Pulpal response to sensibility tests after traumatic dental injuries in permanent teeth

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1 Dental Traumatology 2013; doi: /edt Pulpal response to sensibility tests after traumatic dental injuries in permanent teeth Juliana Vilela Bastos 1, Eugenio Marcos Andrade Goulart 2, Maria Ilma de Souza C^ortes 1 1 Department of Restorative Dentistry, School of Dentistry, Federal University of Minas Gerais; 2 Department of Pediatrics, School of Medicine, Federal University of Minas Gerais, Belo Horizonte, Brazil Key words: tooth luxation; crown fractures; pulpal healing; pulp sensibility tests accuracy Correspondence to: Juliana Vilela Bastos, Faculdade de Odontologia, UFMG, Campus Pampulha Av.Presidente, Ant^onio Carlos 6627, CEP , Brazil Tel.: Fax: Accepted 20 July, 2013 Abstract Background/Aim: The assessment of pulp vitality is one of the major challenges in dental traumatology due to the temporary loss of sensibility after trauma and because of the limitations of conventional pulp tests. The aim of this study was to evaluate pulpal response to sensibility tests and to determine their accuracy after crown fractures and luxation injuries. Materials and methods: A total of 121 permanent anterior teeth from 78 patients treated at the Dental Trauma Clinic of the Federal University of Minas Gerais were evaluated. Responses to pulp sensibility tests were monitored for a minimum period of 24 months or until the diagnosis of pulp necrosis. Results: At the first appointment, 68 teeth responded positively to sensibility tests, one tooth was necrotic and 52 teeth did not respond to sensibility tests but showed no other signs of necrosis. The initial lack of response was not associated with age (P = 0.18), but was related to the presence of luxation (P < 0.001). At the final appointment, 87 teeth were classified as vital and 31 were classified as non-vital. While a positive response shortly after trauma was a good predictor of vitality, a lack of response was not associated with subsequent necrosis. The final pulpal condition of the teeth that initially did not respond was associated with the type of injury, as displaced teeth tended to develop necrosis (P = 0.008). The accuracy of each sensibility test at the initial and final appointments was, respectively, 55.1% and 67.8% for the heat test, 55.9% and 77.9% for the cold test, and 57.6% and 89% for the electrical test. Conclusions. A temporary loss of sensibility was a frequent finding during post-traumatic pulpal healing, especially after luxation injuries. All sensibility tests presented low accuracy shortly after trauma. The electrical test provided the best support for pulpal diagnosis after long-term follow up. The clinician must be aware of additional signs of crown discoloration and radiographic changes before initiating endodontic treatment. Traumatic dental injuries may damage hard dental tissues and pulpal and periodontal structures, compromising function and aesthetics and cause emotional problems, especially among children and adolescents (1, 2). Immediately after an acute dental trauma, healing events begin in an attempt to regenerate nerves and vessels and to replace damaged pulpal tissue (3 12). Within this period, there is also an urgent need to define the pulpal condition in order to restore the aesthetics and function of the affected teeth. However, this diagnosis is a challenge for the clinician due to the temporary loss of pulpal sensibility after trauma (13 26) and to the limitations of conventional pulp tests (27 29). Despite its controversial value after traumatic dental injuries, pulp sensibility testing still represents the most widely used diagnostic procedure for the assessment of pulp vitality. Accuracy is a characteristic used to describe the quality and usefulness of a diagnosis test. This characteristic can be defined as the proportion of all correct results of a diagnostic test, both positive and negative, and is expressed through sensitivity and specificity, negative predictive values (NPV) and positive predictive values (PPV) (30 33). Nevertheless, studies concerning the accuracy of pulp sensibility tests after trauma are non-existent. Therefore, the purpose of this study was to evaluate the pulpal response to thermal and electrical sensibility tests, determining the