Histological response to titanium endodontic endosseous implants in dogs

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JOURNAL OF ENDODONTICS

Copyright © 1996 by The American Association of Endodontists

VOL. 22, No. 4, APRIL1996

Histological Response to Titanium Endodontic Endosseous Implants in Dogs Francis R. Parreira, DDS, J. Douglas Bramwell, DDS, James O. Roahen, DDS, MS, and Leo Giambarresi, PhD

Endodontic endosseous implants stabilize teeth that have crown-root ratios compromised by periodontal disease, trauma, or apical resorption. By increasing the crown-root ratio, the implant improves the prognosis of the tooth, thus increasing its longevity. The purpose of this study was to evaluate, in vivo, the healing response to a newly introduced titanium endodontic implant. Eight implants were placed in the maxillary incisors and mandibular premolars of two adult beagle dogs after completion of root canal and osseous preparation. Peri-implant tissues were examined radiographically and histologically at 6 months postinsertion. Radiographically, the periapical area and tissue surrounding the implants seemed normal. Histologically, fibrous connective tissue and healthy bone intimately surrounded the implant. Epithelium or chronic inflammatory cells were not observed along the length of the implant. These findings suggest that titanium is a biocompatible metal when used as an endodontic endosseous implant.

ful use of endodontic implants. Cranin et al. (7) evaluated 253 endodontic implants and found that 91% were successful 5 yr after insertion. The major reason for failure was iatrogenic in nature, highlighting the need for proper case selection. More recently, long-term success cases were presented in an article by Weine and Frank (8), reinforcing the value of endodontic implants. They highlighted that, too frequently, endodontic implants were used in hopeless cases, leading to a high failure rate. Although the popularity of prosthetic-type implants has increased dramatically in the last 10 yr, the use of endodontic implants has dropped significantly. The American Dental Association Council on Dental Materials supports the safe and effective use of endodontic implants in properly selected cases (9). Many materials have been advocated for use as endodontic implants. Vitallium was originally used, but its biocompatibility was questioned when it was shown to undergo surface corrosion (10). Currently, there are two materials available for clinical use as endodontic implants: a tapered single crystal sapphire implant (Kyocera America, Inc., San Diego, CA) and a parallel, threaded titanium implant (Park Dental Research Group, New York). Although the titanium implant is used clinically as a prosthetic endosseous implant, scientific research evaluating its biocompatibility as an endodontic implant has not been done. The purpose of this study was to evaluate histologically the healing response to the placement of titanium endodontic endosseous implants in dogs.

Prosthetic endosseous implants are widely used to replace missing teeth and to restore function to edentulous areas (1). These implants have shown excellent histological acceptance with osseointegration and a minimal inflammatory response (2). Introduced by Strock and Strock (3) in 1943 and described by Orlay (4) in 1960, endodontic endosseous implants use the root canal as a channel tbr placement of the implant into periapical bone. An advantage of endodontic implants over prosthetic implants is their complete enclosure within the tooth, eliminating communication with the oral cavity. Endodontic implants stabilize teeth with compromised crown-root ratios, thus preserving the natural dentition and returning the teeth to a normal state of function (5). In addition, placement of an endodontic implant alleviates the need to extract the tooth and minimizes the healing period. Its use avoids placing an entirely artificial implant that requires intimate gingival adaptation (6). Numerous case presentations in the literature report the success-

M A T E R I A L S AND METHODS Two adult, purpose-bred beagle dogs weighing between 7 and 9 kg were used for this study. Preanesthetic doses of atropine sulfate (0.12 mg subcutaneous) and xylazine hydrochloride (12 mg IM) were administered. The animals then received general anesthesia using 4% isoflurane in 100% oxygen at a flow rate of 3 L/min through a nose cone mask. The animals were intubated, and surgical anesthesia was maintained with 0.5 to 1.5% isoflurane with 100% oxygen at 1.0 to 1.5 L/min flow rate. The maxillary central incisors and mandibular first premolars were radiographed and evaluated clinically with a periodontal probe. All radiographs were exposed with a Philips Oralix 65 (Philips Co., Shelton, CN) that operates at 65 kVp and 7.5 mA. Each experimental tooth was isolated with a rubber dam and disinfected with a 10% iodine solution. The experimental teeth were taken out of function by reducing the occlusal surfaces to a

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FIG 1. Sealer placed on implant.

