THE ANATOMICAL RECORD 226:367-372 (1990)
Effect of Occlusal Functional Forces on Incisor Socket Morphology and Location in the Rat Mandible ILANA BRIN, SHULAMIT STEIGMAN, AND YAEL MICHAELI Department of Orthodontics (I.B., S.S.) and Department of Anatomy and Embryology (Y.M.), Hebrew University-Hadassah Dental and Medical Schools, Jerusalem, Israel
ABSTRACT The effect of functional occlusal stress on dimensional alterations of the rat incisor socket and mandible were studied from roentgenograms. In 12 rats, the lower left incisor was shortened twice weekly, whereas the lower right incisor was allowed to remain in contact with both upper incisors. Thus, the right incisors were subjected to hyperfunction, and the left ones, to hypofunction. The lower incisors of 16 rats with normal occlusal contact served as control. Following a n experimental period of 3 months, the animals were killed and standardized radiographs were taken of the cleaned mandibles. Socket and mandibular dimensions were measured on magnified tracings of the roentgenograms. Socket area, its posterior length, posterior mandibular length, and gonial angle changed in the same direction under both hyper- and hypofunction. The anterior socket was relocated in opposite directions: under hyperfunction, i t assumed a more inferior position, whereas in hypofunction, it moved superiorly. The angulation of the socket became significantly more acute under hyperfunction, whereas in hypofunction, this parameter remained unchanged. It is concluded that altered functional demands affect the morphology of the incisor socket and its location within the mandibular borders.
*
The intimate relationship between functional stress and bone architecture was already suggested at the end of the last century by Wolff (1892) and Roux (1895). Such association between function and form was further investigated in numerous clinical and experimental studies. Thus, it was found that adaptations occur in the craniofacial skeleton in response to altered functional stress (Washburn, 1947; Avis, 1961; Kreiborg et al., 1978; Schneiderman and Carlson, 1985). The dental supporting structures also react to changes in functional demands, and i t has been shown that decreased or increased function causes dimensional changes in the periodontal ligament (PDL) (Kronfeld, 1931; Coolidge, 1938; Grant et al., 1979; Bondevik, 1984; Steigman e t al., 1989). Other studies reported significant changes in tooth morphology of the rat a s a result of disrupted eruption (Berkovitz, 1972; Steigman et al., 1983, 1988) or of altered function (Steigman et al., 1989). No information is available, however, about a possible change in the location of the lower incisor within the mandibular border following increased or decreased functional loads. The present study addresses the eventual long-term effect of altered occlusal function on the morphology and location of the r a t incisor socket, a s measured on standardized roentgenograms. Within the framework of the measurements, some parameters of the mandibular morphology were also recorded.
weight 200 10 g). The animals were housed in standard metal cages. They were fed a laboratory diet of Purina chow and were provided with water ad libitum. In 12 rats, the lower left incisor was shortened twice weekly to keep it out of occlusal contact (hypofunction), whereas the lower right incisor was allowed to remain in contact with the upper incisors to fulfil1 all the grinding and biting needs of the animals (hyperfunction). Sixteen animals in which both lower incisors remained in normal contact served as control. The rate of eruptionlattrition of the lower incisors was measured twice weekly under ether anesthesia for a period of 3 months, as described elsewhere (Michaeli and Weinreb, 1968). Briefly, after marking the enamel surface of the tooth with a fine carborundum disc, the distances between the notch and the gingival margin and between the notch and the incisal edge were measured by means of a fine caliper that was connected to a digital voltmeter. The migration of the notch in relation to the gingival margin indicated quantitatively the rate of eruption, and that in relation to the incisal edge, the rate of attrition of the tooth. The measurements served for calculation of the mean daily eruption and attrition rates. At the end of 3 months, the animals were killed by a n
MATERIALS AND METHODS
Received April 12, 1989; accepted June 8,1989. Address reprint requests t o I. Brin, DMD, Department of Orthodontics, Hebrew University-Hadassah School of Dental Medicine, P.O. Box 1172, 91010 Jerusalem, Israel.
The investigation was carried out on 28 female adult rats of the Hebrew University Sabra strain (mean 0 1990 WILEY-LISS, INC.
368
I. BRIN ET AL
Fig. 1. a: Tracing of the mandible with landmarks used for measuring angulation, size, and location of the socket. b: Tracing of the mandible with landmarks used for measuring angulation and size.
