Biofilm Related to Dental Implants - EndoExperience

Biofilm Related to Dental ImplantsAngie Lee, DMD,* and Hom-Lay Wang, DDS, MSD, PhD†

Although bacteria are often per-ceived as being harmful to thehuman body causing diseases

such as syphilis and tuberculosis, it isimportant to note that periodontal dis-eases are infections that originate fromindigenous bacteria. Disease occurswhen the harmony between the hostand the microbiota is disrupted, partic-ularly in a susceptible host or when themicroorganism is highly pathogenic.

Peri-implant diseases comprise in-flammatory reactions in the host tissuesand include peri-implant mucositis orperi-implantitis. Peri-implant mucositis,also called “ailing implant,” is definedas a reversible inflammation localized tothe soft tissues with no signs of support-ing bone loss.1–4 Peri-implant mucositismay resolve by itself or persist for anundetermined period of time withthe possibility of developing peri-implantitis and implant failure. Peri-implantitis refers to a destructiveinflammatory reaction with evidence ofloss of supporting bone around a failingbut functional implant.1–3,5 A failed im-plant is defined as one that exhibits clin-ical mobility, pain on function, boneloss more than half of the total length ofthe implant, or uncontrolled exudate.6

The timing at which implant fail-ures occur represents different physi-

ological processes. Hence, an earlyimplant failure indicates an initial lackof osseointegration due to an inabilityto establish an intimate bone-to-implant contact. Various factors maycontribute to early implant failuressuch as premature loading, surgicaltrauma, or impaired healing re-sponse.7,8 Late failure, on the otherhand, occurs after initial integration,physiological remodeling, and load-ing. Causes of late failures includeoverloading and bacterial infection(e.g., peri-implantitis)9 with most fail-ures occurring after the first year ofloading.10,11 In fact, biofilms havebeen associated with almost 65% ofinfectious diseases such as periodontaland peri-implant diseases.12

Because the role of bacterial bio-film in peri-implant diseases has beenrecognized, knowledge of the micro-biology around dental implants is theessence of adequate diagnosis andtreatment of these diseases. This arti-cle focuses on understanding the de-velopment of oral biofilms arounddental implants and their role in peri-implant diseases.

BIOFILM FORMATION AROUNDDENTAL IMPLANTS

After exposure of an osseointe-grated implant in the oral cavity througha transmucosal abutment, an acquiredpellicle is formed on the implant surface

through selective adsorption of the en-vironmental macromolecules such as�-amylase andserum albumin.13 This pellicle is derivedfrom components in the saliva, as wellas bacterial and host tissue products. Itacts as a substrate for bacterial coloni-zation, which occurs as early as 30 min-utes after implant exposure in the oralcavity.14 In comparison to natural teeth,the acquired pellicle on dental implantshas a lower albumin adsorption capabil-ity, which according to some authorscontributed to the lower plaque forma-tion around implants.15

Biofilm represents an organizedstructure in which microorganisms in-teract metabolically as a community.

Biofilm formation around im-plants occurs in a similar way as teeth.After formation of the acquired pelli-cle, bacterial attachment with initialcolonizers followed by cell-to-cell ad-hesion with secondary colonizers oc-curs on the implant surface.16 Biofilmsare the preferred method of growth formost bacteria because they facilitateexchange of nutrients and protect thebacterial community from competingmicroorganisms.17 Moreover, biofilmsalso contribute to the spread of antibi-otic resistance.16

PERI-IMPLANT HEALTH

Peri-implant health is defined as animplant that demonstrates no mobility,

*Resident, Department of Periodontics and Oral Medicine,School of Dentistry, University of Michigan, Ann Arbor, MI.†Professor and Director of Graduate Periodontics, Departmentof Periodontics and Oral Medicine, School of Dentistry,University of Michigan, Ann Arbor, MI. Research Advisor, Eng.A.B. Research Chair for Growth Factors and BoneRegeneration, King Saud University Riyadh, Saudi Arabia.

