Pulpal response to orthodontic tooth movement in adolescents: A radiographic study Thomas W. Popp, DDS, MSD, ~ Jon Artun, DDS, Dr. Odont., b and Leif Linge, DDS, Dr. Odont. °
Chattanooga, Tenn., Seattle, Wash., and Skien, Norway The purpose of this study was to examine the effect of routine orthodontic treatment on the pulp and periodontal ligament. In a group of adolescent patients who were treated consecutively, radiographs were taken before orthodontic intervention, at the end of retention, and approximately 5 years out of retention. These were compared with radiographs taken at comparable time intervals of a group of patients who had not received orthodontic treatment. Damage to the pulp and the periodontal ligament similar to that seen after traumatic injury was observed only occasionally. A narrowing of the pulp canal was observed from before to after appliance therapy and during the follow-up period in the experimental group. A narrowing of the pulp canal was also seen in the untreated group. Thus this narrowing was interpreted as a normal aging process. (AM J ORTHOD DENTOFACORTHOP 1992;101:228-33.)
T h e consequences of traumatic injuries to the teeth are not limited to coronal fracture, avulsion, or root fracture. Traumatic injuries to teeth may also cause a variety of pulpal responses. Serial posttraumatic examinations of traumatized teeth reveal various frequencies of pulpal necrosis, depending on the type and the severity of the injury. ,.2 If the pulp survives the injury, accelerated dentin deposition is a common finding, with pulp canal obliteration as the result."3 Occasionally, internal resorption is reported. ~ It is usually an inflammatory resorption at the interphase between necrotic and vital tissue in partially necrotic teeth. 5 The periodontium may also be injured during trauma, and in such cases, surface resorption is a common sequela. The resorption lacunae usually repair spontaneously with cementum. However, before the repair, inflammatory resorption may arise from the lacuna if infected necrotic tissue is present in the root canal.1 Total disintegration of the periodontal ligament allows direct contact between cementum and bone, which frequently results in eventual replacement resorption (ankylosis). 1.2 Cervical resorption is apparently a rare complication. The cervical region is less often affected by resorption than the apical and middle portions of the root. This process is not completely understood. 6 Financial support for this study was provided by the University of Washington Orthodontic Alumni Memorial Fund. ~Private practice, Chattanooga, Tenn. bAssociate Professor, Department of Orthodontics, University of Washington, Seattle, Wash. cPrivate practice, Skien, Norway. • 8/1/27597
228
As opposed to traumatic displacement, orthodontic tooth movement is usually a slow response to light force. Nevertheless, the process is considered by some to be a controlled trauma to the tooth-supporting structures. Therefore changes similar to those reported after traumatic injuries may be common. Varying degrees of vascular compression after experimental tooth movement have been documented histologically. 79 Studies using radiorespirometric techniques indicate that orthodontic forces cause a depression of the oxygen utilization system within the pulp cells, l°'1' In addition, histologic studies after tooth movement have shown formation of secondary dentin, ~2disruption of the odontoblastic l a y e r , '3'14 and disturbances in the circulat i o n Y 3 The clinical implication of these observations has not been described. However, one speculation is that alteration in pulpal respiration rate may have a deleterious effect on the long-term vitality of the tooth. ,0 Remodeling of periodontal tissues during orthodontic tooth movement has been extensively studied.'5'16 However, no one has reported damage to the root structure other than surface resorption, particularly at the apex. Recent attempts have been made to clarify the longterm effects of orthodontic tooth movement on the pulp and the periodontium. 17 Researchers examined periapical radiographs of maxillary anterior teeth of 25year-old subjects. Changes similar to those reported after traumatic injuries were shown in 50% of those who were treated orthodontically during adolescence as opposed to only 16% of those without a history of orthodontic therapy. The most frequently observed changes were root canal obliteration (17% versus 8%),
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external resorption (12% versus 5%), and e v i d e n c e of necrosis (14% versus 4%). H o w e v e r , the study design was cross-sectional, and only one set o f m e a s u r e m e n t s was performed. T h e r e f o r e the purpose o f our study was to e x a m i n e longitudinally the incidence o f changes in the pulp and the periodontal ligament during and after routine orthodontic treatment in adolescents and compare them with changes seen in a group o f untreated patients.
MATERIALS AND METHODS Subjects. The experimental material consisted of 100 patients who were consecutively treated from one orthodontic practice. Periapical radiographs of maxillary central and lateral incisors and mandibular central incisors taken with the paralleling long-cone technique were available at treatment start (T1), end of retention (T2), and approximately 5 years out of retention (T3). The control material consisted of 76 patients collected from three different general dental practices. None of these patients had experienced any form of orthodontic treatment. Periapical radiographs of maxillary central and lateral incisors taken with the bisecting angle technique were available at three time intervals (T1, T2, and T3). Eleven patients from the experimental group and 23 controls were eliminated because of unsatisfactory radiographs. Another 14 experimental patients were excluded because they were over the age of 17 years at T1, or because they had not been treated with fixed maxillary appliances. The ages of the remaining 75 patients in the experimental group were 9 to 17 years at T1 (mean, 12.81; SD, 2.06), 12 to 21 years at T2 (mean, 16.29; SD, 2.03), and 17 to 26 years at T3 (mean, 21.25; SD, 2.09). Pretreatment overjet and overbite ranged from - 2 to 10 mm (mean, 4.64; SD, 2.59) and - 4 to 9 mm (mean, 2.97; SD, 2.37), respectively. A total of eight patients reported a history of trauma. The ages of the 53 remaining controls were 10 to 14 years at T1 (mean, 12.62; SD, 0.79), 13 to 16 years at T2 (mean, 15.02; SD, 0.54), and 17 to 21 years at T3 (mean, 19.38; SD, 0.81). Information on the type of occlusion and the exposure to trauma was not available. From the experimental material, a subgroup was formed of 27 patients who had not had mandibular appliances. No differences in age at the different time intervals were observed between the patients in the two subgroups. All patients in the experimental group were treated with fixed edgewise appliances. Radiographic examination. The radiographs were placed in slide mounts and projected onto a screen at 40 times the actual size. However, when corrected for the distance between the observer and the screen, the actual observations were made at about 10 × magnification. For each patient, radiographs made at T1, T2, and T3 were evaluated simultaneously. Evaluation and measurements were performed jointly by two of the authors with a standardized sequence. Pulpal necrosis was indicated by the presence of a root canal filling or periapical radiolucency. Presence of internal replacement resorption, internal inflammatory resorption, ex-
Pulpal response to orthodontic tooth movement
229
