Francisco H. Nociti Jr. Maria Angela N. Machado Cristine M. Stefani Enilson A. Sallum Antonio W.

Sallum

Absorbable versus nonabsorbable membranes and bone grafts in the treatment of ligature-induced periimplantitis defects in dogs
Part I. A clinical investigation

Authors afliations: Francisco H. Nociti Jr., Maria Angela N. Machado, Cristine M. Stefani, Enilson A. Sallum, Antonio W. Sallum, Dental School of Piracicaba University of Campinas, Department of Periodontics Piracicaba, Sao Paulo, Brazil Correspondence to: Prof. Francisco Humberto Nociti Jr Faculdade de Odontologia de Piracicaba/ Unicamp, Av. Limeira, 901 CEP: 13414018, Piracicaba, S.P./Brazil Tel: 55 19 4305298 Fax: 55 19 4305218 e-mail: nociti/fop.unicamp.br

Key words: peri-implantitis, absorbable/nonabsorbable membrane, bone graft Abstract: The purpose of this study was to clinically evaluate an absorbable collagen membrane (Bio-GideA) and a nonabsorbable polytetrauoroethylene membrane (PTFE), associated or not with bone grafts, for the treatment of ligature-induced peri-implantitis defects in dogs. The bilateral mandibular premolars were removed from 5 2-year-old mongrel dogs. After 3 months of healing, 3 titanium implants were placed on each side of the mandible. Experimental peri-implantitis was induced after abutment connection. Ligatures and abutments were removed after 1 month and the bone defects were randomly assigned to one of the following treatments: DB: debridement alone; GBRBG-I: debridement plus PTFE membrane associated with mineralized bone graft (Bio-OssA); GBRBG-II: debridement plus collagen membrane (Bio-GideA) associated with mineralized bone graft; GBR-I: debridement plus PTFE membrane; GBR-II: debridement plus collagen membrane; BG: debridement plus mineralized bone graft. The periimplant bone defects were measured before and 5 months after treatment. Results showed the greatest percentage of vertical bone ll for GBRBG-II (27.7714.07) followed by GBR-II (21.7816.19), BG (21.266.87), GBRBG-I (19.5713.36), GBR-I (18.8610.63) and DB (14.035.6). However, the values were not statistically signicant (ANOVA, contrast F test, P0.612). Within the limits of the present investigation, it can be concluded that no difference was detected among treatments.

Date:

Accepted 27 March 2000

To cite this article:

Francisco H. Nociti Jr., Maria Angela N. Machado, Cristine M. Stefani, Enilson A. Sallum, Antonio W. Sallum. Absorbable versus nonabsorbable membranes and bone grafts in the treatment of ligature-induced peri-implantitis defects in dogs. Part I. A clinical investigation Clin. Oral Impl. Res. 12, 2001; 115120 Copyright C Munksgaard 2001 ISSN 0905-7161

The long-term predictability of osseointegrated implants has been documented (Albrektsson et al. 1986). Occasionally, however, peri-implant tissue destruction occurs during the implant maintenance phase (Worthington et al. 1987), resulting in the exposure of the implant surfaces previously embedded in bone. This peri-implant destruction has been associated with the presence of pathogenic bacteria around the implant and is called peri-implantitis (Quirynen et al. 1992). Guided bone regeneration techniques, which exclude connective tissue and epithelium from the defect to permit bone regeneration without the

competition of other tissues, have been successfully applied in the treatment of peri-implant bone defects (Simion et al. 1996, 1997; Zitzmann et al. 1997; Lorenzoni et al. 1998; Hockers et al. 1999). The membranes most often used for guided bone regeneration are bioinert membranes made of expanded polytetrauoroethylene (e-PTFE). Recently, absorbable membranes have been used for guided bone regeneration (Gotfredsen et al. 1994; Lundgren et al. 1994; Simion et al. 1996; Hrzeler et al. 1998). The major benet of using absorbable membranes to deal with bone defects around dental implants is that a second surgical inter-

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Fig. 1. The ligatures around the implants in a submarginal position.