Reprint requests and correspondence to: Hom-LayWang, DDS, MSD, PhD, Department of Periodonticsand Oral Medicine, University of Michigan School ofDentistry, 1011 North University Avenue, Ann Arbor,MI 48109-1078, Phone: (734) 763-3383, Fax: (734)936-0374, E-mail: [email protected]

ISSN 1056-6163/10/01905-387Implant DentistryVolume 19 • Number 5Copyright © 2010 by Lippincott Williams & Wilkins

DOI: 10.1097/ID.0b013e3181effa53

Oral biofilm-related diseases suchas periodontal and peri-implant dis-eases are unique infections in that theydevelop from the resident indigenousmicroflora. As more implants arenowadays being placed, cliniciansmay encounter more complications.Therefore, understanding the etiologyis warranted to establish adequate

diagnosis and provide proper treat-ment. This article focuses on under-standing peri-implant microbiologyand its roles in peri-implant diseases.(Implant Dent 2010;19:387–393)Key Words: implant, microbiology,bacteria, peri-implantitis, peri-mucositis, biofilm

IMPLANT DENTISTRY / VOLUME 19, NUMBER 5 2010 387

�2 mm of radiographic bone loss fromthe initial surgery with no pain on func-tion or history of exudate.18 Similar tothe healthy periodontium around naturalteeth, the microorganisms associatedwith healthy implants are predominantlyGram-positive cocci and rods microor-ganisms.14,19–23 The dominant speciesare members of the yellow and purplecomplexes or are independent of thecomplexes such as Actinomycesnaeslundii or Actinomyces viscosus.24–26

Gram-negative bacteria can be found insmaller proportions and include Pre-votella intermedia, Porphyromonas gin-givalis, Tannerella forsythia, Prevotellanigrescens, and Campylobacter rectus.24

This suggests that certain species areindigenous, host-compatible organisms.

As demonstrated in an experimen-tally induced peri-implant mucositisstudy in humans, plaque accumulationand development of peri-implant mu-cositis were comparable at implant andnatural teeth sites.27,28 Interestingly, witha similar amount of plaque accumula-tion, implant sites had increased hostresponse and proinflammatory cytokineproduction compared with that found inteeth,29,30 suggesting that implants mayact as a foreign body.

Moreover, the composition of thesupra- and submucosal microflora issimilar around healthy implants.31 Onthe other hand, bacterial species in thesupra- and subgingival plaque aroundteeth are rather different. The subgingi-val microflora is initially derived fromthe supragingival plaque and becomesmore anaerobic as the oxygen pressurein the environment is reduced.32 The su-pragingival plaque around teeth couldserve as a reservoir to spread or reinfectsubgingival sites.33,34

TRANSITION FROM HEALTH TOPERI-IMPLANT DISEASES

An adequate permucosal seal ofthe soft tissue to the implant surfaceprotects the base of the sulcus againstthe penetration of chemical and bacte-rial substances. With the loss of thisinitial seal, the peri-implant mucosamay progress from health to mucositisand possibly to peri-implantitis. As theperi-implant tissues undergo the pro-cess from a state of health to that ofdisease, differences in bacterial num-

bers and morphotypes can be found. Ashift from a Gram-positive facultativedominated flora to a Gram-negativeanaerobic biofilm occurs.19

The failing implant is character-ized by a greater proportion of red (P.gingivalis, Treponema denticola, andT. forsythia) and orange (P. interme-dia and Fusobacterium nucleatum)complex, as well as Aggregatibacteractinomycetemcomitans and Eikenellacorrodens with a lower proportion ofthe flora associated with health.9,31,35–39

Hence, the main differences betweenhealth and disease are in the propor-tions of Actinomyces, orange and redcomplex species. Furthermore, in-creasing peri-implant probing depthhas been significantly associated withhigher total anaerobic cultivable mi-crobiota and the frequency of detec-tion of P. gingivalis.40

