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The Journal of Implant & Advanced Clinical Dentistry

VOLUME 2, NO. 5 JUNE 2010

Using Short and Extra-Short Implants in Daily Clinical Practice

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The Journal of Implant & Advanced Clinical Dentistry • 5

The Journal of Implant & Advanced Clinical DentistryVOLUME 2, NO. 5 • JUNE 2010

Table of Contents

19 The Use of Short and Extra-Short BTI Implants In the Daily Clinical Practice Eduardo Anitua

33 Simplifying Implant Placement with Partially Edentulous Arch Surgical StentsGregori M. Kurtzman, Douglas Dompkowski

47 A Comparative Clinical, Histological and Histomorphometric Study of Mineralized Allograft and Xenograft Materials in the Treatment of Atrophic Maxillary Sinuses Sammy S. Noumbissi, Alejandro J. Kleinman

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Table of Contents

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73 Osseointegrated Implant in Myasthenia Gravis Patient: A Case Report Wiroj Suphasiriroj, Theerathavaj Srithavaj

81 Management of a Patient Who Developed Uncontrolled Diabetes After Implant Placements A Case Report John F. Carpenter

91 The E!ect of Methotrexate on Bone Healing of a Simulated

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Tara Aghaloo, DDS, MDFaizan Alawi, DDSMichael Apa, DDSAlan M. Atlas, DMDCharles Babbush, DMD, MSThomas Balshi, DDSBarry Bartee, DDS, MDLorin Berland, DDSPeter Bertrand, DDSMichael Block, DMDChris Bonacci, DDS, MDHugo Bonilla, DDS, MSGary F. Bouloux, MD, DDSRonald Brown, DDS, MSBobby Butler, DDSDonald Callan, DDSNicholas Caplanis, DMD, MSDaniele Cardaropoli, DDSGiuseppe Cardaropoli DDS, PhDJohn Cavallaro, DDSStepehn Chu, DMD, MSD David Clark, DDSCharles Cobb, DDS, PhDSpyridon Condos, DDSSally Cram, DDSTomell DeBose, DDSMassimo Del Fabbro, PhDDouglas Deporter, DDS, PhDAlex Ehrlich, DDS, MSNicolas Elian, DDSPaul Fugazzotto, DDSScott Ganz, DMDDavid Garber, DMDArun K. Garg, DMDRonald Goldstein, DDSDavid Guichet, DDSKenneth Hamlett, DDSIstvan Hargitai, DDS, MSMichael Herndon, DDS

Robert Horowitz, DDSMichael Huber, DDSRichard Hughes, DDSDebby Hwang, DMDMian Iqbal, DMD, MSTassos Irinakis, DDS, MScJames Jacobs, DMDZiad N. Jalbout, DDSJohn Johnson, DDS, MSSascha Jovanovic, DDS, MSJohn Kois, DMD, MSDJack T Krauser, DMDGregori Kurtzman, DDSBurton Langer, DMDAldo Leopardi, DDS, MSEdward Lowe, DMDShannon MackeyMiles Madison, DDSCarlo Maiorana, MD, DDSJay Malmquist, DMDLouis Mandel, DDSMichael Martin, DDS, PhDZiv Mazor, DMDDale Miles, DDS, MSRobert Miller, DDSJohn Minichetti, DMDUwe Mohr, MDTDwight Moss, DMD, MSPeter K. Moy, DMDMel Mupparapu, DMDRoss Nash, DDSGregory Naylor, DDSMarcel Noujeim, DDS, MSSammy Noumbissi, DDS, MSArthur Novaes, DDS, MSCharles Orth, DDSJacinthe Paquette, DDSAdriano Piattelli, MD, DDSGeorge Priest, DMDGiulio Rasperini, DDS

Michele Ravenel, DMD, MSTerry Rees, DDSLaurence Rifkin, DDSGeorgios E. Romanos, DDS, PhDPaul Rosen, DMD, MSJoel Rosenlicht, DMDLarry Rosenthal, DDSSteven Roser, DMD, MDSalvatore Ruggiero, DMD, MDHenry Salama, DMDMaurice Salama, DMDAnthony Sclar, DMDFrank Setzer, DDSMaurizio Silvestri, DDS, MDDennis Smiler, DDS, MScDDong-Seok Sohn, DDS, PhDMuna Soltan, DDSMichael Sonick, DMDAhmad Soolari, DMDNeil L. Starr, DDSEric Stoopler, DMDScott Synnott, DMDHaim Tal, DMD, PhDGregory Tarantola, DDSDennis Tarnow, DDSGeza Terezhalmy, DDS, MATiziano Testori, MD, DDSMichael Tischler, DDSMichael Toffler, DDSTolga Tozum, DDS, PhDLeonardo Trombelli, DDS, PhDIlser Turkyilmaz, DDS, PhDDean Vafiadis, DDSEmil Verban, DDSHom-Lay Wang, DDS, PhDBenjamin O. Watkins, III, DDSAlan Winter, DDSGlenn Wolfinger, DDSRichard K. Yoon, DDS

Editorial Advisory Board

Founder, Co-Editor in ChiefDan Holtzclaw, DDS, MS

Founder, Co-Editor in ChiefNicholas Toscano, DDS, MS


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Dan Holtzclaw, DDS, MSFounder, Co-Editor-In-Chief

Nick Toscano, DDS, MSFounder, Co-Editor-In-Chief

To come

Editorial Commentary

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I really appreciate JIACD because it’s a fundamental tool for both practitioner and researcher in the field of Periodontology and dental implant continuing education. What I prefer most is the reliability, the friendly use, and the extremely high quality of the images and the interesting topics. Clinicians and scientists can find clear clinical suggestions and solutions to new and old problems for daily practice.Dr. Giulio Rasperini, Italy

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Anitua

Background: The aims of this study were to evaluate the long-term survival rates of short (7 mm to 8.5 mm) and extra-short BTI implants (5.5 mm and 6.5 mm) installed both in the maxilla and the mandible.

Methods: Two different retrospective cohort studies are reported. In the short BTI implant study, 340 implants installed in 201 consecu-tive patients were evaluated whereas in the extra-short BTI implant study, 48 implants placed 35 were considered. All implant installations were performed by two experienced surgeons and rehabilitations were done by 3 prosth-odontists. Each implant failure was carefully analyzed. Implant survival was analysed using a life-table analysis (Wilcoxon [Gehan] test).

Results: The overall survival rates of short implants were 100% both for the implant and subject-based analysis respectively. The mean fol-low-up period for short implants was 80.5 ± 8.9 months. In the extra-short BTI implant study, sur-vival rates were 97.9% and 97.1% for the implant and subject-based analysis respectively. In this second study, follow-up period was 23.4 ± 6.4 months. Distal and mesial bone loss of extra-short implants at 24 months post-insertion ranged between 1.30 mm and 1.39 mm respectively.

Conclusions: Results of the present retrospec-tive study show that treatment with short and extra-short BTI implants can be considered safe and predictable if used under strict clinical protocols.

The Use of Short and Extra-Short BTI Implants In the Daily Clinical Practice

Eduardo Anitua, DDS, MD1

1. Private practice in implantology and oral rehabilitation in Vitoria, Spain

Abstract

KEY WORDS: Dental implants, short implants, extra-short implants, treatment planning


20 • Vol. 2, No. 5 • June 2010

INTRODUCTIONIn the past, surgeons aimed for placement of the longest possible implant in any given site as long as its placement did not hinder the final prosthetic result in terms of aesthetics. This was especially crucial when implants presented a machined surface and the most common way to increase implant-to-bone contact was to increase the sur-face area available by placing a wider or longer implant. The progress both in the implant sur-face engineering together with the development of novel strict protocols have opened the doors to new clinical options that are revolutionizing the axiomatic concepts of oral implantology. For example, the posterior maxillae present a uniquely challenging site for implant placement due to several complicating factors including, difficult and challenging access, limited visibility, reduced space, bone resorption and poor bone quality and quantity among others. In these clinical situa-tions, several alternatives such as bone augmenta-tion techniques or the use of short implants may bring new therapeutic options for the surgeons.

Biotechnology Institute (BTI) has developed a family of short implants and more recently extra-short implants with some characteris-tic and distinguishing properties including a micro-rough acid-etched surface, and a bioac-tive implant surface.1,2 The latter is obtained by humidifying the implant surface with plasma rich in growth factors (PRGF®) leading to an overall improved and accelerated implant Osseointegration.3 PRGF® consists on a lim-ited volume of plasma enriched in platelets and growth factors rapidly obtained from the patient and easily prepared and which may enhance and accelerate implant osseointegration.4,5

In the present study, the survival rates of

short BTI implants (7 mm to 8.5 mm) and extra-short BTI implants (5.5 mm and 6.5 mm) installed both in the maxilla and the mandible follow-ing consistent and predictable protocols are evaluated. Briefly, in the first study a total of 340 short BTI implants installed in 201 con-secutive patients were followed whereas in the second study 48 extra-short BTI implants installed in 35 patients were evaluated. In both implant studies an implant-based and a patient-based analysis of failures have been carried out.

MATERIAL AND METHODSThe protocols of both retrospective longitudi-nal studies were approved following the national and international (International Conference of Harmonization rules) policies on clinical studies. All implant installations were performed by two experienced surgeons and rehabilitations were done by 3 prosthodontists. The inclusion crite-ria included subjects demanding rehabilitation of posterior areas by means of dental implants with residual ridges that impede the insertion of implants longer than 8.5 mm. Subject selection was based on an absence of any local or systemic diseases that might contraindicate the treatment On the other hand, the exclusion criteria included subjects with systemic diseases and subjects tak-ing drugs that alter the bone metabolism. All sub-jects gave their written consent to carry out the treatment according to the described protocol.

In the short BTI implant study, subjects with short implants inserted in years 2001 to 2003 were included (follow-up period ranging from 5 to 8 years from the date of insertion). Subjects were treated with short BTI implants with a length raging from 7.0 to 8.5 mm. On the other hand, in the extra-short BTI implant study, subjects with

Anitua


Anitua

extra-short implants (5.5 and 6.5 mm in length) inserted between January 2007 and January 2009 were included. Only implants with at least 1 year of follow-up from their insertion were included.

Amoxicillin 1 g was administered 30 min-utes before the surgery and the same antibi-otic (500 mg every 8h) was prescribed to all patients for the next 6 days. Subjects received acetaminophen 1 gr. 1 hour before the sur-gery and for the next three days (1 gr. / 8 hours). Depending of the clinical situation, sub-jects were prescribed with magnesium met-amizol during two days after the surgery (1 gr. / 8 hours). Saline solution rinses (during 48 hours) and additional twice daily chlorhexidine (0.12% w/v) rinses were recommended until sutures were removed. The latter was mainly used in patients with poor oral hygienic situ-ation. Subjects were instructed how to main-tain proper oral hygiene around implants.

The clinical histories of all patients were evaluated carefully, and the surgical proce-dures were chosen in function of the subjects´ characteristics, the anatomic peculiarities of the insertion places and intrinsic properties of the different short and extra-short implants.

A complete radiological evaluation (conven-tional orthopantomogram plus analysis of three-dimensional reconstruction from CT scan using the BTI Scan program (Biotechnology Institute, Vitoria, Spain) was carried out. In addition, the surgery guides were elaborated and provisional and final prostheses adapted to each patient were prepared. All implant reception sites were prepared using a novel low-speed drilling pro-cedure (50 rpm) without irrigation. Before installation, implants were carefully embedded in liquid PRGF® with the aim of bioactivating the

implant surface. Liquid PRGF® was prepared from patient’s blood using the PRGF® system® (Vitoria, Spain). Briefly, peripheral blood from each patient was taken by venipuncture before surgery and placed directly into 9 mL blood collecting tubes (BTI blood collecting tubes®) which contain 3.8% (wt/vol) sodium citrate as anticoagulant. Liquid PRGF® was prepared by centrifugation at 580 g for 8 minutes at room temperature. The 1 mL plasma fraction located just above the red cell fraction was collected and activated with calcium chloride (50 µL PRGF® activator per mL of preparation) in order to initiate clotting and the continuous release of platelets’ growth factors and proteins.

Short and extra-short BTI implants (BTI Implant system, Biotechnology Institute, Vitoria, Spain) are characterized by their self-tapping apex with “drive” capacity. The same features allow a gentle approach in the posterior max-illa, because it allows the collection of bone by the implant during its advance whereas it avoids the danger of compressing the most apical bone against the mental nerve. In addi-tion, the special design of these short implants allow drilling 1 or 2 mm away from the men-tal nerve and then introducing the implant practically to the limit, placing it with excel-lent depth control. After treatment patients were called in for oral hygiene and clinical and radiographic examinations at least once a year.

The marginal bone loss around extra-short implants was measured mesially and distally in all available radiographs of each patient and data was grouped into 4 groups according to time elapsed since the date of insertion of the implants (from 0 to 6 months, 6 to 12 months, 12 to 24 months, and more than 24 months).

22 • Vol. 2, No. 5 • June 2010

Statistical analysesData collection and analysis was performed by two independent examiners (other than restorative dentists). Descriptive statistics were performed, absolute and relative frequency distributions were

calculated for qualitative variables, and means ± SD were calculated for quantitative variables. A database was employed for the analysis. Implant loss was the principal variable under study and included any implant lost because of biologi-cal (failure to achieve osseointegration or loss of acquired osseointegration) or biomechanical causes. The other variables included demographic factors, clinical factors, surgery-depending factors and prosthetic variables. The full list of variables under analysis included: age; gender; smoking habits; implant position (maxillary; mandibular); implant diameter, implant length, implant stag-ing (one-stage versus two-stage approach); spe-cial techniques including: vertical bone growth, ridge expansion and bone grafting. The overall survival rate of implants was estimated both by an implant-based and subject-based analysis. In the implant based analysis, each inserted implant was considered as the analysis unit whereas in the subject-based analysis each subject was fol-lowed up until the failure of his/her first implant. In both types of analysis, the implant survival as a function of the time was analyzed using a life-table analysis (Actuarial method), comparing

Table 1: Characteristics of the inserted short implants.

Figure 1: Anatomic distribution of the 340 short BTI implants. The y-axis shows the anatomical location of implants whereas the x-axis illustrates both the frequency of the inserted implants (lower side) and the jaw location (upper side).

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Anitua

the survival rates among the different variables with the Wilcoxon test (Gehan). Data analysis was performed with statistical software pack-age (SPSS v15.0 Inc., Chicago, IL, USA). The level of statistical significance was P < 0.05.

RESULTSIn the short BTI implant study, the mean (± S.D.) age of the 201 subjects was 60.2 (±10.4) years (range 28-93) at the beginning of the study. A total of 147 were female (73.1%). Forty eight subjects were smokers (23.9%). The frequency of the lengths and diameters of the 340 short BTI implants is shown in Table 1. Regarding implant position, 145 were inserted in the maxilla (42.6%), whereas 195 inserted in the mandible. The detailed anatomic distribution of the short BTI implants is presented in Figure 1. The surgical approach used for implant insertion was carefully evaluated. In fact, a total of 230 implants (67.6%) were placed using one-stage surgery and 110 fol-

lowed a two-stage surgery. A total of 24 implants (7.1%) were placed following special techniques. Regarding the prostheses employed, most of the implants supported fixed partial dentures (a total number of 279, 82.1%), 44 implants sup-ported hybrid overdentures (12.9%) and only 17 implants had unitary prostheses (5%). In addition, most of the prostheses were cemented (85.9%). Nine short BTI implants were immediate loaded.

At the end of the study period, the sur-vival rate using the actuarial method was 100% both for the implant and subject-based anal-ysis. The mean follow-up period for all the implants was 80.5 ± 8.9 months (6.7 years). Table 2 shows the length of observation by subject and by implant. Figures 2 to 7 illus-trate one clinical case involved in the study.

Regarding the study with extra-short BTI implants, the mean (± S.D.) age of the 35 sub-jects was 55.5 (±8.3) years (range 39-73) at the beginning of the study. Most of the patients

Table 2: Months of follow up by patients and implants from implant insertion.

24 • Vol. 2, No. 5 • June 2010

Figure 2: Example of one case involved in the study of short BTI implants. The case corresponds to a 65 year old female. Pre-operative radiograph.