Fig. 4. Clinical appearance of the soft tissues around the implants 2 weeks after removing the ligatures and after the hygienic phase of treatment. Tissue inammation was drastically reduced.

Fig. 2. Inammatory aspect of the peri-implant tissue after removing the submarginal ligatures.

Fig. 5. Clinical appearance of the stent and the orthodontic wire in position.

Fig. 3. Radiographic appearance of the bone loss around the implants 1 month after placing the ligatures. Note that the morphology of the

peri-implant bone defects was wide and circumferential.

vention to remove the membrane is not necessary and thus the alveolar bone is not exposed. Some researchers have evaluated the use of guided bone regeneration procedures adjacent to periimplant defects resulting from peri-implantitis (Grunder et al. 1993; Jovanovic et al. 1993; Hrzeler et al. 1995, 1997; Persson et al. 1996; Wetzel et al. 1999). However, there is a lack of data comparing the use of absorbable and nonabsorbable membranes in the treatment of ligature-induced peri-implantitis bone defects. The purpose of this study was, therefore, to compare the treatment of ligature-induced peri-implantitis bone defects using an absorbable collagen membrane and a nonabsorbable polytetrauoroethylene membrane, associated or not with bone grafts.

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Nociti Jr et al . Treatment of ligature-induced peri-implantitis in the dog

Material and methods

Five 2-year-old mongrel dogs with good general health were used (approximately 15 kg body weight). The animals received 1.5 ml/10 kg of acepromazine followed by intravenous injection of 25% sodium thiopental solution (0.5 ml/kg) and local administration of 2% xylocaine (1:50,000 epinephrine) in all surgical procedures. At the beginning of the experiment, all mandibular premolars were removed. After 3 months of healing, full-thickness aps were elevated and 3 screw-shaped CP titanium implants with rough acid-etched surfaces (Napio SystemA, Napio, Bauru, SP, Brazil) with a length of 8.5 mm, an outer diameter of 3.75 mm, and a pitch height of 0.6 mm were placed bilaterally and the mucoperiosteal aps sutured. Three months later, mucoperiosteal aps were elevated and titanium abutments positioned. Two weeks after the abutment connection, bilateral alginate impressions were taken and occlusal acrylic stents were prepared for pre- and posttreatment measurements of bone defect depth. Six points were marked on the surface of the stent: mesio-buccal, midbuccal, disto-buccal, mesio-lingual, midlingual and disto-lingual. Cotton ligatures were placed in a submarginal position around the abutments (Fig. 1) and the dogs were fed a soft diet to promote plaque accumulation. After 1 month, signicant inammation could be seen at the peri-implant mucosa and bone loss was detected radiographically (Figs 2, 3). At this time, the ligatures were removed, and a plaque-control regime was initiated (hygienic phase) consisting of daily brushing and topical application of 0.12% chlorhexidine gluconate. Metronidazole hydrochloride (250 mg/day) was administered systemically for 3 weeks. Two weeks after the beginning of the hygienic phase (Fig. 4), full-thickness aps were elevated. The abutments were removed and the granulation tissue around the implants was carefully removed using teon hand curettes. The implant surface was treated with an air-powder abrasive instrument for 30 s. The periimplant bone defects were clinically evaluated and the pretreatment extension of the defect, i.e. the distance from

Fig. 6. Comparisons of vertical bone ll (%) between treatments in each animal. DB: ap debridement; GBRBG-I: debridement plus guided bone regeneration/mineralized bone graft (nonabsorbable membrane); GBRBG-II: debridement plus guided bone regeneration/mineralized bone

graft (absorbable membrane); GBR-I: debridement plus guided bone regeneration (nonabsorbable membrane); GBR-II: debridement plus guided bone regeneration (absorbable membrane); BG: debridement plus mineralized bone graft.

