Journal of Indian Society of Periodontology

: 2013  |  Volume : 17  |  Issue : 2  |  Page : 228--234

Clinical evaluation of porous hydroxyapatite bone graft (Periobone G) with and without collagen membrane (Periocol) in the treatment of bilateral grade II furcation defects in mandibular first permanent molars

Sruthy Prathap, Shashikanth Hegde, Rajesh Kashyap, MS Prathap, MS Arunkumar 
 Department of Periodontics, Yenepoya Dental College, Mangalore, Karnataka, India

Correspondence Address:
Sruthy Prathap
Department of Periodontics, Yenepoya Dental College, Karnataka - 575 018


Background: Furcation invasions represent one of the most demanding therapeutic challenges in periodontics. This investigation assessed and compared the clinical efficacy of hydroxyapatite bone graft material when used alone and with collagen membrane in the treatment of grade II furcation defects. Materials and Methods: Ten patients with comparable bilateral furcation defects in relation to mandibular first molars were selected and treated in a split-mouth design. After the hygiene phase of therapy was completed, the groups were selected randomly either for treatment with hydroxyapatite bone graft (Periobone G) alone or with a combination of bone graft and guided tissue regeneration (GTR) membrane (Periocol). Clinical parameters like plaque index, gingival index, vertical probing depth, horizontal probing depth, clinical attachment level, position of marginal gingiva, and the amount of bone fill were used at baseline and at 3 and 6 months postoperatively. Results: At 6 months, both surgical procedures resulted in statistically significant reduction in vertical and horizontal probing depths and gain in the clinical attachment level. Conclusion: The use of combination technique yielded superior results compared to sites treated with bone graft alone. However, the difference was not statistically significant.

How to cite this article:
Prathap S, Hegde S, Kashyap R, Prathap M S, Arunkumar M S. Clinical evaluation of porous hydroxyapatite bone graft (Periobone G) with and without collagen membrane (Periocol) in the treatment of bilateral grade II furcation defects in mandibular first permanent molars.J Indian Soc Periodontol 2013;17:228-234

How to cite this URL:
Prathap S, Hegde S, Kashyap R, Prathap M S, Arunkumar M S. Clinical evaluation of porous hydroxyapatite bone graft (Periobone G) with and without collagen membrane (Periocol) in the treatment of bilateral grade II furcation defects in mandibular first permanent molars. J Indian Soc Periodontol [serial online] 2013 [cited 2020 Feb 17 ];17:228-234
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Periodontitis results in inflammation within the supporting tissues of the teeth, progressive attachment, and bone loss, and is characterized by pocket formation and/or recession. [1] The reason for early and frequent loss of molar tooth is furcation involvement which increases as periodontitis progresses. Furcation involvement results from loss of periodontal fiber attachment and bone between the roots of multirooted teeth. [2] A proper diagnosis of furcation lesion and tooth morphology is very critical. [3]

Glickman (1953) graded furcation involvement into the following four classes:

Grade I: It is the incipient or early stage of furcation involvement. The pocket is suprabony and primarily affects the soft tissues. Early bone loss may have occurred with an increase in probing depth, but radiographic changes are not usually found

Grade II: It can affect one or more of the furcations of the same tooth. The furcation lesion is essentially a cul-de-sac with a definite horizontal component. If multiple defects are present, they do not communicate with each other, since a portion of alveolar bone remains attached to the tooth. Radiographs may or may not depict the furcation involvement

Grade III: The bone is not attached to the dome of the furcation. In early grade III involvement, the opening may be filled with soft tissue and may not be visible. Properly exposed and angled radiographs of early class III furcations display the defect as a radiolucent area in the crotch of the tooth

Grade IV: The interdental bone is destroyed and the soft tissues have receded apically so that the furcation opening is clinically visible. [4]

Periodontal therapy for treating involved furcations include scaling, rootplaning, conventional flap surgery, root resective procedures, and guided tissue regeneration (GTR). Research conducted on type I collagen has proven its effectiveness for use as a barrier membrane. [5],[6],[7] Periocol is a fibrillar sterile collagen GTR membrane of fish origin, manufactured by Eucare Pharmaceuticals (Chennai, India) and has been used in this study.

In 1989, world workshop on clinical periodontics suggested that the addition of bone graft in combination with barrier membrane improves the defect fill, probing depth reduction, and clinical attachment gain, as compared to a barrier alone in human class II and III furcation involvement. [8] Hydroxyapatite bone graft is a commonly used alloplastic material. Periobone G is a ceramic surgical implant used to treat periodontal defects.