flat plane. Access to the root canals was made through the center of the occlusal surfaces with a high-speed, end-cutting fissure bur (#557). The pulp tissue was extirpated with a barbed broach. Working lengths were established with Flex-R files at the apical delta, --1 mm short of the radiographic apex and confirmed radiographically. A step-back technique with Flex-R and Hedstrom files was used to prepare the canals. Gates Glidden burs were used to enlarge the coronal half of the canals. Sodium hypochlorite (5.25%) was used as a canal irrigant during chemomechanical preparation. The canals were dried with sterile paper points before osseous preparation. The endodontic implants were placed according to the technique described by Frank (5). The apical root and osseous tissue were prepared with a long-shank, parallel guide drill supplied by the manufacturer. The depth of the osseous preparation was --3 to 4 mm past the root apex. The implants were then seated to length and their position confirmed radiographically. The canals were irrigated with saline and completely dried with sterile paper points. A resin cement (AH26, L. D. Caulk Division, Milford, DE) was then applied to the portion of the implant that would remain within the canal (Fig. l). The implants were cemented using a twisting motion. After allowing the sealer to set, the coronal portion of the implants extending out of the access was sectioned with a high-speed 557 bur. The access was sealed with amalgam, and a radiograph was exposed. A total of eight implants were placed. After completion of the procedure, the dogs were returned to the kennel and resumed a normal diet. There were no immediate adverse sequelae noted from the endodontic treatment. Periapical radiographs of the experimental teeth were exposed at 1, 30, 90, and 180 days after treatment. Six months after placement, a final radiograph was exposed. The dogs were then euthanatized under general anesthesia. The common carotid artery and external jugular vein were exposed, and positive pressure perfusion was performed with 10% buffered formalin to ensure adequate fixation of the tissues. Implants and involved teeth were removed in block sections with a Stryker autopsy saw and were further fixed in 10% buffered formalin for 3 wk. A 2-mm thick sagittal section was cut from the midline of each tissue block with an EXAKT cutting/grinding apparatus (EXACT Technologies, Inc., Oklahoma City, OK). These sections, which

FIG 2. Six-month postoperative radiograph.

contained teeth, implants, and adjacent hard and soft tissues were additionally fixed overnight in 10% buffered formalin and then dehydrated in increasing ethanol concentrations (50 to 100%). Infiltration with Technovit 7200 plastic embedding medium (EXAKT Technologies, Inc.) was accomplished by immersion in a 1:1 mixture of 100% ethanohTechnovit 7200, followed by repeated immersions in 100% Technovit 7200. The dehydration and infiltration process was conducted over a 3-wk period. Specimens were embedded in Technovit 7200 with a Histolux automated photopolymerizing unit (EXAKT Technologies, Inc.), and 10- to 40-/xm sections were prepared with the EXAKT cutting/grinding unit and microgrinder as described by Rohrer and Schubert (11). The final undecalcified sections were stained with hematoxylin and eosin and evaluated by light microscopy.

RESULTS Clinically, the dogs experienced no adverse sequelae from the endodontic treatment throughout the experiment. Increased probing depth, swelling, or mobility was not observed with any of the experimental teeth. Radiographically, there were no periradicular changes noted with the placement of the implants. The implant/tooth interface seemed intact, with no osseous changes noted along the length of the implants (Fig. 2). Histologically, the eight titanium implants seemed to be well tolerated. Generally, fibrous connective tissue and bone were intimately associated with the implant surfaces (Fig. 3). Characteristic segments of mature lamellar bone and focal collections of reactive bone with reversal lines were present. Osteoblastic activity was minimal, and no osteoclastic activity was associated with the bone surrounding the implants. The peripheral bone was unremarkable, and osteocytes were seen in lacunae (Fig. 4). There was

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FJG 3. M a t u r e iamellar b o n e (A) and fibrous connective tissue (B) associated with implant (arrow) exiting t o o t h (C) (upper right-hand area is processing artifact).

virtually no chronic inflammatory response associated with the implants, either at the root apices or along the length of the implants. DISCUSSION With the current widespread use of free standing endosseous implants in dentistry, it is interesting that the use of endodontic implants has waned, despite their high success rate. Recent articles on endodontic implants have been limited to case presentations that have highlighted failed cases attributable to poor case selection. A clinician desiring to use endodontic implants today is limited in the type of materials and implant designs currently available. Because a large number of endodontic implants fail at the tooth/ implant interface, the implant should ideally have a tight fit at the root apex. Because of the parallel-sided design of the titanium implant, it is difficult to obtain a tight apical seal. The tapered design of the radiolucent single crystal implant maximizes the contact at the root/implant interface, but is difficult to see radiographically. This in vivo study histologically evaluated the periradicular response to titanium, one of the two materials presently available for endodontic implants. Although there were favorable results with this research, the study was limited in the number of animals available. This restricted the number of implants that could be placed and precluded any comparison between the two types of implants. The healthy, stable tissues that surround an experimental tooth certainly do not duplicate the pathological conditions in which an

