Case Report

Clinical Outcomes of Peri-Implant Peripheral Giant CellGranuloma: A Report of Three Cases

Gonzalo Hernandez,* Rosa M. Lopez-Pintor,* Jesus Torres,† and Juan Carlos de Vicente‡

Background: Peripheral giant cell granuloma(PGCG) is a reactive lesion that occurs on the gingivaor alveolar mucosa and contains numerous giantcells. Its recurrence rate is 10%. Only five cases associ-ated with dental implants have been reported. Thiscase report describes three additional cases with clin-ical courses and outcomes.

Methods: Three women presented with a chiefcomplaint of a gingival mass around the implants.The lesions were surgically excised under local anes-thesia.

Results: The initial diagnosis at presentation waspyogenic granuloma. Radiography showed marginalbone loss accompanying the lesions. Histopathologyconfirmed the diagnosis of PGCG. In two cases, sev-eral recurrences resulted in explantation of the fixture.One case healed uneventfully.

Conclusions: Despite its usually benign clinicalbehavior, peri-implant PGCG may follow an aggres-sive course. Treatment planning for this conditionshould take into account the presence of recurrencesto evaluate the necessity of an aggressive surgical ap-proach that may involve advanced bone loss andexplantation. Further research on the origin of thisimplant-associated condition with a larger series ofcases is necessary to provide a basis for adequatemanagement. J Periodontol 2009;80:1184-1191.

KEY WORDS

Case report; dental implants/complications;disease/diagnosis; granuloma, giant cell.

Peripheral giant cell granuloma (PGCG) is a non-neoplastic, hyperplastic lesion that occurs inthe oral cavity and consists of large multinucle-

ated cells. Four types of reactive lesions occur in thegingiva and alveolar mucosa, including pyogenicgranuloma, peripheral ossifying fibroma, peripheralfibroma, and PGCG; the latter is, by far, the mostuncommon (1.52%).1-3 The PGCG lesion seems tooccur at similar rates in both genders or with a slightfemale predilection, especially in older age groups.There are no marked age and racial predilections, butmost patients are in the fourth to sixth decades of lifeat the time of diagnosis. Although the precise etiologyof PGCG is unknown, it is considered a reactive lesioninduced by trauma or irritation.4 The PGCG arisesmainly from the connective tissue of the gingiva orfrom the periosteum of the alveolar ridge, and itoccurs in the mandible more often than in the maxilla.It is believed that the lesion may originate fromosteoclasts5 or macrophages.6 Its clinical importancelies in the fact that extensive lesions may result inadvanced bone resorption, which can lead to estheticconcerns or even tooth loss. Malignant transformationhas never been described.

Implant therapy is a safe and secure procedure forrestoring tooth loss, with an expectation of long-termsuccess. However, different factors have been sug-gested to influence implant failure, including patientcharacteristics, the type of implant, post-surgicalmaintenance, and occlusal forces. In addition, thepresence of various systemic conditions, including di-abetes, smoking, and bone diseases, was suggestedto influence long-term implant survival.7-10

There are only five published cases of PGCG asso-ciated with the presence of dental implants, and eachhad a different clinical outcome.11-13 This article de-scribes the clinical characteristics of three additionalcases, discusses the implications on the course ofthe implant, and assesses the etiologic potentialof that condition on implant failure and peri-implantbone loss.

* Department of Oral Medicine and Buccofacial Surgery, School of Dentistry,Complutense University, Madrid, Spain.

† Department of Health Sciences III, Faculty of Health Sciences, Rey JuanCarlos University, Alcorcon, Spain.

‡ Department of Oral and Maxillofacial Surgery, Faculty of Medicine andDentistry, University Hospital of Asturias, Oviedo, Spain. doi: 10.1902/jop.2009.090081

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CASE DESCRIPTIONS

Case 1A 45-year-old non-smoking female presented at theDepartment of Oral Medicine and Buccofacial Sur-gery, Complutense University, in June 1999 with achief complaint of a mass located at the mucosaaround an implant-supported bridge. The patient be-gan to feel the lesion 1 month previously, and it grewrapidly, causing some difficulty during eating. The pa-tient was unaware of the problem until the lesion bledconspicuously during toothbrushing.

