Dental Traumatology 2002; 18: 138143 Printed in Denmark .

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Copyright # Blackwell Munksgaard 2002 DENTAL TRAUMATOLOGY ISSN 16004469

Treatment of replacement resorption with Emdogain1 a prospective clinical study

Filippi A, Pohl Y, von ArxT. Treatment of replacement resorption with Emdogain1 a prospective clinical study. Dent Traumatol 2002;18:138^143. # Blackwell Munksgaard, 2002. Abstract ^ The present clinical study investigated the outcome of intentional replantation using Emdogain for periodontal healing following trauma-related ankylosis. Sixteen ankylosed teeth aected by replacement resorption were treated as follows: After tooth extraction, the root canal was obturated with a retrograde titanium post. Emdogain was applied to the root surface and into the extraction socket with subsequent replantation of the tooth. Evaluation parameters included horizontal and vertical Periotest scores, percussion sound and periapical radiographs. All ndings were compared to those of the adjacent teeth. The mean follow-up period was 15 months (range 4^24 months). Eleven teeth showed no signs of recurrence of ankylosis: they were in full function and exhibited no pathological clinical ndings. Four severely traumatized teeth demonstrated a recurrence of ankylosis after a mean period of 6 months, one tooth was lost in a second accident after 7 months. The estimated probability of 1year without recurrence of ankylosis was P 0.66 (95% condence interval [0.40; 0.94]). The mean survival time was 10.2 months (SD 1.1). The results indicate that treatment of replacement resorption following light to moderate trauma with replantation and Emdogain appears to prevent or delay recurrence of ankylosis in many cases. Andreas Filippi1, Yango Pohl2, Thomas von Arx3
Department of Oral Surgery, University of Basel, Basel, Switzerland, 2Department of Oral Surgery, University of Bonn, Bonn, Germany, 3Department of Oral Surgery, University of Berne, Berne, Switzerland
1

Key words: ankylosis; Emdogain; intentional replantation; replacement resorption Andreas Filippi, Department of Oral Surgery, School of Dental Medicine, University of Basel, Hebelstrasse 3, CH-4056 Basel, Switzerland Tel: 4161267 2609 Fax: 4161267 2607 e-mail: andreas.filippi@unibas.ch Accepted September 24, 2001

Severe tooth trauma or nonphysiologic extraoral storage of an avulsed tooth may lead to irreversible damage of the periodontal ligament cells, particularly of the cementoblasts (1^3). The tissue wounding initially provokes an inammatory reaction, which leads to an activation of osteoclasts with resorption of cementum and root dentin. In the case of severe damage and in the absence of spontaneous healing by migration of adjacent viable cementoblasts if present at all ankylosis and replacement resorption will ensue (1, 4^7). Cementum and root dentin are resorbed by osteoclasts with subsequent replacement by alveolar bone deposited by osteoblasts.These teeth are lost usually 3^7 years after initiation of root resorption (8). Ankylosis and replacement resorption can be diagnosedby means of the Periotest examination (Gulden, Bensheim, Germany): the Periotest scores especially those measured in a vertical direction are

clearly reduced inthe early stage ofankylosis andyield negative results (9,10).The horizontal Periotest scores are signicantly reduced compared to the adjacent teeth, and are close to or below zero. On the other hand, percussion sound is altered later and only after approximately 20% of the root surface has been aected (6,11): this sound istypically high and metallic (4, 6). Radiographic changes are initially seldom present and more dicult to assess (4, 12^14). At a later stage, the periodontal ligament space cant be discerned and the contour of the root disappears gradually because of external root resorption (4). In order to reduce the risk of ankylosis with subsequent root resorption, various treatment options have been suggested. These include the use of a special cell culture medium to store avulsed teeth, like VIASPAN1 (DuPont Pharmaceuticals, Wilmington, DE, USA) or DENTOSAFE1 (Medice, Iserlohn, Germany) (2,15^17). DENTOSAFE has a lifetime of

