Porous Titanium Endosseous Dental Implants in Rhesus Monkeys: Microradiography and Histological Evaluation F. A. YOUNG and M. SPECTOR, Department of Biological and Physical Sciences, and C. H. KRESCH, Department of Periodontics, College of Dental Medicine, Medical University of South Carolina, Charleston, South Carolina 29403
Summary Artificial tooth roots with porous surface coatings were fabricated by sintering spherical powder of titanium alloy to solid cylindrical cores. The tooth roots were implanted subgingivally in healed mandibular premolar extraction sites of fifteen Rhesus monkeys. Supracrestal abutments were screwed into pretapped holes in the superior aspect of the primary subgingival stage four to eight weeks after implantation of the root. Clinicalevaluationswere performed monthly. Ten animals were sacrificed for histological evaluation of the functioning free standing implants. Of twenty-nine implants placed, three were lost and four were rated failures on the basis of histological evaluation. Postmortem evaluations revealed bone growth into the porous surface coating of the primary stage of all the implants. The most characteristic features which could be used to describe differences in the implant histology were the buccal and lingual crestal bone heights measured in relation to the root porosity. Twelve of sixteen implants had crestal bone heights within one millimeter of the superior aspect of the root. Four other implants displayed excessive bone recession, revealing as much as o ?e half of the root porosity supracrestally. The four implant failures could be related 1.0 mm. Right side of mandible. There was no bone ingrowth in the porosity along the lingual aspect of the root. a
Tissue areas selected for ultrastructural study were cut from the 150-pm sawed sections and reimbedded in molds designed for ultramicrotomy. “Thick” sections (approximately 1 pm thick) were stained with toluidine blue for light microscopy. Adjacent ultra-thin sections, about 100 nm in thickness, were stained with uranyl acetate and lead citrate for transmission electron microscopy.
RESULTS The sintering process employed in the study yielded a porous surface coating with 34%porosity and an average pore size of 125p m [Fig. 3(a) and 3(b)]. The sintering conditions produced a typical largegrained alpha-beta structure in the titanium material of both the core and porous portions of the implant (Fig. 4). The rounded fillet-
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Fig. 8. Microradiographs of mesiodistal sections of implants in each of the three classifications in Table I: 22 mo. (No. 7R); 10 mo. (No. 16L); 15 mo. (No. 13L).
shaped welds produced between powder particles and between the powder and core demonstrated grain growth across the necks and smooth surfaced interconnecting channels in the porosity (Figs. 3 and 4). Of the twenty-nine implants placed in the fifteen Rhesus monkeys, three implants were lost and sixteen implants were obtained for postmortem histological evaluation. Ten implants ranging from one to two years continue to function successfully in the five surviving animals. The clinical evaluations conducted monthly generally proved inadequate for distinguishing successful from unsuccessful implants because of a lack of difference (in the parameters measured) between more successful and less successful implants. Radiographs and probing revealed an intrabony defect in one of the implants (No. 13R) causing it to be ruled unsuccessful. However, all the other implants presented unremarkable periapical radiographs and zero mobility. A more detailed description of the clinical results is presented elsewhere.21 Microradiography and histological evaluation revealed bone growth into the porous surface coating of the primary stage of all the implants (Fig. 5). In areas where the enveloping bone was cancellous-like,
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Fig. 9. Micrographs of failed dental implants in a mandibular ridge with a narrow profile: (a) left and (b) right premolar sites of monkey No. 12; B-buccal, L-lingual.
marrow elements could be seen within the root porosity. Few pockets of fibrous tissue were seen within the pores of the implants. In many cases the ground section histology revealed bone in immediate apposition to the titanium spheres with no discernible fibrous tissue interposed (Fig. 6). The most characteristic features which could be used to describe differences in the implant histology were the buccal and lingual crestal bone heights measured in relation to the root porosity (Fig. 5). The most favorable histologic picture was presented by five of the implants which displayed crestal bone to the superior aspect of the root porosity. The entire porous surface was encased in bone. Seven implants had 1 mm or less porosity exposed above the crestal bone. These implants were assigned to a second category and considered potentially problematic because of the indication of bone recession. Four implants were rated failures on the basis of unfavorable histology. Crestal bone height had dropped several millimeters below the superior aspect of the root, exposing as much as one-half of the root porosity supracrestally. The four failed implants also displayed adverse changes in the adjacent gingiva. These changes included epithelial invagination apically along the root porosity and breakdown of the connective tissue of the gingiva [Figs. 7(a), 7(b), and 7(c)].
