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Effects of tooth loading on the periodontal vasculature of the mandibular fourth premolar in dogs
Archs oral Bd.
Vol.
‘X03-9969/81/03OlSS-07602.00/O
26, pp. 189 lo 195, 1981
PergamonPress Ltd
Prmtedin Great Britam
EFFECTS OF TOOTH LOADING ON THE PERIODONTAL VASCULATURE OF THE MANDIBULAR FOURTH PREMOLAR IN DOGS G. C. NG,‘.’ T. W. WALKER,“’ W. ZINC& and P. S. BURKE’ ‘Medical Research Council Group in Periodontal Physiology, Faculty of Dentistry, University of Toronto, Toronto, Ontario, Canada ‘Institute of Biomedical Engineering, University of Toronto, Toronto, Ontario, Canada Summary-A surgical technique was developed to isolate the arterial supply to the periodontal ligament, pulp and gingiva of the canine mandibular 4th premolar, and to measure the pressure and flow therein. This model system was used to study the interaction between tooth loading and periodontal blood flow. Intrusive forces of less than 350N were found to produce negligible alteration of the measured blood flow, while loads of 1050 N produced a reduction of flow equivalent to an increase in vascular resistance of approximately 10 per cent, with no effect on arterial pressure. The increase in flow on removal of load was greater than the reduction seen on application, suggesting that reactive hyperemia may occur in the periodontal tissues. The phenomenon ‘of periodontal pulsation first studied by Parfitt (J. dent. Rex 39, 608%618) in humans, was examined in the dog as a part of the present work. It was found that the pulsation of the canine mandibular 4th premolar was still in evidence under applied loads 230 times that which Parfitt found to obliterate the movement of the human incisor. This may be taken to indicate that the density and architecture of the periodontal vasculature may, in part, be determined by the loads applied to the teeth during function.
INTRODUCTlON The blood vessels in the periodontal ligament have long been implicated as a component of the system supporting the teeth. Parfitt (1960) observed a pulsation, synchronous with the arterial pulse, superimposed on the signal measuring the load applied to human incisors. He found that when the load was increased to 4 g (0.04 N), pulsation was strongest, but, with further increase in axial load, pulsation diminished. Above 15 g (0.15 N), pulsation was obliterated. He attributed this observation to a vascular tide which supported the tooth when subjected to a load of less than 0.15 N. This periodontal pulsation has also been demonstrated by Kijrber (1970). Bien (1966) reported that the tooth displacement response in a live rat is different from that in a dead rat. He found that the teeth of a dl:ad animal would not return to the equilibrium position after the removal of load unless the thorax was squeezed. He attributed this difference in responsl: to the cessation of blood flow when the rat was dead. Slatter and Picton (1972) conducted experiments on adult rhesus monkeys to study the effect produced by a local injection of noradrenaline on axial movements of incisors. They reported that the injection of noradrenaline, a vasoconstrictor, reduced tooth mobility for a period of 6@9Omin. No comparable alteration in mobility was detected when physiological saline was injected. It was concluded that collapse of the periodontal vasculature prevented the tooth from returning to the origmal resting position after the initial application of force, and that mobility was thus decreased. The participation of the periodontal vasculature in the support of the teeth during simulated function has been clearly demonstrated. Although the blood
vessels occupy only l-2 per cent of the periodontal ligament space (Giitze, 1965), Wills, Picton and Davies (1976) have demonstrated in macaque monkeys that 30 per cent of tooth mobility is associated with the blood vessels in the ligament space. They concluded that the blood in this space has an energydissipating function, providing a major viscous component in the displacement and recovery of the tooth under occlusal forces. Whereas all these studies confirm the participation of the periodontal vasculature in tooth support, they tell little about the dynamic behaviour of the vasculature itself during and after the application of occlusal force. Other workers have attempted to reveal the vascular responses by a combination of perfusion and histological techniques which only depict static conditions. Castelli and Dempster (1964), applying a perfusion method in monkeys, demonstrated that a horizontal force of 1 N can induce local ischaemia in the ligament. Similarly, Gianelly (1969) showed, also using perfusion, that a lateral force of 1.5 N induced vascular occlusion in the compressed areas of the periodontal ligament in dog incisors. Although these experiments delineate the change in vascularity associated with orthodontic force-application (light horizontal forces of long duration), the dynamic response of the periodontal vasculature to simulated function is still not known. This is the problem we have investigated.
