Dental Traumatology 2014; 30: 477–483; doi: 10.1111/edt.12111
Bone morphology after delayed tooth replantation – case series CASE REPORT Mitsuhiro Tsukiboshi, Taisuke Tsukiboshi Tsukiboshi Dental Clinic, Aichi, Japan
Key words: replantation; decoronation; ankylosis; bone resorption Correspondence to: Mitsuhiro Tsukiboshi, Tsukiboshi Dental Clinic, 6-8 Gakuto, Kaniechou, Amagun, Aichi 497-0050, Japan Tel.: +81 567 95 6868 Fax: +81 567 95 6666 e-mail: [email protected]
Abstract – The purpose of this report was to describe the morphological changes in the alveolar bone after delayed replantation of avulsed teeth using three dimensional cone-beam computed tomography in 11 during the time period 2003–2012. The radiographic observations revealed the following: Delayed replantation results in ankylosis-related replacement root resorption; the resorption is delayed or arrested around the cervical area superior to the alveolar crest. The buccal bone is reduced in thickness but not the palatal bone. The buccal bone resorption of the alveolar crest progresses approximately to the root canal space of the ankylosed root. Delayed replantation does not completely maintain the bone volume. The buccal profile of alveolar bone in the maxillary anterior region is depending on teeth with viable periodontal ligament.
Accepted 20 February, 2014
Delayed replantation after tooth avulsion describes the situation in which avulsed teeth are replanted after the long periods of dry time periods (>1 h) and is a complication in treatment after dental trauma (1–8). The prognosis of replantation depends on a viable and intact periodontal ligament (PDL) on the root of the avulsed tooth (1–8). An optimally treated avulsed tooth will usually be associated with good alveolar bone support and absence of root resorption. A key point for success is to replant avulsed teeth as soon as possible (8), and if necessary, they can be preserved for a while in appropriate media such as milk, saline, or Hank’s solution (9–17). However, avulsed teeth that are allowed to dry for longer time extraorally will suffer damage to the PDL and undergo ankylosis-related root resorption (also called replacement resorption or osseous replacement), following replantation (8). This ankylosis-related resorption is caused by the loss of viable PDL and progresses rapidly in young patients until the whole root is resorbed and replaced with new bone (18). Tooth avulsion with delayed replantation occurs fairly frequently in children and adolescents, where the individual is still growing and can result in infra-occlusion and inhibition of growth of the alveolar process resulting in esthetic problems (19). In recent years, delayed replantation, however, has been recommended as it has been shown that bone volume may be preserved by leaving the resorbing root in place after removing the tooth crown (decoronation) (20–26). At a later time, when the individual has finished growth, the bone would be suitable for dental implants. Since 2003, one author (MT) has been recording dental trauma situations using cone-beam computed tomography (CBCT) both for diagnosis, treatment planning © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
and follow-up evaluation. The aim of this paper was to describe the long-term changes in morphology of the alveolar bone crest in cases with delayed replantation. Subjects and methods
The material comprises eleven young patients with avulsed teeth replanted by referring dentists after long periods of extra-oral dry time periods were treated during the years 2003–2012. The teeth were observed radiographically with CBCT (3D Accuitomo; J MORITA Mfg Corp, Kyoto, Japan). The voxel size was 0.125; the imaging area was 4 cm by 4 cm; radiation was 80 kV, 4 mA; radiation time was 9 s; equivalent radiation dose was 12 lmSv. Sliced images were taken with 1 mm interval. Patients were followed during 4–10 years. Results
The results of alveolar bone crest resorption of the 11 cases of delayed replantation are summarized in Table 1. Root canal treatment was in general carried out within the first 2 weeks after replantation. In one case, endodontic treatment had been carried out before replantation. All of the cases showed ankylosis-related resorption. Decoronation was performed in three cases, and implants were placed some years after decoronation. In three of the cases, autotransplantation of teeth was performed immediately after the removal of the ankylosis teeth. In one of the cases, an implant was placed 2 months after the removal of the tooth. The rest of the cases were diagnosed with CBCT for the future treatment planning. All of the cases showed reduction in buccal bone volume. However, on the 477
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Table 1. Bone volume changes following 11 cases of delayed replantation with subsequent ankylosis Patient
Age of trauma
Sex
Age of CBCT re-evaluation
Buccal bone reduction
1 2 3 4 5 6 7 8 9 10 11
10 18 14 10 11 8 15 16 16 8 12
M F M M M F M M M F M
20 21 17 14 18 19 26 26 32 13 20
++ + + + ++ ++ ++ ++ + + ++
Palatal bone reduction
Treatment DCN/IMP OBS AT AT OBS DCN/IMP IMP AT OBS OBS DCN/IMP
DCN, decoronation; IMP, implant treatment; AT, autotransplantation of teeth; OBS, observed cases; ++, reduction in bone progressing to the pulp; +, bone reduction where the root structure had remained; , no bone reduction.