the top of the stent to the bottom of the peri-implant bone defect, was recorded using an orthodontic wire (0.8 mm) and an electronic digital caliper accurate to 0.01 mm (Starrett, Itu, SP, Brazil) for 6 sites around each implant (Fig. 5). All measurements throughout the study were made by the same examiner, who was unaware of the treatment applied. The defects were randomly assigned to one of the following treatments: DB: debridement alone; GBRBG-I: debridement plus a nonabsorbable membrane (PTFE, Napio, Bauru, SP, Brazil) associated with a bone graft (Bio-OssA, Osteohealth Co., NY, USA); GBRBG-II: debridement plus an absorbable collagen membrane (Bio-GideA, Osteohealth Co.) and bone graft (Bio-OssA); GBR-I: debridement plus nonabsorbable membrane; GBR-II: debridement plus absorbable collagen membrane; BG: debridement plus the mineralized bone graft. The aps were repositioned and sutured. Systemic metronidazole administration was continued for the following week, and 0.12% chlorhexidine gluconate spray was topically applied twice a day for the next 5 months. After a healing period of 4 months, a ap was reected and the PTFE membranes were removed. Five months after treatment, re-entry was made for measurement of post-treatment clinical parameters. The complete randomized block design provided a total of 30 implants (6 implants per animal) for statistical

analysis. Pre- and post-treatment clinical measurements were averaged to obtain a mean value for the bone defect depth. One-way analysis of variance (ANOVA) was performed using the mean values to compare the 6 treatments.

Results
Clinical signs of peri-implant inammation were reduced after 2 weeks of plaque control and systemic anti-

Table 1. Percentage of vertical bone ll (VBF) according to treatment Treatment

DB GBRBG-I GBRBG-II GBR-I GBR-II BG

VBF(%)*
14.035.60 19.5713.36 27.7714.07 18.8610.63 21.7816.19 21.266.87

Data are reported as meanSD. * ANOVA: P0.612. DB: ap debridement; GBRBG-I: debridement plus guided bone regeneration/mineralized bone graft (nonabsorbable membrane); GBRBG-II: debridement plus guided bone regeneration/mineralized bone graft (absorbable membrane); GBR-I: debridement plus guided bone regeneration (nonabsorbable membrane); GBR-II: debridement plus guided bone regeneration (absorbable membrane); BG: debridement plus mineralized bone graft.

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Fig. 7. Percentage of vertical bone ll between treatments. DB: ap debridement; GBRBG-I: debridement plus guided bone regeneration/mineralized bone graft (nonabsorbable membrane); GBRBG-II: debridement plus guided bone regeneration/mineralized bone graft (absorbable

membrane); GBR-I: debridement plus guided bone regeneration (nonabsorbable membrane); GBR-II: debridement plus guided bone regeneration (absorbable membrane); BG: debridement plus mineralized bone graft.

microbial administration (Fig. 4). In 4 sites, exposure of the membrane occurred after 3 months of healing. The membrane exposure involved 2 sites of nonabsorbable (Fig. 6 animals 2 and 3/ GBRBG-I) and two sites of absorbable membranes (Fig. 6 animal 2/GBR-II and GBRBG-II). They were treated twice a day with topical application of 1% chlorhexidine. The portion of collagen membrane that was exposed showed a progressive resorption and disappeared after 2 weeks of exposure. The exposed PTFE membrane was also maintained for a period of 4 weeks with topical application of 1% chlorhexidine, and then it was removed. The peri-implant tissues around the exposed PTFE membrane demonstrated a moderate inammatory process, which was not seen around the collagen membranes. The remaining 26 sites remained covered by the soft tissues until the end of the experimental period. After 5 months of healing, newly formed hard tissue was observed lling the defects around the implants for all treatments (Table 1). Comparison between pre- and post-treatment values revealed a variable degree of hard tissue ll for all treatment procedures. However, one-way ANOVA did not show statistically signicant differences between any of the treatments (P0.612), in spite of the fact that the magnitude of the values indicated better results for GBRBG-II followed by GBR-II, BG, GBRBG-I,

GBR-I and debridement alone (Table 1 and Fig. 7).

