Case Report/Clinical Techniques
Novel Management of Avulsed Tooth by Pulpal and Periodontal Regeneration Dexton Antony Johns, MDS,* Vasundara Yayathi Shivashankar, MDS,* Ramesh Kumar Maroli, MDS,* and Surendran Vidyanath, MDS† Abstract Introduction: The avulsion of anterior teeth of young children is a tragic occurrence and often presents an unparalleled challenge for the dentist. Reimplantation is the state-of-the-art treatment but may incur several complications, particularly with inappropriate posttraumatic management. Methods: In this article we report the emergency and rehabilitation treatment of an avulsed maxillary anterior tooth by using platelet-rich fibrin. The osteoconductive and osteoinductive properties of platelet-rich fibrin were used to stimulate pulpal and periodontal regeneration. Results: During followup, no clinical signs and symptoms were present. After the initial 6 months, no further bone loss and attachment loss were observed. The tooth remained functional and was aesthetically acceptable. Conclusions: When a tooth is avulsed, attachment damage and pulp necrosis occur. Viable periodontal ligament cells are often left on most of the root surface. If the periodontal ligament that is left attached to the root surface does not dry out, the consequences of tooth avulsion are usually minimal. (J Endod 2013;39:1658–1662)
Key Words Avulsion, periodontal, platelet-rich fibrin, pulpal, regeneration
From the *Department of Endodontics, Government Dental College, Calicut, Kerala, and †Department of Oral Pathology, KMCT Dental College, Kerala, India. Address requests for reprints to Dr Dexton Antony Johns, Department of Endodontics, Government Dental College, Kozhikode, Kerala 673008, India. E-mail address: dextonjohns@ gmail.com 0099-2399/$ - see front matter Copyright ª 2013 American Association of Endodontists. http://dx.doi.org/10.1016/j.joen.2013.08.012
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osing a tooth is one of the most distressing events that can befall a young individual. For the patient and his/her parents, the psychological impact is greater than the impact causing the avulsion. The injuries pose a clinical challenge because these changes occur suddenly and unpredictably. Avulsion injury, one of the most severe forms of dental trauma, is characterized by the complete displacement of the tooth from its alveolar socket. The complexity of this injury severely damages the neurovascular supply entering the apical area of the tooth. This usually results in loss of pulp vitality (1). The incidence of complete avulsion ranges from 1%–16% of all traumatic injuries to the permanent dentition (2). Reimplantation is widely accepted as an effective treatment modality for avulsed tooth. However, the long-term fate of avulsed tooth is unpredictable and depends on various factors such as time interval between avulsion and reimplantation, the storage medium used during its extraoral time, the vitality status of pulp and periodontal tissues, and the period of splinting. Various studies have consistently shown that baseline knowledge of emergency management of tooth avulsion by laypeople and even some emergency medical personnel and physicians is less than optimal (3). Thus, it is not always feasible to do tooth reimplantation immediately, which can lead to desiccation of the root surface, which again poses a risk to the vitality of periodontal ligament (PDL) cells. The vitality of the PDL on the surface of the root increases the probability of reinsertion of dental fibers with the alveolar ones, when reimplantation is immediate, that is, when it is done up to 1 hour after avulsion (4). Techniques for repopulating the damaged PDL cells and pulpal cells should be undertaken so as to retain the knocked-out tooth in the socket because most of the avulsed teeth are brought late to the dental operting room. Platelet-rich fibrin (PRF), as described by Choukroun et al (5), is a secondgeneration platelet concentrate that allows one to obtain fibrin membranes enriched with platelets and growth factors after starting from an anticoagulant-free blood harvest without any artificial biochemical modification. The PRF clot forms a strong natural fibrin matrix, which concentrates almost all the platelets and growth factors of the blood harvest (6) and shows a complex architecture as a healing matrix, including mechanical properties that no other platelet concentrate offers. PRF can stimulate cell proliferation of osteoblasts, gingival fibroblasts, and PDL cells but suppresses oral epithelial cell growth (7). These cell type–specific actions of PRF may be beneficial for periodontal regeneration. PRF is also considered an ideal biomaterial for pulp-dentin complex regeneration (8). In this report, avulsion management that uses PRF as the sole scaffold material for pulpal and periodontal regeneration is presented.
