Does Grafting of Third Molar Extraction Sockets Enhance Periodontal ...

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Sockets Enhance Periodontal Measures in. 30- to 35-Year-Old Patients? Khalid S. Hassan, MSc, PhD,*. Hesham F. Marei, MSc, DDs(OMFS),† and. Adel S. Alagl ...
DENTOALVEOLAR SURGERY J Oral Maxillofac Surg 70:757-764, 2012

Does Grafting of Third Molar Extraction Sockets Enhance Periodontal Measures in 30- to 35-Year-Old Patients? Khalid S. Hassan, MSc, PhD,* Hesham F. Marei, MSc, DDs(OMFS),† and Adel S. Alagl, BDS, DSc‡

Purpose: This study was designed to evaluate the use of xenograft plus a membrane as grafting material

for periodontal osseous defects distal to the mandibular second molar compared with nongrafted extraction sites after removal of impacted mandibular third molars. Materials and Methods: We performed a single-blind, randomized, controlled clinical trial, and the sample comprised of subjects at high risk for the development of periodontal osseous defects distal to the second molar after third molar extraction (aged 30-35 years), pre-existing osseous defects distal to the second molar, and horizontal third molar impaction. The predictor variable was the treatment status of the second molar osseous defects. The third molar extraction sites were grafted with an anorganic xenograft plus a membrane. The other sites received a full-thickness flap and extraction of the third molar without placement of the grafting materials. The outcome variables were the change in gingival index, pocket probing depth, and clinical attachment level on the distobuccal aspect of the second molar preoperatively and at 3, 6, 9, and 12 months after surgery. Data were statistically analyzed by multivariate analysis of variance, and the statistical significance was set at P ! .05. Results: The study was composed of 28 sites that were selected by use of a split-mouth design for each patient, and this was randomly determined through a biased coin randomization. Twelve months after third molar removal, there was a statistically significant gain in the clinical attachment level and a reduction in the probing pocket depth in the grafted sites compared with the nongrafted sites (P ! .001). Moreover, there was a significant difference in the alveolar bone height during the monitoring periods for the grafted sites compared with the nongrafted sites (P ! .001). Conclusions: Grafting of osseous defects distal to mandibular second molars with an anorganic xenograft plus a membrane predictably resulted in a significant reduction in the probing pocket depth, clinical attachment level gain, and bone fill, which suggests that grafting the extraction sites with an anorganic xenograft plus a membrane could prevent periodontal disease in the future. This is a US government work. There are no restrictions on its use. Published by Elsevier Inc on behalf of the American Association of Oral and Maxillofacial Surgeons. J Oral Maxillofac Surg 70:757-764, 2012 Periodontal osseous defects frequently occur at the distal aspect of mandibular second molars where there is, or has been, an associated eruption pattern of the third molar.1-4 The retention of impacted third

molars, once they have been exposed to the oral environment and dental plaque, may lead to a more rapid periodontal attachment loss than is usually associated with adult periodontitis.5 Moreover, the

*Assistant Professor, Department of Preventive Dental Sciences, Division of Periodontics, College of Dentistry, University of Dammam, Dammam, Saudi Arabia, and Associate Professor, Department of Oral Medicine and Periodontology, Faculty of Dental Medicine, Al-Azhar University, Assiut, Egypt. †Assistant Professor, Department of Biomedical Dental Sciences, Division of Oral and Maxillofacial Surgery, College of Dentistry, University of Dammam, Dammam, Saudi Arabia, and Lecturer, Department of Oral & Maxillofacial Surgery, College of Dentistry, Suez Canal University, Ismailia, Egypt. ‡Assistant Professor and Chairman, Department of Preventive

Dental Sciences, College of Dentistry, University of Dammam, Dammam, Saudi Arabia. Address correspondence and reprint requests to Dr Hassan: Department of Preventive Dental Sciences, Division of Periodontics, College of Dentistry, University of Dammam, PO Box 1982, Dammam 31441, Saudi Arabia; e-mail: [email protected] This is a US government work. There are no restrictions on its use. Published by Elsevier Inc on behalf of the American Association of Oral and Maxillofacial Surgeons 0278-2391/12/7004-0$36.00/0 doi:10.1016/j.joms.2011.09.010