overdose of ether. The mandibles were dissected, cleaned of soft tissue, and fixed in Bouin-Holland fluid. Standardized orthoradial lateral radiographs were taken of the right and left hemi-mandible. The radiographs were projected on a screen (magnification x 4.5), and the outlines of the mandibular bone and of the incisor socket were traced on acetate paper. The tracings were oriented on the mandibular plane and measured directly. The latter was constructed so a s to form a tangent to the lower border of the mandible. Area measurements were performed by means of a special computer program, after digitizing of the tracings. The following reference points were identified on the tracings (Fig. la,b): 1. the most anterior point on the lingual alveolar bone; 2. the deepest point on the superior alveolar bone contour; 2’. the intersection between the lingual outline of the socket and a perpendicular (through point 2) to the mandibular plane; 3. the intersection between the mandibular alveolar bone and the mesial surface of the first molar; 4. the most anterior point between the coronoid and condylar processes on the curvature; 5. the most posterior point on the condylar process; 6. the most anterior point on the mandibular ramus; 7. the most posterior point on the angular process; 8. the most inferior point on the angular process; 9. the deepest point on the antegonial notch; 10. the most inferior point on the alveolar bone contour; 10’. the intersection between the labial outline of the socket and a perpendicular (through point 10) to the mandibular plane; 11. the most anterior point on the labial alveolar bone; 12. the most posteriorisuperior point of the socket; 12’. the intersection between the coronoid process and a perpendicular (through point 12) to the mandibular plane; 12”. the intersection between the inferior mandibular border and a perpendicular (through point 12) to the mandibular plane; 13. the most inferior point on the labial contour of the socket.
These landmarks were used to delineate the morphology, dimensions, and location of the socket, as well as the morphology and total dimensions of the mandible, a s follows: 1. Morphology, Dimensions, and Location of the Socket (Fig. la)
1. angulation (11-13-12); 2. anterior length (11-13); 3. posterior length (13-12); 4. area; 5. anterior vertical location: a. superior (2-27, b. inferior (10-lO’), c. ratio (2-2’/10-10’); 6. posterior vertical location: a. superior (12-12’), b. inferior (12-12”), c. ratio (12-12’/12-12”); 7. posterior horizontal location (5-12). II. Morphology of the Mandible (Fig. lb)
1. anterior height (measured on the perpendicular from point 2 to the mandibular plane); 2. posterior height (measured on the perpendicular from point 4 to the mandibular plane); 3. anterior length (1-3); 4. posterior length (3-5; 3-6; 3-7; 3-8; 3-9); 5. gonial angle (5-7/mandibular plane); 6. net area (total mandibular area less socket area). Statistical Analysis
The means ( 2 standard errors) of the measurements were calculated. Each experimental group was compared with the control group, using the Mann-Whitney test. For comparison between the hyper- and hypofunction groups, the Wilcoxon matched pairs signed ranks test was applied. P < .05 was chosen as the level of significance. RESULTS
The animals withstood the experimental procedures well and appeared normal and healthy throughout the
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E F F E C T O F OCCLUSAL FUNCTION ON RAT INCISOR
TABLE 1. Mean ( 2 SE) values for socket morphology, area, and location'
Angulation (degrees) Anterior length (mm) Posterior len&h (mm) Socket area (rnm') Anterior vertical location (mm) 2-2' 10-10' Ratio Posterior vertical location (mm) 12-12' 12-12" Ratio Posterior horizontal location (mm) 5-12
Hyperfunction (n = 12) 128.20 f 0.94* 8.81 2 0.24 16.08 f 0.22** 34.17 f 0.60*
Hypofunction (n = 12) 131.00 f 0.54 8.96 t 0.14 16.16 2 0.16** 36.72 f 0.68***
1.75 f 0.06 1.11 f 0.03 1.60 f 0.08*
1.38 t 0.06 1.39 f 0.07 1.0 t 0.09*
5.11 2 0.40*** 9.60 2 0.11* 0.50 2 0.05**
5.06 9.44 0.50
8.00
7.60 t 0.23
f
0.21
f 0.48*** f 0.21
* 0.05**
Control (n = 16) 131.50 t 0.83 8.90 f 0.26 14.86 k 0.32 30.80 2 0.97 1.63 f 0.05 1.20 f 0.04 1.40 f 0.07 6.26 t 0.29 8.43 t 0.37 0.70 t 0.05 7.60
-t
0.12
'See also Figure la. ***P < ,001,**P < .01,*P < .05 for comparison with the controls.
study period. The mean weight of the animals a t the end of the experiment was 227 10 g (with no significant difference between the experimental and control animals). The mean daily eruption and attrition rates of the incisors in the control group were nearly equal (443 5 pm and 438 3 pm, respectively). In the hyperfunction group, eruption rate was 397 16 pm, which was slightly less than that of attrition (406 t_ 24 Fm), causing a very modest gradual shortening of the teeth. In the hypofunction group, the highest eruption rate was measured, giving a mean of 849 ? 30 Frn (no attrition, a s the tooth was shortened regularly). The results of the measurements of the examined parameters are presented in Tables 1 and 2.
*
*
Mandible (Table 2) Posterior length and gonial angle were increased significantly.
