The histology and rate of tooth eruption with and without temporary impaction in the dog.
код для вставкиСкачатьThe Histology and R a t e of Tooth Eruption with and without Temporary Impaction in the Dog' DONALD R. CAHILL* Department of A n a t o m y , T e m p l e University, Philadelphia, Pennsylvania ABSTRACT Eruption was studied b j experimentally impacting and releasing permanent premolars in puppies. Eruption rates of both normal and experimentally delayed teeth were calculated from weekly radiographs. The rate of normal eruption is triphasic and similar to a normal growth curve. It has an initial slow exponential rate which changes to a more rapid exponential rate followed in turn by a terminal plateau. AU of the teeth released from impaction erupted and their rates exceeded or equaled the normal rate. The morphology of the bony trabeculae beneath the erupting teeth and the relative amount of soft tissue between the bone and teeth are expressions of the eruptive rate. The trabeculae around rapidly erupting teeth are thinner, more delicate and more widely separated from one another than those of slowly erupting teeth. Trabecular orientation aligns with the direction of eruption, showing not only its vertical component, but also whether the tooth moved mesially or distally during eruption. When erupting teeth were experimentally immobilized within the mandible, thus eliminating direct and continual pressure on the overlying bone by the tooth, eruption pathways formed in the same marcner as in normal eruption (Cahill, '69;. That investigation demonstrated that the mechanism of pathway formation is nct dependent upon direct and continual pre5;sure from the erupting tooth. The present investigation utilizes the same early immobilization technique except that the teeth were released from impaction by removing the restraining wires. This was done to determine whether the teeth would erupt through pathways which formed during the immobilizatioii period. Furthermore, the normal eruption rate was established to provide a baseline for evaluating the experimental findings. their eruptive movement (Cahill, '69), then after the desired delay, the teeth were allowed to continue eruption by removing the restraining wires. The length of the delays ranged from 4-7 weeks at varying times during the normal eruptive period. Onset, duration and time of release for the impactions is shown in figure 1A and B. Here, the flat portion of the curves illustrates the absence of eruptive movement and the sharp change in slope - the time of wire removal. In all cases, the left side of the animal was the control side; the right, the experimental side. Measurements for the eruption rates were made to the nearest millimeter from a line drawn along the base of the mandible perpendicularly upward to the apex of the crown on a series of dental radiographs taken at weekly intervals. Error in measuring tooth position by this method is negligible because this distance did not MATERIALS AND METHODS change during impaction periods. This inEruption of normal and experimentally dicates that there is no appreciable growth delayed permanent third premolars in the at the lower border of the mandible and mandible of medium-sized mongrel pup- that it is a stable reference for measurepies was studied from the thirteenth ment during the period studied. The tissues were prepared for microthrough the twenty-seventh postnata 1 weeks. The normal eruption rate was cal- scopic examination by decalcification and culated and compared with the eruption Received Aug. 4, '69. Accepted Sept. 24, '69. rates of the experimentally delayed teeth. 1 Supported by USPHS grant 1 SO 1 FR 5417-04-5. 2 Present address: Department of Biostructure, Teeth were impacted by lacing wire Medical and Dental School, Northwestern University, through the mandible (fig. 10A) to sto:3 Chicago, Illinois 60611. ANAT.REC.. 166: 225-238. 