Distraction osteogenesis of the alveolar ridge: a review of the literature

SAULACIC N, GÁNDARA-VILA P, SOMOZA-MARTÍN M, GARCÍA-GARCÍA A. DISTRACTION OSTEOGENESIS OF THE ALVEOLAR RIDGE: A REVIEW OF THE LITERATURE. MED ORAL 2004;9:321-7.

SUMMARY

One of the principal problems in dental implantation is the lack of sufficient bone height or width. In the case of the alveolar ridge, a very effective technique for resolving this problem is distraction osteogenesis, introduced in this context about a decade ago. This technique is based on the gradual separation of a mobile but fully vascularized bone segment from the basal bone, leading to the formation of an intervening soft callus which gradually transforms to mature bone. A key researcher in the development of this technique was the Russian traumatologist Ilizarov. The present article reviews alveolar ridge distraction procedures and their clinical application. Alveolar ridge distraction may often be preferable to bone grafting or guided bone regeneration for increasing ridge height and width prior to implantation.

Key words: Alveolar ridge augmentation, distraction osteogenesis, osteointegration.

INTRODUCTION

Lack of sufficient maxillary bone height or width is one of the most frequent problems in dental implantation. Causes of bone loss include periodontal disease and other pathological processes, trauma, and congenital deformities. Insufficient alveolar ridge height (i.e. in the apico-coronal direction) impedes the use of implants of sufficient length, giving a inadequate crown-to-implant length ratio. Frieberg et al. (1) have demonstrated that short implants fail more frequently than longer implants.

Techniques are currently available that permit placement of long implants without reducing the vertical dimension of the crown, such as the use of pterigoid implants (2), augmentation of the floor of the maxillary sinus (3), and dental nerve transposition (4). Other techniques that can be used to modify crown-to-implant length ratio include autologous alveolar ridge bone grafts (5), guided bone regeneration (GBR) (6) and distraction osteogenesis (7), all of which increase ridge height and thus permit the use of longer implants and shorter crowns.

Bone grafting has disadvantages including the need for secondary surgery, difficulties in the management of soft tissues, morbidity of the donor bed, and unpredictable absorption, particularly during the months prior to implant placement (8). The terms “volume maintenance” and “persistence” are widely used to describe graft performance, but should perhaps be replaced by “survival”, since in fact less than 2% of bone graft cells survive the transplant (9). Marx et al. (10) suggest that autologous grafts are resorbed physiologically by a remodelling mechanism as a result of contraction of adjacent soft tissues.

The principal limitations of GBR are the impossibility of achieving primary stability during implant placement, the possibility of infection of the bone surface, and the need for a long recovery period (6 - 12 months) during which provisional prostheses cannot be used (11).

DISTRACTION OSTEOGENESIS

Basic strategies for tissue engineering include 1) introduction of new cells (i.e. grafting), 2) reconstruction using biomaterials, and 3) the application of physical or chemical stimuli to induce tissue regeneration (12). Distraction osteogenesis techniques fall into this latter category, and have revolutionized tissue engineering in orthopaedics. Distraction osteogenesis is based on callotasis (from the Latin tasis = stretching), the gradual stretching of the reparative callus that forms around bone segments interrupted by osteotomy or fracture. This stretching process is gradual, allowing maintenance of blood flow (13). The bone regeneration involves two processes: osteogenesis (callus formation and generation of new bone) and histiogenesis (lengthening of the soft tissue, i.e. mucoperiosteum, nerves and blood vessels) (14,15). Clinically, the procedure comprises three periods: 1) latency, 2) distraction, and 3) consolidation.

The first experimental studies of epiphyseal bone distraction were reported in 1869 by Berhard von Langenbeck (16). The first clinical application of mandibular distraction was reported in 1927 by Rosenthal (17). Several authors subsequently criticized the technique in view of the numerous complications arising in these early years (18). In 1973, Snyder performed the first distraction of membranous mandibular bone (19). However, the full development of the technique is due to Gabriel Abramowitch Ilizarov, who in the 1950s performed numerous experiments in dogs and greatly advanced the clinical utility of this technique. Ilizarov established the basic biological principles of distraction osteogenesis: 1) the influence of tension-stress on osteogenesis and tissue growth, and 2) the influence of blood supply and mechanical load on the shape of the newly formed bone (14,15).