Discussion
Studies have evaluated the potential of regenerative procedures to generate new bone around dental implants in several clinical situations. The principal sort of bone defects evaluated have been dehiscence and/or fenestration, and bone defects resulting from tooth extraction (Zitzmann et al. 1997; Simion et al. 1997). The number of studies evaluating different treatment options for peri-implantitis bone defects is limited (Jovanovic et al. 1993; Grunder et al. 1993; Hrzeler et al. 1995, 1997; Persson et al. 1996, 1999; Wetzel et al. 1999). The present clinical study compares a collagen membrane and a PTFE membrane in terms of bone regeneration around titanium implant surfaces exposed to contaminants. Many different approaches have been tested to reduce inammation at the peri-implant mucosa (Mombelli & Lang 1992; Lavigne et al. 1994; Flemmig 1994). In the present study, as suggested by Hrzeler et al. (1995), an association of local and systemic treatment was used resulting in a reduction of the clinical signs of inammation in the periimplant mucosa. Pre- and post-treatment clinical evaluations revealed a

variable degree of hard tissue ll of the bone defects after all treatment procedures. In spite of the fact that the values indicated better results for GBRBG-II followed by GBR-II, BG, GBRBG-I, GBR-I and debridement alone, statistical analysis did not show differences between any of the treatments (P0.612), in agreement with Simion et al. (1997) and Zitzmann et al. (1997). However, caution must be taken when comparing the results presented in the present study with previously reported data, due to the fact that bone regeneration using absorbable or nonabsorbable membranes for treating implant surface exposed to plaque accumulation has not been previously evaluated. Three factors can inuence the amount of bone formation around dental implants submitted to regenerative procedures: morphology of the bone defect (Hrzeler et al. 1997; Persson et al. 1999), space-maintaining capability (Simion et al. 1996; Lorenzoni et al. 1998) and the duration of the membrane (Simion et al. 1996). In the present study, after 1 month of plaque accumulation, a chronic circumferential bone defect was observed around the implants, similar to that reported by Hrzeler et al. (1995). The hypothesis that this type of bone defect is the most predictable considering bone regeneration around an implant was conrmed in the present investigation since all treatment modalities showed a signicant hard tissue ll, including ap debridement alone. Furthermore, the presence of the bone graft seemed to compensate for the lack of stiffness presented by the absorbable membrane, avoiding membrane collapse with the implant surface, and resulting in the greatest hard tissue ll (Sandberg et al. 1993; Simion et al. 1997). Within the limits of the present investigation, it can be concluded that no difference could be detected between the treatments. However, the results from the present study should be regarded with caution due to the small sample size.
Acknowledgments: This research was supported by FAPESP (Foundation for Financial Support of Research Sao Paulo State) Grant no. 97/132138. The authors greatly appreciate the assistance of NAPIO (Osseointegrated Implant

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Nociti Jr et al . Treatment of ligature-induced peri-implantitis in the dog

Research Center) for supplying the implants.

abgeschlossener Heilung, implantierte man auf jeder Seite des Unterkiefers drei Titanimplantate. Nach dem Aufsetzen der Sekundarteile wurde eine experi mentelle Periimplantitis induziert. Einen Monat spa ter wurden Ligaturen und Sekundarteile entfernt und die Knochendefekte zufallig einer der folgenden Be handlungsarten zugefuhrt: DB: nur Debridement; GBRBG-I: Debridement, Defektfullung mit einem mineraliserten Knochentransplantat (Bio-OssA) und Defektdeckung mit einer PTFE-Membran; GBRBGII: Debridement, Defektfullung mit einem minerali sierten Knochentransplantat und Defektdeckung mit einer Kollagen-Membran (Bio-GideA); GBR-I: Debridement und Defektdeckung mit einer PTFE-Membran; GBR-II: Debridement und Defektdeckung mit einer Kollagen-Membran; BG: Debridement und Defektful lung mit einem mineralisierten Knochentransplantat; Die periimplantaren Knochendefekte wurden vor der Behandlung und 5 Monate spater vermessen. Die Re sultate zeigten, dass die grosste prozentuale vertikale Knochenauffullung bei der Gruppe GBRBG-II (27.7714.07) stattfand, gefolgt von der Gruppe GBRII (21.7816.19), BG (21.266.87), GBRBG-I (19.5713.36), GBR-I (18.8610.63) und DB (14.035.6). Die Ergebnisse waren jedoch nicht statistisch signikant (ANOVA, Kontrast F Test, P0.612). Mit den gewahlten Vorgaben konnte man also keine Unterschiede zwischen den verschiedenen Behandlungen feststellen.

