Assessing revascularization of avulsed permanent maxillary incisors by laser Doppler flowmetry HEINRICH STROBL, GERALD GOJER, BURGHARD NORER

and RDIGER EMSHOFF J Am Dent Assoc 2003;134;1597-1603

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ABSTRACT
Background. Laser Doppler flowmetry, or LDF, is a noninvasive method used to assess pulpal blood flow, or PBF. Dental avulsion is associated with loss of pulpal sensitivity. The authors conducted this study to assess whether LDF could be used to detect revascularization of replanted teeth. Methods. The authors used LDF to assess the PBF values of avulsed permanent maxillary incisors treated using replantation and splinting in 17 subjects. They took measurements at four sessions: on the day of splint removal and at 12 weeks, 24 weeks and 36 weeks after splint removal. Five vital control teeth and five nonvital control teeth were used to assess the background signal. At 36 weeks, the authors determined clinically and radiographically whether revascularization had occurred. Results. LDF readings correctly predicted the pulp status in 88.2 percent of the readings. Of the readings for vital teeth, 100 percent were correct, and of the readings for nonvital teeth, 80 percent were correct. Univariate analysis of variance demonstrated that in revascularized teeth, the PBF value increased significantly from splint removal to week 12 after splint removal and from week 24 to week 36 after splint removal. In the teeth that failed to revascularize, the PBF value dropped significantly from week 24 to week 36 after splint removal. Conclusions. The results of this study suggest that LDF accurately diagnoses revascularization of avulsed maxillary incisors after replantation and splinting. Clinical Implications. LDF may become useful in detecting revascularization much earlier than standard sensitivity tests.

Assessing revascularization of avulsed permanent maxillary incisors by laser Doppler flowmetry

HEINRICH STROBL, M.D., D.M.D.; GERALD GOJER, M.D., D.M.D.; BURGHARD NORER, M.D., D.M.D.; RDIGER EMSHOFF, M.D., D.M.D.

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ental injuries to permanent incisors are a frequent finding after orofacial trauma. In epidemiologic studies, the prevalence of traumatized permanent anterior teeth varied from 2.6 to 30 percent.1-12 Traumatically avulsed permanent teeth require a splint for stabilization after replantation.13,14 The treatment outcome of avulsed teeth can be influenced by several factors such as concomitant dentoalveolar injuries, root formation stage, time elapsed between trauma and treatment, the preservation conditions of Laser Doppler the avulsed tooth and the type of flowmetry may dental trauma splint. The course of the become useful in severed periodontal ligaments healing detecting and the neurovascular supply to the revascularization pulp determine the treatment outcome of the avulsed teeth.15-22 much earlier Electrical and thermal pulp tests than standard are unreliable after a traumatic sensitivity tests. dental injury, and there may be no response to both tests even if the circulation is restored.23,24 Therefore, the clinical evaluation of a traumatized tooth requires symptomatic, visual and radiographic assessment. If the tooth becomes necrotic and infected, external inflammatory root resorption may occur, which may result in tooth loss in a short period.25 In teeth with incomplete root formation, circulation survival and revascularization are possible23,25,26 and highly desirable, not only to maintain an infection-free pulp space

but also to allow the tooth to continue to develop and strengthen. Measuring pulpal blood flow, or PBF, using laser Doppler flowmetry, or LDF, has been described as being a more sensitive technique for evaluating tooth vitality than using conven1597