Case Report A 15-year-old male patient attended the emergency service of our dental department because of a motorcycle accident. The patient’s medical history was insignificant. On examination, the patient did not show any signs or symptoms of neurologic injury. The extraoral examination revealed a swelling of the upper and lower lip, lacerations in the upper lip and chin, and abrasions on the forehead, below the left eye, below the nostrils, and on the bridge of nose. The patient had lost a left upper central incisor (Fig. 1A). During the extraoral time of 8 hours, the patient’s caretakers had stored the avulsed tooth in milk. Examination of the avulsed tooth (tooth 9) revealed that the crown was intact, and that the root had a nearly closed apex. Oral hygiene was fair, no carious lesions were detected clinically, and blood clot was found in the alveolar socket. No other oral injury was detected clinically. All the adjacent teeth responded
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Figure 1. (A) Preoperative clinical view showing avulsed left central incisor. (B) Root-end resection of 3 mm was accomplished by use of no. 702 tapered fissure bur in low-speed straight handpiece. (C) Avulsed tooth after root resection. (D) Resected root orifice was enlarged by using SX ProTaper rotary instrument.
positively to a vitality test. Without any delay, root-end resection of 3 mm was accomplished by use of a no. 702 tapered fissure bur in a highspeed straight handpiece (Fig. 1B and C). The resected root orifice was enlarged by using SX ProTaper rotary instrument (Dentsply Maillefer, Ballaigues, Switzerland) by a retrograde approach (Fig. 1D), and it was ensured that the apical diameter was greater than 1 mm. The canal was irrigated with 20 mL 5.25% sodium hypochlorite (NaOCl) solution,
and minimal instrumentation of root canal was performed to retain the pulp cells, which could act as a scaffold (Novo Dental Product, Mumbai, India). It was ensured that NaOCl did not come in contact with the root surface during irrigation. The root canal was then rinsed with sodium chloride and dried with absorbent paper points. The root surface of the first maxillary incisor was coated with topical doxycycline hydrochloride (approximately 1 mg/20 mL saline; Sigma-Aldrich, St Louis,
Figure 2. (A) PRF membrane was prepared after compressing PRF in gauze and placed as 1 layer covering the root surface, and PRF was condensed into the canal by using a finger plugger. (B) A semiflexible splint was made with orthodontic wire number 0.012 and composite resin. (C) A semiflexible splint was made with orthodontic wire no. 0.012 and composite resin to stabilize the avulsed tooth. The splint was placed for 10 days.
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Figure 3. (A) Radiographic view of splinting. (B) Six-month follow-up radiographic view. The apex remains open with thick radiolucent area surrounding the root. (C) Twelve-month follow-up radiographic view. The open apex shows no signs of ankylosis or resorption. (D) Twenty-four–month follow-up radiographic view. A thick radiolucent area surrounds the root.
MO). A 12-mL sample of whole blood was drawn intravenously from the patient’s right antecubital vein and centrifuged (REMI Model R-8c with 12 15 mL swing out head; Remi Laboratory Instruments, Mumbai, India) under 3000 rpm for 10 minutes to obtain the PRF, which was jelly-like in consistency. PRF membrane was prepared after compressing the PRF in gauze and was placed as the layer covering the root surface (Fig. 2A). The PRF was condensed into the canal by using a finger plugger (Dentsply Maillefer). An anesthetic solution containing epinephrine was used to anesthetize the patient. The socket was rinsed with saline, and the tooth was replanted by using light pressure. The time spent from the root resection to reimplantation was around 20 minutes. A semiflexible splint was made with orthodontic wire number 0.012 (ORMCO, Glendora, Mexico) and composite resin with dentin adhesive (Figs. 2B and 3A). The splint was left in place for 10 days. Several radiographs were taken during this emergency appointment 1660
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and at each additional periodic follow-up visit. The patient received antibiotic dosage (500 mg amoxicillin, 3 times a day for a week), a nonsteroidal anti-inflammatory drug (50 mg diclofenac, 3 times a day for 3 days), and 0.2% chlorhexidine gluconate oral rinse for a week to prevent infection and pain. In addition, he was instructed to eat a soft diet while healing and to avoid biting with the splinted teeth. Then the patient was referred to the medical practitioner for an antitetanus booster. The patient was followed up at 6, 12, and 24 months (Fig. 3B–D) during which no clinical signs and symptoms were present. Although there was bone loss in the initial 6 months, no further bone loss and attachment loss were observed at 12 and 24 months (Fig. 3B–D). The tooth remained functional and was esthetically acceptable (Fig. 4). The percussion tone and tooth mobility were normal. Radiographically, the apex remained open and showed an area of radiopacity JOE — Volume 39, Number 12, December 2013
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Figure 4. Twenty-four–month follow-up clinical view. The central incisor is lightly discolored.
