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AUTOTRANSPLANTATION OF TEETH IN ORTHODONTICS: A BIOLOGICAL METHOD TO SUBSTITUTE MISSING OR LOST TEETH AND ALVEOLAR BONE H. U. Paulsen Autotransplantation of teeth is an old method of tooth replacement, but it is receiving renewed interest, as treatment today is founded on evidencebased, long-term research. Autotransplantation of premolars has become a reliable treatment option for the treatment of certain orthodontic problems (Slagsvold and Bjercke, 1967, 1970. 1974, 1978a,b; Ravn and Nielsen, 1973; Northway and Konigsberg, 1980; Andreasen, 1981; Kristerson, 1985; Paulsen and Andreasen, 1985, 1990, 1998; Lagerstrom and Kristerson, 1986; Andreasen et al., 1988, 1989, 1999a,b,c,d; Paulsen, 1989, 1999, 2001; Kristerson and Kristerson, 1991; Paulsen and Zachrisson, 1992, Kugelbrg et al., 1994; Paulsen et al., 1995, 2001; Josefsson et al., 1999; Czochrowska et al., 2000a,b). Autotransplantation of incisors, canines and molars are not always as successful due to the more complex severity of the surgical problems during transplantation (Nordenram, 1963; Moss 1968, 1975; Oksala and Kallioniemi, 1977; Berglund et al., 1996; Akiyama et al., 1998; Guthua et al., 1994; Bauss et al., 2002; Gleiser and Jaramillo, 2002; Ioannidou and Makris, 2003). In conventional orthodontics, tooth movements usually are limited to minor distances. However, tooth movement is no longer limited to short distances in a quadrant of the dental arch if tooth transplantation is included as an orthodontic treatment choice. There is greater freedom to place a tooth exactly where it is needed, may it be the contralateral side in the dental arch or the opposing jaw. The periodontium is the key to bone induction and bone modelling in the recipient area. A transplanted tooth can erupt typically and in a similar manner to a contralateral, non-transplanted tooth in its normal area (Paulsen and Andreasen, 1998; Paulsen 1999). However, transplantation of teeth is far more traumatic to the pulp and periodontium than conventional orthodontics. Donor teeth with wide-open apices and with a single root canal are recommended as grafts of choice for long-term survival (Kristerson, 1985; Andreasen et al., 1990b; Paulsen, 1999). The surgical procedure is thus an essential key to the successful outcome of this treatment (Andreasen et al., 1990a). As imaginative as this technique appears to be, very careful case selection and graft choice is necessary to safeguard the health of the soft tissues; i.e. the pulp, the periodontal ligament with 2-3 mm marginal gingiva, and Hertwig´s epithelial root sheath. The technique of premolar transplantation has been described in a series of articles in which the predictors for optimal pulp and periodontal healing, as well as root growth have been described (Andreasen 1981, 1988; 1 Autotransplantation of Teeth Andreasen et al., 1999a,b,c,d). The survival of transplanted premolars has been studied postoperatively for more than 25 years. Orthodontists, however, generally would be the most competent professionals to identify available donor teeth (Northway and Konigsberg, 1980; Paulsen, 1999). Because overall occlusal status must be assessed, the orthodontist should be considered a key person in planning, referring, and coordinating treatment that includes transplantation (Stenvik, 2003). With autotransplantation, it has become possible to move problems in the dental arches to regions where they are easier to solve orthodontically. TREATMENT PLANNING A comprehensive treatment plan needs to be developed prior to autotransplantation. This requires the expertise of the orthodontist, surgeon, periodontist and the restorative dentist. The orthodontist particularly needs to be aware of the patient’s craniofacial morphology and growth tendencies in order to better predict success. A radiographic screening process has been a very useful method of diagnosing premolar agenesis around 9 to 11 years-of-age when there are no erupted premolars (Ravn and Nielsen, 1973; Rolling, 1980). Unfortunately, new restrictions on the use of radiographic screening exposures of a population have stopped this procedure in Scandinavia. However, agenesis also may be diagnosed from radiographs taken during diagnostic procedures for carries of deciduous molars or a late exfoliation of deciduous molars. Furthermore, a new long-term study of agenesis of permanent teeth has indicated a different aetiology and treatment of the deciduous molars. Autotransplantation should be included in the treatment planning for patients who have deciduous molars with agenesis of permanent successors showing surface root resorption or replacement root resorption (ankylosis) over a period of time (Paulsen, 1999). Non-extraction Cases: Agenesis in the Lower Jaw In samples of Danish school children, Rølling found the rate of agencies of lower premolars to be 7.8% (Ravn and Nielsen, 1973; Rolling, 1980). The most frequently missing teeth were the lower second premolars, representing 67% of congenitally missing teeth. Combined with the most frequently occurring mandibular growth pattern (the anterior rotational type; Bjork and Skieller, 1972), this deviation may pose two distinct problems to the clinician. First, where incisal support remains favourable, the mandibular incisors gradually become more proclined in relation to the mandibular base. This generally requires space closure through protraction of the posterior dentition, which is very challenging. Should incisal support fail due to distal 2 Paulsen tipping of the mandibular incisors, a deep bite and increased overjet will result. Second, conventional orthodontic treatment usually consists of a combination of mesial movement of the molars into the site of the agenesis and realignment of anterior teeth. Such treatment often is difficult to perform satisfactorily in patients with a weak and concave profile (Paulsen and Zachrisson 1992). Autotransplantation of second premolars from the maxilla to the affected or converted regions in the mandible shifts the burden of closing space to the maxillary arch. Generally speaking, space closure in the maxilla is much easier to control and carry out. Extraction Cases: Primary Crowding Orthodontic treatment of these types of malocclusions can include a wider donor selection of premolars. Generally, all single-rooted premolars with a wide-open apex may be candidates for transplantation. Premolars from the mandible fit very well in the recipient anterior region of the maxilla (i.e. first mandibular premolars as maxillary laterals, and second mandibular premolars as maxillary centrals). The dove-tailing of transplantation and orthodontic treatment, together with cryopreservation of extracted teeth for later purposes and restoring avulsed areas in the dental arches, provides a novel approach to the management of tooth loss in the anterior region of the maxilla. Autotransplantation of a premolar to the affected region diminishes the severity of the problem, allowing conventional orthodontic treatment approaches to manage the extraction site created (Paulsen et al., 1990). Alternative Treatment Other treatment modalities, including the use of implants, are available to this group of patients. The optimal treatment approach mandates a realistic evaluation of the long-term prognosis of the various treatment methods and cost (Paulsen et al., 1995). In the following section, a summary of the results of our long-term studies on autotransplantation is presented. MATERIALS AND METHODS We evaluated 370 autotransplanted premolars (Andreasen et al., 1999a,b,c,d) from 16 to 26 years post transplantation. All transplantation’s were performed at the Department of Oral Surgery and Oral Medicine, University Hospital, Copenhagen. All treatment planning, controlling, and follow-up for healing and stability was performed at the Department of Orthodontics, Copenhagen Municipal Dental Health Service, Copenhagen, Denmark. Transplantation was used for patients with agenesis of permanent teeth or tooth and alveolar bone loss due to trauma of maxillary incisors. 