The application of distraction osteogenesis in membranous bones has greatly expanded our toolkit for reconstructive procedures in the craniofacial complex. Distraction of the mandibular symphysis was first performed by Guerrero et al. (20) in 1990. In 1992, McCarthy et al. reported results obtained by distraction in patients with craniofacial deformities (21). Subsequently, many authors have reported successful mandibular (22,23) and maxillary (24,25) lengthening, in patients with various disorders including hereditary cleft palate (26,27). To prevent the formation of extraoral scars (28), intraoral distractors began to be used. Distraction osteogenesis has been shown to be useful for the treatment of alveolar fissures (29-31), transverse expansion of the palate (32,33), and expansion of the cranial sutures (34,35).

DISTRACTION OSTEOGENESIS OF THE ALVEOLAR RIDGE

Recently, distraction osteogenesis has become established as a technique for alveolar ridge augmentation (ARA). Various authors (36-38) have evaluated the potential of distraction osteogenesis for ARA in animal experiments. Chin & Toth (7) and Hidding et al. (39) were the first to report clinical use of distraction osteogenesis for ARA. The technique involves freeing a bone segment (the transport segment) from the basal bone, but retaining attachment via the lingual periosteum. The available distractors can be classified as juxtaosseous and intraosseous. Juxtaosseous distractors are placed on the buccal face of the maxillary bone (39). Intraosseous distractors run through the transport segment in the direction of distraction (40). Gaggl et al. (41) have described a simplified technique for ARA using “distraction implants”, which do not require subsequent removal. However, this technique may increase the risk of bacterial infection at or near the implant site as a result of movement of the implant-bone interface during healing (42).

Complications that may arise during alveolar distraction have been classified by us (43) into three groups: 1) problems arising during surgery, generally related to osteotomy and distractor placement; 2) complications arising during distraction, including incorrect direction of distraction and soft-tissue complications; and 3) complications arising after distraction, due to defective bone formation. Uckan et al. (44) reported bleeding in cases of deep osteotomy, and pain and significant resorption of the distracted fragment in distractions of more than 10 mm. Klug et al. (45), Gaggl et al. (46) and Nocini et al. (47) have described other complications, including dysesthesia of the mental nerve and mandibular fracture.

Although there are not yet established protocols for alveolar bone distraction, different authors have recommended a latency period of 5 - 7 days (48), a distraction rate of 0.5 - 1 mm/day (49), and a consolidation period of 8 - 12 weeks (50). So-called “immediate distraction” has shown promising results in dogs (51), but should probably be avoided in view of the possibility of dehiscence formation and the exposure of the newly formed bone to the oral environment (40). According to the results obtained by Robiony et al. (52) and Horiuchi et al. (53), the optimal rate for horizontal alveolar distraction is probably about 0.5 mm/day. Meyer et al. (49) have demonstrated that in fact the magnitude of force applied is more important than its frequency of application. The minimum and maximum force inducing activation and continued function of the cells contributing to osteogenesis is not accurately known. The tension-stress effect (i.e. biological stress due to the mechanical tension exerted by the stretching process) leads to changes at both cellular and subcellular level (54). The stretching process appears to affect the local-scale regulation of bone formation, increasing the expression of bone growth factors, although prostaglandin E2 levels remain constant (55). During distraction and over the 20 days of consolidation, there is a marked increase in the levels of fibroblast growth factor (FGF) (56) and growth factor b1 (TGFb1) (57). The fibrous tissue of the soft callus, as well as the capillary blood vessels and primary osteoid, are oriented longitudinally, in the direction of distraction (58). Cope et al. (59) found that cartilage makes up about 2 - 3% of distracted membranous bone, in line with the results of Aronson et al. (60) in long bones.