palatal side, bone was not reduced. The following cases illustrate the findings. Case 1
A 16-year-old female was referred for treatment after delayed replantation of tooth 21 (#9) 8 years earlier (Fig. 1). The coronal portion of the tooth had broken and been replaced with a temporary crown bonded to adjacent teeth (Fig. 1a). After removing the temporary crown (Fig. 1b), the tooth was examined with a periapical radiograph (Fig. 1c) and CBCT (Fig. 1d,e). When the sagittal images of the both central incisors were compared, it showed that the buccal bone had resorbed extensively along with the root resorption, while no bone resorption was observed on the palatal side. The buccal resorption had progressed to the root canal space. The tooth structure in the cervical area superior to the alveolar crest had not been resorbed. To correct the esthetic problem, decoronation was performed. When the flap was raised, the gutta-percha point was found on the buccal surface of the alveolar bone and was removed. The root was removed to a level 2 mm below the alveolar crest with a high-speed handpiece, Bio-Oss (Geistlich, Princeton, NJ, USA); bone graft material was placed slightly into the pulpal space where the gutta-percha point was first removed and the flap was closed. After 13 months, the healing was observed with CBCT (Fig. 1f–k), and the bone volume around the two central incisors was compared (Fig. 1j,k). There had been some increase in bone volume around the crestal area after decoronation. The volume can be referred to as ‘passive healing bone volume’ (PHBV) (Fig. 1o). Case 2
A boy (12 years 9 months) was referred 1 day after delayed replantation 11 (#8). The pulp canal treatment was performed after 2 weeks, and he was followed for about 4 years (Fig. 2a–d) and examined with CBCT (Fig. 2e–g) before decoronation. The sagittal images of both central incisors were compared, and the same observation as in Case #1 was made: The tooth structure in the cervical area above the alveolar crest had not resorbed completely; along with ankylosis, buccal
bone was reduced but palatal bone was not. The buccal bone resorption progressed approximately to the root canal space, and alveolar bone was composed of TDBV and TIBV (Fig. 2e,f). The patient received a decoronation of the ankylosed tooth (Fig. 2h,i) after which a small amount of Bio-Oss was placed around the crest before closing the flap. Two years after decoronation, the healing was observed using CBCT and PHBV was noted (Fig. 2m). Case 3
A 10-year-old male was referred 2 h after delayed replantation 11 (#8) (Fig. 3a,b). The referring dentist had performed endodontic treatment extra-orally prior to replantation. The case was followed for 5.5 years (Fig. 3c,d) before decoronation. One year after the tooth decoronation, the healing was examined with CBCT (Fig. 3g–i) and the same results were observed as in the previous cases (1, 2). Case 4
An 18-year-old male was referred for evaluation (Fig. 4). Tooth 21 had delayed replantation after avulsion when he was around 11 years old. The CBCT observations matched the findings of the other cases (Fig. 4b,c). Discussion
In the present study of teeth subjected to delayed replantation, bone morphology changed in a different pattern from the current expectation after decoronation procedures, where we have expected the ankylosed root to preserve the alveolar bone volume completely (20, 23, 24, 26). Buccal bone and the ankylosed root were resorbed on the buccal side, while the palatal side of the bone was unaffected. The importance of diagnosis and the risk of radiation of the CBCT were informed to the patients or the mothers of the patients before treatment. The CBCT is routine, and the radiation level with the recent CBCT equipment is not too high compared to conventional periapical film (3 lmSv). Every procedure was performed after informed consent. © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Delayed replantation and bone morphology (a)
(e)
(i)
(m)
(c)
(b)
(d)
(g)
(f)
(k)
(j)
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(h)
(l)
(o)
Fig. 1. A case of delayed replantation. (a) Initial photographs of a 16-year-old female who had a delayed replantation done 8 years earlier. The crown portion had fractured off, and a temporary crown had been bonded to the adjacent teeth. (b) View of the area after the removal of the temporary crown. (c) Periapical radiograph of the remaining root of the replanted tooth. It can be seen that except for the cervical area most of the root has resorbed leaving the root filling in the alveolar bone. (d) CBCT image of the tooth #8 which had not been traumatized. (e) CBCT image of the remains of tooth #9. Note that the buccal bone is missing all the way to the to the pulp canal space while the palatal bone is intact. Root resorption is minimal superior to the alveolar crest. The blue and red mages illustrate what the authors describe as ‘tooth independent bone volume: TIBV’ and ‘tooth dependent bone volume: TDBV.’ The latter (TDBV) refers to the bone volume that is lost after extraction and other loss of teeth, and bone lost following delayed replantation when PDL is not present. TIBV describes the bone volume which is maintained without existence of teeth, and it is congenitally determined. (f–h) 1 year and 10 months after the surgery. Note the labio-palatal alveolar width of the #9 region has been reduced; the gingival level, though, has developed to a fairly normal height. The height of the alveolar crest also seems to have increased radiographically. (i–k) CBCT images 1 year and 10 months after the surgery. Note that only the buccal aspect of the alveolar bone where the root of tooth #9 used to be is missing. TIBV (red area) is maintained, and TDBV (blue area) is absent after the root resorption. (l) A CBCT image before surgery. (m) A CBCT image 1 year and 10 months after the surgery. Note the alveolar crest has increased in height. (n, o) Evaluation of bone increase after the surgery. Passive healing bone volume (PHBV) is observed. PHBV (green area) is the natural bone healing (augmentation) after the extraction of teeth, the expected volume of which will be determined by the bone height and width of the adjacent teeth and in addition may be stimulated by bone graft materials.