Figure 3: Note the occlusal collapse and the lack of several posterior teeth.

Figure 4: The BTI Scan will facilitate correctly planning the case.

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were female (71.4%) and only 7 patients were smokers. Table 3 illustrates the frequency of the lengths and diameters of the 48 extra short BTI implants. Nineteen implants were installed in the upper maxilla and 29 in the lower max-illa (60.4%) according to Figure 8. Forty five out from forty eight implants were placed using two-stage surgery. Fifteen implants followed special techniques and only 3 implants were immediately loaded. Regarding the prostheses employed, all implants supported fixed partial dentures and 31 out from 48 implants were cemented.

The survival rate of the extra-short BTI implants was 97.9% for the implant-based analysis and 97.1% for the subject-based analysis. The mean follow-up period for all the implants was 23.4 ± 6.4 months. Only one implant was lost dur-ing the observation period. The mean (± S.D.) bone loss around implants was calculated. Table 4 shows the maximum, minimum and mean mar-ginal bone loss in function of the time elapse since the date of insertion of the extra-short BTI implants. Figures 9 to 11 illustrate one clini-cal case involved in the second clinical study.

DISCUSSIONImplant therapy based on the principle of implant osseointegration has been widely accepted and very well documented.6-9 However, the placement of long dental implants in some anatomical sites such as the posterior maxilla and mandible may be limited due to the residual ridge height. The pneumatization of the maxillary sinus and the atro-phic ridge resulting from tooth loss significantly reduce the available osseous tissue height in the posterior region, making implant placement more challenging. In fact, a study involving 431 partially edentulous patients revealed that the posterior

Figure 5: Rehabilitation of the lower maxilla using facing porcelain veneers.

Figure 6: Radiograph 3 years after treatment. Short implant has avoided the use of more aggressive treatments.

Figure 7: Final situation of the patient.

26 • Vol. 2, No. 5 • June 2010

Table 3: Characteristics of the Inserted Extra-Short BTI Implants.

existing available bone height was at least 6 mm in only 38% of maxillae and 50% of the mandibles.10

The use of short implants (< 8 mm) has historically been related with low success rates.11,12 However, current data suggest that the same level of clinical success may be reached for short implants compared with longer implants.13,14 In fact, survival rates from 88% to

100% have been reported for the atrophic man-dible15 whereas rehabilitation of partial edentu-lism and severely resorbed maxillae with short implants leads to survival rates around 95%.16

From a biomechanical point of view, the ratio-nale for the use of short implants is well docu-mented.17 It has been reported that when an implant is loaded the majority of the stress is distributed at the level of the first few threads to the crestal cortical bone; therefore once a mini-mum implant height is osseointegrated, implant width is more important than the additional

Figure 8: Anatomic distribution of the 48 extra-short BTI implants.

Figure 9: Example of one case involved in the study of extra-short BTI implants. Pre-operative radiograph.

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Table 4: The maximum, minimum and mean marginal bone loss in function of the time elapse since the date of insertion of the extra-short BTI implants.

length.17,18 In addition, eliminating or minimiz-ing the lateral force on the prosthesis and force distribution from splinting multiple implants play a significant role in reducing stress on implants and especially on short implants. Other potential advantages of using short implants in the pos-terior regions instead of longer ones include the reduction of the need for bone augmentation procedures prior or in conjunction with implant

placement and the reduced surgical risks of sinus perforation or mandibular paresthesia.19

In the first clinical study focused on eval-uating the long-term predictability of short BTI implants an overall survival of 100% was observed. Results are even superior to those reported recently in a retrospective study in which the survival rates of 532 short BTI implants installed in the posterior regions of the

28 • Vol. 2, No. 5 • June 2010

jaws and under different surgical approaches were 99.2% and 98.7% for the implant and subject-based analysis, respectively.1

Regarding the second study with extra-short

BTI implants, results showed that survival rate of implants was 97.9% for the implant-based analysis and 97.1% for the subject-based analy-sis with only one implant failure. One important issue when using these extra-short implants is the drilling sequence according to bone den-sity. In fact, we will find two different bone den-sities in most of the cases when inserting the implants in the posterior regions of the man-dible. One very dense cortical between 1000 and 1600 HU in the first 2-3 mm and a spongy bone between 400 and 100 HU along the rest. Additionally, these implants will be placed in two surgical steps independently to the torque achieved during insertion. Our recommendation is not to overcome 65 Ncm and obtain at least

Figure 10: It is possible to observe an extreme reabsorption with a ridge of 4 mm height. The unique predictable alternative to extra-short implants is the use of block grafts.

Figure 11: Radiograph 2 years after treatment. It is possible to distinguish the perfect bone stability around implants.

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30 Ncm. Placing these implants in one single surgery may provoke that the patient moves the implant during the period of bone remodeling.

As a general rule, extra-short implants constitute an excellent option to avoid can-tilevers and in some cases sinus lift surger-ies, especially when dealing with elder or high risk patients. Implants will always be splinted and the recommendation is to place the wider possible diameter (5 mm is the best option in the mandible and 5.5 mm or 6 mm in the max-illa). The switching platform concept enables obtaining a 4 mm emergency profile and minimizing soft tissue reception during time. The fact of placing the implant in the distal root will make the emergence profile design much easier. To improve biomechanics we will always try to place one implant splinted to another two or at least just to another one.

In summary, the present study reports on the clinical daily use of short and extra-short BTI implants. In our daily practice, the possibil-ity to use these implants in a predictable way enables reducing the indications for especial procedures like sinus lift and bone grafting pro-cedures. The data report in this study might help clinicians to improve their decision-making with the aim of enhancing implant success. L

Correspondence:Dr. Eduardo Anitua Instituto Eduardo Anitua; c/ Jose Maria Cajigal 19 10005 Vitoria (Spain)Phone: +34 945160652 Fax: +34 945155095E-mail: [email protected]

DisclosureDr. Anitua is the scientific director of BTI Biotechnology Institute.

References1. Anitua E, Orive G, Aguirre JJ, Andía I. 5 year clinical evaluation of short dental

implants placed in posterior areas: a retrospective study. J Periodontol 2008; 79: 42-48.

2. Anitua E, Orive G, Aguirre JJ, Ardanza B, Andía I. 5-year clinical experience with BTI dental implants: risk factors for implant failure. J Clin Periodontology 2008; 35: 724-732.

3. Anitua E. Enhancement of osseointegration by generating a dynamic implant surface. J Oral Implant 2006; 32: 72-76.

4. Anitua E, Orive G, Plá R, Román P, Serrano V, Andía I. The effects of PRGF® on bone regeneration and on titanium osseointegration in goats: a histologic and histomorphometric study. J Biomed Mater Res A 2009; 91: 158-165.

5. Anitua E, Sánchez M, Orive G, Andía I. The potential impact of the preparation rich in growth factors (PRGF®) in different medical fields. Biomaterials 2007; 28: 4551-4560.

6. Jemt T, Lekholm U, Adell R. Osseointegrated implants in the treatment of partially edentulous patients: A preliminary study on 876 consecutively placed fixtures. Int J Oral Maxillofac Implants 1989; 4: 211-217.

7. Brånemark PI, Svensson B, van Steenberghe D. Ten year survival of fixed protheses on four or six implants ad modum Brånemark in full edentulism. Clin Oral Implants Res 1995; 6: 227-231.

8. Anitua E. Plasma rich in growth factors: preliminary results of the use in the preparation of future sites for implants. Int J Oral Maxillofac Implants 1999; 14: 529-535.

9. Buser D, Ingimarsson S, Dula K, Lussi A, Hirt HP, Belser UC. Long-term stability of osseointegrated implants in augmented bone: a 5-year prospective study in partially edentulous patients. Int J Periodont Rest Dent 2002; 22: 109-117.

10. Oikarinen K, Raustia AM, Hartikainen M. General and local contradictions for endosteal implants, an epidemiological panoramic radiographic study in 65-year old subjects. Com Dent Oral Epidemiol 1995; 23: 114-118.

11. Bahat O. Treatment planning and placement of dental implants in the posterior maxillae: report on 732 consecutive Nobelpharma implants. Int J Oral Maxillofac Implants 1993; 8: 151-161.

12. Pierrisnard L, Renouard F, Renault P, Barquinis M, Influence of implant length and cortical anchorage on implant stress distribution. Clin Implant Dent Relat Res 2003; 5: 254-26213. Fugazzotto PA, Beagle JR, Ganeles J, Jaffin R, Vlassis J, Kumar A. Success and failure rates of 9 mm or shorter implants in the replacement of missing maxillary molars when restored with individual crowns: preliminary results 0 to 84 months in function. A retrospective study. J Periodontol 2004; 75: 327-332.

14. Goené R, et al. Performance of short implants in partial restorations: 3-year follow-up of Osseotite implants. Implant Dent 2005; 14: 274-280.

15. Stellingsma C, Vissink A, Meijer HJ, Kuiper C, Raghoebar GM. Implantology in the severely resorbed edentulous mandible. Crit Rev Oral Biol Med 2004; 15: 240-248.

16. Renouard F, Nisand D. Short implants in the severely resorbed maxilla: a 2-year retrospective clinical study. Clin Implant Dent Relat Res 2005; 7(Suppl 1): S104-110.

17. Griffin TJ, Cheung WS. The use of short implants in posterior areas with reduced bone height: a retrospective investigation. J Prosthetic Dent 2004; 92: 139-144.

18. Anitua E, Tapia R, Luzuriaga F, Orive G. Influence of implant length, diameter and geometry on stress distribution using finite element analysis. Int J Periodont Rest Dent 2010; 30: 89-95.

19. Misch CE, Steigenga J, Barboza E, Misch-Dietsh F, Cianciola LJ, Kazor C. Short dental implants in posterior partial edentulism: a multicenter retrospective 6-year case series study. J Periodontol 2006; 77: 1340-1347.

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Kurtzman et al

Background: Dental implants are a pros-thetically driven treatment with a surgical com-ponent. It is important to guide the surgical placement so that prosthetics are uncompli-cated and predictable. Surgical stents pro-vide communication between the surgeon and restoring dentist so that implant placement is at the ideal prosthetic position and angulation. Methods: A 3/32 inch twist drill is placed into a slow speed hand piece and a pilot hole is cre-ated through the denture tooth spacing it at the center of the tooth in both the buccal/lingual and mesial/distal dimensions. Angulation should fol-low the long axis of the adjacent teeth so that the implant parallels the roots of those teeth and is not directed into the natural teeth. A pin is placed into the hole within the cast and the Guide Right sleeve is placed upon the pin and a light-curable resin is used to fixate the sleeve in position and create an index to the remaining teeth. The guide can then be carried intraorally to radiographi-cally verify fixture angulation prior to initiation of surgery and provides a stable guide during use of the osteotomy drills at fixture placement.

Results: The custom made stents described in this article are easy to fabricate and help the restoring dentist ensure accurate communica-tion about implant to the surgeon. Additionally, these stents have the ability to avoid complica-tions such as image distortion from metal sleeves during computed tomography evaluations.

Conclusions: Implant dentistry is a prostheti-cally driven treatment modality and commu-nication between the restoring dentist and surgeon is critical to treatment success. The surgical stent is utilized to communicate the desired position and angulation of the implant so that the restorative phase of treatment does not encounter problems that can compromise the esthetic outcome and also complicate oral hygiene for the patient. The Guide Right sur-gical stent system is an easy to use method for in-office fabrication of implant stents for the par-tially edentulous arch. This technique allows the desired/planned implant position and angula-tion to be easily communicated to the surgeon.

Simplifying Implant Placement with Partially Edentulous Arch Surgical Stents

Gregori M. Kurtzman, DDS1 • Douglas Dompkowski, DDS2

1Private practice, Silver Springs, Maryland, USA2 Private practice, Bethesda, Maryland, USA. Clinical associate professor at the University of Maryland/ Dental School,

Baltimore, Maryland, USA

Abstract

KEY WORDS: Dental implants, surgical stent, CBCT, dental labratory


34 • Vol. 2, No. 5 • June 2010

Kurtzman et al

INTRODUCTIONProper implant placement has become less of a prosthetic dilemma with the use of surgical stents.1-3 Surgical stents also provide communication between the surgeon and restoring dentist, so that the implant is placed at the ideal prosthetic position and angulations. We will be addressing simple tech-niques in this article for fabrication of surgical stents.

Surgical StentsImplant surgical stents for the partially edentulous arch can range from the simple to the complex with varying costs and technical expertise involved in their fabrication. Simple stents vary from use of denture teeth to metal tubes in an acrylic or vac-uform template. These require minimal technical expertise and are relatively inexpensive to fabricate. Whereas, complex stents may require a CT or cone beam scan and may be fabricated through a cad/cam process. These raise the total treatment fee higher as the scan has a fee and the stent involves a costly laboratory fee and may place the treat-ment beyond the financial abilities of the patient.

Stents utilized in partially edentulous arches have the benefit of gaining stability from the remaining teeth in the arch. When standard radiographs and clinical evaluation determine that there is adequate bone height and width, a simple surgical stent can provide the guid-ance required to position the fixtures properly.

Treatment of the partially edentulous arch with dental implants is less of a challenge then treatment of the fully edentulous arch.4-6 Fabrication of surgical stents for these par-tially edentulous cases can be easily accom-plished in the office at minimal time and cost.

Surgical stents can be broadly divided into two basic types; restrictive and non-restrictive.

A restrictive stent guides the surgeon as to the exact position and angulation of the implant place-ment. The benefit of these type stents is that the restoring dentist receives back implants placed in the exact planned position they planned when the surgeon uses the guide for placement. Whereas, a non-restrictive stent allows more latitude to the surgeon and the result may be an implant placed at an angulation or a position that complicates the restoration process. As such, the authors, advo-cates preplanning and the use of restrictive type surgical stents. With this in mind, the Guide Right stent system permits easy fabrication of restrictive implant surgical stents for various clinical situa-tions that may be encountered. We will address the following types of clinical situations that are commonly encountered; standard placement, placement in restricted vertical cases and place-ment in conjunction with CT and cone beam scans.

Use of metal tubes to guide the osteotomy drills is not a new concept and has been addressed in simple to complex stent designs. These have pros and cons to the basic concept. The metal tubes do not allow the osteotomy drill to diverge from the trajectory of the tube and, due to their hardness, the drill can not create shaving debris during its use as can be observed with pilot holes through denture teeth. The drawback to use of metal tubes in the past has been in order to retain the tube in the stent, the entire tube had to be encased in resin or acrylic. This prevented the tube from dis-lodging from the stent but resulted in a bulky stent which can obscure the surgical aspect of the crest.

An ideal stent using metal guidance tubes would therefore require only enough resin/acrylic to stabilize the stent on the remaining teeth and to retain the metal tube. A majority of the stent bulk would be absent so that the surgeon had

Kurtzman et al


Kurtzman et al

clear visualization of the crest where the oste-otomy drill was making contact. This would fulfill the accepted criteria of an implant surgical stent without hampering the visibility during surgery.

The Guide Right™ (DePlaque, Victor, NY) system provides a metal or ceramic tube to be incorporated into a stent quickly and inexpen-sively. This is composed of guide posts and vari-ous guide sleeves for planning and fabrication of implant surgical stents. The posts are available as a straight, an angled and an offset pin. Straight posts have a 2.0mm portion that corresponds to a 3/32 inch drill used to create the pilot hole on the cast. Angled posts are available with both a 3 and 6 degree angulation for use in the ante-rior where angled abutments will be utilized. The offset posts allow the practitioner to move the sleeve from 0.5 to 2.0mm from the guide hole placed into the cast correcting positioning prior to stent fabrication. Additionally, a magnetic post is provided for use with the open sleeves in both a straight and offset version. A set of guide posts is also provided for use with the ceramic sleeves that mimic the other posts discussed.