Implants are generally placed about 8 - 12 weeks after distraction (42, 61). The period between the 4th and 6th week is very important for mineralization (62), and in line with this it may be acceptable in some cases to place implants after only 6 weeks. In dogs, one study found that the distraction gap heals within 5 weeks (63), i.e. within the critical period for humans. However, another study found osteointegration of implants placed a mere 3 weeks after distraction (64).

Osteointegration of implants in distracted bone appears to take place in a similar way to osteointegration in native bone. Experimental studies by Block et al. (63) indicated that when implants are well fixed in the distracted bone and basal bone, they survive as long as implants in native bone; though note that implants were only monitored for a year in this study. Gaggl et al. (50) found that 65% of the surface of the distractor implants was osteointegrated 6 months after distraction. In the most extensive study published to date, Jensen et al. (42) reported loss of 8 of 84 implants in the anterior maxillary; these 8 implants were complex distraction cases. Gaggl et al. (46) and Uckan et al. (44) have both reported failures of implants placed in distracted bone. However, most authors consider implantation following distraction to be a highly effective and useful technique (43,65,66,67,68). Chiapasco et al. (61) studied 26 implants placed in distracted bone and loaded for 12 - 18 months, and found that vertical bone loss on the mesial and distal faces was similar to that reported for implants placed in native bone.

FUTURE DIRECTIONS

Robiony et al. (52) achieved sufficient vertical augmentation of class-V and -VI mandibles for implant placement using a novel distraction osteogenesis technique involving the introduction of bone particles and platelet-rich plasma. In severe mandibular atrophy of this type, centrifugal blood supply becomes centripetal, due to loss of teeth and periodont. During the distraction period, local progenitor cells undergo proliferation and differentiation to osteoblasts, which require good vascularization. Thus Robiony et al.'s method, which aims to enhance vascularization, may be useful.

Doubts about the minimum ridge height requirement for distraction osteogenesis were clarified by Schmidt et al. (69), who performed periosteal distraction experiments in rabbits. The method proved successful but certainly requires further evaluation.

The joint use of bone grafts and distraction osteogenesis for major reconstructions still requires detailed investigation. Cho et al. (70) consider that distraction can be commenced within 4 months of grafting. Buis et al. (71) placed a distractor implant one year after grafting, in a patient with unilateral complete cleft palate. Other studies have applied mandibular distraction after implantation of vascularized scapular grafts (72), costochondral grafts (73) or vascularized fibular grafts (74-78). Aparicio and Jensen (79) were the first to report the clinical use of horizontal alveolar distraction, using a free segment in the external mandibular wall. Three implants were fitted in this study, and after 2 years about 1.5 mm of marginal bone around the central implant had been lost. In view of the difficulty of access to and maintenance of the screws, these authors suggest that distraction distance in horizontal distractions should be no more than 3 - 6 mm. Nosaka et al. (80) performed horizontal alveolar distraction of free bone segments in dogs, observing resorption of the transport segment that did not affect osteointegration of the implant. Watzek et al. (81) described a new method in which, after osteointegration, the bone block containing the implant can be moved in any direction. Bavitz et al. (82) attempted periodont regeneration by distraction, but were only able to generate small amounts of cement, not new bone.

In conclusion, and despite the relatively small number of patients studied to date and the relatively short periods for which implants have been monitored, distraction osteogenesis appears to be a reliable technique for alveolar ridge augmentation, reducing both postoperative morbidity and the length of the recovery period. Distraction osteogenesis appears to be at least as reliable as guided bone regeneration and bone grafting as a method for augmenting insufficient height of edentulous ridges (61). It enables bone formation between the transport segment and the basal segment in a relatively short period of time. Since there is no need to obtain bone from elsewhere, surgery time and postoperative morbidity are evidently reduced. Generally only local anaesthesia is required, again reducing postoperative morbidity. The regenerated bone appears to be highly resistant to resorption, is capable of supporting heavy functional loads, and enables the placement of implants with good aesthetics. Most complications arising during distraction osteogenesis can be considered minor, and are readily resolved.