There are limitations of this study in that the methodology slightly differs from other decoronation studies (20–24). For example, in our material, we placed © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
xenogenic bone graft in the area in some of the cases. Moreover, our case series is limited in numbers. One should therefore be careful with drawing too far
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(e)
(i)
(c)
(b)
(a)
(f)
(d)
(g)
(j)
(h)
(k)
(l)
(m)
Fig. 2. A case of delayed replantation. (a, b) Photograph and radiograph of a12 years, 9-month-old boy who had a delayed replantation the day before of tooth #8. (c, d) 3 years and 8 months later. The infraocclusion and the root resorption are now more severe. (e, f, g) CBCT images 3 years and 8 months after the delayed replantation. When the images of #8 (g) and #9 (h) are compared, it can be seen that the buccal bone associated with #8 has resorbed. The buccal bone has resorbed to the pulp canal space. TIBV is maintained, and TDVB is lost after the delayed replantation. (h) 1 week after decoronation. (i) Radiograph taken 1 week after decoronation. (j, k) Photographs and radiograph 2 years after decoronation. Note that the width of the crest of bone where decoronation was performed has been reduced. (l) CBCT before decoronation. (m) CBCT 2 years after decoronation. TIBV (red area) is maintained and PHBV (green area) has been augmented by growth of bone.
conclusions from our findings. However, within all the limitations of our study, our findings indicate that: 1 Following ankylosis, buccal bone is reduced while palatal bone is not. 2 Buccal bone resorption progresses approximately to the position of the root canal space. We suggest that alveolar bone loss can be seen as ‘tooth dependent bone volume’ (TDBV) and ‘tooth independent bone volume’ (TIBV). TDBV can be defined as the bone volume that is lost after extraction
of teeth or the loss of viable PDL, for example, after delayed replantation. TIBV can be defined as the bone volume that is maintained with or without teeth, and the morphology may be congenitally determined. TIBV usually consists of bone with bone marrow, whereas TDBV consists of cortical bone. Ankylosis-related root resorption is initiated by osteoclast being attracted to root surface where the PDL is lost or damaged (27–32). The barrier between the root and bone and the viability of the cementoblasts © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Delayed replantation and bone morphology (a)
(d)
(g)
(b)
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(e)
(f)
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Fig. 3. A case of delayed replantation. (a, b) Photograph and radiograph of a 10-year-old boy 3 h after the delayed replantation. The first dentist had completed the root canal treatment prior to replantation. (c, d) 5.5 years postoperative photograph and radiograph. The infra-occlusion and root resorption have advanced. Decoronation was recommended and accepted. (e, f) 1 year after decoronation. A temporary crown had been bonded to the adjacent teeth for esthetic reasons. The radiograph shows the crest of the bone has increased vertically. (g–i) CBCT images 1 year after decoronation. Note the buccal bone has resorbed to the pulp canal space and TIBV is maintained. Also note the increase in vertical height (green outline).
is compromised osteoclasts from the surrounding bone can then invade and resorb the tooth structures. The osteoclasts followed by osteoblasts forming bone and the resorbed areas are gradually replaced by bone. It is interesting that the palatal bone volume or shape did not change even after the root resorption. Normal maxillofacial growth patterns (33) may provide an explanation for the change of the alveolar bone morphology after delayed replantation. This growth pattern consists of three components: bone deposition at bone sutures, bone apposition and remodeling of cortical bone surfaces (resorption and deposition), and tooth eruption. A clinical study has suggested that alveolar bone increases the vertical height along with © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
tooth eruption (34). The growth is very rapid up to the end of puberty and slows thereafter. In the ontogenesis of periodontal tissues around the dental papilla of an immature tooth, three cells (cementoblasts, fibroblasts, osteoblasts) differentiate from cells of the dental follicle by the induction of enamel matrix proteins which are released by Hertwig’s epithelial root sheath (35–38). These three cells create cementum, Sharpey’s fiber, and alveolar bone, respectively. Alveolar bone grows along with tooth eruption. Of interest is the observation that teeth are covered only with thin bundle bone on the buccal aspect after puberty (around the age of 14). If alveolar bone profiles are characterized with two images, there exists thick alveolar
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Fig. 4. A case of delayed replantation. (a–c) Photographs and a radiograph of an 18-year-old male who had just lost the temporary crown that had been bonded to the adjacent teeth to replace missing coronal structure after delayed replantation of tooth #9 around the age of 11 years. (b, c) CBCT images of the teeth involved and the alveolar ridge. The gutta-percha is located on the buccal surface of the bone. The condition is similar to that seen in Figs 1–3.
