A comparative clinico-radiographic study of guided tissue regeneration with bioresorbable membrane and a composite synthetic bone graft for the treatment of periodontal osseous defects.

AIM: The aim was to evaluate the bonefill in periodontal osseous defects with the help of guided tissue regeneration, bioresorbable membrane (PerioCol) + bone graft (Grabio Glascera) in combination and with bonegraft (Grabio Glascera) alone.
MATERIALS AND METHODS: The study involved total 30 sites in systemically healthy 19 patients. The parameters for evaluation includes plaque index sulcus bleeding index with one or more periodontal osseous defects having (i) probing depth (PD) of ≥ 5 mm (ii) clinical attachment loss (CAL) of ≥ 5 mm and (iii) ≥3 mm of radiographic periodontal osseous defect (iv) bonefill (v) crestal bone loss (vi) defect resolution. The study involved the three wall and two wall defects which should be either located interproximally or involving the furcation area. The statistical analysis was done using Statistical Package for Social Sciences, the Wilcoxon signed rank statistic W + for Mann-Whitney U-test.
RESULTS: The net gain in PD and CAL after 6 months for Group I ([PerioCol] + [Grabio Glascera]) and Group II (Grabio Glascera) was 3.94 ± 1.81 mm, 3.57 ± 2.21 mm and 3.94 ± 1.81, 3.57 ± 2.21 mm, respectively. The results of the study for Group I and Group II with regards to mean net bonefill, was 3.25 ± 2.32 (58%) mm and 5.14 ± 3.84 (40.26 ± 19.14%) mm, crestal bone loss - 0.25 ± 0.68 mm and - 0.79 ± 1.19 mm. Defect resolution 3.50 ± 2.34 mm and 5.93 ± 4.01 mm, respectively.
CONCLUSION: On comparing both the groups together after 6 months of therapy, the results were equally effective for combination of graft and membrane versus bone graft alone since no statistical significant difference was seen between above parameters for both the groups. Thus, both the treatment modalities are comparable and equally effective.

INTRODUCTION

Periodontal disease involves a major part of global problems of oral diseases. Periodontitis is a disease characterized by inflammation of the gingiva that results in periodontal pocket formation with loss of the supporting periodontal ligament and alveolar bone around teeth. Various terminologies including scaling and root planing (SRP) or open flap debridement (OFD) are conventional methods used for treatment of periodontitis. But the use of specific biomaterials was more effective than OFD in improving attachment levels in periodontal defects.[1]

In the past three decades, periodontal regenerative treatment has received increasing attention as an alternative to tooth extraction in patients with periodontal disease. Implant insertion, although highly predictable, has been shown to be less predictable than saving a periodontally compromised tooth with regenerative therapy.[2]

With the advent of guided tissue regeneration (GTR), restoration of periodontium is being achieved more predictably. The technique using barrier was introduced by Nyman in 1982, and the term GTR was coined by Gottlow in 1986.[3] GTR is based upon the biological behavior of different periodontal tissues. During 1980s, researchers published information that led to the conclusion that the periodontal ligament was the most important source of periodontal progenitor regenerative cells.[4] Periodontal ligament stem cells are one of the best candidates for periodontal regeneration.[5] Current concept of GTR membrane, that is, resorbable and nonresorbable membranes act as a physical barrier to avoid connective and epithelial tissue down-growth into the defect, favoring the regeneration of periodontal tissues.[6] The bioabsorbable membranes are the second generation GTR membranes and were developed to avoid the second surgical procedure to remove the barrier.[7] These GTR devices fall into two broad categories, natural products (collagen membrane) and the synthetic (copolymer) materials. In an attempt to further induce attachment gain for intrabony defects, various bone graft materials have been employed in conjugation with membrane.[8] Regenerative therapy with bone replacement grafts did not gain acceptance as predictable therapy until the 1980. The various bonegrafts available are autografts, allografts, xenografts, and alloplasts. These materials act either as osteogenic and osteoinductive or osteoconductive.[9]

Among alloplastic graft materials, bioactive ceramics is a group of osteoconductive materials which include hydroxyapatite (HA), fluorapatite, bioactive glass, and tricalcium phosphate. Bioactive glass is a ceramic, and its principal component is SiO2. The Food and Drug Administration approved original composition of bioactive glass designated 45S5 was 45 mol% of SiO2, 26.9 mol% of CaO, 24.4 mol% of Na2O, and 2.5 mol% of P2O5. This material can bond to bone through development of a surface layer of carbonated HA in situ. The calcium phosphate is layer thought to promote adsorption and concentration of osteoblast derived protein necessary for mineralization of extracellular matrix.[10]

Objectives of periodontal bonegrafts are probing depth (PD) reduction, clinical attachment gain, bonefill of the osseous defect and regeneration of new bone, cementum, and periodontal ligament.