Van Winkelhoff et al studied theearly colonization of the peri-implantpockets by putative periodontal patho-gens in 20 partially edentulous patients.The authors found that most periodontalpathogens (P. gingivalis, F. nucleatum,P. intermedia, and T. forsythia) werealready identified as early as 6 monthsafter loading. In particular, P. gingivaliswas significantly associated with thepresence of fistulas and implant loss.The study also demonstrated that al-though 2 patients exhibited A. actinomy-cetemcomitans during their baselineexamination, A. actinomycetemcomitanswas not isolated from any implantpocket during the experimental period.41

Other microorganisms such asStaphylococcus aureus, Candida albi-cans, and enteric rods have also beenassociated with peri-implantitis.26,38,42,43

S. aureus has high adhesion to titaniumsurfaces,44 and its presence has been as-sociated with suppuration and bleedingon probing.45 C. albicans is the mostcommon fungus found in the oral cavity,and its presence is strongly associatedwith oral candidiasis especially in pa-tients wearing dentures.46,47 C. albicanshas high adhesion to dental implants46

although an in vitro study showed lowerlevels of this microorganism on sand-blasted titanium surfaces.43 Infection ofdental implants with these opportunisticmicroorganisms should be recognized

especially in the immunocompromisedpatient.48

HISTORY OF PERIODONTITIS

Because the implicated microor-ganisms are essentially periodontalpathogens, are patients with a history ofchronic periodontitis at higher risk forperi-implantitis? As discussed previ-ously, the microbiota associated withhealthy and failing implants are similarto the one observed in periodontal healthand disease around the teeth.19,24,49 Theindigenous oral bacteria on the remain-ing teeth serve as reservoirs for coloni-zation on the implant surface, whichexplains the similarity of the biofilmcomposition around implants and natu-ral teeth within the same individual.50–55

In periodontally susceptible patients, thecoexistence of teeth and implants createa local environment in which subgingi-val periodontal pathogens around teethcan cause disease around the implant.56

Recent systematic reviews agreedthat a history of periodontitis repre-sents an increased risk for implant fail-ure, with odds ratios ranging between3.1 and 4.7.57–59 In a 10-year prospec-tive study, Karoussis et al60 evaluatedthe incidence of peri-implantitis in 53patients. Subjects with a history ofchronic periodontitis showed a higherincidence of peri-implantitis (28.6%)in comparison with subjects withoutprevious periodontitis. In agreementwith Karoussis et al, Lee et al24 alsofound that subjects with a history ofperiodontal disease harbored in-creased periodontal pathogens.

In contrast to these findings, Elle-gaard et al61 concluded that implantsuccess remains high (95%) inperiodontally compromised patientsexhibiting good oral hygiene. In a lon-gitudinal study of partially edentulouspatients treated for generalized aggres-sive and chronic periodontitis, Mengelet al examined the microflora after 5 and3 years of implant placement, respec-tively. Healthy conditions around bothteeth and implants were found with asimilar distribution of the microorgan-isms.62 It seems that important factors toconsider in the success of implants aregood oral hygiene, treatment of peri-odontal condition, and appropriate peri-odontal maintenance program.63– 66

388 BIOFILM RELATED TO DENTAL IMPLANTS • LEE AND WANG

Patients with a history of chronic peri-odontitis may still be at increasedrisk for peri-implant diseases be-cause of host-related factors.67 As aconsequence, adequate periodontalinfection control is important beforedental implant placement to helpprevent bacterial complications.41

SURFACE ROUGHNESS

Increased surface roughness hasbeen associated with increased os-seointegration of the dental implant.68–70

Conversely, a higher surface roughnesswith a Ra value �0.2 � increases bio-film formation71,72 and thus contributesto spontaneous progression of peri-implantitis lesions.65,73–75 Berglundh etal75 performed an experimental study indogs and showed that increased plaqueand faster progression of peri-implantitiswere found in rough surface comparedwith polished machined surface im-plants. In agreement with Berglundh etal, Amarante et al76 found that machinedsurface implants harbored significantlyless bacteria than plasma-sprayed im-plants and had increased amount ofStreptococcus sp. compared withbrushed surfaces.

