Augmentation of osseous-implant dehiscence with
membrane alone or with a combination of bone graft and membrane

  Khalid A. Al Ruhaimi, BDS, MSc, Dr Med Dent
Dept. of Maxillofacial Surgery and Diagnostic Sciences, College of Dentistry, King Saud University, Riyadh, Saudi Arabia 

This investigation compared bone contour and the potential for new bone growth in osseous-implant defects grafted with demineralized xerographic bone particles (DXBP) and covered with guided tissue regeneration membrane (GTRM), with defects covered with GTRM alone. In the study, each of seven goats received four implants.  The implants were fixed in the buccal cortex of the left body of the mandible.  Four types of GTRM were used.  These were Capset®, Biomend®, P-BioBarrier®, and NP-BioBarrier®.  The grafting material used was Laddec®.  Twenty-four osseous-implant defects were used as the test group.  Twelve of these defects were grafted and covered with one of the GTRMs used, so that each GTRM covered 3 grafted defects.  The remaining 12 test defects were covered with one of the GTRMs alone; again, each membrane was used for 3 defects.  It was found that both resorbable and non-resorbable GTRMs augmented implant-osseous defects.  The range of bone contour in the ungrafted defects was between 550 and 1135 mmm.  Capset membrane produced the thickest bone in the ungrafted defects (1135 mmm).  Grafting osseous-implant defects increased the bone thickness.  The increase ranged from 512 to 950 mmm.  Of the membranes tested, NP-BioBarrier produced the thickest bone in the grafted defects (1800 mmm).  Control osseous-implant defects were not augmented with new bone.

Different grafting materials have been used to augment the bone in deficient implant sites.  These materials include filling materials that serve as a scaffold for new bone growth (osteocon-duction),1,2 growth factors that transform undifferentiated mesenchymal cells into osteoblasts (osteoinduction),2-4 autogenous bone grafts in the form of particles or blocks that have both osteoinduction and osteoconduction properties,5,6 and guided bone regeneration membrane (GTRM) based on the concept of using a barrier to separate bone from soft tissues and at the same time creating a space into which new bone can grow.7,8

Demineralized xerographic bone particles (DXBP) have been used to fill various bone defects successfully and in conjunction with implant-bone dehiscence.6, 9,18,22-24

Laddec is a resorbable natural hydroxyapatite (HA) material derived from trabecular bone matrix taken from the femoral condyles of 6-month-old calves.  It is a demineralized and deproteinized porous bone graft consisting of cancellous bone granules with a diameter of around 600 mmm. Since all raw mate-rials and organic components are removed during processing, this bone is essentially cancellous bone matrix made of purified mineralized type I collagen that retains the trabecular bone microstructure.13, 16

This study compared bone thickness and the potential for new bone growth in bone-implant defects grafted with DXBP (Laddec) and covered with GTRM to defects covered with GTRM alone.

Different grafting materials have been used to augment the bone in deficient implant sites.  These materials include filling materials that serve as a scaffold for new bone growth (osteocon-duction),1,2 growth factors that transform undifferentiated mesenchymal cells into osteoblasts (osteoinduction),2-4 autogenous bone grafts in the form of particles or blocks that have both osteoinduction and osteoconduction properties,5,6 and guided bone regeneration membrane (GTRM) based on the concept of using a barrier to separate bone from soft tissues and at the same time creating a space into which new bone can grow.7,8

Demineralized xerographic bone particles (DXBP) have been used to fill various bone defects successfully and in conjunction with implant-bone dehiscence.6, 9,18,22-24

Laddec is a resorbable natural hydroxyapatite (HA) material derived from trabecular bone matrix taken from the femoral condyles of 6-month-old calves.  It is a demineralized and deproteinized porous bone graft consisting of cancellous bone granules with a diameter of around 600 mmm. Since all raw mate-rials and organic components are removed during processing, this bone is essentially cancellous bone matrix made of purified mineralized type I collagen that retains the trabecular bone microstructure.13, 16

This study compared bone thickness and the potential for new bone growth in bone-implant defects grafted with DXBP (Laddec) and covered with GTRM to defects covered with GTRM alone.

 Clinical observations

All the animals remained healthy until the day of sacrifice. The osseous defects healed uneventfully without signs of inflammation and all the implants appeared very stable in their bony sockets. After a 4-month healing period, the Biomend had degraded and the Capset was resorbed completely. P-BioBarrier and NP-BioBarrier retained the proper positions (Fig. 3a).  Bone healing in the control osseous-implant defects failed to cover the exposed implant surfaces.  Only a few threads near the bottoms of the defects were covered with new bone ingrowth (Fig. 3b).

