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Extrusive mobility of teeth in adult monkeys (Macaca fascicularis)
0003-9969/86$3.00+ 0.00 Pergamon Journals Ltd
Archs oral Biol. Vol. 31, No. 6, PP. 369-372, 1986 Printed in Great Britain
EXTRUSIVE
MOBILITY (MACACA
OF TEETH IN ADULT MONKEYS FASCICULARIS)
D. C. A. PICTON University College London Dental School, Mortimer Market, London WClE 6JD, England, U.K. Summary-Extrusive mobility of 15 teeth in 4 adult macaques was compared with intrusive mobility of the same teeth. The character of the load displacement and recovery records was similar; the qualitative response to repeated 4 N thrusts, 4 N loads sustained for 30 s and residual loading with SO,30 and 10 mN, was the same whether the force was applied in an intrusive or extrusive direction. Fast and slow loading rates (100 and 1 Ns-‘) both caused greater intrusion than extrusion at 4N (p
principal fibres of the ligament may allow a greater degree of initial intrusive movement, before tension is generated, than occurs in axially-aligned fibres under extrusive force. Extrusive loading may be a convenient method for studying tension in the periodontal ligament.
INTRODUCTION amount of information on the manner in which a tooth is displaced when force is applied to it in viva, so that the load/displacement characteristics can be predicted when the force is horizontal or intrusive (Moxham and Berkovitz, 1982). The study by Daly et al. (1974) indicates that the periodontal ligament responds in a similar manner under rotational forces. Studies employing extrusive forces have been limited to continuouslygrowing incisors of rabbit and to the mandibular canines of adult ferrets (Moxham and Berkovitz, 1979, 1981, 1984). It is doubtful whether these findings can be extrapolated to teeth of limited growth. Both kinds of teeth studied were curved and had more complex geometry; the periodontal ligament of the incisors is restricted to the concave surface and the teeth do not taper towards the end of the root. Nevertheless, there are various features of the extrusive load displacement records which are also seen in the intrusive and horizontal mobility records of teeth from primates and carnivores. These features include load dependence and two phases to displacement and recovery. It seemed worthwhile, therefore, to examine the effect of loading teeth of macaques in an extrusive direction and to compare the findings There is now a substantial
with those obtained when applying intrusive force to the same teeth. The architecture of the periodontal ligament of macaques conforms well to the descriptions in standard texts of histology. Collagen-fibre bundles aligned apparently to restrict extrusive displacement are found in the crestal region, apically and between the roots of multirooted teeth. As these fibres are few compared with the principal oblique fibres, it seems reasonable to predict that extrusive force would produce. greater displacement than application of the same magnitude of force in an intrusive direction. MATERIALS AND
METHODS
Under pentobarbitone sodium anaesthesia (Sagital, May & Baker Ltd), the animal was placed on its back with the head in a cephalostat so that the test tooth was vertical by inspection. The method used for measuring displacement of teeth was a minor modification of that technique described previously (Picton, 1984). A linear variable-differential transformer (LVDT) was bolted to the head holder so that the cranked lower end of the spindle rested on the test tooth and detected vertical movement of the tooth relative to the cephalostat (Fig. 1). As the animal’s head could move slightly within the head holder, a
Dynamometer
Fig. 1. Diagrammatic representation of the experimental layout in zation and plan views. The beam of the dynamometer is shown in the elevation attached to the test tooth by means of a loop of floss silk in the position to extrude the tooth. The linear variable-differential transformers are positioned to detect vertical displacement of the tooth and of the adjacent alveolar process. 08.
11,6-c
370
D. C. A. PICTON
Monkey
1bS
2 ‘M
10s
3min
Fig. 2. A simultaneous U.V.record of force in the upper trace, and displacement of the tooth and adjacent bone in the middle and lower traces. Two 4N loadings at 1 Ns-’ intruded the upper first molar. After the dynamometer was re-arranged, two extrusive loadings were applied to the tooth.