3 Autotransplantation of Teeth All transplants were followed longitudinally using a standardized technique for both clinical and radiographic evaluation of pulpal and periodontal healing, root development and root resorption for a time period ranging between 16-26 years post transplantation. Twenty-four transplants were followed longitudinally with a standardized clinical and radiographic technique to examine tooth eruption at 1, 3, 4, 6, 8, 12, 16, 20 and 24 weeks after surgery (Paulsen and Andreasen, 1998; Paulsen et al., 2001), and yearly thereafter for 6 to 18 years. The study showed that the stage of root development at the time of transplantation was the most important single factor in determining a successful outcome. Transplantation of premolars with three-quarter root formation or full root formation with wide-open apical foramina proved to have the best prognosis for long-term survival (Paulsen et al., 1995). One hundred eighteen premolars in stages 3 and 4 (i.e., 3/4 to 4/4 root length with a wide open apical foramen according to Moorrees and colleagues, 1963) were selected to study the initial healing events following autotransplantation. This stage of root development provided the greatest success for continued root growth as well as periodontal ligament and pulpal healing (Paulsen et al., 1995). Pulp Necrosis CRITERIA FOR EVALUATING HEALING AND COMPLICATIONS Pulp necrosis was considered to be present when there were radiographic signs of periapical radiolucency and/or inflammatory root resorption, plus a negative response to the electrometric sensitivity test. Where an absence of pulp sensitivity was the only sign of pulp necrosis, it was required that the pulp canal show no sign of obliteration six months post transplantation. Periodontal Healing Periodontal healing was classified as being complete when the root periphery was surrounded entirely by a newly formed periodontal ligament space of normal size. Repair-Related Root Resorption Repair-related root resorption was defined as the presence of small resorption cavities on the root surface adjacent to a normal or slightly extended periodontal ligament space and lamina dura, indicating that the root periphery was undergoing repair. 4 Paulsen Inflammatory Root Resorption Inflammatory root resorption was defined by the presence of bowlshaped resorption cavities on the root surface associated with similar resorption cavities on the adjacent alveolar bone. Replacement Root Resorption Replacement root resorption (ankylosis) presented as a disappearance of the periodontal ligament space with or without resorption of the root. Clinically, the percussion test on a tooth demonstrated a high pitched metallic percussion sound. Root Growth Root growth (in mm) was evaluated from successive radiographs, and tooth length was measured to the nearest tenth of a millimetre with a sliding calliper from the cusp tip to the apex . HEALING Pulp Healing This was evaluated clinically using an electrometric test (Siemens Sirotest II, Siemens, Munich, Germany), and employing a standardized radiographic technique using XCP film holders (Rinn Corp., Elgin, Ill., USA) and a fixed film focus distance of 33 cm to evaluate signs of pulp canal obliteration. Periodontal Healing and Root Growth Subsequent to transplantation, this was monitored by radiographic examination. A digital sliding calliper reading to the nearest 0.1 mm was used to measure pulp canal obliteration and root length. Non-transplanted homologous premolars served as controls where possible. Effect on Tooth Eruption From a group of 90 maxillary second premolars transplanted to the region of the mandibular second premolar, 24 premolars transplanted with the cusp at gingival level were selected for a specific study of eruption. Periodontal ligament healing and root growth subsequent to transplantation were monitored from radiographic examination and tooth eruption. Trabecular structures are relatively stable in the jaw. Using these distinct structures in the spongious part of the basal part of the alveolar process as a reference, the prefunctional eruption of transplants was analysed from radiographs. Tooth eruption was measured as the distance from the cusp tip to the reference structure in the bone. Root growth, evaluated from successive radiographs, was measured as the difference in tooth length from the cusp tip to the apex. A Jocal digital sliding calliper (C. E. Johansson, 5 Autotransplantation of Teeth AB, Eskilstuna, Sweden) measuring to the nearest 0.1 mm was used to measure the distance between distinct structures in the anatomy of the medullar bone, tooth eruption, and tooth length. All measurements were repeated, and a mean calculated. In no instance was there a difference of more than 0.2 mm between the individual measurements. The direction and speed of eruption were examined by drawing superimposed sketches from radiographs using the distinct trabecular structures as location references. The radiographs were mounted in 3-mm slide projectors with a standardized focus distance and set-up. The speed of eruption of the transplant relative to the neighbouring reference teeth was analysed by either using the distance to a plane between the buccal cusp of the first premolar and the disto-buccal cusp on the first molar or, alternatively, using the cusp tip of the first premolar as a reference (Paulsen and Andreasen, 1998). Effect of Orthodontic Treatment Upon Healing Eleven patients who received bilateral transplanted premolars (maxillary second premolars transplanted to the regions of second premolars) were studied. Transplants were placed in a 45° distal rotation position at surgery, as the alveolar faciolingual dimension is narrower in the mandible than in the maxilla. In these patients, one of the premolars was orthodontically rotated to a normal position after periodontal healing and before pulp canal obliteration (i.e., 3-9 months after surgery). The contralateral transplanted premolar was not treated orthodontically and, therefore, served as a control. Rotation was accomplished using a fixed appliance with elastic chains (Unitek no 639-0011, Glendora, California, USA) inserted on the lingual side from the first molar to the transplant and on the facial side from the first premolar to the transplant. The initial rotational couple applied to the tooth was 200 gram-mm. The duration of rotation was 4-6 weeks. Postoperative clinical and radiographic examinations were performed as described earlier (Paulsen et al., 1995) Pulp Healing RESULTS Pulp healing was seen in 101 of the transplants. The time for initial pulp healing (cumulative data) is shown in Figures 1 and 2. Pulp healing based on the first appearance of pulp canal obliteration appeared to provide an earlier sign for pulp healing than electrometric pulp testing and demonstrated less variation. A representative example of pulp healing in a second maxillary premolar transplanted in the maxillary anterior region. 