- Email: [email protected]
Comparative radiologic study of bone density and cortical thickness of donor bone used in mandibular reconstruction
Comparative radiologic study of bone density and cortical thickness of donor bone used in mandibular reconstruction Hoon Myoung, DDS, MSD,a Young-Youn Kim, DDS, MSD,a Min-Suk Heo, DDS, MSD, PhD,b Sam-Sun Lee, DDS, MSD, PhD,b Soon-Chul Choi, DDS, MSD, PhD,b and Myung-Jin Kim, DDS, MSD, PhD,a Seoul, Korea SEOUL NATIONAL UNIVERSITY
Objective. The aim of this study was to compare the total cancellous bone density, bone-implant interface density, and cortical thickness of 6 donor bone types commonly used in oral and maxillofacial reconstruction.
Methods. A total of 120 bones from 20 Korean adults—including iliac bones, fibulas, cranial bones, scapulas, ribs, and clavicles—were selected. The implant recipient site was determined by the shape, contour, and anatomical limitations of the bones. The serial cross-sectional images of each bone were then acquired through computed tomography. Total cancellous bone density, bone-implant interface density around the imaginary implant fixture, and the cortical thickness along both sides of the imaginary fixture on each cross-sectional image were evaluated and compared. Results. The cancellous bone density of each donor bone type had a statistically significant difference. The cranial bone showed the highest cancellous bone density, followed by the iliac bone, clavicle, scapula, rib, and fibula (P < .05). The boneimplant interface density of the cranial bone, clavicle, fibula, and scapula each belonged to the same Duncan’s group, whereas the rib and iliac bone showed lower bone-implant interface density. In average cortical thickness, the scapula and fibula had a thicker cortex surrounding the imaginary implant than the other bones, and the rib had the thinnest cortex. Conclusion. Although more extensive testing is needed to explain the clinical implications of these results, the findings of this study may help clinicians choose the most appropriate donor bone.
(Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2001;92:23-9)
The prerequisites to a successful functional oral rehabilitation include extensive ablating surgery of the jaw, the restoration of any morphologic defects, and a functionally stable retentive dentition. The reconstruction of jaw bone defects caused by tumor, infection, or trauma is one of the major procedures in the oral and maxillofacial field. Improved reconstructive techniques and osseointegrated dental implants have resulted in better esthetic and functional results.1 Several autogenous bones have been used for oromandibular reconstruction, and previous reports have documented the successful osseointegration of implants placed directly into the donor bone.2,3 The cortical thickness of the donor bone that supports the implant fixture may have a significant effect on the critical factors of osseointegration, including the initial stability of the implant fixture, which is known to be an important factor for achieving Supported in part by 2001 BK21 project for Medicine, Dentistry and Pharmacy. aDepartment of Oral and Maxillofacial Surgery, Dental Research Institute, College of Dentistry, Seoul National University. bDepartment of Oral and Maxillofacial Radiology, Dental Research Institute, College of Dentistry, Seoul National University. Received for publication Nov 24, 2000; returned for revision Dec 8, 2000; accepted for publication Feb 1, 2001. Copyright © 2001 by Mosby, Inc. 1079-2104/2001/$35.00 + 0 7/12/115027 doi:10.1067/moe.2001.115027
good osseointegration.4 The cancellous bone density is also an important factor when one is choosing a more favorable donor bone because it may be responsible for the biologic response and mechanical support of the implant fixture. In particular, the quality of the bone-implant interface may affect the initial stability that is crucial for obtaining osseointegration.5 Accordingly, a presurgical examination of bone quantity and quality may be important for obtaining an accurate estimate of the expected osseointegration. In contrast to the many reports about the relationships between bone quantity and quality and implant success,6-11 there are few studies that report on the quantity and quality of the donor bone.12-14 The quantity and quality of a bone may be evaluated through many methods. The bone quality can be evaluated by histomorphometry,15 quantitative computed tomography (QCT),16 or biomechanic testing.17 When one is planning the implant installation, CT aids in certain functions, such as reformatting, measuring, window setting, and magnification.18,19 Moreover, CT is a noninvasive method for evaluating the cortex and marrow separately.16 Densitometric studies of bones, using CT, have been undertaken,20,21 but the investigations did not consider the implant placement. The aim of the present study was to evaluate bone quality and quantity by simulating the installation of endosseous implants and comparing the total cancellous bone 23
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Table I. Donor bone types and anatomical reference of implantable site
thickness of 2 mm; IQ scanner, Picker International). Three serial images were obtained at a recipient implant site, and each image was displayed with a window width of 2000 Hounsfield units (HU) and a window level of –250 HU. The pixel densities shown in the ROI were determined, and bone density was expressed in Hounsfield units. An ROI was set within the cancellous bone area by 3 oral and maxillofacial radiologists with many years of experience manipulating CT to evaluate the cancellous bone density (Fig 1, A). The cancellous bone density was defined as the mean CT value of pixels involved in the ROI. To evaluate the bone-implant interface density, we superimposed an imaginary implant fixture (10-mm long and 3.75-mm wide) on each cross-sectional image, and 2 oral and maxillofacial surgeons and 2 prosthodontists determined the optimal angulation and direction of the imaginary implant fixture by consensus. Potential complications, including perforation (Fig 1, B), were considered. The oral and maxillofacial surgeons assessed the scans to decide the angulation and direction of the implant fixture, and this was modified according to the biomechanic and esthetic requirements of the prosthodontists. The boneimplant interface density was defined as the mean CT value of a series of 3 pixels surrounding the imaginary fixture (Fig 1, C). The cortical thickness was digitally measured on the image superimposed with the imaginary implant fixture. The vertical length of the cortical area surrounding the imaginary fixture was measured twice along each side of the imaginary fixture, and the mean value was defined as the cortical thickness of the bone. Any differences in cortical thickness and bone density were analyzed with analysis of variance, followed by Duncan’s test (P = .05).