Several different guide sleeves are available from Guide Right, which provide for various clini-cal situations. All sleeves contain a retentive element to retain the sleeve within the surgical stent. Stainless steel sleeves are available as both straight and angled versions with each hav-ing a bracket attached to the lingual side of the sleeve. The straight sleeves are provided in 3.0, 4.5 and, 5.3mm diameters. Guide sleeve inserts are available to permit use of the Guide Right surgical stent with each osteotomy drill to be used, ensuring that the drills following the initial pilot do not diverge from the intended angula-tion. The angled guide sleeve is ideal for poste-rior applications when vertical dimensions may not allow insertion of the drill into the straight guide sleeve. To accommodate restricted verti-cal dimensions an open sleeve was developed. As with the stainless steel sleeves, a retentive button is present to lock it into the resin used to fabricate the stent. The buccal portion of these sleeves is fully open allowing guidance of the osteotomy drill but not hampering its insertion into the guide. The open sleeves require use of a

Figure 1: Denture tooth placed in the edentulous space on the cast.

Figure 2: A 3/32” twist drill used to create a pilot hole through the denture tooth on the cast.

36 • Vol. 2, No. 5 • June 2010

magnetic post when fabricating the stent so that the sleeve remains where positioned as the stent is fabricated. With the growing use of CT and cone beam scans, metallic sleeves pose issues due to scatter in the images. Ceramic guide sleeves were fabricated to circumvent this issue allowing clear visualization of the sleeve in the scan but eliminating all scatter that may hamper planning.

Standard Implant Placement StentsAt the planning appointment, impressions for study models are made and casts fabricated. Denture teeth are placed into the edentulous space and affixed to the cast with wax to stabilize the tooth. The tooth is placed in the ideal position esthetically following the adjacent teeth (Fig. 1). If immediate implant placement at the time of extraction is planned, then

Figure 3: A guide pin is placed into the pilot hole on the cast to verify position and angulation.

Figure 4: A stainless steel Guide-Right sleeve is placed on the guide pin with the retentive bracket toward the lingual.

Figure 5: Triad gel applied to the lingual of the adjacent teeth and the retentive bracket of the Guide Right sleeve.

Figure 6: Completed Guide Right surgical stent fabricated with Triad gel carried over the incisal edge to create stability of the stent to the adjacent stent.

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the intact tooth is left on the cast or the missing portions of the tooth are built up using composite.

A 3/32 inch twist drill is placed into a slow speed handpiece and a pilot hole is created through the denture tooth spacing it at the center of the tooth in both the buccal/lingual and mesial/distal dimensions (Fig. 2). Angulation should follow the long axis of the adjacent teeth so that the implant parallels the roots of those teeth and is not directed into the natural teeth. Should a screw retained restoration be desired instead of a cement retained crown, then the screw access

Figure 7: Guide Right surgical stent shown intraorally.

Figure 8: Radiograph of the Guide Right surgical stent intraorally showing projection of the long axis of the implant to be placed using the stent.

Figure 9: Radiograph with the Guide Right protractor placed over an X-ray to determine the angle if correction is needed.

38 • Vol. 2, No. 5 • June 2010

Figure 10: A 2mm osteotomy drill being used through the Guide Right surgical stent intraorally.

Figure 11: A radiograph of a guide pin in the initial osteotomy made using the Guide Right surgical stent taken to verify position and parallelism relative to the adjacent teeth.

Figure 12: Radiographs of the implant placed using the Guide Right surgical stent demonstrating !nal positioning relative to the stents sleeve.

can be designed at this stage to emerge lingual to the tooth’s incisal edge. The denture tooth is next removed from the cast and a guide pin is inserted into the pilot hole in the cast (Fig. 3). This is performed to verify the position and angu-lation and if necessary correction may be per-formed at this time before the stent is fabricated.

The cast is lightly lubricated with a water sol-uble lubricant to prevent adhesion of the stent to the cast. A stainless steel guide sleeve is

slipped over the guide post and the bracket posi-tioned on the lingual of the cast (Fig. 4). Triad gel (or other appropriate material) is applied to the bracket and lingual of the adjacent teeth, car-rying it over the incisal edges (or occlusal sur-faces) of the adjacent teeth to provide stability from lateral displacement of the stent intraorally and is light-cured (Fig. 5). The guide post is removed and the stent removed from the cast to finish and polish the peripheral edges (Fig. 6).

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Figure 13: A radiograph showing an open Guide Right sleeve for placement of a lower !rst molar.

Figure 14: Osteotomy drill being used in an open sleeve Guide Right surgical stent for placement of a lower !rst molar.

Figure 15: Final implant placement achieved using the open sleeve Guide Right surgical stent.

Figure 16: CT scan tangential view showing three stainless steel sleeves of the same patient showing in Figure 17, demonstrating scatter and di"culty identifying the sleeves.

40 • Vol. 2, No. 5 • June 2010

The completed stent is disinfected in cold ster-ilizing solution and is ready to try in intraorally to verify fit and stability (Fig. 7). It is important that the stent is stable and have no rocking. Should the stent not be stable adjustment of the resin interproximally may be necessary as this may be preventing full seating of the stent. A radiograph is taken with the stent in place to verify trajectory compared to the adjacent natural tooth roots (Fig. 8). If the angle of the guide sleeve is not aligned correctly, the Guide Right Protractor is used to determine the angle of correction. The protrac-tor is placed over the x-ray and the correct angle determined (Fig. 9) Pre-bent angled guide posts are available in intervals of 2 degrees up to 14. Offset guide posts can also be bent to the desired

angle with the Guide Right Bending Tool. Follow-ing local anesthetic placement the initial osteotomy is created with a 2mm pilot drill for the implant sys-tem being used (Fig. 10). This may be done either flapless or with a traditional flap depending on the practitioners preference. The stent is removed and a sterile guide post is inserted into the osteotomy intraorally and a radiograph taken to verify implant

Figure 17: CT scan tangential view showing three ceramic sleeves in the edentulous space demonstrating clear visibility of the sleeves with minimal scatter.

Figure 18: Cross sectional view with minimal scatter also indicating some alteration in the angle of the sleeve is needed.

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Figure 19: Ceramic Guide Right sleeves in sizes (l-r) 3, 4 and 5mm, showing the retentive element of the sleeve.

Figure 20: Ceramic Guide Right sleeve placed on the post on the model with the retention portion of the sleeve positioned on the palatal.

Figure 22: Radiograph of the !nal implant placement and ceramic sleeve used to achieve guided placement.

Figure 21: A Guide Right surgical stent with a ceramic sleeve shown intraorally for placement of an upper premolar.

position (Fig. 11). Should redirection be neces-sary, additional correction can be made at this time.

Normal implant surgical protocol is followed and the osteotomy is enlarged to the desired diameter and the implant is placed. A radio-graph may be taken at this time with the stent intraorally to document alignment of the stents sleeve and long axis of the implant (Fig. 12).

Posterior Implant Placement with Restricted Vertical DimensionThe Guide Right open sleeves are ideally designed for clinical situations when vertical heights will not permit the osteotomy drill from being inserted into the sleeve within the stent. The open buccal aspect of the sleeve allows an additional 3mm of clearance for the drill to be inserted (from the buc-

42 • Vol. 2, No. 5 • June 2010

cal) without interference from the opposing arch. The stent is fabricated in a similar manner to

the standard Guide Right surgical stent except a magnetic post is used in place of the standard guide post. Either a denture tooth is placed into the edentulous space or one of the Guide Right setup disks is utilized. Should the setup disk be used, a disk corresponding to the diameter of the tooth to be placed is placed onto the cast. The hole in the setup disk positions the center of the implant in the center of the space so that the final crown has equal flare mesially and distally. A 3/32 inch twist drill is introduced through the center of the denture tooth or setup disk to create the hole in the cast. A magnetic guide post is placed into the hole in the cast and an open sleeve is placed on the guide post with the retention portion of the sleeve positioned to the lingual. It is suggested that the open portion of the sleeve may be directed toward the mesial buccal (position the retentive element to the distal lingual) as this will aid inser-tion of the osteotomy drill. The stent is completed by application of Triad gel or other appropriate acrylic to complete the stent as previously outlined.

The stent can then be inserted and a radiograph taken to verify positioning of the guide sleeve (Fig. 13). During surgical use of the stent, the osteotomy drill is guided along the closed portion of the sleeve to allow it to be guided by the stent (Fig. 14). Follow-ing development of the osteotomy with the Guide Right open sleeve stent the implant is placed based on the implant manufacturers instructions (Fig. 15).

Surgical Stents in Conjunction with CT and Cone Beam ScansAs CT and cone beam scans are becoming more popular in implant treatment metal containing stents may result in scatter and poor visibility on

the images7,8 (Fig. 16). Ceramic sleeves in stents provide minimal scatter but clear visibility on the scans and radiographs. They may be used in a scan taken prior to the surgical phase of treat-ment to verify the angle of the guide sleeve or allow correction of the angle prior to implant placement (Fig. 17,18). The ceramic sleeves are available in a 3.0, 4.0 and 5.0mm inside diameter with a retentive bracket with undercuts to attach the ceramic sleeve to the body of the template. The bracket is fused to the body of the sleeve at a high temperature (Fig. 19) and is positioned on the lingual/palatal on the guide post in the cast (Fig. 20) and then the stent is completed with Triad gel or other appropriate material.

Fabrication of the Guide Right stent with ceramic guide sleeves is similar to the stan-dard Guide Right stent with metal sleeves. Care should be taken not to torque the osteotomy drill laterally while in the thin walled sleeve as this may cause fracture of the sleeve or its retentive bracket. Metal sleeve inserts are available for use in the larger ceramic sleeves to allow guid-ance of each drill to be used during the osteot-omy preparation. As with the other Guide Right stents, the stent is tried in prior to surgical use (Fig. 21). A cone beam scan can be taken to verify the proposed trajectory in a buccal-lingual and mesial-distal direction. The ceramic sleeve is clearly visible on the subsequent x-ray (Fig. 22).

CONCLUSIONImplant dentistry is a prosthetically driven treat-ment modality and communication between the restoring dentist and surgeon is critical to treat-ment success. As part of this use of surgical stents communicate the desired position and angulation of the implant so that the restorative

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phase of treatment does not encounter prob-lems that can compromise the esthetic out-come and also complicate oral hygiene for the patient. The Guide Right surgical stent system is an easy to use method for in-office fabrica-tion of implant stents for the partially edentu-lous arch. This technique allows the desired/planned implant position and angulation to be easily communicated to the surgeon. L

Correspondence:Gregori M. Kurtzman, DDS3801 International Drive, Suite 102Silver Spring, MD 20906301-598-3500301-598-9046 (Fax)[email protected]

Acknowledgment:The authors would like to thank Dr. Sean Meitner for reviewing the article and his assistance with images.

DisclosureThe author reports no conflicts of interest with anything mentioned in this article.

References1. Binon PP. Treatment planning complications and surgical miscues. J Oral

Maxillofac Surg. 2007 Jul;65(7 Suppl 1):73-92. Erratum in: J Oral Maxillofac Surg. 2008;66(10):2195-2196.

2. Rosenlicht JL. Simplified implant dentistry for the restorative dentist: integrating the team approach. Int J Dent Symp. 1995;3(1):56-59.

3. John V, Gossweiler M. Implant treatment planning and rehabilitation of the anterior maxilla: Part 1. J Indiana Dent Assoc 2001; 80(2):20-24.

4. Small BW. Surgical templates for function and esthetics in dental implants. Gen Dent. 2001;49(1):30-32, 34.

5. Wat PY, Chow TW, Luk HW, Comfort MB. Precision surgical template for implant placement: a new systematic approach. Clin Implant Dent Relat Res 2002;4(2):88-92.

6. Mason WE, Rugani FC.: Prosthetically determined implant placement for the partially edentulous ridge: a reality today. J Mich Dent Assoc 1999;81(9):28, 30, 32, 34-37.

7. Cehreli MC, Sahin S. Fabrication of a dual-purpose surgical template for correct labiopalatal positioning of dental implants. Int J Oral Maxillofac Implants 2000 ; 15(2):278-282.

8. Kopp KC, Koslow AH, Abdo OS. Predictable implant placement with a diagnostic/surgical template and advanced radiographic imaging. J Prosthet Dent 2003; 89(6):611-615.

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Noumbissi et al

Background: Maxillary sinus augmentation with deproteinized mineralized bovine bone xenografts (DMBBX) alone or in combination with deminer-alized freeze-dried bone allografts (DFDBA) has been well documented. Recently, articles have been published evaluating histologically, histo-morphometrically, and clinically the efficacy of using human mineralized cortical, cancellous, or a combination of both for atrophic maxillary sinuses. This study clinically, histologically and histomorphometrically compares three graft com-binations currently used by practitioners in the augmentation of atrophic human maxillary sinuses.

Methods: Study participants (n = 18) were par-tially or completely edentulous patients who presented with bilateral or unilateral atrophic posterior maxillary sinuses. A total of twenty two sinuses were grafted; they consisted of

MSDBA 100% cancellous (n = 13), MSDBAM 1:1 Cortico-cancellous (n = 6) and DFDBA/DMBBX 1:1 (n = 4). Biopsy cores were har-vested in time frames ranging from 6 months to 12 months. Dental implants were placed into the grafted bone immediately after core collection.

Results: All bone grafts resulted in new bone for-mation and all implants osseointegrated. MSDBA and MSDBAM graft turnover was faster than the DMBBX/DFDBA grafts. No complications with any of the grafts or implants were noted.

Conclusions: Graft resorption and replace-ment by new bone occurred at a faster rate with MSDBA and MSDBAM compared to the bovine component (DMBBX) of the xeno-grafts; however, no differences in graft sta-bility or osseointegration were noted.

A Comparative Clinical, Histological and Histomorphometric Study of Mineralized Allograft

and Xenograft Materials in the Treatment of Atrophic Maxillary Sinuses

Sammy S. Noumbissi, DDS MS1 • Alejandro J. Kleinman, DDS MS2

1. Private Practice Limited to Implant Dentistry, Silver Spring, Maryland, USA2. Associate Professor, Graduate Program in Implant Dentistry, Loma Linda University,

Loma Linda, California, USA

Abstract

KEY WORDS: Bone graft, autograft, allograft, xenograft, sinus augmentation, cortical, cancellous, mineralized bone allograft, histology, histomorphometry


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INTRODUCTIONImplant placement in the posterior maxillary jaw is often complicated by a lack of available bone. After tooth extraction, rapid resorption of the residual maxillary ridge typically occurs in the buccolingual and occlusoapical direc-tions, and often results in a “knife-edge” ridge deformity.1-2 Use of a removable prosthe-sis, the presence of periodontal disease and physical trauma can exacerbate this resorp-tion process.1-2 Pneumatization and enlarge-ment of the sinus can further diminish or eliminate alveolar bone height, which can com-plicate the ability to place dental implants.1-2

Onlay ridge grafting3-4 and subantral aug-mentation via a crestal1,4 or lateral window (modified Caldwell-Luc technique)7-8 approach are commonly used to increase the volume of available bone for implant placement in the pos-terior maxilla. Autogenous bone is currently the only available graft material capable of growing

new bone through the processes of osteogen-esis, osteoinduction and osteoconduction, and is thus widely viewed as the graft material of choice for these procedures.9 Several skeletal locations have been used as donor sites for har-vesting autogenous bone, including the ilium,10 calvarium,11 tibia,12 fibula,13 scapula,14 man-dibular symphysis15 and mandibular ramus.16 Variations in the dimensions, quality and quan-tity of obtainable bone, increased operating time and cost for bone harvesting, and donor site morbidity are some of the inherent limita-tions associated with the use of autografts.2, 4

Deproteinized mineralized bovine bone xenograft (DMBBX) has been widely used as a substitute for autogenous bone. To prevent antigenicity, the bovine bone tissue is chemi-cally treated to remove its organic components (calcium-deficient carbonate apatite).17 When processed under low heat (300° C), the basic trabecular architecture, porosity and apatite

Figure 1: MSDBA: High-power (x10) New bone formation (NB) on the surfaces of MSDBA (P).

Figure 2: DMBBX/DFDBA: New trabeculae (NB) bridges DMBBX (B) particles, while DFDBA particles (D) are incorporated and turning over into new bone (Magni!cation x10).