LVDT was arranged to rest on a dentine screw inserted into the alveolar bone approx. 4mm from the test tooth. The signal from the second LVDT could then be subtracted from the first to give the displacement of the tooth relative to the adjacent alveolar process. Force was applied to the tooth with a solenoid-powered dynamometer monitored by strain gauges. Intrusive loads were delivered via an adjusting screw; extrusive force was applied via a loop of floss silk attached to the occlusal surface of the tooth with the acid-etch-composite technique. Transducers were calibrated before and after each experiment and records were obtained on u.v.-sensitive paper. Loads were delivered in groups of three thrusts, each of 4 N magnitude. The first three were applied at 100Nss’ with 5 s intervals. After a 2 min recovery period, a second group of three thrusts were applied at 1 Ns-‘. The first six thrusts were intrusive. The dynamometer was then re-arranged and the loading sequence was repeated with extrusive forces. Fifteen teeth were studied, five central incisors, five maxillary premolars and five maxillary first molars in four adult male monkeys (Mucuca fascicularis). From the records, the magnitude of displacement due to 4 N load was assessed from the first loading in each series, and the displacements compared for extrusion and intrusion. Experiements were also carried out to determine the effects of series of 10 extrusive loadings, of 4 N force, sustained for 30 s and of small residual forces on recovery. second
RESULTS
A typical record from two intrusive thrusts is shown in Fig. 2, and can be compared with the two
extrusive loadings obtained within 3 min. The form of the load displacement records was similar with the characteristic change from an initial relatively free phase of displacement due to force < 1 N, to progressively less movement as the force increased (Fig. 3). The recovery of the tooth after release of the force also appeared to be similar with a fast linear phase followed by a progressively more gradual return towards the starting position, and the reappearance of pulsatile movements. Whether the tooth returned completely from extrusive force to the rest position of the previous intrusive thrusts was difficult to determine because small forces disturbed the tooth and minor changes were unavoidable when the dynamometer was re-arranged. The impression was gained was that a narrow null zone existed (Fig. 2).
70 ._.-•-•
7
.’
3 E Ptl
5
.’
Intrusion
./ ./
::
6
Load (NJ lNs-’
Fig. 3. Graph of load/displacement of one thrust at 1 Ns-’ in an intrusive direction, followed by an extrusive loading.
Extrusive mobility of teeth
371
Table 1. X Displacement &m) at 4 N load first thrust, slow loading (1 Ns-‘)
Five central incisors Five premolars Five first molars
Intrusion
Extrusion
Difference
58.4 83.4 92.8
38.2 18.4 24.0
20.2 (34.5 per cent) 65.0 (77.9 per cent) 68.8 (74.1 per cent) z 51.33 SD f 32.17 p < 0.001
Table 2. Z Disnlacement (urn) at 4 N load first thrust. fast loadina (100 Ns-‘)
Five central incisors Five premolars Five first molars
Intrusion
Extrusion
Difference
45.0 68.8 59.4
26.4 12.8 18.4
18.6 (41.3 per cent) 56.0 (81.3 per cent) 41.0 (69.0 per cent) E 38.53 SD + 25.41 D < 0.001
Analysis of the displacements produced with 4 N at slow- and fast-loading rates is shown in Tables 1 and 2. Although there was significantly less displacement with extrusive loads for the whole group of teeth for both rates of loading, the contrast was more marked with the multi-rooted posterior teeth. Displacements for two incisors were approximately the same in each direction, but all other teeth were less mobile with extrusive loading. .4 series of ten extrusive loadings produced progressively greater degrees of displacement from the baseline, though the magnitude of successive excursions tended to lessen (Fig. 4). Loads of 4N maintained for 30 s caused a minor degree of extrusive creep to occur, with a prolonged recovery period. Recovery to the baseline following 4 N ramp loads applied at 1 Ns-’ appeared to be complete within approx. 1.5 min but, after the high-loading rate of lOONs-‘, recovery was more rapid for some teeth, being complete within 5 s. Complete recovery was prevented when residual extrusive force of 0.005, 0.03 or 0.01 N remained on the tooth.