6 Paulsen Figure 1. Cumulative pulp healing in 101 immature autotransplanted premolars. Occurrences of the first sign of pulp canal obliteration and the first sign of sensitivity (in months and in percent), and the range (in months). Figure 2. Cumulative clinical and radiographic signs of pulp healing in orthodontic treatment. One tooth with reinnervation showed partial pulp canal obliteration and one tooth without reinnervation showed pulp canal obliteration. Sixteen teeth showed pulp necrosis. This condition was usually detected about 6 months after transplantation. One tooth had partial pulp necrosis. Teeth with pulp necrosis and associated inflammatory root resorption were detected two months after transplantation (Paulsen et al., 1995). Periodontal Healing Partial periodontal ligament healing was seen radiographically after 4 weeks. The majority of transplants showed complete periodontal healing 8 weeks post-transplantation (Fig. 3). Repair-related root resorption and inflammatory root resorption usually were found in the cervical area of the root. Inflammatory root resorption was seen in four cases and was detected 1 to 2 months after transplantation, whereas repair-related root resorption usually was diagnosed within the first year after transplantation. Replacement root resorption occurred in 5 cases. This complication usually 7 Autotransplantation of Teeth Figure 3. Transplantation of a maxillary second premolar to the region of the mandibular second premolar. A clinical photograph and a radiograph taken a few days after transplantation. Note that the transplant is placed in infraocclusion to avoid traumatic occlusion. Eruption of the transplant can be seen in radiographs exposed one, two, three and four months after transplantation. A clinical photograph and radiograph taken 6 months after transplantation when orthodontic treatment was begun to correct rotation. A clinical photograph and radiograph taken 18 months after transplantation. Note that root growth has continued in spite of the orthodontic rotation. 8 Paulsen could be diagnosed within 6 months after transplantation (Andreasen 1981; Andreasen et al., 1990c). Root Development Disturbance Root development either proceeded unimpeded or at a decreased rate, and in some cases was arrested. Arrested root forma- tion was found in 14% of patients studied. Unimpeded root formation was found in 21% of patients studied and a decreased rate of root formation was found in the majority of patients, i.e., 65%. Interrupted root formation was followed by the development of the missing root structure at the donor site. The newly formed root tip growth had attained almost the length of the missing part of the interrupted root form, compared to the contralateral premolar (Kristerson and Andreasen, 1984; Lagerstrom and Kristerson, 1986; Paulsen et al., 1995; Andreasen 1999d). Tooth Eruption Tooth eruption took place from 3 to 24 weeks after transplantation (Figs 3-11). The speed of eruption accelerated from 3 to 8 weeks post transplantation, was fastest during the period of 6-12 post transplantation weeks, and declined after the period of 12-24 weeks post transplantation when the transplant approached the occlusal plane and before any significant root growth had occurred. The maximum rate was 0.24 mm/week (range 0.190.29 mm) 8 weeks post transplantation. Eruption distance from gingival emergence to occlusal plan was 2.4 mm (range 1.2-5.0 mm) over 24 weeks post transplantation. When the occlusal plane had been reached, a very slow but continuous eruption was recorded that was similar to the rate of eruption of the adjacent teeth (Figs 4-7). One tooth with a broken Hertwig´s epithelial root sheath showed similar eruption, but the rate of eruption was slower. The newly formed apex, after extraction, could be seen growing in the donor region during the healing and closing period (Fig 8-10). One tooth with replacement root resorption (ankylosis) showed no sign of eruption and therefore was excluded from the calculation of the eruption rate of transplants (Fig 11). Additionally, the periodontal membrane of the autotransplanted premolars created new alveolar bone growth along with tooth eruption (Paulsen and Andreasen, 1998; Paulsen et al., 2001). Orthodontic Rotation Orthodontic rotation of 11 premolars induced slight repair-related root resorption and a significant shortening of root length (a mean of 1.2 mm) compared with transplanted, nontreated control teeth. After orthodontic treatment, a new periodontal ligament space was established, leaving an indentation in the root surface. In addition, the periodontal ligament of autotransplanted premolars created new alveolar bone growth along with 9 Autotransplantation of Teeth Figure 4. A transplant with normal root development. Radiographs show healing a few days, 4 weeks, 6 weeks, 8 weeks, 12 weeks and 16 weeks post surgery. Refer to schematics in Figures 5, 6, and 7. Figure 5. Drawing of radiographs from the transplant. The speed of eruption, relative to neighbouring reference teeth, measured using the distance to a plane between the buccal cusp of the first premolar and the distobuccal cusp on the first molar as a reference. 10 Paulsen Figure 6. Drawing of radiographs from the transplant. The speed of eruption, relative to neighbouring reference teeth, measured using the buccal cusp of the first pre-molar as a reference. Figure 7. Drawing of transplant radiographs. The speed of eruption is based on distinct structures in the trabecular structures of the medulla bone. The selected measuring point is marked with an arrow. 11 Autotransplantation of Teeth Figure 8. A transplant with arrested root development (i.e. a broken Hertwig´s epithelial root sheath). The specimen during surgery: Note the broken apex region. the healing- and the orthodontic rotation process. Late pulp necrosis occurred in 2 of the 11 treated cases six years after surgery and five years after orthodontic rotation (Paulsen et al., 1995; Paulsen, 1999). Pulp Healing DISCUSSION Pulp healing can be monitored using pulpal sensitivity and/or radiographic signs of pulp canal obliteration (Andreasen et al., 1990b). In most of the teeth transplanted in stages 3-4, both events were observed. Only a few teeth showed signs of only one or the other event. As transplantation of teeth implies, severance of the vascular and nervous supply to the pulp can cause serious damage to the architecture and function of the pulp. Subsequent healing processes usually restore the content of the pulp canal including the nervous supply. Pulpal sensitivity without pulp canal obliteration may take place in rare cases; similarly, pulp canal obliteration without pulp sensitivity may occur where nerve regeneration fails. Early reinnervation and partial pulp canal obliteration or no pulp canal obliteration appear to be signs of fast pulp canal revascularization (i.e., end-to-end anatomises of ruptured vessels) (Paulsen et al., 1995). 