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crystalline content of the natural bone are main-tained.17 The resulting DMBBX is a mineralized xenograft that undergoes physiologic remod-eling and incorporation into the host tissue at a very slow rate over time.17-18 In one canine study,1 for example, DMBBX and B-tricalcium phosphate were placed into surgically created defects. By 24 months, all B-tricalcium phos-phate graft particles had resorbed, whereas DMBBX particles still occupied a remark-able area fraction without discernable resorp-tion after 6 months.18 For this reason, some clinicians advocate only using DMBBX as a composite graft with autogenous or deminer-alized freeze-dried bone allograft (DFDBA).17

Demineralizing allogenic bone exposes the bone morphogenetic protein (BMP) present in the tissue, which is capable of inducing host mesenchymal stem cells to differentiate into osteoblasts and cause osteogenesis throughout the implanted area (osteoinduction).19 Several

variables can negatively affect the osteoinduc-tive capacity of the BMP in DFDBA, however, including donor age20 and factors in tissue pro-cessing (e.g. retrieval time and temperature,21 sterilization method22); consequently, clini-cal results with DFDBA have sometimes been unpredictable. The influence of mineraliza-tion (calcium) on the clinical performance of allogenic bone grafts still remains unclear.17

This article reports on the results of a pro-spective study where the clinical, histologic and histomorphometric results of mineralized cancellous allografts, mineralized cortico-can-cellous allografts and mineralized bovine com-posite grafts placed in human pneumatized maxillary sinuses are evaluated and compared.

MATERIALS AND METHODSPatient Selection Candidates for this study were consecutive healthy patients from two private practices who

Figure 3: DMBBX/DFDBA: High-power (x10) magni!cation shows new bone formation (NB) on the surface and inside a former Haversian canal (box) of a large DMBBX (B) particle.

Figure 4: MSDBA: Thick, dense trabeculae (NB) surrounded some MSDBA particles (P) or incorporated them so well that the graft particles were di"cult to distinguish (magni!cation x10).

50 • Vol. 2, No. 5 • June 2010

desired dental implants, but who presented with less than 5 mm of residual bone inferior to the maxillary sinus floor. Patients with seri-ous health issues (e.g. uncontrolled diabetes, destructive parafunctional habits, pregnancy, mental or psychological impairment), a history of poor oral hygiene and smokers were excluded from the study. Medical and dental histories were reviewed, complete oral and radiographic evaluations were performed and mounted study casts were fabricated for each patient. A surgi-cal template to guide placement of the implants relative to the planned restoration was cre-ated from a prosthetic wax-up or by means of 3D imaging technology. The treatment plan, study requirements and alternative options were reviewed, and each patient signed an informed consent form prior to be admitted into surgery.

Treatment Phase IThe day before surgery, patients commenced a 10-day regimen of prophylactic antibiot-

ics (amoxicillin or erythromycin, 2 g: 1 tab-let 4 times daily). Immediately before surgery, patients received ibuprofen (800 mg) and were asked to rinse with 0.12% chlorhexidine diglu-conate for 2 minutes. Anesthesia was admin-istered by local infiltration using mepivacaine hydrochloride 2% (Polocaine, AstraZenica Phar-maceuticals LP, Wilmington, DE) with 1:20,000 epinephrine (Astra USA Inc., Westborough, MA). An open sinus grafting procedure uti-lizing a lateral window approach7-8 was used.

MSDBA and MSDBAM (Puros Bone Partic-ulate, Zimmer Dental Inc., Carlsbad, CA) grafts consisted respectively of a 100% solvent-dehy-drated mineralized large particle cancellous bone allograft and a 1:1 large particle solvent-dehydrated mineralized cortical and cancellous bone allograft mixture, which was prepared from cancellous and cortical donor bone treated for biological safety through a 5-step proprietary process (Tutoplast Process, Tutogen Medi-cal GmbH, Neunkirchen am Brand, Germany):

Figure 5: DMBBX/DFDBA: A good trabecular pattern (NB) surrounded multiple large DMBBX particles (magni!cation x10).

Figure 6: DMBBX/DFDBA: Thick trabeculae (NB) formed on the surfaces and bridged large residual DMBBX (B) particles (magni!cation x10).

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Figure 7: MSDBA Graft: Two MSDBA particles (P) were encapsulated and connected by newly formed bone (NB) that they were di"cult to distinguish even under high-power magni!cation (x10).

Figure 8: MSDBA Graft: Under high-power (x10) magni!cation, di#erentiation can be made between new bone formation (NB) and small incorporated MSDBA graft particles (P).

Figure 9: MSDBA Graft: MSDBA particles (P) were di"cult to distinguish in newly formed bone (NB), and the lamellar pattern of mature bone (L) could be seen around the MSDBA particles.

Figure 10: Bovine core formed mostly of large DMBBX particles surrounded by islets of new bone.

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(1) delipidization, (2) osmotic contrast treat-ment, (3) oxidation treatment with hydrogen peroxide, (4) solvent dehydration and (5) lim-ited dose Gamma irradiation (17.8 GY).23 The third set of grafts observed consisted of a 1:1 combination of DMBBX (Bio-Oss, Geistlich, Wolhusen, Switzerland) and DFDBA (Mus-culoskeletal Transplant Foundation, Holmdel, NJ; particle size 750-1000 microns). If the Schneiderian membrane tore during surgery, a bioabsorbable collagen membrane (Bio-Mend, Zimmer Dental Inc., Carlsbad, CA) was placed over the perforation with a 2-3 mm over-lap beyond the tear prior to graft placement.24

After grafting, the lateral sinus wall was cov-ered with a collagen membrane (Bio-Mend), and the soft tissues were approximated and sutured (5-0, Vicryl, Ethicon, Sommerfield, NJ). Postoperative instructions included rins-ing 3 times daily for 2 weeks with 0.12% chlorhexidine gluconate (Peridex, Procter and Gamble, Cincinnati, OH). Patients were instructed to try not to blow their noses for

at least 3 days after surgery, and to cough or sneeze with an open mouth to prevent dis-lodging the graft. In addition, the application of pressure and ice at the surgical site, eleva-tion of the head and rest were recommended. To control pain and discomfort, ibuprofen was prescribed as a postoperative analgesic (800 mg: 1 tablet 3 times daily for at least 3 days). The sutures were removed approximately one week later after soft tissue maturation.

Treatment Phase IIThe patients were reappointed periodically every forty five days for a period ranging from 6 to 12 months after graft placement and a panoramic radiograph and/or cone beam com-puted tomography scan (Prexion 3D, Tera Recon) was taken to assess the radiographic appearance and bone density of the grafted sinuses as well as the volume and/or height of new bone between the residual crest ridge and the elevated sinus floor. The DMBBX/DFDBA cores were all harvested at ten (10)

Figure 11: DMBBX particle surrounded by new bone, no DFDBA present at 10 months.

Figure 12: Low magni!cation MSDBA.

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Figure 13: Polarized view of NB formation around and within MSDBA particles.

Figure 14: x10 magni!cation showing various stages of MSDBA turning over into NB.

Figure 15: MSDBA particle almost completely turned over into immature NB.

Figure 16: High magni!cation NB forming at the edges and within MSDBA (P) particle.

Figure 17: Large amounts of NB formation within a MSDBA core.

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months. Seven of the twelve MSDBAM cores were harvested at six (6) months and the other five at twelve (12) months. Six of the thir-teen cancellous (MSDBA) cores were har-vested at six (6) months and the other seven cores were harvested at ten (10) months. Biopsy cores were collected at the planned implantation site in a vertical direction. The 2-mm-diameter biopsy was harvested with a standardized trephine drill from the alveolar crest and ended 2 mm short of the most supe-rior part of the graft. The collected core was kept in the trephine drill and sent to the labo-ratory for processing, and the biopsy site was converted to an implantation site by means of lateral bone condensation in graduated diam-eters but stopping 0.6 to 1.2 mm short of the selected implant diameter for the site. The implants were inserted; the fixture mounts were removed and cover screws installed. The soft tissue was sutured (5-0 Vicryl) over the implants for a two-stage surgical proto-col. The sutures were removed approximately one week later after soft tissue maturation.

Histologic and Histomorphometric AnalysesOnce in the histology laboratory, the biopsy specimens were removed from the trephine drills, fixed in 10% buffered formalin for 4 to 8 weeks then dehydrated in ascending concentra-tions of alcohol and embedded in specialized resin (Technovit 7200 VLC, Kulzer, Wehrheim, Germany). Upon completion of polymerization, the blocks were mounted onto slides and initial midaxial sections of 200 microns were made by means of a cutting-grinding system (Exact Medical Instruments, Oklahoma City, OK). These sections were subsequently ground to 40 µm to 50 µm and used unstained for histo-morphometric analysis and light fluorescence microscopy. The sections were then ground to particle sizes ranging from 10 µm to 20 µm and stained with 1% toluidine blue for histologic

Figure 18: High magni!cation of !gure #17.

Figure 19: Low magni!cation Core cancellous.

Figure 20: Cancellous particle repopulated by osteocytes.

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analysis by means of bright field and polarized microscopic evaluation at x20 magnification in a protocol previously described by Donath.28

The undecalcified sections were analyzed histomorphometrically using backscattered electron image analysis. Before placing the specimens in the scanning electron microscope chamber, the specimen surfaces were plated with gold palladium. Backscattered electron

images were obtained in field sizes of 2 mm x 2 mm, digitized as a 256 x 256 array of 8-bit den-sity values, and transferred into a microcomputer. The histomorphometric analysis was performed on a computer (Apple, Cupertino, CA) using the public domain image program developed at the U.S. National Institutes of Health (available on the Internet at http://rsb.info.nih.gov.nih-image/).

Volume fractions of the following tissue com-

Figure 21: NB formation within particle. Figure 22: Cancellous particle repopulated by osteocytes.

Figure 23: Three levels of bone maturity: 1) Cancellous part, 2) Mature lamellar bone, 3) Immature bone (darker red areas).

Figure 24: NB formation within cortical particle of a MSDBAM core at12 months: turnover in progress on the left and ri ght.

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Table 1: Histomorphometric Findings

Analysis MSDBA Graft1 DMBBX/DFDBA Graft2 MSDBAM Graft2

(Cumulative Percentage) % % %

Percentage of core 45.61 40.33 45.42 that is bone

Percentage of core that 79.15 4.67 74.21 is vital bone

Percentage of new bone ——— 39.10 ——— DMBBX/DFDBA (10 months)

Percentage of new bone 42.14 ——— ——— MSDBA1 (6 months)

Percentage of new bone 45.52 ——— ——— MSDBA1 (10 months)

Percentage of new bone ——— ——— 32.03 MSDBAM3 (6 months)

Percentage of new bone ——— ——— 33.06 MSDBAM3 (12 months)

Percentage of !brous 54.38 54.33 54.63 marrow tissue

1. MSDBA Graft = 100% MSDBA Cancellous2. DMBBX/DFDBA = 50% DMBBX and 50% DFDBA3. MSDBAM Graft = 50 % MSDBA Cancellous and 50% MSDBA Cortical

ponents were computed based on differences in optical density, and the following param-eters were measured and compared: (1) per-centage of core that is bone, (2) percentage of vital bone, (3)percentage of new bone and

(4) percentage of fibrous tissue. These param-eters were evaluated in all three types of grafts. To evaluate the mineralization process in the sinus graft, the grafted region of each speci-men was divided into three equally sized areas

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Figure 25: High magni!cation of Fig 24: turnover of cortical particle at 12 months.

Figure 26: Cortical particle of MSDBAM new bone formation within particle.

Figure 27: More advanced stage of cortical particle turnover in MSDBAM. Figure 28: High Magni!cation of !gure 27.

to determine tissue components at the infe-rior, center and superior levels of the biopsies.

RESULTSPatient and treatment data are summarized in Table 1. A total of 25 patients with a mean age of 67.5 years were selected for participation in this study. Twelve sinuses were grafted with

cortico-cancellous graft. Thirteen sinuses were grafted with cancellous grafts. Four sinuses were grafted with DMBBX/DFDBA. One of the sinuses that were grafted with MSDBAM was perforated and repaired using the Loma Linda pouch technique.31 At 12 months a core was harvested and the amount of new bone in the core harvested from that particular sinus

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amounted to 15.36%, much below the average obtained in the other sinuses during the same time frame. Similar findings were observed in the MSDBA cores harvested from sinuses that were perforated at the time of grafting. These finding are concurrent with observations made in a previous study by Proussaeffs et al.32

At six months, the greatest amount of new bone was observed for MSDBA (42.14 %), fol-lowed by MSDBAM (32.03%). At ten months the amount of new bone for MSDBA was 45.52% versus 39.19% for DMBBX/DFDBA. At twelve months, the amount of new bone in MSDBAM specimens was 33.06% which is virtually identical to the values observed at six months. One of the main reason there is a statistically significant difference in new bone formation between MSDBA and MSDBAM is not the time length of bone healing but the perforation of the sinus membrane in one case of MSDBAM that resulted in an unusu-ally low percentage of new bone formation (15.36%). Overall, new bone in the MSDBA cores was higher than the other two grafts combinations observed in this study. Histol-ogy findings are presented in Figures 1-28. All samples exhibited good bone formation with new bone bridging or growing onto the surfaces of the residual graft particles (Fig 1, 2, 5, 11). DMBBX/DFDBA samples dif-fered from MSDBA and MSDBAM by gen-erally exhibiting a greater number and larger residual graft particles (Fig 5, 6, 10). Residual MSDBA and MSDBAM graft particles were often so well incorporated that they were dif-ficult to distinguish from new bone (Fig 7, 8, 9). The turnover of the cortical particles of MSDBAM graft material was still slower than

that of the cancellous particles of MSDBA (Fig 16, 25, 26). There seems to be albeit slow, an initial turnover of some of the corti-cal particles in MSDBAM, but this appears not to change in any significant manner. In fact at 12 months there were still some mineralized cortical particles in MSDBAM (Fig 24, 25) and the same was observed for the DMBBX/DFDBA grafts at 10 months (Fig 10, 11). In some cases osteocytes appear to be repopu-lating the previous lacunae of the MSDBA graft particles (Fig 7, 16, 18, 20 and 22).

Histomorphometric findings are summarized in Table 1. All grafts successfully achieved new bone formation. The observed percentages of the cores which were bone (vital, and non-vital) was virtually identical across all graft types. With regards to the percentage of vital bone in the cores, the results were significantly higher in the MSDBA and MSDBAM grafts. In terms of graft turnover (i.e. resorption and replace-ment by new bone), significant differences between the three grafts were found. There were far more DMBBX particles found in the cores at 10 months and they were large in size occupying a great portion of the cores. This explains why in terms of percentage of core that is bone the DMBBX/DFDBA core show num-bers very close to that of MSDBA and MSD-BAM. In contrast, a significant amount of the cancellous particles had either turned over or were surrounded by new bone of different maturation levels at six and 10 months (Fig 4, 5, 6, 11 and 23). Within the cortico-cancellous cores which were harvested at twelve months, most of the cortical particles had undergone turnover or were in the advanced stages of the process (Fig 27, 28) but the amount of new

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bone was not statistically different from the six-month cores. It is important to note, how-ever, that the statistical significance of these histomorphometric differences could not be determined because of the small sample size.

DISCUSSIONAfter graft placement, the pattern, rate and quality of new bone formation are directly influ-enced by complex reactions between the nature of the graft material and healing processes of the biological host.4,5,26 Concurrent revascular-ization and substitution of the graft material with host bone without a significant loss of strength or volume are essential for bone grafting to be successful.4,5,26 In the present study, graft turn-over occurred more rapidly with MSDBA and MSDBAM compared to the bovine component (DMBBX) of the composite grafts. The slower turnover rate of DMBBX is consistent with the observations of Artzi et al.18 in their comparative canine study. This phenomenon may be attribut-able, in part, to structural changes that occur in the mineral phase of DMBBX during heat-pro-cessing at 300° C, which reportedly enlarges the xenograft mineral particles to approximately twice the size of MSDBA mineral particles.27 In comparison, processing does not change the mineral particle size of cortical or cancellous MSDBA. Cancellous MSDBA retains a bone-like structure with interconnecting porosity.27

Adverse immunologic response by the patient, infection, impaired graft healing and graft failure are some of the complications associated with allograft placement.2 Host tissue sensitivity can develop from allograft-derived antigens and cause lymphoplasma-cytic infiltration that results in occlusion of

local blood vessels and failure to revascular-ize the graft.4,28 Graft necrosis and the prolif-eration of inflammatory granulation tissue can occur as secondary effects and interfere with a graft’s incorporation and new bone formation.26 While contemporary tissue processing tech-niques can attenuate these responses, some may also diminish the mechanical strength of the allograft.28 Approximately 12.2% of the estimated 40,000 bone allografts placed each year become infected, compared to 3.5% of the autografts placed annually.29-30 Such infec-tions can arise from a number of recipient fac-tors apart from donor disease or contamination from processing.29 Nonetheless, strict donor screening and tissue processing techniques are crucial. The tissue should be harvested according to Good Manufacturing Practices by a certified tissue bank, and processed for bio-logical safety. All of the graft materials used in the present study met these standards.