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758 communication within the oral cavity allows bacteria to colonize to the distal root surface of the resident second molar and either prevent normal development of the periodontium or aid in its destruction. Several studies have evaluated the management of periodontal osseous defects distal to the second molar after extraction. Osborne et al6 showed that little benefit is achieved by root planing the distal aspect of second molars after extraction of an adjacent impacted third molar. The results of these studies showed only a minimal reduction in the probing pocket depth or in inducing the reattachment of gingival tissues to the second molar at or near the cement-enamel junction. Similarly, little or no benefit was found when different flap designs were used in these situations.7-9 Consequently, the use of traditional treatments at the time of extraction of impacted third molars has often resulted in the development of an osseous defect at the distal aspect of the second molar, which may require surgical treatment later. A variety of materials have been used to stimulate regeneration or enhance attachment of the supporting structures in the periodontal defect sites. The use of bone grafting to augment the osseous defect has become one of the most common surgical techniques in recent years. However, the morbidity and limited availability associated with autografts, along with the potential for disease transmission, immunogenic response, and variable quality associated with allograft, have led to a wide variety of alternative materials. Various bone grafting materials are currently being used in alveolar bone grafting procedures, with different degrees of success. These materials have included autogenous bone (harvested from the patient’s iliac crest, rib, mandible, or maxillary tuberosity), allogeneic bone, bone graft substitutes (eg, tricalcium phosphate and porous hydroxyapatite), and a combination of these materials. However, all the materials have had limitations in their ability to restore the alveolar ridge adequately. The limitations have included inadequate blood supply, inconsistent performance, inability to restore alveolar ridge height, prolonged healing, and potential adventitious agent (viral) transmission (allogeneic bone). Moreover, the characteristics of an ideal bone graft substitute have consisted of a product that is nontoxic and noncarcinogenic and has consistently induced bone formation, has been readily available, has had an unlimited supply, and has been easy to use. Given these limitations and characteristics, the ideal agent to restore the alveolar ridge has not yet been identified. One of the grafting materials that has often been used to restore osseous defects is an anorganic xenograft, composed of resorbable anorganic bovine hydroxyapatite. Anorganic xenograft is a safe, effective bone graft material from specially processed bovine

GRAFTING OSSEOUS DEFECT DISTAL TO LAST MOLAR

sources. Under the electron microscope, anorganic xenograft appears very similar to human bone. Because of its similarity to human bone, it has been highly successful in helping form new bone. However, recent research has shown that the material is unpredictable in its amount of bone formation and is not completely resorbable.10,11 Moreover, the use of guided tissue regeneration (GTR) techniques has provided evidence for new attachment.12 Previous authors have suggested that cells necessary for the regeneration of the periodontal attachment apparatus appear to originate from the periodontal ligament.13,14 One of these techniques has involved the use of collagen-GTR, using a thin resorbable membrane made from the natural fiber material collagen. Often, when a bone graft has been needed, the membrane has been placed directly over the grafted material. In addition, the collagen membrane has encouraged new bone to form and has prevented the growth of scar tissue into the grafted site. For the purposes of this study, the primary research question was as follows: Among 30- to 35-year-old patients who had their mandibular third molars extracted, does grafting that uses an anorganic xenograft plus a membrane, when compared with no intervention, enhance the periodontal measures on the distal aspect of the mandibular second molars? The null hypothesis was that the risk of having an osseous defect on the distal aspect of the second molar after third molar extraction was the same between the grafted and nongrafted groups. The specific aim of this study was to evaluate the periodontal parameters and bone sounding measurements of the second molar 1 year after third molar extraction, as well as to evaluate grafting with an anorganic xenograft plus a membrane compared with nongrafted extraction sites.