DISCUSSION The results of the present study have to be viewed in light of the various functional stimuli acting on the tooth and mandible. Changes in diet (Kiliaridis et al., 1985; Kjellberg et al., 1987) or caging conditions (McFadden e t al., 1986) a s a source of altered occlusal function influence the masticatory muscle activity pattern. However, the main occlusal load on the rat incisor stems from its grinding activity rather than from mastication. Since in the above studies the experimental conditions did not interfere with the normal grinding Hyperfunction activity, occlusal function was only marginally disturbed. The present study, on the other hand, was deSocket (Table 1) signed so a s to alter directly occlusal loading of the Angulation became more acute. The entire area and mandibular incisors. By placing the burden of all bitlength of its posterior part increased significantly a s ing and grinding activities on one incisor only, the encompared with the control. In the anterior region, the tire pattern of mandibular movement changed from socket was relocated inferiorly, whereas in the poste- protrusive-retrusive to lateral-protrusive, as is evident rior region, it attained a significantly more superior from the unusual wear on the incisors of the experiposition. The change in posterior horizontal location mental animals (Fig. 2). Previous studies have shown that intrinsic forces was not significant. generated by cessation of the eruptive movement (Berkovitz, 1972), or extrinsic forces induced by meMandible (Table 2) chanical loading (Steigman e t al., 1987), bring about Posterior length, anterior height, and gonial angle changes in incisor morphology and location. The curwere increased significantly. rent work elucidated that altered functional occlusal loads also have a similar effect. From the present reHypofunction sults, it may be inferred that hyperfunction generated sufficient force to cause a change in tooth curvature Socket (Table 1) (Table 1).Two hypotheses seem appropriate in trying Posterior length and area increased. The anterior to explain this phenomenon: the generated occlusal segment was relocated into a more inferior position, force 1)induced deformation of the unmineralized probeing centered within the mandibular borders (ante- genitor compartment, which, in turn, affected final rior ratio = 1.0). In the posterior region, its position tooth formation (Berkovitz, 1972) andlor 2) initiated a was significantly more superior within the mandible, differential rate of development of the tooth-forming elements. Berkovitz (1972) favors the second possibilwithout a change in the posterior horizontal location.
*
*
I. BRIN ET AL.
370
TABLE 2. Mean ( 2 SE) values for mandibular morphology and area'
Anterior height (mm) Posterior height (mm) Anterior length (mm) Posterior length (mm) 3-5 3-6 3 -7 3-8 3 -9
Gonial angle (degrees) Net mandibular area
Hyperfunction
Hypofunction
(n = 12) 5.70 2 0.06* 12.72 2 0.10 8.46 f 0.19
(n = 12) 5.50 0.11 12.75 2 0.20 8.56 0.14
(n = 16) 5.40 f 0.07 12.30 2 0.28 8.62 2 0.14
21.56 2 0.20** 17.61 2 0.25 22.20 2 0.28 18.60 t 0.30" 10.52 k 0.08 90.80 & 1.04**
21.47 2 0.16** 17.81 2 0.17 22.22 2 0.21 18.40 2 0.21* 10.71 & 0.15 90.00 f 1.04*
20.27 2 17.30 2 21.51 k 17.72 10.33 2 86.60
83.72 2 0.20
82.56
* *
2
0.23
Control
* *
0.18 0.13 0.23 0.12 0.14 0.65
82.01 k 0.18
(mml 'See also Figure l b . **P < .01, *P < .05 for comparison with the controls
Fig. 2. The attrition pattern caused by altered grinding movements induced by shortening of the left lower incisor.
ity, explaining that the morphological alterations occurring in arrested eruption are due to changes in the differential production of enamel and dentin. That such changes do occur was shown by Steigman et al. (19891, who found doubled enamel formation without any change in dentin production under condition of prolonged hypofunction.
The finding that the length of the anterior segment remained unaltered (Fig. la, Table 1)was quite unexpected in view of the reported apical movement of the junctional epithelium far beyond the alveolar crest following blockage of eruption (Beertsen et al., 1983). It is plausible, however, that the alveolar crest behaved independently of the junctional epithelium, thus giving rise to a periodontal pocket. (At this stage, this possibility is only conjectured, since the design of the present study did not include measurement of pocket depth.) In support of this assumption, however, is the unchanged anterior mandibular length (Fig. l b , distance 1-3; Table 2) and the therefore stable alveolar crest. The similar linear increase in the posterior segment of the socket (Table 1)following hyper- and hypofunction seems difficult to explain. It may be speculated, however, that the increased occlusal load and the increased eruptive function of the contralateral half of the jaw encouraged incisor growth. This increase in socket length may have served as a functional matrix (Moss, 1968) for the mandibular elongation (Fig. l b , distance 3-5; Table 2). The two noteworthy changes regarding the socket subsequent to both hyper- and hypofunction are its increased area and changed location within the mandibular borders. The increase in socket area, especially under hypofunction, reflected the sum total of the dental and periodontal changes. This observation contradicts reports stating that atrophy of the PDL is the usual response to hypofunction (Grant e t al., 1979). On the other hand, results agreeing with those found in the present study were reported by Bondevik (1984), albeit after only a short (1-3 days) experimental period of hypofunction. He considers augmented periodontal tissue growth a normal response where there is loss of antagonist contact. Steigman et al. (1989) also demonstrated a significant increase in the PDL and tooth volumes following prolonged (3 months) hyper- and, especially, hypofunction: under hyperfunction, the increase was found to originate in the cementum-related PDL, whereas in the case of hypofunction, it stemmed from the enamel-related PDL. This differential response of these two PDL segments to altered functional demands was also observed macroscopically in the
EFFECT OF OCCLUSAL FUNCTION ON RAT INCISOR
371
Fig. 3. Hypofunction (A): increased socket area, mainly seen in the enamel-related region. Hyperfunction (B): socket area somewhat increased (see Table 1); C: control group.
present study (Fig. 3). Steigman et al. (1989)also noted an increase in tooth volume, mainly after hypofunction, which they ascribed to decreased environmental pressure. Thus, in the current study, the effect of an increment in PDL and of enlarged tooth volume is expressed in increased socket area.
