186 HISTOLOGICAL ANALYSIS OF SOFT AND HARD TISSUES IN PERIMPLANTITIS JUNG ET AL

Histological Analysis of Soft and Hard Tissues in a Periimplantitis Lesion: A Human Case Report

Soong-Ryong Jung, DDS, PhD,* Jill D. Bashutski, DDS, MS,† Rami Jandali, DMD, MS,‡ Hari Prasad, BS, MDT,§ Michael Rohrer, DDS, MS,k and Hom-Lay Wang, DDS, MS, PhD¶

eriimplantitis is defined as Background: Little is known revealed significant inflammatory inflammation around a dental regarding the histologic hard and soft infiltrate consisting predominantly P implant or its abutment.1 Several tissue changes that occur in chronic of lymphocytes and plasma cells. animal studies have shown that the periimplantitis situations in humans. It In addition, epithelial migration soft tissues surrounding periimplanti- is critical to gain an understanding of and bone loss to the apical vent tis lesions are characterized by exten- all aspects of periimplantitis to develop were noted. sive inflammatory cell infiltrates that violate the pocket epithelium bar- appropriate therapeutic approaches. Conclusion: This case report rier.2–4 This is similar to that noted in Methods: An 83-year-old African documents a single case of periim- clinical periodontitis lesions.5 In addi- Americanmanpresentedwithafrac- plantitis that was left untreated for 7 tion, osseous defects occupied by large tured implant affected by severe, years. The presence of significant numbers of osteoclasts are typical of chronic periimplantitis and surrounded keratinized tissue and a smooth sur- these types of lesions.2 Furthermore, by keratinized gingiva. A trephine face implant failed to prevent fibrous whether an implant has a smooth or biopsy of the implant and surrounding encapsulation of the implant. (Im- rough surface does not affect the tissues was analyzed histologically. plant Dent 2012;21:186–189) amount of loss during active break- Results: Histological analysis Key Words: keratinized gingiva, peri- down in these sites, although rough of the periimplantitis specimen implant disease, implant therapy implant surfaces seem to be more sus- ceptible to bone loss during inactive periimplantitis situations.6,7 Although periimplantitis lesions A recent study of human fibro- *Codirector, Graduate Prosthodontics Program, John D. Dingell fi Veterans Affairs Hospital, Detroit, MI; Adjunct Clinical Lecturer, have been studied extensively in animal blasts found that broblasts obtained Department of Biologic and Material Science, University of Michigan, School of Dentistry, Ann Arbor, MI. models, few human studies are available from periimplantitis lesions secreted †Clinical Assistant Professor, Department of Periodontics and fi fl Oral Medicine, School of Dentistry, University of Michigan, Ann to validate these ndings. A human more proin ammatory chemokines Arbor, MI. fi ‡Director, Graduate Prosthodontics Program, John D. Dingell histological analysis of retrieved dental than broblasts obtained from healthy Veterans Affairs Hospital, Detroit, MI; Adjunct Clinical Assistant implants reported that implants affected gingiva.12 Another study reported alter- Professor, Department of Biologic and Material Science, University of Michigan, School of Dentistry, Ann Arbor, MI. with periimplantitis were characterized ations in the extracellular matrix of §Assistant Director and Senior Research Scientist, Hard Tissue Research Laboratory at the University of Minnesota School of by bony sequestrate, high levels of periimplantitis lesions, specifically for Dentistry, Minneaplois, MN. kProfessor and Director, Division of Oral and Maxillofacial bacteria, and an associated inflammatory collagen V, tenascin, and matrix met- Pathology, School of Dentistry, University of Minnesota and 8 13 Director of the Hard Tissue Research Laboratory, Minneapolis, infiltrate. T lymphocytes are the pre- alloproteinase 13. Finally, gingival MN. ¶Professor and Director of Graduate Periodontics, Department dominant cell type in periimplantitis samples from periimplantitis patients of Periodontics and Oral Medicine, School of Dentistry, University of Michigan, Ann Arbor, MI. lesions, although macrophages and were reported to contain cytokines plasma cells are also commonly associ- that stimulate osteoclast activity, with Reprint requests and correspondence to: Hom-Lay 9 Wang, DDS, MS, PhD, Department of Periodontics and ated. A study comparing periimplantitis interleukin 1 alpha being the most 14 Oral Medicine, University of Michigan School of and mucositis lesions found greater pro- prevalent. These studies support the Dentistry, 1011 North University Avenue, Ann Arbor, portions of B cells and elastase-positive idea that inflamed periimplant tissues MI 48109-1078, Phone: 734-763-3383, Fax: 734-936- 10 0374. E-mail: [email protected] cells in periimplantitis lesions. Gross may be especially susceptible to break- histological sections of implants down and provide possible explana- ISSN 1056-6163/12/02103-186 Implant Dentistry removed due toperiimplantitis show that tions for why this process is so Volume 21 Number 3 Copyright © 2012 by Lippincott Williams & Wilkins fibrous tissue encapsulation with bone destructive in these situations. Still, 11 DOI: 10.1097/ID.0b013e31824eec0a often present only in the apical portion. there is a lack of information regarding IMPLANT DENTISTRY /VOLUME 21, NUMBER 3 2012 187