Statistical analysis of clinical data is an important standard for determining data integ-rity, especially when comparing the clinical effectiveness of two products. While the find-ings of the present study appeared promis-ing, they also confirmed the slower turnover of cortical particles as well as that of the very slow turnover of the DMBBX component of the Xenograft. The small study population pre-cluded the ability to determine if the faster turn-over of MSDBA cancellous and cortical was statistically significant. In a follow up study the amount of residual graft material in contact with new bone and the amount of residual graft material in the three graft times during the same timeframes will be investigated and reported. For this reason, the present study should be

60 • Vol. 2, No. 5 • June 2010

considered a preliminary inquiry and definitive conclusions should only be drawn from addi-tional research with a larger study population.

CONCLUSIONSGraft turnover (resorption and replacement by new bone) occurred much faster with both cor-tical and cancellous MSDBA compared to the bovine component (DMBBX) of the composite grafts; the percentage of fibrous or marrow tis-sue was virtually identical in all core types, no differences in graft stability or osseointegra-tion were noted. The time between bone graft-

ing and reentry to harvest specimens does not seem to have a significant effect on the amount of new bone formed after six months. L


References1. LeGall MG. Localized sinus elevation and

osteocompression with single-stage tapered dental implants: technical note. Int J Oral Maxillofac Implants 2004;19(3):431-437.

2. Leonetti JD, Koup X. Localized maxillary ridge augmentation with a block allograft for dental implant placement: case reports. Implant Dent 2003;12:217-226.

3. Keller EE, Tolman DE, Eckert S. Surgical-prosthodontic reconstruction of advanced maxillary bone compromise with autogenous onlay block bone grafts and osseointegrated endosseous implant: A 12-year study of consecutive patients. Int J Oral Maxillofac Implants 1999;14:197-209.

4. Keith JD Jr. Localized ridge augmentation with a block allograft followed by secondary implant placement: a case report. Int J Prosthodont Rest Dent 2004;24:11-17.

5. Noumbissi S, Lozada JL, Boyne P, Rohrer MD, Clem D, Kim J, Prasad H. Clinical, Histologic and Histomorphometric Study of Mineralized Solvent-Dehydrated Bone Allograft (PUROS) in Human Maxillary Sinus Grafts. Journal of Oral Implantology 2005; 171-179.

6. Nemcovsky CE, Winocur E, Pupkin J, Artzi Z. Sinus floor augmentation through a rotated palatal flap at the time of tooth extraction. Int J Periodont Rest Dent 2004;24:177-183.

7. Khoury F. Augmentation of the sinus floor with mandibular bone block and simultaneous implantation: a 6-year clinical investigation. Int J Oral Maxillofac Implants 1999;14:557-564.

8. van den Bergh JPA, ten Bruggenkate CM, Krekeler G, Tuinzing DB. Maxillary sinus floor elevation and grafting with human demineralized freeze dried bone. Clin Oral Impl Res 2000;11:487-493.

9. Gross JS. Bone grafting materials for dental applications: a practical guide. Compend Contin Educ Dent 1997;18:1013-1036.

10. Schultze-Mosgau S, Nkenke E, Schlegel AK, Hirschfelder U, Wiltfang J. Analysis of bone resorption after secondary alveolar cleft bone grafts before and after canine eruption in connection with orthodontic gap closure or prosthodontic treatment. J Oral Maxillofac Surg 2003;61:1245-1248.

11. Bianchi AE, Vinci R, Torti S, Sanfilippo F. Atrophic mandible reconstruction using calvarial bone grafts and implant-supported overdentures: radiographic assessment of autograft healing and adaptation. Int J Periodont Rest Dent 2004;24:334-343.

12. Mazock JB, Schow SR, Triplett RG. Proximal tibia bone harvest: Review of technique, complications, and use in maxillofacial surgery. Int J Oral Maxillofac Implants 2004;19:586-593.

13. Matsuura M, Ohno K, Michi K, Egawa K, Takiguchi R. Clincoanatomic examination of the fibula: anatomic basis for dental implant placement. Int J Oral Maxillofac Implants 1999;14:879-884.

14. Mehta RP, Deschler DG. Mandibular reconstruction in 2004: an analysis of different techniques. Curr Opin Otolaryngol Head Neck Surg 2004;12(4):288-293.

15. Balaji SM. Management of deficient anterior maxillary alveolus with mandibular parasymphyseal bone graft for implants. Implant Dent 2002;11:363-369.

16. Proussaefs P, Lozada J, Kleinman A, Rohrer MD. The use of ramus autogenous grafts for vertical alveolar ridge augmentation and implant placement: a pilot study. Int J Oral Maxillofac Implants 2002;17:238-248.

17. Gross JS. Bone grafting materials for dental applications: A practical guide. Compend Contin Educ Dent 1997;18:1013-1036.

18. Artzi Z, Weinreb M, Givol N, Rohrer MD, Nemcovsky CE, Prasad HS, Tal H. Biomaterial resorptin rate and healing site morphology of inorganic bovine bone and �-tricalcium phosphate in the canine: a 24-month longitudinal histologic study and morphometric analysis. Int J Oral Maxillofac Implants 2004;19:357-368.

19. Urist MR, Strates BS. Bone morphogenetic protein. J Dent Res 1971;50(6):1392-1406.

20. Schwartz Z, Sopmers A, Mellonig JT, Carnes DL Jr., Dean DD, Cochran DL, Boyan BD. Ability of commercial demineralized freeze-dried bone allograft to induce new bone formation is dependent on donor age but not gender. J Periodontol 1998;69:470-478.

21. Moore TM, Artal R, Arenas M, Gendler E. Influence of postmortem time and temperature on osteoinductive activity of demineralized microperforated ethylene oxide-sterilized syndeneic bone implant in the rat. Clin Orthop Rel Res 1990;259:239-244.

22. Urist MR, Mikulski A, Boyd SD. A chemosterilized antigen-extracted autodigested alloimplant for bone banks. Arch Surg 1975;110:416-428.

23. Günther KP, Scharf H-P, Pesch H-J, Puhl W. Osteointegration lösungsmittel-konservierter Knoche-transplantate im Tiermodell. Osteologie 1995;5(1):4-12

24. Pikos MA. Maxillary sinus membrane repair: report of a technique for large perforations. Implant Dent 1999;8:29-34.

25. Rosenlicht JL. Advancement in soft bone implant stability. West Indian Dent J 2002;6(1):2-7.

26. Stevenson S, Davy DT, Klein L, Goldberg VM. Critical biological determinants of incorporation on non-vascularized cortical bone grafts. J Bone Joint Surg 1997;79-A(1):1-16.

27. Buser D, Dula K, Belser U, Hirt JP, Berthold H. Localized ridge augmentation using guided bone regeneration. I. Surgical procedure in the maxilla. Int J Periodont Rest Dent 1993;13:29-45.

28. Tadic D, Epple M. A thorough physicochemical characterisation of 14 calcium phosphate-based bone substitution materials in comparison to natural bone. Biomater 2004;25:987-994.

29. American Medical Association. Report 5 of the Council on Scientific Affairs (I-01). Safety of Tissues for Transplantation. Chicago: American Medical Association, 2001 (Dec). Available online at: http://www.ama-assn.org/ama/pub/category/13615.html.

30. Proussaefs P, Lozada J The “Loma Linda pouch”: a technique for repairing the perforated sinus membrane. Int Journal Periodontics Restorative Dent 2003;23(6):593-597.

31. Sutherland AG, Raafat A, Yates P, Hutchison JD. Infection associated with the use of allograft bone from the north east Scotland Bone Bank. Hosp Infect 1997;35:215-222.

32. Proussaefs P, Lozada J, Kim J. Effects of sealing the perforated sinus membrane with a resorbable collagen membrane: a pilot study in humans. J Oral Implantol 2003;29(5):235-41

Correspondence: Sammy S. Noumbissi, DDS MS 801 Wayne Avenue, Suite G200Silver Spring, MD 20910Tel: 301 588-0768Fax: 301 588-0873E-Mail: [email protected]: www.marylandintegrativedentistry.net

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Cóppola et al

Connective tissue as protection to under-lying periodontal support has long been recognized. There are multiple ways

to increase connective tissue including palatal tissue, tissue from the maxillary tuberosity, as well as acellular dermal matrix allograft taken from a cadaver. The advantage of allograft is the lack of the need for a donor site, while its disadvantage is that it must be covered by a mucoperiosteal flap. This sometimes cre-ates a need for a second procedure to free any

mucosal tissue present and uncover underlying connective tissue. Although acellular dermal matrix allograft may not convert to keratinized tissue, it does have characteristics of connec-tive tissue which serve as tissue to protect the periodontium. The cases presented are both for covering root surfaces as well as adding connective tissue for protection of the peri-odontium from retraction cords during restor-ative procedures and cementation procedures where irritation to the gingiva may take place.

Case of the MonthAcellular Dermal Matrix Allograft

Used for Root Coverage and Increased Connective Tissue in Restorative Cases

Daniel Melker, DDS1

1. Private practice, Clearwater, Florida, USA

Abstract

KEY WORDS: Acellular dermal matrix, connective tissue, root coverage, periodontal surgery


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DisclosureThe authors report no conflict of interest with anything mentioned in this article

Correspondence:Dr. [email protected]

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Myasthenia Gravis (MG) is an autoim-mune neuromuscular disease char-acterized by muscular weakness and

fatigability. Dental management of patients diagnosed with MG present a challenge to the dental profession. This article describes a

generalized MG patient who was treated with dental implant therapy in the maxilla. Dental implant delivery was carried out in a conven-tional manner with special considerations to prevent complications. As a result, healing and restoration of the dental implant were uneventful.

Osseointegrated Implant in Myasthenia Gravis Patient:

A Case Report

Wiroj Suphasiriroj DDS, MS1 • Theerathavaj Srithavaj DDS, MS1

1. Maxillofacial Prosthetic Service, Department of Prosthodontics, Faculty of Dentistry, Mahidol University, Rajthevee, Bangkok, Thailand

Abstract

KEY WORDS: Myasthenia Gravis, dental implant


74 • Vol. 2, No. 5 • June 2010

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INTRODUCTIONMyasthenia Gravis (MG), an autoimmune neuro-muscular disease, is characterized by fluctuat-ing weakness of voluntary muscles and abnormal fatigue on exertion.1 The etiology of MG results from decreasing acetylcholine receptors at the neuromuscular junction2,3 by three possible mech-anisms: 1) accelerated endocytosis and degra-dation of the receptors; 2) functional blockade of the acetylcholine-binding sites; 3) Complement-mediated damage to the acetylcholine recep-tors. The thymus gland has also been implicated in the pathogenesis of MG but it is not known whether thymic changes play a primary or sec-ondary role in disease pathogenicity.1 MG has age and gender related peaks.1,2 The first peak of prevalence, in the second and third decades, affects mostly women, and the second, in the sixth and seventh decades, affects mostly men.

Onset of symptoms is often gradual, start-ing with weakness in ocular muscles. Movement of the eyes and eyelids are initially affected with the levator palpebrae, orbicularis oculi, and extra-ocular muscles becoming involved. As a result, patients often experience diplopia, ptosis, and nystagmus.4-5 Approximately one-fourth of diag-nosed MG patients have bulbar muscle involve-ment, so named for the nerves originating from the brain stem’s bulb like portion.1,6 With bulbar involvement, muscle weakness causes problems with chewing,7 swallowing,8 facial movement,9 and articulation.10 Masticatory muscle weak-ness occurs in a considerable number of patients with myasthenia gravis.6,11-12 In most patients with MG, muscle weakness spreads from ocu-lar and oropharyngeal muscles to the upper and lower extremities, resulting in generalized form of MG.1 Neck flexors, deltoids, hip flexors, and

finger/wrist extensors are muscles most com-monly affected in the generalized form. Affect-ing 20 to 40% of patients with MG, respiratory muscle weakness can be life threatening result-ing in a myasthenic crisis, an acute exacerbation of symptoms with respiratory failure.1,13 Medical management of MG is primarily directed toward generating normal muscle strength in minimal time and includes four main treatment modali-ties: 1) anticholinesterase agents (pyridostigmine bromide: Mestinon® and neostigmine bromide: Prostigmin®)2,14; 2) immunosuppressive ther-apy (corticosteroids)15-17; 3) thymectomy18,19; 4) short-term immunotherapy (plasmapheresis and intravenous immunoglobulin: IVIg).14,20,21

Dental implants are an alternative treat-ment to restore missing teeth. To the best of our knowledge, there have been no reports in the literature regarding the placement of dental implants in the MG patient. In this case report, we present a MG patient who was treated with dental implant therapy to rehabilitate an edentu-lous area of the maxilla. Patient considerations, drug use selection, and the effect of prolonged immunosuppressive therapy are discussed.

CASE REPORTA 45-year-old Asian woman presented for exami-nation in our dental clinic with a 6 month history of generalized Myasthenia Gravis. At an earlier presentation in a neurological clinic, the patient’s chief complaints were irritation of eyes and fati-gability of lower limbs. Physical examination showed drooping of eyelids (ptosis), limiting of eye movement and leading to double vision (dip-lopia), and upper/lower extremity muscle weak-ness. Neurophysical findings from the patient at rest demonstrated power scores of 4 (out of

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a possible 5) for the neck, flexors and extensors muscles about 4. The bulbar sign innervated by cranial nerves V, VII, IX-XII (e.g., dysarthria, dysphagia) were not prominent. Difficulties in chewing, swallowing and speech were not pre-sented while chest radiographs and computed tomography (CT) scans of the mediastinum were normal. The patient’s clinical degree of MG severity was classified as moderate gener-alized according to the Osserman scale.5 The patient was treated by using a combination of anticholinesterase agents and immunosuppres-sive therapy. After remission of the disease, the patient was referred to the dental clinic for resto-ration of the missing maxillary right lateral incisor.

Implant PlacementOne hour prior to the morning scheduled sur-gical procedure, the patient took anticholin-esterase agent with 60 mg of pyridostigmine (Mestinon®) and corticosteroid with 5 mg of prednisolone. Antibiotic prophylaxis with 2.0 g of amoxicillin along with presurgical non-steroi-dal anti-inflammatory drugs (400 mg of ibupro-

fen) was also prescribed to the patient. Neither supplemental steroid nor sedation was necessary in this case after consultation with her neurolo-gist. Vital signs were routinely monitored. Local anesthesia was administered with 2% lidocaine with epinephrine 1:100,000 and mucoperios-teal flaps were raised. Subsequently, two-stage implant therapy was performed by installation of a 4.3!10.0 mm Replace Select Tapered® implant (Noble Biocare, USA). Buccal bone augmen-tation was also performed using the combina-tion of bone graft materials (BioOss®, Geistlich, Switzerland) and resorbable collagen membrane (BioGide®, Geistlich, Switzerland) since buc-cal implant threads (4 threads) were exposed.

Figure 1a: Facial view of site #7 dental implant at time of the 2nd stage surgery.

Figure 1b: Radiograph of site #7 dental implant at time of the 2nd stage surgery.

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The flaps were closed by suturing with resorb-able sutures (Vicryl®, Johnson&Johnson, USA). Antibiotic, NSAIDs and chlorhexidine mouth-wash were prescribed during the first 2 weeks after implant placement. Post-operative care was instructed to the patient. The follow up visits were scheduled at 1, 3, and 6 months after implant placement. Soft tissue healing around the implant was delayed and completed within 1 month after surgery. Otherwise, healing was uneventful.