accuracy of such tests after traumatic dental injuries. Materials and methods The sample comprised 78 patients with 121 teeth with crown fractures and luxations, either isolated or associated, which were treated at the Dental Trauma Clinic of the School of Dentistry at the Federal University of Minas Gerais in Belo Horizonte, Brazil. The subjects ages at the time of injury ranged from 6.3 to 22.5 years (mean ). The distribution by injured tooth group was as follows: 86% maxillary central incisors, 11.6% maxillary lateral incisors and 2.4% mandibular incisors. Teeth were grouped into five categories as follows: Group 1 (G1) 39 teeth with enamel and dentin fractures (32.2%); Group 2 (G2) 30 teeth with 1

2 2 Bastos et al. enamel and dentin fractures associated with concussion or subluxation (24.8%); Group 3 (G3) 6 teeth with enamel and dentin fracture associated with tooth displacement (5.0%); Group 4 (G4) 29 teeth with concussion or subluxation (24.0%); Group 5 (G5) 17 teeth with lateral or extrusive luxation (14.0%). Patients were treated and underwent follow-up examinations to observe the pulpal condition according to established guidelines (34). The following clinical data concerning the pulpal condition were collected at the initial visit and during the follow-up appointments: tooth colour, response to pulp sensibility tests, tenderness to percussion and the presence of swelling or fistula. The sensibility tests consisted of thermal (refrigerant spray and hot gutta-percha) and electrical pulp tests. All teeth were tested with all three methods, and the tests were performed by one of the authors (JVB) after drying the tooth with air and isolating it with a cotton roll. A 2-min interval between different tests was observed. The cold test with refrigerant spray consisted of placing a cotton pellet soaked with a pressurized mixture of butane, propane and isobutane (Endo-Frost; Roeko, Langenau, Germany) on an intact surface of the tooth. The heat test consisted of the application of Gutta-percha, heated to melting temperature, on a previously lubricated intact surface of the tooth. Thermal tests were applied for up to 10 s, and patients were instructed to indicate when they felt a light sensation of pain, which was recorded as a positive response. A negative response was recorded if the tooth failed to respond twice consecutively in the same section. For the electrical test, the Analytic Technology Pulp Tester (Analytic Technology Redmond, WA, USA) was used. The tooth was lubricated with toothpaste to facilitate the conduction of electrical impulses, and the probe tip was placed on an intact surface within the incisal two-thirds of the crown. The rate of voltage increase was set midway between fast and slow, and this rate was used throughout the study. A tingling sensation felt by the patient, at any level of the scale, was considered to be a positive response. A negative response was established after the digital display reached its maximum level of 80, with no reaction from the patient, twice consecutively in the same section. Radiographic data collected during the initial and follow-up examinations included the presence and type of root resorption, periapical lesions and pulp canal obliteration (PCO). The standardization of radiographs was based on previously defined criteria (34). Occlusal radiographs were taken in the first examination with the bisecting angle technique, using a large film (size 4; Kodak â Ultra-speed, Eastman Kodak Company, Rochester, NY, USA). The orientation of the central beam was directed between the two central incisors. Periapical radiographs were taken in the first visit and during the follow-up examination, with the paralleling technique, using a small film (Kodak â Ultra-speed DF 58, size 2), and film holders with a fixed object focus distance of 33 cm (Cone â ; Maquira Dental Products, Maringa, PR, Brazil). The orientation of the central beam was directed between the two central incisors or between the right or left lateral and central incisors depending upon the traumatized teeth. All radiographs were taken at 70 kvp, 8 ma (Spectro 70X Eletronic â Dabi Atlante S/A Medical & Dental Industry, Ribeir~ao Preto SP, Brazil). The diagnosis of necrosis was based on the presence of dark coronal discoloration, the absence of a response to pulp sensibility tests, the