Abutment surface roughness mayalso impact the accumulation of biofilm.With increasing abutment surfaceroughness, higher supramucosal plaqueaccumulation is noted.77 Quirynen et alexamined 9 patients and found that abut-ments with a rough surface harboredmore bacterial pathogens and less coc-coid microorganisms than that onsmooth surfaces. In fact, up to 25 timesmore bacteria was found in the su-pramucosal plaque of rough abutmentscompared with smooth abutment.78 In-terestingly, this increase is not observedin submucosal areas, suggesting thatperiodontal pathogens in this area weremore influenced by the patient’s oralhygiene rather than surface texture.77,78

Although a relationship betweensurface roughness and plaque forma-tion has been assessed, other authorsreported conflicting results. Martins etal79 conducted an experimental peri-implantitis study in dogs, and theirdata suggested that different surfaceroughness implants were equally sus-ceptible to the accumulation of plaqueand to peri-implantitis. In addition,

Esposito et al4 in a literature reviewconcluded that roughened implantabutment surfaces caused by differentmaintenance techniques were not as-sociated with increased implant com-plications. It seems from these studiesthat the impact of surface roughness isdependent on the individual patient,with personal and professional oralhygiene exerting a great influence.

TREATMENT INFLUENCEON MICROBIOTA

Treatment of dental implant-associated infections consists of an anti-infective protocol that can be achievedthrough mechanical debridement of theimplant surface or chemical treatmentincluding local and systemic antibiotics.The selected treatment modality de-pends on the established diagnosisof peri-implant mucositis or peri-implantitis. Treatment success is as-sessed using outcome measures such asreduction of inflammation, probingdepth, and pathogenic bacteria.80 None-theless, the presence of a specific bacte-ria had little or no value in predictingtreatment failure.81

In a recent literature review, non-surgical mechanical therapy was effec-tive in treating peri-implant mucositiswith improved results observed in con-junction with an antimicrobial mouthrinse.12 A reduction in the proportion ofpathogenic species after mechanicaltherapy has been reported.82

However, nonsurgical treatmentof sites with peri-implantitis was notfound to be effective at reducing in-flammation, pathogenic microorgan-isms, and bleeding on probing.12 Theaddition of antimicrobial mouth rinsein this nonsurgical treatment of peri-implantitis only provided minimalbeneficial effects.12,83 On the otherhand, the use of local drug deliverysuch as minocycline and tetracyclineto treat peri-implantitis has generatedreduced levels of T. forsythia, P. gin-givalis, and T. denticola, with the mosteffect on A. actinomycetemcomitans.81

After surgical treatment of sites withperi-implantitis such as open debride-ment, a reduction in the proportion ofred complex species was observed.82

In the past decades, laser therapysuch as diode, CO2, and Er:YAG laser

has gained popularity based on therationale of surface decontamination,hemostatic properties, calculus re-moval, and bactericidal effects.84 – 86

However, only minor clinical and mi-crobiological improvement has beenreported.12,87 Further studies are man-dated to evaluate the beneficial effectsof laser therapy.

CONCLUSION

Implant complications have signifi-cant health and financial implications toboth the patient and clinician. Peri-implantitis has a multifactorial etiologyin which oral biofilm is a recognizableetiologic agent. It is well demonstratedthat the combination of multiple patho-genic bacteria increases the risk ofperi-implant diseases and can better de-termine disease activity rather than theidentification of a single microorgan-ism.52,88 The reduction of the bacterialload to a level compatible with health isan important aspect of implant therapy.With the emergence of new technolo-gies, identification of bacteria in the oralcavity continues to improve. It is likelythat new pathogens may emerge fromuncultured microorganisms.

Disclosure

The authors claim to have no fi-nancial interests, either directly or in-directly, in the products or informationlisted in the article.