The medical history was uneventful, with no allergiesor other diseases. Three years previously, in September1996, she had undergone a two-stage procedureduringwhich three and two self-tapping implants§ (3.75 · 7-mm long) were placed in the right and left posterioredentulous areas of the mandible, respectively. Fourmonths later, three transepithelial abutments wereplaced, and a screw-retained, noncemented fixed pros-thesisof threeunitswasbuilt. Thepatientwas examined4 months later for control and evaluation and then onceevery 12 months for maintenance.

An intraoral examination disclosed the presenceof a well-defined, purple, dome-shaped, smooth-surfaced sessile lesion, 2 cm in diameter, whichsurrounded the transepithelial abutments of the twomesial implants (Fig. 1A). X-rays showed 1 mm ofbone loss around the distal aspect of the mesial im-plant and around the mesial aspect of the second im-plant (Fig. 1B). Clinical examination of the abutmentsrevealed no mobility or plaque accumulation. Underthe suspicion of pyogenic granuloma, an excisionalbiopsy was performed with local anesthesia. Thelesion was completely removed, with some bonecurettage, and the area was covered with a surgicaldressing. Histopathology revealed normal epitheliumand underlying connective tissue with abundantmultinucleated giant cells and hemosiderin deposits(Fig. 2). The histopathologic diagnosis was PGCG.

Wound healing followed a tortuous course. After 3weeks, a new lesion appeared around the mesial im-plant that required surgical removal. Weobserved min-imal bone loss around the implant, performed carefulcurettage of the bone around the implants, and gentlypolished the surface of the implant neck with an abra-sive paste. Again, histopathology demonstrated aPGCG. Blood chemistry did not reveal any remarkableabnormalities. After removal of the second lesion, it re-curred four more times with subsequent bone loss dueto the surgical curettage and ostectomy (Fig. 3A). Fi-nally, we removed the mesial fixture and used a dia-mond burr to polish the mesial aspect of the secondimplant, which had lost ‡3 mm of bone height (Fig.3B). After 3 weeks, the alveolar ridge healed unevent-fully. The patient was examined 4 months later to eval-

uate the replacement implant. Because of the shortremaining bone height between the alveolar ridgeand the mental foramen (4 mm), we decided not toplace another implant in that area. The two remainingimplants were loaded onto the bridge that the patientwore previously. A careful recall program was carriedout for maintenance and occlusal readjustment.After 9years, no recurrence was observed.

Case 2A 36-year-old white, non-smoking female was re-ferred to the Department of Oral Medicine and Bucco-facial Surgery, Complutense University, in May 2005with a chief complaint of profuse bleeding around animplant-supported crown during teeth cleaning. Thepatient did not mention additional symptoms. Hermedical history was unremarkable. The dental historyincluded a root canal treatment in the first right uppermolar in 1997 that was lost because of a fracturein June 2002. In February 2003, the patient received

Figure 1.Case 1. A) The lesion located between the two anterior implants hadspread toward the lingual and buccal aspects. B) A periapicalradiograph shows minimal bone loss at the distal aspect of the firstfixture and at the mesial aspect of the second implant.

§ Mk II Branemark System, Nobel Biocare, Goteborg, Sweden.

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a 4 · 13-mm self-tapping implanti with a non-sub-merged approach. A healing abutment was applied,and the patient was referred to her dentist 6 monthslater for prosthetic rehabilitation. At that time, theperi-implant tissue showed no signs of inflammation.A screwed ceramo-metallic crown was placed to re-store the tooth. The patient was examined at 4 monthsfor control and then once every 12 months for main-tenance.

A clinical intraoral examination revealed a nodularlesion that surrounded the buccal aspect of the crownon the upper right first molar (Fig. 4A). The lesion waspurple-red, smooth-surfaced, and 0.8 cm long. Therewas no plaque accumulation on the crown, but therewas some calculus debris and abundant plaque on thesecond upper right molar. Once the crown was re-moved, it was evident that the lesion was limited tothe buccal aspect of the gingiva and had spread tothe neck of the implant. Probing the area indicateda depth of 5 mm and caused profuse bleeding. Therewas no mobility of the implant, and percussion did notproduce pain. Radiographs revealed that 3 mm ofbone had been lost around the implant (Fig. 4B).The preliminary diagnosis was pyogenic granuloma.Surgical excision was performed under local anesthe-

sia accompanied by curettage of the area. A healingabutment was placed during the post-surgical period.Histopathologic examination revealed an intact epi-thelium covering a granulation-like connective tissuethat contained scattered multinucleated giant cellsand extravasated blood (Fig. 4C). The histopatho-logic diagnosis was PGCG.