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FiG 4. Representative section s h o w i n g o s s e o u s c o n t a c t (A) with implant (arrow) with minimal inflammation and normal peripheral b o n e (B).

endodontic implant may be placed clinically. Implants placed into healthy tissues would be expected to enjoy higher success than those implants placed in teeth with existing periradicular lesions, root resorption, fracture, or severe periodontal disease. Pathological conditions that are true indications for endodontic implants may ultimately contribute to their failure. In addition, occlusal stresses were not placed on the experimental teeth in this study. By eliminating or minimizing the stresses at the root apex, there would be less chance of disturbing the apical seal. Most clinicians would agree that endodontic implants are a viable treatment option. Their broader use and acceptance may suffer from the paucity of thorough research involving the placement of implants into conditions of pathosis, the lack of optimally designed implants, and minimal clinician training. Only when there is clinician confidence that implants will be consistently successful when placed in diseased and stressed conditions will their use increase. We would like to thank DT2 E. Dagnachew, Major Theresa Gonzales, and the staff at the Armed Forces Radiobiologic Research Institute for their invaluable assistance during this study. The assertions contained herein are those of the authors and are not to be construed as official or as reflecting the views of the Department of the Navy, Department of Defense, or the U.S. government. Dr. Parreira is a former resident at the Naval Dental School, Bethesda, MD, and is now the staff endodontist and Command Consultant in Endodontics at the Naval Dental Clinic, Pearl Harbor, HI. Dr. Bramwell is the staff endodontist at Branch Dental Clinic, Washington Navy Yard, Washington, DC. Dr. Roahen is former chairman of the Endodontics Department, Naval Dental School, Bethesda, MD, and is now in private practice limited to endodontics in Annapolis, MD. Dr. Giambarresi is chief of the Laboratory Division, Research Department, Naval Dental School, Bethesda, MD. Address requests for reprints to Captain J. Douglas Bramwell, DC, USN, Endodontics Department, Branch Dental Clinic, Washington Navy Yard, Washington, DC 20374-1116.

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Parreira et al. References

1. Madison S, Bjorndal A. Clinical application of endodontic implants. J Prosthet Dent 1988;59:603-8. 2. Albrektsson T, Branemark P, Hansson H, Lindstrom J. Osseointegrated titanium implants. Acta Orthop Scand 1981 ;52:155-70. 3. Strock A, Strock M. Method of reinforcing pulpless anterior teeth: preliminary report. J Oral Surg 1943;1:252-5. 4. Orlay H. Endodontic splinting treatment in periodontal disease. Br Dent J 1960;108:118-21. 5. Frank A. Improvement of the crown-root ratio by endodontic endosseous implants. J Am Dent Assoc 1967;74:451-62. 6. Schroeder A, van der Zepen E, Stich H, Sutter F. The reactions of bone, connective tissue, and epithelium to endosteal implants with titanium sprayed

surfaces. J Max-Fac Surg 1981;9:15-25. 7. Cranin A, Rabkin M, Garfinkel I. A statistical evaluation of 952 endosteal implants in humans. J Am Dent Assoc 1967;94:315-20. 8. Weine F, Frank A. Survival of the endodontic endosseous implant. J Endodon 1993;19:524-8. 9. Council on Dental Materials, Instruments, and Equipment. Dental endosseous implants. J Am Dent Assoc 1986;113:949-50. 10. Seltzer S, Green D, De la Guardia R, Maggia J, Barnett A. Vitallium endodontic implants: a scanning electron microscope, electron microprobe, and histologic study. Oral Surg 1973;35:828-60. 11. Rohrer M, Schubert C. The cutting-grinding technique for histologic preparation of undecalcified bone and bone-anchored implants. Oral Surg 1992;74:73-8.

You Might Be Interested Connoisseurs of quaint and colorful medical diagnoses will revel in the names of several of the specific forms of hypersensitivity pneumonitis. These include cheese washer's lung, bagassosis, and potato riddler's lung and are caused respectively by sensitivity to molds specific to cheese, bagasse (sugar cane), and moldy hay found around potatoes (a riddler was a person who sifted potatoes from the hay, often moldy, in which they had been stored), Yuppies! Do not scorn these outmoded ills! Also recognized are winegrower's lung and--wait for it--hot tub lung. Well, at least spare me from bagassosis. William Cornelius