ternal replacement resorption (ankylosis), external inflammatory resorption, and cervical resorption were evaluated according to established criteria. 6,'8 Restoration and caries were scored as present or absent. A pulp stone was diagnosed by the presence of a calcified structure in the pulp. ~9 Partial obliteration was diagnosed when a thin line of the pulp canal could be observed, and total obliteration was diagnosed when there was no evidence of the canal. 3 Narrowing of the pulp canal from one time to the next was scored subjectively as present or absent. In addition, the width of the canal was measured at the levels of the cementoenamel junction (CEJ) and at the middle of the root (AP). Measurements were made to the nearest 0.1 mm with prefabricated templates calibrated at 4 mm increments (4 mm = 0.1 mm at 40 × magnification). Different templates were held in position over the pulp canal, and the best fit was determined. Location of the CEJ was determined as the deepest area where the labial outline of the crown overlapped the root. Location of the middle of the root was subjectively determined. Consistency in determination among intervals in individual patients was attempted by orientation according to details in root anatomy. Method error. The reproducibility of the measurements of the pulp canal width was assessed by analyzing the statistical difference between two measurements from radiographs of 10 patients who were randomly selected from each group. The error of the method was calculated with the following equation SX =
/ ~D2 V2N
where D is the difference between duplicate measurements of pulp canal narrowing from one time to the next, and N is the number of double measurements. 2° The error was 0.08 for measurements at the CEJ and 0.06 for measurements at the AP. Pearson's product-moment correlation coefficient between duplicate measurements was r = 0.85 for measurements at the CEJ and r = 0.82 for measurements at the AP. The subjective evaluation of conditions present and the pulp canal narrowing were the same in 95% of the duplicate evaluations. Data analysis. The number of teeth developing radiographic signs of change from T1 to T2 and from T2 to T3 were determined for each patient. From the subjective evaluation, the number of teeth with pulp canal narrowing during treatment and follow-up periods was determined. Fisher's exact tests were used to evaluate statistically significant differences in the frequency of pulp canal narrowing of maxillary incisors between patients from experimental and control groups and of mandibular incisors between the subgroups of patients with and without mandibular appliances. For each tooth in each patient, differences in pulp canal widths at the CEJ and at the AP were calculated from TI to T2 and from T2 to T3. For maxillary central and lateral incisors, differences were calculated between the patients from the experimental and control groups. For mandibular central incisors, differences were calculated between the two subgroups of patients with and without mandibular appliances. The analysis
230
.
~,y°o--. ~'~rtun, and
Linge
Am.
J. Orthod.Dentofac.Orthop. March 1992
Table I. Number and frequency of experimental and control teeth with subjective pulp canal narrowing from before treatment to after treatment (T1 to T2) and from after treatment to follow-up examination (T2 to T3) T1 toT2
T2 to T3
Experimental
Tooth Maxillary Right lateral incisor Right central incisor Left central incisor Left lateral incisor Mandibular Right central incisor Left central incisor
Control
Experimental
Control
No.
Frequency (%)
No.
Frequency (%)
No.
Frequency (%)
No.
Frequency (%)
65 61 58 64
(86.7)* (82.4) (78.4) (85.3)
35 34 43 38
(66.0)* (68.0) (81 .l) (73.1)
74 74 73 75
(98.7) (100) (98.6) (100)
52 48 52 49
(98.1) (94.1) (98.1) (94.2)
34 34
(70.8) (70.8)
18 18
(66.7) (66.7)
48 48
(100) (100)
27 27
(100) (100)
*p < 0.05.
of variance (ANOVA) was used to test any statistically significant differences5 ~Initial width of the pulp canal and time lapse from T1 to T2 and from T2 to T3 were included in the regression model. If significance was indicated, 95% simultaneous confidence intervals were constructed for the difference in mean change for each variable. To test whether actual change in width did occur with increasing age in the groups, both separately and combined, a multivariate t test procedure was used (one-sample Hotelling t2 test)?-~ Regression analyses were used to test the relationship between overjet, overbite, history of trauma at T1, and presence of fillings at T2 and T3 and changes in pulp canal width. Generalized estimating equations were used to account for dependencies in the data caused by multiple observations in each subject. 22
RESULTS
Signs of damage to periodontal ligament. External replacement or inflammatory resorption did not develop in the teeth in the groups. Cervical resorption was diagnosed in a maxillary incisor of one patient from the experimental group at T2. This patient presented with 4 m m overjet, 2 m m overbite, and no history o f trauma before treatment. Signs of repair were evident at T3. Signs of damage to pulp. In a patient in the experimental group who had pretreatment overjet and overbite at 9 m m and 1 mm, respectively, and a history of trauma, a periapical radiolucency from T1 to T2 developed in one maxillary incisor. A filling of identical size was present at all three intervals. Root canal treatment had been performed at T3. In the control group one maxillary incisor without other restorations had a root canal filling at T2 that was not present at T1. The pulp of one maxillary incisor in a patient in the experimental group showed total obliteration at all three observations. In another patient in the same group who
had 3 m m overjet, 5 m m overbite, no history of trauma prior to treatment, and no restorations, the pulp of a maxillary incisor showed partial obliteration at T2 and total obliteration at T3. Pulp obliteration was not observed in the control material. Internal resorption did not develop in the teeth in the groups. Pulp stones. Pulp stones seen at T2 that were not visible at T1 were observed in five maxillary incisors and two mandibular incisors from the experimental group and in two maxillary incisors from the control group. At T3 pulp stones that were not visible at T2 were seen in four maxillary incisors from the experimental group and two maxillary incisors from the control group. Ten additional teeth from the experimental group had pulp stones present at all three times. Caries and restorations. In the experimental group, 0.3% of the maxillary incisors had a restoration at T1, 82.7% at T2, and 99.3% at T3. In the control group, there were no teeth with fillings at T1, 70.8% at T2, and 96.2% at T3. Unfilled caries was not observed. Subjective evaluation of pulp canal narrowing. The majority of teeth from the subjective evaluation showed reduction of pulp canal width from T 1 to T2 (Table I and Fig. 1). Nearly all observed teeth showed reduction from T2 to T3. Differences between the experimental and control groups were statistically significant only for the maxillary right lateral incisor from T 1 to T2. Measurements of pulp canal width changes. The difference in mean changes between the two groups was significant for maxillary right, left central, and lateral incisors both from T1 to T2 (F = 4.58, df = 4/122, P = 0.0018) and from T2 to T3 (F = 4.66, df = 4 / 1 2 2 , P = 0.0016). The 95% simultaneous confidence intervals indicated that the amount of change
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Pulpal response to orthodontic tooth movement
231
ii;i:iii:iiiiiiiiiiii!ijilili
Fig. 1. Periapical radiographs of a typical patient from the experimental group showing pulp canal narrowing over time. A, Before treatment; B, end of retention; C, 5 years after retention.