After 2 weeks, the patient complained of a new gran-ulomatous-like tissue in the same location, emergingfrom the junction between the healing abutment andthe implant. A flap was raised to evaluate the peri-im-plant area. We found 3 mm of bone loss around the im-plant, which left some threads of the implant exposed.There was a dehiscence of 5 mm at the buccal area.The soft tissue was removed again with bone curet-tage, and the surface of the implant was carefullycleaned, irrigated with chlorhexidine (0.12%), andpolished with an abrasive paste. The histopathologic

Figure 3.Case 1. A) Periapical radiograph taken after the third recurrence. Notethe peri-implant bone loss around the two mesial implants. B) Finalradiograph. Note that the first implant was removed, and the mesialaspect of the second fixture was polished.

Figure 2.Case 1. A) Photomicrograph of gingival lesion showing a stratifiedsquamous epithelium covering a connective tissue showingmultinucleated giant cells, congestion, and deposits of hemosiderin.B) High-power view of the connective tissue. The lesion displayednumerous large multinucleated giant cells. (Hematoxylin and eosin;original magnification: A, ·100; B, ·400.)

i TiUnite Branemark System, Nobel Biocare.

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examination confirmed the diagnosis of PGCG. Bloodanalyses were conducted to determine the presenceof any associated diseases. The results showed no ab-normalities in the serum levels of calcium, phospho-rus, or other parameters.

One month later, the patient returned with a com-plaint of bleeding in the same area, and we found that

a new soft-tissue lesion had appeared. A flap wasraised, the lesion was removed, an ostectomy wasperformed around the implant, and the surface ofthe implant was polished with an abrasive paste.The area was gently irrigated with chlorhexidine.We observed 5 mm of bone loss around the neckof the implant at that time, but the implant did notshow any mobility. Subsequently, the patient expe-rienced two more recurrences of PGCG. The fourthrecurrence, observed 2 months later, was accom-panied by an abscess in that area and 7 mm ofbone loss at the buccal plate; thus, we decidedto remove the fixture. The healing was uneventful;1 year later, the bone height appeared to have im-proved. The patient decided against another implantin the area.

Case 3A 62-year-old white, non-smoking female presentedat the Department of Oral and Maxillofacial Surgery,University Hospital of Asturias, in September 2007with a chief complaint of a mucosal mass adjacentto the left lower distal implant that had been placed3 months earlier. The patient was unaware of the le-sion until 20 days before the examination, when sheexperienced moderate pain in that area and bleedingunder the overdenture she wore. The family historywas uninformative. The medical history included auterine myoma that had been successfully removed12 years prior. The patient had been under periodon-tal maintenance for 18 years for advanced chronicperiodontitis, which had caused complete tooth lossin the mandibular arch. Six years prior to the currentexamination, six implants had been placed for screw-retained, fixed prosthesis in the maxillary posteriorareas, and three implants had been placed for a bar-supported overdenture in the anterior mandible. InJune 2007, the patient wanted to exchange the re-movable lower prosthesis for a fixed prosthesis. Two4 · 15-mm and one 4 · 13-mm self-tapped implants¶

were placed in a distal position: two on the left side andone on the right side. The surgical procedure was per-formed using a one-stage approach. The removabledenture was gently reduced, and hygiene instructionswere emphasized. The patient was examined 1 monthlater to readjust her overdenture.

Intraoral examination revealed the presence of anexophytic mass, 2 cm in diameter, which surroundedthe distal aspect of the distal left healing abutment.The lesion had a soft, elastic consistency, a smoothred-pink surface with reddish areas, and a peduncu-lated base (Fig. 5A). X-rays revealed 2 mm of boneloss around the implant on the distal aspect and4 mm on the mesial aspect (Fig. 5B). Under the

Figure 4.Case 2. A) A localized mass emerged between the crown and thegingiva. B) A radiograph shows the marginal bone loss around thehead of the implant. C) Multinucleated giant cells near some fociof extravasated erythrocytes (hematoxylin and eosin; originalmagnification ·250).

