Detection of predominant subgingival periopathogens around submerged and non submerged hydroxy apatite implants

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1 [Downloaded free from on Sunday, January 26, 2014, IP: ] Click here to download free Android application for this journa ORIGINAL ARTICLE Detection of predominant subgingival periopathogens around submerged and non submerged hydroxy apatite implants Sultan Zeb Khan 1,2, Nobuhiro Sasaki 2, Noriko Sasaki 2, Kuniko Sasaki 2, Matsuzaka Kenichi 1, Takashi Inoue 1 ABSTRACT Background: The microbiota associated with healthy peri implant tissues has been studied in many cases. However, gram negative anaerobic rods may also be found in small numbers and in low proportions around the endosseous dental implants. Objective: The purpose of this study was to investigate colonization of the peri implant sulcus around two different types of implants by periopathogenic microbiota in a healthy patient. Materials and Methods: A patient with a healthy periodontium was selected. One hydroxy apatite coated one stage (AQB) implant was implanted at the site of the missing upper Right maxillary 1 st molar; the two units two stage (PLATON) were implanted at the sites of the missing 1 st and 2 nd molars in the Left maxillary region. Saliva samples were collected from the peri implant sulcus using paper points every 3 months for 9 months after implantation and fixation of porcelain crowns. Real Time Polymerase Reaction (RT PCR Invader method) was used to detect periodontal pathogens. Results: Salivary periodontal pathogens were checked prior to implantation and Tannerella forsythia (0.06%) was detected. No periodontal pathogens were observed at 3 months. T. forsythia (0.06%) was detected at 6 months around the AQB implant; it was not detected in the PLATON implant. At 9 months, periopathogens increased in number around both types of implants; there was a major difference in numbers of Fusobacterium nucleatum (10.81%), and T. forsythia (0.057%) around the submerged and non submerged implant systems. Conclusions: Submerged implants with screw retained superstructures are more vulnerable to pathogenic microflora colonization than non submerged implants. KEY WORDS: Microbiota colonization, non submerged implant, periopathogens, real time polymerase reaction invader method, submerged implant INTRODUCTION Many different implant systems have been introduced, 1 Department of Clinical Pathophysiology, Tokyo Dental College, 2 Katsutadai Dental Clinic, Chiba, affiliated with Tokyo Dental College Japan. Address for correspondence: Dr. Sultan Zeb Khan, Oral Health Science Center (HRC 8), Tokyo Dental College, Graduate School, Masago, Mihama Ku, Chiba , Japan. E mail: sultanzb@yahoo.com Quick Response Code: Access this article online Website: DOI: / and the indications for their application have gradually been extended. Root form endosseous implants are commonly used for the fixation of prosthetic restorations. Brånemark et al. [1] initially described anchorage of dental prostheses with osseointegrated dental implants. Two surgical approaches are commonly used: Submerged and non submerged (merged). The submerged implant system (two stage implant) was advocated by Brånemark et al. [1] and the non submerged (merged) system by Schroeder et al. [2] Studies have shown that approximately 400 different microbial species are capable of colonizing the dentate oral cavity and that any individual may harbor over 150 different species. [3] Samples from healthy gingival sulci contained relatively few ( ) cultivable organisms, with Gram positive cocci and rods predominant, Journal of Dental Implants Jul - Dec 2013 Vol 3 Issue 2 111