Table II. Mean changes in width (millimeters) of teeth for each patient in the experimental and control group from before treatment to after retention (T1 to T2) and from after retention to follow-up examination (T2 to T3). Measurements were performed at the CEJ and at the middle of the root (AP). No significant differences were seen between the groups after correction for differences in time interval and differences in initial pulp canal width Maxillary lateral incisor
Maxillary central incisor Experimental
T1-T2 Tl-T2 T2-T3 T2-T3
CEJ AP CEJ AP
Control
Experimental
Mandibular central incisor
Control
Experimental
x
(SE)
x
(SE)
x
(SE)
x
(SE)
x
0.23 0.21 0.24 0.21
(0.02)* (0.02)* (0.02) (0.01)*
0.11 0.13 0.20 0.12
(0.02)* (0.01)* (0.03) (0.01)*
0.17 0.18 0.18 0.15
(0.01)* (0.02)* (0.01) (0.01)*
0.08 0.09 0.17 0.11
(0.01)* (0.01)* (0.02) (0.01)*
0.07 0.06 0.10 0.07
J
Control
(SE)
x
(SE)
(0.01) (0.01) (0.01)* (0.01)
0.09 0.04 0.13 0.09
(0.02) (0.01) (0.01)* (0.01)
*p < 0.05. x = Mean. SE = Standard error of mean, values for contralateral averaged since analyses demonstrated no differences between right and left side.
was different for all variables from T1 to T2 and only for variables at the AP from T2 to T3 (Table II). No difference was found between the two subgroups from T l t o T 2 ( F = 1.42, d f = 2 / 7 1 , P = 0.2491). However, the difference was significant from T2 to T3 (F = 4.01, df = 2/71, P = 0.0225). The simultaneous confidence intervals indicated that the amount of change was different only for variables at the CEJ (Table II). No significant differences in mean changes were seen after correcting for differences in time lapse between observation intervals and for pulp canal width at T1. Changes in pulp canal width from T1 to T2 and T2 to T3 were significantly different from zero (P < 0.001) in both groups. No relationship was found between pretreatment overjet, overbite, and history of
trauma, and changes in pulp canal width. The presence of a filling at T2 was significant in the regression models for change from T1 to T2 (P < 0.01) but not from T2 to T3. DISCUSSION Our study indicates that orthodontic treatment performed during adolescence causes no increased risk of damage to the pulp and the periodontium. Therefore the circulation changes demonstrated histologically7-9'13'j4 and the observed changes in pulpal respiration ~°'j~ incident to experimental tooth movement may be of limited clinical significance. One explanation for this lack of damage is spontaneous tissue repair may occur during periods of rest between orthodontic pro-
232
Popp, Artun, and Linge
Am. J. Orthod. Dentofac. Orthop. March 1992
cedures. Another explanation is the force magnitudes used under usual clinical conditions do not exceed the physiologic limits of healthy dental tissues. Accordingly, on the basis of this study, there is no justification for classifying routine orthodontic tooth movement in adolescents as pathologic. Our results are in marked contrast to the findings of Cwyk et al.]7 They reported change in 50% of the patients who had experienced orthodontic treatment. In their study only one set of measurements was performed. Therefore they could not control for presence of pathosis before the time of appliance therapy. Nor could they rule out etiologic factors other than orthodontic intervention. Finally, the measurements were done by only one observer, and the method error was not reported. Maxillary incisor pulp canal narrowing was more pronounced from before treatment to after treatment in the patients who had experienced orthodontic treatment than in the control patients during a similar period. This finding supports the theory that orthodontic tooth movement stimulates the odontoblasts to form secondary dentin.12 However, narrowing of the pulp canal from one observation to the next also occurred in the control group. Also, it should be noted that the intervals between observations were longer in the experimental grOup than among the controls. In addition, the pulp canals in the patients in the experimental group were measured to be wider initially. No statistically significant differences between the groups were found when we controlled for these discrepancies. These facts support the theory that the pulp canal narrowing observed in our study is a natural aging process. Any additional influence of orthodontic tooth movement may only be minimal. Initial overjet and overbite were not associated with the observed degree of pulp canal narrowing in our material. However, a conclusion that pulpal response is unrelated to the amount of tooth movement should be done with care. Few patients with extreme front-bite deviations were included in the study, and all malrelationships may not have been fully corrected. In addition, our material was limited to the incisors. Only eight subjects in the experimental group reported a history of trauma. Also, information on type and severity of the injury was not available. We are therefore reluctant to make conclusions regarding pulp changes during and after orthodontic movement of teeth subjected to trauma. We had access to detailed information regarding treatment variables, such as length of active appliance therapy and time periods with rectangular arch wires and intermaxillary elastics. However, because of the
negative findings, we did not consider the testing of any relationship between such variables and pulp changes to be meaningful. The pulpal response to orthodontic tooth movement may be different in adults. Particularly, tooth intrusion in patients with reduced tissue support may be associated with a high degree of vascular changes. In a recent study 23 necrosis was diagnosed in seven front teeth in 6 of 24 patients during realignment of teeth that had migrated due to advanced periodontitis. It is possible that compression of periapical vessels and pulpal edema may occur when the forces are transmitted over a smaller percentage of the periodontium. Also, adult patients are more likely to have restorations. Our results give reason to speculate that the presence of fillings increases formation of secondary dentin during orthodontic treatment and retention. The cause of calcified areas within the pulp is unclear. 19 However, our study indicates that orthodontic treatment is not a significnt factor in the development of pulp stones. Blinding is an established way to minimize examiner bias. Accordingly, it may be criticized that individual radiographs were not coded and examined randomly in our study. However, details of tooth alignment and apical structure usually indicated whether a radiograph belonged to a patient who had experienced orthodontic treatment. In addition, variations in apical closure, abrasion of incisal edges, and presence of restorations usually showed whether the radiograph was taken early or late in the series. Our opinion is that simultaneous evaluation of radiographs from all time intervals reduced examiner bias. This observation method allowed evaluation of individual changes in shape and size of pulp canal, pulp stones, external or internal resorptions, and periapical radiolucencies over time. A possible source of error in our analysis was that the middle of the root was located subjectively when measuring pulp canal widths. However, differences in projection from one radiograph to the next, particularly in the control material, ruled out location on the basis of the absolute distances from the CEJ or the apex. Another possibility would have been to use the fraction of the distance to the apex relative to the length of the root. 24 However, then root resorption of the teeth in the experimental material could induce a bias. 2s We tried to ensure consistent location by using root structure as a guide. All evaluations were made jointly by two of the authors, one located close to the screen and one at a distance. Differences in magnification of the radiographs at time of exposure was not accounted for in our study.