MATERIALS AND
METHODS
The periodontium of the mandibular 4th premolar was selected because the mandibular artery is relatively free from branches in the vicinity of this tooth. Blood Aow and blood pressure in the mandibular 189
G. C. Ng
190
et al.
T : Tourniquet L: Ligature
Fig. 1. The canine mandible, showing the two windows through which access to the mandibular artery was gained, and the locations at which the instruments for measuring arterial blood flow and pressure were placed.
artery were continuously monitored while the tooth was subjected to occlusal force. This technique offers the advantage of recording the dynamic response of the vasculature in situ but has the disadvantage of being invasive in nature. The study was conducted on dogs weighing between 17 and 25 kg. This size range of dog was selected to ensure that the mandibular artery would be sufficiently large (approx. 1 mm in outside diameter) to permit cannulation. Animals were of either sex and of no particular breed; all were in good genera1 health, with healthy orat tissues, visually assessed. Eight dogs were used to perfect the surgical technique and the instrumentation. Nine more animals constituted the experimental group. After sedation with Atrovit (Acepromazine Maleate, Ayerst, McKenna & Harrison Ltd, Montreal, Canada), the dogs were anaesthetized using intravenous Nembutal (Pentobarbital sodium, Abbott Laboratories, Montreal, Canada). A tracheal cannula was inserted as an artificial airway. An intravenous catheter was placed in the cephalic vein for the administration of a 0.9 per cent saline: 0.5 per cent dextrose drip (Travenol Lab. Inc., Morton Grove, Ill., U.S.A.) to reduce shock. The eyelid reflex of the dog was tested regularly and additional anaesthetic was administered as necessary. A sample of venous blood was withdrawn to measure the haematocrit value in order to establish the probe factor for the electromagnetic flowmeter. Blankets and an infrared heat lamp were used to stabilize the animal’s body temperature, which had a profound effect on the blood flow being measured. The animal was placed in a supine position with its four legs tied to the table. A cut-down technique was employed to cannulate one femoral artery in order to monitor the systemic arterial pressure. With an electro-cautery, the inferior border of the mandible was exposed along its entire length. The periosteum and soft tissues were stripped and the inferior
alveolar neurovascular bundle exposed in two locations (Fig. 1) by cutting windows in the bone with an air rotor and a round carbide bur. Under a stereo-microscope, the mandibular artery was separated from the rest of the neurovascular bundle at both anterior and posterior windows using blunt dissection, A cannula of 0.965 mm polyethylene tubing was then inserted into the mandibular artery at the site indicated in Fig. 1, and a No. 4 electromagnetic flow probe (Carolina Medical Electronics, King North Carolina, U.S.A.) secured around the posterior portion of the mandibuIar artery. The neck of the flow probe was fitted into a Teflon bracket and the whole assembly was taped to the mandible to ehminate any movement of the flow probe which could generate artifacts in the flow recordings. A tourniquet was applied to the artery, posterior to the flow probe, arresting the mandibular blood flow. Since blood could still reach the ~riodontium of the 4th premolar via the posterior mental artery, this vessel was ligated at the posterior mental foramen. This measure, coupled with the insertion of the pressure-measurement cannula, ensured that the only major vessel supplying blood to the 4th premolar was the mandibular artery, the flow in which was measured. The ffowmeter was adjusted to give a zero output and the tourniquet released. After a period of approx. 10min to allow the blood flow to return to a stable equilibrium state, the mandibular arterial pressure and the volumetric flow rate were recorded on the storage oscilloscope. A Polaroid oscilloscope camera (Model CS, Tektronix, Beaverton, Oreg., U.S.A.) was used to obtain a hard copy of the recording. The experimentation proper was then begun. A pneumatic loading device (Fig. 2) was installed with one arm seated at the crown of the 4th premolar and the other arm firmly against the mandible at a location between the two windows. Intrusive forces of 20 and 35 N were applied for periods of approx. 8 s, separated by recovery periods of at least 2 min. Mandibular arterial pressure and flow rate were recorded
Effects of tooth loading on the periodontal vasculature
191
Pressure regulator Compressed air
Movable arm
Fig. 2. Diagram of the pneumatic loading system with which intrusive loads of up to 35 N were applied to the 4th premolar. during load application. This apparatus was also used to study the periodontal puisation. A manual force applicator [Fig. 3) was used to apply larger forces (350, 500, 700, 900, 105ON) to the 4th premolar. Blood pressure and flow rate were again recorded during load application. RESULTS Systemic urferia~ pressure, ~~~~~~r and volumetric Hood jiow rate
arterial pressure
The data from one dog (No. B6) were omitted from the general analysis because this animal had a high
peripheral vascular resistance suggestive of some constricting peripheral vascular disorder. For the other 16 dogs, systolic and diastolic pressures were 185 zfr11 and 130 & 8 mm Hg respectively (mean f 95 per cent confidence limit). The mandibular arterial pressures for 12 dogs averaged 136 &- 17 and 104 & 13 mm Hg (systolic and diastolic pressures, respectively) and had a functional mean of 114 + 14 mm Hg. [Functionai mean pressure = diastolic pressure + l/3 (systolic - diastolic) pressure.] The votumetric blood flow rate was measured for 8 dogs, averaging 5.6 f 1.7ml/min. From these values, the peripheral vascular resistance, the quotient obtained by dividing
Socket to fit hex. coupling on pliers
Fig. 3. The manual force applicator, used to apply intrusive toads of up to 1050 N to the 4th premolar.