Materials and Methods STUDY DESIGN/SAMPLE

To address the research purpose, we designed and implemented a split-mouth, randomized, single-blind, controlled clinical trial (Fig 1). The study population was composed of all patients who presented for evaluation and management of a bilateral extraction of horizontally impacted third molars between September 2009 and September 2010. To be included in the study sample, the patients had to be free from any systemic diseases, nonsmokers, not pregnant, and aged 30 to 35 years. In addition, they had to have bilateral impacted mandibular third molars and an adjacent second molar and had to agree to return for follow-up visits. Finally, the patients were prohibited from taking antibiotic, antimicrobial, or nonsteroidal anti-inflammatory medications in the preceding 3-month period.

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Study Population Patients with M3s (N=32) Excluded (n=18) Not meeting inclusion criteria (n=18) Refused to participate (n=0) Subjects randomly assigned and divided by split-mouth design into 2 treatment groups Study Sample (meets inclusion criteria (n=28)

Xenograft plus membrane group (n=14) randomly assigned

Non-grafted group (n=14) randomly assigned

Clinical parameters & radiographs measured up to 1 year

Clinical parameters & radiographs measured up to 1 year

Lost to follow-up (n=0)

Lost to follow-up (n=0)

Compare Xenograft plus membrane -treated to Nongrafted-treated sites FIGURE 1. Protocol schema. Hassan, Marei, and Alagl. Grafting Osseous Defect Distal to Last Molar. J Oral Maxillofac Surg 2012.

Patients were excluded as study subjects under the following conditions: they did not have bilateral impacted mandibular third molars; they were aged less than 30 years; they did not have adjacent second molars; they had pre-existing medical conditions that may impair wound healing, which included previous radiotherapy to the maxilla or mandible and liver or renal failure (including dialysis patients); they had no permanent address; they did not agree to return for follow-up visits; or they were mentally retarded individuals. STUDY VARIABLES

The primary predictor variable was treatment type, which was divided into 2 categories: the grafted site with xenograft plus membrane and the nongrafted site (control). Twenty-eight sites were selected by use of a split-mouth design for each patient, which was randomly determined through a biased coin randomization. One site received a pyramidal-shaped, full-

thickness mucoperiosteal flap with 1 vertical releasing incision, and the extraction sites distal to the second molars were filled with an anorganic xenograft plus a membrane (Bio-Oss covered by Bio-Gide membrane; Geistlich Pharma AG, Wolhusen, Switzerland) (group I). The other site received a pyramidalshaped, full-thickness mucoperiosteal flap with 1 vertical releasing incision and an extraction of the third molar without placement of the grafting materials (group II). Each patient was prepared for surgery with an initial phase of therapy, which included oral hygiene instructions, as well as scaling and root planing. Approximately 4 weeks after the initial therapy, the patients were re-evaluated to assess the clinical parameters and plaque control. All subjects were required to achieve good oral hygiene (O’Leary plaque index !20%) before progressing to the surgical phase of therapy. Written informed consent was obtained from each patient before the surgical procedure, and the proto-

760 col was reviewed and approved by the Ethical Committee of the College of Dentistry, University of Dammam, Dammam, Saudi Arabia. SURGICAL PROCEDURE

The same surgeon performed all procedures. After adequate anesthesia was obtained in the patients, the pyramidal-shaped, full-thickness mucoperiosteal flaps with 1 vertical releasing incision were elevated to expose the impacted third molars. Sectioning with a rotary instrumentation (No. 702 surgical bur fitted into the surgical headpiece) was accomplished with irrigation by use of sterile normal saline solution (0.9% sodium chloride) to facilitate removal and reserve the alveolar bone. After the extractions, any remaining dental follicle was curetted from the surgical sites, and the exposed distal root surfaces of the second molars were root planed with hand instruments. The surgical sites were then irrigated with sterile normal saline solution. The test sites were filled with a xenograft plus a membrane. The soft tissue flaps were then reapproximated to gain primary closure and ensure complete coverage of the membrane. The control contralateral extraction sites were similarly treated without filling with grafting materials. The buccal flaps were sutured to their original positions with No. 3-0 resorbable Vicryl chromic suture (Johnson & Johnson, New Brunswick, NJ). Sterile gauze packs were then placed over the surgical sites as pressure packs. The patients were instructed to take 1 g of Amoxicillin/ clavulanate potassium twice daily for 7 days and to use 0.12% chlorhexidine gluconate oral rinse twice daily for 6 weeks for plaque control. OUTCOME VARIABLES AND THEIR ASSESSMENT