The opposing behavior of the labial and lingual alveolar bone widths in the anterior region (Table l, anterior vertical ratio) in groups A and B and the significantly increased total anterior vertical dimension under hyperfunction (Table 2) reflect the differential bone remodeling in this region induced by the altered
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direct occlusal force. This anatomical response again supports the functional matrix theory of Moss (1968). When addressing the issue of socket location in the posterior mandibular region, the masticatory muscle activity must be taken into account. The force exerted by the muscles in this area causes remodeling of the mandibular borders, thereby indirectly changing the socket’s location. A feasible assumption would be that the muscle pull affects both sides to a similar extent, overriding any possible effect from the direct occlusal force. The positional change in the vertical dimension of the socket was not accompanied by a significant change in the horizontal direction (Table 1). Considering the equal increase in the posterior mandibular length in both experimental groups (Table 2, distance 3-51, it is reasonable that dental and skeletal responses to changed functional loads occur in a coordinated fashion. Previous studies in rats have shown that altered masticatory function causes changes in gross anatomy, as well as in the microscopic structure of the facial skeleton (Kiliaridis et al., 1985; Kjellberg et al., 1987). The significant changes observed in the posterior length and gonial angle induced by hyper- and hypofunction probably reflect the altered muscle activity in the posterior mandibular region. These findings agree with McFadden e t al.’s (1986) exposition that the posterior area of the mandible, by virtue of its close proximity to the heavy activity muscle group, is affected to a larger degree by the experimental condition than by the anterior area. The lack of further significant differences between groups A and B regarding the mandibular morphology, such as in net mandibular area, which is known to differ under various functional loads (McFadden et al., 19861, remains to be explained. It should be noted, however, that most of the studies, like the one by McFadden et al. (19861, compared groups of young, growing animals that were maintained under various conditions, whereas in the current work, each half of the same mandible was subjected to different functional demands. Thus, the functional stimulus that enhanced remodeling under hyperfunction concomitantly caused compensatory changes in the contralateral side of the mandible that was exposed to hypofunction. ACKNOWLEDGMENTS
The authors wish to thank Mrs. Pnina Ever-Hadani for the statistical workup. LITERATURE CITED Avis, V. 1961 The significance of the angle of the mandible: An experimental and comparative study. Am. J . Phys. Anthropol., 19: 55-61.
Beertsen, W., V. Everts, and K. Hoeben 1983 Loss of connective tissue attachment in the marginal periodontium of the mouse following blockage of eruption. J. Period. Res., 18:276-291. Berkovitz, B.K.B. 1972 The effect of preventing eruption on the proliferative basal tissues of the rat lower incisor. Arch. Oral. Biol., 17:1279-1288. Bondevik, 0. 1984 Tissue changes in the rat molar periodontium following alteration of normal occlusal forces. Eur. J. Orthod., 6: 205-212. Coolidge, D.E. 1938 Traumatic and functional injuries occurring in the supporting tissues of human teeth. J. Am. Dent. Assoc., 25: 343-357. Grant, D.A., I.B. Stern, and F.G. Everett 1979 Periodontics. C.V. Mosby Co., St. Louis, MO, 5th ed., pp. 282-286, 400-427. Kiliaridis, S., C. Engstrom, and B. Thilander 1985 The relationship between masticatory function and craniofacial morphology. 1. A cephalometric longitudinal analysis in the growing rat fed a soft diet. Eur. J. Orthod., 7:273-283. Kjellberg, H., S.Kiliaridis, and C. Engstrom 1987 Effect of low masticatory function on condylar growth. Presented to the European Orthodontic Society (Abstract No. 46). Kreiborg, S., B.L. Jensen, E. Moller, and A. Bjork 1978 Craniofacial growth in cases of congenital muscular dystrophy. Am. J. Orthod., 74,207-215. Kronfeld, R. 1931 Histologic study of the influence of function on the human periodontal membrane. J. Am. Dent. Assoc., 18,12421274. McFadden, L.R., K.D. McFadden, and D.S. Precious 1986 Effect of controlled dietary consistency and cage environment on the rat mandibular growth. Anat. Rec., 215t390-396. Michaeli, Y., and M.M. Weinreb 1968 Role of attrition and occlusal contact in the physiology of the rat incisor. 