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S u c h i n c o n s i s t e n c i e s m a y b e p a r t i c u l a r l y p r e v a l e n t in the control m a t e r i a l . O t h e r p r o b l e m s w e r e the effects o f d i f f e r e n c e s in t o o t h a l i g n m e n t b e f o r e a n d after orthodontic i n t e r v e n t i o n o n the r a d i o g r a p h i c i m a g e . O n e possibility w o u l d b e to m e a s u r e the pulp w i d t h as a f r a c t i o n o f total tooth w i d t h . H o w e v e r , this m e t h o d w o u l d inc r e a s e bias in s i t u a t i o n s w i t h d i f f e r e n c e s in m e s i o d i s t a l projections. It w a s a s s u m e d that any v a r i a t i o n in ima g i n g as the r e s u l t o f r a d i o g r a p h i c d i s t o r t i o n w a s e v e n l y a n d r a n d o m l y d i s t r i b u t e d in the m a t e r i a l . H o w e v e r , it c a n n o t be r u l e d o u t t h a t the finding o f w i d e r p u l p c a n a l s at the first o b s e r v a t i o n in the e x p e r i m e n t a l m a t e r i a l was d u e to a s y s t e m a t i c error. D i f f e r e n c e s in r a d i o g r a p h i c p r o j e c t i o n will o n l y influence the s h a p e o f t h e p u l p c a n a l i m a g e . R a d i o g r a p h i c signs o f p a t h o l o g y are not likely to b e a f f e c t e d . In spite o f the p r o b l e m s w i t h t h e m e t h o d i n h e r e n t in o u r study, we m a y t h e r e f o r e c o n c l u d e that r o u t i n e o r t h o d o n t i c t r e a t m e n t p e r f o r m e d d u r i n g a d o l e s c e n c e c a u s e s minim a l d a m a g e to the p u l p a n d p e r i o d o n t a l l i g a m e n t . T h e o b s e r v e d n a r r o w i n g o f the p u l p canal m a y b e r e g a r d e d as a n o r m a l a g i n g p r o c e s s . We express our sincere gratitude to Drs. K. K. Rognes, A. B. Utkilen, and A. G. Beck Andersen for providing the control material.
REFERENCES 1. Andreasen JO. Luxation of permanent teeth due to trauma: a clinical and radiographic follow-up study of 189 injured teeth. Scand J Dent Res 1970;78:273-86. 2. St~dhaneI, Hedeg~dB. Traumatized permanent teethin children aged 7-15 years. Part II. Swed Dent J 1975;68:157-69. 3. Jacobsen I, Kerekes K. Long-term prognosis of traumatized permanent anterior teeth showing calcifying processes in the pulp cavity. Scand J Dent Res 1977;85:588-98. 4. Arwill T. Histopathic studies of traumatized teeth. Odont Tidskr 1962;70:91-117. 5. Gustafson G, Granath L-E. Pathology of the pulp. In: Gustafson G, ed. Oral pathology for students. Stockholm: Esselte Stadium, 1975. 6. Tronstad L. Pulp reactions in traumatized teeth. In: Gutman J, Harrison J, eds. Proceedings of the International Conference on Oral Trauma. American Association of Endodontists Endowment and Memorial Foundation, 1986:55-77. 7. Butcher E, Taylor A. The vascnlarity of the incisor pulp of the monkey and its alteration by tooth retraction. J Dent Res 1952;31:239-47.
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8. Oppenheim A. Human tissue response to orthodontic intervention of short and long duration. AM J ORTHOD 1942;28:263-301. 9. Butcher E, Taylor A. The effects of denervation and ischemia upon the teeth of the monkey. J Dent Res 1951;30:265-75. 10. Hamersky P, Weimar A, Taintor J. The effect of orthodontic force application on the pulpal tissue respiration rate in the human premolar. AM J ORTHOD 1980;77:368-78. 11. Unterseher R, Nieberg L, Weimar A, Dyer J. The response of human pulpal tissue after orthodontic force application. AM J ORTHOO DENTOFACORTHOP 1987;92:220-4. 12. Marshall JA. A study of bone and tooth changes incident to experimental tooth movement and its application to orthodontic practice. Int J Orthod Dent Child 1933;19:1-17. 13. Stenvik A, Mj0r A. Pulp and dentine reactions to experimental tooth intrusion. AM J ORTHOD 1970;57:370-85. 14. Anstendig H, Kronman J. A histologic study of pulpal reaction to orthodontic tooth movement in dogs. Angle Orthod 1972; 42:50-5. 15. Reitan K. Clinical and histological observations on tooth movement during and after orthodontic treatment. AM J ORTHOD 1967;53:721-45. 16. Rygh P. Ultrastructural changes in pressure zones of human periodontium incident to orthodontic tooth movement. Scand J Dent Res 1973;81:467-80. 17. Cwyk F, Saint-Pierre F, Tronstad L. Endodontic implications of orthodontic tooth movement. IADR Abstracts 1984;#1039. 18. Andreasen JO. Traumatic injuries of the teeth. Philadelphia: WB Saunders; 1981:178-97. 19. Moss-Salentijn L, Hendricks-Klyvert M. Calcified structures in human dental pulps. J Endod 1988;14:184-9. 20. Dalberg G. Statistical methods for medical and biological students. London: George Allen & Ltd., 1940:122-32. 21. Morrison DF. Multivariate statistical methods. San Francisco: McGraw-Hill, Inc. 1976. 22. Liang K-Y, Zeger SL. Longitudinal data analysis using generalized linear models. Biometrikon 1986;73:13-22. 23..~-tun J, Urbye KS. The effect of orthodontic treatment on periodontal bone support in patients with advanced loss of marginal periodontium. AM J ORTHODDENTOFACORTHOP 1988;93:143-8. 24. Schei O, Waerhaug J, Lovdal A, Arno A. Alveolar bone loss as related to oral hygiene and age. J Periodontol 1959;30:7-16. 25. Sj01ien T, Zachrisson BU. Periodontal bone support and tooth length in orthodontically treated and untreated persons. AM J ORTHOD 1973;64:28-37. Reprint requests to: Dr. Jon ,z~-tun University of Washington Department of Orthodontics SM-46 Seattle, WA 98195
Chattanooga, Tenn., Seattle, Wash., and Skien, Norway The purpose of this study was to examine the effect of routine orthodontic treatment on the pulp and periodontal ligament. In a group of adolescent patients who were treated consecutively, radiographs were taken before orthodontic intervention, at the end of retention, and approximately 5 years out of retention. These were compared with radiographs taken at comparable time intervals of a group of patients who had not received orthodontic treatment. Damage to the pulp and the periodontal ligament similar to that seen after traumatic injury was observed only occasionally. A narrowing of the pulp canal was observed from before to after appliance therapy and during the follow-up period in the experimental group. A narrowing of the pulp canal was also seen in the untreated group. Thus this narrowing was interpreted as a normal aging process. (AM J ORTHOD DENTOFACORTHOP 1992;101:228-33.)