The primary outcome variables were assessed at baseline and at 3, 6, 9, and 12 months postoperatively by use of the same periodontal probe (NUC-15 probe; Hu-Friedy, Chicago, IL) and were as follows: gingival index,15 pocket probing depth (PPD), and clinical attachment level (CAL).16 In addition, before and after the augmentation procedures, the bone sounding measurements were taken with a calibrated Williams periodontal probe to the nearest millimeter. The vertical height of the defect was measured from the most apical extent of the defect to a fixed point on the tooth surface because the coronal aspect of the gingival margin may have changed postoperatively. After the administration of local anesthesia to the patients, these measurements were taken again after 3, 6, 9, and 12 months. RADIOGRAPH EVALUATION

Standardized radiographs were taken with the use of film holder device (Rinn centering device, Dentsply Ltd, Weybridge, UK) before surgery and at intervals of

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3, 6, 9, and 12 months postoperatively.17 Identical exposure parameters were used during all examinations, and the examination film was automatically processed. All periapical radiographs were digitized and saved in a tagged image file format (TIFF). Then, the bone density and marginal bone levels were measured by use of ImageJ software (National Institutes of Health, Bethesda, MD).18 With this software, the areas to be measured, called regions of interest (ROIs), were selected (color density selection); a single pixel that represented a specific color (white pixels on radiographs) could be selected, or a threshold that allowed for the automatic selection of all other pixels in the ROI threshold areas could be traced and counted as the number of pixels to calculate the ratio of the whole ROI. The mean density was determined based on a scale of 0 to 256, where 256 (8 bits) represented the whitest pixel on the screen and 0 represented the areas of the darkest pixels on the screen. The ROI of these radiographs was a circle of a fixed size that precisely contained the critical size defect. The program calculated every pixel in the image and then performed the necessary calculations to obtain 1 number representing the mean density of all the pixels; this number must be between 0 and 256. The marginal bone level measurements were obtained by measuring points from the cementenamel junction to the defects on the preoperative radiographs and then comparing these measurements with the postoperative radiographs. DATA ANALYSIS

The data were analyzed with the SPSS program, version 13 (SPSS, Chicago, IL). The primary analyses of interest were to compare the various study variables between the control and tested sites (sites with xenograft plus membrane and nongrafted sites) in the presence of confounding variables. A repeated-measures analysis (multivariate analysis of variance) was used to detect differences between the 2 study sites (ie, tested vs control) over time in each treatment for the various clinical outcome variables. Within-group changes over time were assessed with the paired t test. The level of significance was set at P ! .05.

Results We selected 14 patients (8 men and 6 women with a mean age of 32 " 2.03 years) with bilateral, horizontally impacted third molars to participate in this randomized, split-mouth design study. The patients were selected from the outpatient clinic at the College of Dentistry, University of Dammam. The patient-specific and tooth-specific variables for each treatment group (ie, xenograft plus membrane or nongrafted) are summarized in Tables 1, 2, and 3.

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Table 1. CHANGES IN CLINICAL PARAMETERS AT BASELINE AND FOR DIFFERENT POSTOPERATIVE PERIODS

GI (Mean " SD) Group I (n # 14)

Baseline 3 mo 6 mo 12 mo

0.3 " 0.2 0.3 " 0.2 0.3 " 0.2 0.4 " 0.2

P value‡

.035

Group II (n # 14)

PPD (Mean " SD) P value*

0.3 " 0.4 $.99 (NS) 0.3 " 0.2 $.99 (NS) 0.3 " 0.2 $.99 (NS) 0.3 " 0 .111 (NS) .49

Group I (n # 14)

Group II (n # 14)

7.5 " 0.7 3.8 " 0.4 3.6 " 0.3 3.1 " 0.4

7.8 " 0.8 5.8 " 0.6 5.1 " 0.6 4.9 " 0.5

!.001†

!.001†

CAL (Mean " SD) Group I (n # 14)

Group II (n # 14)

5.1 " 0.4 2.3 " 0.3 2.1 " 0.3 1.5 " 0.3 4 !.001†

5.4 " 0.7 4.8 " 0.2 4.0 " 0.2 0.2 " 0.2

P Value*

.30 (NS) !.001† !.001† !.001†

P Value*

.43 (NS) !.001† !.001† !.001†

!.001†

Abbreviations: GI, gingival index; NS, nonsignificant difference. *Control versus xenograft plus membrane (multivariate analysis of variance). †Significant difference. ‡Paired t test. Hassan, Marei, and Alagl. Grafting Osseous Defect Distal to Last Molar. J Oral Maxillofac Surg 2012.