bone with bone marrow on buccal aspect before puberty and none or little bone marrow after puberty. In other words, roots of anterior teeth are covered and maintained only with alveolar bone proper derived from PDL cells after puberty. These characteristics may be explained by the mechanism of maxillary growth (33). The maxilla increases its height with bone remodeling (resorption and deposition mechanism under the periosteum of cortical bone) (33). It is interesting that the buccal surfaces of alveolar bone in the anterior area have resorption areas programmed congenitally. Teeth will try to erupt in the same direction as the longitudinal line of the teeth and make the maxilla grow in that direction also, but such a remodeling mechanism changes the direction of the growth to a more vertical one. Animal studies in which bone morphology after tooth extraction was examined showed the same tendency of bone resorption with or without graft materials (39–43). But those studies could be criticized for failing to evaluate expected bone volume or biologic aspects of the bone formation and resorption more carefully. Socket preservation techniques have been developed and recommended in implant therapy (44– 46). But the buccal bone may be reduced eventually, and the bone reduction will be arrested at the TIBV. The buccal profile of alveolar bone in the anterior region will be determined by the position of teeth with viable PDL if the tooth is located out of TIBV. The ability of periodontal ligament to preserve bone has been shown after transplantation where the periodontal ligament is preserved (47). On the contrary, the bone profile will be determined by TIBV if the tooth is located within TIBV or the tooth is extracted. For example, in implant therapy, an implant will be covered with new bone when it is placed within TIBV. However, we do not know the long-term effects on the alveolar bone morphology after dental implant treatment. With the increased use of CBCT, we may have more knowledge this field in the future. As is shown in Table 1, decoronation was performed when the patients were around 15 years of age. The gutta-percha was removed, and the root was shortened to a level 2 mm below the alveolar crest, and the pulpal space was filled with bone graft materials. Decoronation
is aiming at preserving the alveolar bone and to correct esthetic problems with infra-occlusion. The results of the present study indicate that the preservation of the buccal alveolar bone crest may be questionable over time. However, the palatal side of the alveolar bone crest does not seem to change. We believe that delayed replantation and decoronation are still worthwhile as patients can maintain function and esthetics and some bone preservation (19–26). However, the long-term effects on the buccal alveolar bone preservation need to be further investigated. With the introduction of CBCT, it will be possible to do long-term follow-up studies of the alveolar bone after delayed replantation and decoronation. Conclusions
Delayed replantation causes ankylosis and replacement of the root by bone. Buccal bone is reduced over time, but palatal bone is not reduced to the same extent. Future prospective long-term follow-up studies with the use of CBCT should be encouraged to better understand the changes in bone morphology. Acknowledgements
The authors express appreciation to Dr. Leif K. Bakland and the Ronald E. Buell, Professor of Endodontics at Loma Linda University, for his advice and assistance in preparation of this manuscript. References 1. Soder PO, Otteskog P, Andreasen JO, Modeer T. The effect of drying on the viability of the periodontal membrane. Scand J Dent Res 1977;85:164–8. 2. Andreasen JO. A time related study of periodontal healing and root resorption activity after replantation of mature permanent incisors in monkeys. Swed Dent J 1980;4:101–10. 3. Oswald RJ, Harrington GW, Van Hassel HJ. A post replantation evaluation of air-dried and saliva-stored avulsed teeth. J Endod 1980;6:546–51. 4. Andreasen JO. Effect of extra-alveolar period and storage media upon periodontal and pulpal healing after replantation of mature permanent incisors in monkeys. Int J Oral Surg 1981;1:43–53. © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Delayed replantation and bone morphology 5. Andreasen JO. Periodontal healing after replantation and autotransplantation of incisors in monkeys. Int J Oral Surg 1981;10:54–61. 6. Andersson L, Bodin I, Sorensen S. Progression of root resorption following replantation of human teeth after extended extraoral storage. Endod Dent Traumatol 1989;5:38–47. 7. Trope M, Friedman S. Periodontal healing of replanted dog teeth stored in Viaspan, milk and Hank’s balanced salt solution. Endod Dent Traumatol 1992;8:183–8. 8. Andreasen JO, Borum MK, Jacobsen HL, Andreasen FM. Replantation of 400 avulsed permanent incisors.4. Factors related to periodontal ligament healing. Endod Dent Traumatol 1995;11:76–89. 9. Patil S, Dumsha TC, Sydiskis RJ. Determining periodontal ligament (PDL) cell vitality from exarticulated teeth stored in saline or milk using fluorescein diacetate. Int Endod J 1994;27:1–5. 10. Lindskog S, Blomlof L. Influence of osmolality and composition of some storage media on human periodontal ligament cells. Acta Odontol Scand 1982;40:435–41. 11. Courts FJ, Mueller WA, Tabeling HJ. Milk as an interim storage medium for avulsed teeth. Pediatr Dent 1983;5:183–6. 12. Blomlof L, Otteskog P. Viability of human periodontal ligament cells after storage in milk or saliva. Scand J Dent Res 1980;88:436–40. 13. Blomlof L, Lindskog S, Andersson S, Hedstrom KG, Hammarstrom L. Storage of experimentally avulsed teeth in milk prior to replantation. J Dent Res 1983;62:912–6. 14. Blomlof L, Lindskog S, Hammarstrom L. Periodontal healing of exarticulated monkey teeth stored in milk or saliva. Scand J Dent Res 1981;89:251–9. 15. Blomlof L. Milk and saliva as possible storage media for traumatically exarticulated teeth prior to replantation. Swed Dent J Suppl 1981;8:1–26. 16. Blomlof L, Lindskog S, Hedstrom KG, Hammarstrom L. Vitality of periodontal ligament cells after storage of monkey teeth in milk or saliva. Scand J Dent Res 1980;88:441–5. 17. Hiltz J, Trope M. Vitality of human lip fibroblasts in milk, Hank’s balanced salt solution and Viaspan storage media. Endod Dent Traumatol 1991;7:69–72. 18. Andreasen JO. Review of root resorption systems and models. Etiology of root resorption and the homeostatic mechanisms of the periodontal ligament. The biological mechanisms of tooth eruption and root resorption. Birmingham: EBSCO Media; 1988. p. 9–21. 