Aims and objectives

To evaluate regenerative potential of the combination of GTR (PerioCol, Eucare pharmaceuticals private limited, Chennai, India) and bonegraft (Grabio Glascera, Dorthom Medi Dents Pvt Ltd, Coimbathore, India); and bonegraft (Grabio Glascera) alone individually with respect to clinical parameter including clinical attachment level and radiographically the bonefill, change in alveolar crest (AC) bone and defect resolution

To compare the regenerative potential of the combination of GTR (PerioCol) and bonegraft (Grabio Glascera); and bonegraft (Grabio Glascera) alone between each other with respect to clinical parameter including clinical attachment level and radiographically the bonefill, change in AC bone and defect resolution.

MATERIALS AND METHODS

In the present study, a total of 30 sites of systemically healthy 19 patients (14 males and 5 females) who referred to the Department of Periodontology and Implantology of Sardar Patel Postgraduate Institute of Dental and Medical Sciences Lucknow with moderate to severe periodontitis having one or more periodontal osseous defects were treated during the period of 2009–2010. The other inclusion criteria were (i) PD of ≥ 5 mm (ii) clinical attachment loss (CAL) of ≥ 5 mm after phase one therapy of 4–6 weeks and (iii) ≥3 mm of radiographic periodontal osseous defect.[11] For study, three wall and two wall defects were considered. Each patient exhibited at least one site chosen randomly which should be either located interproximally or involving the furcation area:[12] (i) Medically compromised patient, (ii) lactating and pregnant women, (iii) smokers and (iv) teeth with hopeless prognosis were excluded from the study. The patient had completed basic periodontal therapy including scaling oral hygiene instruction and reinforcement, SRP with both hand and ultrasonic instrumentation at the time of enrollment before 4–6 weeks of surgeries. Endodontic treatment involving root canal treatment and crown rehabilitation was done in the required cases. Patient who agreed to participate signed an informed consent. Using randomized parallel method the defects were randomly assigned (flip of the coin) to the two treatment groups designated as Group I and Group II.

Group I (16 sites) was treated with bioresorbable GTR membranes (PerioCol™) – (sterile collagen periodontal membrane-fish origin 25 mm × 30 mm) and bone graft in combination (Grabio Glascera™) - containing 50% bioactive glass ([17% silicon [SiO2], 53% calcium [CaO], 30% phosphorous [P2O5]) and 50% synthetic hydroxyapatite (HA) with particle size of 0.15–0.50 mm). Group II - (14-sites) was treated with bonegraft alone (Grabio Glascera™).

Recordings

All preoperative clinical parameters were made on the day of surgery. Clinical measurements including both soft tissue and hard tissue measurements. Soft tissue measurements include plaque index, (Löe, 1967) sulcus bleeding index, (Muhlemman and Son, 1971),[913] PD and clinical attachment level which were performed with University of North Carolina Probe (UNC-15) and hard tissue measurements (bonefill, AC bone change and defect resolution) were recorded in radiographs which were studied preoperatively and at 6 months postoperatively by single examiner. The maximum PD and clinical attachment were measured at four aspects of the tooth, that is, buccal, lingual, mesial, and distal. The radiographic measurement includes[11] standardized reproducible intraoral periapical radiographs which were taken before surgery preoperatively (baseline) and 6 months postoperatively by the paralleling technique with Rinn Holder XCP System, dentsply [dentsply] Hamm Moor Lane/Addlestone/Weybridge/surrey KT15 2SE (X-ray machine - Sansin Dig 7° with Microprocessor Controlled Digital Timer and calibrated by National Physical Laboratory with settings of 70 KVP, 10 mA). Exposure time varied from 0.7 to 0.8 s depending upon the site. Radiographic measurements were made utilizing a millimeter X-ray grid, which consisted of vertical and horizontal squares, with small squares measuring 1 mm. Vertical linear distances between the cementoenamel junction (CEJ) and the most apical extension of the defect were obtained by counting the number of squares of 1 mm in a grid [Figure 1].[9]

Figure 1

(a) Measurement of preoperative, (b) Six months postoperative radiograph with 1 mm grid, also showing landmarks CEJ, AC, and BD

Correction factor for radiographs

Although the radiographic pairs were almost identical, still some amount of the vertical distortion between baseline radiographs and the 12-month radiograph was estimated. In order to get the exact values, the following measures were taken. In order to estimate this distortion, an anatomically nonvariable distance as the root length (distance from CEJ to root apex was measured on both the radiographs and a correction factor was calculated as follows:[11]

In case where it was not possible to measure the root length, the crown length was assessed (distance from incisal margin of the crown to the CEJ).