Abutment Connection and ProsthodonticsThe 2nd stage surgery was carried out 8 months after implant placement and guided bone regen-eration, providing a longer healing period than in the case of a normal maxilla or guided bone regeneration. The implant had clinically osseo-integrated and demonstrated adequate sur-rounding soft tissue (figure 1a) Radiographic evaluation showed that the crestal bone was intact at the implant platform level (figure 1b). A healing abutment of 3.0 mm in height (Noble Biocare, USA) was connected to the implant and an implant level impression procedure was

performed 3 weeks later. A 15o esthetic abut-ment was connected to implant (figure 2a) and a cement-retained crown was inserted (figure 2b). A radiograph taken at 1 year post-placement showed no abnormalities (figure 3). The patient was both comfortable and satisfied with the result.

DISCUSSIONMyasthenia Gravis is a disease characterized by intermittent muscle weakness, which improves after anticholinesterase and immunosuppressive medications. Patients with this condition may present with problems that necessitate special consideration when managing their dental treat-ment.1,5 For example, patients should receive dental treatment at the time of day when cholines-terase inhibitor medication has maximum effective-ness, typically within 1 and 1" hours after taking. Morning appointment should be scheduled to avoid daily added muscle weakness. Basic under-standing of the nature of the disease is essential to avoid complication, such as myasthenia crisis. Infection, surgical procedures, emotional stress and drugs may predispose a myasthenia crisis.5,13

Figure 2a: Angled (15º) esthetic abutment connected to osseointegrated implant.

Figure 2b: Final prosthesis delivered to implant at site #7.

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Effective pain management, soothing music, elimi-nation of extraneous noises, aromatherapy, and anticipatory guidance may promote relaxation and decrease stress during dental treatment. In some situations, use of sedatives may be helpful.5

MG patients on long term corticosteroid involvement need to be medically evaluated for antibiotic premedication due to immune sup-pression.5,22 Patients should be also evaluated for adrenal insufficiency, which would require supplemental glucocorticoid medication prior to treatment.22,23 Additionally, immunosup-pressant therapy may further predispose MG patients to fungal infections and delayed wound healing.5,24 In this case, the soft tissue around implant was completely healed within 1 month.

Many common drugs used in dentistry have

the potential to produce complications for MG patients by exacerbating their muscle weakness or by interfering with breathing.1,4-5,12 Amide-type local anesthetics, such as lidocaine (Xylocaine) or mepivacaine (Carbocaine), can be adminis-tered safely in MG patients. Generally, penicillin and its derivatives are not associated with neu-romuscular blocking properties. They can be safely used, although aggravation of MG follow-ing administration of those has been reported.25 Some antibiotics (e.g., erythromycin, tetracy-cline) demonstrate muscle relaxing properties, so their uses in MG patients should be carefully considered since MG patients have increased sensitivity to the effect of the muscle relaxants.

Most MG patients need to use long-term cor-ticosteroids in combination with anticholinester-ase agents for improving the treatment outcome. From previous studies, the long term systemic use of corticosteroids is known to induce (second-ary) osteoporosis and it is reported that cortico-steroids can inhibit bone healing and increase the spontaneous fractures.26-28 Thereby, MG patients treated with long term corticosteroids have a chance to be corticosteroid-induced osteoporo-sis. Osteoporosis is considered to be a risk fac-tor for periodontal diseases, temporomandibular disorders, fail implant therapy and denture insta-bility due to alveolar ridge absorption. Neverthe-less, whether osteoporosis is a contraindication or a risk factor for dental implants remains a mat-ter of controversy. A number of reports point to the possibility that osteoporosis or a reduction in bone mass or density could be problematic to the initiation and maintenance of osseointegration of dental implants.29-32 On the contrary, several reports indicate that osteoporosis may not be nec-essarily problematic for dental implant placement

Figure 3: One year post-placement radiograph.

Suphasiriroj et al

78 • Vol. 2, No. 5 • June 2010

Suphasiriroj et al

or maintenance.33-37 Moreover, there is debate as to whether the diagnosis of skeletal osteopo-rosis is in fact manifested in the oral cavity.38-40

CONCLUSIONThis case report of a MG patient treated with a dental implant and GBR was carried out in a con-ventional manner with special considerations to prevent complications. As a result, healing and restoration of the dental implant were uneventful. L

Correspondence:Wiroj Suphasiriroj D.D.S., M.S. Maxillofacial Prosthetic Service, Department of Prosthodontics, Faculty of Dentistry, Mahidol University, 6 Yothe Road, Rajthevee, Bangkok 10400, Thailand. Tel: 66(81)-644-3022E-mail: [email protected]

DisclosureThe authors report no conflicts of interest with anything mentioned in this article.

Referrences1. Tolle L. Myasthenia gravis: a review for dental

hygienists. J Dent Hyg 2007;81:12-12(1).2. Drachman DB. Myasthenia Gravis. N Engl J Med

1994;330(25):1797-1810.3. Vincent A, Palace J, Hilton-Jones D. Myasthenia

Gravis. Lancet 2001;357:2122-2128.4. Patton LL, Howard JF Jr. Myasthenia gravis:

dental treatment considerations. Spec Care Dent 1997;17:25-32.

5. Yarom N, Barnea E, Nissan J, Gorsky M. Dental management of patients with myasthenia gravis: a literature review. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2005;100:158- 163.

6. Beekman R, Kuks JB, Oosterhuis HJ. Myasthenia gravis; diagnosis and follow up of 100 consecutive patients. J Neurol 1997;244:112-118.

7. Van der Bilt A, Weijnen FG, Bosman F, van der Glas HW, Kuks JB. Eur J Oral Sci 2001;109:160 -164.

8. Ertekin C, Yuceyar N, Aydogdu I. Clinical and electrophysiological evaluation of dysphagia in myasthenia gravis. J Neurol Neurosurg Psychiatry 1998;65:848-856.

9. Weijnen FG, van der Bilt A, Wokke JH, Kuks JB, van der Glas HW, Bosman F. What’s in a smile? Quantification of the vertical smile of patients with myasthenia gravis. J Neurol Sci 2000;173:124-128.

10. Sellman MS, Mayer RF. Weakness and ‘tiredness’: when to suspect myasthenia gravis. Geriatrics 1985;40:92-112.

11. Weijnen FG, van der Bilt A, Wokke JH, Kuks JB, van der Glas HW, Bosman F. Maximal bite force and surface EMG in patients with myasthenia gravis. Muscle Nerve 2000;23:1694-1699.

12. Weijnen FG, van der Bilt A, Kuks JB, van der Glas HW, Oudenaarde I, Bosman F. Masticatory performance in patients with myasthenia gravis. Arch Oral Biol 2002;47(5):393-398.

13. Berrouschot J, Baumann I, Kalischewski P, Sterker M, Schneider D. Therapy of myasthenia gravis. Crit Care Med 1997;25:1228-1235.

14. Richman D, Agius A. Treatment of autoimmune myasthenia gravis. Neurology 2004;63:1652-1661.

15. Seybold ME, Drachman DB. Gradually increasing doses of prednisone in myasthenia gravis: reducing the hazards of treatment. N Engl J Med 1974;290:81-84.

16. Evoli A, Di Schino C, Marsili F, Punzi C. Successful treatment of myasthenia gravis with tracolimus. Muscle Nerve 2002;25:111-114.

17. Chaudhry V, Cornblath DR, Griffin JW, O’Brien R, Drachman DB. Mycophenolate mofetil: a safe and promising immunosuppressant in neuromuscular diseases. Neurology 2001;56:94-96.

18. Seybold ME, Howard FM Jr, Duane DD, Payne WS, Harrison EG Jr. Thymectomy in juvenile myasthenia gravis. Arch Neurol 1971;25:385-392.

19. Kuks JB, Oosterhuis HJ, Limburg PC, The TH. Anti-acetylcholine receptor antibodies decrease after thymectomy in patients with myasthenia gravis: clinical correlations. J Autoimmun 1991;4:197-211.

20. Arsura EL, Bick A, Brunner NG, Namba T, Grob D. High-dose intravenous immunoglobulin in the management of myasthenia gravis. Arch Intern Med 1986;146:1365-1368.

21. Fateh-Moghadam A, Wick M, Besinger U, Geursen RG. High-dose intravenous gammaglobulin for myasthenia gravis. Lancet. 1984;1:848-849.

22. Little JW, Falace DA, Miller CS, Rhodus NL. Dental management of the medically compromised patient, 6th ed. St.Louis: CV Mosby; 2002:271-282.

23. Miller CS, Little JW, Falace DA. Supplemental corticosteroids for dental patients with adrenal insufficiency. J Am Dent Assoc 2001;132:1570-1579.

24. Bahn SL. Glucocorticoids in dentistry. J Am Dent Assoc 1982;105:476-481.

25. Argov Z, Brenner T, Abramsky O. Ampicillin may aggravate clinical and experimental myasthenia gravis. Arch Neurol 1986;43:255-256.

26. Aslan M, Simsek G, Yildirim U. Effects of short-term treatment with systemic prednisolone on bone healing: an experimental study in rats. Dent Traumatol 2005;21:222-225.

27. Kozai Y, Kawamata R, Sukurai T, Kanno M, Kashima I. Influence of prednisolone-induced osteoporosis on bone mass and bone quality of the mandible in rats. Dentomaxillofac Radiol 2009;38:34-41.

28. Yao W, Cheng Z, Busse C, Pham A, Nakamura MC, Lane NE. Glucocorticoid excess in mice results in early activation of osteoclastogenesis and adipogenesis and prolonged suppression of osteogenesis: a longitudinal study of gene expression in bone tissue from glucocorticoid-treated mice. Arthritis Rheum 2008;58:1674-1686.

29. Baxter JC, Fattore L. Osteoporosis and osseointegration of implants. J Prosthodont 1993;2:120-125.

30. Garg AK, Winkler S, Bakaeen LG, Mekayarajjananonth T. Dental implants and the geriatric patient. Implant Dent 1997;6:168-173.

31. Keller JC, Stewart M, Roehm M, Schneider GB. Osteoporosis-like bone conditions affect osseointegration of implants. Int J Oral Maxillofac Implants 2004;19:687-694.

32. Cho P, Schneider GB, Kellogg B, Zaharias R, Keller JC. Effect of glucocorticoid-induced osteoporotic-like conditions on osteoblast cell attachment to implant surface microtopographies. Implant Dent 2006;15:377-385.

33. Dao TT, Anderson JD, Zarb GA. Is osteoporosis a risk factor for osseointegration of dental implants? Int J Oral Maxillofac Implants 1993;8:137-144.

34. Friberg B. Treatment with dental implants in patients with severe osteoporosis: a case report. Int J Periodontics Restorative Dent 1994;14:348-353.

35. Fujimoto T, Niimi A, Nakai H, Ueda M. Osseointegrated implants in a patient with osteoporosis: a case report. Int J Oral Maxillofac Implants 1996;11:539-542.

36. Fujimoto T, Niimi A, Sawai T, Ueda M. Effects of steroid-induced osteoporosis on osseointegration of titanium. Int J Oral Maxillofac Implants 1998;13:183-189.

37. Mori H, Manabe M, Kurachi Y, Nagumo M. Osseointegration of dental implants in rabbit bone with low mineral density. J Oral Maxillofac Surg 1997;55:351-361.

38. Kribbs PJ, Chesnut CH III, Ott SM. Kilcoyne RF. Relationships between mandibular and skeletal bone in an osteoporotic population. J Prosthet Dent 1989;62:703-707.

39. Kribbs PJ. Comparison of mandibular bone in normal and osteoporotic women. J Prosthet Dent 1990;63:218-222.

40. von Wowern N, Storm TL, Olgaard K. Bone mineral content by photon absorptiometry of the mandible compared with that of the forearm and the lumbar spine. Calcif Tissue Int1988;42:157-161.

Suphasiriroj et al

Carpenter

Background: Diabetes is a serious metabolic disorder with complications including cardiovas-cular disease, kidney disease, eye disease, nerve disorders and delayed wound healing. Severe periodontal disease is another recognized compli-cation of diabetes. Diabetes and poor glycemic control lead to an exaggerated oral tissue response. Method: A case is presented describing a patient who was treated with dental implants to replace her lower incisors. Returning in 20 months, with an exaggerated tissue response, she was diag-nosed with uncontrolled diabetes with concur-rent severe periodontitis and peri-implantitis.

Results: The existing implant screw-retained fixed prosthesis was easily removed provid-ing access for treatment of the implant fixtures which had developed peri-implantitis. The emer-gence profile of the prosthesis was modified before re-attaching it to the treated implant fix-tures. An improved tissue response was obtained. Conclusion: Diabetes and periodontal disease have a bidirectional relationship. Just as diabetes can worsen periodontitis, studies have shown that periodontitis has an adverse affect on the glyce-mic control of a diabetic. Diagnosing diabetes is the responsibility of the physician, but a dentist may be the first to notice the signs and symptoms of a poorly controlled or undiagnosed diabetic.

Management of a Patient Who Developed Uncontrolled Diabetes After Implant Placement:

A Case Report

John F. Carpenter, DMD, MAGD1

1. Private Practice, New Windsor, NY, USA

Abstract

KEY WORDS: Dental implants, diabetes, management, prosthetics


82 • Vol. 2, No. 5 • June 2010

INTRODUCTIONDiabetes is a metabolic disorder of insulin deficiency and/or dysfunction. This leads to a hyperglycemic state and causes a variety of metabolic abnormalities involving carbohy-drates, fats and proteins. An estimated 17.9 million people (6%) in the United States have been diagnosed with diabetes and another 2% are undiagnosed diabetics.1 It is the most common cause of blindness (retinopa-thy) and lower extremity amputation (neuropa-thy). Poor wound healing, end stage renal disease (nephropathy), myocardial infarc-tion and stroke are other complications.2-4

Uncontrolled diabetes compounded with poor oral hygiene can lead to an increased risk of dental caries, xerostomia, taste disor-ders, candidiasis, gingivitis and periodontal disease.5,6 About one-third of people with dia-betes have severe periodontal disease.7 Dia-betes is not an absolute contraindication to implant treatment but most practitioners feel that a patient’s glycemic levels must be well controlled before undergoing implant treatment.

This case report first describes the con-struction of a well-designed screw retained fixed implant prosthesis. Approximately two years later, the patient returned and presented with severe periodontal disease and implan-titis. Upon referral to a physician, she was diagnosed with uncontrolled diabetes. Gradu-ally with Phase I periodontal care and medica-tion for her diabetes, we were able to control her periodontal and perimplant complications. The screw retained prosthesis allowed for easy removal, so its design could be modified to allow better patient access for cleansability.

CASE REPORTThe patient is a 4’7” 175 pound non-smoking 50 year old female. Twenty months previously, an implant-retained FP-3 restoration to replace her lower incisors had been inserted. This is a fixed prosthesis to replace teeth crowns and has pink restorative material to replace bone and soft tissue.8 Tissue colored porcelain pro-vides a non-surgical alternative to replace tissue and enhance esthetics.9,10 The con-struction of the screw-retained fixed prosthe-sis had progressed smoothly and the patient was very happy. The patient was instructed in oral hygiene including the use of floss thread-ers and a 3 month recare appointment was set.

PATIENT DEVELOPS UNCONTROLLED DIABETES

The first sign of trouble was after patient missed her first scheduled recall appointment. After mul-tiple calls and communication with other fam-ily members, we were finally able to schedule the patient 20 months after the prosthesis was placed. At this appointment, suppuration around several teeth, pyogenic granuloma, and epulis fis-suratum lesions were noted (Figures 1, 2).11 While oral hygiene was poor, the tissue response to local irritants was excessive, suggesting a pos-sible disease-altering systemic complication.

Reviewing medical history with patient, it was apparent that she had not visited a phy-sician in the last 3 years. Clinical and radio-graphic assessment concluded a relapse and worsening of periodontal disease and concur-rent peri-implantitis (Figure 3). The patient was encouraged to visit her physician immediately. It took several months of building rapport before the patient could be convinced to visit her physician.

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Carpenter

It was subsequently determined by her physician that she had developed uncontrolled diabetes.