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tional methods such as electrical and thermal layer of bonding agent (Heliobond, Ivoclar pulp testing.27,28 Several authors reported using Vivadent) to the etched enamel surface using a flowmetric values to demonstrate the remicrobrush and left it on for 20 seconds before we establishment of vitality in traumatized teeth27polymerized it with a light source for another 40 29 or to show significant blood flow reduction in seconds. the maxillary teeth of patients who underwent Apparatus. We took PBF measurements with Le Fort I osteotomy.30-35 In instances of dental a laser Doppler flowmeter (Periflux 4001 Master, trauma, LDF may be useful in detecting tranPerimed, Jrflla, Sweden). Light with a wavesient ischemic episodes and identifying teeth at length of 632.8 nanometers was produced by a risk of developing adverse sequelae such as 1-milliwatt helium-neon laser within the avascular necrosis and tissue loss. flowmeter and was transmitted along a flexible As longitudinal avulsion typerelated LDF fiber-optic conductor inside a specially designed PBF data are not available in the literature, we round dental probe that was 2 millimeters in conducted this study to evaluate the efficacy of diameter (PeriFlux Probe 416, Perimed).23,31-33 A LDF in diagnosing revascularization of avulsed fraction of the backscattered light from the tooth permanent maxillary central was returned to the flowmeter incisors after replantation and along a pair of afferent optical splinting. fibers within the probe. The optical Laser Doppler fibers diameter was 125 micromeflowmetry may be MATERIALS AND METHODS ters, and the fiber-to-fiber distance useful in detecting Subjects. The study group comwas 500 m. The flowmeter then transient ischemic prised 17 subjects who were underprocessed the amount of Dopplerepisodes and going replantation and splinting shifted light that was returned and after dental trauma. Ten subjects produced an output signal. The identifying teeth at were female, and seven were male; measured voltage is linearly risk of developing their mean age was 9 years (range, related to the flux of red blood cells adverse sequelae. 7 to 10 years). The subjects parents (number of cells multiplied by their or guardians were informed about average velocity) encountered the study procedure, and we within the tooth and represents a relative PBF measure. received informed consent from each subjects We calibrated the flowmeter before each data parent or guardian. Inclusion criteria were prescollection session. We adjusted the narrow band ence of a single maxillary central incisor affected to read zero voltage when the probe was placed by an avulsion type injury, absence of concomiagainst a motionless object, while we used a tant dentoalveolar injuries and that trauma had commercially available motility standard (Peroccurred within the past two hours. We treated imed) to calibrate the flowmeter on the wide each of the subjects with a 0.16- by 0.50-inch band to a specific value of 250 perfusion units, standard edgewise wire (Leibinger, Mlheim, or PUs. We activated the artifact filter and colGermany). We did not collect LDF data if a maxillected the PBF data on a wide band setting. lary incisor was missing or the injured maxillary Voltage output values were sent from the central incisor had a crown, had received flowmeters RS-232 port at a rate of 32 signals endodontic treatment or had a large restoration. Splint application. We bonded the splints to per second to a computer for storage and subsethe labial aspect of both the lateral and central quent analysis. maxillary incisors. We cut the wire to the desired PROCEDURE length and then adapted it to the curvature of the incisors using pliers. We secured the splints with We took the measurements on the labial aspect of light-curing composite. After placing cotton rolls each experimental tooth about 5 mm from the in the vestibule, we air-dried the incisors. We gingival margin. Each subject underwent four etched the enamel surface with 37 percent phosmeasurement sessions: on the day of splint phoric acid gel (Totaletch, Ivoclar Vivadent, Ellremoval (T1), at 12 weeks after splint removal wangen, Germany) for 30 seconds. We then rinsed (T2), at 24 weeks after splint removal (T3) and at off the gel with water from the dental unit and 36 weeks after splint removal (T4). To ensure air-dried the etched surfaces. We applied a thin accurate and reproducible spatial positioning of
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the probe at each session, we prepared custommade clear plastic splints (Bioplast, ScheuDental, Iserlohn, Germany) that covered the maxillary teeth and provided appropriately placed holes with a diameter similar to that of the flowmeter probe. At each measurement session, we had the subject rest in a supine position in the dental chair for approximately 10 minutes and then we collected blood flow data for three minutes. At the end of the follow-up sessions, we assessed revascularization both clinically and radiographically. Our criteria for diagnosing a vital tooth were the absence of clinical symptoms, the absence of periapical radiolucency and a positive response to sensitivity testing. We diagnosed a nonvital tooth if there was progressive gray discoloration of the crown, a reaction to percussion, a periapical radiolucency and an unresponsiveness to sensitivity testing.36-38 The clinical diagnostic procedures we used included sensitivity testing with carbon dioxide ice, percussion and mobility testing with a calibrated instrument (Periotest, Medizintechnik Gulden, Bensheim, Germany), and evaluation of crowns for the presence of color changes.38 The radiographic examination of the anterior region consisted of one occlusal film and three periapical exposures, in which the central beam was directed between the lateral and central incisors and between the central incisors.38 We found that seven of the 17 avulsed teeth were vital while 10 teeth were nonvital. To eliminate background signals and thus isolate the signal from the pulp, we had to eliminate reflected signals from the surrounding periodontal structures. At each session, we used five vital control teeth and five nonvital control teeth to assess the background signal. In 10 subjects, when we took measurements for an avulsed and splinted permanent maxillary incisor, we selected the respective contralateral homologous tooth as a control. The five vital control teeth remained vital during the follow-up. Using the control data as a template, a single evaluator (H.S.) assessed the 17 teeth as vital or nonvital. He considered the teeth to be vital if the flowmetric signals at T2 were similar to those of the positive controls or if a continuous increase of PBF value occurred from T1 to T2. He considered the teeth to be nonvital if the flowmetric signals at T2 were similar to those of the negative controls or if the PBF value decreased dramatically from T1 to T2. He then