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Bone loss adjacent to the implants occurred more often as buccal and lingual recession than as intrabony defects. Bone recession along the buccal aspect was greater than that along the lingual aspect for most implants (Table I). Mesiodistal sections revealed osseous profiles comparable to those seen in buccolingual sections (Fig. 8). There was no correlation between the amount of bone loss observed and the length of time the implants were in function (Table I). Histological evaluations revealed cellular infiltrates in the sulcular region of implants in each of the three categories noted.
DISCUSSION The results demonstrate that the bone growth into the porous surface coatings of artificial tooth roots is an efficacious method of dental implant fixation. So complete is the bone growth into the coating and so effective is the fixation that conventional clinical evaluation is not sensitive to potentially adverse tissue changes that may occur. Mobility measurements for all the implants were zero even though two specimens had as much as one-half of their porosity exposed supracrestally. Because of the insensitivity of the clinical evaluation parameters the final verdict for the ten implants remaining in function in the five surviving monkeys must await postmortem histological evaluation. T o date there is no radiographic sign of bone loss around these implants. One characteristic feature of the implanthone profile seen in buccolingual sections was the difference in the crestal bone height along the buccal and lingual sides of the implant. A t implantation the edentulous ridge presented an angular profile with a high lingual aspect and a lower buccal aspect. In most cases the primary, endosseous root stages were placed so that the superior collar was at about the same level as the superior surface of the buccal bone. Any remodeling of crestal bone thereafter tended to reveal more of the porosity along the buccal than along the lingual aspects. The buccal and lingual bone recession seen in the Class I1 implants probably is the result of initial remodeling associated with the implantation of a porous root into an angular edentulous site rather than the result of active bone resorption associated with a failing implant. The Class I1 implants could thus be added to those of Class I in compiling the number of functionally successful implants.
POROUS TITANIUM ENDOSSEOUS DENTAL IMPLANTS
855
Examination of two of the implant failures from the same monkey revealed an alveolar ridge profile that was more angular than most (Fig. 9). In each case 2 mm of the root porosity along the buccal aspect remained exposed after placement of the implants. Failure was probably potentiated because the implant was oversized for the recipient bone. Implantation thus produced a loss of bone from the buccal crest and resulted in thin cortical plates buccally and lingually. In the case of the other two failed implants from a second monkey the width of the alveolar crest was wider than most but lacked a thick, dense crestal cortical plate (Fig. 5). The reason for the relatively thin, porous overlying cortical plate in one of the sites was that it was the site of a prior implant failure and may not have been given sufficient time to heal before reimplantation.
CONCLUSIONS An inert porous coated artificial tooth root is capable of supporting a single free-standing artificial tooth for periods up to two years in Rhesus monkeys. Bone growth into the porosity is an adequate medium for support and retention of implants. Anatomical factors such as crestal bone height, width, and density at the recipient site are critical to the successful long-term function of the artificial tooth root. A two-stage method of implantation can be successfully employed for endosseous dental implants. This research was supported by the National Institutes of Health-National Institute of Dental Research, Research Grant Nos. DE03497 and DE70205. The assistance of Scott Harmon and Joan Eldridge is gratefully acknowledged. J. R. Natiella, D.D.S., of the State University of New York at Buffalo, assisted in the histolopathological evaluations.
References 1. Edentulous Persons i n the U S . , 1971 Vital and Health Statistics, Data for a National Health Survey 10 (#89),HEW Publication #(HRA 74-15161, June 1974. 2. L. I. Linkow and R. Chercheve, Theories and Techniques of Oral Irnplantology, Vols. I and 11, C. V. Mosby, St. Louis, 1970. 3. A. N. Cranin, Oral Implantology, C. Thomas, Springfield, Ill., 1970. 4. D. Grenoble, in Dental Biornaterials: Research Priorities, DHEW Publication NIH 74-548,1974, pp. 139-165.
