The International Journal of Periodontics & Restorative Dentistry
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1 The International Journal of Periodontics & Restorative Dentistry
2 485 Bacterial Biofilm Morphology on a Failing Implant with an Oxidized Surface: A Scanning Electron Microscope Study Massimo Simion, MD, DDS 1 David M. Kim, DDS, DMSc 2 Stefano Pieroni, DDS 3 Myron Nevins, DDS 4 Clara Cassinelli 5 This case report provided a unique opportunity to investigate the extent of microbiota infiltration on the oxidized implant surface that has been compromised by peri-implantitis. Scanning electron microscopic analysis confirmed the etiologic role of the bacteria on the loss of supporting structure and the difficulty in complete removal of bacterial infiltration on the implant surface. This case report emphasizes the need to perform definitive surface decontamination on failing dental implants prior to a regeneration procedure. Int J Periodontics Restorative Dent 2016;36: doi: /prd.2804 Peri-implantitis is a chronic destructive inflammatory disease that affects soft and hard tissue attachment to an osseointegrated implant in function. 1 Thoughts differ as to whether the etiology relates to the mechanical force of the prostheses or inflammation relative to bacterial infection, but in either case it poses a catastrophic inconvenience. 2,3 The purpose of this case report is to demonstrate the presence and describe the morphology of embedded colonies of oral bacteria on the oxidized surface of a failing implant using scanning electron microscopy (SEM). Materials and methods 1 Full Professor, Department of Periodontology, UOC Maxillofacial Surgery and Odontostomatology Fondazione IRCCS Ospedale Policlinico, Milan, Italy. 2 Associate Professor, Department of Oral Medicine, Infection and Immunity, Harvard School of Dental Medicine, Boston, Massachusetts, USA. 3 Department of Implantology, UOC Maxillofacial Surgery and Odontostomatology, Fondazione IRCCS Ospedale Policlinico, Milan, Italy. 4 Associate Professor (Part-Time), Department of Oral Medicine, Infection and Immunity, Harvard School of Dental Medicine, Boston, Massuchusetts, USA. 5 Biologist, Nobil Bio Ricerche, Via Valcastellana 26, Portacomaro, Asti, Italy. Correspondence to: Dr Massimo Simion, Via della Commenda 10, Milan, Italy. Fax: Massimo.simion@unimi.it 2016 by Quintessence Publishing Co Inc. A 40-year-old patient who had a mandibular second premolar implant placed about 4 years previously in a private practice presented with peri-implantitis. The referring dentist had unsuccessfully treated the diseased site with multiple nonsurgical treatments using plastic scalers and local applications of 0.2% chlorhexidine. At the time of the present authors observation, clinical inflammation associated with bleeding on probing and purulent exudate were evident (Fig 1). Periodontal probing depth was 9 mm on the mesial aspect and 11 mm on the distal aspect. A periapical radiograph demonstrated bone loss to Volume 36, Number 4, 2016
3 486 Fig 1 A clinical examination revealed inflamed gingiva as well as exposure of implant threads around a mandibular right second premolar implant. Fig 2 Periapical radiograph demonstrating bone loss to the apical third of the implant. the apical third of the implant (Fig 2). Due to lack of soft and hard tissue support for this implant, a recommendation was made to remove the implant and consent was obtained. The failed implant was fixed in 5% glutaraldehyde (FLUKA, Sigma- Aldrich) in Dulbecco s Phosphate- Buffered Saline (DPBS GIBCO, Life Technology) for 2 weeks. Following fixation, the implant was dehydrated by immersion for approximately 5 days in each step of an alcoholwater series (the final step being in absolute ethanol [FLUKA, Sigma- Aldrich]). The fixed and dehydrated sample was placed on sample holders on suitable conducting adhesive supports and coated with a thin layer of 99.99% gold (Agar Sputter Coater, Agar Scientific). SEM observations were performed using EVO MA10 instruments (Zeiss). Results SEM images of the smooth surface of the titanium abutment demonstrated minimal plaque accumulation and large areas free from bacteria (Fig 3). The implant-abutment interface revealed significant bacterial infiltrations on the rough oxidized implant surface, filling the porosity of the oxidized surface (Fig 4). Polymorphous aggregates of bacteria were visible immediately under the abutment-implant interface, filling the porosity of the oxidized surface (Fig 5). Cocci, rods, and filamentous bacteria were identified. In the middle portion of the implant, large aggregates of subgingival biofilm were visible, consisting mainly of rods and filamentous bacteria (Figs 6a and 6b). The porous oxidized surface appears to be