T h e consequences of traumatic injuries to the teeth are not limited to coronal fracture, avulsion, or root fracture. Traumatic injuries to teeth may also cause a variety of pulpal responses. Serial posttraumatic examinations of traumatized teeth reveal various frequencies of pulpal necrosis, depending on the type and the severity of the injury. ,.2 If the pulp survives the injury, accelerated dentin deposition is a common finding, with pulp canal obliteration as the result."3 Occasionally, internal resorption is reported. ~ It is usually an inflammatory resorption at the interphase between necrotic and vital tissue in partially necrotic teeth. 5 The periodontium may also be injured during trauma, and in such cases, surface resorption is a common sequela. The resorption lacunae usually repair spontaneously with cementum. However, before the repair, inflammatory resorption may arise from the lacuna if infected necrotic tissue is present in the root canal.1 Total disintegration of the periodontal ligament allows direct contact between cementum and bone, which frequently results in eventual replacement resorption (ankylosis). 1.2 Cervical resorption is apparently a rare complication. The cervical region is less often affected by resorption than the apical and middle portions of the root. This process is not completely understood. 6 Financial support for this study was provided by the University of Washington Orthodontic Alumni Memorial Fund. ~Private practice, Chattanooga, Tenn. bAssociate Professor, Department of Orthodontics, University of Washington, Seattle, Wash. cPrivate practice, Skien, Norway. • 8/1/27597
228
As opposed to traumatic displacement, orthodontic tooth movement is usually a slow response to light force. Nevertheless, the process is considered by some to be a controlled trauma to the tooth-supporting structures. Therefore changes similar to those reported after traumatic injuries may be common. Varying degrees of vascular compression after experimental tooth movement have been documented histologically. 79 Studies using radiorespirometric techniques indicate that orthodontic forces cause a depression of the oxygen utilization system within the pulp cells, l°'1' In addition, histologic studies after tooth movement have shown formation of secondary dentin, ~2disruption of the odontoblastic l a y e r , '3'14 and disturbances in the circulat i o n Y 3 The clinical implication of these observations has not been described. However, one speculation is that alteration in pulpal respiration rate may have a deleterious effect on the long-term vitality of the tooth. ,0 Remodeling of periodontal tissues during orthodontic tooth movement has been extensively studied.'5'16 However, no one has reported damage to the root structure other than surface resorption, particularly at the apex. Recent attempts have been made to clarify the longterm effects of orthodontic tooth movement on the pulp and the periodontium. 17 Researchers examined periapical radiographs of maxillary anterior teeth of 25year-old subjects. Changes similar to those reported after traumatic injuries were shown in 50% of those who were treated orthodontically during adolescence as opposed to only 16% of those without a history of orthodontic therapy. The most frequently observed changes were root canal obliteration (17% versus 8%),
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external resorption (12% versus 5%), and e v i d e n c e of necrosis (14% versus 4%). H o w e v e r , the study design was cross-sectional, and only one set o f m e a s u r e m e n t s was performed. T h e r e f o r e the purpose o f our study was to e x a m i n e longitudinally the incidence o f changes in the pulp and the periodontal ligament during and after routine orthodontic treatment in adolescents and compare them with changes seen in a group o f untreated patients.
MATERIALS AND METHODS Subjects. The experimental material consisted of 100 patients who were consecutively treated from one orthodontic practice. Periapical radiographs of maxillary central and lateral incisors and mandibular central incisors taken with the paralleling long-cone technique were available at treatment start (T1), end of retention (T2), and approximately 5 years out of retention (T3). The control material consisted of 76 patients collected from three different general dental practices. None of these patients had experienced any form of orthodontic treatment. Periapical radiographs of maxillary central and lateral incisors taken with the bisecting angle technique were available at three time intervals (T1, T2, and T3). Eleven patients from the experimental group and 23 controls were eliminated because of unsatisfactory radiographs. Another 14 experimental patients were excluded because they were over the age of 17 years at T1, or because they had not been treated with fixed maxillary appliances. The ages of the remaining 75 patients in the experimental group were 9 to 17 years at T1 (mean, 12.81; SD, 2.06), 12 to 21 years at T2 (mean, 16.29; SD, 2.03), and 17 to 26 years at T3 (mean, 21.25; SD, 2.09). Pretreatment overjet and overbite ranged from - 2 to 10 mm (mean, 4.64; SD, 2.59) and - 4 to 9 mm (mean, 2.97; SD, 2.37), respectively. A total of eight patients reported a history of trauma. The ages of the 53 remaining controls were 10 to 14 years at T1 (mean, 12.62; SD, 0.79), 13 to 16 years at T2 (mean, 15.02; SD, 0.54), and 17 to 21 years at T3 (mean, 19.38; SD, 0.81). Information on the type of occlusion and the exposure to trauma was not available. From the experimental material, a subgroup was formed of 27 patients who had not had mandibular appliances. No differences in age at the different time intervals were observed between the patients in the two subgroups. All patients in the experimental group were treated with fixed edgewise appliances. Radiographic examination. The radiographs were placed in slide mounts and projected onto a screen at 40 times the actual size. However, when corrected for the distance between the observer and the screen, the actual observations were made at about 10 × magnification. For each patient, radiographs made at T1, T2, and T3 were evaluated simultaneously. Evaluation and measurements were performed jointly by two of the authors with a standardized sequence. Pulpal necrosis was indicated by the presence of a root canal filling or periapical radiolucency. Presence of internal replacement resorption, internal inflammatory resorption, ex-
Pulpal response to orthodontic tooth movement
229