During the last decade, our understanding of the biological basis and clinical potential of distraction osteogenesis has increased dramatically, in parallel with advances in our understanding of the function, aesthetics and stability of the teeth, facial bones and soft tissues. Many apparently revolutionary surgical techniques have subsequently proved to be problematic, or indeed detrimental to patient health (83): by contrast, our ongoing experience with distraction osteogenesis is very positive, and strongly suggests that this technique is here to stay (84). In the future, it seems likely that distraction osteogenesis may replace guided bone regeneration and bone grafting for alveolar ridge augmentation. Detailed studies will no doubt lead to improvements in methodology, making this a reliable procedure offering good functional outcome, good aesthetic outcome, and long-term stability.

REFERENCES

1. Friberg B, Jemt T, Lekholm U. Early failures in 4,641 consecutively placed Branemark dental implants: a study from stage 1 surgery to the connection of completed prostheses. Int J Oral Maxillofac Implants 1991;6:142-6.        [ Links ]

2. Krekmanov L, Kahn M, Rangert B, Lindstrom H. Tilting of posterior mandibular and maxillary implants for improved prosthesis support. Int J Oral Maxillofac Implants 2000;15:405-14.        [ Links ]

3. Lorenzetti M, Mozzati M, Campanino PP, Valente G. Bone augmentation of the inferior floor of the maxillary sinus with autogenous bone or composite bone grafts: a histologic-istomorphometric preliminary report. Int J Oral Maxillofac Implants 1998;13:69-76.        [ Links ]

4. Jensen J, Reiche-Fischel O, Sindet-Pedersen S. Nerve transposition and implant placement in the atrophic posterior mandibular alveolar ridge. J Oral Maxillofac Surg 1994;52:662-8.        [ Links ]

5. Triplett RG, Schow SR. Autologous bone grafts and endosseous implants: complementary techniques. J Oral Maxillofac Surg 1996;54:486-94.        [ Links ]

6. Tinti C, Parma-Benfenati S. Vertical ridge augmentation: surgical protocol and retrospective evaluation of 48 consecutively inserted implants. Int J Periodontics Restorative Dent 1998;18:434-43.        [ Links ]

7. Chin M, Toth BA. Distraction osteogenesis in maxillofacial surgery using internal devices: review of five cases. J Oral Maxillofac Surg 1996;54:45-53.        [ Links ]

8. Lundgren S, Rasmusson L, Sjostrom M, Sennerby L. Simultaneous or delayed placement of titanium implants in free autogenous iliac bone grafts. Histological analysis of the bone graft-titanium interface in 10 consecutive patients. Int J Oral Maxillofac Surg 1999;28:31-7.        [ Links ]

9. Zins JE. Discussion. En: Chen NT, Glowacki J, Bucky LP, Hong HZ, Kim WK, Yaremchuk MJ: The roles of revascularization and resorption on endurance of craniofacial onlay bone grafts in the rabbit. Plast Reconstr Surg 1994;93: 714-22.        [ Links ]

10. Marx RE, Shellenberger T, Wimsatt J, Correa P. Severely resorbed mandible: predictable reconstruction with soft tissue matrix expansion (tent pole) grafts. J Oral Maxillofac Surg 2002;60:878-88.        [ Links ]

11. Simion M, Jovanovic SA, Tinti C, Benfenati SP. Long-term evaluation of osseointegrated implants inserted at the time or after vertical ridge augmentation. A retrospective study on 123 implants with 1-5 year follow-up. Clin Oral Implants Res 2001;12:35-45.        [ Links ]

12. Bertolami CN. Principles of Tissue Engineering. J Oral Maxillofac Surg 1998;56:24.        [ Links ]

13. Yasui N, Kojimoto H, Shimizu H, Shimomura Y. The effect of distraction upon bone, muscle, and periosteum. Orthop Clin North Am 1991;22:563-7.        [ Links ]