2 principally Actinomyces naeslundii (14%), Actinomyces gerencseriae (11%), Streptococcus oralis (14%), and Peptostreptococcus micros (5%). Gram negative anaerobic rods accounted for 13% of the total cultivable organisms on average. [4] Esposito et al. suggested that implant failure indicated the inability of the host tissue to establish or maintain osseointegration. [3] Mombelli et al. defined peri implantitis as inflammation functionally affecting the tissue around an osseointegrated implant, resulting in loss of supporting bone. [5] Clinically, implant failure after osseointegration is believed to result from progressive change in the loading conditions in relation to bone quality and volume and peri implantitis. [6] Thus, peri implantitis represents a major risk factor for implant failure after osseointegration, and infection can sometimes occur due to the installation technique chosen or excessive occlusal force. [7] These earlier studies suggest that periodontal pathogens, and especially Gram negative anaerobic rods, play an important role in the development of peri implantitis. In the present case report, the colonization of two different implant systems (AQB and PLATON) in the same healthy patient under similar conditions by microbiota was evaluated over a 9 month period. Purpose The aim of this study was to investigate colonization of the peri implant sulcus around two different types of osseointegrated implant (two stage submerged or one stage non submerged; PLATON and AQB, respectively) by periopathogenic microbiota in a healthy patient. The systems were placed in the load carrying posterior area of the maxillary dentition of a healthy patient under similar conditions using either two stage (submerged) or one stage (non submerged) implant installation protocols. MATERIALS AND METHODS This study was a longitudinal follow up clinical study of submerged and non submerged dental implants over a 9 month period. Patient selection The patient was a 60 year old partially dentate man admitted to the Katsutadai Dental Clinic for implant treatment. The general health of the patient was evaluated and considered good. There were no anesthetic complications, and there was sufficient bone height and bone width to accommodate the implants. The patient had no history of previous radiation therapy for malignancies in the head and neck region. Oral conditions The patient s oral health status was evaluated by checking plaque, probing depth, bleeding index and the values for these tests were all found to be within the normal healthy range. No smoking habit was confirmed. Ethical consideration This study was carried out with the patient s informed consent. Surgical procedure Three implants, one non submergible and two submergible, were used in this study. The non submergible AQB was placed at the site of the missing right maxillary 1 st molar ([Figure 2a and b], site before implant fixation; [Figure 2c and d], after implant fixation). Similarly, two submergible implants were also placed at the sites of the missing left maxillary 1 st and 2 nd molars ([Figure 1a and b], before implantation; [Figure 1c and d], after fixation). All procedures were performed under local or general anesthesia. The surgical procedures for the two, two stage submergible implants included crestal incision, raising a full thickness mucoperiosteal flap, exposing the bone and placing the implant units under copious water irrigation. The mucosal incisions were sutured using resorbable materials and allowed to heal until the second stage procedure 6 months later. The one non submergible implant (AQB) was placed directly into the bone after incision and removal of the mucoperiosteal flap. The patient received antibiotics (amoxicillin, 500 mg) from the day of operation 3 times daily for 5 days postoperatively and was requested to rinse with a 0.2% chlorhexidine solution 4 times/day for 5 days. RESULTS Saliva was checked at before installation of both types of implant system. Tannerella forsythia (0.06%) was observed, as shown in Figure 3. No other periopathogens were observed. At 6 months, T. forsythia (0.06%) was detected around the non submerged (merged) implant only, as shown in Figure 4, as the submerged implant had not been exposed to the oral flora at that point. After 9 months, periopathogens increased in number around both types of implant system. There was major difference, however, in the numbers of Fusobacterium nucleatum (10.81%) and T. forsythia (0.057%) around the submerged and non submerged implant systems, respectively. DISCUSSION Heydenrijk et al. reported that the microbiota of the oral cavity before implant placement determines the composition of the peri implant microflora. [8] In this 112 Journal of Dental Implants Jul - Dec 2013 Vol 3 Issue 2

a b a b c Figure 1: (a) Digital radiographic picture of extracted left maxillary 1 st molar. (b) Clinical photograph of area around extracted left maxillary 1 st and 2 nd molars.

(d) Clinical photographs of area around left maxillary 1 st and 2 nd molar where two submerged dental implants were adjoined with one superstructure porcelain and metal abutments d c Figure 2: (a)

3 a b a b c Figure 1: (a) Digital radiographic picture of extracted left maxillary 1 st molar. (b) Clinical photograph of area around extracted left maxillary 1 st and 2 nd molars. (c) Digital radiographic picture of area around left maxillary 1 st and 2 nd molar where two submerged dental implants were adjoined with superstructure porcelain abutments. (d) Clinical photographs of area around left maxillary 1 st and 2 nd molar where two submerged dental implants were adjoined with one superstructure porcelain and metal abutments d c Figure 2: (a) Digital radiographic picture of right maxillary 1 st molar after removal of metal bridge. (b) Clinical photograph of right maxillary 1 st molar area with metal bridge between two units. (c) Digital radiographic picture of area around right maxillary 1 st molar where one non-submerged dental implant was adjoined with superstructure porcelain abutment. (d) Clinical photograph of area around right maxillary 1 st molar where one non-submerged dental implant was adjoined with one superstructure porcelain abutment d Figure 3: Saliva: Real-time polymerase reaction-invader method analysis for periopathogenic microbiota before implant fixation study, the patient was placed under a regular periodontal maintenance care program. Before the implant operation, we performed a routine checkup including scaling, the plaque index, the bleeding index, and probing depth. The elimination of potential reservoirs of periodontal pathogens before implant placement and the importance of maintaining periodontal health in partially dentate patients with oral implants has been emphasized in previous reports. [9,10] However, peri implant disease following successful integration of an endosseous implant is the result of an imbalance between the bacterial challenge and the host response. Peri implant diseases may affect the peri implant mucosa only (peri implant mucositis) or also involve the supporting bone (peri implantitis). [11] In recent years, studies have focused on the colonization of implants in partially dentate individuals. It was shown that bacterial colonization occurred immediately following transmucosal implant placement (30 min) and was stable after 2 weeks. [12 14] Moreover, the composition of the microbiota after 3 months was shown to be predictive of colonization after 1 year. [15] In addition, it was found that the composition of biofilm on the implant surface corresponded closely with that on teeth surrounded by healthy tissues. Hence, it can be anticipated that the microbiota in the oral cavity may have a substantial impact on biofilm formation on newly placed implants. [15] This is why in this study the patient s saliva prior to implant operation was analyzed for Gram negative periodontal pathogens (Aggregatibacter actinomycetemcomitans, Journal of Dental Implants Jul - Dec 2013 Vol 3 Issue 2 113