19. Andreasen JO, Andreasen FM. Textbook and color atlas of traumatic injuries to the teeth, 3rd edn. Copenhagen: Munksgaard; 1994. p. 383–425, 691–717. 20. Malmgren B, Cvek M, Lundberg M, Frykholm A. Surgical treatment of ankylosed and infrapositioned reimplanted incisors in adolescents. Scand J Dent Res 1984;92:391–9. 21. Malmgren B. Decoronation: how, why, and when? J Calif Dent Assoc 2000;28:846–54. 22. Filippi A, Pohl Y, von Arx T. Decoronation of an ankylosed tooth for preservation of alveolar bone prior to implant placement. Dent Traumatol 2001;17:93–5. 23. Malmgren O, Malmgren B. Rate of infraposition of reimplanted ankylosed incisors related to age and growth in children and adolescents. Dent Traumatol 2002;18:28–36. 24. Cohenca N, Stabholz A. Decoronation - a conservative method to treat ankylosed teeth for preservation of alveolar ridge prior to permanent prosthetic reconstruction: literature review and case presentation. Dent Traumatol 2007;23:87–94. 25. Day PF, Kindelan SA, Spencer JR, Kindelan JD, Duggal MS. Dental trauma: part 2. Managing poor prognosis anterior teeth - treatment options for the subsequent space in a growing patient. J Orthod 2008;35:143–55. 26. Sapir S, Shapira J. Decoronation for the management of an ankylosed young permanent tooth. Dent Traumatol 2008; 24:131–5. © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
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27. Andersson L, Jonsson BG, Hammarstrom L, Blomlof L, Andreasen JO, Lindskog S. Evaluation of statistics and desirable experimental design of a histomorphometrical method for studies of root resorption. Endod Dent Traumatol 1987;3: 288–95. 28. Andreasen JO. Experimental dental traumatology: development of a model for external root resorption. Endod Dent Traumatol 1987;3:269–87. 29. Wesselink P, Beertsen W. Initiating factors in dental root resorption. The biological mechanisms of tooth eruption and root resorption. Birmingham: EBSCO Media; 1988. p. 329–34. 30. Boyde A, Ali NN, Jones SJ. Resorption of dentine by isolated osteoclasts in vitro. Br Dent J 1984;156:216–20. 31. Jone SJ, Boyde A. The resorption of dentine and cementum in vivo and vitro. The biological mechanisms of tooth eruption and root resorption. Birmingham: EBSCO Media; 1988. p. 335–54. 32. Lindskog SF, Dreyer CW, Pierce AM, Torabinejad M, Shabahang S. Steoclast activity. Textbook and color atlas of traumatic injuries to the teeth, 4th edn. Oxford: Blackwell; 2007. p. 137–71. 33. Enlow DH. Handbook of facial growth. Philadelphia: W.B.Saunders Company; 1975. p. 10–146. 34. Iseri H, Solow B. Growth displacement of the maxilla in girls studied by the implant method. Tandlaegebladet 1991;95: 839–46. 35. MacNeil RL, Thomas HF. Development of the murine periodontium. I. Role of basement membrane in formation of a mineralized tissue on the developing root dentin surface. J Periodontol 1993;64:95–102. 36. Ten Cate AR. The role of epithelium in the development, structure and function of the tissues of tooth support. Oral Dis 1996;2:55–62. 37. Hammarstrom L. Enamel matrix, cementum development and regeneration. J Clin Periodontol 1997;24:658–68. 38. Cho MI, Garant PR. Development and general structure of the periodontium. Periodontol 2000 2000;24:9–27. 39. Araujo MG, Lindhe J. Dimensional ridge alterations following tooth extraction. An experimental study in the dog. J Clin Periodontol 2005;32:212–8. 40. Araujo M, Linder E, Wennstrom J, Lindhe J. The influence of Bio-Oss collagen on healing of an extraction socket: an experimental study in the dog. Int J Periodontics Restorative Dent 2008;28:123–35. 41. Araujo MG, Lindhe J. Ridge preservation with the use of Bio-Oss collagen: a 6-month study in the dog. Clin Oral Implants Res 2009;20:433–40. 42. Araujo MG, Liljenberg B, Lindhe J. Dynamics of Bio-Oss Collagen incorporation in fresh extraction wounds: an experimental study in the dog. Clin Oral Implants Res 2010;21: 55–64. 43. Araujo MG, Lindhe J. Socket grafting with the use of autologous bone: an experimental study in the dog. Clin Oral Implants Res 2011;22:9–13. 44. Nevins M, Camelo M, De Paoli S, Friedland B, Schenk RK, Parma-Benfenati S et al. A study of the fate of the buccal wall of extraction sockets of teeth with prominent roots. Int J Periodontics Restorative Dent 2006;26:19–29. 45. Schropp L, Wenzel A, Kostopoulos L, Karring T. Bone healing and soft tissue contour changes following single-tooth extraction: a clinical and radiographic 12-month prospective study. Int J Periodontics Restorative Dent 2003;23:313–23. 46. Ten Heggeler JMAG, Slot DE, Van der Weijden GA. Effect of socket preservation therapies following tooth extraction in non-molar regions in humans: a systematic review. Clin Oral Implants Res 2011;22:779–88. 47. Andreasen JO. Atlas of replantation and transplantation of teeth. Philadelphia: Saunders; 1992. p. 15–222.
Bone morphology after delayed tooth replantation – case series CASE REPORT Mitsuhiro Tsukiboshi, Taisuke Tsukiboshi Tsukiboshi Dental Clinic, Aichi, Japan
Key words: replantation; decoronation; ankylosis; bone resorption Correspondence to: Mitsuhiro Tsukiboshi, Tsukiboshi Dental Clinic, 6-8 Gakuto, Kaniechou, Amagun, Aichi 497-0050, Japan Tel.: +81 567 95 6868 Fax: +81 567 95 6666 e-mail: [email protected]
Abstract – The purpose of this report was to describe the morphological changes in the alveolar bone after delayed replantation of avulsed teeth using three dimensional cone-beam computed tomography in 11 during the time period 2003–2012. The radiographic observations revealed the following: Delayed replantation results in ankylosis-related replacement root resorption; the resorption is delayed or arrested around the cervical area superior to the alveolar crest. The buccal bone is reduced in thickness but not the palatal bone. The buccal bone resorption of the alveolar crest progresses approximately to the root canal space of the ankylosed root. Delayed replantation does not completely maintain the bone volume. The buccal profile of alveolar bone in the maxillary anterior region is depending on teeth with viable periodontal ligament.