presence of fistulas, or the presence of radiographic signs of periapical bone resorption or inflammatory external root resorption. The absence of a response to pulpal sensibility tests was considered to be a criterion for the diagnosis of necrosis only when associated with one of the other signs described above. Patients were first seen up to 1 month after the trauma and were followed for at least 24 months or until teeth became necrotic. Patients whose teeth initially responded positively to tests were evaluated every 3 months for a minimum period of 24 months. Patients whose teeth did not respond initially were followed monthly until necrosis was confirmed or a positive response to sensibility tests was obtained; after a positive response, patients were re-evaluated every 3 months for a minimum period of 24 months. Therefore, the mean follow-up period was 20.2 months, ranging from 2 to 67 months. Patients who had suffered previous trauma were not included. Similarly, those patients who suffered a second injury during the follow-up period were excluded. For these cases, only data obtained up to the moment of the second trauma were recorded. Statistical analysis was performed using Epi-info software (35). To determine the frequency distribution, the Chi-squared (v 2 ) test and Fisher s exact test were used. The confidence interval at 95% was calculated for measures of association, sensitivity, specificity, PPV and NPV. All tests showing p values less than 5.0% (0.05) were considered to be significant. Approval was obtained from the Human Ethics Committee of the Federal University of Minas Gerais (COEP- UFMG). Results During the first month after trauma, 53 teeth did not respond positively to sensibility tests. Of these, one tooth showed a grey brown discoloration and was considered to be necrotic. The other 52 teeth did not show any other signs of necrosis. Sixty-eight teeth responded positively to at least one of the sensibility tests applied. During the follow-up period, 31 teeth developed necrosis (25.6%) and 87 teeth were considered to be vital (71.9%). Three teeth could not have their pulp condition defined because the patients abandoned the study and were excluded from the analysis. Table 1 shows the correlation between the initial response to sensibility tests and the final pulpal status. The initial response was considered to be negative when teeth showed an absence of sensibility to all tests and positive when teeth responded to at least one of the tests performed. Only 19 teeth that had an initial negative response were classified as non-vital in the final visit (38%). The majority of teeth that showed a positive initial response to pulp sensibility tests were vital at the final appointment (82.4%).

3 Pulpal sensibility after traumatic injuries 3 Table 1. Association between the initial response to pulp sensibility tests and final pulp condition Initial response to pulp sensibility tests Final pulpal condition Non-vital n(%) Vital n(%) Negative 19 (38.0) 31 (62.0) 50 (100) Positive 12 (17.6) 56 (82.4) 68 (100) Total 31 (26.3) 87 (73.7) 118 (100) v 2 = 5.16; P = Table 2. Association between the age at the moment of trauma and pulp response to sensibility tests at the first visit Age at trauma Initial response to pulp sensibility tests Negative n(%) Positive n(%) < 9 years 23 (51.1) 22 (48.9) 45 (100) 9 years 27 (37.0) 46 (63.0) 73 (100) Total 50 (42.4) 68 (57.6) 118 (100) v 2 = 1.73; P = Table 3. Association between the type of the injury and initial response to pulp sensibility tests Type Initial response to pulp sensibility tests Negative n(%) Positive n(%) Crown fractures 6 (15.4) 33 (84.6) 39 (100) Crown fractures associated 10 (33.3) 20 (66.7) 30 (100) with concussion or subluxation Crown fractures associated 2 (33.3) 4 (66.7) 6 (100) with lateral or extrusive luxation Concussion or subluxation 18 (64.3) 10 (35.7) 28 (100) Lateral or extrusive luxation 14 (93.3) 1 (6.7) 15 (100) Total 50 (42.4) 68 (57.6) 118 (100) v 2 = 34.30; P < No significant association between age and the response to sensibility tests was found when the cut-off point was established at the age of 9 years (Table 2). Initial negative response to the sensibility tests was found to be related to the occurrence of tooth luxation injuries (Table 3). When examining the final pulp condition of the 50 