DISCUSSION
The records of intrusive mobility from the single and multi-rooted teeth conformed well to the wellestablished pattern. Extrusive force clearly produced a similar range of characteristics with regard to loaddependent factors, i.e. magnitude of the load, and for factors related to time, i.e. loading rate, duration and interval between thrusts. The similarity in behaviour under extrusive loads and subsequent recovery indicates that the several mechanisms which are probably involved in horizontal and intrusive tooth support, that is, tension, compression, haemodynamic damping and v&co-elasticity, are also involved when extrusive force is applied to a tooth. The similarity between these findings and extrusive mobility of mandibular canines of adult ferret and continuously-growing incisors noted by Moxham and Berkovitz (1979, 1981, 1983, 1984) indicates that the ligament of the several tooth types responds to load in a similar manner, in spite of the different morphology of the root and periodontal ligament,
Intrusion
t
I
Tooth 1 Extrusion 10
OE
10
Bone
--yrrrr~-~-~-~-
-* 10s
2min
105
Fig. 4. Ultraviolet record of a series of 10 intrusive loadings followed by 10 extrusive loadings, The rate of loading was lONs-i.
312
D. C. A. FWTON
though the displacements of the incisors of rabbit are superimposed on the underlying persistent eruptive movements. The finding that both high- and low-loading rates produced significantly less extrusion than intrusion was unexpected and requires explanation. The simplest answer lies with the alignment of the periodontal collagen bundles. Thus, to resist intrusive force, all fibre groups are orientated obliquely or even horizontally to the force but, few though they may be, fibres to oppose extrusive loads are in line with the force. Evidence that collagen takes an active part in tooth support was provided by Moxham and Berkovitz (1984) who found lathyritic incisors were extruded to a greater extent under loads of 0.01 to 0.1 N than were teeth from normal animals. If, in the monkeys, the width of the ligament around the apex and furcation region is similar to the width of the majority of the lateral areas of the ligament, it follows that the oblique fibres are longer than the axial fibres. If these several fibre groups are equally relaxed per unit length at the moment -when force is applied to the tooth, a substantially greater displacement of the tooth would be necessary before the oblique fibres come under tension than would be needed to generate tension in the axially-aligned fibres. Some confirmation of this explanation is evident from the large initial displacement with low intrusive force, whereas much less increase in displacement was produced with loads in excess of 1 N (Fig. 3). The mobility with extrusive load was noticeably less distinct for the two phases, suggesting that a greater total slackness may be present in the oblique fibres than is present in the shorter axial fibres. When tension is generated in the more numerous oblique fibres, the restriction on displacement as load increases is likely to be greater for an increment of force above 1 N than for the more sparse axial fibres. The second point of interest from Tables 1 and 2 is the greater difference between extrusion and intrusion at 4N for three-rooted teeth than for the central incisors. This is partly due to the lower level of
intrusive displacement of the incisors. It may also be explained by the difference in proportion between axial and oblique fibres. For maxillary molars and premolars, three groups of axial fibres can be presumed to lie around the three apices, together with furcational fibres, whereas axial fibres are found only round the apex of the incisors. As the root area of central incisors in monkeys is large compared with the root area of molars and premolars, the proportion of axial to oblique fibres is likely to be appreciably greater for the posterior teeth. This difference in proportion may explain the greater disparity between extrusive and intrusive mobility for posterior teeth. REFERENCES Daly C. H., Nicholls J. I., Kydd W. L. and Newpan P. D. (1974) The response of the human periodontal ligament to torsional loading. J. Biomechan. 7, 517-522. Moxham B. J. and Berkovitz B. K. B. (1979) The effect of axially-directed extrusive loads on movements of the mandibular incisors of rabbits. Archs oral Biol. 24, 259-163.
Moxham B. J. and Berkovitz B. K. B. (1981) A quantitative assessment of the effects of axially-directed extrusive loads on displacement of the impeded and unimpeded rabbit mandibular incisors. Archs oral Biol. 26, 209-216. Moxham B. J. and Borkovitz B. K. B. (1982) The effect of external forces on the periodontal ligament. In: The Periodontal Ligament in Health and Disease (Edited by Berkovitz B. K. B.. Moxham B. J. and Newman H. N.) pp. 249-290. Pergamon Press, Oxford. Moxham B. J. and Berkovitz B. K. B. (1983) Continuous monitoring of the position of the ferret mandibular canine tooth to enable comparisons with the continuouslygrowing rabbit incisors. Archs oral Biol. 28, 477481. Moxham B. J. and Berkovitz B. K. B. (1984) The mobility of the lathyritic rabbit mandibular incisor in response to axially-directed extrusive loads. Archs oral Biol. 29, 113-778.
Picton D. C. A. (1984) Changes in axial mobility of undisturbed teeth and following sustained intrusive forces in adult monkeys (Macaca fascicularis). Archs oral Biol. 29, 959-964.