ternal replacement resorption (ankylosis), external inflammatory resorption, and cervical resorption were evaluated according to established criteria. 6,'8 Restoration and caries were scored as present or absent. A pulp stone was diagnosed by the presence of a calcified structure in the pulp. ~9 Partial obliteration was diagnosed when a thin line of the pulp canal could be observed, and total obliteration was diagnosed when there was no evidence of the canal. 3 Narrowing of the pulp canal from one time to the next was scored subjectively as present or absent. In addition, the width of the canal was measured at the levels of the cementoenamel junction (CEJ) and at the middle of the root (AP). Measurements were made to the nearest 0.1 mm with prefabricated templates calibrated at 4 mm increments (4 mm = 0.1 mm at 40 × magnification). Different templates were held in position over the pulp canal, and the best fit was determined. Location of the CEJ was determined as the deepest area where the labial outline of the crown overlapped the root. Location of the middle of the root was subjectively determined. Consistency in determination among intervals in individual patients was attempted by orientation according to details in root anatomy. Method error. The reproducibility of the measurements of the pulp canal width was assessed by analyzing the statistical difference between two measurements from radiographs of 10 patients who were randomly selected from each group. The error of the method was calculated with the following equation SX =
/ ~D2 V2N
where D is the difference between duplicate measurements of pulp canal narrowing from one time to the next, and N is the number of double measurements. 2° The error was 0.08 for measurements at the CEJ and 0.06 for measurements at the AP. Pearson's product-moment correlation coefficient between duplicate measurements was r = 0.85 for measurements at the CEJ and r = 0.82 for measurements at the AP. The subjective evaluation of conditions present and the pulp canal narrowing were the same in 95% of the duplicate evaluations. Data analysis. The number of teeth developing radiographic signs of change from T1 to T2 and from T2 to T3 were determined for each patient. From the subjective evaluation, the number of teeth with pulp canal narrowing during treatment and follow-up periods was determined. Fisher's exact tests were used to evaluate statistically significant differences in the frequency of pulp canal narrowing of maxillary incisors between patients from experimental and control groups and of mandibular incisors between the subgroups of patients with and without mandibular appliances. For each tooth in each patient, differences in pulp canal widths at the CEJ and at the AP were calculated from TI to T2 and from T2 to T3. For maxillary central and lateral incisors, differences were calculated between the patients from the experimental and control groups. For mandibular central incisors, differences were calculated between the two subgroups of patients with and without mandibular appliances. The analysis
230
.
~,y°o--. ~'~rtun, and
Linge
Am.
J. Orthod.Dentofac.Orthop. March 1992
Table I. Number and frequency of experimental and control teeth with subjective pulp canal narrowing from before treatment to after treatment (T1 to T2) and from after treatment to follow-up examination (T2 to T3) T1 toT2
T2 to T3
Experimental
Tooth Maxillary Right lateral incisor Right central incisor Left central incisor Left lateral incisor Mandibular Right central incisor Left central incisor
Control
Experimental
Control
No.
Frequency (%)
No.
Frequency (%)
No.
Frequency (%)
No.
Frequency (%)
65 61 58 64
(86.7)* (82.4) (78.4) (85.3)
35 34 43 38
(66.0)* (68.0) (81 .l) (73.1)
74 74 73 75
(98.7) (100) (98.6) (100)
52 48 52 49
(98.1) (94.1) (98.1) (94.2)
34 34
(70.8) (70.8)
18 18
(66.7) (66.7)
48 48
(100) (100)
27 27
(100) (100)
*p < 0.05.
of variance (ANOVA) was used to test any statistically significant differences5 ~Initial width of the pulp canal and time lapse from T1 to T2 and from T2 to T3 were included in the regression model. If significance was indicated, 95% simultaneous confidence intervals were constructed for the difference in mean change for each variable. To test whether actual change in width did occur with increasing age in the groups, both separately and combined, a multivariate t test procedure was used (one-sample Hotelling t2 test)?-~ Regression analyses were used to test the relationship between overjet, overbite, history of trauma at T1, and presence of fillings at T2 and T3 and changes in pulp canal width. Generalized estimating equations were used to account for dependencies in the data caused by multiple observations in each subject. 22
RESULTS
Signs of damage to periodontal ligament. External replacement or inflammatory resorption did not develop in the teeth in the groups. Cervical resorption was diagnosed in a maxillary incisor of one patient from the experimental group at T2. This patient presented with 4 m m overjet, 2 m m overbite, and no history o f trauma before treatment. Signs of repair were evident at T3. Signs of damage to pulp. In a patient in the experimental group who had pretreatment overjet and overbite at 9 m m and 1 mm, respectively, and a history of trauma, a periapical radiolucency from T1 to T2 developed in one maxillary incisor. A filling of identical size was present at all three intervals. Root canal treatment had been performed at T3. In the control group one maxillary incisor without other restorations had a root canal filling at T2 that was not present at T1. The pulp of one maxillary incisor in a patient in the experimental group showed total obliteration at all three observations. In another patient in the same group who
had 3 m m overjet, 5 m m overbite, no history of trauma prior to treatment, and no restorations, the pulp of a maxillary incisor showed partial obliteration at T2 and total obliteration at T3. Pulp obliteration was not observed in the control material. Internal resorption did not develop in the teeth in the groups. Pulp stones. Pulp stones seen at T2 that were not visible at T1 were observed in five maxillary incisors and two mandibular incisors from the experimental group and in two maxillary incisors from the control group. At T3 pulp stones that were not visible at T2 were seen in four maxillary incisors from the experimental group and two maxillary incisors from the control group. Ten additional teeth from the experimental group had pulp stones present at all three times. Caries and restorations. In the experimental group, 0.3% of the maxillary incisors had a restoration at T1, 82.7% at T2, and 99.3% at T3. In the control group, there were no teeth with fillings at T1, 70.8% at T2, and 96.2% at T3. Unfilled caries was not observed. Subjective evaluation of pulp canal narrowing. The majority of teeth from the subjective evaluation showed reduction of pulp canal width from T 1 to T2 (Table I and Fig. 1). Nearly all observed teeth showed reduction from T2 to T3. Differences between the experimental and control groups were statistically significant only for the maxillary right lateral incisor from T 1 to T2. Measurements of pulp canal width changes. The difference in mean changes between the two groups was significant for maxillary right, left central, and lateral incisors both from T1 to T2 (F = 4.58, df = 4/122, P = 0.0018) and from T2 to T3 (F = 4.66, df = 4 / 1 2 2 , P = 0.0016). The 95% simultaneous confidence intervals indicated that the amount of change
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231
ii;i:iii:iiiiiiiiiiii!ijilili
Fig. 1. Periapical radiographs of a typical patient from the experimental group showing pulp canal narrowing over time. A, Before treatment; B, end of retention; C, 5 years after retention.