Over the next year, her oral health improved slowly, aided by her physician concurrently con-trolling her diabetes. Dental treatment con-sisted of root planing, scaling, curettage, oral hygiene instruction and motivation. The advan-tage of the screw retained prosthesis became quickly apparent. Access to the implant fix-tures and adjacent teeth were easily obtained by unscrewing the prosthetic fixation screws and removing the prosthesis (Figure 4).

Upon removal of the prosthesis, the serious-ness of the disease was obvious (Figure 5). To prevent collapse of the inflamed edematous tis-sue, healing collars were immediately placed (Fig-ures 6, 7). Next, the prosthesis was placed in an ultrasonic cleaning solution followed by gentle mechanical debridement of the implant fixtures and teeth. Intrasulcular irrigation was performed with chlorhexidine, the tissue with the epulis

Figure 1: Patient returned after 20 months displaying severe periodontal disease, pyogenic granuloma and epulis !ssuratum.

Figure 2: In"amed tissue and an epulis !ssuratum alongside the FP-3 pink porcelain.

Figure 3: Radiograph displaying peri-implantitis.

84 • Vol. 2, No. 5 • June 2010

appearance was excised and the pink porcelain thinned in this area, eliminating any ridge lap. At a subsequent appointment, Atridox (Tolmar Inc., Fort Collins, CO, USA) (doxycycline hyclate 10%) was used as a localized chemotherapeutic agent around the implant fixtures after debridement.

Figure 4: Lingual view of screw-retained prosthesis. Chimneys provide for easy removal of prosthesis.

Figure 5: View of infected tissue and implant !xtures.

Figure 6: Healing collars are placed to prevent collapse of tissue while the tissues are treated and prosthesis is modi!ed.

Figure 7: Radiograph with healing collars in place.

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Carpenter

Figure 8: View of prosthesis before modi!cation. Figure 9: View of prosthesis after modi!cation.

After 6 months of monitoring, it was decided to remove the prosthesis for the 3rd time and continue to modify its emergence profile12-14 to allow for better patient oral hygiene access. This was accomplished by attaching the pros-thesis to an abutment holder with the appropri-ate implant analog. At the lab bench, a more

bulbous design (Figure 8) was converted to a more slender design (Figure 9). This modi-fication sacrificed some esthetics but health improved (Figures 10, 11). This metal collar will not be visible in normal function since the lip functions as a curtain. Eighteen months after the patient was first diagnosed with uncon-

Figure 10: Oral view of slenderized prosthesis to facilitate oral hygiene. A metal collar is visible in this retracted view.

Figure 11: View with prosthesis o# and healing taking place.

86 • Vol. 2, No. 5 • June 2010

trolled diabetes, in spite of less than ideal home care, a healthier state is achieved (Figure 12).

DISCUSSIONIt has been estimated that many patients with diabetes may have the disease at least 10 years before it is diagnosed clinically.7 The oral cav-ity may exhibit the first signs and symptoms of an undiagnosed or poorly controlled diabetic.5 This certainly was the case with this patient who returned 26 months after initial treatment.

Periodontal disease is a recognized and well documented complication of diabe-tes. This has been determined by epidemio-logic and animal model studies.15-17 Diabetes is believed to promote periodontitis due to an exaggerated inflammatory response to a sulcu-lar microflora that has been found to be equiv-alent in both periodontal patients with and without diabetes.18 This altered immunity as a result of hyperglycemia may be the patho-

physiologic basis for the increase preva-lence and severity of periodontal disease.19

Diagnosing diabetes is the responsibil-ity of the physician, but the dentist plays an important role. The dentist may be the first to notice the signs and symptoms of a poorly controlled diabetic. Often patients do not have a physician or are non-compliant as was the case with this patient. Much time was spent on education and encouraging her to seek proper medical care. As health care providers, we must often function as psy-chologists and listen carefully to our patients.

Just as diabetes has been shown to worsen periodontitis, it has been demonstrated that periodontitis and oral infection may have an adverse effect on the glycemic control in diabetic patients. When a diabetic patient receives treatment for periodontal disease, resolution of inflammation and improved gly-cemic control may be obtained.20,21 Mealy suggested that many physicians are unaware of the inter-relationship between periodontal disease and diabetes.5 They are aware that other infections can wreak havoc with glyce-mic control, but may not understand that peri-odontal disease, which dentists treat every day, may have a major impact on glycemic control.

Physicians and dentists must better com-municate in order to diagnose and optimize their diabetic patient’s systemic and oral health. It appears obvious that diabetes may cre-ate a less than ideal environment for implant placement.22,23 However, Klokkevold24 per-formed a systematic review of the dental lit-erature and did not find a lower percentage of implant success between patients with and without diabetes. Such optimistic results may

Figure 12: View of patient 18 months after !rst diagnosed with uncontrollable diabetes.

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Carpenter

have been obtained perhaps because trial subjects typically are well-controlled diabet-ics with good glycemic levels. Physicians measure diabetic control with HbA1c (gly-cated hemoglobin) and the American Diabetes Association recommends HbA1c level < 7%.25

CONCLUSIONThis case report clearly documents how uncontrolled diabetes can worsen a patient’s periodontal and perimplant situation. Peri-odontal disease and diabetes seem to have a bi-directional relationship. Periodonti-tis is a complication of diabetes and glyce-mic control is difficult to obtain if an infection such as periodontal disease is present.

The easily removable screw retained pros-thesis provided excellent access for peri-odontal and perimplant treatment. It also made possible the modification of the tis-sue side of the prosthesis. By slenderiz-ing the prosthesis’s emergence profile, the patient’s oral hygiene was facilitated. L

Correspondence:Dr. John F. Carpenter, DMD, MAGD272 Quassaick AvenueNew Windsor, NY 12553 USA (845) 561-2330 [email protected]


References1. National Institute of Diabetes and Digestive and Kidney Diseases. National

Diabetes Statistics, 2007. “diabetes.niddk.nih.gov/dm/pubs/statistics”

2. Wei M, Gaskill SP, Haffner SM, et al. Effects of diabetes and level of glycemia on all-cause and cardiovascular mortality: the San Antonio Heart Study. Diabetes Care 1998;21:1167-1172.

3. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus: The Diabetes Control and Complications Trial Research Group. N Engl J Med 1993:977-986.

4. Mealey BL, Ocampo GL. Diabetes mellitus and periodontal disease. Periodontol 2000 2007;44:127-153.

5. Mealey BL. The interactions between physicians and dentists in managing the care of patients with diabetes mellitus. J Am Dent Assoc;139(suppl):4S-7S.

6. Lamster IB, Lalla E, Borgnakke WS, et al. The relationship between oral health and diabetes mellitus. J Am Dent Assoc;139(suppl):19S-24S.

7. Kidambi S, Patel SB. Diabetes mellitus: considerations for dentistry. J Am Dent Assoc;139(suppl):8S-18S.

8. Misch CE: Prosthetic options in implant dentistry, Int J Oral Implantol 1991; 7:17-21.

9. Taleghani M, Roshan S, Baker F, et al. Nonsurgical management of interdental papillae loss following extraction of anterior teeth: Gen Dent 2008; 326-331.

10. Hannon SM, Colvin CJ, Zurek DJ, et al. Selective use of gingival-toned ceramics: Case reports, Quintessence Int 1994; 25:233-238.

11. Newland JR, Meiller TF, Wynn R, et al. Oral soft tissue diseases: A reference manual for diagnosis and management, Hudson, OH: Lexi-Comp:2001:96-98.

12. Pissis P. Emergence profile considerations of implant abutments. Pract Periodontics Aesthet Dent 1994; 6:69-76.

13. Davarpanah M, Martinez H, Celletti R, et al. Three-Stage Approach to Aesthetic Implant Restoration: Emergence Profile Concept. Pract Proced Aesthet Dent 2001; 13:761-767.

14. Saba S. Anatomically correct soft tissue profiles using fixed detachable provisional implant restorations. J Can Dent Assoc 1997;63:767-770.

15. Pontes Anderson CC, Flyvbjerg A, Buschard K, et al. Relationship between periodontitis and diabetes: lessons from rodent studies. J Periodontol 2007;78:1264-1275.

16. Graves DT, Liu R, Alikhani M, et al. Diabetes-enhanced inflammation and apoptosis-impact on periodontal pathology. J Dent Res 2006; 85:15-21.

17. Taylor GW. Bidirectional interrelationships between diabetes and periodontal diseases: an epidemiologic perspective. Ann Periodontol 2001; 6:99-112.

18. Lalla E, Kaplan S, Chang SM, et al. Periodontal infection profiles in type 1 diabetes. J Clin Periodontol 2006; 33:855-862.

19. Tyan, ME, Carnu O, Kamer A. The influence of diabetes on the periodontal tissue. J Am Dent Assoc 2003; 134(suppl): 34S-40S.

20. Taylor GW, Burt BA, Becker MP, et al. Severe periodontitis and risk for poor glycemic control in patients with non-insulin-dependent diabetes mellitus. J Periodontol 1996;67(suppl):1085-1093.

21. Mealey BL, Oates TW. American Academy of Periodontology. Diabetes mellitus and periodontal diseases. J Periodontol 2006;77:1289-1303.

22. Hwang D, Wang HL. Medical Contraindications to Implant Therapy: Part II: Relative Contraindications. Implant Dentistry 2007;16:13-20.

23. Fiorellini JP, Nevins ML. Dental implant considerations in the diabetic patient. Periodontol 2000 2000;23:73-77.

24. Klokkevold PR, Han TJ. How do smoking, diabetes, and periodontitis affect outcomes of implant treatment? Int J Oral Maxillofac Implants, 2007; 22(Suppl):173-202.

25. American Diabetes Association. Standards of medical care in diabetes. Diabetes Care 2005;28(suppl 1):S4-S36.

Preliminary List of Invited SpeakersDr Eduardo Anitua, SpainDr R. Cancedda, ItalyDr Joseph Choukroun, FranceDr Paulo Coelho, USADr Danilo Di Stefano, ItalyDr Matteo Danza, ItalyDr Marco Degidi, ItalyDr Stefano Fanali, ItalyDr Pietro Felice, ItalyDr Massimo Frosecchi, ItalyDr Scott Ganz, USADr Dan Holtzclaw, USADr Robert Horowitz, USADr Michelle Jacotti, ItalyDr Adi Lorean, IsraelDr Jack Krauser, USADr Carlo Mangano, Italy

Dr Ziv Mazor, IsraelDr Eitan Mijiritsky, IsraelDr Robert Miller, USADr Stefano Pagnutti, ItalyDr G. Papaccio, ItalyDr Gabriele Edoardo Pecora, ItalyProf Adriano Piatelli, ItalyDr Roberto Pistilli, ItalyDr Lorenzo Ravera, ItalyDr U. Ripamonti, South Africa Dr Paul Rosen, USADr Philippe Russe, FranceDr Gilberto Sammartino, ItalyDr Marius Steigmann, GermanyDr Tiziano Testori, Italy Dr Nicholas Toscano , USA

SecretariatParagon Conventions18 Avenue Louis-Casai, 1209 Geneva, SwitzerlandTel: +41-(0)-22-5330-948, Fax: +41-(0)-22-5802-953Email: [email protected]

Aguiar et al

The aim of this study was to verify the effect of methotrexate (MTX) on bone repair of mandibular fractures in rats. A 50-µm defect

was created in the mandible of eighty rats subdi-vided in 4 groups, which received intraperitone-ally: saline; 0.25 and 1.6 mg/Kg of MTX weekly; and 0.15 mg/Kg of dexamethasone (DX) after surgery. Groups of 5 animals were sacrificed at 1, 7, 15 and 30 days after surgery. Radiographic and histomorphometric evaluations were per-formed to evaluate cartilage and bone formation. Treatments did not alter any parameter at 1 and 7 days after surgery. On the 15th day, only saline-treated animals presented a reduction in the dis-tance between bony ends (21.8±0.11 µm). At

this time, cartilage formation was increased in the saline group (14.08±6.9 %), low-dose MTX group (12.2±7.8%) and DX group (13.2±8.6%). The higher-dose MTX group presented less cartilage formation (0.81±0.7%). Thirty days after surgery, the saline and lower-dose MTX groups had almost complete closure of the fracture (5.3±0.01 and 8.07±0.03 µm respec-tively), while animals treated with 1.6 mg/Kg of MTX and DX kept an open bone defect (52.86±7.5 and 34.7±3.7 µm respectively). Our data show that low-dose MTX did not affect bone healing of mandibular fractures. In con-trast, the high-dose here employed impairs car-tilage formation that precedes bone healing.

The E!ect of Methotrexate on Bone Healing of a Simulated Fracture Defect in Rat Mandible

�Leonardo Toledo de Aguiar, DDS, MSc1 Suzana Beatriz Veríssimo de Mello, PhD2

João Gualberto de Cerqueira Luz, DDS, PhD3

1. Oral and Maxillofacial Surgeon, Hospital of the Southeast of Pará State, Fellow of Experimental Physiopathology Department, School of Medicine, and Fellow of Oral and Maxillofacial Surgery Department, School of Dentistry,

University of Sao Paulo, Brazil.

2. Associate Professor of Rheumatology Division, Department of Internal Medicine, School of Medicine, University of Sao Paulo, Brazil.

3. Associate Professor of Oral and Maxillofacial Surgery, Department of Oral and Maxillofacial Surgery, School of Dentistry, University of Sao Paulo, Brazil.

Abstract

KEY WORDS: Mandibular fracture, methotrexate, bone, cartilage, dexamethasone


92 • Vol. 2, No. 5 • June 2010

INTRODUCTIONMandibular fractures represent the great major-ity of facial trauma in road crashes and other accidents.1 Moreover, the treatment of maxil-lofacial injuries is mainly surgical and patients that arrive at a hospital are frequently under-going treatment with different medications.2

Immunosuppressive drugs can cause a sig-nificant delay in the consolidation of fractures and bone formation.3 Exogenous Glucocorticoid (GC) promotes bone loss and after a long-term administration, these drugs frequently promote osteoporosis in humans.4 This group of drugs includes Methotrexate (MTX), used in high doses as chemotherapy agent and as an anti-rheumatic agent in low doses.5 The literature is conclu-sive regarding the effect of high doses of MTX. Clinical studies have demonstrated that MTX decreases bone growth and reduces bone min-eral density (BMD), which persists into adult life and may increase bone fracture risk at an older age.6,7 Osteoporosis is verified in growing rats treated with high doses of MTX and is also asso-ciated with osteopenia in adult animals.8 Short-term administration of high-dose MTX can have a toxic effect on osteoblasts by reducing their vol-ume, without altering their number. In addition, this schedule of treatment impairs osteoid thickness.9

Concerning low-dose MTX effect on bone, osteoporosis has not been detected in humans.10 Contrarily, it has shown decreased BMD in growing rabbits chronically treated with MTX, which was reverted by concomitant treatment with folic acid.11 Nilsson et al12 dem-onstrated a lower effect of MTX on bone neofor-mation during the drug washout period, prior to surgery. A single report from a Brazilian regional journal showed that the MTX treatment did not

alter the repair process after unilateral condy-lectomy in mice.13 In humans, Gester et al14 reported two cases of rheumatic patients treated with low-dose MTX (7.5 and 15mg/week) who failed to recover from osteotomy. In both cases, bone union was observed soon after the MTX was discontinued. Moreover, a protective MTX effect on bone resorption has been described in rheumatoid patients.15 Patients with juvenile idio-pathic arthritis showed less temporomandibular destruction while undergoing MTX treatment.3

The clinical importance of this issue, the great variability of the previous results with different schedules of MTX treatments and the lack of a controlled study in mandibles led us to develop the present protocol to verify the effect of two increasing doses of MTX and dexamethasone (DX) on bone repair of mandibular fractures in rats.

MATERIALS AND METHODSAnimalsEighty female Wistar rats weighing 200-250g at the beginning of the study were employed. The animals were allowed a standard pellet diet and water ad libitum. During experimen-tal procedures, the animals were anaesthetized to avoid any stress condition. The Animal Eth-ics Committee of COBEA (Brazilian College of Experimental Animals) approved all experimen-tal procedures performed on animals in accor-dance with the procedures set by UFAW (The Universities Federation for Animals Welfare).