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Treatment of replacement resorption with Emdogain1 3 years and can be stored at room temperature. Other major issues include the splinting technique of traumatized teeth (4, 18), topical or systemic application of tetracyclines to reduce the number of microorganisms and to inhibit the osteoclastic activity (19), and the administration of steroids to minimize the inammatory reaction (20). In adults or following completion of jaw growth, an ankylosed tooth can be readily replaced with a xed restoration or with an implant. When the ankylosed tooth is not removed, the alveolar process usually remains preserved, provided the root is replaced with bone and no infection has occurred (4, 21). In children and adolescents, i.e. in the growing jaw, root resorption takes place at a much faster rate than in adults, thereby aecting the growth of the alveolar bone (4, 8, 22).While the maxilla is developing in a downward and forward direction, the ankylotic tooth remains more or less in infraocclusion, depending on the age at the time of injury and the individual growth pattern. This will lead to poor esthetics and functional loss. After tooth loss, a large bone deciency may be present particularly in a vertical direction which later requires an augmentation procedure.Therefore, the aected teeth should be removed early while the jaw is still growing (4, 21). One option is to transplant a premolar to replace the extracted tooth. Premolars show a high healing rate and are easily reshaped to meet esthetic requirements (23). In children younger than10 years, the transplantation of a primary canine can also be considered: preliminary ndings have demonstrated good results in terms of function and esthetics (24). As an alternative therapy, intentional replantation using Emdogain (Biora, Malmo , Sweden) has been reported (25). This protein complex may facilitate cementoblast growth onto the denuded root surface by enhancing migration and dierentiation of progenitor cells thereby regenerating the attachment apparatus (26). Studies of humans and experimental animals have shown promising results (27^29). Preliminary data after trauma-related ankylosis and intentional replantation using Emdogain have also showed promising results (25). Material and methods During an evaluation period of 2.5 years, ankylosis at an early stage or aecting only a circumscribed area of the root (the latter characterizedby normalvertical Periotest scores but with infraocclusion) was diagnosed in 16 patients (mean age 14.4 years, range 7^ 23 years). The original trauma included avulsion in six patients, palatal displacement in four patients and moderate intrusion in two patients. Four patients could not recall the dental trauma. Nine teeth only traumatized a few months ago, showed a normal vertical position compared to the adjacent teeth.

Fig. 1. Replacement resorption of UL central incisor, 2 years after avulsion and replantation.

However, Periotest scores were clearly reduced and six of these teeth had a high percussion tone. Seven teeth had been traumatized more than 1year before retreatment. They presented with an infraocclusion of up to 7 mm. Periotest scores measured horizontally and vertically were almost normal or only slightly reduced. Orthodontic movement of these seven teeth was not possible. Obvious radiographic changes could only be seen in two cases (Fig.1).The endodontic ndings were as follows: 6 teeth reacted normally to thermal stimulation. In 7 teeth, a sensible reaction was uncertainbut the teeth showed no signs of pulp necrosis such as tenderness to percussion, pain, discoloration, periapical lesions or infection related root resorption. In the remaining three teeth, endodontic treatment had been initiated or completed. In all sixteen patients, the ankylosed tooth was removed under local anesthesia. In 15 patients, the tooth could be easily extracted, whereas only one case showed an rm osseous connection to be feactured. The root surfaces of the extracted teeth usually presented only small and circumscribed areas of resorption. Only one case showed a complete resorption of the apical root portion (Fig.2). After resection of the root apex and using a standard drill (Retropost1, Brasseler-Komet, Lemgo, Germany), the pulp including adjacent dentin was removed extending the retrograde preparation into the crown. After drying the enlarged canal, a cylindrical titanium post was inserted with cement (Fig.3). The overall length of the post^root complex should mimic the root of the adjacent tooth. Finally, the root surface was carefully dried with sterile gauzes and Emdogain was applied direct to the root surface. In contrast to periodontal

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Fig. 2. Extracted UL central incisor shows complete resorption of the apical root portion.