a breeding ground for microbiota (Fig 6c). The apical portion of the implant surface, which was embedded in the bone until the time of removal, did not show bacterial infiltration (Figs 7 and 8). Discussion This is a case report describing the consequences of a failed implant with a moderately rough oxidized surface affected by peri-implantitis, which was subsequently removed and analyzed using SEM. The patient had previously undergone conservative treatment with plastic hand scalers and local antibiotic therapy without success. Mechanical debridement using both hand scalers and ultrasonic instrumentation has been proposed as the initial treatment of choice, followed by adjunctive local and systemic antibiotic therapies. Chemical decontaminations, photodynamic therapy, and laser applications have been used with some success However, there is no reliable evidence suggesting a single effective and predictable intervention for peri-implantitis treatment. The clinical community considers use of implants with a moderately rough surface to be advantageous for patients compromised by class IV bone, medications, and various bone augmentations. The pores created by the oxidation process, once thought to house bone and connective tissue fibers, actually contain significant bacterial population. 12 The findings of the present case reports are related to a specific implant surface characterized not only by roughness but also by extended porosity. Other moderately rough surfaces could demonstrate different biofilm characteristics. However, these findings are in accordance with previous studies demonstrating that early plaque formation starts from pits and grooves on the The International Journal of Periodontics & Restorative Dentistry
4 487 surface of the supporting substances and increased plaque growth on rough surfaces could be due to increased surface area and embedding of micro organisms in surface irregularities The small size of these pores precludes conservative clinical activities short of removing the oxidized surface that must be cleaned to accept regenerative therapeutics. Decontamination of a failing dental implant surface is complicated due to a shift from the use of turned surface implants to use of moderately roughsurface implants. The use of Er:YAG lasers has been demonstrated to decontaminate an infected dental implant surface by removing the oxidized layer. 16 This prepared the surface to accommodate reestablishment of bone-toimplant contact. The complete removal of the treads and the rough surface with open-flap implantoplasty and resective bone has been proposed as an alternative treatment, but limited data are available in the literature However, this technique may expose implants to the risk of fracture by reducing the thickness of the implant body. The manufacturing community has made advances aimed to reduce inflammation of the soft tissues following microgap investigations Fig 3 (left) Low-magnification ( 52) SEM image of the coronal portion of the implant with abutment. Fig 4 (center) High-magnification ( 500) image of the implant-abutment interface (white arrows). The smooth-surface titanium abutment shows little plaque accumulation and large areas free of bacteria, whereas the adjacent rough oxidized implant surface is deeply colonized by bacteria, as shown at higher magnification in Figs 5 and 7. Fig 5 (right) High-magnification ( 10,000) image of the supragingival portion of the rough oxidized implant surface. Polymorphous aggregates of bacteria are visible immediately under the abutmentimplant interface, filling the porosity of the oxidized surface. Cocci, rods, and filamentous bacteria are organized in a biofilm. a b c Fig 6 (a) Low-magnification ( 52) image of the middle (subgingival) portion of the implant. Large aggregates of subgingival contaminants are visible. (b) High-magnification ( 1,000) image of the subgingival biofilm at the middle portion of the implant. A complex microbiota composed mainly of rods and filamentous bacteria is visible. (c) Higher magnification ( 10,000) image of the same area. Fig 7 (left) Apical portion of the implant ( 52). Bone remnants are attached to the implant surface. Fig 8 (right) High-magnification ( 1,000) image of the residual bone attached to the implant surface. No bacteria can be found on the surface. Volume 36, Number 4, 2016