G. C. Ng et al.
192 Mandibular
blood flow
Mondibulor
orteriol
(a)
Mandibular
blood
t
(b)
Mandibular
pressure
flow
1050 arterial
.S E \
N Force t pressure
c-
Lood
on Is -
Mandibular
n
(Cl
arterial
pressure
w
_
Load (off)
Periodontal on load
pulsation
superimposed
signal
Fig. 4. (a) Oscilloscope recording of flow and pressure in the mandibular artery. No load is applied to the teeth. (b) Oscilloscope recording of flow and pressure in the mandibular artery. The fourth premolar is subjected to an intrusive force of 1050 N for approx. 8 s, then released. (c) Oscilloscope tracing which demonstrates the phenomenon of periodontal pulsation. Note that an oscillation of the load signal (approx. 0.5 N peak-to-peak), synchronized with the arterial pressure pulsation, appears after application of a force of 20 N. functional mean pressure by flow, was calculated to have a value of 20.4 f 1.8 PRU (Peripheral Resistance Unit, 1 PRU = 1 mm Hg/ml/min). Peripheral uascular resistance changes associated with occlusal forces In the occlusal force-response experiments, light forces, up to 35 N, produced no measurable changes in vascular resistance. Occlusal forces of between 350 and lOSON, however, produced alterations in blood flow as shown in Figs 4a and b, and listed in Table 1.
Note that for dog B6 (with high peripheral resistance at rest) no peripheral vascular response was observed when forces up to 1050N were applied (Table 1). The results for dog Bl do not appear because of artifacts generated by motion of the flow probe relative to the mandibular artery coincident with the application or removal of force. The main changes in flow for various load values are shown in Fig. 5. Forces of 350N or less yielded negligible change. Larger forces caused the vascular resistance to rise by as much as 10.3 f 1.2 per cent (at
MAP: Mandibular tlow (ml/min).
4.9 5.5 5.2 5.5 5.6
0 0 4.8 3.9 11.6
arterial pressure (mm Hg); PRU: Peripheral resistance unit; DPRU:
18.9 18.2 18.9 17.9 18.9
4.8
0
18.9 16.9 17.9 16.9 16.6
- 7.2 - 3.0 - 3.0
0 - 7.3 -4.0 - 7.2
0
blood
0 -7.1 -5.3 - 5.6 - 12.1 Mandibular
0 -1.3 -1.0 -1.0 -2.3
-1.5 -0.6 - 0.6
0 -1.4 - 0.8 - 1.3
20.0 17.8 19.2 16.8 19.3 19.7 19.7
0
42.0
resistance unit; FLOW:
3.: 57
4.8
4.5 4.8
5.1 9.0
change in peripheral
0 0 0.9 0.7 2.2
18.9 18.2 19.8 18.6 21.1
4.9 5.1 4.7 5.0 4.4
350 500 700 900 1050
4.9 5.1 4.9 5.2 4.9
93 93 93 93 93
22
B9M
2
4.2 4s 4.1
- 2.4 2.5 5.0
,O.S 0.5 1.0
20.3 20.8 21.3
4.0 3.9 3.8
500
20.8 20.3 20.3
3.9 4.0 4.0
81 81 81
21
B8M
0 4.2 4.0 10s
0 0.8 0.8 1.9
20.0 20.0 20.8 20.0
4.8 4.8 4.6 4.8
350 700 900 1050
20.0 19.2 20.0 18.1
4.8 5.0 4.8 5.3
96 96 96 96
21
B7M
0
42.0
4.8
1050
42.0
4.8
201
22
B6F
- 6.7 -4.3
-1.7 -1.0 23.7 22.3
1.3 2.1
:::
26.7 25.4
0 - 3.9 -4.6 -9.7 - 12.5
0 -0.9 -1.1 - 2.2 -3.3 23.0 22.1 22.7 20.5 23.0
6.5 6.8 6.6
4.0 4.2
0 1.7 3.4 10.1 9.5
MO 900
4.2 4.6
107 107
17
BSM
23.0 23.0 23.8 22.7 26.3
25.4 23.3
:: 6:6 5.7
6.5
0 0.4 0.8 2.3 2.5
0 -8.5 - 3.8 -3.8
0
- 2.0 -0.8 -0.8
2.5
%
0.5
DPRU
23.3 21.3 20.0 20.0
19.5
PRU
After the release of force
4.2 4.6 4.9 4.9
23.0 23.4 24.6 25.0 28.8
0 5.2 9.6 9.6
0 1.2 2.0 2.0
23.3 24.5 22.8 22.8
4.2 4.0 4.3 4.3
350 700 900 1050
6.8
FLOW
6.5 6.4 6.1 6.0 5.2
15.7
%
3.0
DPRU
22.0
PRU
6.0
FLOW
During force application
900
Force (N)
350 500 700 900 1050
150 150 150 150 150
24 ‘
B4M
23.3 23.3 20.8 20.8
4.2 4.2 4.7 4.7
98 98 98 98
18
83b
19.0
PRU
7.0
FLOW
133
MAP
19
Wt (kg)
B2F
-
Before force application
Table 1. The peripheral vascular resistance before, during and after occlusal force application
194
G. C. Ng et al.
Percentage
14
force
increase in PRU during
opplicotion
12
T
st 6
I
4 i
2I 300
0
I 500
+
f
Occlusol force (N) I I1 I s 700 900 1100
-IO
_,2
Percentage
++
force
decrease PRU after
release
Fig. 5. Mean changes (and 95 per cent confidence limits) in vascular resistance produced by the application and release of forces of various magnitudes.