The present study was designed to test whether the use of resorbable collagen membrane would enhance the clinical results obtained with porous hydroxapatite (HA) bone grafts in the treatment of class II furcation defects in first mandibular molars.

 Materials and Methods

The patients who participated in this study were selected randomly from the out-patients reporting to the Department of Periodontics, Yenepoya Dental College, Mangalore, India. Informed consent was taken from all the patients who participated in the study. Prior clearance was obtained from the institutional ethical committee.

Selection criteria

Patients of age group 25-60 years, with bilateral grade II furcation involvement in relation to mandibular first molars, who fulfilled the inclusion criteria were included in the study.

Inclusion criteria

Vertical probing depth (VPD) ≥4 mmHorizontal probing depth ≥4 mmGingival margin (GM) coronal to or at the level of the roof of the furcation.

Exclusion criteria

No history of any systemic diseasesNo history of smokingNo history of administration of antibioticsNo history of any periodontal therapy in the last 6 monthsNo known allergic responses to collagen products and hydroxyapatite material.

Study design

The sample size was determined according to the power of the study (80%) and as per the recommendations of the statistician (minimum of nine patients were required). In this study, 10 patients were selected and treated on a split-mouth study design. Bilateral furcation defects in relation to mandibular first molars were randomly divided into control and test groups. A total of 20 sites were treated.

Group I (control group) - Consisted of 10 sites where the HA bone graft material (Periobone G) was placed.

Group II (test group) - Consisted of 10 sites where HA bone graft (Periobone G) material was placed in conjunction with the collagen membrane (Periocol).

Periobone G is a ceramic surgical implant used to treat periodontal defects, extraction sites, and ridge augmentation, available in 2 × 0.5 g vials and granule size of 0.5-1 mm. It has been manufactured by Topnotch health care products, pvt Ltd, Palakkad, Kerala, India with a technical knowhow from Sree Chitra Tirunal Institute of Medical Sciences and Technology, Thiruvananthapuram, India.

Periocol is a fibrillar sterile collagen GTR membrane of fish origin, available in 25 × 30 mm size, manufactured by Eucare Pharmaceuticals. It is an orange-brown type I collagen membrane and is gamma sterilized and supplied in individual blister packing. Since collagen is derived from fish sources (skeleton, fins, skin, and air bladder), there is no threat of bovine spongiform encephalopathy (BSE)/transmissible spongiform encephalopathy (TSE). It is non-toxic, non-allergenic, non-immunogenic, and biocompatible. The material can be stored in a dry place at or below 25°C with a shelf life of 3 years.

The following clinical parameters were recorded at baseline and at 3 and 6 months postoperatively.

Plaque indexThe index was described by Silness P. and Loe H. in 1967. The scoring was done on selected teeth (selected mouth basis).

Gingival index Gingival index developed by Loe H. and Silness J. (1963) was used.

Vertical probing depthA customized acrylic stent with an occlusoapical groove was prepared to standardize the insertion of the probe. The stent was stored on the cast [Figure 1].{Figure 1}

The base of the stent served as the reference point (RP) to record the measurements. VPD was calculated by measuring the distance from a fixed RP on the stent to the base of the pocket (BOP) along the groove using the Williams periodontal probe which is calibrated in millimeters, and subtracting it by the distance from the fixed RP to the GM [Figure 2].{Figure 2}

VPD = (RP - BOP) − (RP - GM)

Horizontal probing depthHorizontal component of the furcation involvement was measured using an orthodontic wire which was incorporated into the stent which extended from the distal interproximal area of the involved tooth directed towards the furcation entrance. Horizontal probing depth was measured using a customized Nabers probe calibrated in millimeters. The pointed end of the orthodontic wire served as the reference point [Figure 3].{Figure 3}

Clinical attachment levelClinical attachment level (CAL) was calculated by measuring the distance from the RP to the BOP and subtracting it by the distance from the RP to the cementoenamel junction (CEJ).

CAL = (RP - BOP) − (RP - CEJ)

Position of GMPosition of GM was calculated by measuring the distance from a fixed RP to CEJ and subtracting it by the distance from the RP to the GM.