12 Paulsen Figure 9. Radiographs show healing and eruption a few days, three weeks, four weeks, six weeks, three months, four months and nine months after surgery and one month of orthodontic rotation of the transplant (first seven radiographs). Donor region nine months after surgery; note the newly formed apex (second last radiograph). Donor region 16 months after surgery; note that the apex has grown (last radiograph). 13 Autotransplantation of Teeth Figure 10. Drawing of radiographs from the transplant. The speed of eruption is based on distinct structures in the medullary bone. The selected measuring point is marked with an arrow. Periodontal Healing Root resorption occurred in some patients even though transplantation was performed during the initial stages of root development. Inflammatory root resorption diagnosed within two months after transplantation was mostly related to later stages of root development. Replacement root resorption (ankylosis) also was noted in situations where more than 25% of the periodontal ligament was damaged (Paulsen et al., 1995; Andreasen 1999c). Root Development Disturbances Transplantation of premolars requires surgical removal while root growth is still not complete. Continued root growth is anticipated, therefore, after transplantation. Findings that some of the transplants attained nearly normal root lengths demonstrate that the Hertwig´s epithelial root sheath can function adequately subsequent to transplantation. Arrest of root development in other transplants was related to a severance of the Hertwig´s root sheath during transplant removal (Andreasen et al., 1988, 1999d; Paulsen et al., 1995; Paulsen and Andreasen, 1998;). The initial arrest of root formation due to transplant usually is followed by development of the missing root structure (a newly formed apex) at the donor site. The root tip can grow almost to the anticipated tooth length including the length of the transplant (Paulsen and Andreasen, 1998). 14 Paulsen Figure 11. A transplant with normal root development but replacement root resorption. Radiographs show healing at a few days, 12 weeks, 24 weeks, one year and two years after transplantation (left). Note that orthodontic force was applied to the ankylosed tooth immediately after surgical luxation to accelerate eruption. Radiographs taken three years, four years, and five years after transplantation (right: first three radiographs). Treatment was unsuccessful with pronounced infraposition of the transplant during puberty. A radiograph taken seven years after transplantation shows a marked internal resorption of the crown (right: last radiograph). The relative eruption of neighbouring teeth resulted in further infraposition of the transplant (as it became part of the bone) like an implant inserted in the jaw of a growing person. 15 Autotransplantation of Teeth Tooth Eruption After Transplantation Tooth eruption after transplantation appears to depend on wound healing and nerve induction. The fibroblasts will produce and replicate collagen with a high rate of turnover. Newly synthesized collagen fibrils will reorganize the periodontal ligament with an increase in tensile strength during wound healing and probably will cause the tooth to erupt. By the third week post-transplantation, a new socket has formed, and newlydeveloped periodontal fibers extending from the cementum to the alveolar surface might cause the tooth to erupt together with an ingrowth of nerve fibers. Furthermore, the autotransplanted premolars create new alveolar bone growth along with the eruption process; the periodontal membrane induces the bone formation. Transplantation of teeth thus can be used as a viable method for restoring missing or lost alveolar bone in edentulous areas. In contrast, the autotransplanted premolar with ankylosis showed the same reaction as implants with osseous-integration. Disturbance in jaw growth is found when implants are placed before termination of alveolar growth (Paulsen and Andreasen, 1998). Furthermore, teeth will not erupt without nerve supply (Bank et al., 1995). Reestablishment of the nerve connection will probably stimulate tooth eruption. Orthodontic Treatment of Transplanted Premolars The extent of apical root resorption found in this study is equivalent to that found in previous investigations of orthodontic treatment of non-traumatized teeth. The occurrence of pulp necrosis subsequent to orthodontic rotation could be related to a strangulation of the blood vessels entering the apical foramen. It is known that the apical foramen may deviate slightly from the anatomic apex. If the foramen is located eccentrically, orthodontic rotation might damage the apical blood vessels, especially in late stages of pulp canal obliteration (Paulsen et al., 1995). Restoration of Transplanted Teeth Subsequent to transplantation, an intense production of secondary dentin occurs that contributes to the rapid maturation of the root (i.e. pulp canal obliteration). The newly formed dentin contains vascular canals, and if a deep preparation of a transplant is performed, these canals may be exposed and lead to pulp necrosis. For similar reasons, carious lesions may invade post-traumatic formed dentin rapidly. Tooth preparation for restorative purposes should involve only enamel preferably. If dentin has to be removed, it should be removed only to the level of post-traumatic formed dentin (Paulsen et al., 1990; Paulsen and Zachrisson, 1992). The use of composite materials for young patients and porcelain veneers for adult patients is advocated due to the difference in pulp maturity. 16 Paulsen Osseousintegrated Implants Versus Autotransplantation of Teeth. Single standing implants have been found to be a reliable substitute for missing teeth. However, because osseointegration occurs with such implants, they behave like ankylosed teeth; i.e., they limit the growth of the alveolar process in their vicinity because they lack the potential to erupt. However, no soft tissue is transferred with this procedure (i.e., no marginal gingiva and papillae). Autotransplanted teeth continue erupting allowing for normal development of the alveolar processes (Paulsen and Andreasen, 1998). Furthermore, soft tissue is transferred with this procedure, including marginal gingiva with papillae. The optimal treatment approach mandates a realistic evaluation of the long-term prognosis of the various treatment methods and cost. However, no commercial interests measures to make tooth transplantation more available, such as companies arranging training courses in the surgical procedure for implants. Treatment must be initiated by professionals, because there is no demand for treatment option with which the public is unfamiliar (Stenvik, 2003). Autotransplantation of teeth in orthodontics is a biological method of replacing missing or lost teeth. However, a prerequisite for using this method is a thorough knowledge of the prognosis. Thus the stage of root development of the transplant is very important. Performing transplantation when there is 3/4 to full root development of the transplant with wide open apices, employing a surgical technique that preserves the periodontal ligament, and using a light-force orthodontic tooth movement or tooth rotation three to nine months after surgery are the most crucial factors for the survival of transplants and their continued development. The periodontal ligament, with bone induction potential, will induce new alveolar bone. Furthermore, the transplanted tooth will erupt in a similar manner to that of the contralateral, non-transplanted tooth if the transplanted tooth is not ankylosed to the alveolar bone (Paulsen and Andreasen, 1998; Paulsen et al., 2001). Autotransplantation provides the potential to replace a missing tooth with a natural tooth with bone formation, rather than with a prosthesis or an endosseous implant without bone formation. It provides a unique orthodontic treatment approach for young patients as a complex orthodontic problem (i.e., premolar agencies and avulsed or malformed anterior teeth) can be transferred to anther region in the dental arch where it can be treated more easily. A prerequisite for the use of this treatment approach mandates a thorough knowledge of the risk factors associated with poor prognosis. If used with care, transplantation may greatly enhance orthodontic treatment results in selected cases (Paulsen and Zachrisson, 1992; Paulsen et al., 1995). 