105ON). The resistance did not return to normal when load was removed, but dropped below the steady-state value. As Fig. 5 indicates this decrease exceeded the initial increase by as much as 8.5 f 4.5 per cent (at 105ON). Periodontal
pulsation
When the pneumatic loading device was used for tooth intrusion, a fluctuation in the load output signal, of approx. 0.5 N peak-to-peak, synchronized with the blood pressure pulse and thought to be caused by the periodontal pulsation (Korber, 1970), was observed. The magnitude of the pulsation was not seen to vary with the application of forces up to 35 N. A typical waveform is shown in Fig. 4c. DISCUSSION
The technique for exposing and cannulating the mandibular artery we have developed offers a useful method for the study of the isolated periodontium (i.e. periodontal ligament, gingiva and alveolar bone) in situ. Its use will facilitate future studies of the effects of drugs, hormones and surgical procedures on the periodontal vasculature. The values of mandibular arterial pressure, volumetric blood flow and peripheral vascular resistance obtained are comparable to those presented by Bishop et al. (1959), which is the only other study of pressure and flow in this region. It is surprising that the heavy forces we used produce a change in vascular resistance of 10 per cent or less. This may mean that the vessels of the periodontal ligament are well protected from occlusion, or it may indicate only that the blood flow to the periodontal ligament is but a small fraction of the measured flow, the remainder going to the pulp and the gingiva. The question may be resolved by the observation that, on the removal of force, the flow resistance consistently dropped to a level significantly
below the steady-state. This, plus the fact that flow resistance returned, slightly toward the steady-state condition while load was maintained, is highly suggestive of the occurrence of reactive hyperaemia in the periodontal ligament. This implies that functional tooth loading can compromise blood flow to the point of making the periodontal ligament ischaemic. This affirms that only a portion of the measured flow passes through the ligament, but suggests an extremely strong connection between the periodontal vasculature and the tooth supporting system. To look at only the flow through the periodontal ligament, one must cut off the flow to the gingiva, alveolar bone and pulp. This can only be accomplished by more extensive surgery which causes a more radical departure from the physiological state. A mathematical model might be constructed to subtract the flow through these paths from the measured flow, but the apportionment of the flow among these vascular beds must first be established. The extent of the participation of the periodontal vasculature in tooth support is implied by the observations of periodontal pulsation we recorded. Birn’s (1966) observation that the vascular density of the periodontal ligament increases posteriorly implies that, if the blood vessels play a major role in tooth support, the threshold force which stops pulsation should also increase posteriorly. Our findings indicate that this may be true, although the fact that the force required to stop the pulsation of the canine 4th premolar is greater than 35 N, or more than 200 times Parfitt’s (1960) observation, is surprising. The cause of this huge difference may lie in the normal functional forces seen by the respective teeth. The functions and shapes of the individual teeth suggest that the functional load on each tooth may increase posteriorly. Taken with Birn’s findings, this implies a correlation between functional loading and periodontal vascularity. Difference in diet between dog and man could also result in the premolars of dog encountering much larger functional loads than those applied to human molars. The difference from incisor to premolar in vascularity and in the force required to obliterate