Introduction

Bone augmentation products are readily available for veterinary dental use. Many different products are available, however, differ greatly in composition, cost, and vary in their mechanism of bone regeneration properties. The goal for use of these products is to assist with the repair or regeneration of the periodontal attachment (alveolar bone, periodontal ligament, and cementum), resulting in the reduction of periodontal pocketing and the maintenance of alveolar bone height.¹ Common applications for these products include placement in certain extraction sites to maintain alveolar bone, surgical periodontal therapy as described in this report, use in fracture repair, certain palatal defects, and use with implants to maintain alveolar bone.^2,3 All of the products discussed in this report have shown clinical success when used correctly. With any oral treatment, it is critical to have owner consent, awareness, and commitment.³ Daily home care and follow-up monitoring and treatments are vital to the short and long-term healing and well-being of the patient.⁴ Throughout this document, the modified Triadan system was used to identify teeth (available at: www.avdc.org).

Case Report

Case 1

A 7 yr old, 10.4 kg, female spayed cocker spaniel was presented for complete oral examination and prophylaxis with general anesthesia. No previous dental procedures had been performed. No oral home care had been administered; however, the owner did indicate a desire to limit extractions if possible and commit to daily oral home care. General physical examination excluding the oral cavity was within normal limits. Presurgical blood chemistries and complete blood count were within normal reference range. Oral examination prior to anesthesia revealed moderate generalized calculus worse on the maxillary posterior teeth, mobility to three maxillary incisors (101, 102, 201) and one mandibular incisor (302), and a visible foreign body in the buccal sulcus of the left mandibular first molar (309) (Figure 1A).

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Premedication was achieved using butorphanol tartrate^a 0.29 mg/kg subcutaneously. After 20 min, a 22 gauge catheter^b was aseptically placed in the right cephalic vein followed by induction using 4.4 mg/kg propofol^c intravenously. The patient was intubated with a size 8 mm cuffed endotracheal tube^d and maintained with isoflourane^e gas (1.5–2%) and oxygen (1 L/min) for the procedure. Intravenous lactated ringers solution^f at 10 mL/kg/hr was administered during the procedure. The patient was wrapped with an electric warming blanket unit^g and monitored continuously during anesthesia for the parameters of temperature, pulse oximetry, O2 saturation, end tidal CO2, and electrocardiogram. Noninvasive blood pressure was recorded every 5 min. The patient's oral cavity was irrigated with 0.12% chlorhexidine gluconate solution^h. A combination of piezoelectric and hand scaling was preformed to remove all supra and subgingival plaque and calculus. Polishing of all scaled surfaces was completed using a slow speed hand piece with a disposable prophy angle cupⁱ and medium grit fluoride paste^j. Periodontal probing depths were measured for every tooth and radiographs taken using a number two size digital sensor^k. A diagnosis of periodontal disease index (PDI) stage 4 was made for teeth 101, 102, 201, 209, 302, and 310. Intra-operative pre-emptive analgesia at this time included buprenorphine^l 0.01 mg/kg intravenously and a bupivacaine^m 0.15 mg/kg left mandibular local nerve block. The mobile teeth were appropriately extracted. Simple interrupted 4-0 poliglecaprone 25 sutureⁿ was used for closure with the exception of the left mandibular second molar (310). Periodontal probing depths of 4mm on the buccal aspect of the distal root of the left mandibular fourth premolar (308) with radiographic bone loss of 45–50% was treated with closed root planing and doxycycline hyclate gel^o therapy. A larger defect with three walls and a depth of 8mm on the distal root of the left mandibular first molar (309) required open root planing to allow adequate visualization for cleaning and debridement (Figure 1B, C). A full thickness gingival flap was created by making a vertical releasing incision on the distal line angle of 309. Both open and closed root planing were accomplished with a combination of thin-line-tip^p piezoelectric scaling and hand curettes. Once debridement was complete and the defect flushed, rinsed, and lightly blown dry, an allograft^q material was used to fill the defect. Once filled, the vertical releasing incision as well as the extraction site for 310 was closed as previously described. After closure of the gingiva, doxycycline hyclate gel was placed in the sulcus of the distal root repair site to create a barrier covering the allograft material. Postextraction and posttreatment radiographs were completed (Figure 1D). The patient recovered from anesthesia uneventfully and was sent home later that day with medication instructions, including clindamycin 75mg^r per per os (PO) q 12 hr for 2 wk and both tramadol hydrochloride^s 25mg PO q 12 hr and carprofen^t 25mg PO q 12 hr for 5 days. Food was to be softened for the next 7 days and removal of all chew toys until the first oral recheck recommended in 2 wk. Daily oral home care would commence after this recheck. Follow-up examination with radiographs was recommended for 6 mo and then annually.