17 Autotransplantation of Teeth CONCLUSIONS The first evidence of pulp canal obliteration as seen radiographically appeared to provide an earlier sign of pulp healing than electrometric pulp testing. Root growth of transplanted premolars usually continued. Arrest of root development usually was followed by development of the missing root structure at the donor site. Marginal gingiva with papillae normally was transferred with the soft tissue. Periodontal ligament of autotransplanted teeth created new alveolar bone surrounding the transplant. During orthodontic tooth movement and/ or rotation, alveolar bone reformed alveolar bone to fit the contour of the root. Eruption of transplanted premolars occurred from 3 to 24 weeks after transplantation and apparently before root growth continued, with a maximal eruption rate occurring from 6 to 12 weeks after transplantation. During the eruption process, new alveolar bone appeared and followed the eruption path of the transplant. Orthodontic rotation induced a slight surface resorption and a significant shorter tooth length (the mean was 1.2 mm), and few cases showed late pulp necrosis. To prevent late pulp necrosis, orthodontic rotation is recommended after periodontal healing and before total pulp canal obliteration (i.e., three to nine months after transplantation). There should be clinical and radiographic follow-up for many years to ensure long-term results. Osseousintegrated Implants Versus Autotransplantation of Teeth Implants. Implants can be a substitute for normal tooth material without soft tissue. No transmission of marginal gingiva with gingival papillae is possible. No periodontal ligament induction of alveolar bone modelling and growth occurs. Eruption of implants not possible along growth. 18 Paulsen Orthodontic tooth movement and/or rotation is not possible. Autotransplanted Teeth Patient’s normal tooth material with soft tissue is used. Transmission of marginal gingiva with gingival papillae is possible. Periodontal ligament induction of alveolar bone modelling and growth occurs. Normal tooth eruption is possible along with growth. Orthodontic movement and/or rotation are possible. REFERENCES Akiyama Y, Fukuda H, Hashimoto K. A clinical and radiographic study of 25 autotransplanted third molars. J Oral Rehab 1998;25:640-644. 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Treatment of lower second premolar agenesis by autotransplantation: Four year evaluation of eighty patients. Acta Odontol Scand 1999;57:111-115. Kristerson L. Autotransplantation of human premolars. A clinical and radiographic study of 100 teeth. Int J Oral Surg 1985;14:200-213. Kristerson L, Andreasen JO. Influence of root development on periodontal and pulpal healing after replantation of incisors in monkeys. Int J Oral Surg 1984;13:313-323. Kristerson L, Kristerson L. Autotransplantation of teeth in cases with agenesis or traumatic loss of maxillary incisors. Eur J Orthod 1991;13: 486-492. Kugelberg R, Tegsjo U, Malmgren O. Autotransplantation of 45 teeth to the upper incisor region in adolescence. Swed Dent 1994;18:165-172. 20 Paulsen Lagerström L, Kristerson L. Influence of orthodontic treatment on root development of autotransplanted premolars. Am J Orthod 1986;89: 146-149. Moorrees CFA, Fanning FA, Hunt EE Jr. Age variation of formation stages for ten permanent teeth. J Dent Res 1963;42:1490-1502. Moss J. Autogeneous transplantation of maxillary canines. Int J Oral Surg 1968;26:775-783. Moss JP. The indication for the transplantation of maxillary canines in the light of 100 cases. Br J Oral Surg 1975;12:268-274. Nordenram Å. Autotransplantation of teeth. A clinical and experimental investigation. Acta Odont Scand 1963;21:sup 33. Northway W, Konigsberg S. Autogenic tooth transplantation. The "State of the Art." Am J Orthod 1980;77:146-162. Oksala E, Kallioniemi H. A longitudinal clinical and radiographic study of autotransplantation of the maxillary canine. Pr Fin Dent Soc 1977;73: 117-125. Paulsen HU, Andreasen JO. Autotransplantation in orthodontic treatment. Nederlandse vereniging voor orthodontische studie. Int Studyweek 1985:248-264. Paulsen HU. L'autotransplantation de prémolaires lors des traitements orthodontiques. Une nouvelle possibilité thérapeutique. Rev Orthop Dento-Faciale 1989;23:209-223. Paulsen HU, Andreasen JO, Schwartz O. Treatment of tooth loss in the front by autotransplantation of premolars. T N T 1990;5:70-75. Paulsen HU, Andreasen JO. Pulp survival, periodontal healing and root development of autotransplanted premolars. From a long-term study of 370 autotransplanted premolars. Nederlandse vereniging voor orthodontische studie. Int Studyweek 1990:93-119. Paulsen HU, Zachrisson BU. Autotransplantation of teeth and orthodontic treatment planning. In: Atlas of Replantation and Transplantation of Teeth. Andreasen JO (ed), Medi Globe, Fibourg 1992:258-274. Paulsen HU, Andreasen JO. Tooth eruption subsequent to transplantation. A longitudinal study of autotransplanted premolars. Eur J Orthod 1998; 20:45-55. Paulsen HU, Andreasen JO, Schwartz O. Pulp survival, periodontal healing and root development of autotransplanted premolars in orthodontic treatments. Am J Orthod Dentofacial Orthop 1995;108:630-640. 21 Autotransplantation of Teeth Paulsen HU. Autotransplantation of teeth in orthodontic treatment. Am J Orthod Dentofacial Orthop 2001;119:336-337. Paulsen HU, Shi XQ, Welander U, Huggare J, Scheutz F. Eruption pattern of autotransplanted premolars visualized by radiographic color-coding. Am J Orthod Dentofacial Orthop 2001;119:338-345. Paulsen HU. Premolar autotransplantation in orthodontic treatment. A clinical and radiographic long-term study. Thesis, Kgl Carol Med Chir Inst, Stockholm, Sweden 1999. Ravn JJ, Nielsen LA. Supernumerary teeth and aplasia among Copenhagen school children. Tandlægebladet 1973;77:12-22. Rølling S. Hypodontia of permanent teeth in Danish school children. Scan J Dent Res 1980;88:365-369. Slagsvold O, Bjercke B. Autotransplantation av premolarer. Göteborgs Tandläk. Sällsk. Årsbok 1967;351:45-85. Slagsvold O, Bjercke B. Autotransplantation of premolars in cases of missing anterior teeth. Trans Eur Orthod Soc 1970;46:473-485. Slagsvold O, Bjercke B. Autotransplantation of premolars with partly formed roots. A radiographic study of root growth. Am J Orthod 1974;66:355-366. Slagsvold O, Bjercke B. Applicability of autotransplantation in cases of missing upper anterior teeth. Am J Orthod 1978a;74:241-257. Slagsvold