225 226 DONALD R. CAHILL paraffin processing, cited in greater detail by Cahill, '69. Serial sections were cut at 12 and stained with hematoxylin and eosin. OBSERVATIONS Tooth eruption rates: Normal and after release from impaction To calculate the eruption rate of third permanent mandibular premolars in the puppy, tooth position versus animal age (distance vs time) was plotted on semilog paper (figs. 2A,B) from the measurements taken from the weekly radiographs. The time range studied (thirteenth through the twenty-seventh postnatal weeks) includes the normal eruption period of this tooth. Since the individual graphs (figs. 2A,B) were remarkably similar in shape, the average rate was plotted by superimposing them (fig. 2C, solid line). The twentieth week was selected for superimposition because all curves, whether complete or incomplete, crossed this midpoint of the time range studied. Tooth position at 1 3 weeks was arbitrarily designated 1.0 and thus positions on the average rate curve are relative to one another and not actual distances from the base of the mandible to any particular crown. On semilog paper, the average eruption rate (fig. 2C) is triphasic and its first two parts are exponential. The first part, from 13 to 18 weeks, depicts a slow exponential rate with root formation commencing on the fifteenth week. Shortly after the eighteenth week the teeth begin the second phase which is characterized by a much more rapid exponential rate. At 21.3 weeks, about halfway through the rapid phase, the crowns begin emerging from the bone and at 22.4 weeks pierce the gingiva. The third part of the curve shows that the rate decreases late in the twentythird week when the teeth gain functional occlusion. Release from impaction was studied in seven of the eight animals; their rate curves are shown in figures 1A-D. The mandible, as shown radiographically in cross section (fig. 6B), developed atypically in one case in which the eruption path- way failed to form in the usual manner. This caused the tooth to erupt noticeably slower than others after release and as an exception, it was not included in the graphs. As in figure 2, the data for eruption after delay are presented as tooth position (from the crown to the base of the mandible) versus animal age. Figures IC and D are composites formed by normalizing all curves to a common origin where distance at release equals 1.0 and time at release equals zero. The data are presented in this manner to emphasize characteristics of movement after release from impaction. All of the released teeth showed eruptive movement and, during the first week, six of the seven erupted at the maximal rate (fig. l D , Oj) after the restraining wires were removed. The eruption rate diminished after the first week but in two specimens it was only slightly slower than the maximal rate (fig. lD, Or). The remaining three, although even slower (fig. l C , C; fig. l D , Oc), were comparable to the rapid rate of normal eruption. Histologic and radiologic findings of teeth released from impaction These observations are grouped and presented in the sequence: ( 1 ) the group sacrificed one week after release, i.e., showing the maximal rate (figs. 3,4); (2) the group continuing a rapid but slightly slower rate after the first week (figs. 8 , l O ) ; and ( 3 ) the lowest group, a rate which, however, matched the normal eruptive rate after the first week (fig. 1 1 ) . The most striking finding after a week of movement is the new, relatively radiolucent tissue that separates the tooth in its new position from the rim of old bone that marked its previous location (figs. 3, 4,5). This tissue contains thin, interconnected trabeculae radiating upward from the outline of old bone to the tooth (figs. 3,4). It also contains the prospective periodontal ligament and clusters of osteoblasts (fig. 7) forming the rapidly developing trabeculae. After the first week of maximal movement, distance between the tooth and the old bone can be measured EXPERIMENTAL STUDY OF TOOTH ERUPTION radiographically (fig. 5), however, as remodeling takes place, the sharp outline of old bone is gradually lost and from that time accurate measurement can no longer be made. Group 11, demonstrating continued rapid movement at a slightly reduced rate, is characterized by the specimen shown in figure 8. Prior to release, this tooth was experimentally immobilized for seven weeks. After release, it erupted for three weeks and then process was terminated for histologic examination. The stringy, radiate pattern of delicate trabeculae beneath the roots, and in the interradicular area is similar to that described for the first group. These features are characteristic of rapid movement. Trabecular orientation aligns with the direction of eruption, showing not only its vertical coniponent, but also whether the tooth moved mesially or distally during eruption. Comparison of the rapidly erupting released teeth (fig. 8) with controls (fig. 9 ) shows that the trabeculae beneath the normally erupting teeth