There were 14 patients in each group. There were no statistically significant differences in the study variables between the groups at baseline, which suggested that the final differences between the treated sites were not influenced by the initial defect characteristics, thus allowing the postoperative results to be compared. A reduction in the PPD was found after grafting with an anorganic xenograft plus a membrane. The following mean values for grafting with an anorganic xenograft plus a membrane were obtained: 7.5 " 0.7 mm at baseline, 3.8 " 0.4 mm at 3 months, 3.6 " 0.3 mm at 6 months, and 3.1 " 0.4 mm at 12 months. The previous values were compared with the following mean values for the nongrafted sites: 7.8 " 0.8 mm at baseline, 5.8 " 0.6 mm at 3 months, 5.1 " 0.6 mm at 6 months, and 4.8 " 0.5 mm at 12 months (P ! .001). The difference in the change in CAL from baseline to the postoperative monitoring periods between the

Table 2. PROBING BONE LEVEL MEASUREMENTS (BONE SOUNDING) AT BASELINE AND FOR DIFFERENT MONITORING PERIODS

grafted and nongrafted sites was statistically significant, with the grafted sites showing a mean gain in the CAL of 3.01 " 1.03 mm compared with 1.25 " 0.65 mm for the nongrafted sites at 12 months (P ! .001). There were no statistically significant differences between the groups for the gingival index (Table 1). Table 2 summarizes the changes in vertical bone sounding over time stratified by treatment group. The mean values for vertical bone sounding (vertical height of defect) were 8.0 " 0.04 mm at baseline, 4.5 " 0.02 mm at 3 months, 4.1 " 0.02 mm at 6 months, and 4.0 " 0.03 mm at 12 months for group I and 8.3 " 0.06 mm at baseline, 7.6 " 0.05 mm at 3 months, 7.4 " 0.04 mm at 6 months, and 7.3 " 0.04 mm at 12 months for group II (P ! .001). Table 3 summarizes the radiographic changes over time for the grafted and nongrafted sites. Significant differences in the alveolar bone height from baseline to the different monitoring periods were found for

Table 3. CHANGES IN ALVEOLAR BONE HEIGHT AT BASELINE AND FOR DIFFERENT MONITORING PERIODS

VHD (Mean " SD) (mm)

Baseline 3 mo 6 mo 12 mo P Value‡

Group I (n # 14)

Group II (n # 14)

8.0 " 0.04 4.5 " 0.03 4.1 " 0.04 4.0 " 0.03 !.001†

8.3 " 0.06 7.6 " 0.05 7.4 " 0.04 7.3 " 0.04 !.001†

Alveolar Bone Height (Mean " SD) (mm)

P Value*

.073 (NS) !.001† !.001† !.001†

Abbreviations: VHD, vertical height of defect; NS, nonsignificant difference. *Control versus xenograft plus membrane (multivariate analysis of variance). †Significant difference. ‡Paired t test. Hassan, Marei, and Alagl. Grafting Osseous Defect Distal to Last Molar. J Oral Maxillofac Surg 2012.

Baseline 3 mo 6 mo 12 mo P value‡

Group I (n # 14)

Group II (n # 14)

6.0 " 0.21 2.57 " 0.22 2.51 " 0.21 2.42 " 0.21 !.001†

6.21 " 0.40 6.01 " 0.41 5.67 " 0.42 5.01 " 0.40 !.001†

P Value*

. 38 (NS) !.001† !.001† !.001†

Abbreviation: NS, nonsignificant difference. *Control versus xenograft plus membrane (multivariate analysis of variance). †Significant difference. ‡Paired t test. Hassan, Marei, and Alagl. Grafting Osseous Defect Distal to Last Molar. J Oral Maxillofac Surg 2012.