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YOUNG, SPECTOR, AND KRESCH
5. J. R. Natiella, J. E. Armitage, G. W. Greene, and M. A. Meenaghan, J . A m . Dent. Assoc., 84,1358 (1972). 6. T. D. Driskell, M. J. O’Hara, H. D. Sheets, G. W. Greene, J. R. Natiella, and J. Armitage, J . Biomed. Mater. Res. Symp., 2,345 (1972). 7. J. E. Hamner and 0.M. Reed, J . Biomed. Mater. Res. Symp., 4,217 (1973). 8. D. E. Grenoble and R. Voss, Oral Zmplantol., 6 (4), 509 (1977). 9. J. J. Klawitter, A. M. Weinstein, J. Kent, C. Farrell, and J. Bokros, in Transactions of the 4th Annual Meeting of the Society for Biomaterials, 1978, p. 74. 10. M. Hodosh, M. Povar, and G. Shklar, J. Am. Dent. Assoc., 70,362 (1965). 11. L. L. Hench, R. J. Splinter, T. K. Greenlee, and W. C . Allen, J. Biomed. Muter. Res. Symp., 2, 117 (1972). 12. V. V. Strunz, M. Bunte, R. Stellmach, U. M. Gross, K. Kuhl, H. Bromer, and K. Deutscher, Dtsch. Zahnaerztl. Z., 32,287 (1977). 13. L. I. Linkow, Dent. Clin. N . Am., 14,185 (1970). 14. D. E. Grenoble, R. L. Kim, R. Voss, R. J. Melrose, G. Wullschlager, A. C. Knoell, and K. K. Gupta, in Proceedings of the 18th National Society of Aerospace, Materials and Process Engineers Symposium, 1973, p. 276-283. 15. S. Sandhaus, Reu. Trim. Implant., 7, May 1969. 16. T. D. Driskell and A. L. Heller, Oral Zmplantol., 7(1), 53 (1977). 17. C. Hassler, L. McCoy, R. Downes, L. Clark, and B. Russell, in Transactions o f t h e 4th Annual Meeting of the Society for Biomaterials, 1978, p. 114115. 18. M. B. Weiss and W. Rostoker, in Transactions of the 4 t h Annual Meeting of the Society for Biomaterials, 1978, p. 45. 19. J. J. Klawitter, T. Sander, A. M. Weinstein, and L. Peterson, in Transactions o f the 4 t h Annual Meeting of t h e Society for Biomateriak, 1978, p. 48. 20. A. R. Spurr, J. Ultrastruct. Res., 25,31 (1969). 21. F. A. Young, C. H. Kresch, and M. Spector, J. Prosthet. Dent., 41,561 (1979).
Received October 20,1978 Revised February 2,1979
Summary Artificial tooth roots with porous surface coatings were fabricated by sintering spherical powder of titanium alloy to solid cylindrical cores. The tooth roots were implanted subgingivally in healed mandibular premolar extraction sites of fifteen Rhesus monkeys. Supracrestal abutments were screwed into pretapped holes in the superior aspect of the primary subgingival stage four to eight weeks after implantation of the root. Clinicalevaluationswere performed monthly. Ten animals were sacrificed for histological evaluation of the functioning free standing implants. Of twenty-nine implants placed, three were lost and four were rated failures on the basis of histological evaluation. Postmortem evaluations revealed bone growth into the porous surface coating of the primary stage of all the implants. The most characteristic features which could be used to describe differences in the implant histology were the buccal and lingual crestal bone heights measured in relation to the root porosity. Twelve of sixteen implants had crestal bone heights within one millimeter of the superior aspect of the root. Four other implants displayed excessive bone recession, revealing as much as o ?e half of the root porosity supracrestally. The four implant failures could be related 1.0 mm. Right side of mandible. There was no bone ingrowth in the porosity along the lingual aspect of the root. a
Tissue areas selected for ultrastructural study were cut from the 150-pm sawed sections and reimbedded in molds designed for ultramicrotomy. “Thick” sections (approximately 1 pm thick) were stained with toluidine blue for light microscopy. Adjacent ultra-thin sections, about 100 nm in thickness, were stained with uranyl acetate and lead citrate for transmission electron microscopy.