¶ TiUnite Branemark System, Nobel Biocare.

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suspicion of a pyogenic granuloma, an excisional bi-opsy was performed with local anesthesia, and the le-sion was completely removed. Histopathology showedthat the lesion was composed of connective tissue thatcontained a large number of multinucleated giant cellsand deposits of hemosiderin. A diagnosis of PGCG wasestablished. The postoperative course was uneventful,and no recurrence was observed (Fig. 5C). Twomonths later, a screw-retained, fixed prosthesis wasplaced. The patient has maintained excellent function.

DISCUSSION

Peri-implant soft tissue conditions and their effects onthe course of an implant have been extensively de-scribed since the beginning of the era of implantology.Most cases of peri-implant soft tissue lesions areplaque-associated and seem to occur at the samerate as those that occur around natural teeth.8,14,15 In1999, Goodacre et al.16 provided an excellent compre-hensiveworkregardingperi-implant soft tissuecompli-cations that were reported in clinical dental implantstudies from1981to1997.Those includeddehiscence,fistulas, and gingival inflammation/proliferation; thelast was the most frequent complication, with a preva-lence ranging from 1% to 32%. According to somelong-term studies,8,17 peri-implant lesions commonlyoccurred adjacent to titanium implants when system-atic supportive treatment was not carried out; theseincluded peri-implant mucositis (48%), progressivebone loss (7.7%), and peri-implantitis (6.6%). Influ-encing factors were related to the patient or implantcharacteristics,e.g.,ahistoryofperiodontitis,smoking,andplaqueaccumulation.Thosestudiesdidnot includePGCG as an etiologic factor for implant complications.

The prevalence of PGCG has not been well estab-lished in the general population. The first three casereports of implant-associated PGCG were describedby Hirshberg et al.11 in 2003 and were included in astudyof25biopsied peri-implant lesions. To ourknowl-edge, only two other cases have been published.12,13

Therefore, theprevalence of this lesion in the field of im-plantology may be considered rare. Among ;12,000implants placed by the authors during the past15 years, the three cases reported here represent anextremely low prevalence.

We have presented several features that deservespecial mention. All subjects were women, consistentwith a slight female predilection;1 this may indicatean influence of sex hormones, as occurs with large le-sions.18 Each case displayed an exophytic appear-ance, consistent with most clinical reports on lesionsassociated with natural teeth or edentulous areas1-3

and consistent with the five cases previously describedthat were associated with dental implants11-13 (Table1). PGCG can appear in anterior or posterior areas,2

but the latter seems to be more prevalent; this was truefor the three cases in this study, and for four of the fiveimplant-associated cases of PGCG reported previ-ously.11-13 The initial clinical diagnosis in our caseswas pyogenic granuloma; this inflammatory hyper-plasia is very difficult, if not impossible, to distinguishfrom PGCG clinically. Pyogenic granuloma usuallyshowsdifferentsurfacecharacteristics,suchasabrightred color and evidence of ulcerated and white patches(necrotic areas). Also, its clinical behavior tends to beless aggressive, and it is more unlikely to cause bone

Figure 5.Case 3. A) Clinical appearance of the lesion surrounding the distalaspect of the healing abutment. B) A radiograph of the area shows themarginal bone loss around the fixture. C) Note the excellent healingaround the abutment 1 month after the lesion was removed.

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resorption than PGCG, although recurrences afterremoval may occur. To our knowledge, no cases ofperi-implant pyogenic granuloma have been reported.The clinical differential diagnosis must also includeother lesions: peripheral ossifying fibromas, hemangi-omas, lymphangiomas, metastatic tumors,nevi, amel-anotic nodular melanomas, fibromas, and Kaposi’ssarcoma. Inrecurrentcases,bloodanalysesforcalciumand phosphorus must be performed to exclude thepresence of a brown tumor of hyperparathyroidism.