Accepted 20 February, 2014
Delayed replantation after tooth avulsion describes the situation in which avulsed teeth are replanted after the long periods of dry time periods (>1 h) and is a complication in treatment after dental trauma (1–8). The prognosis of replantation depends on a viable and intact periodontal ligament (PDL) on the root of the avulsed tooth (1–8). An optimally treated avulsed tooth will usually be associated with good alveolar bone support and absence of root resorption. A key point for success is to replant avulsed teeth as soon as possible (8), and if necessary, they can be preserved for a while in appropriate media such as milk, saline, or Hank’s solution (9–17). However, avulsed teeth that are allowed to dry for longer time extraorally will suffer damage to the PDL and undergo ankylosis-related root resorption (also called replacement resorption or osseous replacement), following replantation (8). This ankylosis-related resorption is caused by the loss of viable PDL and progresses rapidly in young patients until the whole root is resorbed and replaced with new bone (18). Tooth avulsion with delayed replantation occurs fairly frequently in children and adolescents, where the individual is still growing and can result in infra-occlusion and inhibition of growth of the alveolar process resulting in esthetic problems (19). In recent years, delayed replantation, however, has been recommended as it has been shown that bone volume may be preserved by leaving the resorbing root in place after removing the tooth crown (decoronation) (20–26). At a later time, when the individual has finished growth, the bone would be suitable for dental implants. Since 2003, one author (MT) has been recording dental trauma situations using cone-beam computed tomography (CBCT) both for diagnosis, treatment planning © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
and follow-up evaluation. The aim of this paper was to describe the long-term changes in morphology of the alveolar bone crest in cases with delayed replantation. Subjects and methods
The material comprises eleven young patients with avulsed teeth replanted by referring dentists after long periods of extra-oral dry time periods were treated during the years 2003–2012. The teeth were observed radiographically with CBCT (3D Accuitomo; J MORITA Mfg Corp, Kyoto, Japan). The voxel size was 0.125; the imaging area was 4 cm by 4 cm; radiation was 80 kV, 4 mA; radiation time was 9 s; equivalent radiation dose was 12 lmSv. Sliced images were taken with 1 mm interval. Patients were followed during 4–10 years. Results
The results of alveolar bone crest resorption of the 11 cases of delayed replantation are summarized in Table 1. Root canal treatment was in general carried out within the first 2 weeks after replantation. In one case, endodontic treatment had been carried out before replantation. All of the cases showed ankylosis-related resorption. Decoronation was performed in three cases, and implants were placed some years after decoronation. In three of the cases, autotransplantation of teeth was performed immediately after the removal of the ankylosis teeth. In one of the cases, an implant was placed 2 months after the removal of the tooth. The rest of the cases were diagnosed with CBCT for the future treatment planning. All of the cases showed reduction in buccal bone volume. However, on the 477
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Table 1. Bone volume changes following 11 cases of delayed replantation with subsequent ankylosis Patient
Age of trauma
Sex
Age of CBCT re-evaluation
Buccal bone reduction
1 2 3 4 5 6 7 8 9 10 11
10 18 14 10 11 8 15 16 16 8 12
M F M M M F M M M F M
20 21 17 14 18 19 26 26 32 13 20
++ + + + ++ ++ ++ ++ + + ++
Palatal bone reduction
Treatment DCN/IMP OBS AT AT OBS DCN/IMP IMP AT OBS OBS DCN/IMP
DCN, decoronation; IMP, implant treatment; AT, autotransplantation of teeth; OBS, observed cases; ++, reduction in bone progressing to the pulp; +, bone reduction where the root structure had remained; , no bone reduction.
palatal side, bone was not reduced. The following cases illustrate the findings. Case 1
A 16-year-old female was referred for treatment after delayed replantation of tooth 21 (#9) 8 years earlier (Fig. 1). The coronal portion of the tooth had broken and been replaced with a temporary crown bonded to adjacent teeth (Fig. 1a). After removing the temporary crown (Fig. 1b), the tooth was examined with a periapical radiograph (Fig. 1c) and CBCT (Fig. 1d,e). When the sagittal images of the both central incisors were compared, it showed that the buccal bone had resorbed extensively along with the root resorption, while no bone resorption was observed on the palatal side. The buccal resorption had progressed to the root canal space. The tooth structure in the cervical area superior to the alveolar crest had not been resorbed. To correct the esthetic problem, decoronation was performed. When the flap was raised, the gutta-percha point was found on the buccal surface of the alveolar bone and was removed. The root was removed to a level 2 mm below the alveolar crest with a high-speed handpiece, Bio-Oss (Geistlich, Princeton, NJ, USA); bone graft material was placed slightly into the pulpal space where the gutta-percha point was first removed and the flap was closed. After 13 months, the healing was observed with CBCT (Fig. 1f–k), and the bone volume around the two central incisors was compared (Fig. 1j,k). There had been some increase in bone volume around the crestal area after decoronation. The volume can be referred to as ‘passive healing bone volume’ (PHBV) (Fig. 1o). Case 2
A boy (12 years 9 months) was referred 1 day after delayed replantation 11 (#8). The pulp canal treatment was performed after 2 weeks, and he was followed for about 4 years (Fig. 2a–d) and examined with CBCT (Fig. 2e–g) before decoronation. The sagittal images of both central incisors were compared, and the same observation as in Case #1 was made: The tooth structure in the cervical area above the alveolar crest had not resorbed completely; along with ankylosis, buccal
bone was reduced but palatal bone was not. The buccal bone resorption progressed approximately to the root canal space, and alveolar bone was composed of TDBV and TIBV (Fig. 2e,f). The patient received a decoronation of the ankylosed tooth (Fig. 2h,i) after which a small amount of Bio-Oss was placed around the crest before closing the flap. Two years after decoronation, the healing was observed using CBCT and PHBV was noted (Fig. 2m). Case 3
A 10-year-old male was referred 2 h after delayed replantation 11 (#8) (Fig. 3a,b). The referring dentist had performed endodontic treatment extra-orally prior to replantation. The case was followed for 5.5 years (Fig. 3c,d) before decoronation. One year after the tooth decoronation, the healing was examined with CBCT (Fig. 3g–i) and the same results were observed as in the previous cases (1, 2). Case 4