Archs oral Biol. Vol. 31, No. 6, PP. 369-372, 1986 Printed in Great Britain
EXTRUSIVE
MOBILITY (MACACA
OF TEETH IN ADULT MONKEYS FASCICULARIS)
D. C. A. PICTON University College London Dental School, Mortimer Market, London WClE 6JD, England, U.K. Summary-Extrusive mobility of 15 teeth in 4 adult macaques was compared with intrusive mobility of the same teeth. The character of the load displacement and recovery records was similar; the qualitative response to repeated 4 N thrusts, 4 N loads sustained for 30 s and residual loading with SO,30 and 10 mN, was the same whether the force was applied in an intrusive or extrusive direction. Fast and slow loading rates (100 and 1 Ns-‘) both caused greater intrusion than extrusion at 4N (p
principal fibres of the ligament may allow a greater degree of initial intrusive movement, before tension is generated, than occurs in axially-aligned fibres under extrusive force. Extrusive loading may be a convenient method for studying tension in the periodontal ligament.
INTRODUCTION amount of information on the manner in which a tooth is displaced when force is applied to it in viva, so that the load/displacement characteristics can be predicted when the force is horizontal or intrusive (Moxham and Berkovitz, 1982). The study by Daly et al. (1974) indicates that the periodontal ligament responds in a similar manner under rotational forces. Studies employing extrusive forces have been limited to continuouslygrowing incisors of rabbit and to the mandibular canines of adult ferrets (Moxham and Berkovitz, 1979, 1981, 1984). It is doubtful whether these findings can be extrapolated to teeth of limited growth. Both kinds of teeth studied were curved and had more complex geometry; the periodontal ligament of the incisors is restricted to the concave surface and the teeth do not taper towards the end of the root. Nevertheless, there are various features of the extrusive load displacement records which are also seen in the intrusive and horizontal mobility records of teeth from primates and carnivores. These features include load dependence and two phases to displacement and recovery. It seemed worthwhile, therefore, to examine the effect of loading teeth of macaques in an extrusive direction and to compare the findings There is now a substantial
with those obtained when applying intrusive force to the same teeth. The architecture of the periodontal ligament of macaques conforms well to the descriptions in standard texts of histology. Collagen-fibre bundles aligned apparently to restrict extrusive displacement are found in the crestal region, apically and between the roots of multirooted teeth. As these fibres are few compared with the principal oblique fibres, it seems reasonable to predict that extrusive force would produce. greater displacement than application of the same magnitude of force in an intrusive direction. MATERIALS AND
METHODS
Under pentobarbitone sodium anaesthesia (Sagital, May & Baker Ltd), the animal was placed on its back with the head in a cephalostat so that the test tooth was vertical by inspection. The method used for measuring displacement of teeth was a minor modification of that technique described previously (Picton, 1984). A linear variable-differential transformer (LVDT) was bolted to the head holder so that the cranked lower end of the spindle rested on the test tooth and detected vertical movement of the tooth relative to the cephalostat (Fig. 1). As the animal’s head could move slightly within the head holder, a
Dynamometer
Fig. 1. Diagrammatic representation of the experimental layout in zation and plan views. The beam of the dynamometer is shown in the elevation attached to the test tooth by means of a loop of floss silk in the position to extrude the tooth. The linear variable-differential transformers are positioned to detect vertical displacement of the tooth and of the adjacent alveolar process. 08.
11,6-c
370
D. C. A. PICTON
Monkey
1bS
2 ‘M
10s
3min
Fig. 2. A simultaneous U.V.record of force in the upper trace, and displacement of the tooth and adjacent bone in the middle and lower traces. Two 4N loadings at 1 Ns-’ intruded the upper first molar. After the dynamometer was re-arranged, two extrusive loadings were applied to the tooth.