teeth that did not respond to sensibility tests at the first visit, a significant association was found between tooth displacement and the development of necrosis (Table 4). The time of obtaining vitality for teeth that initially responded negatively to pulp sensibility tests ranged from 2 to 67 months. The time for conclusive diagnosis of necrosis ranged from 2 to 30 months. There was a significant difference between the median months for vitality and necrosis diagnosis (the 12th month and the 4th month, respectively) (Kruskal Wallis = 7.9, P = 0.005). In this study, there was no association between the type of the injury and the time of diagnosis of necrosis (v 2 = 0.00, P = 0.97). Table 4. Association between the type of the injury and final pulp condition in teeth with initial negative response to pulp sensibility tests Type The accuracies of pulp sensibility tests performed just after trauma (Table 5) and at the final appointment (Table 6) were calculated using the sensitivity, specificity and predictive values. Discussion Final pulp condition Non-vital n(%) Vital n(%) Crown fractures 6 (100) 6 (100) Crown fractures associated 4 (40.0) 6 (60) 10 (100) with concussion or subluxation Concussion or subluxation 4 (22.2) 14 (77.8) 18 (100) Crown fractures associated 9 (64.3) 5 (35.7) 14 (100) with lateral or extrusive luxation Lateral or extrusive luxation 2 (100.0) 2 (100) Total 19 (38.0) 31 (62) 50 (100) Fisher s exact test P = The assessment of pulp vitality is one of the major challenges in dental traumatology, especially during the period immediately after trauma, and important factors that affect this assessment must be considered. The temporary loss of pulpal sensibility is an important issue (13 25) and was confirmed in the present study. An initial negative response to sensibility tests was not associated with the later development of pulp necrosis. Although an immediate negative response indicated pulpal damage, this response did not predict pulp necrosis because sensibility tests assess nerve activity rather than the vascular supply, which is ultimately responsible for pulp survival (27, 29). As neural regeneration in traumatized teeth is slower than vascular regeneration or is even absent, the tooth may remain vital even though it does not respond to sensibility tests (10, 36, 37). The present findings showed that most of the teeth with concussion or subluxation that did not respond to initial tests recovered a positive response, while displaced teeth tended to develop necrosis. This outcome is in accordance with previous clinical (15, 19 21, 23, 26) and experimental data and corroborates the theory that transient damage to pulpal nerve fibres explains the transition from a negative to a positive response to sensibility tests (37). The time elapsed from the moment of trauma should also be considered when evaluating the pulp s response after trauma. This study analysed the time interval between trauma and the definitive diagnosis of the pulp condition. It is important to stress that only teeth that initially responded negatively to pulp sensibility tests were included. Necrosis was confirmed significantly earlier than pulp vitality, and these results are consistent with results presented in the literature. (18, 19, 21). Another factor that must be taken into account is that pulp testing in young patients has technical and psychological limitations (27, 29, 38 40). Studies

4 4 Bastos et al. Table 5. Accuracy sensitivity, specificity and predictive values of pulp sensibility tests performed at the first visit Test Sensitivity Specificity Negative Predictive Value (NPV) Positive Predictive Value (PPV) Accuracy Heat (Gutta-percha) 50.6% ( ) 67.7% ( ) 81.5% ( ) 32.8% ( ) 55.1% ( ) Cold (Endo-Frost) 64.5% ( ) 52.9% ( ) 80.7% ( ) 32.8% ( ) 55.9% ( ) Electric 61.3% ( ) 56.3% ( ) 80.3% ( ) 33.3% ( ) 57.6% ( ) Confidence interval 95%. Table 6. Accuracy sensitivity, specificity and predictive values of pulp sensibility tests performed at the final visit Test Sensitivity Specificity Negative Predictive Value (NPV) Positive Predictive Value (PPV) Accuracy Heat (Gutta-percha) 87.1% ( ) 60.9% ( ) 93.0% ( ) 44.3% ( ) 67.8% ( ) Cold (Endo-Frost) 83.9% ( ) 75.9% ( ) 93.0% ( ) 55.3% ( ) 77.9% ( ) Electric 90.3% ( ) 88.5% ( ) 73.7% ( ) 96.3% ( ) 89.0% ( ) Confidence interval 95%. conducted in