Position of GM = (RP - CEJ) − (RP - GM)

Amount of bone fillIn addition to the clinical measurements, Radiovisiography technique was used as an additional method to observe the possible changes in the furcation region at baseline and 6 months postoperatively. Long cone technique, holding devices, and an aiming ring were used to standardize the technique [Figure 4].{Figure 4}

A software called SOPRO imaging was used for measurements using grids. The measurements were recorded from the furcation fornix by calculating the radiolucency in the furcation area in millimeters. [2]


Surgical protocol

After anesthetizing the surgical area, a full-thickness mucoperiosteal flap was reflected. The defect was debrided and roots planed. The planed root surfaces were then conditioned with topical application of tetracycline hydrochloride. Root biomodification eliminates the degenerated Sharpey's fibers, bacteria, bacterial products, disintegrated cementum, and dentin from the root surfaces, which can interfere with the new attachment. Bone graft (Periobone G) was placed on the control sites. The graft material was mixed with saline using a spatula in a sterile dappen dish and was compacted into the bone defect, compressing against the surrounding bone layer by layer till the furcation defect was filled. The test sites were treated with a combination of collagen membrane (Periocol) and bone grafts. The membrane was cut into appropriate size and shape with the help of a template using sterile surgical scissors and soaked in distilled water before placement, to improve adhesion properties and malleability. If adequate retention was not available, resorbable sutures were used to stabilize the GTR membranes. The flaps were sutured and periodontal dressing (Vocopak) was placed over it. Antibiotics and analgesics were prescribed. The patient was given postoperative instructions. The dressing and the sutures were removed after 10 days.

Surgical procedure - control group: [Figure 5] shows the furcation defect and [Figure 6] shows bone graft placement.{Figure 5}{Figure 6}

Surgical procedure - test group: [Figure 7] shows the bone graft placement and [Figure 8] shows GTR membrane placement.{Figure 7}{Figure 8}


The evaluation of clinical parameters of both the groups was done by comparing the plaque index, gingival index, mean VPD, mean horizontal probing depth, gingival marginal position changes, and CALs at baseline and at 3 months and 6 months.

Statistical analysis

The statistical constants like arithmetic mean, standard deviation, and P value were computed using SPSS 10.0 version software program. The paired t-test was used for testing the statistical significance of changes in parameters within the groups and also between the test and control groups.

Plaque index and gingival index

In this study, a reduction in plaque index score was observed in both test and control groups at 3 and 6 months postoperatively. This downward shift was maintained throughout the study period. The comparisons between the groups did not show any statistically significant difference.

Vertical probing depth

The results are shown in [Table 1] and [Table 2].{Table 1}{Table 2}

Horizontal probing depth

The results are shown in [Table 3] and [Table 4].{Table 3}{Table 4}

Clinical attachment level

The results are shown in [Table 5] and [Table 6].{Table 5}{Table 6}

Gingival margin position

Gingival recession recorded in the test group was 0.8 ± 1.033 mm at 3 months and 0.7 ± 0.948 mm at 6 months. In the control group, it was 0.6 ± 1.174 mm at 3 months and 0.7 ± 1.16 mm at 6 months. Between the groups, the difference was not statistically significant.

Bone fill

Among the 10 test sites, 6 sites showed radiolucency at baseline and 5 sites incidentally showed detectable bone fill after 6 months, whereas in the control sites, out of the 5 sites which showed radiolucency at baseline, only 4 sites showed a detectable bone fill after 6 months postreatment and so could not be subjected to statistical analysis.

Control group

[Figure 9] shows the RVG image at baseline and [Figure 10] shows the RVG image at 6 months.{Figure 9}{Figure 10}

Test group

[Figure 11] shows the RVG image atbaseline and [Figure 12] shows theRVG image at 6 months.{Figure 11}{Figure 12}


There is conclusive evidence that patient factors like plaque control and/or compliance, [9] systemic conditions like diabetes mellitus, [10] age, [11] smoking, [12] tooth and defect factors like endodontic status, [13] mobility, [14] and defect characteristics [15] can affect the outcome following the regenerative surgery.