LVDT was arranged to rest on a dentine screw inserted into the alveolar bone approx. 4mm from the test tooth. The signal from the second LVDT could then be subtracted from the first to give the displacement of the tooth relative to the adjacent alveolar process. Force was applied to the tooth with a solenoid-powered dynamometer monitored by strain gauges. Intrusive loads were delivered via an adjusting screw; extrusive force was applied via a loop of floss silk attached to the occlusal surface of the tooth with the acid-etch-composite technique. Transducers were calibrated before and after each experiment and records were obtained on u.v.-sensitive paper. Loads were delivered in groups of three thrusts, each of 4 N magnitude. The first three were applied at 100Nss’ with 5 s intervals. After a 2 min recovery period, a second group of three thrusts were applied at 1 Ns-‘. The first six thrusts were intrusive. The dynamometer was then re-arranged and the loading sequence was repeated with extrusive forces. Fifteen teeth were studied, five central incisors, five maxillary premolars and five maxillary first molars in four adult male monkeys (Mucuca fascicularis). From the records, the magnitude of displacement due to 4 N load was assessed from the first loading in each series, and the displacements compared for extrusion and intrusion. Experiements were also carried out to determine the effects of series of 10 extrusive loadings, of 4 N force, sustained for 30 s and of small residual forces on recovery. second
RESULTS
A typical record from two intrusive thrusts is shown in Fig. 2, and can be compared with the two
extrusive loadings obtained within 3 min. The form of the load displacement records was similar with the characteristic change from an initial relatively free phase of displacement due to force < 1 N, to progressively less movement as the force increased (Fig. 3). The recovery of the tooth after release of the force also appeared to be similar with a fast linear phase followed by a progressively more gradual return towards the starting position, and the reappearance of pulsatile movements. Whether the tooth returned completely from extrusive force to the rest position of the previous intrusive thrusts was difficult to determine because small forces disturbed the tooth and minor changes were unavoidable when the dynamometer was re-arranged. The impression was gained was that a narrow null zone existed (Fig. 2).
70 ._.-•-•
7
.’
3 E Ptl
5
.’
Intrusion
./ ./
::
6
Load (NJ lNs-’
Fig. 3. Graph of load/displacement of one thrust at 1 Ns-’ in an intrusive direction, followed by an extrusive loading.
Extrusive mobility of teeth
371
Table 1. X Displacement &m) at 4 N load first thrust, slow loading (1 Ns-‘)
Five central incisors Five premolars Five first molars
Intrusion
Extrusion
Difference
58.4 83.4 92.8
38.2 18.4 24.0
20.2 (34.5 per cent) 65.0 (77.9 per cent) 68.8 (74.1 per cent) z 51.33 SD f 32.17 p < 0.001
Table 2. Z Disnlacement (urn) at 4 N load first thrust. fast loadina (100 Ns-‘)
Five central incisors Five premolars Five first molars
Intrusion
Extrusion
Difference
45.0 68.8 59.4
26.4 12.8 18.4
18.6 (41.3 per cent) 56.0 (81.3 per cent) 41.0 (69.0 per cent) E 38.53 SD + 25.41 D < 0.001
Analysis of the displacements produced with 4 N at slow- and fast-loading rates is shown in Tables 1 and 2. Although there was significantly less displacement with extrusive loads for the whole group of teeth for both rates of loading, the contrast was more marked with the multi-rooted posterior teeth. Displacements for two incisors were approximately the same in each direction, but all other teeth were less mobile with extrusive loading. .4 series of ten extrusive loadings produced progressively greater degrees of displacement from the baseline, though the magnitude of successive excursions tended to lessen (Fig. 4). Loads of 4N maintained for 30 s caused a minor degree of extrusive creep to occur, with a prolonged recovery period. Recovery to the baseline following 4 N ramp loads applied at 1 Ns-’ appeared to be complete within approx. 1.5 min but, after the high-loading rate of lOONs-‘, recovery was more rapid for some teeth, being complete within 5 s. Complete recovery was prevented when residual extrusive force of 0.005, 0.03 or 0.01 N remained on the tooth.
DISCUSSION
The records of intrusive mobility from the single and multi-rooted teeth conformed well to the wellestablished pattern. Extrusive force clearly produced a similar range of characteristics with regard to loaddependent factors, i.e. magnitude of the load, and for factors related to time, i.e. loading rate, duration and interval between thrusts. The similarity in behaviour under extrusive loads and subsequent recovery indicates that the several mechanisms which are probably involved in horizontal and intrusive tooth support, that is, tension, compression, haemodynamic damping and v&co-elasticity, are also involved when extrusive force is applied to a tooth. The similarity between these findings and extrusive mobility of mandibular canines of adult ferret and continuously-growing incisors noted by Moxham and Berkovitz (1979, 1981, 1983, 1984) indicates that the ligament of the several tooth types responds to load in a similar manner, in spite of the different morphology of the root and periodontal ligament,
Intrusion
t
I
Tooth 1 Extrusion 10
OE
10
Bone
--yrrrr~-~-~-~-
-* 10s
2min
105
Fig. 4. Ultraviolet record of a series of 10 intrusive loadings followed by 10 extrusive loadings, The rate of loading was lONs-i.