RESULTS The sintering process employed in the study yielded a porous surface coating with 34%porosity and an average pore size of 125p m [Fig. 3(a) and 3(b)]. The sintering conditions produced a typical largegrained alpha-beta structure in the titanium material of both the core and porous portions of the implant (Fig. 4). The rounded fillet-
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YOUNG, SPECTOR, AND KRESCH
Fig. 8. Microradiographs of mesiodistal sections of implants in each of the three classifications in Table I: 22 mo. (No. 7R); 10 mo. (No. 16L); 15 mo. (No. 13L).
shaped welds produced between powder particles and between the powder and core demonstrated grain growth across the necks and smooth surfaced interconnecting channels in the porosity (Figs. 3 and 4). Of the twenty-nine implants placed in the fifteen Rhesus monkeys, three implants were lost and sixteen implants were obtained for postmortem histological evaluation. Ten implants ranging from one to two years continue to function successfully in the five surviving animals. The clinical evaluations conducted monthly generally proved inadequate for distinguishing successful from unsuccessful implants because of a lack of difference (in the parameters measured) between more successful and less successful implants. Radiographs and probing revealed an intrabony defect in one of the implants (No. 13R) causing it to be ruled unsuccessful. However, all the other implants presented unremarkable periapical radiographs and zero mobility. A more detailed description of the clinical results is presented elsewhere.21 Microradiography and histological evaluation revealed bone growth into the porous surface coating of the primary stage of all the implants (Fig. 5). In areas where the enveloping bone was cancellous-like,
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853
Fig. 9. Micrographs of failed dental implants in a mandibular ridge with a narrow profile: (a) left and (b) right premolar sites of monkey No. 12; B-buccal, L-lingual.
marrow elements could be seen within the root porosity. Few pockets of fibrous tissue were seen within the pores of the implants. In many cases the ground section histology revealed bone in immediate apposition to the titanium spheres with no discernible fibrous tissue interposed (Fig. 6). The most characteristic features which could be used to describe differences in the implant histology were the buccal and lingual crestal bone heights measured in relation to the root porosity (Fig. 5). The most favorable histologic picture was presented by five of the implants which displayed crestal bone to the superior aspect of the root porosity. The entire porous surface was encased in bone. Seven implants had 1 mm or less porosity exposed above the crestal bone. These implants were assigned to a second category and considered potentially problematic because of the indication of bone recession. Four implants were rated failures on the basis of unfavorable histology. Crestal bone height had dropped several millimeters below the superior aspect of the root, exposing as much as one-half of the root porosity supracrestally. The four failed implants also displayed adverse changes in the adjacent gingiva. These changes included epithelial invagination apically along the root porosity and breakdown of the connective tissue of the gingiva [Figs. 7(a), 7(b), and 7(c)].
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YOUNG, SPECTOR, AND KRESCH
Bone loss adjacent to the implants occurred more often as buccal and lingual recession than as intrabony defects. Bone recession along the buccal aspect was greater than that along the lingual aspect for most implants (Table I). Mesiodistal sections revealed osseous profiles comparable to those seen in buccolingual sections (Fig. 8). There was no correlation between the amount of bone loss observed and the length of time the implants were in function (Table I). Histological evaluations revealed cellular infiltrates in the sulcular region of implants in each of the three categories noted.
DISCUSSION The results demonstrate that the bone growth into the porous surface coatings of artificial tooth roots is an efficacious method of dental implant fixation. So complete is the bone growth into the coating and so effective is the fixation that conventional clinical evaluation is not sensitive to potentially adverse tissue changes that may occur. Mobility measurements for all the implants were zero even though two specimens had as much as one-half of their porosity exposed supracrestally. Because of the insensitivity of the clinical evaluation parameters the final verdict for the ten implants remaining in function in the five surviving monkeys must await postmortem histological evaluation. T o date there is no radiographic sign of bone loss around these implants. One characteristic feature of the implanthone profile seen in buccolingual sections was the difference in the crestal bone height along the buccal and lingual sides of the implant. A t implantation the edentulous ridge presented an angular profile with a high lingual aspect and a lower buccal aspect. In most cases the primary, endosseous root stages were placed so that the superior collar was at about the same level as the superior surface of the buccal bone. Any remodeling of crestal bone thereafter tended to reveal more of the porosity along the buccal than along the lingual aspects. The buccal and lingual bone recession seen in the Class I1 implants probably is the result of initial remodeling associated with the implantation of a porous root into an angular edentulous site rather than the result of active bone resorption associated with a failing implant. The Class I1 implants could thus be added to those of Class I in compiling the number of functionally successful implants.