14. Ilizarov GA. The tension-stress effect on the genesis and growth of tissues. Part I. The influence of stability of fixation and soft-tissue preservation. Clin Orthop 1989;238:249-81.        [ Links ]

15. Ilizarov GA. The tension-stress effect on the genesis and growth of tissues: Part II. The influence of the rate and frequency of distraction. Clin Orthop 1989;239:263-85.        [ Links ]

16. Von Langebeck B. Ueber krankhaftes Längenwachsthum der Röhrenknochen und seine Verwerthung für die chirurgische Praxis. Berl Klin Wochenschr 1869; 26:265.        [ Links ]

17. Sonntag E, Rosenthal W eds. Lehrbuch der Mund- und Kieferchirurgie. Leipzig: Georg Thieme; 1930. p. 173-5.        [ Links ]

18. Abbott LC. The operative lengthening of the tibia and fibula. J Bone Joint Surg 1927;9:128-52.        [ Links ]

19. Snyder CC, Levine GA, Swanson HM, Browne EZ Jr. Mandibular lengthening by gradual distraction. Preliminary report. Plast Reconstr Surg 1973; 51:506-8.         [ Links ]

20. Guerrero C. Rapid mandibular expansion. Rev Venez Ortod 1990;48:1-2.        [ Links ]

21. McCarthy JG, Schreiber J, Karp N, Thorne CH, Grayson BH. Lengthening the human mandible by gradual distraction. Plast Reconstr Surg 1992;89:1-8; discussion 9-10.        [ Links ]

22. Diner PA, Kollar EM, Martinez H, Vazquez MP. Intraoral distraction for mandibular lengthening: a technical innovation. J Craniomaxillofac Surg 1996; 24:92-5.        [ Links ]

23. Guerrero CA, Bell WH, Contasti GI, Rodriguez AM. Mandibular widening by intraoral distraction osteogenesis. Br J Oral Maxillofac Surg 1997;35:383-92.        [ Links ]

24. Chin M, Toth BA. Le Fort III advancement with gradual distraction using internal devices. Plast Reconstr Surg 1997;100:819-30;831-2.        [ Links ]

25. Carls FR, Sailer HF. Seven years of clinical experience with mandibular distraction in children. J Craniomaxillofac Surg 1998;26:197-208.        [ Links ]

26. Molina F, Ortiz Monasterio F, de la Paz Aguilar M, Barrera J. Maxillary distraction: aesthetic and functional benefits in cleft lip-palate and prognathic patients during mixed dentition. Plast Reconstr Surg 1998;101:951-63.         [ Links ]

27. Polley JW, Figueroa AA. Rigid external distraction: its application in cleft maxillary deformities. Plast Reconstr Surg 1998; 102: 1360-72;1373-4.        [ Links ]

28. Mofid MM, Manson PN, Robertson BC, Tufaro AP, Elias JJ, Vander Kolk CA. Craniofacial distraction osteogenesis: a review of 3278 cases. Plast Reconstr Surg 2001; 108: 1103-14;1115-7.        [ Links ]

29. Liou EJ, Chen PK, Huang CS, Chen YR. Interdental distraction osteogenesis and rapid orthodontic tooth movement: a novel approach to approximate a wide alveolar cleft or bony defect. Plast Reconstr Surg 2000;105:1262-72.        [ Links ]

30. Yen SL, Gross J, Wang P, Yamashita DD. Closure of a large alveolar cleft by bony transport of a posterior segment using orthodontic archwires attached to bone: report of a case. J Oral Maxillofac Surg 2001;59:688-91.         [ Links ]

31. Henkel KO, Ma L, Lenz JH, Jonas L, Gundlach KK. Closure of vertical alveolar bone defects with guided horizontal distraction osteogenesis: an experimental study in pigs and first clinical results. J Craniomaxillofac Surg 2001; 29:249-53.        [ Links ]