non-traumatized young permanent teeth reported an increased threshold to electrical stimulation (38 40) or the absence of a response (41). In the present study, the absence of a response to pulp sensibility tests in the initial visit could not be linked to age. This phenomenon corroborates previous results in teeth bearing crown fractures (13, 18), but conflicts with the results presented by Rock and Grundy (20), who found an increase in the temporary loss of sensibility among children younger than 9 years of age with luxated and subluxated teeth. Differences in sampling and methodology between the previous studies and the present one may explain the discrepant results. Finally, it is important to emphasize the limitations of conventional pulp sensibility tests. Studies that calculated the accuracy of such tests in non-traumatized teeth demonstrated that these tests were better predictors of the absence of pulp disease than its presence. In other words, current pulp tests are more valid in identifying vital teeth than necrotic teeth (30 33). Although many studies have reported the temporary loss of pulp sensibility after traumatic injuries (13, 14, 17, 18, 20, 21, 23, 26), the present study was the first to calculate predictive values and accuracy of pulp sensibility tests carried out in traumatized teeth. Such an analysis was performed by comparing the initial and final responses to thermal and electrical tests with the final diagnosis of pulpal status established during long-term follow up. The pulp condition was classified as non-vital only if one of the following signs were found: crown discoloration, fistula, periapical bone resorption and/or inflammatory external root resorption. Accuracy was calculated based on predictive values because the sample consisted of patients with unknown disease states. There was a high probability that an initial positive response would be later confirmed as pulp vitality, as evidenced by the high NPV found in the first visit. However, all tests failed to disclose disease (necrosis). There was a small probability that a non-sensitive reaction observed in the first visit would be associated with necrosis, as shown by low PPV. This analysis reveals a low accuracy for all pulp sensibility tests when they are applied soon after trauma. The present results also demonstrated that heat tests maintained a low accuracy over time, whereas cold tests with refrigerant spray and electrical tests showed higher accuracy values in the final exam. Electrical tests provided the best support for pulpal diagnosis due to the high number of correct results among necrotic teeth in the final visit, demonstrated by the high PPV. Even though current results showed similarities and differences with those reported for non-traumatized teeth, this comparison remains impaired by the major differences between the samples. While only traumatized incisors from children with a mean age of 10.6 years were evaluated in the present study, previous studies included only non-traumatized teeth, of all groups, from adult patients. In conclusion, the present results showed that a positive reaction to pulp sensibility tests during the period immediately after trauma represented a good prediction of vitality; however, the lack of response could not be associated with the later development of pulp necrosis. Our results confirm that the temporary loss of sensibility is a frequent finding during post-traumatic pulpal healing, especially after luxation injuries. While all sensibility tests exhibited a low accuracy shortly after trauma, the electrical test provided the best support for pulpal diagnosis after traumatic injuries due to its high long-term accuracy. Acknowledgements This research was funded by Dean of Extension PROEX-UFMG. References 1. Cortes MIS, Sheiham A, Marcenes W. Impact of traumatic injuries to the permanent teeth on oral-health related quality of life of 12 to 14 year old Brazilian school-children. Community Dent Oral Epidemiol 2002;30: Traebert J, de Lacerda JT, Foster Page LA, Thomson WM, Bortoluzzi MC. Impact of traumatic dental injuries on the quality of life of schoolchildren. Dent Traumatol 2012; 28: Stanley HR, Weisman MI, Michanowicz AE, Bellizzi R. Ischemic infarction of the pulp: sequential degenerative changes of the pulp after traumatic injury. J Endod 1978;4:25 55.