correlated the assessments with the vitality statuses that were determined clinically and radiographically at T4. Data analysis. We calculated the mean PUs for each recording site during each session by averaging each of the PUs collected for three minutes, or 180 seconds. We excluded PUs that registered as movement artifacts from this average. We used univariate analysis of variance, or ANOVA, for repeated measurements to test for statistically significant differences between session-related variations in PBF measurements. Statistical significance was set at P < .05. We used the SPSS X package (SPSS, Chicago) for all statistical analyses.

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RESULTS

The LDF data we collected for the five vital control teeth demonstrated that the mean PBF values from T1 to T2 were almost the same (range, 9.9 to 10.4 PUs; mean, 10.2 PUs 1.4 standard deviation, or SD). The PBF values showed heartbeat-synchronous oscillations. The LDF recordings from the five negative controls showed an average PBF value of 4.1 PUs 1.1 SD at T1, and they stayed at almost the same level until the end of follow-up sessions (range, 3.8 to 4.4 PUs; mean, 4.0 PUs 1.1 SD). The heartbeatsynchronous oscillations were irregular and low in amplitude. After the LDF values of the surrounding tissue (negative controls) had been subtracted from the PBF values (positive controls), the net PBF values of the vital control teeth showed that the mean PBF measured was 60.8 percent (range, 56.4-63.5 percent) of the original values. After subtracting the net PBF value of surrounding tissue (negative controls), the net PBF values of the vital teeth ranged from 1.5 to 10.0 PUs. Of the seven teeth we evaluated as vital at T4, five had a net PBF value of between 50 percent and 71.4. percent of the original value at T2. Two teeth had a net PBF value of 33.3 percent and 14.3 percent of the original value, respectively. Thus, in all vital teeth (100 percent), we saw a net PBF value that was distinctly different from that of the nonvital teeth (Table 1). When we subtracted the PBF value of the surrounding tissue (negative controls) from the value at T2, the net PBV value was close to zero. Moreover, the pulsative signal was not present. Of the 10 teeth that we evaluated clinically and radio1599