surrounding the implant was performed (Fig. 3, C). Then, a full- thickness muco- periosteal flap was elevated circumferen- tially and reflected apically. The implant and surrounding soft tissues were removed under copious irrigation with reduced speed to prevent damage to the bone implant specimen (Fig. 3, D). The implant specimen in 10% neutral buff- Fig. 1. Panoramic radiograph of the patient ered formalin was sent for histological revealing #13 and 15 restored as a fixed Fig. 2. Periapical radiograph of fractured analysis to the Hard Tissue Research implant-supported bridge opposing an implants in #13 and 15 positions. Laboratory at the university of Minne- implant-supported bridge. sota. Upon receipt in the Hard Tissue Research Laboratory, specimen was stated that the implant was irritating his sectioned in half through the area of in- the periimplantitis disease process in tongue and his pain score was 2/10. terest and immediately dehydrated with humans. In this case report, we present Oral examination revealed a frac- a graded series of alcohols for 9 days. the clinical and histological findings of tured implant that was level with the soft Following dehydration, the specimen a biopsy of a fractured implant affected tissue, exposed to the oral cavity, but not was infiltrated with a lightcuring embed- by chronic periimplantitis. in function (Fig. 3, A). The implant was ding resin (Technovit 7200 VLC, surrounded entirely by keratinized gin- Kulzer, Germany). Following 20 days CASE DESCRIPTION AND RESULTS giva. The soft tissue surrounding the of infiltration with constant shaking at On October 26, 2006, an 83-year- implant was red and edematous with normal atmospheric pressure, the speci- old African American man patient rolled margins indicating active inflam- men was embedded and polymerized by presented to the Veteran’s Association mation. Bleeding on probing was pres- 450 nm light with the temperature of Hospital in Detroit, Michigan, with ent at 4/6 sites around the implant (MB, the specimen never exceeding 40°C. a chief complaint of mild pain associ- DB, MP, DP) and probing depths ranged The specimen was then prepared by the ated with an implant in #15 area. The from 4 to 5 mm on the buccal and 6 to cutting/ grinding method of Donath.15,16 patient’s medical history was sig- 7 mm on the palatal aspect (Fig. 3, B). The specimen slides were cut to a nificant for a penicillin allergy and Because the implant had fractured at the thickness of 150 mm on an EXAKT Parkinson’s disease involving oral par- level of the body, it was deemed un- re- cutting/ grinding system (EXAKT Tech- afunctional habits. His vital signs were storable and the patient consented to nologies, Oklahoma City, OK). Follow- within normal limits, and he was not have the implant removed. ing this, the slides were polished to taking any medications. The patient Onecarpuleof2%lidocainewith a thickness of 40 mm using the EXAKT stated that he had implants placed in 1:100,000 epinephrine was administered microgrinding system followed by the maxillary left posterior area in the via buccal and palatal infiltration around alumina polishing paste. The slides early 1980s. Dental records were the implant. An elliptical incision were stained with Stevenel’sblueand obtained for the patient revealing that encompassing 3 mm of soft tissue Van Gieson’s picrofuchsin. Following a two-unit implant-supported fixed bridge was placed to replace teeth #13 to 15 (Fig. 1). On July 15, 1999, probing depths up to 10 mm with bleeding on probing were recorded on both #13 and #15 implants. On November 24, 1999, the distal abutment fractured and could not be retrieved (Fig. 2). Consequently, on December 29, 1999, #15 was ground to the level of the alveolar crest and maintained in the mouth underneath a removable partial denture. At the same time, pocket reduction surgery was performed on #13. Bony exostoses were also removed from the facial and lingual aspects