11. Prevention of attrition and occlusal contact in the non-articulating incisors. J. Dent. Res., 47:633-640. Moss, M.L. 1968 The primacy of the functional matrices in orofacial growth. Dent. Pract., 19:65-73. Roux, W. 1895 Gesammelte Abhandlungen ueber Entwicklungsmechanik der Organismen. Leipzig, W. Engelman, cited by Graber, T.M. 1985 Functional appliances. In: Orthodontics, Current Principles and Techniques. T.M. Graber and B.F. Swain, eds. C.V. Mosby Co., St. Louis, MO, Toronto, Canada, Princeton, NJ, p. 369. Schneiderman, E.D., and D.S. Carlson 1985 Cephalometric analysis of condylar adaptations to altered mandibular position in adult rhesus monkeys, Macaca mulatu. Arch. Oral Biol., 30t49-54. Steigman, S., D. Harari, and Y. Michaeli 1983 Long term effect of intrusive loads of varying magnitude upon the eruptive potential of rat incisors. Am. J. Orthod., 84t254-259. Steigman, S., Y. Michaeli, and M. Weinreb, Jr. 1987 Structural changes in the dental and periodontal tissues of the rat incisor following application of orthodontic loads. Am. J. Orthod. Dentofacial Orthop., 91:49-56. Steigman, S., A. Barad, and Y. Michaeli 1988 The effect of load duration on long term recovery of the eruptive function in the rat incisor. Am. J. Orthod. Dentofacial Orthop., 93:310-314. Steigman, S., Y. Michaeli, M. Yitzhaki, and M. Weinreb 1989 The effect of functional occlusal forces on the morphology of dental and periodontal tissues of the rat incisor: A three-dimensional evaluation. J. Dent. Res., in press. Washburn, S.L. 1947 The relation of the temporal muscle to the form of the skull. Anat. Rec., 99:239-248. Wolff, J. 1892 Das Gesetz der transformation der Knochen. Berlin, Hirschwald, cited by Graber T.M. 1985 Functional appliances. In: Orthodontics, Current Principles and Techniques. T.M. Graber and B.F. Swain, eds. C.V. Mosby Co., St. Louis, MO, Toronto, Canada, Princeton, NJ, p. 369.
Effect of Occlusal Functional Forces on Incisor Socket Morphology and Location in the Rat Mandible ILANA BRIN, SHULAMIT STEIGMAN, AND YAEL MICHAELI Department of Orthodontics (I.B., S.S.) and Department of Anatomy and Embryology (Y.M.), Hebrew University-Hadassah Dental and Medical Schools, Jerusalem, Israel
ABSTRACT The effect of functional occlusal stress on dimensional alterations of the rat incisor socket and mandible were studied from roentgenograms. In 12 rats, the lower left incisor was shortened twice weekly, whereas the lower right incisor was allowed to remain in contact with both upper incisors. Thus, the right incisors were subjected to hyperfunction, and the left ones, to hypofunction. The lower incisors of 16 rats with normal occlusal contact served as control. Following a n experimental period of 3 months, the animals were killed and standardized radiographs were taken of the cleaned mandibles. Socket and mandibular dimensions were measured on magnified tracings of the roentgenograms. Socket area, its posterior length, posterior mandibular length, and gonial angle changed in the same direction under both hyper- and hypofunction. The anterior socket was relocated in opposite directions: under hyperfunction, i t assumed a more inferior position, whereas in hypofunction, it moved superiorly. The angulation of the socket became significantly more acute under hyperfunction, whereas in hypofunction, this parameter remained unchanged. It is concluded that altered functional demands affect the morphology of the incisor socket and its location within the mandibular borders.
*
The intimate relationship between functional stress and bone architecture was already suggested at the end of the last century by Wolff (1892) and Roux (1895). Such association between function and form was further investigated in numerous clinical and experimental studies. Thus, it was found that adaptations occur in the craniofacial skeleton in response to altered functional stress (Washburn, 1947; Avis, 1961; Kreiborg et al., 1978; Schneiderman and Carlson, 1985). The dental supporting structures also react to changes in functional demands, and i t has been shown that decreased or increased function causes dimensional changes in the periodontal ligament (PDL) (Kronfeld, 1931; Coolidge, 1938; Grant et al., 1979; Bondevik, 1984; Steigman e t al., 1989). Other studies reported significant changes in tooth morphology of the rat a s a result of disrupted eruption (Berkovitz, 1972; Steigman et al., 1983, 1988) or of altered function (Steigman et al., 1989). No information is available, however, about a possible change in the location of the lower incisor within the mandibular border following increased or decreased functional loads. The present study addresses the eventual long-term effect of altered occlusal function on the morphology and location of the r a t incisor socket, a s measured on standardized roentgenograms. Within the framework of the measurements, some parameters of the mandibular morphology were also recorded.
