J Clin Periodontol 1999; 26: 313–317 Copyright C Munksgaard 1999Printed in Denmark . All rights reserved

ISSN 0303-6979

Case ReportØ. Fardal 1, A. C. Johannessen 2 andI. Olsen 3Severe, rapidly progressing1Private Practice, 4370 Egersund, Norway,2Department of Odontology,Oral Pathologyand Forensic Odontology, University ofperi-implantitis Bergen, Norway; 3Department of OralBiology, Dental Faculty, University of Oslo,Norway

Fardal Ø, Johannessen AC, Olsen I: Severe, rapidly progressing peri-implantitis.J Clin Periodontol 1999; 26: 313–317. C Munksgaard, 1999.

Abstract. The replacement of teeth by means of titanium implants is a safe andpredictable procedure in most patients. Some studies show that a small numberof patients lose the majority of their implants. Unfortunately, it is impossible toidentify these patients prior to surgery. It is important to report such cases so thatwe may, in the future, be able to identify them before surgery. The present case

Key words: peri-implantitis; severe earlyshowed a severe and rapid exfoliation of titanium implants. Out of 8 implants onsetinserted in the anterior lower jaw of this patient, only two maintained osseointe-gration over a 2-year period. Accepted for publication 4 August 1998

Surgical placement of implants in thejaws represents a predictable procedurefor replacing lost teeth. For well-docu-mented implant systems, long-term suc-cess rates of 85–100% have been re-ported. Especially high success rateshave been found for implants placed inthe anterior mandible (Adell et al. 1981,Kent et al. 1990, Lekholm et al. 1994).The majority of failures occur betweenthe time of implant installation and the2nd stage surgery or soon after loading(Quirynen et al. 1991).

Early failures have been attributed tosurgical trauma, inadequate bone qual-ity and quantity, lack of primary sta-bility, transmucosal loading duringhealing, premature loading after un-covering, and bacterial contaminationof the recipient site (Baumgarten &Chiche 1995). Some studies (Apse et al.1989, Quirynen & Listgarten 1990, Pa-paioannou et al. 1996) have suggestedthat micro-organisms from periodontalpockets around natural teeth may serveas a reservoir for the colonisation of thesubgingival environment of implants inpartially edentulous patients. This ar-ticle presents a case of refractory mar-ginal periodontitis involving the naturalteeth and with a marked exfoliative re-action to dental implants.

Case Report

The patient was a 45-year-old femaleCaucasian. Her medical history re-vealed no significant findings exceptthat she was a heavy smoker (10–15cigarettes/day). Her dental history in-cluded lengthy periodontal and restora-tive/prosthetic therapy. She reported asevere familial periodontal problemwith both parents becoming edentulousat an early age and periodontal prob-lems in all siblings (one brother and twosisters). She was referred for specialistperiodontal therapy 17 years ago.

In spite of periodontal therapy, goodplaque control, regular maintenancecare and minimal marginal inflam-mation, the periodontal attachmentloss continued over the next 17 years,resulting in increasing mobility of herteeth. The maxillary arch was stabilisedwith the help of a full bridge from teeth16 to 25. After 17 years, all the remain-ing teeth in the lower jaw had grade 2–3mobilities and were given the diagnosisterminal periodontitis (Fig. 1).

At this time, she requested that herlower teeth be removed and replacedwith implants. It was decided to removeall the teeth except 31, 41 and 37 at thetime of implant surgery. These teeth

were kept temporarily to give retentionfor a partial denture. 5 implants wereinserted in the following areas: 33, 34,42, 43, 44. The implants used were No-belpharma MK II 3.75 mm in diameterand 13 mm in length. Standard surgerywas carried out using Citanest Octap-ressin and Xylocain-Adrenalin local an-aesthetics. The implants were placedwithout complications. Phenoxymethyl-penicillin V 660 mg was prescribed 4¿/day for 1 week. Sufficient pain killersfor the patient’s needs were also pre-scribed (paracetamol/codeine). 2¿ dailychlorhexidine digluconate 0.2% wasused throughout the treatment period.Sutures were removed after 2 weeks.Healing progressed uneventfully withlittle or no discomfort for the patient;all the implants remaining covered withsoft tissue. No surface areas of the par-tial denture were left in contact with thesoft tissues over the implants. The den-ture was not worn for the initial 4weeks, and thereafter only for ‘‘socialevents’’. She was advised that smokingcould adversely affect the success of im-plant therapy and asked to stop or re-duce her smoking habit. After 6 weeks,the patient contacted the dental officeby phone because of sudden pain andbilateral swellings in the anterior lower

314 Fardal et al.

jaw. She was seen a few hours laterwhen implants 33, 43 and 44 were half-way out of the oral mucosa and couldbe removed with a pair of tweezers (Fig.2). The bone surrounding the failingimplants showed a marked verticalbone loss.