the periodontal pulsation may well be disproportionately magnified by the change in species between Parfitt’s work and our own. This does, however, imply that the force necessary to stop the periodontal pulsation may be determined by the vascular density which may, in turn, be a product of functional loading. This supports the idea that the vasculature participates directly and significantly in the support of the teeth. In our opinion, further work should be directed toward the measurement of the flow and pressure in localized areas of the periodontal vasculature. Although this approach presents numerous technical problems with respect to gaining access to the periodontal ligament, it will offer more direct evidence as to the exact mechanisms through which the vascular supply to the periodontal ligament participates in tooth support. REFERENCES Bien S. M. 1966. Fluid
dynamic mechanisms which regulate tooth movement. Adu. oral Biol. 2, 173200. Birn H. 1966. The vascular supply of the periodontal membrane. J. periodont. Res. 1, 5146.
Effects of toatb loading on the periodontal vasculature Bishop J. G., Matthews J. L., Dorman II. L. and Moore E. E. 1959. Blood flow and blood pressure in the mandibutar artery. J. derrr. Res. 38,244252. Castehi W. A. and Dempster W. T. 1964. The ~rj~onta~ vasculature and its responses to experimental pressures. J, Am.
dent. Ass. 70. 1194-905.
Ganong W. F. l969.‘1;!evlew of Medical Physiology. 4th edn, Lange, Los Altos, Cahf. Giannelly A. 1969. Force induced changes in the vascularity of the periodomal tigament. rim. J. Orthod. 55, 5-11. GStze W. 1965. Ueber ~~ternsverander~ge~ des Parodon-
195
tiums. Dt. Zahniirzt[. Z. 15,4655470. Kiirber K. Ii. 1970. Periodontal pulsation. J. Periudont. 41, 382-390. Par&t G. 1960. Measurement of the physiological mobility of individual teeth in an axial direction J. denr. Res. 39, 608-618.
Slatter J. and Picton D. C. A. 1972. The effect on intrusive tooth mobility of noradrenaline iniected locallv in monkeys. J. Periohont. Res. 7, 144150: Wills D. 3, P&on D. C, A. and Davies W. I. I976 A study of the fiuid systems of the periodontium in macaque monkeys. Archs oraf Biol. tl, 175-185.
Vol.
‘X03-9969/81/03OlSS-07602.00/O
26, pp. 189 lo 195, 1981
PergamonPress Ltd
Prmtedin Great Britam
EFFECTS OF TOOTH LOADING ON THE PERIODONTAL VASCULATURE OF THE MANDIBULAR FOURTH PREMOLAR IN DOGS G. C. NG,‘.’ T. W. WALKER,“’ W. ZINC& and P. S. BURKE’ ‘Medical Research Council Group in Periodontal Physiology, Faculty of Dentistry, University of Toronto, Toronto, Ontario, Canada ‘Institute of Biomedical Engineering, University of Toronto, Toronto, Ontario, Canada Summary-A surgical technique was developed to isolate the arterial supply to the periodontal ligament, pulp and gingiva of the canine mandibular 4th premolar, and to measure the pressure and flow therein. This model system was used to study the interaction between tooth loading and periodontal blood flow. Intrusive forces of less than 350N were found to produce negligible alteration of the measured blood flow, while loads of 1050 N produced a reduction of flow equivalent to an increase in vascular resistance of approximately 10 per cent, with no effect on arterial pressure. The increase in flow on removal of load was greater than the reduction seen on application, suggesting that reactive hyperemia may occur in the periodontal tissues. The phenomenon ‘of periodontal pulsation first studied by Parfitt (J. dent. Rex 39, 608%618) in humans, was examined in the dog as a part of the present work. It was found that the pulsation of the canine mandibular 4th premolar was still in evidence under applied loads 230 times that which Parfitt found to obliterate the movement of the human incisor. This may be taken to indicate that the density and architecture of the periodontal vasculature may, in part, be determined by the loads applied to the teeth during function.