5 488 in the 1990s. Platform switching has been demonstrated to reduce crestal bone remodeling by moving the inflammatory cell infiltrations in a horizontal direction. 20 More recently, lasers have been used to provide microgrooves to the coronal portion of the implant and the apical portion of the abutment, resulting in physical attachment of connective tissue to prevent apical migration of the epithelium. 21 Surgical techniques must be optimal in placing the implants, and the patient s oral hygiene compliance is essential. Conclusions It is necessary to select an appropriate implant surface as part of the treatment plan. Periodontal disease should be eliminated prior to implant placement, surgical diligence should be exercised, and the patient must be enrolled in a well-defined maintenance program. This will reduce potential risk of inflammation. Further long-term studies are necessary to determine whether other techniques, such as lasers, acid agents, air powder abrasion, or combinations of these, could decontaminate these areas or implantoplasty is the only option. Acknowledgments The authors reported no conflict of interest related to this study. References 1. Zitzmann NU, Berglundh T. Definition and prevalence of peri-implant diseases. J Clin Periodontol 2008;35:S286 S Heitz-Mayfield LJ, Needleman I, Salvi GE, Pjetursson BE. Consensus statements and clinical recommendations for prevention and management of biologic and technical implant complications. Int J Oral Maxillofac Implants 2014; 29:S346 S Hsu YT, Mason SA, Wang HL. Biological implant complications and their management. J Int Acad Periodontol 2014; 16: Mombelli A, Lang NP. Antimicrobial treatment of peri-implant infections. Clin Oral Implants Res 1992;3: Tang Z, Cao C, Sha Y, Lin Y, Wang X. Effects of non-surgical treatment modalities on peri-implantitis. Zhonghua Kou Qiang Yi Xue Za Zhi 2002;37: Büchter A, Meyer U, Kruse-Lösler B, Joos U, Kleinheinz J. Sustained release of doxycycline for the treatment of periimplantitis: Randomised controlled trial. Br J Oral Maxillofac Surg 2004;42: Karring ES, Stavropoulos A, Ellegaard B, Karring T. Treatment of peri-implantitis by the vector system. Clin Oral Implants Res 2005;16: Romeo E, Ghisolfi M, Murgolo N, Chiapasco M, Lops D, Vogel G. Therapy of peri-implantitis with resective surgery. A 3-year clinical trial on rough screw-shaped oral implants. Part I: Clinical outcome. Clin Oral Implants Res 2005;16: Schwarz F, Sculean A, Rothamel D, Schwenzer K, Georg T, Becker J. Clinical evaluation of an Er:YAG laser for nonsurgical treatment of peri-implantitis: A pilot study. Clin Oral Implants Res 2005; 16: Schwarz F, Bieling K, Bonsmann M, Latz T, Becker J. Nonsurgical treatment of moderate and advanced periimplantitis lesions: A controlled clinical study. Clin Oral Investig 2006:10: Schwarz F, Sculean A, Bieling K, Ferrari D, Rothamel D, Becker J. Two-year clinical results following treatment of periimplantitis lesions using a nanocrystalline hydroxyapatite or a natural bone mineral in combination with a collagen membrane. J Clin Periodontol 2008;35: Sridhar S, Wilson TG Jr, Palmer KL, et al. In vitro investigation of the effect of oral bacteria in the surface oxidation of dental implants. Clin Implant Dent Relat Res 2015;17:e562 e Quirynen M, Marechal M, Busscher HJ, Weerkamp AH, Darius PL, Van Steenberghe D. The influence of surface free energy and surface roughness on early plaque formation. An in vivo study in man. J Clin Periodontol 1990;17: Lie T. Morphologic studies on dental plaque formation. Acta Odontol Scand 1979;37: Siegriest BE, Brecx MC, Gusberti FA, Joss A, Lang NP. In vivo early human dental plaque formation on different supporting substances. A scanning electron microscopic and bacteriological study. Clin Oral Implants Res 1991;2: Nevins M, Nevins ML, Yamamoto A, et al. Use of Er:YAG laser to decontaminate infected dental implant surface in preparation for reestablishment of boneto-implant contact. Int J Periodontics Restorative Dent 2014;34: Schwarz F, Sahm N, Iglhaut G, Becker J. Impact of the method of surface debridement and decontamination on the clinical outcome following combined surgical therapy of peri-implantitis: A randomized controlled clinical study. J Clin Periodontol 2011;38: Froum SJ, Froum SH, Rosen PS. Successful management of peri-implantitis with a regenerative approach: A consecutive series of 51 treated implants with 3- to 7.5-year follow-up. Int J Periodontics Restorative Dent 2012;32: Froum SJ, Froum SH, Rosen PS. A regenerative approach to the successful treatment of peri-implantitis: A consecutive series of 170 implants in 100 patients with 2- to 10-year follow-up. Int J Periodontics Restorative Dent 2015;35: Nevins M, Carmelo M, Koo S, Lazzara RJ, Kim DM. Human histologic assessment of a platform switched osseointegrated dental implant. Int J Periodontics Restorative Dent 2014;34:S71 S Nevins M, Nevins ML, Camelo M, Boyesen JL, Kim DM. Human histologic evidence of a connective tissue attachment to a dental implant. Int J Periodontics Restorative Dent 2008;28: The International Journal of Periodontics & Restorative Dentistry
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