Follow-up radiographs and periodontal probing measurements for tooth 309 were taken 6 mo posttreatment (Figure 1E, F). The owner had been diligent with daily dental chew treats, however, not with daily brushing. Probing depths for the allograft treatment region were 2mm and considered within normal limits. Radiographs illustrated a homogenous density consistent with alveolar bone to the previous defect site with normal crestal bone margins. A uniformly thin radiolucent space was present between the treated root and adjacent alveolar bone consistent with normal periodontal ligament space. Alveolar bone height appeared normal over the region of the extracted 310. The owner was instructed to be as diligent as possible with daily oral home care and to have annual oral examination and prophylaxis with radiographs.

Case 2

A 5 yr old, 6.9 kg, male neutered bichon frise presented for complete oral examination and prophylaxis with general anesthesia. This patient had a dental prophylaxis 2.5 yr prior that included six extractions due to periodontal disease. No oral home care had been administered; however, the owner did indicate a desire to limit extractions if possible and commit to daily oral home care. General physical examination excluding the oral cavity was within normal limits. Presurgical blood chemistries and complete blood count were within normal reference range. Oral examination prior to anesthesia was limited to moderate generalized plaque and calculus with six missing teeth. Mobility was noted to three of the remaining five maxillary incisors as well as the three right side mandibular incisors.

Premedication, general anesthesia, and patient monitoring were initiated using the same protocol as previously described. Complete oral examination, scaling, polishing, probing, charting, and radiographs were also completed as previously described. All noted mobile incisors as well as mobile left maxillary first molar were diagnosed as PDI stage 4 and consequently extracted, flushed, and closed with simple interrupted 4-0 poliglecaprone 25. The left mandibular first molar (309) had 6 mm periodontal probing depths on the distal-lingual aspect of the distal root. The right mandibular first molar (409) had 9mm probing depths on the distal buccal aspect of the distal root. Radiographs of both 309 and 409 (Figure 2A, E) indicated mild mesial crestal bone loss and severe widening of the periodontal ligament space of the distal root with greater than 50% bone loss. Tooth 409 radiographs show the vertical bone loss near the distal root apex as well as furcational bone loss. Compromise of apical root attachment may alter treatment prognosis dramatically. Radiographs are limited to two-dimensional viewing and should be combined with periodontal probing depths and visual inspection for complete analysis. Tooth 409 was treated with open root planing as described in case 1 for complete visualization, analysis, and debridement. Open visualization confirmed the ventral most aspect of the defect was located closer to the buccal plate and did not involve the distal root apex. Tooth 309 was cleaned and debrided utilizing closed root planing technique. After thorough cleaning and rinsing, both defects were filled with an alloplast^u material. The incision to the buccal gingiva of tooth 409 allowing open treatment was closed with 4-0 simple interrupted poliglecaprone 25. Both 309 and 409 then had doxycycline hyclate gel placed in the sulcus of the distal root repair site to create a barrier covering the alloplast material. Posttreatment radiographs were taken (Figure 2B, 2F). The patient was discharged later the same day with the same postprocedure protocol as described for case 1. Medications included clindamycin 25mg^r PO q 12 hr for 2 wk and both tramadol hydrochloride^s 25mg PO q 12 hr and carprofen^t 12.5mg PO q 12 hr for 5 days.