INTRODUCTlON The blood vessels in the periodontal ligament have long been implicated as a component of the system supporting the teeth. Parfitt (1960) observed a pulsation, synchronous with the arterial pulse, superimposed on the signal measuring the load applied to human incisors. He found that when the load was increased to 4 g (0.04 N), pulsation was strongest, but, with further increase in axial load, pulsation diminished. Above 15 g (0.15 N), pulsation was obliterated. He attributed this observation to a vascular tide which supported the tooth when subjected to a load of less than 0.15 N. This periodontal pulsation has also been demonstrated by Kijrber (1970). Bien (1966) reported that the tooth displacement response in a live rat is different from that in a dead rat. He found that the teeth of a dl:ad animal would not return to the equilibrium position after the removal of load unless the thorax was squeezed. He attributed this difference in responsl: to the cessation of blood flow when the rat was dead. Slatter and Picton (1972) conducted experiments on adult rhesus monkeys to study the effect produced by a local injection of noradrenaline on axial movements of incisors. They reported that the injection of noradrenaline, a vasoconstrictor, reduced tooth mobility for a period of 6@9Omin. No comparable alteration in mobility was detected when physiological saline was injected. It was concluded that collapse of the periodontal vasculature prevented the tooth from returning to the origmal resting position after the initial application of force, and that mobility was thus decreased. The participation of the periodontal vasculature in the support of the teeth during simulated function has been clearly demonstrated. Although the blood
vessels occupy only l-2 per cent of the periodontal ligament space (Giitze, 1965), Wills, Picton and Davies (1976) have demonstrated in macaque monkeys that 30 per cent of tooth mobility is associated with the blood vessels in the ligament space. They concluded that the blood in this space has an energydissipating function, providing a major viscous component in the displacement and recovery of the tooth under occlusal forces. Whereas all these studies confirm the participation of the periodontal vasculature in tooth support, they tell little about the dynamic behaviour of the vasculature itself during and after the application of occlusal force. Other workers have attempted to reveal the vascular responses by a combination of perfusion and histological techniques which only depict static conditions. Castelli and Dempster (1964), applying a perfusion method in monkeys, demonstrated that a horizontal force of 1 N can induce local ischaemia in the ligament. Similarly, Gianelly (1969) showed, also using perfusion, that a lateral force of 1.5 N induced vascular occlusion in the compressed areas of the periodontal ligament in dog incisors. Although these experiments delineate the change in vascularity associated with orthodontic force-application (light horizontal forces of long duration), the dynamic response of the periodontal vasculature to simulated function is still not known. This is the problem we have investigated.
MATERIALS AND
METHODS
The periodontium of the mandibular 4th premolar was selected because the mandibular artery is relatively free from branches in the vicinity of this tooth. Blood Aow and blood pressure in the mandibular 189
G. C. Ng
190
et al.
T : Tourniquet L: Ligature
Fig. 1. The canine mandible, showing the two windows through which access to the mandibular artery was gained, and the locations at which the instruments for measuring arterial blood flow and pressure were placed.