Table II. Mean changes in width (millimeters) of teeth for each patient in the experimental and control group from before treatment to after retention (T1 to T2) and from after retention to follow-up examination (T2 to T3). Measurements were performed at the CEJ and at the middle of the root (AP). No significant differences were seen between the groups after correction for differences in time interval and differences in initial pulp canal width Maxillary lateral incisor
Maxillary central incisor Experimental
T1-T2 Tl-T2 T2-T3 T2-T3
CEJ AP CEJ AP
Control
Experimental
Mandibular central incisor
Control
Experimental
x
(SE)
x
(SE)
x
(SE)
x
(SE)
x
0.23 0.21 0.24 0.21
(0.02)* (0.02)* (0.02) (0.01)*
0.11 0.13 0.20 0.12
(0.02)* (0.01)* (0.03) (0.01)*
0.17 0.18 0.18 0.15
(0.01)* (0.02)* (0.01) (0.01)*
0.08 0.09 0.17 0.11
(0.01)* (0.01)* (0.02) (0.01)*
0.07 0.06 0.10 0.07
J
Control
(SE)
x
(SE)
(0.01) (0.01) (0.01)* (0.01)
0.09 0.04 0.13 0.09
(0.02) (0.01) (0.01)* (0.01)
*p < 0.05. x = Mean. SE = Standard error of mean, values for contralateral averaged since analyses demonstrated no differences between right and left side.
was different for all variables from T1 to T2 and only for variables at the AP from T2 to T3 (Table II). No difference was found between the two subgroups from T l t o T 2 ( F = 1.42, d f = 2 / 7 1 , P = 0.2491). However, the difference was significant from T2 to T3 (F = 4.01, df = 2/71, P = 0.0225). The simultaneous confidence intervals indicated that the amount of change was different only for variables at the CEJ (Table II). No significant differences in mean changes were seen after correcting for differences in time lapse between observation intervals and for pulp canal width at T1. Changes in pulp canal width from T1 to T2 and T2 to T3 were significantly different from zero (P < 0.001) in both groups. No relationship was found between pretreatment overjet, overbite, and history of
trauma, and changes in pulp canal width. The presence of a filling at T2 was significant in the regression models for change from T1 to T2 (P < 0.01) but not from T2 to T3. DISCUSSION Our study indicates that orthodontic treatment performed during adolescence causes no increased risk of damage to the pulp and the periodontium. Therefore the circulation changes demonstrated histologically7-9'13'j4 and the observed changes in pulpal respiration ~°'j~ incident to experimental tooth movement may be of limited clinical significance. One explanation for this lack of damage is spontaneous tissue repair may occur during periods of rest between orthodontic pro-
232
Popp, Artun, and Linge
Am. J. Orthod. Dentofac. Orthop. March 1992
cedures. Another explanation is the force magnitudes used under usual clinical conditions do not exceed the physiologic limits of healthy dental tissues. Accordingly, on the basis of this study, there is no justification for classifying routine orthodontic tooth movement in adolescents as pathologic. Our results are in marked contrast to the findings of Cwyk et al.]7 They reported change in 50% of the patients who had experienced orthodontic treatment. In their study only one set of measurements was performed. Therefore they could not control for presence of pathosis before the time of appliance therapy. Nor could they rule out etiologic factors other than orthodontic intervention. Finally, the measurements were done by only one observer, and the method error was not reported. Maxillary incisor pulp canal narrowing was more pronounced from before treatment to after treatment in the patients who had experienced orthodontic treatment than in the control patients during a similar period. This finding supports the theory that orthodontic tooth movement stimulates the odontoblasts to form secondary dentin.12 However, narrowing of the pulp canal from one observation to the next also occurred in the control group. Also, it should be noted that the intervals between observations were longer in the experimental grOup than among the controls. In addition, the pulp canals in the patients in the experimental group were measured to be wider initially. No statistically significant differences between the groups were found when we controlled for these discrepancies. These facts support the theory that the pulp canal narrowing observed in our study is a natural aging process. Any additional influence of orthodontic tooth movement may only be minimal. Initial overjet and overbite were not associated with the observed degree of pulp canal narrowing in our material. However, a conclusion that pulpal response is unrelated to the amount of tooth movement should be done with care. Few patients with extreme front-bite deviations were included in the study, and all malrelationships may not have been fully corrected. In addition, our material was limited to the incisors. Only eight subjects in the experimental group reported a history of trauma. Also, information on type and severity of the injury was not available. We are therefore reluctant to make conclusions regarding pulp changes during and after orthodontic movement of teeth subjected to trauma. We had access to detailed information regarding treatment variables, such as length of active appliance therapy and time periods with rectangular arch wires and intermaxillary elastics. However, because of the
negative findings, we did not consider the testing of any relationship between such variables and pulp changes to be meaningful. The pulpal response to orthodontic tooth movement may be different in adults. Particularly, tooth intrusion in patients with reduced tissue support may be associated with a high degree of vascular changes. In a recent study 23 necrosis was diagnosed in seven front teeth in 6 of 24 patients during realignment of teeth that had migrated due to advanced periodontitis. It is possible that compression of periapical vessels and pulpal edema may occur when the forces are transmitted over a smaller percentage of the periodontium. Also, adult patients are more likely to have restorations. Our results give reason to speculate that the presence of fillings increases formation of secondary dentin during orthodontic treatment and retention. The cause of calcified areas within the pulp is unclear. 19 However, our study indicates that orthodontic treatment is not a significnt factor in the development of pulp stones. Blinding is an established way to minimize examiner bias. Accordingly, it may be criticized that individual radiographs were not coded and examined randomly in our study. However, details of tooth alignment and apical structure usually indicated whether a radiograph belonged to a patient who had experienced orthodontic treatment. In addition, variations in apical closure, abrasion of incisal edges, and presence of restorations usually showed whether the radiograph was taken early or late in the series. Our opinion is that simultaneous evaluation of radiographs from all time intervals reduced examiner bias. This observation method allowed evaluation of individual changes in shape and size of pulp canal, pulp stones, external or internal resorptions, and periapical radiolucencies over time. A possible source of error in our analysis was that the middle of the root was located subjectively when measuring pulp canal widths. However, differences in projection from one radiograph to the next, particularly in the control material, ruled out location on the basis of the absolute distances from the CEJ or the apex. Another possibility would have been to use the fraction of the distance to the apex relative to the length of the root. 24 However, then root resorption of the teeth in the experimental material could induce a bias. 2s We tried to ensure consistent location by using root structure as a guide. All evaluations were made jointly by two of the authors, one located close to the screen and one at a distance. Differences in magnification of the radiographs at time of exposure was not accounted for in our study.