It was suggested that PGCG might be associatedwith several factors, such as extraction sockets, cal-culus, tooth caries, dental plaque, and food impaction.Because of the small number of published cases, it isdifficult to speculate about the pathogenesis of theselesions around implants. In the three cases reportedherein, factors associated with tooth extraction maybe excluded because it occurred many months priorto the appearance of the lesion. Some investiga-tors11,19 pointed out that the significance of tooth ex-traction in PGCG formation is unknown and may becoincidental. In all three cases described here, plaqueformation was minimal around the crowns and healingabutments, although bleeding on probing was a con-

stant feature. This may be related to the presence ofthe lesion or to the gingival inflammation around theimplants, which is a frequent finding with this proce-dure,8,17 and it may be associated with the develop-ment of reactive conditions.

The inflammatory reaction in the marginal bonearound the implants is another factor that may be in-volved in the pathogenesis of peri-implant PGCG. Allthree cases presented with 1 to 4 mm of marginal bonelossaroundtheheadofthe implant. Implantproceduresareknowntoproducechanges inthemarginalbone,es-pecially in the first months after insertion and loading,and additional resorption may continue over time.14,20

Thedegreeofmarginalbonelosshasbeenrelatedtotheimplant configuration, location, surface characteris-tics, surgical trauma, stress at the bone–implant inter-face, overloading, plaque accumulation, and implanttiming.21-23 It remains unclear whether PGCG is thecauseofthisboneresorptionor itsconsequence.Unlikeits intraosseous counterpart, PGCG is not usually asso-ciated with bone loss,1,2 and it typically exhibits only asoft-tissue overgrowth. In accordance with other inves-tigators,22 we observed radiographic marginal boneloss around the implants in all three cases and

Table 1.

Characteristics of the Reported Cases of PGCG Associated With Dental Implants

Reference

Age

(years)/

Gender Location

TSI

(months)

Clinical

Appearance

Clinical

Diagnosis RX

Initial

Treatment

Bone at

Presentation Recurrence

Final

Outcome

Implant

Type

Hirshberg

et al.,

200311

31/

Male

Posterior

mandible

Several Gingival

mass

Pyogenic

granuloma/

PGCG

No data Curettage Affected One time Good Screw

type*

Hirshberg

et al.,

200311

69/

Female

Anterior

maxilla

14 Gingival

mass

Pyogenic

granuloma/

PGCG

No data Curettage Affected One time Explantation Screw

type*

Hirshberg

et al.,

200311

44/

Male

Posterior

mandible

72 Gingival

mass

Pyogenic

granuloma/

PGCG

Mild

horizontal

bone loss

Curettage Affected Three

times

Explantation Screw

type*

Bischof

et al.,

200412

56/

Female

Posterior

mandible

24 Gingival

mass

Pyogenic

granuloma

Marginal

bone loss

Excision and

curettage

Affected No Good Screw

type†

Cloutier

et al.,

200713

21/

Male

Posterior

mandible

72 Gingival

mass

No data Severe

bone loss

Excision

and

explantation

Affected No Explantation Screw

type‡

Current

report.

Case 1

45/

Female

Posterior

mandible

34 Gingival

mass

Pyogenic

granuloma

Marginal

bone loss

1 mm

Excision

and

curettage

Affected Five

times

Explantation Screw

type†

Current

report.

Case 2

36/

Female

Posterior

maxilla

27 Gingival

mass

Pyogenic

granuloma

Marginal

bone loss

3 mm

Excision

and

curettage

Affected Three

times

Explantation Screw

type§

Current

report.

Case 3

62/

Female

Posterior

mandible

3 Gingival

mass

Pyogenic

granuloma

Marginal

bone loss

2 to 4 mm

Excision

with

wide margins

and curettage

Affected No Good Screw

type§

TSI = time since implantation; RX = initial radiologic appearance.* Not known.† Self-tapping Mk II Branemark System, Nobel Biocare.‡ Straumann ITI dental implant, Straumann, Waldenburg, Switzerland.§ TiUnite Branemark implant, Nobel Biocare.

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interpreted this as an indication that bone loss is a fre-quent feature in implant therapy.