artery were continuously monitored while the tooth was subjected to occlusal force. This technique offers the advantage of recording the dynamic response of the vasculature in situ but has the disadvantage of being invasive in nature. The study was conducted on dogs weighing between 17 and 25 kg. This size range of dog was selected to ensure that the mandibular artery would be sufficiently large (approx. 1 mm in outside diameter) to permit cannulation. Animals were of either sex and of no particular breed; all were in good genera1 health, with healthy orat tissues, visually assessed. Eight dogs were used to perfect the surgical technique and the instrumentation. Nine more animals constituted the experimental group. After sedation with Atrovit (Acepromazine Maleate, Ayerst, McKenna & Harrison Ltd, Montreal, Canada), the dogs were anaesthetized using intravenous Nembutal (Pentobarbital sodium, Abbott Laboratories, Montreal, Canada). A tracheal cannula was inserted as an artificial airway. An intravenous catheter was placed in the cephalic vein for the administration of a 0.9 per cent saline: 0.5 per cent dextrose drip (Travenol Lab. Inc., Morton Grove, Ill., U.S.A.) to reduce shock. The eyelid reflex of the dog was tested regularly and additional anaesthetic was administered as necessary. A sample of venous blood was withdrawn to measure the haematocrit value in order to establish the probe factor for the electromagnetic flowmeter. Blankets and an infrared heat lamp were used to stabilize the animal’s body temperature, which had a profound effect on the blood flow being measured. The animal was placed in a supine position with its four legs tied to the table. A cut-down technique was employed to cannulate one femoral artery in order to monitor the systemic arterial pressure. With an electro-cautery, the inferior border of the mandible was exposed along its entire length. The periosteum and soft tissues were stripped and the inferior
alveolar neurovascular bundle exposed in two locations (Fig. 1) by cutting windows in the bone with an air rotor and a round carbide bur. Under a stereo-microscope, the mandibular artery was separated from the rest of the neurovascular bundle at both anterior and posterior windows using blunt dissection, A cannula of 0.965 mm polyethylene tubing was then inserted into the mandibular artery at the site indicated in Fig. 1, and a No. 4 electromagnetic flow probe (Carolina Medical Electronics, King North Carolina, U.S.A.) secured around the posterior portion of the mandibuIar artery. The neck of the flow probe was fitted into a Teflon bracket and the whole assembly was taped to the mandible to ehminate any movement of the flow probe which could generate artifacts in the flow recordings. A tourniquet was applied to the artery, posterior to the flow probe, arresting the mandibular blood flow. Since blood could still reach the ~riodontium of the 4th premolar via the posterior mental artery, this vessel was ligated at the posterior mental foramen. This measure, coupled with the insertion of the pressure-measurement cannula, ensured that the only major vessel supplying blood to the 4th premolar was the mandibular artery, the flow in which was measured. The ffowmeter was adjusted to give a zero output and the tourniquet released. After a period of approx. 10min to allow the blood flow to return to a stable equilibrium state, the mandibular arterial pressure and the volumetric flow rate were recorded on the storage oscilloscope. A Polaroid oscilloscope camera (Model CS, Tektronix, Beaverton, Oreg., U.S.A.) was used to obtain a hard copy of the recording. The experimentation proper was then begun. A pneumatic loading device (Fig. 2) was installed with one arm seated at the crown of the 4th premolar and the other arm firmly against the mandible at a location between the two windows. Intrusive forces of 20 and 35 N were applied for periods of approx. 8 s, separated by recovery periods of at least 2 min. Mandibular arterial pressure and flow rate were recorded
Effects of tooth loading on the periodontal vasculature
191
Pressure regulator Compressed air
Movable arm
Fig. 2. Diagram of the pneumatic loading system with which intrusive loads of up to 35 N were applied to the 4th premolar. during load application. This apparatus was also used to study the periodontal puisation. A manual force applicator [Fig. 3) was used to apply larger forces (350, 500, 700, 900, 105ON) to the 4th premolar. Blood pressure and flow rate were again recorded during load application. RESULTS Systemic urferia~ pressure, ~~~~~~r and volumetric Hood jiow rate
arterial pressure
The data from one dog (No. B6) were omitted from the general analysis because this animal had a high
peripheral vascular resistance suggestive of some constricting peripheral vascular disorder. For the other 16 dogs, systolic and diastolic pressures were 185 zfr11 and 130 & 8 mm Hg respectively (mean f 95 per cent confidence limit). The mandibular arterial pressures for 12 dogs averaged 136 &- 17 and 104 & 13 mm Hg (systolic and diastolic pressures, respectively) and had a functional mean of 114 + 14 mm Hg. [Functionai mean pressure = diastolic pressure + l/3 (systolic - diastolic) pressure.] The votumetric blood flow rate was measured for 8 dogs, averaging 5.6 f 1.7ml/min. From these values, the peripheral vascular resistance, the quotient obtained by dividing
Socket to fit hex. coupling on pliers
Fig. 3. The manual force applicator, used to apply intrusive toads of up to 1050 N to the 4th premolar.