Histologic Analysis

 All the membrane-protected defects were augmented with new bone without evidence of connective tissue growing between the implant threads and the newly deposited bone (Fig. 4a).  Most of the Laddec granules had been resorbed and the space was occupied by active stroma or newly formed bone.  Resorption of the material was observed with active bone remodeling as demonstrated by the appearance of active osteogenesis between the partially resorbed Laddec particles.  None of the bone defects covered with GTRM showed signs of inflammation.  Bone-implant thread contact confirmed osseointegration of the newly formed bone to the surface of the implant (Figs. 4b & c).  The polarized light view of the same section showed a mixture of woven and lamellar bone capping the remnants of the Laddec granules.  In addition, new growing bone was in contact with the implant threads (Fig. 4d).

In the control defects, only a few implant threads were covered with new bone and the remaining threads were exposed.  The entire length of the lingual side of the implant waó covered with bony matrix extending from the host bone (Fig. 4e).

Radiographic Examination (Fig. 5, Table1)

 Radiographically, all the defects covered with GTRM alone or with graft showed bone in contact with the implant surfaces.  The bone thickness near the implant-bone defect border varied within the membrane alone and membrane plus grafting groups.  However, the bone was thicker in the grafted defects compared to the ungrafted one.  The thickness in the ungrafted defects ranged from 550 to 1135 mm, while the bone increase in the grafted defects was from 512 to 950 mm greater.  The greatest thickness in the non-grafted defects was seen in the Capset-covered defects (1135 mm), followed by NP-BioBarrier, P-BioBarrier, and Biomend, in order.  In the grafted defects, the greatest thickness was seen with NP-BioBarrier (1800 mm), followed by P-BioBarrier, Capset, and Biomend, in order.

In control defects, the entire lingual length of the implant was lined with bony matrix growing from the host bone, while on the buccal side, the implant surface was exposed and only a few threads at the bottom of the implant were covered with new bone.

Bone grafting is used in osseous-implant defects to maintain a space between the implant and the overlying GTRM, and to promote bone growth over the exposed implant threads.  This study showed that placing grafting material underneath GTRM helped to prevent the membranes from collapsing towards the exposed implant surface, and resulted in increased bone thickness.

DXBP (Laddec) has the same trabecular structure as natural bone and acts as a scaffold for physiologic remodeling.  Remodeling is activated by osteoclasts that resorb the material and the subsequent deposition of new bone by osteoblasts.1  In the manufacture of Laddec, all antigenic proteins and cellular elements contained in the intra-trabecular spaces are eliminated.  Animal and human histologic studies have proven its biocompatibility, safety, and potency as an osteoconductive bone substitute.13,16

In an animal investigation, Becker et al19,20 compared implant-bone defects filled with demineralized freeze-dried bone allograft (DFDBA) and covered with expanded polytetrafluoroethylene (ePTFE), defects filled with autogenous bone graft and covered with the same membrane, and defects covered with ePTFE membrane alone.  They found regeneration was least favorable when DFDBA was covered with e-PTFE, and concluded that DFDBA did not increase bone thickness on exposed implant surfaces.  They observed no osteoblastic or osteoclastic activity in the grafted field.  The purity of the demineralized bone grafting material with respect to fatty debris or residual protein is very important in determining a successful outcome.21  Their laboratory produced the DFDBA material used in their experiments, and this might be why the material that Becker et al. used failed to induce physiologic bone remodeling.  However, it is difficult to conclude that all DFDBA materials on the market would have the same results.

Our findings disagree with those of Becker et al.  In the grafted site, evidence of new bone growth and active osteogenesis between the Laddec particles undergoing resorption and the exposed implant surface were observed.  Lorenzoni et al12 found that the application of ePTFE membrane in combination with bovine DXBP (Bio-Oss®) appeared to enhance new bone formation on exposed implant threads, in agreement with our results. Landsberg et al22 also evaluated augmentation procedures on implants using human DFDBA in clinical cases. Their implants were covered with ePTFE membrane for 6 months.  Bone biopsies of the augmented bone examined histologically revealed osteogenic activity and the presence of osteoblastic and osteoclastic reactions in between the DFDBA particles.  Resorption of DXBP material and continuous deposition of new bone have also been documented in earlier studies.1, 2, 13, 16-18

This author32 compared the osteogenic potential of six osteoconductive materials derived from human, animal, and synthetic sources.  The study examined osseous cavities in the tibial condyles of rabbits and concluded that DXBP (Laddec) possessed the optimal criteria for an osteoconductive grafting material.