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Follow-up radiographs and periodontal probing measurements for 309 and 409 were taken 6 mo posttreatment (Figure 2C, G). The owner had been diligent with daily dental chew treats and the use of a prescription dental diet. Periodontal probing depths were less than 1mm and considered within normal limits. Radiographs indicated an improvement in the mesial aspect crestal bone height for both teeth as well as a homogenous density filling the previous defect, consistent with alveolar bone repair and remodeling. Periodontal ligament space is visible and may be considered slightly widened at this 6 mo postprocedure. Due to the width of the periodontal ligament space, a follow-up was recommended again in 6 mo.

Discussion

Periodontal disease is an extremely common problem in small animal veterinary patients.¹ Periodontal disease is defined as pathology in any part of the surrounding tissues that hold the tooth in place (alveolar bone, cementum, periodontal ligament, and gingiva).¹ It has been reported that by 2 yr of age, 80% of dogs have some form of periodontal disease present.⁵ The most common patterns of alveolar bone loss with periodontal disease are horizontal bone loss and vertical bone loss.¹ Horizontal bone loss is the most common in veterinary patients and is seen when the crestal bone defect is at the same level across the arcade.⁶ Vertical bone loss is classified when the bone defect surrounding the tooth is apical to the surrounding crestal bone level.⁶ Vertical or angular bone loss is further classified by the number of walls to the defect. Two-walled defects have a good prognosis for cure with periodontal therapy. Three and four-walled lesions have an excellent prognosis for cure with regenerative osseous treatment when performed correctly.¹ In veterinary patients, the most common locations for vertical defects are the palatine surface of the maxillary canines and the distal root of the mandibular first molars.⁷

The first consideration in any treatment planning should be a commitment by the owner to perform the necessary home care and recommended follow-up monitoring and treatments. In both of these cases with PDI stage 4, the prognosis must be considered guarded. Initial 6 mo follow-up is essential, as any failure may result in pain and discomfort to the patient. Although osseous surgery may have a successful outcome initially, if the owner is not committed to long-term oral care and routine prophylaxis, then other options such as extraction may be considered in the best interest of the patient.

Oral radiography is extremely important in the identification of the severity of periodontal disease, even though it is limited to creating a two-dimensional image.⁷ Therefore, complete evaluation of any defect should also include periodontal probing for more precise dimensions and direct visualization by the surgeon to establish the scope of the three-dimensional lesion. Direct visualization of the lesion may require some type of gingival flap to be created. This will aid considerably in the ability to clean and debride not only the root surface but also the diseased surface of the gingiva. Recommended guidelines have been established for periodontal pocket depth and the need to create an open flap for visualization. For dogs, pockets up to 5 mm (possibly up to 6mm) not associated with mobility, furcation defects, or caries may be effectively treated with closed root planing.^1,8 Pockets with >5 mm depth and other pathology cannot be visualized adequately for appropriate root cleaning and therefore require periodontal flap surgery and open root planing to remove all plaque, calculus, and granulation tissue.^1,8 Once the appropriate form of root planing has been determined (open versus closed), preparation of the root for regenerative surgery can be completed. The root surface must be completely debrided of all embedded plaque, calculus, and debris. This can be accomplished with a combination of sharp hand instrumentation and ultrasonic scaling. Slightly more force is used against the tooth for root planing compared to crown scaling to leave a clean and smooth root surface.¹ Ultrasonic scaling must be used with care, as excessive heat may cause damage to the periodontium. Specialized root planing tips are available specifically for this purpose. Ultrasonic scaling does have the advantage of reducing the bacterial load in the subgingival area and thus has the ability to sterilize the root surface.^1,8 Once the boney defect has been completely debrided, the type of graft used to fill the defect will need to be selected. Barrier membranes are recommended to cover the bone augmentation product to prevent the down growth of long junctional epithelial tissue into the defect. Epithelial migration (gingiva) occurs more quickly than osteogenesis. In these reported cases, doxycycline hyclate gel was selected and applied as a barrier after the vertical defect was filled. This product is marketed for veterinary use and conforms well to the anatomy of the tooth as it hardens in the sulcus. Many different types of barrier membranes exist. First generation membranes are non-resorbable and therefore not typically chosen as first choice for veterinary patients, as they require additional anesthetic episodes to remove. Second generation membranes are resorbable, and numerous products are available.¹ Most commonly, these are prepackaged sheets of bovine or porcine derived collagen. Freeze-dried cortical bone sheets are also marketed for veterinary use for this purpose. It should be noted that bone augmentation may be ideally performed at a separate anesthetic episode after the initial periodontitis treatments have been performed.⁷ This can be challenging in veterinary patients because of the need for, and risk associated with, additional anesthetic episodes as well as owner consent.