Following landmarks were identified on the radiographs

The following anatomical landmarks of the intrabony defect that is, CEJ, AC, and BD were identified on the radiographs [Figure 1a] based on the criteria set by Bjorn et al. (1969) and Schei et al. (1959). CEJ: The CEJ of the tooth with the intrabony defect. AC: The most coronal position of the alveolar bone crest of the intrabony defect when it touches the root surface of the adjacent tooth before treatment, thst is, the top of the crest. BD: The most apical extension of the intrabony destruction where the periodontal ligament space still retained its normal width before treatment, that is, the bottom of the defect. If the restoration was present, the apical margin of the restoration was used to replace the CEJ as a fixed reference point.[11]

The following linear measurements were performed with the help of grid mount:

CEJ-BD (CEJ to bottom of the defect)[1415]

CEJ-AC (CEJ to the most coronal extent of the interdental crest)[1415]

AC-BD (depth of intabony defect at baseline was obtained by subtracting above parameters [(CEJ-BD)−(CEJ-AC)]).[1415]

Radiographic measurements (radiographic bone changes)

Pre- and post-treatment radiograph pairs were analyzed in order to measure[11] [Figures 1a, b and 2a–c] the following.

Figure 2

(a) Preoperative radiograph, (b) Postoperative after 6 months with grid, (c) Postoperative after 6 months without grid

The radiographic bonefill

The radiographic bonefill after 6-month was calculated after applying the correction factor as follows:

(CEJ-BD [baseline]) − (CEJ-BD [6-month] × correction factor) = Bonefill

The radiographic alveolar bone crest change

(CEJ-AC [baseline]) − (CEJ-AC [6-month] × correction factor) = AC bone change

If the results were negative, this meant that a process of bone resorption had occurred.

The radiographic defect resolution

The radiographic defect resolution was evaluated subtracting radiographic alveolar bone crest change from radiographic bonefill.

Defect resolution = Bonefill − Alveolar bone crest change.

Surgical procedure

After a preoperative radiographic assessment, surgical therapy was planned. Prior to surgery, a presurgical rinse with chlorhexidine (0.2%) (Clohex Plus™, 0.2% w/v chlorhexidine gluconate, DR Reddys, Hyderabad) to maintain asepsis followed with local anesthesia 2% lignocaine containing adrenaline at a concentration of 1:80,000 was administered. Intracrevicular incision along with vertical releasing incisions was performed if necessary for a better access. Mucoperiosteal flaps were raised, granulation tissue was removed, roots were thoroughly scaled and planned, followed by conditioning with tetracycline. Group I received combination of GTR (PerioCol™) − (sterile collagen periodontal membrane-fish origin 25 30 mm × 30 mm soaked in normal saline about half an hour prior to its placement) and bone graft (Grabio Glascera™) - containing 50% bioactive glass (17% silicon [SiO2], 53% calcium [CaO], 30% phosphorous [P2 O5]) and 50% synthetic HA with particle size of 0.15–0.50 mm was used and mixed with normal saline 5 min prior to the placement[16] in the defect. Whereas Group II received bone graft alone. The defect was filled in both the groups with bone graft (bioactive ceramic composite granule with particle size of 0.15–0.50 mm). The graft material was moistened in sterile saline for 5 min before placement into the defects, care was taken not to overfill the defect. Following bone grafting, an aluminum foil template was trimmed and adapted over the entire defect so as to cover 2–3 mm of the surrounding alveolar bone, followed by a membrane of the same size and shape was trimmed and adapted over the entire defect so as to cover 2–3 mm of surrounding alveolar bone. Sutures (5–0 vicryl resorbable), if needed, were placed to secure the membrane and to ensure stability of the graft material. Finally, the mucoperiosteal flap was repositioned and sutured at the original level using 3–0 silk with an interrupted suture. Periodontal dressing was placed over the area. The same surgical technique was used for Group II except the placement of the membrane, only bone graft was used. The postsurgical medicinal treatment includes antibiotic (500 mg t.d.s. amoxicillin for 7 days) and analgesic (ibuprofen 400 mg t.d.s for 3 days). The postoperative care consisted of 0.2% chlorhexidine rinse twice daily for 4 weeks. For clinical and radiographic measurement purposes, the patient was recalled after 6 months [Figures 1a, b, and 2a–c].