Donor bone type Iliac bone
Fibula Scapula
Cranial bone
Clavicle Rib
Anatomical reference of implantable site From the anterior superior iliac spine (ASIS); 3 implant recipient sites were marked at 2.5-cm intervals. From the central part of a 15-cm-long harvested fibular shaft; 3 implant recipient sites were marked. In the lateral scapular border, a 10-cm-long bony shaft was positioned; 3 implant recipient sites were marked. In the parietotemporal region, a 10 × 10-cm rectangular shape of cranial bone was positioned; 3 implant recipient sites were marked at 2.5-cm intervals. From the center of clavicle shaft; 3 implant recipient sites were marked at 2.5-cm intervals. In the 6th or 7th rib, a 10-cm-long bony shaft; 3 implant recipient sites were chosen randomly and marked.
density, interface bone density, and cortical thickness of 6 donor bone types commonly used in oral and maxillofacial reconstruction.
MATERIAL AND METHODS Bone selection and marking of implant recipient site A total of 120 bones from 20 Korean adults (12 men and 8 women) were selected. The donor bones included iliac bones, fibulas, cranial bones, scapulas, ribs, and clavicles. The material consisted of bones from individuals 41 to 71 years of age (mean age, 57.5 years) who had elected to donate their bodies to medical research. There was no medical history of disease or treatment that might have altered bone metabolism, including systemic osteoporosis. All of the bones were acquired from autopsy specimens and prepared20 at the Department of Oral Anatomy, Seoul National University. Briefly, each body was fixed in formalin by using a mortal perfusion technique. Each bone was removed, degloved, and postfixed in 10% neutralized buffered formalin solution. The anatomical landmarks were checked and the clinical implantable site was determined by donor bone shape, contour, and anatomical limitations, as shown in Table I. Radiopaque marking was done with metal pins, which are too short and thin to produce any artifacts on the region of interest (ROI), to obtain reference points for crosssectional images (Table I). CT examination The cross-sectional images were acquired at each bone site with CT (130 kVp and 20 mAs, with a slice
RESULTS Cancellous bone density The cranial bone showed the highest cancellous bone density (–185.35 ± 131.6), followed by the iliac bone (–559.25 ± 130.8), clavicle (–570.85 ± 243.4), scapula (–587.13 ± 281.7), rib (–708.5 ± 268.5), and fibula (–891.5 ± 320.9) (Fig 2). Each donor bone showed a statistically significant difference in cancellous bone density (P < .05). Bone-implant interface density With respect to bone-implant interface density, the cranial bone (677.9 ± 261.6), clavicle (615.0 ± 219.3), fibula (610.5 ± 258.4), and scapula (582.0 ± 223.0) belonged to the same Duncan’s group, but the rib (181.7 ± 84.5) and iliac bone (–408.6 ± 230.7) showed markedly lower bone-implant interface
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A
B
C Fig 1. A, Schematic drawing of cross-sectional images illustrating that ROI was allocated between cortical (A) and trabecular (B) bone. B, Imaginary implant (10-mm long and 3.75-mm wide) is superimposed on crosssectional image to determine optimal angulation and direction. C, Measurement of bone density between bone and imaginary implant interface.
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Fig 2. Cancellous bone density of respective donor bone types (P < .05).
Fig 3. Bone-implant interface density of respective donor bone types. The bones marked with an asterisk belong to the same Duncan’s group (P < .05).
density (P < .05). In particular, the ilium, which has been used most often in our hospital for bone grafting procedures, had the lowest bone-implant interface density (Fig 3).
Cortical thickness There was significant variation in the average cortical thickness of the implantable site in each bone. The scapula and fibula each had a thicker cortex sur-
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Fig 4. Cortical thickness of respective donor bone types. Bones marked with each symbol (asterisk, dagger) belong to the same Duncan’s group (P < .05).
rounding the imaginary implant than the other bones (average thickness, 3.8 ± 0.95 mm and 3.46 ± 0.96 mm, respectively), and were followed in cortical thickness by the clavicle (2.77 ± 0.7 mm). The cranial bone and iliac bone showed relatively thin cortical thickness (2.22 ± 0.55 mm and 2.39 ± 1.38 mm, respectively), and the rib showed the thinnest cortex (1.81 ± 0.47 mm) (Fig 4).