An 18-year-old male was referred for evaluation (Fig. 4). Tooth 21 had delayed replantation after avulsion when he was around 11 years old. The CBCT observations matched the findings of the other cases (Fig. 4b,c). Discussion
In the present study of teeth subjected to delayed replantation, bone morphology changed in a different pattern from the current expectation after decoronation procedures, where we have expected the ankylosed root to preserve the alveolar bone volume completely (20, 23, 24, 26). Buccal bone and the ankylosed root were resorbed on the buccal side, while the palatal side of the bone was unaffected. The importance of diagnosis and the risk of radiation of the CBCT were informed to the patients or the mothers of the patients before treatment. The CBCT is routine, and the radiation level with the recent CBCT equipment is not too high compared to conventional periapical film (3 lmSv). Every procedure was performed after informed consent. © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Delayed replantation and bone morphology (a)
(e)
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(m)
(c)
(b)
(d)
(g)
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(j)
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Fig. 1. A case of delayed replantation. (a) Initial photographs of a 16-year-old female who had a delayed replantation done 8 years earlier. The crown portion had fractured off, and a temporary crown had been bonded to the adjacent teeth. (b) View of the area after the removal of the temporary crown. (c) Periapical radiograph of the remaining root of the replanted tooth. It can be seen that except for the cervical area most of the root has resorbed leaving the root filling in the alveolar bone. (d) CBCT image of the tooth #8 which had not been traumatized. (e) CBCT image of the remains of tooth #9. Note that the buccal bone is missing all the way to the to the pulp canal space while the palatal bone is intact. Root resorption is minimal superior to the alveolar crest. The blue and red mages illustrate what the authors describe as ‘tooth independent bone volume: TIBV’ and ‘tooth dependent bone volume: TDBV.’ The latter (TDBV) refers to the bone volume that is lost after extraction and other loss of teeth, and bone lost following delayed replantation when PDL is not present. TIBV describes the bone volume which is maintained without existence of teeth, and it is congenitally determined. (f–h) 1 year and 10 months after the surgery. Note the labio-palatal alveolar width of the #9 region has been reduced; the gingival level, though, has developed to a fairly normal height. The height of the alveolar crest also seems to have increased radiographically. (i–k) CBCT images 1 year and 10 months after the surgery. Note that only the buccal aspect of the alveolar bone where the root of tooth #9 used to be is missing. TIBV (red area) is maintained, and TDBV (blue area) is absent after the root resorption. (l) A CBCT image before surgery. (m) A CBCT image 1 year and 10 months after the surgery. Note the alveolar crest has increased in height. (n, o) Evaluation of bone increase after the surgery. Passive healing bone volume (PHBV) is observed. PHBV (green area) is the natural bone healing (augmentation) after the extraction of teeth, the expected volume of which will be determined by the bone height and width of the adjacent teeth and in addition may be stimulated by bone graft materials.
There are limitations of this study in that the methodology slightly differs from other decoronation studies (20–24). For example, in our material, we placed © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
xenogenic bone graft in the area in some of the cases. Moreover, our case series is limited in numbers. One should therefore be careful with drawing too far
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(e)
(i)
(c)
(b)
(a)
(f)
(d)
(g)
(j)
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(k)
(l)
(m)
Fig. 2. A case of delayed replantation. (a, b) Photograph and radiograph of a12 years, 9-month-old boy who had a delayed replantation the day before of tooth #8. (c, d) 3 years and 8 months later. The infraocclusion and the root resorption are now more severe. (e, f, g) CBCT images 3 years and 8 months after the delayed replantation. When the images of #8 (g) and #9 (h) are compared, it can be seen that the buccal bone associated with #8 has resorbed. The buccal bone has resorbed to the pulp canal space. TIBV is maintained, and TDVB is lost after the delayed replantation. (h) 1 week after decoronation. (i) Radiograph taken 1 week after decoronation. (j, k) Photographs and radiograph 2 years after decoronation. Note that the width of the crest of bone where decoronation was performed has been reduced. (l) CBCT before decoronation. (m) CBCT 2 years after decoronation. TIBV (red area) is maintained and PHBV (green area) has been augmented by growth of bone.
conclusions from our findings. However, within all the limitations of our study, our findings indicate that: 1 Following ankylosis, buccal bone is reduced while palatal bone is not. 2 Buccal bone resorption progresses approximately to the position of the root canal space. We suggest that alveolar bone loss can be seen as ‘tooth dependent bone volume’ (TDBV) and ‘tooth independent bone volume’ (TIBV). TDBV can be defined as the bone volume that is lost after extraction
of teeth or the loss of viable PDL, for example, after delayed replantation. TIBV can be defined as the bone volume that is maintained with or without teeth, and the morphology may be congenitally determined. TIBV usually consists of bone with bone marrow, whereas TDBV consists of cortical bone. Ankylosis-related root resorption is initiated by osteoclast being attracted to root surface where the PDL is lost or damaged (27–32). The barrier between the root and bone and the viability of the cementoblasts © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Delayed replantation and bone morphology (a)
(d)
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Fig. 3. A case of delayed replantation. (a, b) Photograph and radiograph of a 10-year-old boy 3 h after the delayed replantation. The first dentist had completed the root canal treatment prior to replantation. (c, d) 5.5 years postoperative photograph and radiograph. The infra-occlusion and root resorption have advanced. Decoronation was recommended and accepted. (e, f) 1 year after decoronation. A temporary crown had been bonded to the adjacent teeth for esthetic reasons. The radiograph shows the crest of the bone has increased vertically. (g–i) CBCT images 1 year after decoronation. Note the buccal bone has resorbed to the pulp canal space and TIBV is maintained. Also note the increase in vertical height (green outline).