Fig. 4. Radiograph following replantation and nonrigid splinting (TitaniumTrauma Splint).

indications, the root surface is not conditioned prior to application of Emdogain in order to minimize injury to cementoblasts and other periodontal ligament cells adhering to the root surface. Emdogain was also placed into the alveolar socket. The tooth was then gently replanted. In the case of infraocclusion, the tooth was repositioned for correct vertical alignment. Occasional soft tissue deciencies on the labial aspect were treated with coronal ap advancement. Stabilization of the replanted tooth was secured for 10^ 14 days by means of a non-rigid bracket splint or the

TitaniumTrauma Splint (30) (Fig.4). Postoperatively, the tooth was examined after one and two weeks, with additional follow-ups each month. Evaluation parameters included horizontal and vertical Periotest scores, percussion sound and periapical radiographs. All ndings were compared to those of the adjacent teeth. The data were analyzed by the Working Group of Statistics, Institute of Medical Informatics,University of Giessen, Germany, using SAS 6.12 (Cary, NC, USA). Main parameter was the survival time without recurrence of ankylosis. Product-limit estimators of the probability of one-year survival without ankylosis and the mean survival time without ankylosis were computed. Results Over a period of 2.5 years, 16 replanted teeth were followed for an average of 15 months (range 4^ 24 months). 11 teeth (observation period 15 months, range 4^24 months) showed an uneventful healing without any clinical or radiographic pathology (Fig.5). After eight weeks, the Periotest scores were identical to those of the adjacent teeth, and remained unchanged during the follow-up period. Following treatment, ve teeth could be successfully included in an orthodontic therapy (Figs 6, 7). The estimator of the probabilityof one-year survivalwithout ankylosis was P 0.66 with a 95% condence interval of [0.40; 0.94]. One tooth was lost after 7 months in a new traumatic event. Up to that time, replantation had been successful and there were no signs of re-ankylosis.

Fig. 3. Situation following extraoral endodontic treatment using the Retropost1 system.

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Treatment of replacement resorption with Emdogain1

Fig. 5. Clinical situation 6 months after replantation. No signs of ankylosis are present.

Fig. 8. Proportion of patients without recurrence of ankylosis depending on time.

Fig. 6. Clinical situation 12 months after replantation. UL central incisor is included in the orthodontic therapy.

Four teeth presented with a recurrent ankylosis. Recurrence was diagnosed after four months in three cases and after twelve months in one case (Fig. 8). All the aected teeth showed negative vertical and reduced horizontal Periotest scores; two of these teeth had a high percussion tone. For all these re-ankylosed teeth, the original trauma was avulsion with nonphysiologic extraoral storage (between 90 and120 minute in water, plastic box and aluminum foil). In one case the extraoral storage time could not be exactly determined due to unconsciousness. In this study, the statistically most probable time of recurrence of ankylosis after replantation (mean survival time) was10.2 months with a standard deviation of s 1.1months. Discussion Ankylosis and replacement resorption of teeth replanted after trauma in children and adolescents may result in localized disturbance of jaw growth and eventually in tooth loss (8, 21, 22). However, a permanent restoration can not be placed before completion of jaw growth. Provisionals like removable partial dentures are normally a nuisance to the patient in terms of functional, esthetic and psychological aspects. Ankylosis in children and adolescents may result in extended bone defects particularly in a vertical direction which later often requires an augmentation procedure. Therefore, the aected teeth should be removed while the jaw is still growing (21). When the tooth is not replaced by another tooth with a vital functional PDL (i.e. autotransplantation) the alveolar process will collapse. If the transplantation of a premolar or of a primary canine (23, 24) is not indicated, and when replacement resorption is diagnosed at an early stage, the presented technique of intentional replantation using Emdogain appears to be a promising treatment option. Compared to tooth transplantation, this is

Fig. 7. Periapical radiograph of UL central incisor, 12 months after replantation shows no pathological changes.