are thicker than the trabeculae beneath the released teeth. Furthermore, there is considerably more soft tissue (mainly osteoblasts and osteoid material) between the bone and the tooth on the more rapidly erupting side than on the normal side; thus the size of the trabeculae and the amount of soft tissue between the old bone and the tooth i n dicate the rate of movement. A radiographic series in figure 10 shows the rapid eruption of the tooth just dcscribed. The radiolucent area above thse impacted tooth (fig. 10A) is the eruption pathway. This pathway formed during thipreceding period of immobilization. Figurls 10B shows the tooth one week after release i.e., after the maximal rate period, and figure 1OC shows its position threlc weeks after release. In the three weeks following release, the tooth erupted almost as much as a normal tooth (fig. 10D) in six weeks of rapid eruption. The third group ( 3 specimens) showed an eruptive rate nearly identical with the rate at the middle of the normal eruptive curve. This slower eruption rate is characterized histologicaIIy by the bony trabeculae which are similar to those of the controls. Assumed reasons for the slower 227 eruptive rate are not conclusive; however, two of the three impacted teeth in this group became misdirected into adjacent bone (fig. 11) rather than into the preformed emption pathway. This probably retarded a potentially greater rate. Reasons for the slower rate in the third case were not apparent. DISCUSSION Releasing teeth from experimental impactions, maintained for varying periods during prefunctional eruption, is a useful method for studying tooth eruption. It is particularly valuable as it reveals that released teeth erupt rapidly through channels which formed during the impaction. Characteristics and significance of delayed eruption were compared both histologically and radiologically with normal eruption, wherein establishment of the normal eruption rate was an essential factor. Normal eruption The normal prefunctional eruption rate is triphasic showing successive slow and fast periods of exponential movement and a terminal plateau. Root formation begins on the fifteenth week, that is during the slower period of exponential movement, about three weeks before the rapid exponential phase. This finding supports Weinmann's ('41) study of human embryos. More recently descriptions of prefunctional emption, partially stemming from Weinmann ('41), have drifted away from this observation as they now key the onset of rapid eruption to root formation (Orban, '66) and (Provenza, '64). In the dog, the prefunctional phase terminates late in the twenty-third week (fig. 2C) when the teeth reach the occlusal plane. The exponential character of the eruption rate is a previously unreported finding, and the general shape of its curve resembles the normal growth curve. It is significant that the rapid exponential phase commences about three weeks before the crown begins to emerge from the mandible. The exponential eruption rate is possibly a reflection of a corresponding exponential increase in tissue mass by cells responsible for eruptive movement. 228 DONALD R. CAHILL However, such a volumetric increase in tissue through cellular activity would entail more than cell division; it would also involve the formation or deposition of a considerable amount of extracellular material, i.e. collagen and mineral matter. Correlating eruption rate with tissue mass increase is further complicated because at present, it is not possible to attribute eruption rate specifically to any of the various cell types (osteoblasts, fibroblasts, cementoblasts) or to their relative participation, Along this line, however, Kenny and Ramfjord ('69) show that the radioactive index (percentage of labelled cells) of osteoblasts near the root apex during eruption is considerably higher than cementoblasts. That both cell types become differentially labelled during normal eruption indicates their approximate contribution to increase in tissue mass through mitosis, but not through such functions as collagen formation. At present, relating exponential increase in tissue mass to the known exponential eruption rate remains an interesting possibility; however, the requisite details about cellular activity during eruption which would be necessary to test this hypothesis are not currently available. Delayed eruption Rapid eruptive movement began as soon as the restraining wires were removed; some