DISCUSSION In a densitometric study of donor bone, Becker et al12 compared some donor bones with CT images to determine endosseous dental implant sites. Their study showed that the iliac crest was the most consistently implantable donor site, followed by the scapula, fibula, and radius.1 The quality of the bone is often referred to in the implant literature as the amount of cortical and trabecular bone bed in which the recipient socket is drilled.22,23 Lower cancellous bone density may cause compromised osteogenesis or excessive resorption compared with higher density bone, thereby upsetting osseous healing. Clinically, bone quality in the jaw has often been evaluated with the classification described by Lekhom and Zarb.24 Although this classification of bone quality grade is clinically useful, it has 2 critical weaknesses. One is that it is so subjective that the bone quality data may vary according to the observer, and
the other is that it gives only a mean value for the entire arch, so that of the individual site cannot be reported. In addition, it can be used only to evaluate the bone density in the jaw and not in other bones. A standardized index for evaluating the various donor bones was needed. Our data may represent the structural integrity and trabecular pattern in the quantitative scale. A low bone density at the interface site may be relatively unfavorable for osseointegration because the excessive movement of the implant can discourage early bone healing. Micromotion in the osseointegration period can cause an increasing number microstrains that lead to the formation of fibrous tissue at the interface.25 A self-tapping technique and sequential osteotome have been used clinically to increase the bone-implant interface density by compacting the bone at the interface.26-28 Theoretically, implantation in thicker cortical bone may result in improved postoperative immobilization of the dental implant and a higher probability of successful osseointegration. In the present study, the fibula and scapula outranked the other bones with respect to cortical thickness. In situations involving unfavorable bone quality (bone with type IV grade quality, by Lekhom and Zarb24), the initial stability would depend on the marginal cortical bone. Therefore, it could be postulated that the fibula
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and scapula both had an advantage over the other bones with respect to increased implant surface area engaging cortical bone. The scapula scored a relatively high grade of bone quantity and quality, which was in accordance with a previous study.12 The clavicle and cranial bones have been less commonly used as donor bones for oral and maxillofacial reconstruction. However, as shown in our data, the clavicle and cranial bones showed relatively high cortical thickness, cancellous bone density, and bone-implant interface density. Therefore, the clavicle or cranial bones may be considered as possible donor bones in oromandibular reconstruction. In our study, the fibula had the lowest cancellous bone density of all the studied bones, whereas it scored a relatively high grade in cortical thickness and boneimplant interface density. In our experience, the fibula has been proven successful in oromandibular reconstruction and implant installation. The thick cortex and high implant-bone interface density may explain its favor as a donor bone. The iliac bone is frequently used as a donor bone in oral and maxillofacial reconstruction because it has greater bone quantity and is possible to use during a 2team operation.29 As shown in our results, the boneimplant interface density of the iliac bone was lower than that of the other bones. However, we have obtained good results after the implant fixture was installed in the iliac bone, although the soft cancellous bone predominated in the iliac bones. This can be explained by 2 aspects of bone quality. One is the mechanical property, characterized by initial physical support of the implant fixture, and the other is the biologic aspect, which has a part in the remodeling capacity. The process of osseointegration not only depends on the trabecular structure but also on the presence of viable, living osteocytes in the peri-implant region.1 In an animal experiment, Chappard et al30 demonstrated that the remodeling process appeared to improve bone quality and increase the bone-titanium interface around the implant. The apposition of the neocortical bone on the implant appeared to be achieved quickly by the abundant cancellous bone, which involved an abundance of viable, living osteocytes. This ability could sufficiently compensate for the lower mechanical property at the interface site, although more evidence is needed to confirm this hypothesis. The rib has also been frequently used as a grafting material, primarily due to its relatively easy harvesting procedure. However, the rib showed relatively low grades of bone density and cortical thickness, so it may be unreasonable to use it alone for oromandibular reconstruction.
CONCLUSION Clearly, other factors can be assumed to affect the prognosis of the implant, including patient age, sex, vascularity of the donor bone, and metabolic diseases like osteoporosis.1,31 It is unknown whether the vascularity of the donor bone, age, and sex are related to the long-term survival of the implant. Although our results are independent of these other factors, the results shown here may assist the clinician in choosing the most appropriate donor bone for improved functional oromandibular reconstruction. REFERENCES 1. Moscoso JF, Keller J, Genden E, Weinberg H, Biller HF, Buchbinder D, et al. Vascularized bone flaps in oromandibular reconstruction: a comparative anatomic study of bone stock from various donor sites to assess suitability for endosseous dental implants. Arch Otolaryngol Head Neck Surg 1994;120:36-43. 2. Urken ML, Buchbinder D, Weinberg H, Vickery C, Sheiner A, Parker R, et al. Functional evaluation following microvascular oromandibular reconstruction of the oral cancer patient: a comparative study of reconstructed and nonreconstructed patients. Laryngoscope 1991;101:935-50. 