The involved areas were swollen with

Fig. 1. Pre-treatment panoral view of the patient. Fig. 4. Helper/inducer T-cells (CD4π) (original magnification ¿64).

Fig. 2. Photograph showing implant (33) in the process of exfoliation. Fig. 5. Suppressor/cytotoxic T-cells (CD8π) in the corresponding areaas in Fig. 4 (original magnification ¿64).

Fig. 3. T-cells (CD3π) located subadjacent to the epithelium sur- Fig. 6. B-cells (CD19π) located in the connective tissue stroma, espe-rounding one of the rejected implants (original magnification ¿48). cially perivascularly (original magnification ¿76).

pus. The remaining 2 implants were ex-posed but remained firm.

At the next visit 1 month later, theremaining implants seemed to be wellintegrated as determined by firmness,percussion tests, absence of tendernessto counter-torque, X-ray investigationsand absence of marginal inflammation.

2 months later, a 10 mm¿3.75 mmD MK II Nobelbiocare implant wasplaced surgically in the 33 region (33,2)and a 13 mm¿3.75 mm D MK II Nob-elbiocare implant was placed in the 43region. Phenoxymethylpenicillin V 660mg tablets were prescribed for 1 week.Sutures were removed 2 weeks post-op-

Peri-implantitis 315

Table 1. Specificities and dilutions of monoclonal antibodies (Mab) used

Mab Antigen Cell specificity

Leu 41 CD3 T cellsLeu 3aπ3b1 CD4 Helper/inducer T cellsLeu-2a1 CD8 Suppressor/cytotoxic T cellsLeu-121 CD19 B cells

OKM1 CD68 monocytes/macrophages1 Becton Dickinson, Mountain View, CA, USA.2 Ortho diagnostic System Inc, Raritan. NJ USA.

eratively and no complications werenoted. However, at this stage, the pa-tient complained of a gingival swellingin association with tooth 14. The areawas debrided, irrigated with chlorhex-idine digluconate and amoxillin 250 mgtablets no. 20, 3 tablets/day and metron-idazole 200 mg tablets, 3 tablets/daywere prescribed for 1 week.

7 months after implant 42 (1) wasplaced, obtaining osseointegration after3 months, the area suddenly gave riseto pain and discomfort for the patient.The implant became mobile and was re-moved. At this stage, the patient was in-formed that further treatment involvingplacement of implants would probablynot be successful. However, the patientwished to proceed with surgical implanttherapy.

Following the removal of teeth 31and 41 and healing of the area, 2 newimplants 13 mm¿3.75 MK II Nobel Bi-ocare were inserted in the area (41,3,42,3). Tetracycline, 250 mg tablets, 4¿a day was prescribed for 1 week.

At suture removal 12 days later, thepatient reported pain and discomfortpost-operatively. 1 month after inser-tion, both implants totally exfoliatedduring a few hours before she couldmake it to the dental office. When seenin the office, implant 34, (1) was alsomobile. This fixture had been inserted 8months previously and had been deter-mined to be osseointegrated 5 monthspreviously. The fixture was observedregularly as it became exposed throughthe mucosa. The mucosal reaction as-sociated with the exfoliation of im-plants 41, (3) and 42, (3) had not, as faras could be clinically determined,crossed the mid-line to the exposed im-plant 34, (1). The implant had to be re-moved.

8 months after these events, implants33, (2) and 43, (2) were surgically ex-posed and diagnosed as osseointe-grated. Transmucosal healing compo-nents were fitted and used for 4 monthswithout loading. The only remaining

tooth was removed, a gold bar wasmade between the implants, and anoverdenture was finally constructed.