O, Bjercke B. Indications for autotransplantation in missing premolars. Am J Orthod 1978b;74:241-257. Stenvik A. US orthodontist´s reluctance to include autotransplantation. Am J Orthod Dentofacial Orthop 2003;123:18A. 22 Hans Ulrik Paulsen, Odont Dr1 Jens Ove Andreasen, DDS, PhD2 Ole Schwartz, DDS, PhD3 TOOTH LOSS TREATMENT IN THE ANTERIOR REGION: AUTOTRANSPLANTATION OF PREMOLARS AND CRYOPRESERVATION Avulsed and lost anterior teeth are common in young people. Using autotransplantation, it is possible to move problems in dental arches to regions where they are more easy to solve orthodontically. Transplantation of premolars with three-quarter root formation or full root formation with wide-open apical foramina provides the best prognosis for long-term survival. This article describes the use of autotransplantation and orthodontic treatment, together with cryopreservation, in connection with complicated trauma in the anterior region of an 8year-old girl. World J Orthod 2006;7:27–34. A 1Department of Orthodontics, Karolinska Institute, Stockholm, Sweden and Municipal Dental Health Service, Copenhagen, Denmark. 2Department of Maxillo-Facial Surgery, Copenhagen University Hospital, Copenhagen, Denmark. 3Department of Maxillo-Facial Surgery, Copenhagen University Hospital, Copenhagen, Denmark. CORRESPONDENCE Hans Ulrik Paulsen Moelleaaparken 46 2800 Lyngby Denmark E-mail: [email protected] ut ot r ansplantation of t eet h has become a predictable treatment approach for certain orthodontic conditions, namely aplasia of premolars and malformation or tooth loss of permanent incisors. In conventional orthodontics, tooth movements are usally limited to relatively small distances in sagittal, ver tical, and transverse dimensions. Including tooth transplantation in the or thodontic equipment, tooth movement is no longer limited to short distances in a quadrant of the dental arch, but wider freedom is achieved to place the tooth exactly where needed, may it be the contralateral side in the dental arch or the opposing jaw. The periodontium is the key for bone induction and bone modeling in the recipient area, and the tooth will normally erupt in a similar manner as a contralateral, nontransplanted tooth in its normal area. However, transplantation of teeth is more traumatic to the pulp and periodontium than conventional orthodontics. Donor teeth with wide-open apices and a sing le root canal are recom mended as graf ts of choice for longterm survival. The surgical procedure is thus an essential key for the successful outcome of this treatment selection and outcome. However, orthodontists are generally the most competent professionals to identify available donor teeth; because o v er all occlusa l s tatus m u s t be assessed, the orthodontist should be considered a key person in planning, referring, and coordinating treatment that includes transplantation of teeth. With autotransplantation, it has become possible to move problems in the dental arches to regions where they are easier to solve orthodontically. 27 VOLUME Paulsen7,etNUMBER al 1, 2006 WORLD JOURNAL OF ORTHODONTICS Paulsen et al The survival of transplanted premolars has been studied postoperatively for more than 25 years. A prerequisite for the use of this method is, however, a thorough knowledge of the prognosis. Thus, the stage of root development of transplants has been found to be of great importance. Transplantation at 3/4 to 4/4 root development of transplants with wide-open apices, a careful surgical technique preserving the periodontal ligament, and a light-force orthodontic tooth movement or tooth rotation carried out from 3 to 9 months after surgery are the most crucial factors for the survival of transplants and their continued development. Autotransplantation, if applied with knowledge of the predictive outcomes, is a method that supplements and enhances conventional orthodontic treatment.1–16 This article describes the use of autotransplantation and or thodontic treatment, together with cryopreservation, in connection with a complicated trauma in the anterior region in an 8-year-old girl. Despite improved possibilities for treating trauma injuries in the anterior region, there are unfortunately still some types of trauma (eg, exarticulation with replantation, intrusion and crown/root fractures), in which the permanent tooth is lost after treatment. This is due to root resorption. The definitive treatment of such tooth loss includes an evaluation of the following treatment options: tion of the anterior region of the maxillary jaw is therefore sometimes indicated. In that connection, the question of autotransplantation of premolars to the damaged area can arise. However, because of their root anatomy, these premolars are not suitable as donor teeth. The most suitable teeth for transplantation are second premolars from the maxillary jaw and premolars from the mandibular jaw because of suitably shaped roots and a possibility of altering the shape of the crown. Furthermore, for transplantation of premolars to the anterior region, a complete analysis of the development of the patient’s teeth and jaws is required. Therefore, it is necessary to draw up an orthodontic treatment plan. The plan will depend on whether the patient has a malocclusion that requires treatment, as well as the dental injury. If the orthodontic treatment plan means that several premolars have to be extracted, there is a further treatment option—namely, freezing and storage of premolars in a tooth bank (cryopreservation) for possible later use. In addition, an evaluation must be carried out to determine: (1) the type of premolar that best replaces a given incisor; (2) the timing of the treatment; (3) coordination of transplantation and orthodontic treatment; (4) restoration of the transplanted tooth; and (5) the possibility of storing premolars in a tooth bank for possible later use. • Prosthetic replacement in the form of a fixed partial denture • Orthodontic closure of the diastema that has occurred • Autotransplantation of a premolar to the anterior region followed by orthodontic closure of the donor area and morphologic reconstruction of the crown on the transplanted premolar TREATMENT OF A PATIENT WITH REPLANTATION OF 3 INCISORS COORDINATION OF SURGICAL AND ORTHODONTIC TREATMENT Many serious dental injuries are related to extreme maxillary overjet. Extraction of first premolars in connection with retrac- Description of the trauma While playing in the schoolyard, a girl, 8 years of age (Fig 1), fell and hit her face on a bench. This resulted in serious laceration of about 1 cm of the mandibular jaw at the transition to the prolabia. Both maxillary central incisors and the right mandibular central incisor were exarticulated with gingival lacerations in the traumatized regions, and the facial bone lamella was pushed in at the right maxillary central incisor region. Immediately after the fall, the teeth were gath- VOLUME Paulsen7,etNUMBER al 1, 2006 WORLD JOURNAL OF ORTHODONTICS Paulsen et al Fig 1 (left) Facial morphology of trauma patient (8 years 1 month of age). Fig 2 (center) Serious laceration in the anterior region shown immediately after arrival to the hospital, about 90 minutes after the trauma. The right maxillary central incisor has been placed in physiologic saline solution for resetting. Fig 3 (right) Three years after the trauma, the right maxillary