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TABLE 1

DISTRIBUTION OF TEETH IN VITAL AND NONVITAL GROUPS AND NET PULPAL BLOOD FLOW VALUES AT 12 WEEKS AFTER SPLINT REMOVAL (N = 17).
NET PULPAL BLOOD FLOW (% OF THE ORIGINAL VALUE AT T2*) CLINICALLY AND RADIOGRAPHICALLY VITAL AT T4 CLINICALLY AND RADIOGRAPHICALLY NONVITAL AT T4

were between T3 and T4 (P < .01) and T1 and T4 (P < .05) (Table 2).
DISCUSSION

The results of our study showed that LDF was able to No. of Teeth Teeth (%) No. of Teeth Teeth (%) detect changes in PBF 7 100 2 20 14 values after splint removal. Normal PBF 0 0 8 80 < .05 values for maxillary 7 100 10 100 SUM central incisors in * T2: Twelve weeks after splint removal. adults range from 7.6 T4: Thirty-six weeks after splint removal. PUs to 14 PUs.30,39 From a clinical perspective, it is imporTABLE 2 tant to note that in our MEAN SESSION-RELATED DIFFERENCES IN PULPAL study the PBF values for vital teeth BLOOD FLOW MEASUREMENTS (N = 17). remained above 8.5 TOOTH VITALITY PULPAL BLOOD FLOW VALUE (PERFUSION UNITS SD*) PUs, whereas in nonSTATUS vital teeth the PBF (NO. OF TEETH) Sessions value approached and T1-T2 T2-T3 T3-T4 T1-T4 dropped below 3.5 PUs. 0.5 0.7 2.1 1.9 0.8 0.8 3.4 2.3 Vital (7) Traumatic avulsion 0.9 1.7 0.1 1.1 0.9 0.8 1.9 2.3 Nonvital (10) involves displacement * SD: Standard deviation. of the tooth out of the T1: Immediately after splint removal; T2: 12 weeks after splint removal; T3: 24 weeks after splint removal; alveolar socket. It conT4: Thirty-six weeks after splint removal. P < .05. stitutes 0.5 to 16 per P < .01. cent of all traumatic injuries to permanent anterior teeth,40 it usually involves the maxillary graphically and found to be nonvital at T4, eight (80 percent) had an LDF value of less than 0.05 anterior teeth, and it is more common in the pripercent of the original value at T2. Two teeth did mary dentition than the permanent dentition.2 not fit this pattern, as they had a net PBF value Tooth avulsion is a very complex wound and of 27.2 percent and 33.3 percent of the original involves disruption of the marginal gingival seal, value, respectively. We considered these to be alveolar bone, periodontal ligament fibers, false-negative results (Table 1). cementum and the neurovascular supply to the Using LDF, we correctly assessed tooth vitality pulp.38 Complications after replantation include in all teeth 88.2 percent of the time. Among the ankylosis, pulp necrosis, pulp obliteration, successfully revascularized teeth, we assessed external root resorption and loss of marginal bone 100 percent (seven of seven) correctly, and among support.19,20,41 The most significant prognostic the nonvital teeth, we assessed 80 percent (eight factor for pulpal healing appears to be the stage of 10) correctly. of root formation at the time of injury and the ANOVA for repeated measurements demonperiod between trauma and treatment.42-45 In strated that in teeth we confirmed were revascuteeth with incomplete root formation, blood veslarized, there was a significant increase in PBF sels may pass through the apical foramen, value from T1 to T2 (P < .05), T3 to T4 (P < .05) allowing revascularization and normal root forand T1 to T4 (P < .01). In teeth we confirmed mation to occur. Treatment outcome, however, were nonvital, the only significant differences may depend not only on the root formation stage
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and time elapsed between trauma and treatment, tized incisor, however, is to revascularize and to but also on other factors such as the presence of continue normal root development in immature contamination, the type and condition of storage incisors. Therefore, LDF may be used to monitor medium, concomitant dentoalveolar injuries and incisors during the immediate posttrauma phase, the type of dental trauma splint.46,47 Further and it may help identify revascularization long investigation is necessary to answer the question before it may be detected using traditional sensiabout which additional trauma-related features tivity tests. may have to be defined as diagnostic for disThis study confirms that LDF signals obtained order, namely with significant elevated risk of from human teeth do not reveal the blood flow developing adverse sequelae. solely from the pulp but also reflect blood flow We conducted this study to evaluate the effifrom the surrounding