4 Figure 4: Saliva: Real-Time Polymerase Reaction (RT-PCR-Invader method) analysis for periopathogenic microbiota after submerged and non-submerged dental implant fixation. Figure shows microbiota percentages at 6 and 9 months Prevotella intermedia, Porphyromonas gingivalis, T. forsythia, Treponema denticola, and F. nucleatum) using the RT PCR (invader method). Only T. forsythia (0.06%) was observed in the saliva of the patient before implant fixation, and at a level considered to be acceptable and not likely to cause peri implantitis. The similarity between the composition of the microbiota around teeth and that around implants within the same subject has been clearly demonstrated. [16,17] In the present report, the microbiota around the two different types of implant system was checked every 3 months for up to 9 months. No Gram negative periodontal pathogens were observed at 3 months around either type of implant system. These results are in accordance with an earlier report by Tanner et al., who observed colonization of the peri implant surface by putative periodontal pathogens (anaerobic) in healthy subjects without signs of gingival inflammation. [18] The same results were reported in our previous study, in which no evidence of anaerobic microbiota around one stage AQB implants was found at 3 months of implant fixation. [19] The transmission of bacteria from the tooth to implant sites has been confirmed in studies investigating the dynamics of microbiota colonization. [10,20] In an earlier study, [19] we reported that periopathogens (P. gingivalis, P. intermedia, F. nucleatum) started to colonize the pockets around implants after an approximately 4 6 month period, which agreed with the results of Mombelli et al. [9] The roughness and chemical composition of the implant surface may also affect the development of biofilm on dental implants. [21] In the present study, T. forsythia (0.06%) was detected at 6 months around a one stage AQB implant, which was in agreement with the results of our previous report. [19] However, no pathogens were found in the sulci around the submerged implants at 6 months as the abutments had not been exposed to the oral cavity at that point. Both the implant systems had an hydroxy apatite coating; the only difference was in the surgical fixation protocol. At 9 months, A. actinomycetemcomitans, T. forsythia, and F. nucleatum increased in number around both implant systems. These results are in agreement with the most recent study of Giorgio et al., [22] who reported that the most common periodontopathic bacteria in peri implant sites were F. nucleatum and T. forsythia. In the present study, F. nucleatum showed a 25 fold increase (10.81%) around the submerged implant as compared to around the non submerged implant (0.43%). These results are in accordance with those of Hermann et al. [23] and Ugo Covani et al., [24] who noted that the presence of a micro gap (component interface) in two stage implant systems might play an important role in the development of peri implantitis due to heavy bacterial colonization at this interface. Similarly, other reports have noted that differences in implant design or surface chemistry may affect the potential risk for invasion of oral microorganisms into the fixture abutment interface. [25,26] This indicates that two stage implant systems are more vulnerable to colonization by periodontopathic pathogens than one stage implant systems. Therefore, it was concluded that the connecting metal or porcelain crowns of submerged implants provide a colonization friendly environment for bacteria around implants. 114 Journal of Dental Implants Jul - Dec 2013 Vol 3 Issue 2