3. Lukash FN, Sachs SA, Fischman B, Attie JN. Osseointegrated denture in a vascularized bone transfer: functional jaw reconstruction. Ann Plast Surg 1987;19:538-44. 4. Kido H, Schulz EE, Kumar A, Lozada J, Saha S. Implant diameter and bone density: effect on initial stability and pull-out resistance. J Oral Implantol 1997;23:163-9. 5. Boss JH, Shajrawi I, Mendes DG. The nature of the boneimplant interface. The lessons learned from implant retrieval and analysis in man and experimental animal. Med Prog Technol 1994;20:119-42. 6. Branemark PI. Osseointegration and its experimental background. J Prosthet Dent 1983;50:399-410. 7. Lekholm AV. Branemark system: surgical phase. Presented at the International Symposium on Osseointegrated Dental Implants, Philadelphia, 2 Jun 1988. 8. Branemark PI, Hansson BO, Adell R, Breine U, Lindstrom J, Hallen O, et al. Osseointegrated implants in the treatment of the edentulous jaw. Experience from a 10-year period. Scand J Plast Reconstr Surg Suppl 1977;16:1-132. 9. Linkow LI, Rinaldi AW, Weiss WW Jr, Smith GH. Factors influencing long-term implant success. J Prosthet Dent 1990;63:64-73. 10. Diederichs CG, Engelke WG, Richter B, Hermann KP, Oestmann JW. Must radiation dose for CT of the maxilla and mandible be higher than that for conventional panoramic radiography? Am J Neuroradiol 1996;17:1758-60. 11. Jacobs R, Adriansens A, Naert I, Quirynen M, Hermans R, Van Steenberghe D. Predictability of reformatted computed tomography for pre-operative planning of endosseous implants. Dentomaxillofac Radiol 1999;28:37-41. 12. Becker A, Schneck C, Klesper B, Koebke J. Comparative densitometric of iliac crest and scapula bone in relation to osseous integrated dental implants in microvascular mandibular reconstruction. J Craniomaxillofac Surg 1998;26:75-83. 13. Urken ML, Buchbinder D, Weinberg H, Vickery C, Sheiner A, Biller HF. Primary placement of osseointegrated implants in microvascular mandibular reconstruction. Otolaryngol Head Neck Surg 1989;101:56-73. 14. Frodel JL, Funk GF, Capper DT, Fricrich KL, Blumer JR, Haller JR, et al. Osseointegrated implants: a comparative study of bone thickness in four vascularized bone flaps. Plast Reconstr Surg 1993;92:449-55. 15. Razavi R, Zena RB, Khan Z, Gould AR. Anatomic site evalua-
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tion of edentulous maxillae for dental implant placement. J Prosthodont 1995;4:90-4. Lindh C, Nilsson M, Klinge B, Petersson A. Quantitative computed tomography of trabecular bone in the mandible. Dentomaxillofac Radiol 1996;25:146-50. Valen M, Schulman A. Establishment of an implant selection protocol for predetermined success. J Oral Implantol 1990;16: 166-71. Todd AD, Gher ME, Quintero G, Richardson AC. Interpretation of linear and computed tomograms in the assessment of implant recipient sites. J Periodontol 1993;64:1243-9. Weinberg LA. CT scan as a radiologic data base for optimum implant orientation. J Prosthet Dent 1993;69:381-95. Lindh C, Petersson A, Klinge B, Nilsson M. Trabecular bone volume and bone mineral density in the mandible. Dentomaxillofac Radiol 1997:26;101-6. Quirynen M, Lamoral Y, Dekeyser C, Peene P, van Steenberghe D, Bonte J, et al. CT scan standard reconstruction technique for reliable jaw bone volume determination. Int J Oral Maxillofac Implants 1990;5:384-9. Bass SL, Triplett RG. The effects of preoperative resorption and jaw anatomy on implant success. A report of 303 cases. Clin Oral Implants Res 1991;2:193-8. Jaffin RA, Berman CL. The excessive loss of Branemark fixtures in type IV bone: a 5-year analysis. J Periodontol 1991;62:2-4. Lekhom U, Zarb GA. Patient selection and preparation. In: Branemark P-I, Zarb GA, Albrektsson TA, editors. Tissueintegrated prostheses: osseointegration in clinical dentistry. Chicago: Quintessence; 1985. Blomberg S. Psychological response. In: Branemark P-I, Zarb GA, Albrektsson TA, editors. Tissue-integrated prostheses: osseointegration in clinical dentistry. Chicago: Quintessence; 1985.
26. Graves SL, Jansen CE, Siddiqui AA, Beaty KD. Wide diameter implants: indications, considerations and preliminary results over a two-year period. Aust Prosthodont J 1994;8:31-7. 27. Langer B, Langer L, Herrmann I, Jorneus L. The wide fixture: a solution for special bone situations and a rescue for the compromised implant. Part 1. Int J Oral Maxillofac Implants 1993;8: 400-8. 28. Summers RB. A new concept in maxillary implant surgery: the osteotome technique. Compendium 1994;15:152,1546,158passim;quiz,162. 29. Granick MS, Newton ED, Hanna DC. Scapular free flap for repair of massive lower facial composite defects. Head Neck Surg 1986;8:436-41. 30. Chappard D, Aguado E, Hure G, Grizon F, Basle MF. The early remodeling phases around titanium implants: a histomorphometric assessment of bone quality in a 3- and 6-month study in sheep. Int J Oral Maxillofac Implants 1999;14:18996. 31. Blomqvist JE, Alberius P, Isaksson S, Linde A, Hansson BG. Factors in implant integration failure after bone grafting: an osteometric and endocrinologic matched analysis. Int J Oral Maxillofac Surg 1996;25:63-8.
16. 17. 18. 19. 20. 21.
22. 23. 24.
25.
Reprint requests: Sam-Sun Lee, DDS, MSD, PhD Department of Oral and Maxillofacial Radiology College of Dentistry Seoul National University 28 Yongon-dong, Chongno-gu Seoul, 110-749, Korea [email protected]
CALL FOR REVIEW ARTICLES The January 1993 issue of Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontics contained an Editorial by the Journal’s Editor in Chief, Larry J. Peterson, that called for a Review Article to appear in each issue. These Review Articles should be designed to review the current status of matters that are important to the practitioner. These articles should contain current developments, changing trends, as well as reaffirmation of current techniques and policies. Please consider submitting your article to appear as a Review Article. Information for authors appears in each issue of Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontics. We look forward to hearing from you.