weight 200 10 g). The animals were housed in standard metal cages. They were fed a laboratory diet of Purina chow and were provided with water ad libitum. In 12 rats, the lower left incisor was shortened twice weekly to keep it out of occlusal contact (hypofunction), whereas the lower right incisor was allowed to remain in contact with the upper incisors to fulfil1 all the grinding and biting needs of the animals (hyperfunction). Sixteen animals in which both lower incisors remained in normal contact served as control. The rate of eruptionlattrition of the lower incisors was measured twice weekly under ether anesthesia for a period of 3 months, as described elsewhere (Michaeli and Weinreb, 1968). Briefly, after marking the enamel surface of the tooth with a fine carborundum disc, the distances between the notch and the gingival margin and between the notch and the incisal edge were measured by means of a fine caliper that was connected to a digital voltmeter. The migration of the notch in relation to the gingival margin indicated quantitatively the rate of eruption, and that in relation to the incisal edge, the rate of attrition of the tooth. The measurements served for calculation of the mean daily eruption and attrition rates. At the end of 3 months, the animals were killed by a n
MATERIALS AND METHODS
Received April 12, 1989; accepted June 8,1989. Address reprint requests t o I. Brin, DMD, Department of Orthodontics, Hebrew University-Hadassah School of Dental Medicine, P.O. Box 1172, 91010 Jerusalem, Israel.
The investigation was carried out on 28 female adult rats of the Hebrew University Sabra strain (mean 0 1990 WILEY-LISS, INC.
368
I. BRIN ET AL
Fig. 1. a: Tracing of the mandible with landmarks used for measuring angulation, size, and location of the socket. b: Tracing of the mandible with landmarks used for measuring angulation and size.
overdose of ether. The mandibles were dissected, cleaned of soft tissue, and fixed in Bouin-Holland fluid. Standardized orthoradial lateral radiographs were taken of the right and left hemi-mandible. The radiographs were projected on a screen (magnification x 4.5), and the outlines of the mandibular bone and of the incisor socket were traced on acetate paper. The tracings were oriented on the mandibular plane and measured directly. The latter was constructed so a s to form a tangent to the lower border of the mandible. Area measurements were performed by means of a special computer program, after digitizing of the tracings. The following reference points were identified on the tracings (Fig. la,b): 1. the most anterior point on the lingual alveolar bone; 2. the deepest point on the superior alveolar bone contour; 2’. the intersection between the lingual outline of the socket and a perpendicular (through point 2) to the mandibular plane; 3. the intersection between the mandibular alveolar bone and the mesial surface of the first molar; 4. the most anterior point between the coronoid and condylar processes on the curvature; 5. the most posterior point on the condylar process; 6. the most anterior point on the mandibular ramus; 7. the most posterior point on the angular process; 8. the most inferior point on the angular process; 9. the deepest point on the antegonial notch; 10. the most inferior point on the alveolar bone contour; 10’. the intersection between the labial outline of the socket and a perpendicular (through point 10) to the mandibular plane; 11. the most anterior point on the labial alveolar bone; 12. the most posteriorisuperior point of the socket; 12’. the intersection between the coronoid process and a perpendicular (through point 12) to the mandibular plane; 12”. the intersection between the inferior mandibular border and a perpendicular (through point 12) to the mandibular plane; 13. the most inferior point on the labial contour of the socket.
These landmarks were used to delineate the morphology, dimensions, and location of the socket, as well as the morphology and total dimensions of the mandible, a s follows: 1. Morphology, Dimensions, and Location of the Socket (Fig. la)
1. angulation (11-13-12); 2. anterior length (11-13); 3. posterior length (13-12); 4. area; 5. anterior vertical location: a. superior (2-27, b. inferior (10-lO’), c. ratio (2-2’/10-10’); 6. posterior vertical location: a. superior (12-12’), b. inferior (12-12”), c. ratio (12-12’/12-12”); 7. posterior horizontal location (5-12). II. Morphology of the Mandible (Fig. lb)
1. anterior height (measured on the perpendicular from point 2 to the mandibular plane); 2. posterior height (measured on the perpendicular from point 4 to the mandibular plane); 3. anterior length (1-3); 4. posterior length (3-5; 3-6; 3-7; 3-8; 3-9); 5. gonial angle (5-7/mandibular plane); 6. net area (total mandibular area less socket area). Statistical Analysis
The means ( 2 standard errors) of the measurements were calculated. Each experimental group was compared with the control group, using the Mann-Whitney test. For comparison between the hyper- and hypofunction groups, the Wilcoxon matched pairs signed ranks test was applied. P < .05 was chosen as the level of significance. RESULTS
The animals withstood the experimental procedures well and appeared normal and healthy throughout the
369
E F F E C T O F OCCLUSAL FUNCTION ON RAT INCISOR
TABLE 1. Mean ( 2 SE) values for socket morphology, area, and location'
Angulation (degrees) Anterior length (mm) Posterior len&h (mm) Socket area (rnm') Anterior vertical location (mm) 2-2' 10-10' Ratio Posterior vertical location (mm) 12-12' 12-12" Ratio Posterior horizontal location (mm) 5-12
Hyperfunction (n = 12) 128.20 f 0.94* 8.81 2 0.24 16.08 f 0.22** 34.17 f 0.60*
Hypofunction (n = 12) 131.00 f 0.54 8.96 t 0.14 16.16 2 0.16** 36.72 f 0.68***
1.75 f 0.06 1.11 f 0.03 1.60 f 0.08*
1.38 t 0.06 1.39 f 0.07 1.0 t 0.09*
5.11 2 0.40*** 9.60 2 0.11* 0.50 2 0.05**
5.06 9.44 0.50
8.00
7.60 t 0.23
f
0.21
f 0.48*** f 0.21
* 0.05**
Control (n = 16) 131.50 t 0.83 8.90 f 0.26 14.86 k 0.32 30.80 2 0.97 1.63 f 0.05 1.20 f 0.04 1.40 f 0.07 6.26 t 0.29 8.43 t 0.37 0.70 t 0.05 7.60
-t
0.12
'See also Figure la. ***P < ,001,**P < .01,*P < .05 for comparison with the controls.