DISCUSSION

Regeneration of lost structures has become the primary therapeutic goal in periodontics over the past several decades. In the present study, the material used was bioresorbable collagen membrane of fish origin. The purpose to use this was to avoid a second surgery. Before its placement, the patient was informed about its origin. A priority was given to synthetic graft that is, bioactive glass. Among the various comparative clinical trials involving the use of synthetic graft and various other types of graft, better results were shown in favor of synthetic bone graft.[17] Though autogenous bone is still the gold standard in bone augmentation procedures but due to its low availability and donor site morbidity necessitates the development of alternative products for it[18] and with allogenic graft there is a possibility of disease transfer, e.g., with freeze-dried bone allografts.[19] Clinically and statistically, a significant improvement was seen PD, CAL, bonefill, crestal bone loss, and defect resolution from baseline till an observation duration of 6 months individually in both the groups. However, no statistically significant difference was seen between both the groups.

The change in PD and CAL for both the groups shows a statistically significant difference between preoperative and postoperative values, that is, both the treatment modalities are effective [Tables 1 and 2] [Graphs 1 and 2] but on comparing the net gain between Group I and Group II, Group I, that is, combination therapy shows slightly higher values than Group II, yet there was no statistically significant difference (P = 0.790) between the two groups. The net gain in PD and CAL for combination and bonegraft were 3.94 ± 1.81 mm, 3.57 ± 2.21 mm and 3.94 ± 1.81 and 3.57 ± 2.21 mm, respectively [Table 3 and Graph 3]. A similar type of study done by Prathap et al.,[20] also shows slightly higher values in combination therapy than the bone graft alone and concluded that statistically no significant difference was found between both the treatment modalities.

Table 1

Comparison of pre- and post-operative periodontal health status in group I

Table 2

Comparison of pre- and post-operative periodontal health status in group II

Graph 1

Comparison of pre- and post-operative periodontal health status in Group I

Graph 2

Comparison of pre- and post-operative periodontal health status in Group II

Table 3

Comparison of net PD change, net CAL change, net bone fill, net alveolar bone crest change and net defect resolution in two study groups

Graph 3

Comparison of net probing depth change, net clinical attachment loss change, Net bone fill, net alveolar bone crest change, and net defect resolution in two study groups

The results of the study with respect to mean net bonefill for Group I and Group II in terms of percentage were 33.23 ± 15.58% and 40.26 ± 19.14% [Table 4 and Graph 4], respectively. Though the value was higher in Group II than in Group I statistically, there was no significant difference found between the two groups. In accordance, the present study, some other similar type of clinical trials also shows no statistically significant difference between combination and bone graft alone type of therapy.[1721] Tsao et al.,[17] showed the vertical bone fill of 1.9 ± 1.4 mm in mineralized cancellous bone allograft (MBA) and 0.7 ± 0.9 mm in combination, while Keles et al.[21] used autogenous cortical bone grafting (ACB) and Atrisorb as an absorbable polylactide membrane, and the values regarding the gain in radiographic alveolar bone height were 5.50 ± 2.24 mm in the ACB graft with GTR-treated group and 5.92 ± 1.83 mm in the ACB graft-treated group. Both the studies show slightly higher values for the bonegraft group with no statistically significant difference between the two treatment modalities as in the case of the present study. These studies were in agreement with our study which records no additional benefit of GTR membrane together with bone graft alone.

Table 4

Comparison of Proportional Change (in percentage) in Net PD Change, Net CAL Change, Net Bone Fill, Net Alveolar Bone Crest Change and Net Defect Resolution in two study groups

Graph 4

Comparison of proportional change (in percentage) in net probing depth change, net clinical attachment loss change, net bone fill, net alveolar bone crest change, and net defect resolution in two study groups

However, there are certain studies which favor the combination therapy with respect to bonefill.[22] Nygaard-Østby et al.,[22] used autogenous bone graft + GTR and autogenous bonegraft alone and recorded probing bone level gain as 3.9 ± 0.8 versus 1.3 ± 0.9 mm, P = 0.034, respectively. Contrary to the above study designs, there are few studies which use only bonegraft, though of different types, without the use of any membrane and showed significant improvement in defect fill.[192324] Meffert et al.[23] used hydroxylapatite as an alloplastic material for a period of 9 months and showed a defect fill of 66.89%. Yukna[19] used hard tissue replacement polymer for a period of 6-month and showed 60.8% defect fill respectively when compared with control groups. Grover et al.,[24] used bioactive glass and showed a mean radiographic defect fill of 64.76% (2.49 ± 0.5 mm) after 6-month observation. All the above studies used synthetic bone graft and showed the positive results thus again favoring the use of synthetic bone grafts as a regenerative material.