5 CONCLUSION The present results suggest that non submerged implants with separately cemented superstructures (porcelain or metal crowns) show better results in terms of colonization by periopathogens than submerged implants, irrespective of implant installation protocol. Submerged implants (two stage) with screw retained superstructures (porcelain or metal crowns) are more vulnerable to pathogenic microflora colonization than non submerged (merged) implants. The connecting metal or porcelain crowns of submerged implants provide a peri implant colonization friendly environment for bacteria. REFERENCES 1. Brånemark P I, Zarb GA, Albrektsson T, editors. Tissue Integrated Prostheses: Osseointegration in Clinical Dentistry. Chicago: Quintessence; Schroeder A, Pohler O, Sutter F. Tissue reaction to an implant of a titanium hollow cylinder with a titanium surface spray layer. SSO Schweiz Monatsschr Zahnheilkd 1976;86: Esposito M, Hirsch JM, Lekholm U, Thomsen P. Biological factors contributing to failures of osseointegrated oral implants. (I). Success criteria and epidemiology. Eur J Oral Sci 1998;106: Ximenez Fyvie LA, Haffajee AD, Socransky SS. Microbial composition of supra and subgingival plaque in subjects with adult periodontitis. J Clin Periodontol 2000;27: Mombelli A, Lang NP. The diagnosis and treatment of peri implantitis. Periodontol ;17: Esposito M, Hirsch JM, Lekholm U, Thomsen P. Biological factors contributing to failures of osseointegrated oral implants. (II). Etiopathogenesis. Eur J Oral Sci 1998;106: Lee KH, Maiden MF, Tanner AC, Weber HP. Microbiota of successful osseointegrated dental implants. J Periodontol 1999;70: Heydenrijk K, Meijer HJ, van der Reijden WA, Raghoebar GM, Vissink A, Stegenga B. Microbiota around root form endosseous implants: A review of the literature. Int J Oral Maxillofac Implants 2002;17: Mombelli A, Nyman S, Brägger U, Wennström J, Lang NP. Clinical and microbiological changes associated with an altered subgingival environment induced by periodontal pocket reduction. J Clin Periodontol 1995;22: van Winkelhoff AJ, Goené RJ, Benschop C, Folmer T. Early colonization of dental implants by putative periodontal pathogens in partially edentulous patients. Clin Oral Implants Res 2000;11: Zitzmann NU, Berglundh T. Definition and prevalence of peri implant diseases. J Clin Periodontol 2008;35: Fürst MM, Salvi GE, Lang NP, Persson GR. Bacterial colonization immediately after installation on oral titanium implants. Clin Oral Implants Res 2007;18: Quirynen M, Vogels R, Pauwels M, Haffajee AD, Socransky SS, Uzel NG, et al. Initial subgingival colonization of pristine pockets. J Dent Res 2005;84: Quirynen M, Vogels R, Peeters W, van Steenberghe D, Naert I, Haffajee A. Dynamics of initial subgingival colonization of pristine peri implant pockets. Clin Oral Implants Res 2006;17: Salvi GE, Fürst MM, Lang NP, Persson GR. 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Early colonization of non submerged dental implants in patients with a history of advanced aggressive periodontitis. Clin Oral Implants Res 2006;17: Teughels W, Van Assche N, Sliepen I, Quirynen M. Effect of material characteristics and/or surface topography on biofilm development. Clin Oral Implants Res 2006;17 Suppl 2: Tabanella G, Nowzari H, Slots J. Clinical and microbiological determinants of ailing dental implants.clinical Implant Dentistry and Related Research. 2009;11 (1): Hermann JS, Buser D, Schenk RK, Schoolfield JD, Cochran DL. Biologic width around one and two piece titanium implants. Clin Oral Implants Res 2001;12: Covani U, Marconcini S, Crespi R, Barone A. Bacterial plaque colonization around dental implant surfaces. Implant Dent 2006;15: Subramani K, Jung RE, Molenberg A, Hammerle CH. Biofilm on dental implants: A review of the literature. Int J Oral Maxillofac Implants 2009;24: Tesmer M, Wallet S, Koutouzis T, Lundgren T. Bacterial colonization of the dental implant fixture abutment interface: An in vitro study. J Periodontol 2009;80: How to cite this article: Khan SZ, Sasaki N, Sasaki N, Sasaki K, Kenichi M, Inoue T. Detection of predominant subgingival periopathogens around submerged and non-submerged hydroxy-apatite implants. J Dent Implant 2013;3: Source of Support: Nil, Conflict of Interest: None. Journal of Dental Implants Jul - Dec 2013 Vol 3 Issue 2 115

Bacterial colonization of the peri-implant sulcus in dentate patients: a prospective observational study

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