At 1 year follow-up, the implantswere still in place and appeared to beosseointegrated as determined clinicallyand radiographically.

Bacterial samples were taken usingsterile paper points inserted into theperimplant spaces of the failing im-plants. The samples were transported tothe Microbial Diagnostic Service of theDental Faculty, University of Oslo onprereduced anaerobically sterilisedVMG III medium (Møller 1966). Mi-crobial culturing was performed anaer-obically (80% N2, 10% H2 and 10%CO2) for 5–7 days at 37æC on non-selec-tive blood agar plates supplementedwith hemin and vitamin K, and onselective agar plates for Actinobacillusactinomycetemcomitans, enterics andyeasts. Identification of the micro-or-ganisms was carried out according tostandard biochemical tests, includinguse of the bioMerieux databased sys-tem. The cultures showed a rich growthof mixed bacteria where black colonieswere abundant. The predominant bac-teria were: Porphyromonas gingivalis,Streptococcus sanguis, Streptococcusoralis, and Capnocytophaga spp. Actino-bacillus actinomycetemcomitans was notisolated.

Histological sections. Tissue sur-rounding some of the failing implantswas removed, and transported in Histo-coneA to the laboratory. The tissue wastaken from areas without presence ofpus or signs of acute inflammation. Thetissue was immediately embedded inTissue-TekA (OCT compound, MilesInc., Elkhart, IN, USA), frozen in 2-methylbutane (ª140æC) prechilled inliquid nitrogen and stored at ª80æC un-til sectioning.

Cryostat sections (6–8 mm) werestained with haematoxylin and eosin(H&E) for morphological studies. Animmunohistochemical staining tech-nique, the avidin-biotin complex (ABC)

method, was used in order to furtherspecify the various cell types of the cellinfiltrates. Table 1 lists the monoclonalantibodies (Mab) employed.

The sections were fixed in cold ace-tone, followed by blocking of endoge-nous peroxidase activity with 0.3%H2O2 for 5 min. After a brief rinse inTBS (Tris-buffered saline; 0.05M Tris/HCl, 0.15 M NaCl, pH 7.6), the sec-tions were incubated for 15 min in a bi-otin blocking solution (Vector, Bur-lingame, CA, USA). After washing inTBS, the slides were incubated withblocking protein (normal horse serum)for 15 min. The slides were then incu-bated with Mab with different speci-ficities (Table 1), followed by incubationwith biotinylated anti-mouse IgG.Binding of biotin-labelled antibodieswas detected after incubation with avid-in-biotin complexes including peroxi-dase followed by the use of H2O2 and3-amino-9-ethyl-carbazole-containingbuffer. Between each step, the slideswere washed in TBS for 10 min. All sec-tions were counterstained with Mayer’shaematoxylin.

Sections stained with HE showeddowngrowth of unkeratinized sulcularepithelium. The connective tissuestroma contained a chronic cellular in-filtrate, primarily located subjacent tothe apically migrated epithelium. Bothlymphocytic cells, plasma cells, andmacrophages could be observed. Poly-morphonuclear granulocytes werelocated within the epithelium.

Immunohistochemistry showed thatT-cells (CD3π cells) were the predomi-nating lymphocytic cell (Fig. 3). Amongthese, CD4π cells were the most numer-ous subgroup (Fig. 4). CD8π cells werefewer, and were also observed intra-epithelially (Fig. 5). B cells (CD19πcells) were rare, but were observedmainly in the perivascular infiltrates(Fig. 6). Macrophages were observed asscattered cells, both intraepitheliallyand in the connective tissue stroma.

Discussion

This case presents a notably rapid anddestructive peri-implantitis. Treatmentspanned over a 2-year period and only2 of 8 implants maintained their osseo-integration. With such a high failurerate, one could suspect faulty techniqueand equipment or an inadequate clini-cian. However, the clinician had 12years of implant experience initially ac-quired as part of a post-graduate pro-

316 Fardal et al.

gram. A number of implants had beenplaced every year to maintain the surgi-cal skills. During the 2-year period, im-plants were successfully placed (±85%)for other patients using the same tech-niques and equipment without similarcomplications.