Bone grafting materials can be classified as autografts, allografts, xenografts, and alloplasts.^3,9 The different types of graft materials will vary in their mechanism of bone regeneration properties. These properties include bioactivity, osteoconductivity, osteoinduction, and osteogenesis.⁹ Bioactivity is the ability of osteogenic cells to attach and differentiate on the surface of ceramic particles. Osteoconductivity relates to the ability of the product to act as a temporary or permanent scaffold for bone formation. Osteoinduction refers to the ability to induce bone formation through the induction of osteoprogenitor cells into osteoblasts. Osteogenesis refers to products that already contain bone forming cells. Other properties that would create an ideal bone graft material are not limited to, but would include: bio-compatibility, non-reactive (non-allergic), space maintaining, no risk of disease transmission, resorption rate similar to bone, consistent particle size, appropriate porosity, extensively researched, easy handling, and cost efficient.³ Currently, there are no commercially available products for bone augmentation that contain all of these properties.

Autografts are bone material harvested from the same animal. This is considered the “gold standard” that all other bone grafts are compared to.^1,9 Autografts can be further classified by their location of harvest. A cortical bone graft is harvested from the outer, more dense bone; whereas, cancellous bone grafts are harvested from softer trabechular or spongy bone from the center of long bones.¹⁰ Cancellous autografts are typically considered superior because of the higher content of osteoprogenitor cells. The cancellous material is typically more challenging to harvest and may add to donor morbidity. Cortical autografts have been shown to be successful for periodontal regeneration when harvested from the buccal plate of other extraction sites within the oral cavity.¹⁰ With autografts there is ideal bone composition and particle size with no chance for rejection. Autografts contain osteogenic cells, and care must be taken for these cells to survive the transport. Disadvantages to autografts are the extended anesthetic time and risk to the patient to harvest while only yielding a small quantity for use. Autografts also can have poor structural integrity, as they are resorbed rapidly by the host. Autografts exhibit all three properties involved with new bone formation: osteoinduction, osteoconduction, and osteogenesis.¹

Allografts are bone material from the same species as the recipient. The product currently marketed for veterinary use is canine demineralized freeze-dried bone allograft (DFDBA) and is harvested from cadaver bone. Although the freezing process used to produce the product causes a lysis of most of the osteogenic cells, the demineralization process preserves the bone morphologic proteins (growth factors), thus making the product osteoinductive.¹ Particle size and porosity are the same as cancellous bone, creating a scaffold for bone formation, yielding allografts osteoconductive. An advantage of the freeze-dried product is a long shelf life (5 yr). Disadvantages of the allograft product are that due to the demineralization process, it is poorly radiopaque post filling and can be considered costly compared to other products. DFDBA can be used to extend autografts and, even now, are commercially available for veterinary patients combined with alloplasts as a more cost effective product, while retaining the advantages of being osteoinductive. Veterinary-specific label allografts for dogs are available in different forms and volumes. Bone membrane sheets are available as well as intact bone blocks and segments of various sizes. Cancellous chips are available in fine and ultrafine granules and volumes of as small as 0.3 cc quantity up to 3.0 cc.