32. Mommaerts MY. Transpalatal distraction as a method of maxillary expansion. Br J Oral Maxillofac Surg 1999;37:268-72.        [ Links ]

33. Pinto PX, Mommaerts MY, Wreakes G, Jacobs WV. Immediate postexpansion changes following the use of the transpalatal distractor. J Oral Maxillofac Surg 2001;59:994-1000;1001.        [ Links ]

34. Persing JA, Morgan EP, Cronin AJ, Wolcott WP. Skull base expansion: craniofacial effects. Plast Reconstr Surg 1991;87:1028-33.        [ Links ]

35. Sasaki A, Sugiyama H, Tanaka E, Sugiyama M. Effects of sutural distraction osteogenesis applied to rat maxillary complex on craniofacial growth. J Oral Maxillofac Surg 2002; 60: 667-75.        [ Links ]

36. Nishimura T, Jinbo M, Ikeda H, Sasaki M, Nara J, Toriyabe Y. Study on ridge audmentation by callus distraction (callotasis). Jpn J Oral Maxillofac Surg 1992;38:1357-63.        [ Links ]

37. Block MS, Chang A, Crawford C. Mandibular alveolar ridge augmentation in the dog using distraction osteogenesis. J Oral Maxillofac Surg 1996;54: 309-14.        [ Links ]

38. Oda T, Sawaki Y, Ueda M. Alveolar ridge augmentation by distraction osteogenesis using titanium implants: an experimental study. Int J Oral Maxillofac Surg 1999;28:151-6.        [ Links ]

39. Hidding J, Lazar F, Zoller JE. The vertical distraction osteogenesis of the alveolar bone. J Craniomaxillofac Surg 1998;26:72-3.        [ Links ]

40. Chin M. Distraction osteogenesis for dental implants. Atlas Oral Maxillofac Surg Clin North Am 1999;7:41-63.         [ Links ]

41. Gaggl A, Schultes G, Karcher H. Distraction implants: a new operative technique for alveolar ridge augmentation. J Craniomaxillofac Surg 1999;27: 214-21.        [ Links ]

42. Jensen OT, Cockrell R, Kuhike L, Reed C. Anterior maxillary alveolar distraction osteogenesis: a prospective 5-year clinical study. Int J Oral Maxillofac Implants 2002;17:52-68.        [ Links ]

43. García AG, Martín MS, Vila PG, Maceiras JL. Minor complications arising in alveolar distraction osteogenesis. J Oral Maxillofac Surg 2002;60:496-501.        [ Links ]

44. Uckan S, Dolanmaz D, Kalayci A, Cilasun U. Distraction osteogenesis of basal mandibular bone for reconstruction of the alveolar ridge. Br J Oral Maxillofac Surg 2002;40:393-6.        [ Links ]

45. Klug C, Millesi G, Millesi W, Schopper C, Ewers R. Vertical callus distraction for mandibular augmentation: L-shaped osteotomy and GBR by titanium membranes. J Craniomaxillofac Surg 2000;28:55.        [ Links ]

46. Gaggl A, Schultes G, Kärcher H. Distraction implants in alveolar ridge augmentation: a 2-year follow-up. J Craniomaxillofac Surg 2000; 28:101.        [ Links ]

47. Nocini PF, Wangerin K, Cortelazzi R, Kretschmer W, Albanese M. Distraction osteogenesis in preposthetic surgery. J Craniomaxillofac Surg 2000; 28:100.        [ Links ]

48. Burchardt H. The biology of bone graft repair. Clin Orthop 1983;174:28-42.        [ Links ]

49. Meyer U, Meyer T, Wiesmann HP, Stratmann U, Kruse-Losler B, Maas H et al. The effect of magnitude and frequency of interfragmentary strain on the tissue response to distraction osteogenesis. J Oral Maxillofac Surg 1999; 57: 1331-9;1340-1.        [ Links ]

50. Gaggl A, Schultes G, Regauer S, Karcher H. Healing process after alveolar ridge distraction in sheep. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000;90:420-9.         [ Links ]