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Pulp and root development after partial extrusion in immature rat molars: a histopathological study. Endod Dent Traumatol 1998;14: Ozcßelik B, Kuraner T, Kendir B, Asßan E. Histopathological evaluation of the dental pulps in crown-fractured teeth. J Endod 2000;26: Skieller V. The Prognosis for young teeth loosened after mechanical injuries. Acta Odontol Scand 1960;8: Teitler D, Zadick DT, Eidelman E, Chosack A. A clinical evaluation of vitality tests in anterior teeth following fracture of enamel and dentin. Oral Surg Oral Med Oral Pathol 1972;34: Bhaskar S, Rappaport H. Dental vitality tests and pulp status. J Am Dent Assoc 1973;86: Barkin PR. Time as a factor in predicting the vitality of traumatized teeth. ASDC J Dent Child 1973;40: Rock NP, Gordon PH, Friend LA, Grundy MC. The relationship between trauma and pulp death in incisor teeth. Br Dent J 1974;136: Zadik D, Chosack A, Eidelman E. The prognosis of traumatized permanent anterior teeth with fracture of the enamel and dentin. Oral Surg Oral Med Oral Patol 1979;47: Jacobsen I. Criteria for diagnosis of pulp necrosis in traumatized permanent incisors. Scand J Dent Res 1980;88:306 l Rock NP, Grundy MC. The effect of luxation and subluxation upon the prognosis of traumatized incisor teeth. J Dent 1981;9: Ravn JJ. Follow-up study of permanent incisors with enamel dentin fractures after acute trauma. Scand J Dent Res 1981;89: Andreasen FM, Pedersen BV. Prognosis of luxated permanent teeth the development of pulp necrosis. Endod Dent Traumatol 1985;1: Andreasen FM. Transient apical breakdown and its relation to color and sensitivity changes after luxation injuries to teeth. Endod Dent Traumatol 1986;2: Andreasen FM. Pulpal healing after luxation injuries and root fractures in the permanent dentition. Endod Dent Traumatol 1989;5: Rusmah M. Traumatized anterior teeth in children. A 24-month follow-up study. Aust Dent J 1990;35: Crona-Larsson G, Bjarhason S, Noren JG. Effect of luxation injuries on permanent teeth. Endod Dent Traumatol 1991;7: Gopikrishna V, Pradeep G, Venkateshbabu N. Assessment of pulp vitality: a review. Int J Paediatr Dent 2009;19: Newton CW, Hoen MM, Goodis HE, Johnson BR, McClanahan SB. Identify and determine the metrics, hierarchy, and predictive value of all the parameters and/or methods used during endodontic diagnosis. J Endod 2009;35: Andreasen FM, Andreasen JO, Tsukiboshi M. Examination and diagnosis of dental injuries. In Andreasen JO, Andreasen FM, Andersson L, editors. Textbook and color atlas of traumatic injuries to teeth, 4th edn. Oxford: Blackwell Publishing; p Hyman JJ, Cohen ME. The predictive value of endodontic diagnostic tests. Oral Surg Oral Med Oral Pathol 1984;58: Peterson K, S oderstr om C, Kiani-Anaraki M, Levy G. Evaluation of the ability of thermal and electrical tests to register pulp vitality. Endod Dent Traumatol 1999;15: Gopikrishna V, Tinagupta K, Kandaswamy D. Evaluation of Efficacy of a new custom-made pulse oximeter dental probe in comparison with the electrical and thermal tests for assessing pulp vitality. J Endod 2007;33: Chen E, Abbott PV. Evaluation of accuracy, reliability, and repeatability of five dental pulp tests. J Endod 2011;37: Andreasen FM, Andreasen JO. Diagnosis of luxation injuries. The importance of standardized clinical, radiographic and photographic techniques in clinical investigation. Endod Dent Traumatol 1985;1: Dean AG, Dean JA, Coulombier D, Brendel KA, Smith DC, Burton AH et al. Epi info, Version 6: a word processing, database, and statistics program for epidemiology on microcomputers. Atlanta, Georgia: Centers of Disease Control and Prevention; Schendel KU, Schawartz O, Andreasen JO, Hoffmeister B. Reinnervation of autotransplanted teeth. A histological investigation in monkeys. Int J Oral Maxillofac Surg 1990;19: Pilleggi R, Dumsha TC, Myslinksi NR. The reliability of eletric pulp test after concussion injury. Endod Dent Traumatol 1996;12: Fulling H-J, Andreasen JO. Influence of maturation status and tooth type of permanent teeth upon electrometric and thermal pulp testing. Scand J Dent Res 1976;84: Fuss Z, Trowbridge H, Rickoff B, Sorin S. Assessment of reliability of electrical and thermal pulp testing agents. J Endod 1986;12: Brandt K, Kortegaard K, Poulsen S. Longitudinal study of electrometric sensitivity of young permanent teeth. Scand J Dent Res 1988;96: Klein H. Pulp responses to an electric pulp stimulator in the developing permanent anterior dentition. ASDC J Dent Child 1978;45:

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