central incisor is in infraocclusion as a result of ankylosis. Management is by the interdisciplinary orthodontic and surgical treatment plan. ered up from the asphalt and kept in a serviette for a few minutes, after which they were immediately reset by the dentist at the school. On arrival at the hospital it was found that the right maxillary c e n t r al i nc iso r w as o nl y p a r t ia ll y re- implanted. Primary trauma treatment and observation The right maxillary central incisor was removed from the alveolus about 90 minutes after the accident and was stored for 30 minutes in physiologic saline solution, while the alveolar bone fracture was reset (Fig 2). The tooth was then replanted. All the damaged teeth were fixed with a scutaneous rail. (A scutaneous rail is made of an elastic material. It is placed on the facial side of the traumatized and neighboring teeth. It allows the teeth to move during a fixation period, to prevent ankylosis.) Two months after the trauma, ankylosis of the replanted teeth was suspected, particularly of the right maxillary central incisor, which was in slight infraposition. One year after the trauma, a combined r adiog r aphic and mobility examination showed that there was no ankylosis of the lef t maxillar y central incisor and the right mandibular central incisor. Pulp sensitivity was positive in all the replanted teeth. After 2 years, the right maxillary central incisor was clearly in infraposition. The right mandibular central incisor showed reparative-related root resorption in the middle of the distal root face and pulp obliteration. Three years after the trauma, a coordinated orthodontic and surgical treatment plan was established because the infraposition of the right maxillar y central incisor had increased (Fig 3). Due to the untreatable ankylosis, the patient was offered autotransplantation of a premolar to the right maxillary central incisor region. Orthodontic examination All the teeth were forming (except all third molars); the right maxillary central incisor was in pronounced infraposition and ankylosis, t he lef t maxillar y canine showed mesial ectopic eruption. The first molars were poorly mineralized, with large restorations, particularly in the maxillary jaw. The maxillary overjet was caused by an enlarged inclination of the maxillary incisors, together with an enlarged sagittal jaw relation due to bimaxilliary retrognathy. Both jaws were inclined posteriorly, particularly the mandible, resulting in an increased vertical jaw relationship. The maxillary jaw zone had increased to compensate a basal-based open bite. Furthermore, there was crowding of the anterior regions of the maxillary and mandibular jaws (Fig 4). 29 VOLUME Paulsen7,etNUMBER al 1, 2006 WORLD JOURNAL OF ORTHODONTICS Paulsen et al Fig 4 (a) The right maxillary central incisor was in p r o nounce d infrapositio n and ankylosis. There was additional crowding of the anterior regions of the maxillary and (b) mandibular jaws. a Fig 5 Three and one-half years after the trauma. The right mandibular second premolar—as a donor tooth—is estimated to have reached 3/4 root length. b Fig 6 The ankylosed right maxillary central incisor is extracted just before transplantation. Treatment plan Transplantation of the right mandibular second premolar (Fig 5) (alternatively, the left mandibular second premolar) was advised since extraction of the maxillary first molars would be part of the orthodontic treatment plan. The left mandibul a r s e c o n d p r e mola r w ould ac t as “reserve donor tooth,” either directly from the oral cavity or after an observation period during which the tooth was cryopreserved in Copenhagen University Hospital’s tooth bank. Extensive preliminary and subsequent orthodontic treatment had to be anticipated. Treatment When the patient was 11 years 3 months of age, both mandibular second premolars were estimated to have reached 3/4 root length. To create room for transplantation of the right mandibular second premolar to the right maxillary central 30 Fig 7 The apical part of the root shows the fracture to the ankylosed part of the apex. incisor region, an expansion plate was used for 2 months. At the time of transplantation, the right maxillar y central incisor was extracted (Figs 6 and 7), after which the right mandibular second premolar was surgically removed and placed in the right maxillar y central incisor region after expansion of the alveole with a drill with internal cooling (Figs 8 and 9). Three months after the transplantation, electrometric sensitivity reaction of the pulp was positive for the new right maxillary central incisor (Fig 10). Ten months after autotransplantation, the maxillary first molars and the remaining temporary teeth were extracted to speed up eruption of the permanent teeth (Fig 11). At that time, incipient obliteration of the right maxillary central incisor and incipient eruption of both maxillar y second molars were found. Six months later, a fixed appliance was inser ted on both jaws (Figs 12 and 13). Two years after the transplantation, a radiograph of the new right maxillar y central incisor showed total obliteration of the pulp formed VOLUME Paulsen7,etNUMBER al 1, 2006 WORLD JOURNAL OF ORTHODONTICS Paulsen et al Fig 8 (left) The donor tooth is estimated to have reached 3/4 root length. The periodontal membrane and the tooth sac are intact. Fig 9 (center) The transplant is fixated with a single suture in infraposition (patient is 11 years 3 months of age). Fig 10 (right) Three months after the transplantation. The transplant shows normal periodontal healing and incipient pulp obliteration. Fig 11 Transplant 10 months after transplantation. Both maxillary first molars were extracted a few days earlier. Fig 12 Fixed appliance inserted the mandibular jaw for orthodontic closure of the donor region (patient is 12 years of age). before the transplantation, together with continued root growth of the transplant. In addition, the right mandibular central incisor had healed, with the distal root face almost remodeled, pulp obliterated, and the length of the root shorter t han t he h o mo lo gou s i nci so r. Six months later, the transplant’s crown morphology was altered by selective grinding in the enamel and subsequent buildup with composite plastic (Fig 14). Three years after the transplantation, the prognosis for the transplant was considered so satisfactory that the alternative tooth, the left mandibular second Fig 13 Fixed appliance inserted the maxillary jaw. The second molars have been guided to erupt to the first molar region. premolar, could be extracted and cryopreserved for later use in case the new right maxillary central incisor or another tooth was later lost. A reverse headgear was placed for mesial shifting of the left firs t and second molars. Four years af te r t h e t r ansplantation, when t h e patient was 16 years of age, the root of the new maxillary right central incisor w as finall y full y for med and a little longer than that of the maxillar y lef t central incisor (Fig 15). All appliances were then removed and retainers were inser ted and glued to the canines in both jaws (Figs 16 and 17). 