51. Tavakoli K, Walsh WR, Bonar F, Smart R, Wulf S, Poole MD. The role of latency in mandibular osteodistraction. J Craniomaxillofac Surg 1998;26:209-19.        [ Links ]

52. Robiony M, Polini F, Costa F, Politi M. Osteogenesis distraction and platelet-rich plasma for bone restoration of the severely atrophic mandible: preliminary results. J Oral Maxillofac Surg 2002;60:630-5.        [ Links ]

53. Horiuchi K, Uchida H, Yamamoto K, Hatano N. Anteroinferior distraction of the atrophic subtotal maxillary alveolus for implant placement: a case report. Int J Oral Maxillofac Implants 2002;17:416-23.        [ Links ]

54. Holbein O, Neidlinger-Wilke C, Suger G, Kinzl L, Claes L. Ilizarov callus distraction produces systemic bone cell mitogens. J Orthop Res 1995;13:629-38.        [ Links ]

55. Meyer U, Meyer T, Schlegel W, Scholz H, Joos U. Tissue differentiation and cytokine synthesis during strain-related bone formation in distraction osteogenesis. Br J Oral Maxillofac Surg 2001;39:22-9.        [ Links ]

56. Tavakoli K, Yu Y, Shahidi S, Bonar F, Walsh WR, Poole MD. Expression of growth factors in the mandibular distraction zone: a sheep study. Br J Plast Surg 1999;52:434-9.        [ Links ]

57. Mehrara BJ, Rowe NM, Steinbrech DS, Dudziak ME, Saadeh PB, McCarthy JG et al. Rat mandibular distraction osteogenesis: II. Molecular analysis of transforming growing factor beta – 1 and osteocalcin gene expression. Plast reconstr Surg 1999;103:536-47.        [ Links ]

58. Yasui N, Kojimoto H, Sasaki K, Kitada A, Shimizu H, Shimomura Y. Factors affecting callus distraction in limb lengthening. Clin Orthop 1993;293:55-60.        [ Links ]

59. Cope JB, Samchukov ML. Regenerate bone formation and remodeling du-ring mandibular osteodistraction. Angle Orthod 2000;70:99-111.        [ Links ]

60. Aronson J, Harrison BH, Stewart CL, Harp JH Jr. The histology of distraction osteogenesis using different external fixators. Clin Orthop 1989;241:106-16.        [ Links ]

61. Chiapasco M, Romeo E, Vogel G. Vertical distraction osteogenesis of eden-tulous ridges for improvement of oral implant positioning: a clinical report of preliminary results. Int J Oral Maxillofac Implants 2001;16:43-51.        [ Links ]

62. Smith SW, Sachdeva RC, Cope JB. Evaluation of the consolidation period during osteodistraction using computed tomography. Am J Orthod Dentofacial Orthop 1999;116:254-63.        [ Links ]

63. Block MS, Gardiner D, Almerico B, Neal C. Loaded hydroxylapatite-coated implants and uncoated titanium-threaded implants in distracted dog alveolar ridges. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000;89:676-85.        [ Links ]

64. Nosaka Y, Tsunokuma M, Hayashi H, Kakudo K. Placement of implants in distraction osteogenesis: a pilot study in dogs. Int J Oral Maxillofac Implants 2000;15:185-92.        [ Links ]

65. McAllister BS. Histologic and radiographic evidence of vertical ridge augmentation utilizing distraction osteogenesis: 10 consecutively placed distractors. J Periodontol 2001;72:1767-79.        [ Links ]

66. Lehrhaupt NB. Alveolar distraction: a possible new alternative to bone grafting. Int J Periodontics Restorative Dent 2001;21:121-5.        [ Links ]

67. Gaggl A, Schultes G, Rainer H, Karcher H. The transgingival approach for placement of distraction implants. J Oral Maxillofac Surg 2002;60:793-6.        [ Links ]