surrounding the resected root, no inflammatory or replacement root resorption was detected, and the adjacent anterior teeth remained asymptomatic. Thermal tests were done with carbon dioxide snow ( 78 C), which showed a positive response.
Discussion Tooth avulsion occurs when a tooth sustains a trauma that displaces the tooth from its socket. The maxillary central incisors are the most commonly affected ones in both the dentitions because of their prominence in the jaws. When a tooth is avulsed, attachment damage and pulp necrosis occur. The tooth is ‘‘separated’’ from the socket, mainly because of the tearing of the PDL, which leaves viable PDL cells on most of the root surface. If the PDL that is left attached to the root surface does not dry out, the consequences of tooth avulsion are usually minimal (9). The inflammatory response increases as the extraoral dry time elapses. Because a large area of root surface is affected, the PDL cells need to be repaired by new tissues. The cementoblast cells, which are slow moving, cannot cover the entire root surface in time, and the bone cells come in direct contact with the root surface, leading to ankylosis; clastic activity may also be initiated, leading to resorption. Pulp necrosis is also an inevitable consequence of exarticulation injuries, and this necessitates endodontic procedures. Doxycycline is an antibiotic with a wide antibacterial range including anaerobic and facultative bacteria. Its mechanism of action involves prevention of protein synthesis in the bacterial cell (10). Doxycycline can also minimize the damage of the inflammatory process by delaying the action of the enzyme matrix metalloproteinase, a collagenase that breaks down collagen in connective tissue (11). Doxycycline encourages the action of fibroblasts and healing of connective tissue, which contributes to the recovery of the PDL after injury (12). When extracted monkey teeth were treated with topical doxycycline (1 mg/ 10 mL for 5 minutes) before reimplantation, the use of antibiotics significantly increased the frequency of revascularization to 41% (control group, 18%) and lowered the frequency of inflammatory root resorption to 30% and ankylosis to 48% (control group, 66% and 68%, respectively) (13). Doxycycline was used in this case to retain as many viable PDL cells as possible and to disinfect the pulp canal space. As membrane and grafting material, PRF offers an improved spacemaking effect of the barrier, which is conducive to cell events leading to periodontal regeneration, and facilitation of mineralized tissue formation because of osteoconductive and/or osteoinductive properties possibly inherent in PRF. PRF can up-regulate phosphorylated extracellular signal-regulated protein kinase expression and suppress osteoclastogenesis by promoting the secretion of osteoprotegerin in JOE — Volume 39, Number 12, December 2013
osteoblast cultures (14). As the osteoclastic activity is subdued, chances of external resorption can be curbed to some extent. Studies have demonstrated that the PRF membrane has a very significant slowsustained release of key growth factors for at least a week (15) and up to 4 weeks (7), which means that the PRF membrane stimulates its environment for a significant time during remodeling. Thus, the properties of this natural fibrin biomaterial offer great potential during wound healing. Fibrin matrix leads directly to angiogenesis (16). It also constitutes a natural support to immunity, thereby reducing the inflammatory process (17), which assists in the repopulation of PDL cells. PRF was also demonstrated to stimulate osteogenic differentiation of human dental pulp cells by up-regulating osteoprotegerin and alkaline phosphatase expression (18). The thick radiolucent area surrounding the root viewed radiographically could be the function of PRF in forming the periodontal apparatus. The International Association of Dental Traumatology guidelines for management of mature avulsed tooth with extraoral time greater than 60 minutes include root canal treatment carried out before reimplantation. This tooth usually has a poor longterm prognosis, the expected eventual outcome is ankylosis, and resorption of the root and the tooth will be lost eventually (19). Studies have shown