312
D. C. A. FWTON
though the displacements of the incisors of rabbit are superimposed on the underlying persistent eruptive movements. The finding that both high- and low-loading rates produced significantly less extrusion than intrusion was unexpected and requires explanation. The simplest answer lies with the alignment of the periodontal collagen bundles. Thus, to resist intrusive force, all fibre groups are orientated obliquely or even horizontally to the force but, few though they may be, fibres to oppose extrusive loads are in line with the force. Evidence that collagen takes an active part in tooth support was provided by Moxham and Berkovitz (1984) who found lathyritic incisors were extruded to a greater extent under loads of 0.01 to 0.1 N than were teeth from normal animals. If, in the monkeys, the width of the ligament around the apex and furcation region is similar to the width of the majority of the lateral areas of the ligament, it follows that the oblique fibres are longer than the axial fibres. If these several fibre groups are equally relaxed per unit length at the moment -when force is applied to the tooth, a substantially greater displacement of the tooth would be necessary before the oblique fibres come under tension than would be needed to generate tension in the axially-aligned fibres. Some confirmation of this explanation is evident from the large initial displacement with low intrusive force, whereas much less increase in displacement was produced with loads in excess of 1 N (Fig. 3). The mobility with extrusive load was noticeably less distinct for the two phases, suggesting that a greater total slackness may be present in the oblique fibres than is present in the shorter axial fibres. When tension is generated in the more numerous oblique fibres, the restriction on displacement as load increases is likely to be greater for an increment of force above 1 N than for the more sparse axial fibres. The second point of interest from Tables 1 and 2 is the greater difference between extrusion and intrusion at 4N for three-rooted teeth than for the central incisors. This is partly due to the lower level of
intrusive displacement of the incisors. It may also be explained by the difference in proportion between axial and oblique fibres. For maxillary molars and premolars, three groups of axial fibres can be presumed to lie around the three apices, together with furcational fibres, whereas axial fibres are found only round the apex of the incisors. As the root area of central incisors in monkeys is large compared with the root area of molars and premolars, the proportion of axial to oblique fibres is likely to be appreciably greater for the posterior teeth. This difference in proportion may explain the greater disparity between extrusive and intrusive mobility for posterior teeth. REFERENCES Daly C. H., Nicholls J. I., Kydd W. L. and Newpan P. D. (1974) The response of the human periodontal ligament to torsional loading. J. Biomechan. 7, 517-522. Moxham B. J. and Berkovitz B. K. B. (1979) The effect of axially-directed extrusive loads on movements of the mandibular incisors of rabbits. Archs oral Biol. 24, 259-163.
Moxham B. J. and Berkovitz B. K. B. (1981) A quantitative assessment of the effects of axially-directed extrusive loads on displacement of the impeded and unimpeded rabbit mandibular incisors. Archs oral Biol. 26, 209-216. Moxham B. J. and Borkovitz B. K. B. (1982) The effect of external forces on the periodontal ligament. In: The Periodontal Ligament in Health and Disease (Edited by Berkovitz B. K. B.. Moxham B. J. and Newman H. N.) pp. 249-290. Pergamon Press, Oxford. Moxham B. J. and Berkovitz B. K. B. (1983) Continuous monitoring of the position of the ferret mandibular canine tooth to enable comparisons with the continuouslygrowing rabbit incisors. Archs oral Biol. 28, 477481. Moxham B. J. and Berkovitz B. K. B. (1984) The mobility of the lathyritic rabbit mandibular incisor in response to axially-directed extrusive loads. Archs oral Biol. 29, 113-778.
Picton D. C. A. (1984) Changes in axial mobility of undisturbed teeth and following sustained intrusive forces in adult monkeys (Macaca fascicularis). Archs oral Biol. 29, 959-964.