teeth continuing to move more rapidly than others after the initial fast period. In every instance, however, eruption rates of released teeth exceeded or equaled the normal rate. Their eruption pathways were formed by osteoclastic activity during the period of restraint (Cahill, '69). Although no attempt was made to determine whether more prolonged impaction would prevent subsequently released teeth from erupting, observations show that the capacity for eruptive movement remains active during 4-7 weeks delay. The rate (Oj, fig. 1D) during the first week after release was the maximal rate of eruption, a full expression of the potential rate. It was achieved because the pathway for eruption was already formed, because the teeth had room to reorient regardless of slight misdignment and be- cause the development or maturation of the eruption system had proceeded during the delay thereby eliminating the slow exponential phase seen in normal eruption. The continued maximal eruption rate of two of the seven released specimens is further evidence of this finding. The weekly radiographs showed that the eruptive pathways of these two had formed sufficiently and that they were not misoriented in the pathway. The morphology of the bony trabeculae beneath the erupting teeth and the relative amount of soft tissue between the bone and teeth are expressions of the eruptive rate. The trabeculae around rapidly erupting teeth are thinner, more delicate and more widely separated from one another than those of more slowly erupting teeth. They also, in radiating upward, accurately reflect the directional movement of the teeth. This finding agrees with those of Meyer ('35) and Massler and Schour ('41); but apparently the orientation of the trabecular pattern varies in different species since Weinmann ('41) reports trabeculae in man are at right angles to the long axis of the teeth. Prefunctional tooth eruption is a normal growth process wherein physical factors involving mass, acceleration and inertia probably play no effective role. In the present investigation teeth were studied as they emerged from the bony crypt and moved through the eruption pathway to pierce the gingiva and finally reach the occlusal plane. The eruption process can be considered as a balance between osteoclastic activity above the tooth (with directional reference to the mandible) and principally osteoblastic activity below the tooth. Both of these factors implicate incompletely understood functions of the dental follicle. The eruption pathway forms by osteoclastic activity along the sides of the follicle above the tooth (in the part that connects to the oral mucosa) and by osteoblastic activity at the base of the follicle. The follicle appears to act as a reservoir to provide the necessary osteoblasts and osteoclasts for the bony changes that occur in eruption. Because of this profound bone remodeling, it appears that origin and differentiation of osteoclasts EXPERIMENTAL STUDY OF TOOTH ERUPTION can be studied by experimentally controlling eruption. If the follicle plays a primary role in eruption (OBrien et al., '58; Cahill, '69) it would be important to know factors regulating its performance i.e., temporal scheduling of its activity. Questions of this nature may be answered by experimentation. Transplantation of the follicle, of its contents or both into various sites at different developmental stages is presently being carried out in the puppy. ACKNOWLEXMENTS Again it is a pleasure to express rny appreciation to Dr. Carson D. Schneck for his guidance throughout the study. I would also like to acknowledge Dr. Alan D. Conger for the valuable discussions concerning the eruption rates and the work of Mr. Dewey Blackstone for the radiologic assistance is greatly appreciated. 229 LITERATURE CITED Cahill, D. R. 1969 Eruption pathway formation in the presence of experimental tooth impaction in puppies. Anat. Rec., 164: 67-78. Kenney, E. B., and S. P. Ramfjord 1969 Cellular dynamics in root formation of teeth in rhesus monkeys. J. Dent. Res., 48: 114-119. Massler, M., and I. Schour 1941 Studies in tooth development: Theories of eruption. Amer. J. Orthodont., Oral Surg., 27: 552-576. Meyer, W. 1935 Meyer's Normal Histology and Histogenesis of the Human Teeth and Associated Parts. Translated and edited by H. R. Churchill, J. B. Lippincott Co., Philadelphia, London and Montreal. Chap. 14, pp. 237-248. O'Brien, C., S. N. Bhaskar and A. G. Brodie 1958 Eruptive mechanism