periodontal tissue.56-60 The cacy of LDF in diagnosing revascularization of teeth in the control groups clearly demonstrated avulsed permanent maxillary central incisors that these background readings need to be taken after replantation and splinting. The data indiinto account. It has been proposed that the cate that an accurate LDF reading can be estabreflected signals from nonpulpal tissues in lished at the 12-week follow-up humans be minimized with the use appointment, which is much earlier of opaque black rubber dams.58,60 than would be expected from stanLDF can be used to assess the An accurate laser dard sensitivity tests. The method degree and duration of dental Doppler flowmetry of measuring PBF values is a welltrauma-related ischemic episodes, reading can be established physical assessment of and identify patients who are at established at the pulpal sensitivity and may be used risk of developing adverse sequelae 12-week follow-up as a diagnostic tool in dental trausuch as avascular necrosis and appointment. matology. It also may be a useful tissue loss. Avulsion of an incisor is tool in monitoring PBF in splinted a common traumatic injury in the teeth to optimize the splinting time permanent dentition. Attention and to detect early changes in PBF in replanted should be given to the pulp tissue and periodontal avulsed teeth. A dog model has been used to structures, owing to the high frequency of complidemonstrate revascularization,48-51 and the ability cations after this type of injury. In addition, comof LDF to differentiate vital from nonvital pulp plications may be unpredictable, and the treathas been demonstrated.27,28,52 In our study, LDF ment can become complex. Therefore, the readings were found to be highly accurate in diftreatment has to be adaptable to address any ferentiating a revascularized tooth from a tooth complications that may arise. The outcomes of replantation may vary and may not be prewith necrotic pulp, and an accurate LDF reading dictable from the appearance or extent of injury of pulpal revascularization could be established sustained clinically. about 30 days after reimplantation. In addition, we found a continued increase in blood supply In our study, we did not evaluate the validity of with pulpal blood anastomoses after 30 days, an the revascularization by comparing it with the histologic condition of the pulp. Instead, we make observation that corresponds to the report that our diagnoses on the basis of the clinical and PBF values continued to increase from four weeks radiographic parameters of vital and nonvital to 12 weeks after reimplantation.48 Therefore, it teeth. These findings, however, may be difficult to appears that the LDF assessment for human interpret or even may be misleading. From preteeth should be performed for the first time about vious studies, there appears to be a general agree30 days after trauma and be continued intermitment that single signs such as loss of pulpal sentently for three months. The risk of developing pulp necrosis increases sitivity,23,36,61 coronal dicoloration36 or development with the extent of the injury to the pulp and periof periapical radiolucency37 are not enough to jusodontal ligament and in teeth with complete root tify a diagnosis of pulp necrosis. Even the conformation.37,42 With regard to the high incidence of comitant presence of the these classic signs of pulp necrosis,38,53 prophylactic extirpation of the pulp necrosis may be followed by pulpal repair.37 pulp has been recommended to prevent other Further studies are needed to assess the validity complications from arising from the pulp of posttraumatic PBF measurements taken by necrosis.54,55 The best outcome for the posttraumaLDF by comparing them with histologic tooth
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pulp changes and by determining how well PBF diagnoses can predict course and response to treatments in clinical trials.
CONCLUSION

The results of this study suggest that LDF accurately diagnoses revascularization of avulsed permanent maxillary central incisors after replantation and splinting. Further studies are needed to assess the validity of posttraumatic revascularization by comparing it with histologic tooth pulp changes. LDF may become useful in detecting revascularization much earlier than standard sensitivity tests. s
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