In a study by Eto et al., use of anorganic bovine-derived hydroxyapatite matrix/cell binding peptide (P15) in grade II furcation yielded favorable results in grade II furcation involvement, but there was no difference compared to open flap debridement. [16] Khanna et al. compared open flap debridement with the use of collagen membrane and bone graft, and concluded that the use of bone graft in combination with membrane showed better improvement in the clinical parameters. [17] Surgical considerations like wound stability, [1] space maintenance, [18] and postoperative conditions [1] are particularly important aspects of GTR surgeries. Second-generation bioabsorbable membranes eliminate the need for second surgery for barrier removal, reduce the risk of loss of regenerated attachment, increase patient acceptance, integrate well with host tissues, enhance tissue coverage, reduce barrier exposure, and resist or prevent microbial colonization. [19] However, there is very little use of GTR membranes in the treatment of such advanced grade disease. It should only be attempted with lesions that are under control, isolated, and when the patients can easily maintain hygiene. [20]

The rationale for using collagen in this study is based on the following observations: First, collagen has hemostatic properties. Wikesjo et al.[5] and Haney et al.[6] have indicated that in order for regeneration to occur, the developing clot must form and adhere to the root surface, thereby facilitating proper wound maturation. Second, a collagen membrane once infiltrated by vascular channels may serve as a lattice for migrating periodontal ligament fibroblasts. [7] Third, collagen has been found to be chemotactic for fibroblasts in vitro, a property that may enhance cell migration. [21] Additionally collagen can be formed into many shapes and can easily be manipulated and adapted to the root surface. It is a weak immunogen which is bioabsorbable, eliminating the need for re-entry surgery to remove it.

Porous HA has been shown to be osteoconductive when placed in the long bones and mandibles of dogs. [22] Several bone substitutes have been used in clinical periodontal therapy, but histologically new attachment has not been achieved.

The results of the study indicated that the use HA bone graft alone and the combination of GTR + HA had significant effect on the clinical parameters when comparing values of baseline to 3 and 6 months post-treatment values.

Vertical probing depth

The mean reduction in the VPDs was noted to be highly significant in both the groups at 3 and 6 months postoperatively, compared to the baseline values. Comparison between the groups showed a higher probing depth reduction in test group (2.9 ± 0.878) compared to control group (2.5 ± 0.972), but the difference was not statistically significant. These findings are in accordance with the results of the studies by Lekovic et al., [23],[24] but the study conducted by Tsao et al., [25] which compared mineralized human cancellous bone allograft with and without collagen membrane, showed a higher vertical bone fill in the group treated with graft alone compared with the group treated using the combination. The positive changes in VPD could be partly due to gingival recession or an improvement in CAL.

Horizontal probing depth

A highly significant reduction in the horizontal probing depth was noticed both in the test group (0.8 ± 0.422) and control group at 6 months (0.5 ± 0.527). Though the test group showed better results, the difference was not statistically significant, which was similar to the findings of Tsao et al.,[2] who reported reduction to be 1.1 ± 0.9 and 1.1 ± 0.9 mm in the test and control groups, respectively.

Gingival margin position

An apical shift in the gingival margin was observed in both groups at 3 and 6 months, similar to the study results of Tsao et al., [2] Wang et al.,[26] and Lekovic et al. [27]

Clinical attachment level

The gain in clinical attachment was recorded both in the test group (1.7 mm) and the control group (1.4 mm) postoperatively. Between the groups, there was no significant difference either at 3 months or at 6 months postoperatively. The results are in agreement with the study results of Wang et al., [26] in which the test sites showed a CAL gain of 1.67 ± 0.22 mm and the control sites showed a CAL gain of 0.67 ± 0.62 mm. The study by Lekovic et al.[24] suggested an improved CAL in sites treated using the combination technique.

Percentage of bone fill using RVG

In some of the images, it was not possible to detect any radiographic changes. This shortcoming could have arisen due to the two-dimensional representation of a three-dimensional structure and as grade II furcations need not necessarily show radiographic change. [4] Some of the test and control sites showed bone fill at 6 months, which could be compatible with new bone growth, but it is difficult to ascertain if regeneration or new bone growth has occurred, since this would require surgical re-entry or histological evaluation. Due to the inherent limitations in assessing bone fill using these techniques, bone fill was considered only as an additional parameter. Studies have shown that radiographs, even those taken with standardized methods, are less reliable than clinical probing techniques. [28],[29]


The present study results indicate that at 6 months after surgery, both therapies resulted in significant horizontal and vertical probing depth reduction and gain in clinical attachment level. The use of combination technique yielded superior results compared to sites treated with bone graft alone. However, the difference was not statistically significant. Further studies should include longer follow-up time and surgical re-entry to determine the long-term effects of the treatment.


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