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Abstract Translations

GERMAN / DEUTSCHAUTOR(EN): Angie Lee, DMD, Hom-Lay Wang, DDS,MSD, PhDBiofilm in Verbindung mit Zahnimplantaten

ZUSAMMENFASSUNG: Erkrankungen in Verbindung mitoralem Biofilm, so wie beispielsweise Erkrankungen desZahnbetts und des Implantatumfelds sind spezifische Infek-tionen dadurch, dass sie sich aus der ureigenen Mikrofloraentwickeln. Da heutzutage haufiger Implantate eingepflanztwerden, kann es auch fur die behandelnden Kliniker zu mehrKomplikationen kommen. Daher ist ein Verstandnis der Ati-ologie erforderlich, um eine entsprechende Diagnose vorne-hmen und richtig diagnostizieren und behandeln zu konnen.Die vorliegende Arbeit konzentriert sich auf die Vermittlungeines Verstandnisses der Mikrobiologie im das Implantatumgrenzenden Gewebe sowie dessen Beteiligung anErkrankungen im das Implantat umlagernden Gewebe.

SCHLUSSELWORTER: Implantat, Mikrobiologie, Bakte-rien, Peri-Implantitis, Peri-Mukositis, Biofilm

SPANISH / ESPAÑOLAUTOR(ES): Angie Lee, DMD, Hom-Lay Wang, DDS,MSD, PhDBiopelícula relacionada a los implantes dentales

ABSTRACTO: Las enfermedades relacionadas con la biopelículaoral tales como las enfermedades periodontales y periimplante soninfecciones especiales ya que aparecen de la microflora indígenaresidente. A medida que se colocan mas implantes en la actualidad,los clínicos podrían encontrar mas complicaciones. Por lo tanto,entender la etiología es necesario para poder establecer un diagnos-tico adecuado y ofrecer un tratamiento correcto. Este trabajo seconcentra en entender la microbiología periimplante y sus papelesen las enfermedades periimplante.

PALABRAS CLAVES: Implante, microbiología, bacteria,periimplantitis, perimucositis, biopelícula

PORTUGUESE / PORTUGUÊSAUTOR(ES): Angie Lee, Doutora em Medicina Dentaria, Hom-Lay Wang, Cirurgia-Dentista, Mestre em Odontologia, PhDBiofilme Relacionado a Implantes Dentarios

RESUMO: As doencas orais relacionadas a biofilme tais comoas doencas periodontais e de peri-implante sao infeccoes unicaspelo fato de que se desenvolvem a partir da microflora residentenativa. A medida que mais implantes estao sendo colocados hoje

em dia, os clínicos podem encontrar mais complicacoes. Por-tanto, entender a etiologia e justificado a fim de estabelecerdiagnostico adequado e fornecer tratamento apropriado. Esteartigo focaliza o entendimento da microbiologia de peri-implante e seus papeis em doencas de peri-implante.

PALAVRAS-CHAVE: Implante, microbiologia, bacterias,peri-implantite, perimucosite, biofilme

RUSSIAN /��: Angie Lee, �� , Hom-LayWang, �� , ��, ��

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TURKISH / TURKCEYAZARLAR: Angie Lee, DMD, Hom-Lay Wang, DDS,MSD, PhDDental Implantlar ile Baglantılı Biyofilm

OZET: Periodontal ve peri-implant hastalıklar gibi oral biyo-film ile baglantılı hastalıklar, olgunun kendi dogal mikrofloras-ından gelistikleri icin benzersiz enfeksiyonlardır. Gunumuzdeimplant uygulaması daha da sıklastıgından klinisyenlerin dahafazla komplikasyonlar ile karsılasmaları olasıdır. Bu nedenle,tanının yeterli ve tedavinin uygun olabilmesi icin etyolojininanlasılması gerekir. Bu yazı, peri-implant mikrobiyolojisini vebunun peri-implant hastalıklarındaki rolunu anlamak amacıylatasarlandı.

ANAHTAR KELIMELER: Implant, mikrobiyoloji, bakteri,peri-implantit, peri-mukozit, biyofilm


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Biofilm Related to Dental Implants - EndoExperience