of the #13 and 15 area. For 7 years, the patient functioned well Fig. 3. Clinical photographs of implant removal. Preoperative photographs (A and B) dem- with this situation, until October 26, onstrating deep probing depths. Soft tissue incision to preserve gingiva surrounding implant 2006, when the patient presented with (C). Implant following removal with hard and soft tissue (D). pain associated around implant #15. He 188 HISTOLOGICAL ANALYSIS OF SOFT AND HARD TISSUES IN PERIMPLANTITIS JUNG ET AL histologic preparation, the specimen or ligature-induced periimplantitis.6,7 This case report highlights the slides were evaluated. All the specimen chronic lesions are different than acute problem of epithelial downgrowth and slides were digitized at the X2, X4,X10, periimplantitis lesions with the pres- its role in the failure of adequate and X20 magnification using a NIKON ence of more proinflammatory cyto- integration of bone on the implant. ECLIPSE 50i microscope (Nikon Corp., kines produced by fibroblasts and Furthermore, a widespread inflamma- Tokyo, Japan) and a SPOT INSIGHT 2 alterations in the extracellular matrix, tory reaction resulted in bone resorption mega sample digital camera (Diagnostic enhancing tissue breakdown.12–14 the and eventual fibrous encapsulation of Instruments Inc., Sterling Heights, MI). amount of destruction in this case may the implant. In this situation, the The defect was irrigated with saline have been intensified by local tissue destruction was substantial and may and primary soft tissue closure was changes in response to a chronic bacte- be due to the longstanding chronicity achieved using periosteal scoring and rial insult, resulting in increased suscep- of the lesion, emphasizing the need for 3-0 polyglactin 910 sutures. Ibuprofen tibility to tissue destruction. early intervention in these cases. 600 mg every 6 hours was recommen- The fractured implant was com- ded for pain control. The wound healed posed of a smooth surface and was uneventfully without complications. surrounded by a wide band of keratin- CONCLUSION Histological analysis revealed ized gingiva. Despite these features, Chronic periimplantitis is charac- epithelial downgrowth, extensive extensive inflammatory infiltrate terized by extensive inflammation that inflammatory infiltrate, and fibrous extending to the apical portion of the increases the susceptibility of surround- encapsulation (Fig. 4). The epithelium implant was observed, which is consis- ing tissues to additional breakdown if 4,7,8,17 was detected in the internal surface of tent with previous studies. Fur- left untreated. Ultimately, epithelial the vent at the apical portion of the thermore, the epithelium has migrated downgrowth, bone resorption, and soft implant. The inflammatory infiltrate all the way to the vent and covers the tissue encapsulation ensues rendering consisted of primarily lymphocytes and internal surface of the vent. Chronic the implant hopeless. This case presents plasma cells. Small bone fragments were periimplantitis that was untreated for clinical and histological data of a peri- noted, although the majority of the a period of 7 years resulted in near implantitis lesion of long-standing implant was surrounded by soft tissue. complete fibrous encapsulation of duration that was removed due to lack the implant. Recent studies reported of osseointegration. successful treatment of periimplantitis DISCUSSION lesions that were detected in a timely Chronic periimplantitis lesions are manner, suggesting that not all periim- DISCLOSURE difficult to evaluate because few human plantitis leads to implant failure The authors do not have any finan- studies are available and most animal provided there is early treatment 18 cial interests, either directly or indi- studies use acute models with surgical intervention. rectly, in the products or information listed in the article.

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