68. García García A, Somoza Martin M, Gandara Vila P, Lopez Maceiras J. Alveolar ridge osteogenesis using 2 intraosseous distractors: uniform and nonuniform distraction. J Oral Maxillofac Surg 2002;60:1510-2.        [ Links ]

69. Schmidt BL, Kung L, Jones C, Casap N. Induced osteogenesis by periosteal distraction. J Oral Maxillofac Surg 2002;60:1170-5.        [ Links ]

70. Cho BC, Seo MS, Baik BS. Distraction osteogenesis after membranous bone onlay grafting in a dog model. J Oral Maxillofac Surg 2001; 59: 1025-33.        [ Links ]

71. Buis J, Rousseau P, Soupre V, Martinez H, Antoine Diner P, Paule Vazquez M. “Distraction” of Grafted Alveolar Bone in Cleft Case Using Endosseous Implant. Cleft Palate Craniofac J 2001;38:405-9.        [ Links ]

72. Polley JW, Breckler GL, Ramasastry S, Figueroa AA, Cohen M. Simultaneous distraction osteogenesis and microsurgical reconstruction for facial asymmetry. J Craniofac Surg 1996;7:469-72.        [ Links ]

73. Corcoran J, Hubli EH, Salyer KE. Distraction osteogenesis of costochondral neomandibles: a clinical experience. Plast Reconstr Surg 1997;100:311-5;316-7.        [ Links ]

74. Friedrich RE, Hellner D, Plambeck K, Schmelzle R. Application of B-scan ultrasonography for analysis of callus distraction in vascularized fibular grafts of the mandible: a report of three patients. J Oral Maxillofac Surg 1997;55: 635-40.        [ Links ]

75. Yonehara Y, Takato T, Harii K, Hirabayashi S, Susami T, Komori T, et al. Secondary lengthening of the reconstructed mandible using a gradual distraction technique—two case reports. Br J Plast Surg 1998;51:356-8.        [ Links ]

76. Nocini PF, Wangerin K, Albanese M, Kretschmer W, Cortelazzi R. Vertical distraction of a free vascularized fibula flap in a reconstructed hemimandible: case report. J Craniomaxillofac Surg 2000;28:20-4.        [ Links ]

77. Chiapasco M, Brusati R, Galioto S. Distraction osteogenesis of a fibular revascularized flap for improvement of oral implant positioning in a tumor patient: a case report. J Oral Maxillofac Surg 2000;58:1434-40.        [ Links ]

78. Klesper B, Lazar F, Siessegger M, Hidding J, Zoller JE. Vertical distraction osteogenesis of fibula transplants for mandibular reconstruction—a preliminary study. J Craniomaxillofac Surg 2002;30:280-5.        [ Links ]

79. Aparicio C, Jensen OT. Alveolar ridge widening by distraction osteogenesis: a case report. Pract Proced Aesthet Dent 2001;13:663-8.        [ Links ]

80. Nosaka Y, Kitano S, Wada K, Komori T. Endosseous implants in horizontal alveolar ridge distraction osteogenesis. Int J Oral Maxillofac Implants 2002; 17:846-53.        [ Links ]

81. Watzek G, Zechner W, Crismani A, Zauza K. A distraction abutment system for 3-dimensional distraction osteogenesis of the alveolar process: technical note. Int J Oral Maxillofac Implants 2000;15:731-7.        [ Links ]

82. Bavitz JB, Payne JB, Dunning D, Glenn A, Koka R. The use of distraction osteogenesis to induce new suprabony periodontal attachment in the beagle dog. Int J Periodontics Restorative Dent 2000;20:596-603.         [ Links ]

83. Booth RP. Reflections on distraction osteogenesis. A surgical distraction or the ‘future’? Br J Oral Maxillofac Surg 2001;39:179-80.         [ Links ]

84. Reyneke JP. Reflections on: distraction osteogenesis. Distraction osteogenesis—the future? Br J Oral Maxillofac Surg 2001;39:180-1.         [ Links ]