study period. The mean weight of the animals a t the end of the experiment was 227 10 g (with no significant difference between the experimental and control animals). The mean daily eruption and attrition rates of the incisors in the control group were nearly equal (443 5 pm and 438 3 pm, respectively). In the hyperfunction group, eruption rate was 397 16 pm, which was slightly less than that of attrition (406 t_ 24 Fm), causing a very modest gradual shortening of the teeth. In the hypofunction group, the highest eruption rate was measured, giving a mean of 849 ? 30 Frn (no attrition, a s the tooth was shortened regularly). The results of the measurements of the examined parameters are presented in Tables 1 and 2.
*
*
Mandible (Table 2) Posterior length and gonial angle were increased significantly.
DISCUSSION The results of the present study have to be viewed in light of the various functional stimuli acting on the tooth and mandible. Changes in diet (Kiliaridis et al., 1985; Kjellberg et al., 1987) or caging conditions (McFadden e t al., 1986) a s a source of altered occlusal function influence the masticatory muscle activity pattern. However, the main occlusal load on the rat incisor stems from its grinding activity rather than from mastication. Since in the above studies the experimental conditions did not interfere with the normal grinding Hyperfunction activity, occlusal function was only marginally disturbed. The present study, on the other hand, was deSocket (Table 1) signed so a s to alter directly occlusal loading of the Angulation became more acute. The entire area and mandibular incisors. By placing the burden of all bitlength of its posterior part increased significantly a s ing and grinding activities on one incisor only, the encompared with the control. In the anterior region, the tire pattern of mandibular movement changed from socket was relocated inferiorly, whereas in the poste- protrusive-retrusive to lateral-protrusive, as is evident rior region, it attained a significantly more superior from the unusual wear on the incisors of the experiposition. The change in posterior horizontal location mental animals (Fig. 2). Previous studies have shown that intrinsic forces was not significant. generated by cessation of the eruptive movement (Berkovitz, 1972), or extrinsic forces induced by meMandible (Table 2) chanical loading (Steigman e t al., 1987), bring about Posterior length, anterior height, and gonial angle changes in incisor morphology and location. The curwere increased significantly. rent work elucidated that altered functional occlusal loads also have a similar effect. From the present reHypofunction sults, it may be inferred that hyperfunction generated sufficient force to cause a change in tooth curvature Socket (Table 1) (Table 1).Two hypotheses seem appropriate in trying Posterior length and area increased. The anterior to explain this phenomenon: the generated occlusal segment was relocated into a more inferior position, force 1)induced deformation of the unmineralized probeing centered within the mandibular borders (ante- genitor compartment, which, in turn, affected final rior ratio = 1.0). In the posterior region, its position tooth formation (Berkovitz, 1972) andlor 2) initiated a was significantly more superior within the mandible, differential rate of development of the tooth-forming elements. Berkovitz (1972) favors the second possibilwithout a change in the posterior horizontal location.
*
*
I. BRIN ET AL.
370
TABLE 2. Mean ( 2 SE) values for mandibular morphology and area'
Anterior height (mm) Posterior height (mm) Anterior length (mm) Posterior length (mm) 3-5 3-6 3 -7 3-8 3 -9
Gonial angle (degrees) Net mandibular area
Hyperfunction
Hypofunction
(n = 12) 5.70 2 0.06* 12.72 2 0.10 8.46 f 0.19
(n = 12) 5.50 0.11 12.75 2 0.20 8.56 0.14
(n = 16) 5.40 f 0.07 12.30 2 0.28 8.62 2 0.14
21.56 2 0.20** 17.61 2 0.25 22.20 2 0.28 18.60 t 0.30" 10.52 k 0.08 90.80 & 1.04**
21.47 2 0.16** 17.81 2 0.17 22.22 2 0.21 18.40 2 0.21* 10.71 & 0.15 90.00 f 1.04*
20.27 2 17.30 2 21.51 k 17.72 10.33 2 86.60
83.72 2 0.20
82.56
* *
2
0.23
Control
* *
0.18 0.13 0.23 0.12 0.14 0.65
82.01 k 0.18
(mml 'See also Figure l b . **P < .01, *P < .05 for comparison with the controls
Fig. 2. The attrition pattern caused by altered grinding movements induced by shortening of the left lower incisor.
ity, explaining that the morphological alterations occurring in arrested eruption are due to changes in the differential production of enamel and dentin. That such changes do occur was shown by Steigman et al. (19891, who found doubled enamel formation without any change in dentin production under condition of prolonged hypofunction.