Other non-inflammatory factors may have played arole in the origin of these lesions. The implants werelocated in posterior locations in the three cases, andthe implants had to support more occlusal forces thanthose located in anterior areas. In natural dentition,PGCG occurs in anterior and posterior areas, butit shows a slight predilection for posterior areas(51.35% versus 48.65%).2 However, seven of eightimplant-associated cases were located in posteriorareas (Table 1). To the best of our knowledge, no ev-idence-based randomized controlled study or pro-spective cohort study proved an association betweenocclusal forces and marginal bone loss; however, ananimal study24 demonstrated a relationship. Stress re-sulting from load may result in marginal bone loss,25

and excessive loading on the peri-implant bone is re-lated to implant mobility and marginal bone loss.7,24

These factors may also produce inflammatorychanges, e.g., mucositis, that may lead to a reactive re-sponse like PGCG. However, the exact etiology of im-plant-associated PGCG remains to be determined.

Two of the cases presented here displayed multiplerecurrences. In the five cases previously reported, 11-13

three displayed recurrences; thus, recurrences inthese studies were more frequent than the 10% ofrecurrences displayed in other larger series of patientswith similar conditions.1,2 We hypothesize that lesionrecurrence in both cases was probably due to an in-complete lesion excision. This emphasizes the impor-tance of eliminating the entire base of the lesion, withwide margins, to prevent recurrences, even with a le-sion that is not extensive, as in cases 1 and 2. How-ever, the high rate of recurrence observed in theliterature for implant-associated PGCG11 suggeststhat clinicians should consider factors that might influ-ence this aggressive pattern, as occurs with centralgiant cell lesions, e.g., the implant surface or theimplant–bone interface, among others.

Finally, we want to emphasize some aspects of themanagement of implant-associated PGCG. In ouropinion, the loss of the implants in cases 1 and 2 wasnot due to the bone loss associated with the PGCGper se but rather with the bone curettage and the min-imal ostectomy performed to treat the lesions. Further-more, it is well established that the bone exposurerelated to the surgical procedures is associated withminimal bone loss.26 In five of the eight cases reported,including two of this study, the implant had to be ex-planted.11,13 In one case, advanced bone loss occurredprior to excision of the PGCG, and the implant was re-moved to obtain adequate access for curettage and le-sion excision;13 in two cases, bone loss was associatedwithsurgical lesionexcisionandtheimplantwasunsup-ported(case2 intheseriesofHirshbergetal.11andcase

2 in this report); and in two other cases, the failure toeliminate the lesionand theassociatedbone lossneces-sitated implant removal (case3 in theseriesofHirshbergetal.11andcase1 inthis report) (Table1). In threecases,initial simple curettage did not provide any benefit;11

however, in three cases, excision combined with gentlecurettage and mechanical cleansing of the implant wassuccessful (case 1 after first recurrence in the series ofHirshberg et al.,11 case of Bishchof et al.,12 and case 3in this report). Therefore, a conservative approach forthetreatmentof thiscondition is recommended,consist-ing of an excision with wide margins accompanied bymechanical debridement, as is performed in cases ofperi-implant mucositis.27,28 However, these measureswillnotprecludetheappearanceofmultiplerecurrences.Thus,athoroughevaluationbytheclinicianmustbeper-formed to decide whether removal of the implant is anappropriate alternative to the risk for progressive bonelossduetotherepetitivesurgeries thatmaybenecessaryto definitively eliminate the lesion.

CONCLUSIONS

The cause of PGCG remains unknown. Further studiesthat include a larger number of cases are necessary toprovide the basis for a management plan appropriatefor this implant-associated condition.

ACKNOWLEDGMENTS

The authors thank Dr. Eduardo Sanz, Hospital Puertade Hierro, Madrid, Spain, and Dr. Felipe LLanes, Hos-pital Clınico de San Carlos, Madrid, Spain, for their as-sistance and support with the histopathologic aspectsof the cases. The authors report no conflicts of interestrelated to this case report.

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Correspondence: Dr. Gonzalo Hernandez, Department ofOral Medicine and Buccofacial Surgery, School of Dentis-try, Ciudad Universitaria s/n, 28040 Madrid, Spain. E-mail:ghervall@odon.ucm.es.

Submitted February 7, 2009; accepted for publicationMarch 3, 2009.

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