is compromised osteoclasts from the surrounding bone can then invade and resorb the tooth structures. The osteoclasts followed by osteoblasts forming bone and the resorbed areas are gradually replaced by bone. It is interesting that the palatal bone volume or shape did not change even after the root resorption. Normal maxillofacial growth patterns (33) may provide an explanation for the change of the alveolar bone morphology after delayed replantation. This growth pattern consists of three components: bone deposition at bone sutures, bone apposition and remodeling of cortical bone surfaces (resorption and deposition), and tooth eruption. A clinical study has suggested that alveolar bone increases the vertical height along with © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
tooth eruption (34). The growth is very rapid up to the end of puberty and slows thereafter. In the ontogenesis of periodontal tissues around the dental papilla of an immature tooth, three cells (cementoblasts, fibroblasts, osteoblasts) differentiate from cells of the dental follicle by the induction of enamel matrix proteins which are released by Hertwig’s epithelial root sheath (35–38). These three cells create cementum, Sharpey’s fiber, and alveolar bone, respectively. Alveolar bone grows along with tooth eruption. Of interest is the observation that teeth are covered only with thin bundle bone on the buccal aspect after puberty (around the age of 14). If alveolar bone profiles are characterized with two images, there exists thick alveolar
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Fig. 4. A case of delayed replantation. (a–c) Photographs and a radiograph of an 18-year-old male who had just lost the temporary crown that had been bonded to the adjacent teeth to replace missing coronal structure after delayed replantation of tooth #9 around the age of 11 years. (b, c) CBCT images of the teeth involved and the alveolar ridge. The gutta-percha is located on the buccal surface of the bone. The condition is similar to that seen in Figs 1–3.
bone with bone marrow on buccal aspect before puberty and none or little bone marrow after puberty. In other words, roots of anterior teeth are covered and maintained only with alveolar bone proper derived from PDL cells after puberty. These characteristics may be explained by the mechanism of maxillary growth (33). The maxilla increases its height with bone remodeling (resorption and deposition mechanism under the periosteum of cortical bone) (33). It is interesting that the buccal surfaces of alveolar bone in the anterior area have resorption areas programmed congenitally. Teeth will try to erupt in the same direction as the longitudinal line of the teeth and make the maxilla grow in that direction also, but such a remodeling mechanism changes the direction of the growth to a more vertical one. Animal studies in which bone morphology after tooth extraction was examined showed the same tendency of bone resorption with or without graft materials (39–43). But those studies could be criticized for failing to evaluate expected bone volume or biologic aspects of the bone formation and resorption more carefully. Socket preservation techniques have been developed and recommended in implant therapy (44– 46). But the buccal bone may be reduced eventually, and the bone reduction will be arrested at the TIBV. The buccal profile of alveolar bone in the anterior region will be determined by the position of teeth with viable PDL if the tooth is located out of TIBV. The ability of periodontal ligament to preserve bone has been shown after transplantation where the periodontal ligament is preserved (47). On the contrary, the bone profile will be determined by TIBV if the tooth is located within TIBV or the tooth is extracted. For example, in implant therapy, an implant will be covered with new bone when it is placed within TIBV. However, we do not know the long-term effects on the alveolar bone morphology after dental implant treatment. With the increased use of CBCT, we may have more knowledge this field in the future. As is shown in Table 1, decoronation was performed when the patients were around 15 years of age. The gutta-percha was removed, and the root was shortened to a level 2 mm below the alveolar crest, and the pulpal space was filled with bone graft materials. Decoronation
is aiming at preserving the alveolar bone and to correct esthetic problems with infra-occlusion. The results of the present study indicate that the preservation of the buccal alveolar bone crest may be questionable over time. However, the palatal side of the alveolar bone crest does not seem to change. We believe that delayed replantation and decoronation are still worthwhile as patients can maintain function and esthetics and some bone preservation (19–26). However, the long-term effects on the buccal alveolar bone preservation need to be further investigated. With the introduction of CBCT, it will be possible to do long-term follow-up studies of the alveolar bone after delayed replantation and decoronation. Conclusions
Delayed replantation causes ankylosis and replacement of the root by bone. Buccal bone is reduced over time, but palatal bone is not reduced to the same extent. Future prospective long-term follow-up studies with the use of CBCT should be encouraged to better understand the changes in bone morphology. Acknowledgements
The authors express appreciation to Dr. Leif K. Bakland and the Ronald E. Buell, Professor of Endodontics at Loma Linda University, for his advice and assistance in preparation of this manuscript. References 1. Soder PO, Otteskog P, Andreasen JO, Modeer T. The effect of drying on the viability of the periodontal membrane. Scand J Dent Res 1977;85:164–8. 2. Andreasen JO. A time related study of periodontal healing and root resorption activity after replantation of mature permanent incisors in monkeys. Swed Dent J 1980;4:101–10. 3. Oswald RJ, Harrington GW, Van Hassel HJ. A post replantation evaluation of air-dried and saliva-stored avulsed teeth. J Endod 1980;6:546–51. 4. Andreasen JO. Effect of extra-alveolar period and storage media upon periodontal and pulpal healing after replantation of mature permanent incisors in monkeys. Int J Oral Surg 1981;1:43–53. © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
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