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855
Examination of two of the implant failures from the same monkey revealed an alveolar ridge profile that was more angular than most (Fig. 9). In each case 2 mm of the root porosity along the buccal aspect remained exposed after placement of the implants. Failure was probably potentiated because the implant was oversized for the recipient bone. Implantation thus produced a loss of bone from the buccal crest and resulted in thin cortical plates buccally and lingually. In the case of the other two failed implants from a second monkey the width of the alveolar crest was wider than most but lacked a thick, dense crestal cortical plate (Fig. 5). The reason for the relatively thin, porous overlying cortical plate in one of the sites was that it was the site of a prior implant failure and may not have been given sufficient time to heal before reimplantation.
CONCLUSIONS An inert porous coated artificial tooth root is capable of supporting a single free-standing artificial tooth for periods up to two years in Rhesus monkeys. Bone growth into the porosity is an adequate medium for support and retention of implants. Anatomical factors such as crestal bone height, width, and density at the recipient site are critical to the successful long-term function of the artificial tooth root. A two-stage method of implantation can be successfully employed for endosseous dental implants. This research was supported by the National Institutes of Health-National Institute of Dental Research, Research Grant Nos. DE03497 and DE70205. The assistance of Scott Harmon and Joan Eldridge is gratefully acknowledged. J. R. Natiella, D.D.S., of the State University of New York at Buffalo, assisted in the histolopathological evaluations.
References 1. Edentulous Persons i n the U S . , 1971 Vital and Health Statistics, Data for a National Health Survey 10 (#89),HEW Publication #(HRA 74-15161, June 1974. 2. L. I. Linkow and R. Chercheve, Theories and Techniques of Oral Irnplantology, Vols. I and 11, C. V. Mosby, St. Louis, 1970. 3. A. N. Cranin, Oral Implantology, C. Thomas, Springfield, Ill., 1970. 4. D. Grenoble, in Dental Biornaterials: Research Priorities, DHEW Publication NIH 74-548,1974, pp. 139-165.
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YOUNG, SPECTOR, AND KRESCH
5. J. R. Natiella, J. E. Armitage, G. W. Greene, and M. A. Meenaghan, J . A m . Dent. Assoc., 84,1358 (1972). 6. T. D. Driskell, M. J. O’Hara, H. D. Sheets, G. W. Greene, J. R. Natiella, and J. Armitage, J . Biomed. Mater. Res. Symp., 2,345 (1972). 7. J. E. Hamner and 0.M. Reed, J . Biomed. Mater. Res. Symp., 4,217 (1973). 8. D. E. Grenoble and R. Voss, Oral Zmplantol., 6 (4), 509 (1977). 9. J. J. Klawitter, A. M. Weinstein, J. Kent, C. Farrell, and J. Bokros, in Transactions of the 4th Annual Meeting of the Society for Biomaterials, 1978, p. 74. 10. M. Hodosh, M. Povar, and G. Shklar, J. Am. Dent. Assoc., 70,362 (1965). 11. L. L. Hench, R. J. Splinter, T. K. Greenlee, and W. C . Allen, J. Biomed. Muter. Res. Symp., 2, 117 (1972). 12. V. V. Strunz, M. Bunte, R. Stellmach, U. M. Gross, K. Kuhl, H. Bromer, and K. Deutscher, Dtsch. Zahnaerztl. Z., 32,287 (1977). 13. L. I. Linkow, Dent. Clin. N . Am., 14,185 (1970). 14. D. E. Grenoble, R. L. Kim, R. Voss, R. J. Melrose, G. Wullschlager, A. C. Knoell, and K. K. Gupta, in Proceedings of the 18th National Society of Aerospace, Materials and Process Engineers Symposium, 1973, p. 276-283. 15. S. Sandhaus, Reu. Trim. Implant., 7, May 1969. 16. T. D. Driskell and A. L. Heller, Oral Zmplantol., 7(1), 53 (1977). 17. C. Hassler, L. McCoy, R. Downes, L. Clark, and B. Russell, in Transactions o f t h e 4th Annual Meeting of the Society for Biomaterials, 1978, p. 114115. 18. M. B. Weiss and W. Rostoker, in Transactions of the 4 t h Annual Meeting of the Society for Biomaterials, 1978, p. 45. 19. J. J. Klawitter, T. Sander, A. M. Weinstein, and L. Peterson, in Transactions o f the 4 t h Annual Meeting of t h e Society for Biomateriak, 1978, p. 48. 20. A. R. Spurr, J. Ultrastruct. Res., 25,31 (1969). 21. F. A. Young, C. H. Kresch, and M. Spector, J. Prosthet. Dent., 41,561 (1979).
Received October 20,1978 Revised February 2,1979