Objective. The aim of this study was to compare the total cancellous bone density, bone-implant interface density, and cortical thickness of 6 donor bone types commonly used in oral and maxillofacial reconstruction.
Methods. A total of 120 bones from 20 Korean adults—including iliac bones, fibulas, cranial bones, scapulas, ribs, and clavicles—were selected. The implant recipient site was determined by the shape, contour, and anatomical limitations of the bones. The serial cross-sectional images of each bone were then acquired through computed tomography. Total cancellous bone density, bone-implant interface density around the imaginary implant fixture, and the cortical thickness along both sides of the imaginary fixture on each cross-sectional image were evaluated and compared. Results. The cancellous bone density of each donor bone type had a statistically significant difference. The cranial bone showed the highest cancellous bone density, followed by the iliac bone, clavicle, scapula, rib, and fibula (P < .05). The boneimplant interface density of the cranial bone, clavicle, fibula, and scapula each belonged to the same Duncan’s group, whereas the rib and iliac bone showed lower bone-implant interface density. In average cortical thickness, the scapula and fibula had a thicker cortex surrounding the imaginary implant than the other bones, and the rib had the thinnest cortex. Conclusion. Although more extensive testing is needed to explain the clinical implications of these results, the findings of this study may help clinicians choose the most appropriate donor bone.
(Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2001;92:23-9)
The prerequisites to a successful functional oral rehabilitation include extensive ablating surgery of the jaw, the restoration of any morphologic defects, and a functionally stable retentive dentition. The reconstruction of jaw bone defects caused by tumor, infection, or trauma is one of the major procedures in the oral and maxillofacial field. Improved reconstructive techniques and osseointegrated dental implants have resulted in better esthetic and functional results.1 Several autogenous bones have been used for oromandibular reconstruction, and previous reports have documented the successful osseointegration of implants placed directly into the donor bone.2,3 The cortical thickness of the donor bone that supports the implant fixture may have a significant effect on the critical factors of osseointegration, including the initial stability of the implant fixture, which is known to be an important factor for achieving Supported in part by 2001 BK21 project for Medicine, Dentistry and Pharmacy. aDepartment of Oral and Maxillofacial Surgery, Dental Research Institute, College of Dentistry, Seoul National University. bDepartment of Oral and Maxillofacial Radiology, Dental Research Institute, College of Dentistry, Seoul National University. Received for publication Nov 24, 2000; returned for revision Dec 8, 2000; accepted for publication Feb 1, 2001. Copyright © 2001 by Mosby, Inc. 1079-2104/2001/$35.00 + 0 7/12/115027 doi:10.1067/moe.2001.115027
good osseointegration.4 The cancellous bone density is also an important factor when one is choosing a more favorable donor bone because it may be responsible for the biologic response and mechanical support of the implant fixture. In particular, the quality of the bone-implant interface may affect the initial stability that is crucial for obtaining osseointegration.5 Accordingly, a presurgical examination of bone quantity and quality may be important for obtaining an accurate estimate of the expected osseointegration. In contrast to the many reports about the relationships between bone quantity and quality and implant success,6-11 there are few studies that report on the quantity and quality of the donor bone.12-14 The quantity and quality of a bone may be evaluated through many methods. The bone quality can be evaluated by histomorphometry,15 quantitative computed tomography (QCT),16 or biomechanic testing.17 When one is planning the implant installation, CT aids in certain functions, such as reformatting, measuring, window setting, and magnification.18,19 Moreover, CT is a noninvasive method for evaluating the cortex and marrow separately.16 Densitometric studies of bones, using CT, have been undertaken,20,21 but the investigations did not consider the implant placement. The aim of the present study was to evaluate bone quality and quantity by simulating the installation of endosseous implants and comparing the total cancellous bone 23
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Table I. Donor bone types and anatomical reference of implantable site
thickness of 2 mm; IQ scanner, Picker International). Three serial images were obtained at a recipient implant site, and each image was displayed with a window width of 2000 Hounsfield units (HU) and a window level of –250 HU. The pixel densities shown in the ROI were determined, and bone density was expressed in Hounsfield units. An ROI was set within the cancellous bone area by 3 oral and maxillofacial radiologists with many years of experience manipulating CT to evaluate the cancellous bone density (Fig 1, A). The cancellous bone density was defined as the mean CT value of pixels involved in the ROI. To evaluate the bone-implant interface density, we superimposed an imaginary implant fixture (10-mm long and 3.75-mm wide) on each cross-sectional image, and 2 oral and maxillofacial surgeons and 2 prosthodontists determined the optimal angulation and direction of the imaginary implant fixture by consensus. Potential complications, including perforation (Fig 1, B), were considered. The oral and maxillofacial surgeons assessed the scans to decide the angulation and direction of the implant fixture, and this was modified according to the biomechanic and esthetic requirements of the prosthodontists. The boneimplant interface density was defined as the mean CT value of a series of 3 pixels surrounding the imaginary fixture (Fig 1, C). The cortical thickness was digitally measured on the image superimposed with the imaginary implant fixture. The vertical length of the cortical area surrounding the imaginary fixture was measured twice along each side of the imaginary fixture, and the mean value was defined as the cortical thickness of the bone. Any differences in cortical thickness and bone density were analyzed with analysis of variance, followed by Duncan’s test (P = .05).