762 the sites treated with xenograft plus a membrane compared with the nongrafted sites (2.42 " 0.21 mm and 5.01 " 0.40 mm, respectively; P ! .001).

Discussion For the purposes of this study, the research question was as follows: Among 30- to 35-year-old patients who had their mandibular third molars extracted, does grafting that uses an anorganic xenograft plus a membrane result in a decreased risk of the development of a periodontal osseous defect on the distal aspect of mandibular second molars? The aim of this study was to evaluate the use of an anorganic xenograft plus a membrane for periodontal osseous fill distal to the mandibular second molar compared with nongrafted extraction sites after removal of impacted mandibular third molars. Periodontal defects have been a frequent occurrence postoperatively at the distal aspect of the mandibular second molar after the removal of impacted third molars. Among several studies, it was shown that 43.3% of the cases result in probing depths of 7 mm or greater 2 years after removal of the third molar.19-21 Our study was designed to evaluate the use of a xenograft plus a membrane as a graft material for periodontal osseous defects distal to the mandibular second molar compared with nongrafted extraction sites after removal of impacted mandibular third molars. Most of these procedures have been studied and performed in a distal bony defect after third molar extraction sites. Particular attention has been focused on an anorganic xenograft because of its biocompatibility, lack of disease transfer risks, and ease of use. Because of these advantages, an anorganic xenograft has remained a viable choice as a regenerative material. Several clinical22,23 and histologic24,25 studies have promoted the use of anorganic bovine bone for grafting in intraosseous defects. In this context, an anorganic xenograft was developed for bone regeneration procedures. An anorganic xenograft is similar to human bone; it is readily accepted by our defense mechanisms as a “friendly” graft and, therefore, is not rejected. In addition, an anorganic xenograft has acted as a framework onto which bone-forming cells, blood vessels, and so on can migrate. As these cells and blood vessels travel along the anorganic xenograft framework, healthy new bone is formed and the defect is repaired. This study did not include the collection of tissues for histologic examination because of ethical considerations. The histologic examination of an anorganic xenograft at graft sites has been studied in animal models by Cardaropoli et al.26 The results showed that most of the newly formed mineralized tissue in the aug-

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mented defect sites with an anorganic xenograft has the character of woven bone (about 80%), which— over time—will most likely remodel and will mainly be replaced by bone marrow. In our study the randomized, split-mouth design was chosen, because it was intended to exclude patient-specific characteristics. The healing result of a single site, however, was dependent on a number of factors at baseline that may differ from site to site.25 In addition, at the time of each follow-up examination, we made the measurements without consulting the randomization schedule to determine which side was the treatment or control or what treatment the subject received. All patients were followed up for 1 year, and at the 1- and 2-week postoperative visits, there were no signs of infection or complications. When evaluating the periodontal parameters in this study, we established that we would only perform measurements at the distobuccal aspect of the second molar. This site was selected because it was readily accessible for measurements and was easily visualized, thus minimizing random measurement errors and simplifying the analyses and interpretations of the findings. This study is in agreement with that of Dodson,27 in which he elected to measure periodontal parameters at only 1 site (ie, distobuccal aspect of mandibular second molars). On the other hand, other studies that had multiple measurements per site have significantly complicated the analyses because of the issue of clustered, correlated observations.28,29 The results of our study showed that there is an overall increased gain in the CAL associated with both surgical sites (grafted and nongrafted). The mean CAL for the grafted sites was 4.25 " 1.28 mm at baseline and 1.24 " 0.52 mm at 12 months. The mean gain in CAL was 3.01 " 1.03 mm. However, the mean gain in CAL at 1 year was significantly less in the nongrafted sites (1.25 " 0.65 mm). The mean difference in CAL for the grafted versus nongrafted sites involved a mean gain of 1.76 mm on the grafted side. Moreover, in our study a significant reduction in the pocket depth reduction was obtained after the use of an anorganic xenograft plus a membrane material. These results are in accordance with the study performed by Scabbia and Trombelli,30 which claimed that there is a clinically and statistically significant improvement in terms of CAL gain, PPD reduction, and radiographic findings when an anorganic xenograft is used for the treatment of deep intraosseous defects. Furthermore, Sammartino et al31 grafted mandibular third molar extraction sites with only bovine porous bone mineral and with bovine porous bone mineral plus collagen membrane. Their results showed that both treatment modalities are successful in PPD reduction and increased CAL gain. The bovine porous bone mineral