The finding that the length of the anterior segment remained unaltered (Fig. la, Table 1)was quite unexpected in view of the reported apical movement of the junctional epithelium far beyond the alveolar crest following blockage of eruption (Beertsen et al., 1983). It is plausible, however, that the alveolar crest behaved independently of the junctional epithelium, thus giving rise to a periodontal pocket. (At this stage, this possibility is only conjectured, since the design of the present study did not include measurement of pocket depth.) In support of this assumption, however, is the unchanged anterior mandibular length (Fig. l b , distance 1-3; Table 2) and the therefore stable alveolar crest. The similar linear increase in the posterior segment of the socket (Table 1)following hyper- and hypofunction seems difficult to explain. It may be speculated, however, that the increased occlusal load and the increased eruptive function of the contralateral half of the jaw encouraged incisor growth. This increase in socket length may have served as a functional matrix (Moss, 1968) for the mandibular elongation (Fig. l b , distance 3-5; Table 2). The two noteworthy changes regarding the socket subsequent to both hyper- and hypofunction are its increased area and changed location within the mandibular borders. The increase in socket area, especially under hypofunction, reflected the sum total of the dental and periodontal changes. This observation contradicts reports stating that atrophy of the PDL is the usual response to hypofunction (Grant e t al., 1979). On the other hand, results agreeing with those found in the present study were reported by Bondevik (1984), albeit after only a short (1-3 days) experimental period of hypofunction. He considers augmented periodontal tissue growth a normal response where there is loss of antagonist contact. Steigman et al. (1989) also demonstrated a significant increase in the PDL and tooth volumes following prolonged (3 months) hyper- and, especially, hypofunction: under hyperfunction, the increase was found to originate in the cementum-related PDL, whereas in the case of hypofunction, it stemmed from the enamel-related PDL. This differential response of these two PDL segments to altered functional demands was also observed macroscopically in the
EFFECT OF OCCLUSAL FUNCTION ON RAT INCISOR
371
Fig. 3. Hypofunction (A): increased socket area, mainly seen in the enamel-related region. Hyperfunction (B): socket area somewhat increased (see Table 1); C: control group.
present study (Fig. 3). Steigman et al. (1989)also noted an increase in tooth volume, mainly after hypofunction, which they ascribed to decreased environmental pressure. Thus, in the current study, the effect of an increment in PDL and of enlarged tooth volume is expressed in increased socket area.
The opposing behavior of the labial and lingual alveolar bone widths in the anterior region (Table l, anterior vertical ratio) in groups A and B and the significantly increased total anterior vertical dimension under hyperfunction (Table 2) reflect the differential bone remodeling in this region induced by the altered
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direct occlusal force. This anatomical response again supports the functional matrix theory of Moss (1968). When addressing the issue of socket location in the posterior mandibular region, the masticatory muscle activity must be taken into account. The force exerted by the muscles in this area causes remodeling of the mandibular borders, thereby indirectly changing the socket’s location. A feasible assumption would be that the muscle pull affects both sides to a similar extent, overriding any possible effect from the direct occlusal force. The positional change in the vertical dimension of the socket was not accompanied by a significant change in the horizontal direction (Table 1). Considering the equal increase in the posterior mandibular length in both experimental groups (Table 2, distance 3-51, it is reasonable that dental and skeletal responses to changed functional loads occur in a coordinated fashion. Previous studies in rats have shown that altered masticatory function causes changes in gross anatomy, as well as in the microscopic structure of the facial skeleton (Kiliaridis et al., 1985; Kjellberg et al., 1987). The significant changes observed in the posterior length and gonial angle induced by hyper- and hypofunction probably reflect the altered muscle activity in the posterior mandibular region. These findings agree with McFadden e t al.’s (1986) exposition that the posterior area of the mandible, by virtue of its close proximity to the heavy activity muscle group, is affected to a larger degree by the experimental condition than by the anterior area. The lack of further significant differences between groups A and B regarding the mandibular morphology, such as in net mandibular area, which is known to differ under various functional loads (McFadden et al., 19861, remains to be explained. It should be noted, however, that most of the studies, like the one by McFadden et al. (19861, compared groups of young, growing animals that were maintained under various conditions, whereas in the current work, each half of the same mandible was subjected to different functional demands. Thus, the functional stimulus that enhanced remodeling under hyperfunction concomitantly caused compensatory changes in the contralateral side of the mandible that was exposed to hypofunction. ACKNOWLEDGMENTS
The authors wish to thank Mrs. Pnina Ever-Hadani for the statistical workup. LITERATURE CITED Avis, V. 1961 The significance of the angle of the mandible: An experimental and comparative study. Am. J . Phys. Anthropol., 19: 55-61.
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