucleatum (% not stated)
Bacteroides spp. 89%
Actinobacillus actinomycetemcomitans 89%
Fusobacterium nucleatum 22%
Capnocytophaga spp.
27.8% Eikenella corrodens 17%
Porphyromonas gingivalis 67%
Campylobacter rectus 42%
Eikonella corrodens 42%
Treponema denticola 42%
Prevotella intermedia 33%
Tannerella forsythia 33%
Actinobacillus actinomycetemcomitans 17%
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.

theatre conditions compared to a less environmentally controlled dental school clinic.48 This may imply
that the operative environment is not as critical to
the success of dental implants compared to implant
placement within other body sites. Several strategies
to reduce contamination from the oral flora during
surgery have been postulated.49,50 One such strategy
involves rinsing preoperatively with chlorhexidine as
this may reduce microbial complications following
implant placement.51 An in-vivo study showed that
chlorhexidine in suspension form is more effective
in inhibiting Porphyromonas gingivalis than the use
of antibiotics.52 Others, however, failed to reach
these conclusions.53
During the surgical procedure, the implant
should be stored in the manufacturers sterile
packaging and only used in conjunction with the
recommended instruments. Previously, the drills
used for bone preparation were not designated
single use and were decontaminated according to

local protocols. Manufacturers are gradually


introducing single-use drills for use with their
implant systems.

The role of antibiotics


The use of prophylactic antibiotics during implant placement remains controversial. A Cochrane review found insufficient evidence
advocating or dissuading their use.54 An update
of the review, however, determined there was
some evidence that 2 g of amoxicillin given
orally 1 h preoperatively significantly reduced
early failures of dental implants.55 The review
concluded by recommending the routine use of
one dose of 2 g of prophylactic amoxicillin immediately prior to placing dental implants. However, it also stated that further research was
required to confirm the findings.

108
Table III Suggested treatments for infected dental
implants20,29,57
Mechanical debridement
Pharmaceutical treatment e irrigation with
chlorhexidine, local antibiotics (e.g. tetracycline
fibre) and systemic antibiotics
Surgical procedures e open flap debridement (to
decontaminate and smooth the implant surface)
Correct anatomical conditions that impair plaque
control and encourage the formation of an anaerobic
environment (includes both resective procedures and
regenerative techniques such as guided tissue
regeneration)

At present, there is no reliable evidence for the


most successful method of treating peri-implantitis.56 Despite a variety of therapeutic options
(Table III), infected implants are difficult to treat
and usually require removal.21 Some clinicians
advise systemic antibiotics for the treatment of
failing implants and a variety of drug regimens
are described.58 Oral agents such as doxycycline,
clindamycin, co-amoxiclav, penicillin V, amoxicillin and a combination of amoxicillin and metronidazole have been recommended. Nevertheless,
no double-blind, randomised, placebo-controlled
trial has been undertaken.

Monitoring of success/failure
In the UK there are no surveillance programmes in
place providing epidemiological data on the microbiology, success and failure rates of dental implants.
Conversely, in Finland an Implant Register provides
comprehensive data on the number of implants
inserted and removed together with any complications related to the treatment.14 The programme
strives to ensure safe treatment for patients and
has been operational for nearly 20 years.

Conclusion
Dental implants are an increasingly common form of
prosthetic device implanted into patients. The
apparent high success rate for the placement of
endosseous dental implants under uncontrolled environmental conditions and through a heavily colonised oral environment appears counterintuitive. If
dental implants become infected the causative
micro-organisms are usually those implicated in
periodontal disease and include a range of Gramnegative anaerobes and spirochaetes. Since
S. aureus and coliforms are infrequently detected

A.D. Pye et al.


in oral infection, their presence at implant infection
sites may represent cross-infection episodes
although further data are required to support this.
As occurs with orthopaedic implants, infected dental
implants are difficult to treat and removal is frequently required.
Data on failure and complications of dental
implants should be collected and reported in
a systematic fashion. This would enable a more
detailed analysis of the microbiology, treatment
outcomes and assist in the formulation of clinical
guidelines in implant placement and treatment of
implant-associated infections. Concerns have been
raised over the efficacy of dental instrument decontamination, and this, coupled with the highly
invasive nature of the insertion of dental implants,
suggests that the introduction of a generic surveillance programme with appropriate microbiological
monitoring should be urgently considered.
Conflict of interest statement
None declared.
Funding sources
None.

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