HASSAN, MAREI, AND ALAGL

with collagen membrane had the best outcome for the prevention of a second molar periodontal defect. Notably, the intraoral radiograph taken immediately after the third molar removal and before the placement of graft was used as a baseline because of the difficulty of determining the bottom of the defect with the third molar in place. The radiographic changes in the alveolar bone height that were recorded over the 1-year period in our study showed a loss in height at both the treated sides when compared with baseline. At the end of 1 year, the mean alveolar height for the grafted side was 2.42 " 0.21 mm. This represented a net increase of 3.59 " 1.14 mm when compared with baseline. The mean alveolar height for the nongrafted side was 5.01 " 0.40 mm, which resulted in a net gain of 1.20 " 1.32 mm. The difference between the 2 sides at 1 year was a net mean increase in alveolar height of 2.59 mm on the grafted sides. However, a patient population may exist that would predictably benefit from grafting of the extraction sites after removal of the third molars. In the study performed by Pecora et al,32 they observed a statistically significant benefit of using GTR therapy over no intervention in a sample limited to subjects aged 26 years or greater, with at least 1 horizontal impaction and a probing depths of 5 mm or greater for at least 1 of the sites. In our study the therapeutic studies were not limited to subjects aged 26 years or greater; they included older subjects, probing depths of 5 mm or less, and CALs of 5 mm or less. However, in the study performed by Etiene et al,33 they reported that socket grafting with xenogeneic materials did not change the bone height and bone radiographic density in the long-term. The bone density values increased significantly in the first 6 months, with no alterations observed up to 24 months. From the results of this study, it can be concluded that grafting of osseous defects distal to mandibular second molars with an anorganic xenograft plus a membrane will predictably result in significant PPD reduction, CAL gain, and bone fill, suggesting that grafting the extraction sites with an anorganic xenograft plus a membrane could prevent periodontal disease in the future. Further research is recommended for evaluating grafting extraction sites after the surgical removal of impacted third molars in older patients. Acknowledgments The authors express many thanks to the assistant staff at the College of Dentistry, King Fahd Hospital, and Dr Suliman Al-Mansour at the University of Dammam.

References 1. Kugelberg CE, Ahlstrom U, Ericson S, et al: Periodontal healing after impacted lower third molar surgery. A retrospective study. Int J Oral Maxillofac Surg 14:29, 1985