desbridamiento mas membrana de colageno (Bio GideA) asociado con injerto oseo mineralizado; GBR I: desbridamiento mas membrana de PTFE; GBR-II: desbridamiento mas membrana de colageno; BG: des bridamiento mas injerto oseo mineralizado. Los defec tos oseos se midieron antes y cinco meses despues del tratamiento. Los resultados mostraron un mayor por centaje de relleno oseo vertical para GBRGB-II (27.7714.07) seguido por GBR-II (21.7816.19), BG (12.266.87), GBRBG-I (19.5713.36), GBR-I (18.8610.63) y DB (14.035.6). De todos modos los valores no fueron estadsticamente signicativos (ANOVA, test de contraste F, P0.612). Dentro de los limites de la presente investigacion se puede concluir que no se detectaron diferencias entre los tratamientos.

Resume
Le but de cette etude a ete devaluer cliniquement une ` membrane en collagene absorbable (Bio-GuideA) et une en teon non-absorbable (PTFE) associees ou non ` a des greffons osseux pour le traitement de lesions paromplantites induites par ligature chez le chien. Les premolaires inferieures ont ete avulsees chez cinq ba` tards de deux ans. Apres trois mois de guerison, trois implants en titane ont ete places de chaque cote de la mandibule. La paroimplantite experimentale a ete ` induite apres la connection des piliers. Les ligatures et ` les piliers ont ete enleves apres un mois et les lesions ` osseuses ont ete reparties de maniere randomisee vers un des traitements suivants: DB: nettoyage seul, GBRBG-I: nettoyage plus Bio-Oss plus membrane en teon, GBRBG-II: nettoyage plus Bio-GideA plus greffe dos mineralise, GBR-I: nettoyage plus membra ne en teon, GBR-II: nettoyage plus membrane colla` gene, BG: nettoyage plus greffe dos mineralise. Les lesions osseuses paromplantaires ont ete mesurees ` avant et cinq mois apres le traitement. Les resultats ont montre le plus grand pourcentage de remplissage osseux vertical pour GBRBG-II (27,814,1) suivi de GBR-II (21,816,2), BG (21,36,9), GBRBG-I (19,613,4), GBR-I (18,910,6) et DB (14,05,6). Ce pendant ces valeurs netaient pas statistiquement signicatives (ANOVA, test F contraste, P0,612). Dans les limites de letude presente, il peut etre conclu quaucune difference na ete detectee entre ces traitements.

Resumen
La intencion de este estudio fue evaluar clnicamente una membrana reabsorvible de colageno (Bio-GuideA) y una membrana no reabsorvible de politetrauoroe tileno (PTFE), asociada o no con injertos oseos, para el tratamiento de defectos de periimplantitis inducida por ligaduras en perros. Se extrajeron los premolares mandibulares bilateralmente de cinco perros mongrel de dos anos de edad. Tras tres meses de cicatrizacion se colocaron tres implantes de titanio en cada lado de la mandbula. Se indujo periimplantitis experimental tras la conexion de los pilares. Las ligaduras y los pila res se retiraron despues de un mes y los defectos oseos fueron asignados aleatoriamente a uno de los siguien tes tratamientos: DB: solo desbridamiento; GBRBG I. desbridamiento mas membrana de PTFE asociada con injerto oseo mineralizado (Bio-OssA); GBRBG-II:

Zusammenfassung
Das Ziel dieser Studie war es, klinisch eine resorbierbare Kollagenmembran (Bio-GideA) und eine nicht resorbierbare Polytetrauoroethylen-Membran (PTFE) mit oder ohne Fuller (Knochentransplantat) zur Be handlung von ligatureninduzierten Periimplantitisdefekten von Hunden zu untersuchen. Bei 5 zweijahri gen Bastarden wurden beidseitig die Unterkieferpra molaren extrahiert. Drei Monate spater, nach

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