The present study observed an increase in bone thickness when DXBP material was applied in combination with GTRM.  Obviously, the use of grafting materials prevented collapse of the GTRM against the exposed implant surfaces.  The thickest bone in the grafted defects was seen with NP-BioBarrier (Table 1).

Shanaman24 reported a clinical evaluation of 237 implant sites treated with GTRM alone or in combination with DFDBA.  He noticed enhanced bone ingrowth when DFDBA was used.  However, the study did not observe a statistically significant difference in bone thickness between implants that were grafted with allografts and those that were not grafted.  Gher et al15 conducted a clinical study to analyze the efficacy of bone allograft and Gore Tex® membranes in osseous-implant dehiscence. They noticed that the use of membrane in combination with allograft resulted in complete bone fill compared to defects that had not been grafted.

Hammerle et al9 evaluated the application of ePTFE membrane to osseous-implant defects alone and in conjunction with DXBP (Bio-Oss®).  They observed 90 and 100% bone fill in the defects, respectively.  Furthermore, the direct bone-to-implant contact fractions were 55 and 65%, respectively.

Hockers et al6 evaluated the effect of the combined use of resorbable collagen membrane (BioGuide®) with bovine DXBP (Bio-Oss®) and autogenous bone particles in the treatment of bone defects around implants in dogs.  They concluded that collagen membrane enhanced bone regeneration.  DXBP and autogenous grafts were equally well integrated into the regenerated bone and autogenous bone and DXBP had no additional effect on bone growth. The comprehensive review of literature by Tolman5 concluded that autogenous bone is optimal for grafting bone-implant defects.  Block and onlay autogenous bone grafts were the optimal materials for augmenting a resorbed ridge in conjunction with implants.

The different GTRMs used in our experiment all promoted bone regeneration around the exposed implant surfaces.  Calcium sulfate (Capset) barrier resulted in the thickest bone contour in ungrafted defects (1135 mmm) (Table 1).  This author33 found in another animal investigation that adding calcium sulfate to various grafting materials used to fill osseous defects resulted in increased bone deposition and increased mineralization.  The increase of bone contour may be due to the direct calcium supply to the newly regenerated bone and avoidance of the collapse of the material to the underlying exposed implant surface that can happen with other membranes.

One major problem that has been reported as associated with the use of non-resorbable GTRM is a high rate of complications if the membrane is exposed to the oral environment and a subsequent infection develops.  This is in addition to the disadvantage of needing a second procedure to remove the membrane.25-29  On the other hand, the use of bioabsorbable GTRM could result in the use of limited gingival flap reflection in a one-step procedure and, consequently, better adaptation of the gingival tissues to the titanium abutments.30

Soft tissue pressure can lead to collapse of the GTRM and consequent reduced bone regeneration.  A Gore-Tex® GTRM with a titanium net (TR-GTAM® was introduced to help prevent collapse of the membrane towards the exposed implant surface.  The reinforcement in this membrane stabilizes the position of the membrane after adaptation, and provides more space for bone ingrowth for the duration of the healing period.  Jovanovic and Spiekermann31 reported increased bone formation with TR-GTAM compared to standard Gore-Tex membrane.  Lorenzoni et al12 also reported relatively increased bone gain with TR-GTAM membrane compared to standard ePTFE.  However, the need for a second time surgery to remove it, and the possible complications that can appear with the use of non-resorbable membranes if they are exposed to the oral cavity, remain major disadvantages for the use of this kind of membrane.

This study concluded that resorbable and non-resorbable GTRM successfully augmented implant-osseous defects.  Laddec (DXBP) increased bone thickness in defects covered with GTRMs and  was well integrated into the regenerated bone.  A calcium sulfate (Capset) barrier resulted in the thickest bone among the ungrafted osseous-implant defects, while NP-BioBarrier had the best result for the grafted defects.

This research was awarded a grant by King Abdul Aziz City for Science and Technology  with Research # LG 28. The author would like to thank Prof. H.A. Mosadomi during the histologic preparation, Mrs. Sawsan Elmot for the preparation of the histologic slides and Mr. Michael S. Giwa in the Animal House.

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Address reprint requests to:

Dr. Khalid A. Al Ruhaimi

PO Box 60169,  Riyadh 11545

Saudi Arabia

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