Donor bone type Iliac bone
Fibula Scapula
Cranial bone
Clavicle Rib
Anatomical reference of implantable site From the anterior superior iliac spine (ASIS); 3 implant recipient sites were marked at 2.5-cm intervals. From the central part of a 15-cm-long harvested fibular shaft; 3 implant recipient sites were marked. In the lateral scapular border, a 10-cm-long bony shaft was positioned; 3 implant recipient sites were marked. In the parietotemporal region, a 10 × 10-cm rectangular shape of cranial bone was positioned; 3 implant recipient sites were marked at 2.5-cm intervals. From the center of clavicle shaft; 3 implant recipient sites were marked at 2.5-cm intervals. In the 6th or 7th rib, a 10-cm-long bony shaft; 3 implant recipient sites were chosen randomly and marked.
density, interface bone density, and cortical thickness of 6 donor bone types commonly used in oral and maxillofacial reconstruction.
MATERIAL AND METHODS Bone selection and marking of implant recipient site A total of 120 bones from 20 Korean adults (12 men and 8 women) were selected. The donor bones included iliac bones, fibulas, cranial bones, scapulas, ribs, and clavicles. The material consisted of bones from individuals 41 to 71 years of age (mean age, 57.5 years) who had elected to donate their bodies to medical research. There was no medical history of disease or treatment that might have altered bone metabolism, including systemic osteoporosis. All of the bones were acquired from autopsy specimens and prepared20 at the Department of Oral Anatomy, Seoul National University. Briefly, each body was fixed in formalin by using a mortal perfusion technique. Each bone was removed, degloved, and postfixed in 10% neutralized buffered formalin solution. The anatomical landmarks were checked and the clinical implantable site was determined by donor bone shape, contour, and anatomical limitations, as shown in Table I. Radiopaque marking was done with metal pins, which are too short and thin to produce any artifacts on the region of interest (ROI), to obtain reference points for crosssectional images (Table I). CT examination The cross-sectional images were acquired at each bone site with CT (130 kVp and 20 mAs, with a slice
RESULTS Cancellous bone density The cranial bone showed the highest cancellous bone density (–185.35 ± 131.6), followed by the iliac bone (–559.25 ± 130.8), clavicle (–570.85 ± 243.4), scapula (–587.13 ± 281.7), rib (–708.5 ± 268.5), and fibula (–891.5 ± 320.9) (Fig 2). Each donor bone showed a statistically significant difference in cancellous bone density (P < .05). Bone-implant interface density With respect to bone-implant interface density, the cranial bone (677.9 ± 261.6), clavicle (615.0 ± 219.3), fibula (610.5 ± 258.4), and scapula (582.0 ± 223.0) belonged to the same Duncan’s group, but the rib (181.7 ± 84.5) and iliac bone (–408.6 ± 230.7) showed markedly lower bone-implant interface
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A
B
C Fig 1. A, Schematic drawing of cross-sectional images illustrating that ROI was allocated between cortical (A) and trabecular (B) bone. B, Imaginary implant (10-mm long and 3.75-mm wide) is superimposed on crosssectional image to determine optimal angulation and direction. C, Measurement of bone density between bone and imaginary implant interface.
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Fig 2. Cancellous bone density of respective donor bone types (P < .05).
Fig 3. Bone-implant interface density of respective donor bone types. The bones marked with an asterisk belong to the same Duncan’s group (P < .05).
density (P < .05). In particular, the ilium, which has been used most often in our hospital for bone grafting procedures, had the lowest bone-implant interface density (Fig 3).
Cortical thickness There was significant variation in the average cortical thickness of the implantable site in each bone. The scapula and fibula each had a thicker cortex sur-
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Fig 4. Cortical thickness of respective donor bone types. Bones marked with each symbol (asterisk, dagger) belong to the same Duncan’s group (P < .05).
rounding the imaginary implant than the other bones (average thickness, 3.8 ± 0.95 mm and 3.46 ± 0.96 mm, respectively), and were followed in cortical thickness by the clavicle (2.77 ± 0.7 mm). The cranial bone and iliac bone showed relatively thin cortical thickness (2.22 ± 0.55 mm and 2.39 ± 1.38 mm, respectively), and the rib showed the thinnest cortex (1.81 ± 0.47 mm) (Fig 4).