that to obtain a vital pulp in an autotransplanted or replanted tooth, the apical foramen should not be smaller than 1 mm in diameter (20). Resecting 3 mm and enlarging the apex by using SX ProTaper file not only helped us achieve an apical diameter greater than 1 mm but also facilitated easy placement of PRF into the root canal. Crown-to-root ratio has been considered one of the most important deciding factors for determining when a tooth with compromising prognosis should be treated to ensure its long-term survival (21). A recent review on crown-to-root ratio from a prosthodontic point of view has emphasized that the decision of keeping a tooth or removing it should be made case by case (22). In the present case, despite unfavorable crown-to-root ratio, the patient enjoyed normal mobility, pocket depth, and reasonable esthetics up to 2 years. Absence of traumatic occlusion and immediate splinting after reimplantation facilitated successful treatment. The coronal discoloration could be the result of degraded blood products entering the dentinal tubules after trauma or from PRF placed inside the root canal. The slight extrusion of tooth could be due to PRF membrane covering the root; the volume of the socket could accommodate only the root and not the membrane and the root. However, the revitalized tooth demonstrated a positive response to vitality tests. The root apex was not closed even after the follow-up period because the tooth was mature, and the remnant epithelial root sheath cells and stem cells of apical papilla were eliminated when the apical 3 mm was resected. Further research needs to be done to delineate the use of this fibrin matrix, enriched with growth factors, in various regenerative procedures.
Acknowledgments The authors deny any conflicts of interest related to this study.
References 1. Martin MP, Pileggi R. A quantitative analysis of Propolis: a promising new storage media following avulsion. Dent Traumatol 2004;20:85–9. 2. Fountain SB, Camp JH. Traumatic injuries. In: Cohen S, Burns RC, eds. Pathways of the Pulp, 7th ed. St Louis: CV Mosby; 1998. 3. Santos ME, Habecost AP, Gomes FV, et al. Parent and caretaker knowledge about avulsion of permanent teeth. Dent Traumatol 2009;25:203–8. 4. Flores MT, Andersson L, Andreasen JO, et al. Guidelines for the management of traumatic dental injuries: II—avulsion of permanent teeth. Dent Traumatol 2007;23: 130–6. 5. Choukroun J, Adda F, Schoeffer C, Vervelle A. PRF: an opportunity in perio-implantology. Implantodontie 2000;42:55–62.
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15. Mazor Z, Horowitz RA, Del Corso M, et al. Sinus floor augmentation with simultaneous implant placement using Choukroun’s PRF (platelet-rich fibrin) as sole grafting material: a radiological and histological study at 6 months. J Periodontol 2009; 80:2056–64. 16. Diss A, Dohan DM, Mouhyi J, Mahler P. Osteotome sinus floor elevation using Choukroun’s platelet-rich fibrin as grafting material: a 1-year prospective pilot study with microthreaded implants. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008;105:572–9. 17. Dohan DM, Choukroun J, Diss A, et al. Platelet-rich fibrin (PRF): a secondgeneration platelet concentrate—part III: leucocyte activation—a new feature for platelet concentrates? Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2006; 101:51–5. 18. Huang FM, Yang SF, Zhao JH, Chang YC. Platelet-rich fibrin increases proliferation and differentiation of human dental pulp cells. J Endod 2010;36:1628–32. 19. Andersson L, Andreasen JO, Day P, et al. International Association of Dental Traumatology guidelines for the management of traumatic dental injuries: 2—avulsion of permanent teeth. Dent Traumatol 2012;28:88–96. 20. Andreasen JO, Paulsen HU, Yu Z, Bayer T. A long-term study of 370 autotransplanted premolars: part IV—root development subsequent to transplantation. Eur J Orthod 1990;12:38–50. 21. McGuire MK, Nunn ME. Prognosis versus actual outcome: III—the effectiveness of clinical parameters in accurately predicting tooth survival. J Periodontol 1996;67: 666–74. 22. Grossmann Y, Sadan A. The prosthodontic concept of crown-to-root ratio: a review of the literature. J Prosthet Dent 2005;93:559–62.
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