763 2. Kugelberg CF: Periodontal healing two and four years after impacted lower third molar surgery. A comparative retrospective study. Int J Oral Maxillofac Surg 19:341, 1990 3. Szmyd L, Hester WR: Crevicular depth of the second molar in impacted third molar surgery. J Oral Surg Anaesth Hosp Dent Surv 21:185, 1963 4. Gröndahl HG, Lekholm U: Influence of mandibular third molars on related supporting tissues. Int J Oral Surg 2:137, 1973 5. Ash MM: Third molars as periodontal problems. Dent Clin North Am 8:51, 1964 6. Osborne WH, Snyder KJ, Tempel TR: Attachment levels and crevicular depths at the distal of mandibular second molars following removal of adjacent third molars. J Periodontol 53: 93, 1982 7. Labelle RE: The influence of third molars on periodontal health. Minn Dent J 53:25, 1969 8. Groves BJ, Moore JR: The periodontal implications of flap design in lower third molar extractions. Dent Pract Dent Res 20:297, 1970 9. Woolf RH, Malmquist JR: Third molar extraction: Periodontal implications of 2 flap designs. J Gen Dent 26:52, 1978 10. Block MS, Kent JN: Sinus augmentation for dental implants: The use of autogenous bone. J Oral Maxillofac Surg 55:1281, 1997 11. Skoglund A, Hising P, Young C: A clinical and histologic examination in humans of the osseous response to implanted natural bone mineral. Int J Oral Maxillofac Implants 12:194, 1997 12. Nyman S, Lindhe J, Karring T, et al: New attachment following surgical treatment of human periodontal disease. J Clin Periodontol 9:290, 1982 13. Nyman S, Gottlow T, Karring T, et al: The regenerative potential of the periodontal ligament. An experimental study in the monkey. J Clin Periodontol 9:257, 1982 14. Isidor E, Karring T, Nyman S, et al: The significance of coronal growth of periodontal ligament tissue for new attachment formation. J Clin Periodontol 13:145, 1986 15. Löe H, Silness J: Periodontal disease in pregnancy. I. Prevalence and severity. Acta Odontol Scand 21:533, 1963 16. Ramfjord SP: The periodontal disease index (PDI). J Periodontol 38:602, 1967 17. McDonald SP: A method to reduce interproximal overlapping and improve reproducibility of bitewing radiographs for use in clinical trials. Community Dent Oral Epidemiol 11:289, 1983 18. Burger B: Digital Image Processing—An Algorithmic Approach Using Java. New York, NY, Springer-Verlag, 2008 19. Kugelberg CF, Ahlström U, Ericson S, et al: Periodontal healing after impacted lower third molar surgery in adolescents and adults. A prospective study. Int J Oral Maxillofac Surg 20:18, 1991 20. Kugelberg CF, Ahlström U, Ericson S, et al: The influence of anatomical, pathophysiological and other factors on periodontal healing after impacted lower third molar surgery. A multiple regression analysis. J Clin Periodontol 18:37, 1991 21. Scopp IW, Kassouny DY, Morgan FH: Bovine bone (Boplant). J Periodontol 37:400, 1966 22. Older LB: The use of heterogenous bovine bone implants in the treatment of periodontal pockets. An experimental study in humans. J Periodontol 38:539, 1967 23. Arrocha R, Wittwer JW, Gargiulo AW: Tissue response to heterogeneous bone implantation in dogs. J Periodontol 39:40, 1968 24. Nielsen IM, Ellegaard B, Karring T: Kielbone in healing interradicular lesions in monkeys. J Periodont Res 15:328, 1980 25. Nielsen IM, Ellegaard B, Karring T: Kielbone in new attachment attempts in humans. J Periodontol 52:723, 1981 26. Cardaropoli G, Araújo M, Hayacibara R, et al: Healing of extraction sockets and surgically produced—augmented and nonaugmented— defects in the alveolar ridge. An experimental study in the dog. J Clin Periodontol 32:435, 2005 27. Dodson TB: Management of mandibular third molar extraction sites to prevent periodontal defects. J Oral Maxillofac Surg 62:1213, 2004

764 28. Chuang S-K, Tian L, Wei L-J, et al: Kaplan-Meier analysis of dental implant survival: A strategy for estimating survival with clustered observations. J Dent Res 80:2016, 2001 29. Panageas KS, Begg MD, Grbic JT, et al: Analysis of multiple 2x2 tables with site-specific periodontal data. J Dent Res 82:514, 2003 30. Scabbia A, Trombelli L: A comparative study on the use of a HA/collagen/chondroitin sulphate biomaterial (Biostite) and a bovine-derived HA xenograft (Bio-Oss) in the treatment of deep intra-osseous defects. J Clin Periodontol 31:348, 2004

GRAFTING OSSEOUS DEFECT DISTAL TO LAST MOLAR 31. Sammartino G, Tia M, Bucci T, et al: Prevention of mandibular third molar extraction-associated periodontal defects: A comparative study. J Periodontol 80:389, 2009 32. Pecora G, Celleti R, Davapanah M, et al: The effects of guided tissue regeneration on healing after impacted mandibular third molar surgery: 1-Year results. Int J Periodontics Restorative Dent 13:397, 1993 33. Etiene AM, Augusto B, Osny FJ, et al: Bone crestal height and bone density after third-molar extraction and grafting: A longterm follow-up study. Clin Oral Investigat 15:123, 2011