A review of dental implants and infection

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 b Infection Research Group, Glasgow Dental Hospital and School, Faculty of Medicine, Glasgow University, Glasgow, UK 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. Theroleof 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. ª 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.: þ44 0141 211 9747; fax: þ44 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 ª 2009 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.jhin.2009.02.010

Dental implants and infection 105 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. Brånemark 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 Brånemark 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 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 Brånemark 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 implants 21e27 Factor Implant Mechanical overloading Patient (local factors) Patient (systemic factors) Surgical technique/ environment Comment Previous failure Surface roughness Surface purity and sterility Fit discrepancies Intra-oral exposure time Premature loading Traumatic occlusion due to inadequate restorations Oral hygiene Gingivitis 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 Alcoholism Predisposition to infection, e.g. age, obesity, steroid therapy, malnutrition, metabolic disease (diabetes) Systemic illness Chemotherapy/radiotherapy Hypersensitivity to implant components Surgical trauma Overheating (use of handpiece) 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 patient s 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 107 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) Brånemark Culture Prevotella intermedia/p. nigrescens 60% (37/1e4 per patient) 32 Actinobacillus actinomycetemcomitans 60% Staphylococci, coliforms, Candida spp. 55% Not stated (41/not stated) 33 Culture/indirect immunofluorescence Bacteroides forsythus 59% Spirochetes 54% Fusobacterium spp. 41% Peptostreptococcus micros 39% Porphyromonas gingivalis 27% Titanium hollow cylinder implants (7/not stated) 34 Culture/dark field microscopy 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 technique P. nicrescens, P. micros, Fusobacterium nucleatum (% 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 Astra 16 Brånemark 5 ITI Staumann (17/30) 40 PCR, polymerase chain reaction. 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% 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 manufacturer s 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 A.D. Pye et al. Table III implants 20,29,57 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 Suggested treatments for infected dental 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) 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 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. References 1. Mupparapu M, Beideman R. Imaging for maxillofacial reconstruction and implantology. In: Fonseca RJ, editor. Oral and maxillofacial surgery: reconstructive and implant surgery. Philadelphia: Saunders; 2000. p. 17e34. 2. Worthington P. Introduction: history of implants. In: Worthington P, Lang BR, Rubenstein JE, editors. Osseointegration in dentistry: an overview. 2nd ed. Illinois: Quintessence; 2003. p. 2. 3. Brånemark PI. Osseointegration and its experimental background. J Prosthet Dent 1983;50:399e410. 4. Hobo S, Ichida E, Garcia LT. Osseointegration and occlusal rehabilitation. Tokyo: Quintessence; 1990. pp. 3e4. 5. Brunski JB. In vivo response to biomechanical loading at the bone/dental implant interface. Adv Dent Res 1999;13:99e119. 6. Jokstad A, Brägger U, Brunski JB, Carr AB, Naert I, Wennerberg A. Quality of dental implants. Int Dent J 2003; 53:409e443. 7. Adell R, Lekholm U, Rockler B, Brånemark PI. A 15-year study of osseointegrated implants in the treatment of the edentulous jaw. Int J Oral Surg 1981;10:387e416. 8. Esposito M, Hirsch JM, Lekholm U, Thomsen P. Biological factors contributing to failures of osseointegrated implants (I). Success criteria and epidemiology. Eur J Oral Sci 1998; 106:527e551. 9. Quirynen M, De Soete, van Steenberghe D. Infectious risks for oral implants: a review of the literature. Clin Oral Implants Res 2000;13:1e19. 10. Brånemark PI, Adell R, Breine U, Hansson BO, Lindstrom J, Ohlsson A. Intraosseous anchorage of dental prostheses. I. Experimental studies. Scand J Plast Reconstr Surg 1969;3:81e100. 11. Hansson HA, Albrektsson T, Brånemark PI. Structural aspects of the interface between tissue and titanium implants. J Prosthet Dent 1983;50:108e113.

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