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Number 3
S u c h i n c o n s i s t e n c i e s m a y b e p a r t i c u l a r l y p r e v a l e n t in the control m a t e r i a l . O t h e r p r o b l e m s w e r e the effects o f d i f f e r e n c e s in t o o t h a l i g n m e n t b e f o r e a n d after orthodontic i n t e r v e n t i o n o n the r a d i o g r a p h i c i m a g e . O n e possibility w o u l d b e to m e a s u r e the pulp w i d t h as a f r a c t i o n o f total tooth w i d t h . H o w e v e r , this m e t h o d w o u l d inc r e a s e bias in s i t u a t i o n s w i t h d i f f e r e n c e s in m e s i o d i s t a l projections. It w a s a s s u m e d that any v a r i a t i o n in ima g i n g as the r e s u l t o f r a d i o g r a p h i c d i s t o r t i o n w a s e v e n l y a n d r a n d o m l y d i s t r i b u t e d in the m a t e r i a l . H o w e v e r , it c a n n o t be r u l e d o u t t h a t the finding o f w i d e r p u l p c a n a l s at the first o b s e r v a t i o n in the e x p e r i m e n t a l m a t e r i a l was d u e to a s y s t e m a t i c error. D i f f e r e n c e s in r a d i o g r a p h i c p r o j e c t i o n will o n l y influence the s h a p e o f t h e p u l p c a n a l i m a g e . R a d i o g r a p h i c signs o f p a t h o l o g y are not likely to b e a f f e c t e d . In spite o f the p r o b l e m s w i t h t h e m e t h o d i n h e r e n t in o u r study, we m a y t h e r e f o r e c o n c l u d e that r o u t i n e o r t h o d o n t i c t r e a t m e n t p e r f o r m e d d u r i n g a d o l e s c e n c e c a u s e s minim a l d a m a g e to the p u l p a n d p e r i o d o n t a l l i g a m e n t . T h e o b s e r v e d n a r r o w i n g o f the p u l p canal m a y b e r e g a r d e d as a n o r m a l a g i n g p r o c e s s . We express our sincere gratitude to Drs. K. K. Rognes, A. B. Utkilen, and A. G. Beck Andersen for providing the control material.
REFERENCES 1. Andreasen JO. Luxation of permanent teeth due to trauma: a clinical and radiographic follow-up study of 189 injured teeth. Scand J Dent Res 1970;78:273-86. 2. St~dhaneI, Hedeg~dB. Traumatized permanent teethin children aged 7-15 years. Part II. Swed Dent J 1975;68:157-69. 3. Jacobsen I, Kerekes K. Long-term prognosis of traumatized permanent anterior teeth showing calcifying processes in the pulp cavity. Scand J Dent Res 1977;85:588-98. 4. Arwill T. Histopathic studies of traumatized teeth. Odont Tidskr 1962;70:91-117. 5. Gustafson G, Granath L-E. Pathology of the pulp. In: Gustafson G, ed. Oral pathology for students. Stockholm: Esselte Stadium, 1975. 6. Tronstad L. Pulp reactions in traumatized teeth. In: Gutman J, Harrison J, eds. Proceedings of the International Conference on Oral Trauma. American Association of Endodontists Endowment and Memorial Foundation, 1986:55-77. 7. Butcher E, Taylor A. The vascnlarity of the incisor pulp of the monkey and its alteration by tooth retraction. J Dent Res 1952;31:239-47.
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8. Oppenheim A. Human tissue response to orthodontic intervention of short and long duration. AM J ORTHOD 1942;28:263-301. 9. Butcher E, Taylor A. The effects of denervation and ischemia upon the teeth of the monkey. J Dent Res 1951;30:265-75. 10. Hamersky P, Weimar A, Taintor J. The effect of orthodontic force application on the pulpal tissue respiration rate in the human premolar. AM J ORTHOD 1980;77:368-78. 11. Unterseher R, Nieberg L, Weimar A, Dyer J. The response of human pulpal tissue after orthodontic force application. AM J ORTHOO DENTOFACORTHOP 1987;92:220-4. 12. Marshall JA. A study of bone and tooth changes incident to experimental tooth movement and its application to orthodontic practice. Int J Orthod Dent Child 1933;19:1-17. 13. Stenvik A, Mj0r A. Pulp and dentine reactions to experimental tooth intrusion. AM J ORTHOD 1970;57:370-85. 14. Anstendig H, Kronman J. A histologic study of pulpal reaction to orthodontic tooth movement in dogs. Angle Orthod 1972; 42:50-5. 15. Reitan K. Clinical and histological observations on tooth movement during and after orthodontic treatment. AM J ORTHOD 1967;53:721-45. 16. Rygh P. Ultrastructural changes in pressure zones of human periodontium incident to orthodontic tooth movement. Scand J Dent Res 1973;81:467-80. 17. Cwyk F, Saint-Pierre F, Tronstad L. Endodontic implications of orthodontic tooth movement. IADR Abstracts 1984;#1039. 18. Andreasen JO. Traumatic injuries of the teeth. Philadelphia: WB Saunders; 1981:178-97. 19. Moss-Salentijn L, Hendricks-Klyvert M. Calcified structures in human dental pulps. J Endod 1988;14:184-9. 20. Dalberg G. Statistical methods for medical and biological students. London: George Allen & Ltd., 1940:122-32. 21. Morrison DF. Multivariate statistical methods. San Francisco: McGraw-Hill, Inc. 1976. 22. Liang K-Y, Zeger SL. Longitudinal data analysis using generalized linear models. Biometrikon 1986;73:13-22. 23..~-tun J, Urbye KS. The effect of orthodontic treatment on periodontal bone support in patients with advanced loss of marginal periodontium. AM J ORTHODDENTOFACORTHOP 1988;93:143-8. 24. Schei O, Waerhaug J, Lovdal A, Arno A. Alveolar bone loss as related to oral hygiene and age. J Periodontol 1959;30:7-16. 25. Sj01ien T, Zachrisson BU. Periodontal bone support and tooth length in orthodontically treated and untreated persons. AM J ORTHOD 1973;64:28-37. Reprint requests to: Dr. Jon ,z~-tun University of Washington Department of Orthodontics SM-46 Seattle, WA 98195