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Filippi et al. an easier procedure.T ooth transplantation requires a second surgical site to harvest the graft. Following transplantation the transplanted tooth must be reshaped and the extraction site must be closed orthodontically. Four of the treatedteeth showed recurrence of ankylosis in the rst year following replantation. The trauma leading to the initial ankylosis was severe, probably resulting in large defects on the root surface or destroying the whole cementoblast population. Compared to these four teeth, cases without recurrence of ankylosis had sustained less severe trauma (avulsions with physiological storage, moderate intrusions or palatal dislocations). Four patients without recurrence of ankylosis could not recall the original type of trauma. This also implies a very moderate trauma. In these cases the aected teeth only showed localized ankylosis, as typically seen after less severe trauma. Emdogain is supposed to facilitate cell growth on root surfaces by enhancing migration and maybe differentiation of vital progenitor cells (26). Periodontal investigations on localizeddefects have shownpromising results (27, 29). According to these studies and in accordance to our own results, Emdogain is not able to regenerate severely damaged PDL.Without Emdogain, osteoclasts attack the root after 7^10 days. Regularly, ankylosis or recurrence of ankylosis can be diagnosed within 4 to 8 weeks following replantation without Emdogain (6, 14). In our study, ankylosis could be diagnosed at 4 months at the earliest in cases with severe trauma. Thus Emdogain appeared to delay the recurrence of ankylosis. The statistically most probable time of recurrence of ankylosis after replantation (mean survival time) was 10.2 months. 3 teeth still without recurrence of ankylosis have been followed for only 4, 5 and 7 months, and therefore, have not passed this timeline. 9 teeth without recurrence of ankylosis have been followed for more than 12 months. With focus to these teeth Emdogain appeared to either prevent ankylosis completely or at least delay dramatically the recurrence of ankylosis. The extraoral rootcanaltreatment with resection of the root tip and insertion of posts comprises several advantages (31^33). The ankylosed sites were mainly located inthe apical region and removed. Even higher resection is possible, a length of 2^3 mm of remaining root attachment is usually sucient (34).The removal should have contributed to the good results. The post extends the root to its original length. The fulcrum is shifted more apically and enhances tooth stabilization. This is conrmed by the Periotest which shows values comparable to these of the adjacent teeth. T o avoid infection related resorption, an extraoral root-canal treatment should be performed at the time of intentional replantation. The outcome of the present study shows, that incase of the periodontal defects on the root surface no endodontic problems were observed (such as periapical lesions or infection related root resorption). This is in accordance with a publication on intentional replantation of immature teeth with noninfected pulp necrosis (33) which also demonstrated that extraoral insertion of titanium posts does not negatively inuence periodontal healing and does not hinder orthodontic movements. An immediate and denitive endodontic treatment will prevent postoperative infection of the pulp or infection-related resorption after replantation. In addition, periodontal lesions are prevented as use of endodontic irrigation andcalcium-hydroxide maycause localirritation or interfere with Emdogain when escaping from the root canal via the apical foramen or dentin canals (35). Conclusions The presentedtechnique of intentional replantation of ankylosed teeth with Emdogain delayed or even prevented recurrence of ankylosis in 12 out of 16 teeth. This technique allows treatment of young patients without esthetic, functional and psychological compromises. Normal jaw growth is not inhibited, thereby maintaining the width of the alveolar crest until permanent tooth restoration is feasible. Some of these teeth could be included in an orthodontic therapy, which was not possible before. However, the followup periodof 2.5 years does not allowa nal conclusion. Therefore, it is not possible to know, whether these teeth will be preserved until jaw growth is complete. However, the potential of the presented technique should be analyzed in further studies with extended follow-up periods. Intentional replantation with application of Emdogain is a promising attempt to preserve teeth with limited ankylosis. The indication should be strict following severe dental injuries. Depending on jaw growth of the patient the use of alternative therapies, such as transplantation of primary canines (24) or premolars, and decoronation (21, 36) must be considered. References
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