The clinical reaction appeared to be asevere peri-implant infection. As the pa-tient had a previous history of refractoryperiodontal disease, the remaining teethprobably acted as a reservoir for the col-onisation of the subgingival environ-ment around implants (Apse et al. 1989,Quirynen & Listgarten 1990, Papaioan-nou et al. 1996). Microbiologic findingsfrom failing implants indicate that bac-teria frequently implicated as pathogensin periodontal disease might play a rolein the development of peri-implantitis.Capnocytophaga, P. gingivalis, Fusobac-teria spp. Porphyromonas gingivalis, Pre-votella intermedia and Actinobacillusactinomycetemcomitans have been cul-tured in increased proportions from fail-ing implants (Alcoforado et al. 1991,Rams & Link 1983, Mombelli et al.1987, 1995, Becker et al. 1990, Quiryn-en & Listgarten 1990, Sanz et al. 1990,Sbordone et al. 1996). The fact that peri-odontal pathogens are identified in theperi-implant space permits a compari-son with the pathology of marginal peri-odontitis. Although bacteria are necess-ary to cause peri-implantitis, it is thecomplex interplay between the bacterialchallenge and innate and acquired hostfactors which determine the outcome(Page et al. 1997). The acquired host fac-tor such as tobacco smoking plays an im-portant part in the progression of peri-odontal disease; it could have done thesame in this patient‘s severe peri-im-plantitis. In addition, defects in the pa-tient’s innate host defences may havecontributed to peri-implantitis. Bothparents and all 4 siblings suffered fromsevere periodontal disease which mayhave been due to intrafamilial transfer ofP. gingivalis and/or genetic involvementin the disease. Although the patient wasadvised to stop or reduce her smokinghabit, she admitted that she only man-aged a reduction in the numbers of ciga-rettes over a short period of time. How-ever, as implants are provided success-fully for other smoking patients, thiscould not be the only reason for the se-vere rejection of the implants seen in thiscase.

Immunohistochemical studies of thetissue surrounding some of the failingimplants showed a mixed chronic cellu-

lar infiltrate with a composition com-parable to what is found in chronicmarginal periodontitis. Epositio et al.(1997) showed in their immunohisto-chemical study of late failures of Bråne-mark implants, that macrophages werenumerous and distributed along thesurface of failed implants. This picturecould not be observed in our case.However, in the present case, the im-plants were rejected after a shorterperiod of time.

Since many studies on implant sur-vival show that a relatively small num-ber of patients lose the majority of theirimplants, it is imperative to report onthese patients, so that common featurescan be identified and investigated aspart of a presurgical risk assessment.

Zusammenfassung

Schwere fortschreitende PeriimplantitisDer Ersatz von Zahnen durch Titanimplan-tate ist ein sicheres und vorhersagbares Ver-fahren bei den meisten Patienten. Einige Stu-dien zeigen, daß eine kleine Anzahl von Pati-enten die Mehrzahl ihrer Implantate verliert.Leider kann man diese Patienten vor derChirurgie nicht erkennen. Es ist deshalbwichtig, uber solche Falle zu berichten, daßwir in der Zukunft lernen konnen, wie diesevor der Chirurgie identifiziert werden kon-nen. Die vorliegende Fallbeschreibung zeigteine schwere und rasche Exfoliation von Ti-tanimplantaten. Von 8 Implantaten, die inden anterioren Unterkiefer eingesetzt wordenwaren, war die Osseointegration uber die 2-Jahresperiode nur bei 2 Implantaten erhaltengeblieben.

Resume

Paro-implantite severe progressant rapide-mentChez la plupart des patients, le remplace-ment de dents a l’aide d’implants en titanerepresente un processus sur et previsible.Quelques etudes ont montre qu’un petitnombre de patients perdent la majorite deleurs implants. Malheureusement, il est im-possible d’identifier ces patients avant la chi-rurgie. Il est important de rapporter de telscas afin de pouvoir dans le futur cibler lescas a risque avant la chirurgie. Le cas presentdecrit une exfoliation severe et rapide d’im-plants en titane. Des huit implants placesdans la zone mandibulaire anterieure seule-ment deux ont maintenu une osteo-integra-tion apres deux annees.

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Address:

Ø. FardalP. Box 443N-4370 EgersundNorway

Fax: π47 51 49 27 67e-mail: fardal/odont.uio.no