The eighty rats were randomly distributed in 4 groups of 20 animals: the control groups included a saline-treated group (1 ml after sur-gery) and a group (DX) intraperitoneally treated with 1 ml of dexamethasone (0.15 mg/Kg, one dose after surgery); this dose has been described

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as increasing bone resorption and decreasing bone formation.5 Groups of animals were intra-peritoneally treated with two doses of Methotrex-ate; 1.6 mg/Kg and 0.25 mg/Kg, both diluted in 1 ml of saline one hour before surgery and once a week during the post-surgical period. Gain in body weight was indistinguishable between groups (p = 0.105). No adverse gastrointesti-nal effects (vomiting or diarrhea) were observed as a consequence of treatments. The proto-col consisted in sacrificing groups of five ani-mals at 1, 7, 15 and 30 days after surgery.

Surgical ProcedureA surgical bone defect with near 50µm of width that simulates a mandibular fracture was pro-duced in rats anaesthetized with 0.4 ml of 1.0 mg/kg of xylazine and 0.75 mg/kg of ketamine. After trichotomy, the skin was cleansed and an inci-sion of approximately 15 mm was made exposing mandible bone by blunt dissection. A bicortical osteotomy was performed with a multi-laminated conical carbide bur number 701, from the base of the mandible towards the cranium (vertical ori-entation) with 10 mm of length. Soft tissues were replaced and sutured. The animals were kept in individual cages with food and water ad libi-tum and weighed weekly for drug administration.

Radiographic AnalysisAfter the animals were sacrificed, the mandi-bles were surgically excised and submitted to radiographic examination with a dental X-Ray equipment (Spectro II, Dabi Atlante), under 56 kV, 10 mA and 0.4 sec of exposure.

The radiographic analysis of mandibles was performed by two investigators blinded to the treatment regimen. In each digitized radi-

ography panel, the Image Pro Plus program was used to evaluate the distance between bony ends, measured in three regions, as well as the lesion area. The mean of two measurements were expressed in pixels.

Histomorphometric AnalysisSubsequently, the mandibles were paraffin-embedded and routinely processed. Sequen-tial Sections (7mm) were obtained and stained by Hematoxylin-Eosin (H&E) and tolu-idine blue. Images were captured (Leica Qwin Imaging Systems Ltd., Cambridge, Eng-land) and digitized in the computer, using an image analyzer software (Image Pro-plus 6).

The H&E-stained bone lesion was semi-quantitatively evaluated at 100x magnification for the following parameters: bone callus forma-tion, bony ends distance, presence of inflamma-tory cells, as well as cartilage amount and bone neoformation. These observations were made by 2 pathologists blinded to the treatment and expressed as the mean of two recorded values.

Statistical AnalysisResults are expressed as the mean of 5 ani-mals ± S.E. The results were analyzed by repeated measure ANOVA and com-pared with Student-Newman Keul’s test. The chosen level of significance was 0.05.

RESULTSBone Histomorphometric AnalysisIn order to quantify bone repair, we mea-sured the distance between the stumps of the bone defect at different times after the osteotomy. Slices of paraffin including man-dibles stained with hematoxylin-eosin were

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analyzed under a magnification of 100x. In figures 1A-E, representative pictures of a saline-treated rat in each experimental period are depicted in figures 1B to 1E. The data about the effect of treatments on the distances between bony ends is summarized in figure 1A.

Data on the animals sacrificed one day after surgery clearly showed that the surgical procedure generated homogenous fractures, which did not significantly differ among groups (p=0.222, ANOVA). At 7 days after the sur-gery, a slight, but not significant increase in this distance was recorded in all groups, which may reflect retraction of tissues in the fracture region. In figure 1C, we can observe granula-tion tissue (asterisk) in the osteotomy region on the 7th day, without treatment influence. At 15 days (figures 1A, 1D), we verified that saline-

injected animals presented a significant reduc-tion in the distance between bony ends when compared to values observed on day 7. It is possible to observe (figure 1D) a concomitant formation of cartilage tissue (double arrow) and bone neoformation (arrow). Animals treated with DX and 0.25 mg/Kg/week of MTX did not attain significant change at this time. The group treated with 1.6 mg/Kg/week of MTX exhibited an additional increase in the distance between bony ends. At the end of the experi-mental period (30 days after surgery) bone repair (figure 1E, arrow) in control animals and in those treated with low-dose MTX was still far from having the gap closed (figure 1, panels A and E), with a significant reduction in bony end distance (mean 5.3 ± 0.47 and 8.1 ± 0.73 µm respectively). In the mandible of animals treated

Figure 1a: E!ect of MTX, DX and saline on the distance between bony ends of mandibular fractures in rats at 1, 7, 15 and 30 days after surgery. Data is expressed as the mean of 5 animals ± SE, (N = control animals, S= MTX (1.6 mg/Kg/week), "= MTX (0.25mg/Kg/week) and M= DX (0.15mg/Kg one dose after surgery). * = p<0.05 vs. control at 7 days; # = p< 0.05 vs. control animals at 30 days and ** = p<0.05 vs. control animals at 15 days after surgery.

Figure 1b: Representative picture of the evolution of bone callus in saline-treated animals at 1 days after surgery. Magni#cation of x100, H&E stain.

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with high-dose MTX and DX, the osteotomy still remained open 30 days after surgery (mean 52.86 ± 9.3 and 34.7 ± 6.5 µm respectively).

Bone Radiographic AnalysisThe effect of the treatments on bone formation was also evaluated in radiographic panels (figures 2A,2C). Figures 2B and 2D exemplify the extent of the defect and how the distance between the bony ends (figure 2B, arrow) and the total area of osteotomy (figure 2D) were measured. Fig-ures 2A and 2C summarizes the effect of the treatments on these evaluated parameters. The homogeneity of the surgical procedure outcome could be also verified in radiographies of man-dibles taken one day after surgery and no differ-ence was observed among the groups at 7 days after surgery, regarding both parameters. Saline-injected animals and those treated with 0.25mg/

Figure 1c: Representative picture of the evolution of bone callus in saline-treated animals at 7 days after surgery. Magni#cation of x100, H&E stain.

Figure 1d: Representative picture of the evolution of bone callus in saline-treated animals at 15 days after surgery. Magni#cation of x100, H&E stain.

Figure 1e: Representative picture of the evolution of bone callus in saline-treated animals at 30 days after surgery. Magni#cation of x100, H&E stain.

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Kg/week of MTX were indistinguishable through-out all assessed periods. DX and the high dose of MTX promoted a significant increase in the distance between the bony ends and in the area of the osteotomy 15 days after sur-

gery, when compared with saline-injected ani-mals. Although there is a trend of reduction in that distance at 30 days after surgery, animals treated with higher doses of MTX and DX per-sisted with higher values than control animals.

Figure 2a: Radiographic evaluation of mandibular fracture in rats treated with MTX, DX and saline at 1 (white column), 7 (black column), 15 (gray column) and 30 days (hatched column) after surgery. This #gure shows the distance between bony ends measured at di!erent times after surgery.

Figure 2b: Representative radiography of normal rat mandible 1 day after surgery, the arrow show the 3 measurements of bone end distance.

Figure 2c: Area of the bone defect 1 (white column), 7 (black column), 15 (gray column) and 30 days (hatched column) after surgery. Data expressed as the mean of 5 animals ± SE, * p<0.05 vs. control animals.

Figure 2d: Representative radiography of normal rat mandible 1 day after surgery. In red the measured area of bone defect.

Cartilage NeoformationBone repair is accompanied by cartilage neo-formation. The effect of the treatments was also evaluated in slices of fractured mandibles simul-taneously stained with toluidine blue. Results are expressed as the percentage of cartilage in the total area of the bone callus (mm2). Figure 3A summarizes the results, and panels B and C exemplify the appearance of a control slice of the bone callus at 15 and 30 days, respectively. Using this software, we can highlight in red all cartilage tissue present in the area. The pattern of carti-lage tissue formation kinetics observed in control animals was an absence of this tissue in the first period (first 7 days), followed by a great increase at 15 days, with subsequent reduction at 30 days after surgery. (figure 3A). Regarding cartilage for-mation, animals treated with low-dose MTX and DX clearly presented the same pattern registered

in control groups. Animals treated with high-dose MTX did not present the characteristic upslope in cartilage formation at 15 days after the fracture.

DISCUSSIONOur study demonstrated that 0.25mg/Kg/week of MTX did not affect bone healing of mandibular fractures in rats. Interestingly, an


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Figure 3a: Percentage of newly formed cartilage amount in the fracture region 7, 15 and 30 days after surgery. Data are expressed as the mean of 5 animals ± s.e.m., black column= seven days, white column= 15 days, hatched column= 30 days after surgery. * = p<0.05 vs. values obtained 7 days after surgery # = p<0.05 by comparison with the control group at 15 days.

Figure 3b: Representative image of newly formed cartilage (red) on the 15th day (toluidine blue stained, original magni#cation $ 100)

Figure 3c: Representative image of the replacement of cartilage by bone veri#ed 30 days after surgery in normal rat mandible (toluidine blue stained, original magni#cation $ 100).

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almost six-fold higher MTX dose promoted bone regeneration impairment of the same magni-tude of dexamethasone. The above statement was based on the following findings: first, the chosen model, simulating jaw bone fracture in rats, is a helpful experimental model because it re-creates fracture in humans and nearly com-pletes closure at around 30 days. Eighty per-cent of mandibular fractures treated by open or closed reduction with intermaxillary immo-bilization are clinically united in 4 weeks.16,17

Additionally, our histological and radiologi-cal findings obtained on the first day after surgery clearly demonstrates that the bone defect was homogeneous among the groups.

The choice of DX as a negative control of bone neoformation was appropriate to com-pare with a possible deleterious effect of MTX on bone. The histological analysis of mandi-bles in osteoporotic (ovariectomized) rats with tooth extraction revealed a significant decrease in the bone volume at 14, 21, and 28 days after the extraction, as well as a decreased amount of granulation tissue.18 In accordance with that, our results also revealed a reduc-tion in bone and cartilage formation in animals treated with a single dose of DX after surgery.

Seven days after surgery, bone healing is still occurring in all groups with the forma-tion of granulation and cartilage tissues; our assessment showed that in this first phase of the study, no treatment significantly affected the process of bone restoration. On the 15th day of the postoperative period, a reduction in the frac-ture defect was clearly seen in animals treated with 1.6 mg/Kg/week of MTX, which presented a retraction of tissues in the fracture region and almost no cartilage formation. Concern-

ing this issue, studying newborn rats treated with much lower doses of MTX, Kameyama et al.19 reported that the MTX treatment inhibited the formation of cartilage and bone in the grow-ing mandibular condyle. At this phase, newborn animals present an intense growing process, so that the administration of a single dose of an immunosuppressive drug such as MTX can promote a deleterious effect on the craniofa-cial skeleton.20 However, adult rats treated with MTX, 0.1 mg/kg i.p., administered five times a week (cumulative dose of 0.5 mg /week), also exhibited a significant alteration in the strength of the healing osteotomies compared with the control group.21 Another in vivo study using a cumulative dose of 3.75 mg/Kg/ of MTX dur-ing one week described bone growth defects as a consequence of the reduction in chon-drocyte proliferation.22 The effect of low doses on bone healing can also occur in humans, as seen in the report of two cases of bone fracture nonunion in patients taking MTX, which used a therapeutic schedule similar to the one used by us, about 7.5 and 15 mg/patient/week.14

At the end of the study period, all groups including the one treated with higher-dose MTX presented some degree of bone tissue forma-tion in the fracture region. This finding suggests that the MTX treatment did not stop or prevent the repair, although it probably promoted a delay in the repair process. In the bone formation pro-cess, newly formed cartilage is followed by the osteoclastic degradation of the matrix. Osteo-blasts then migrate into the cavities that are formed by osteoclasts to produce the new bone matrix. As low-dose MTX has been described as reducing osteoblast cell proliferation along the trabecular surface 22,23 a possible mechanism for

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delaying the union is the inhibition of this cell.Together, our results show that low-dose

MTX did not affect cartilage or bone neoforma-tion in fracture healing. In contrast, the use of a higher dose of MTX had a worse prognosis in bone regeneration suggesting that, in cases of jaw fracture, there is no need to withdraw low-dose MTX treatment, whereas patients undergoing chemotherapy should be the tar-get of greatest concern among surgeons. L

Correspondence:Suzana Beatriz Veríssimo de MelloDepartamento de Clínica Médica, Disciplina de ReumatologiaAv. Dr. Arnaldo, nº 455, 3º andar, sala 3118Reumatologia. Cerqueira Cesar. CEP:01246-903São Paulo, SP – BrasilPhone: (11) 30617200 • Fax: (11) 30617490

DisclosureThe authors report no conflicts of interest with anything mentioned in this article.

AcknowledgmentsThe authors are grateful to Dr. Walcy Rosolia Teodoro for the helpful discussion of histopathological data, as well as to Viviane R Storto and Lucimar Rodrigues for their technical assistance.

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and pattern of maxillofacial fractures in the elderly. Int J Oral Maxillofac Surg 2003; 32: 206-208.

2. Hupp JR, Duddleston DN. Medical Management of the Surgical Patient. In: Miloro M, Ghali GE, Larsen PE, Waite PD. Peterson’s Principles of Oral and Maxillofacial surgery (ed 2). London, BC Decker Inc, 2004: 17.

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4. Sinigaglia L, Mazzochi D, Varenna M. Bone involvement in exogenous hypercortisolism. J Endocrinol Invest 2008; 31: 364-370.

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8. Spadaro JA, Damron TA, Horton JA, Margulies BS, Murray GM, Clemente DA, Strauss JA. Density and structural changes in the bone of growing rats after weekly alendronate administration with and without a methotrexate challenge. J Orthop Res 2006; 24: 936-944.

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13. Silva LA, Hetem S, Denardin OVP. Efeito do metotrexato sobre o reparo ósseo após condilectomia unilateral em camundongos (Mus musculus). Revista de Odontologia Unesp 2006: 35: 89. URL: http://rou.hostcentral.com.br/viewpub.php?id=404 [Accessibility verified May 20, 2009]

14. Gester JC, Bossy R, Dudler J. Bone non-union after osteotomy in patients treated with methotrexate. J Rheumatol 1999; 26(12):2695-2697.

15. El Miedany YM, Abubakr IH, El Baddini M. Effect of low dose methotrexate on markers of bone metabolism in patients with rheumatoid arthritis. J Rheumatol 1998;25: 2083-2087.

16. Juniper RP, Awty MD. The immobilization period for fractures of the mandibular body. Oral Surg Oral Med Oral Pathol 1973; 36: 157-163.

17. Amaratunga NA. The relation of age to the immobilization period required for healing of mandibular fractures. J Oral Maxillofac Surg 1995: 45: 111-113.

18. Pereira MC, Zecchin KG, Campagnoli EB, Jorge J. Ovariectomy delays alveolar wound healing after molar extractions in rats. J Oral Maxillofac Surg 2007; 65: 2248-2253.

19. Kameyama Y, Nakashima T, Sugita Y, Kubo K, Suzumura Y, Kawanishi K, Bessho M, Sato E, Maeda H. Effect of methotrexate on the mandibular condyles of growing rats. Int J Oral and Maxillofacial Surgery 2005; 34: 117.

20. Karsila S, Salmi TT, Ronning O. Effect of methotrexate alone and in combination with vincristine on craniofacial morphology in growing rats. Acta Odontol Scand 1999; 57: 271-276.

21. Pelker RR, Friedlaemder GE, Panjabi MM, Marham T, Hausman M, Doganis AC, Mckay J. Chemotherapy-induced alterations in the biomechanics of rat bone. J Orthop Res 1985; 3: 91-95.

22. Xian CJ, Cool JC, Scherer MA, Macsai CE, Fan C, Covino M, Foster BK. Cellular mechanisms for methotrexate chemotherapy-induced bone growth defects. Bone 2007; 41: 842-850.

23. Wheller DL, Vander Griend RA, Wronski TJ, Miller GJ, Keith EE, Graves JE. The short- and long-term effects of methotrexate on the rat skeleton. Bone 1995; 16: 215-221.

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