Xenografts are bone material from a species different than the recipient. These products most commonly utilize bovine bone, as it is readily available and relatively inexpensive. Veterinary-labeled equine bone graft materials are available and would be considered a xenograft when used in dogs. This product is manufactured in the same way as the canine DFDBA. An advantage to using the equine origin product in dogs is that it is supplied in larger quantities and can therefore be more cost efficient to fill large defects compared to the canine allograft material. Xenografts are typically only considered osteoconductive; however, many homologies in bone morphologic proteins exist between species and may therefore have some osteoinductive properties.¹

Alloplasts are bone grafts that are composed of synthetic material. Although many types of alloplastic materials are available, the most common products available to the veterinary patients are composed of bioglass, hydroxyapatite (HA), and beta-tricalcium phosphate (TCP). Physical properties of these products vary greatly in regards to particle size and porosity. Typically, alloplasts have been considered only osteoconductive in nature and poorly resorbed by the body. Bioglass material readily available to veterinarians is composed of silicon, sodium, calcium, and phosphorous oxides.^u When placed in the body, the bioglass forms a layer of hydroxyapatite-type material on the surface that is conducive to osteoblast attachment. Bioglass particles tend to be smooth and variable size, allowing bone to fill in between the spaces. When used as a filling agent, the bioglass has mechanical hemostatic properties and has shown to prevent the down growth of tissue.¹¹ Also readily available in the veterinary market is a combination product of HA and TCP^v. Composed of 15% HA and 85% TCP, these two compounds are sintered (melted and fused into a single product) together into a rough and porous ceramic that is very similar to cancellous bone. HA provides the dimensional stability for osteoconduction, and the TCP provides calcium and phosphorous ions for mineralization of new bone. The TCP is resorbed and dissolves away slowly, allowing more space for natural bone to migrate, thereby creating more natural bone than a bioglass product. Advantages to the alloplasts are that they are readily available, have a long shelf life, and are inexpensive when compared to other marketed products. Also, when placed in a defect, these alloplasts are radiopaque and easily differentiated from the existing alveolar bone.¹¹ Disadvantages of alloplasts are that as a synthetic product, a potential immunogenic reaction is possible. Also, the absorption rates of these products are extremely variable. TCP is typically a very poor structural product alone, as it tends to be resorbed by the body in months, whereas HA can last for years.⁹ Bioglass products are poorly absorbed by the body, and the resulting bone tends to be primarily composed of the original glass particles.

When reviewing the different classifications and properties of bone graft products marketed specifically for veterinary use, it is evident that not one class of product is ideal for every treatment option. Patient planning, benefit of use, cost, and long-term care must all be discussed first with the owner. There is no bone substitute available that has the strength of cortical bone. Bone substitute products should not be used in areas of active infection and tend to slow the healing process. The use of no bone graft product (a simple blood clot) will typically yield bone in a socket faster than when using bone substitute. A simple blood clot, however, will typically not maintain the crestal bone margin heights.³ Historically, very few veterinary specific products have been available for bone augmentation treatments. Currently, there are several products in these bone graft classifications directly marketed for veterinary use. These products have also been used in combination with each other to potentiate the benefits of each class. Recently, a specific product has been marketed for veterinary use that combines canine DFDBA with TCP and HA^w. This combination adds the advantage of osteoinduction over alloplasts alone and yet is not as costly as DFDBA. Other potential bioactive agents available to the veterinarian would include the addition of platelet-rich plasma from the patient to mix with the bone graft.⁹ The addition of platelet-derived growth factors adds more potential for osteoinduction and bioactivity. This, however, requires a specific collection kit and centrifuge that will add additional cost. Many other graft additives used in humans are being researched such as enamel matrix proteins and bone morphogenic proteins. These products may have great potential, however are not currently marketed directly to the veterinary field.¹

Conclusion

Several different bone augmentation products are available for veterinary use. Although there are a variety of properties and costs associated with these products, these two cases illustrate successful outcome of a similar defect using different bone augmentation material. Several very important factors must be taken into account during the case selection process. For these two cases in particular, owner awareness and long-term commitment to oral health was critical. Attention to detail in diagnosis (radiographs and actual visual presentation with probing) and defect preparation (closed and open root planing and defect debridement) were critical to the successful outcome. These two cases illustrate dogs that have had the ability to maintain the structure and function of their first mandibular molars through bone repair and regeneration utilizing different bone augmentation products that are marketed directly to the veterinary professional.