and movement in the first molar of the rat. J. Dent. Res., 37: 467-484. Orban, B. J. 1966 Orban's Oral Histology and Embryology. H., Sicher, ed. C. V. Mosby Co., St. Louis, 6th ed. Provenza, D. V. 1964 Oral Histology, Inheritance and Development. J. B. Lippincott Co., Philadelphia and Montreal. Weinmann, J. P. 1941 Bone changes related to eruption of the teeth. Angle Orthodont., 11: 83-99. PLATE 1 EXPLANATION OF FIGURE 1 Four graphs of the impaction-release eruption rates o n semilog paper. A and B, show the individual curves i n mm (from the base of the mandible to the top of the crown) against weekly age. The impaction durations are identifiable as the flat parts of the curves. C, shows the curves normalized, where time of release equals zero and impaction height equals 1.0, ( C , is equivalent to rapid exponential portion of the normal rate). D, shows the findings in simplified form where ej is the maximal rate, Or is a rapid but slightly diminished rate and 8 c is a rate nearly identical to the rapid part of the normal rate. EXPERIMENTAL STUDY OF TOOTH ERUPTION Donald R. Cahill PLATE 1 2( 10 € E_ 1( 5:e 11 U i L 1: E n , ' " " a 16 ia PI G E , weeks k - C. - !.O 1.5 1.0 D. - 1.0 -2 -'I 0 *l + 2 +3 *4 +5 Time from release, weeks ERUPTION RATES AFTER RELEASE FROM IMPACTION 231 PLATE 2 EXPLANATION OF FIGURE 2 232 Three graphs showing the normal eruptive rate of the third permanent mandibular premolar on semilog paper. A and B, show individual curves plotted as height in mm (measured from the base of the mandible to the top of the crown) against weekly age. C , shows the average eruption rate curve (solid line) and the range (dotted lines). The average is triphasic with a n initial period of slow exponential growth, a middle rapid rate and a terminal plateau. This curve was computed by superimposing the individual curves of A and B at 20 weeks and by designating 1.0 for height at 13 weeks. EXPERIMENTAL STUDY OF TOOTH ERUPTION Donald R. Cahill PLATE 2 233 PLATE 3 EXPLANATION O F FIGURES 3 Anteroposterior section showing the third permanent premolar (3p) one week after release from three-week impaction. ( a ) apex of old bone before release;" shown at higher magnification in figure 7. x 5.0. 4 Anteroposterior section through the third permanent premolar one week after release from a five-week impaction. Notice the trabecular pattern ( T ) radiating toward the tooth from the old bone. Its radiograph is seen in figure 5. x 5.0. 5 Dental radiograph: The space between the arrows demonstrates the distance moved ( a t the maximal eruption rate) in one week after releasing the impaction. Same specimen as in figure 4. x 2.3. 6 Radiographs from the frontal aspect of dissected mandibles showing the control side ( A ) and its atypical experimental side (B). The eruption pathway (arrow) failed to enlarge i n the usual manner and also, cross-sectional shape of the mandible became distorted. x 2.0. 7 The area marked ( * ) in figure 3, ( e d ) epithelial diaphragm. Ossification centers are seen within clusters of osteoblasts ( T ) . 234 x 26. EXPERIMENTAL STUDY OF TOOTH ERUPTION Donald R. Cahill PLATE 3 235 PLATE 4 EXPLANATION OF FIGURES 8 Anteroposterior section of a rapidly erupting tooth three weeks after release; its radiograph is seen in figure 1OC. Notice the stringy, thin bony trabeculae that rzdiate toward the tooth. They are characteristic of rapid eruption and are comparatively more delicate than the trabeculae of the more slowly erupting control (fig. 9). X 5.0. 9 Anteroposterior section through the fully erupted control side of figure 8. x 5.0. 10 Dental radiographs: A, shows the impacted tooth surrounded by its restraining wires. This film, made six weeks after wire placement, shows the eruption pathway (arrow) as a radiolucent area. B, same specimen one week after wire removal where comparison of crown position with the preceding film shows the amount of eruptive movement during the first week after release. C, shows the same tooth three weeks after release (histologic section of this tooth is shown i n figure 8). D, control side taken at the same time as B. Actual size. 11 236 Anteroposterior section of a slowly erupting release specimen of group 111. As a result of the impaction, the tooth became misdirected into overlying bone (arrows) rather than directly into its eruption pathway. x 5.0. EXPERIMENTAL STUDY OF TOOTH ERUPTION Donald R. Cahill PLATE 4 237
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