DISCUSSION In a densitometric study of donor bone, Becker et al12 compared some donor bones with CT images to determine endosseous dental implant sites. Their study showed that the iliac crest was the most consistently implantable donor site, followed by the scapula, fibula, and radius.1 The quality of the bone is often referred to in the implant literature as the amount of cortical and trabecular bone bed in which the recipient socket is drilled.22,23 Lower cancellous bone density may cause compromised osteogenesis or excessive resorption compared with higher density bone, thereby upsetting osseous healing. Clinically, bone quality in the jaw has often been evaluated with the classification described by Lekhom and Zarb.24 Although this classification of bone quality grade is clinically useful, it has 2 critical weaknesses. One is that it is so subjective that the bone quality data may vary according to the observer, and
the other is that it gives only a mean value for the entire arch, so that of the individual site cannot be reported. In addition, it can be used only to evaluate the bone density in the jaw and not in other bones. A standardized index for evaluating the various donor bones was needed. Our data may represent the structural integrity and trabecular pattern in the quantitative scale. A low bone density at the interface site may be relatively unfavorable for osseointegration because the excessive movement of the implant can discourage early bone healing. Micromotion in the osseointegration period can cause an increasing number microstrains that lead to the formation of fibrous tissue at the interface.25 A self-tapping technique and sequential osteotome have been used clinically to increase the bone-implant interface density by compacting the bone at the interface.26-28 Theoretically, implantation in thicker cortical bone may result in improved postoperative immobilization of the dental implant and a higher probability of successful osseointegration. In the present study, the fibula and scapula outranked the other bones with respect to cortical thickness. In situations involving unfavorable bone quality (bone with type IV grade quality, by Lekhom and Zarb24), the initial stability would depend on the marginal cortical bone. Therefore, it could be postulated that the fibula
28 Myoung et al
ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY July 2001
and scapula both had an advantage over the other bones with respect to increased implant surface area engaging cortical bone. The scapula scored a relatively high grade of bone quantity and quality, which was in accordance with a previous study.12 The clavicle and cranial bones have been less commonly used as donor bones for oral and maxillofacial reconstruction. However, as shown in our data, the clavicle and cranial bones showed relatively high cortical thickness, cancellous bone density, and bone-implant interface density. Therefore, the clavicle or cranial bones may be considered as possible donor bones in oromandibular reconstruction. In our study, the fibula had the lowest cancellous bone density of all the studied bones, whereas it scored a relatively high grade in cortical thickness and boneimplant interface density. In our experience, the fibula has been proven successful in oromandibular reconstruction and implant installation. The thick cortex and high implant-bone interface density may explain its favor as a donor bone. The iliac bone is frequently used as a donor bone in oral and maxillofacial reconstruction because it has greater bone quantity and is possible to use during a 2team operation.29 As shown in our results, the boneimplant interface density of the iliac bone was lower than that of the other bones. However, we have obtained good results after the implant fixture was installed in the iliac bone, although the soft cancellous bone predominated in the iliac bones. This can be explained by 2 aspects of bone quality. One is the mechanical property, characterized by initial physical support of the implant fixture, and the other is the biologic aspect, which has a part in the remodeling capacity. The process of osseointegration not only depends on the trabecular structure but also on the presence of viable, living osteocytes in the peri-implant region.1 In an animal experiment, Chappard et al30 demonstrated that the remodeling process appeared to improve bone quality and increase the bone-titanium interface around the implant. The apposition of the neocortical bone on the implant appeared to be achieved quickly by the abundant cancellous bone, which involved an abundance of viable, living osteocytes. This ability could sufficiently compensate for the lower mechanical property at the interface site, although more evidence is needed to confirm this hypothesis. The rib has also been frequently used as a grafting material, primarily due to its relatively easy harvesting procedure. However, the rib showed relatively low grades of bone density and cortical thickness, so it may be unreasonable to use it alone for oromandibular reconstruction.
CONCLUSION Clearly, other factors can be assumed to affect the prognosis of the implant, including patient age, sex, vascularity of the donor bone, and metabolic diseases like osteoporosis.1,31 It is unknown whether the vascularity of the donor bone, age, and sex are related to the long-term survival of the implant. Although our results are independent of these other factors, the results shown here may assist the clinician in choosing the most appropriate donor bone for improved functional oromandibular reconstruction. REFERENCES 1. Moscoso JF, Keller J, Genden E, Weinberg H, Biller HF, Buchbinder D, et al. Vascularized bone flaps in oromandibular reconstruction: a comparative anatomic study of bone stock from various donor sites to assess suitability for endosseous dental implants. Arch Otolaryngol Head Neck Surg 1994;120:36-43. 2. Urken ML, Buchbinder D, Weinberg H, Vickery C, Sheiner A, Parker R, et al. Functional evaluation following microvascular oromandibular reconstruction of the oral cancer patient: a comparative study of reconstructed and nonreconstructed patients. Laryngoscope 1991;101:935-50. 