31 VOLUME Paulsen7,etNUMBER al 1, 2006 WORLD JOURNAL OF ORTHODONTICS Paulsen et al Fig 14 Result 4 years 7 months after transplantation . Morphology of the transplant has changed from a premolar to a central incisor, by selective grinding in the enamel and composite plastic. Fig 15 Radiograph 4 years 7 months after transplantation. The transplant’s root length has now finally formed. Fig 16 Result in occlusal view. The left mandibular second premolar was extracted and cryopreserved 3 years after the transplantation. Orthodontic treatment was completed with mesial shifting of the m a nd ibu lar molars (patient is 16 years of age). Fig 17 Result in occlusal view. The transplant and second molars are in correct positions. Fig 18 Treatment analysis: 11 to 16 years of age; both maxillary second molars have been moved to the maxillar y first molar region, and both m andibular first molars have been moved to second premolar region. Fig 19 Facial morphology, patient is 16 years 2 months of age. WORLD JOURNAL OF ORTHODONTICS Paulsen et al AU: pleae provide label (%) VOLUME Paulsen7,etNUMBER al 1, 2006 100 90 80 70 60 50 40 30 20 10 Root length Normal periodontal ligament Pulp healing 1 Fig 20 Healing of autotransplanted premolars related to stage of root development. 2 3 4 5 6 7 Stage of root development Analysis of treatment The pattern of growth was mainly vertical for both jaws. The alveolar prognathy was not reduced as a result of the extraction treatment (Figs 18 and 19). DISCUSSION This case demonstrates the result of coordinated traumatologic, orthodontic, and surgical treatment, including the possibility of later use of a cryopreserved premolar in the event one of the traumatized teeth is later lost.1,2 The entire therapy took more than 7 years due to continued observation of the trauma, timing of the transplantation, guided eruption of maxillary jaw premolars and molars, orthodontic treatment, waiting for the premolar to develop to full root length for the tooth bank, and concluding orthodontic treatment. Experimental and clinical research of autotransplantation of teeth in recent years has shown that it is now advantageous to include this method as an orthodontic treatment option. 3–12 When the method is used in the anterior region, it is important to conduct a thorough analysis and evaluation of the dif ferences (esthetic, functional) and risks (durability, root resorption) resulting from intervention in the recipient region, and also of the problems created in the donor region and how these can be solved in a traum a t o l o g i c , o r t hodontic tr e at m e n t plan.6,11–16 The risks connected with the intervention relate mainly to the occurrence of pulp and periodontal complications in connection with the revascularization of these structures. A prospective study of the long-term prognosis for 370 autotransplanted premolars has shown that most healing complications can be predicted and avoided if the transplantation is performed at specific root stages. For example, Fig 20 shows that root length, pulp healing (ie, without partial or total pulp necrosis), healing of periodontal membrane (ie, without root resorption), and achievement of expected root lengt h, are decisive l y related to th e choice of donor tooth and its root development stage. In that connection, it seems obvious to transplant premolars at the 3/4 to full root-development stage, assuming a fully open apex (stages 4 to 5, see Fig 20). In these stages, the transplantation is a predictable procedure that ensures optimum healing in more than 90% of cases.7–10 33 VOLUME Paulsen7,etNUMBER al 1, 2006 OSSEOINTEGRATED IMPLANTS VERSUS AUTOTRANSPLANTATION OF TEETH Implants • A substitute to normal tooth material without soft tissue • No transmission of marginal gingiva with gingival papillae possible • No periodontal ligament induction of alveolar bone modeling and growth • Eruption of implants not possible during growth • Orthodontic movement and rotation not possible Autotransplanted teeth • Patient’s normal tooth material with soft tissue • Transmission of marginal gingiva with gingival papillae possible • Periodontal ligament induction of alveolar bone modeling and growth • Tooth eruption normal during growth • Orthodontic movement and rotation possible CONCLUSION The value of autotransplantation of premolars to the anterior region has been demonstrated. The treatment example shows careful coordination of a traumatologic, orthodontic, and surgical treatment, including cryopreservation of a premolar. With careful case selection and correct surgical and or thodontic techniques, it can be invaluable to the clinical orthodontist because long-term results are encouraging. REFERENCES 1. Schwartz O. Cryopreservation as long-term storage of teeth for transplantation or replantation. Int J Oral Maxillofac Surg 1986:15;30–32. 2. Schwartz O, Rank PC. Autotransplantation of cryopreserved teeth in connection with orthodontic treatment. Am J Orthod Dentofacial Orthop 1986:90;67–72. WORLD JOURNAL OF ORTHODONTICS Paulsen et al 3. Kristerson L. Autotransplantation of human premolars. A clinical and radiographic study of 100 teeth. Int J Oral Surg 1985:14;200–213. 4. Schwartz O, Bergmann P, Klausen B. Autotransplantation of human teeth. A life table analysis of prognostic factors. Int J Oral Surg 1985:14; 25–58. 5. Schwartz O, Bergmann P, Klausen B. Resorption of autotransplanted human teeth: A retrospective study of 291 transplantations over a period of 25 years. Int Endod J 1985:18;119–131. 6. Paulsen HU, Andreasen JO. Autotransplantation in orthodontic treatment. Nederlandse Vereniging Voor Orthodontische Studie Studieweek 1985:248–264. 7. Andreasen JO, Paulsen HU, Yu Z, Ahlquist R, Bayer T, Schwartz O. A long-term study of 370 autotransplanted premolars—Part I. Surgical procedure and standardized techniques for monitoring healing. Eur J Orthod 1990;12:3–13. 8. Andreasen JO, Paulsen HU, Yu Z, Bayer T, Schwartz O. A long-term study of 370 autotransplanted premolars—Part II. Tooth survival and pulp healing subsequent to transplantation. Eur J Orthod 1990;12:14–24. 9. Andreasen JO, Paulsen HU, Yu Z, Bayer T, Schwartz O. A long-germ study of 370 autotransplanted premolars—Part III. Periodontal healing subsequent to transplantation. Eur J Orthod 1990;12:25–37. 10. Andreasen JO, Paulsen HU, Yu Z, Bayer T. A long-germ study of 370 autotransplanted premolars—Part IV. Root development subsequent to transplantation. Eur J Orthod 1990;12: 38–50. 11. Paulsen HU, Andreasen JO, Schwartz O. Pulp and periodontal healing, root development and root resorption subsequent to transplantation and orthodontic rotation. A long-term study of autotransplanted premolars. Am J Orthod Dentofacial Orthop 1995;108:630–640. 12. Paulsen HU, Andreasen JO. Tooth eruption subsequent to transplantation. A longitudinal study of autotransplanted premolars. Eur J Orthod 1998;20:45–55. 13. Papika S, Paulsen HU, Shi X-Q, Welander U, Linder-Aronson S. Orthodontic application of color image addition to visualize differences between sequential radiographs. Am J Orthod Dentofacial Orthop 1999;115:488–493. 14. Paulsen HU. Commentary. Autotransplantation of teeth in orthodontic treatment. Am J Orthod Dentofacial Orthop 2001;119:336–337. 15. Paulsen HU, Shi X-Q, Welander U, Huggare J, Scheutz F. Eruption patterns of autotransplanted premolars visualized by radiographic color-coding. Am J Orthod Dentofacial Orthop 2001;119:338–345. 16. Paulsen HU. Premolar autotransplantation in orthodontic treatment. A clinical and radiographic long-term study [thesis]. Stockholm: Kongl Carolinska Medico Chirurgiska Instituttet, 1999.