The net alveolar crestal bone change value was negative which showed that a crestal bone resorption had occurred in both the groups, [Tables 3 and 4] [Graphs 3 and 4] yet there was no statistically significant difference found between both the groups (P > 0.05). This was a significant finding as many of the synthetic bone graft reported bone fill still resulted in some amount of crestal bone loss. The net value was higher in Group II which showed that more crestal resorption occurred in Group II than in Group I, but there was no statistically significant difference present between both the groups (P > 0.05) Tsao et al.[17] showed the 1.3 ± 1.1 mm crestal bone resorption in MBA alone and 0.7 ± 0.9 mm in combination with GTR. The study of Luepke et al.[14] showed that when combination therapy was used, that is, bioabsorbable alone and its combination with decalcified freeze-dried bone allograft (DFDBA), the crestal bone resorption seen was − 0.10 ± 1.11 mm and − 0.27 ± 1.15 mm. The result of the study was almost comparable to combination group as seen in the present study. In terms of defect resolution, the mean net defect resolution in Group I and Group II [Table 3 and Graph 3] in terms of percentage 62.86 ± 26.49 and 80.58 ± 24.09, [Table 4 and Graph 4] respectively, the above observation shows that the net value is higher in Group II than in Group I yet there was no significant difference between both the groups. The defect resolution value was obtained after taking into consideration of the net crestal bone resorption and net bone fill. If the net crestal bone resorption would have not taken into consideration, then the values of defect resolution would have been different as compared to the actual value. Thus, this error was rectified initially and after rectifying it only the net mean defect resolution was calculated. Guillemin et al.[25] evaluated the combination of expanded polytetrafluoroethylene and DFDBA versus DFDBA alone but showed no statistically significant difference regarding defect resolution (81% vs. 64%) thus supporting to our study. Liñares et al.[11] used a combination of deproteinized bovine mineral and a collagen membrane in the treatment of intrabony defects and compared with papilla preservation flap alone and showed the radiographic resolution of approximately 60% which was almost comparable to the present study with respect to combination therapy. Meffert et al.,[23] showed the radiographic resolution of 53.57 ± 4.79% with hydroxylapatite as an alloplastic graft and 19.49 ± 4.52% with the control group, that is, without graft. Richardson et al.,[15] compared the graft, that is, Bio-Oss (Wolhusen) and DFDBA and showed the defect resolution of 77.6% for Bio-Oss and 59.4% for DFDBA.

In the present study, the results were evaluated up to the end of 6-month following surgeries. Had the time been permitted longer for the observation the results might have been better. The radiographic outcome after the two treatment modalities should be interpreted with caution as these grafts in the radiograph are hardly distinguishable from the host bone and the graft appearing on radiographs may not necessarily be incorporated in bone. This could introduce some bias in the radiographic examination process and overestimation of radiographic bone level in both the groups. Liñares et al.[11] The calculation of a correction factor assessing the level of distortion between preoperative and postoperative radiograph helped to minimize errors. The correction factor for both the groups was close to one which means that the projection of pre- and post-operative radiographs was similar in both the groups. The methods used for evaluating the results of this study were simple. All the clinical measurements were done using UNC-15 probe. Since in most of the studies the measurements such as bonefill, crestal resorption, and defect resolution were done with re-entry procedure which is traumatic to the patient and on other ethical issues. Therefore in our study, we use X-rays for the above evaluation.

CONCLUSION

Within the limitations of present study, it can be concluded that the combination of GTR + bone graft and bone graft alone resulted in a significant reduction in both the hard and soft tissue parameters when compared individually from baseline data to 6-month duration. On comparing both the groups together after 6 months of therapy, the results were equally effective with combination of graft + membrane versus bone graft alone since no significant difference was seen between any of the parameters between both the groups. Thus, both the treatment modalities are comparable and effective. Taking combination of membrane and bone graft into consideration, it can be concluded that using GTR membrane with bonegraft does not have any additional benefit as compared to bone graft alone.