3. Lukash FN, Sachs SA, Fischman B, Attie JN. Osseointegrated denture in a vascularized bone transfer: functional jaw reconstruction. Ann Plast Surg 1987;19:538-44. 4. Kido H, Schulz EE, Kumar A, Lozada J, Saha S. Implant diameter and bone density: effect on initial stability and pull-out resistance. J Oral Implantol 1997;23:163-9. 5. Boss JH, Shajrawi I, Mendes DG. The nature of the boneimplant interface. The lessons learned from implant retrieval and analysis in man and experimental animal. Med Prog Technol 1994;20:119-42. 6. Branemark PI. Osseointegration and its experimental background. J Prosthet Dent 1983;50:399-410. 7. Lekholm AV. Branemark system: surgical phase. Presented at the International Symposium on Osseointegrated Dental Implants, Philadelphia, 2 Jun 1988. 8. Branemark PI, Hansson BO, Adell R, Breine U, Lindstrom J, Hallen O, et al. Osseointegrated implants in the treatment of the edentulous jaw. Experience from a 10-year period. Scand J Plast Reconstr Surg Suppl 1977;16:1-132. 9. Linkow LI, Rinaldi AW, Weiss WW Jr, Smith GH. Factors influencing long-term implant success. J Prosthet Dent 1990;63:64-73. 10. Diederichs CG, Engelke WG, Richter B, Hermann KP, Oestmann JW. Must radiation dose for CT of the maxilla and mandible be higher than that for conventional panoramic radiography? Am J Neuroradiol 1996;17:1758-60. 11. Jacobs R, Adriansens A, Naert I, Quirynen M, Hermans R, Van Steenberghe D. Predictability of reformatted computed tomography for pre-operative planning of endosseous implants. Dentomaxillofac Radiol 1999;28:37-41. 12. Becker A, Schneck C, Klesper B, Koebke J. Comparative densitometric of iliac crest and scapula bone in relation to osseous integrated dental implants in microvascular mandibular reconstruction. J Craniomaxillofac Surg 1998;26:75-83. 13. Urken ML, Buchbinder D, Weinberg H, Vickery C, Sheiner A, Biller HF. Primary placement of osseointegrated implants in microvascular mandibular reconstruction. Otolaryngol Head Neck Surg 1989;101:56-73. 14. Frodel JL, Funk GF, Capper DT, Fricrich KL, Blumer JR, Haller JR, et al. Osseointegrated implants: a comparative study of bone thickness in four vascularized bone flaps. Plast Reconstr Surg 1993;92:449-55. 15. Razavi R, Zena RB, Khan Z, Gould AR. Anatomic site evalua-
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tion of edentulous maxillae for dental implant placement. J Prosthodont 1995;4:90-4. Lindh C, Nilsson M, Klinge B, Petersson A. Quantitative computed tomography of trabecular bone in the mandible. Dentomaxillofac Radiol 1996;25:146-50. Valen M, Schulman A. Establishment of an implant selection protocol for predetermined success. J Oral Implantol 1990;16: 166-71. Todd AD, Gher ME, Quintero G, Richardson AC. Interpretation of linear and computed tomograms in the assessment of implant recipient sites. J Periodontol 1993;64:1243-9. Weinberg LA. CT scan as a radiologic data base for optimum implant orientation. J Prosthet Dent 1993;69:381-95. Lindh C, Petersson A, Klinge B, Nilsson M. Trabecular bone volume and bone mineral density in the mandible. Dentomaxillofac Radiol 1997:26;101-6. Quirynen M, Lamoral Y, Dekeyser C, Peene P, van Steenberghe D, Bonte J, et al. CT scan standard reconstruction technique for reliable jaw bone volume determination. Int J Oral Maxillofac Implants 1990;5:384-9. Bass SL, Triplett RG. The effects of preoperative resorption and jaw anatomy on implant success. A report of 303 cases. Clin Oral Implants Res 1991;2:193-8. Jaffin RA, Berman CL. The excessive loss of Branemark fixtures in type IV bone: a 5-year analysis. J Periodontol 1991;62:2-4. Lekhom U, Zarb GA. Patient selection and preparation. In: Branemark P-I, Zarb GA, Albrektsson TA, editors. Tissueintegrated prostheses: osseointegration in clinical dentistry. Chicago: Quintessence; 1985. Blomberg S. Psychological response. In: Branemark P-I, Zarb GA, Albrektsson TA, editors. Tissue-integrated prostheses: osseointegration in clinical dentistry. Chicago: Quintessence; 1985.
26. Graves SL, Jansen CE, Siddiqui AA, Beaty KD. Wide diameter implants: indications, considerations and preliminary results over a two-year period. Aust Prosthodont J 1994;8:31-7. 27. Langer B, Langer L, Herrmann I, Jorneus L. The wide fixture: a solution for special bone situations and a rescue for the compromised implant. Part 1. Int J Oral Maxillofac Implants 1993;8: 400-8. 28. Summers RB. A new concept in maxillary implant surgery: the osteotome technique. Compendium 1994;15:152,1546,158passim;quiz,162. 29. Granick MS, Newton ED, Hanna DC. Scapular free flap for repair of massive lower facial composite defects. Head Neck Surg 1986;8:436-41. 30. Chappard D, Aguado E, Hure G, Grizon F, Basle MF. The early remodeling phases around titanium implants: a histomorphometric assessment of bone quality in a 3- and 6-month study in sheep. Int J Oral Maxillofac Implants 1999;14:18996. 31. Blomqvist JE, Alberius P, Isaksson S, Linde A, Hansson BG. Factors in implant integration failure after bone grafting: an osteometric and endocrinologic matched analysis. Int J Oral Maxillofac Surg 1996;25:63-8.
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Reprint requests: Sam-Sun Lee, DDS, MSD, PhD Department of Oral and Maxillofacial Radiology College of Dentistry Seoul National University 28 Yongon-dong, Chongno-gu Seoul, 110-749, Korea [email protected]
CALL FOR REVIEW ARTICLES The January 1993 issue of Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontics contained an Editorial by the Journal’s Editor in Chief, Larry J. Peterson, that called for a Review Article to appear in each issue. These Review Articles should be designed to review the current status of matters that are important to the practitioner. These articles should contain current developments, changing trends, as well as reaffirmation of current techniques and policies. Please consider submitting your article to appear as a Review Article. Information for authors appears in each issue of Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontics. We look forward to hearing from you.