G. C. Ng et al.
192 Mandibular
blood flow
Mondibulor
orteriol
(a)
Mandibular
blood
t
(b)
Mandibular
pressure
flow
1050 arterial
.S E \
N Force t pressure
c-
Lood
on Is -
Mandibular
n
(Cl
arterial
pressure
w
_
Load (off)
Periodontal on load
pulsation
superimposed
signal
Fig. 4. (a) Oscilloscope recording of flow and pressure in the mandibular artery. No load is applied to the teeth. (b) Oscilloscope recording of flow and pressure in the mandibular artery. The fourth premolar is subjected to an intrusive force of 1050 N for approx. 8 s, then released. (c) Oscilloscope tracing which demonstrates the phenomenon of periodontal pulsation. Note that an oscillation of the load signal (approx. 0.5 N peak-to-peak), synchronized with the arterial pressure pulsation, appears after application of a force of 20 N. functional mean pressure by flow, was calculated to have a value of 20.4 f 1.8 PRU (Peripheral Resistance Unit, 1 PRU = 1 mm Hg/ml/min). Peripheral uascular resistance changes associated with occlusal forces In the occlusal force-response experiments, light forces, up to 35 N, produced no measurable changes in vascular resistance. Occlusal forces of between 350 and lOSON, however, produced alterations in blood flow as shown in Figs 4a and b, and listed in Table 1.
Note that for dog B6 (with high peripheral resistance at rest) no peripheral vascular response was observed when forces up to 1050N were applied (Table 1). The results for dog Bl do not appear because of artifacts generated by motion of the flow probe relative to the mandibular artery coincident with the application or removal of force. The main changes in flow for various load values are shown in Fig. 5. Forces of 350N or less yielded negligible change. Larger forces caused the vascular resistance to rise by as much as 10.3 f 1.2 per cent (at
MAP: Mandibular tlow (ml/min).
4.9 5.5 5.2 5.5 5.6
0 0 4.8 3.9 11.6
arterial pressure (mm Hg); PRU: Peripheral resistance unit; DPRU:
18.9 18.2 18.9 17.9 18.9
4.8
0
18.9 16.9 17.9 16.9 16.6
- 7.2 - 3.0 - 3.0
0 - 7.3 -4.0 - 7.2
0
blood
0 -7.1 -5.3 - 5.6 - 12.1 Mandibular
0 -1.3 -1.0 -1.0 -2.3
-1.5 -0.6 - 0.6
0 -1.4 - 0.8 - 1.3
20.0 17.8 19.2 16.8 19.3 19.7 19.7
0
42.0
resistance unit; FLOW:
3.: 57
4.8
4.5 4.8
5.1 9.0
change in peripheral
0 0 0.9 0.7 2.2
18.9 18.2 19.8 18.6 21.1
4.9 5.1 4.7 5.0 4.4
350 500 700 900 1050
4.9 5.1 4.9 5.2 4.9
93 93 93 93 93
22
B9M
2
4.2 4s 4.1
- 2.4 2.5 5.0
,O.S 0.5 1.0
20.3 20.8 21.3
4.0 3.9 3.8
500
20.8 20.3 20.3
3.9 4.0 4.0
81 81 81
21
B8M
0 4.2 4.0 10s
0 0.8 0.8 1.9
20.0 20.0 20.8 20.0
4.8 4.8 4.6 4.8
350 700 900 1050
20.0 19.2 20.0 18.1
4.8 5.0 4.8 5.3
96 96 96 96
21
B7M
0
42.0
4.8
1050
42.0
4.8
201
22
B6F
- 6.7 -4.3
-1.7 -1.0 23.7 22.3
1.3 2.1
:::
26.7 25.4
0 - 3.9 -4.6 -9.7 - 12.5
0 -0.9 -1.1 - 2.2 -3.3 23.0 22.1 22.7 20.5 23.0
6.5 6.8 6.6
4.0 4.2
0 1.7 3.4 10.1 9.5
MO 900
4.2 4.6
107 107
17
BSM
23.0 23.0 23.8 22.7 26.3
25.4 23.3
:: 6:6 5.7
6.5
0 0.4 0.8 2.3 2.5
0 -8.5 - 3.8 -3.8
0
- 2.0 -0.8 -0.8
2.5
%
0.5
DPRU
23.3 21.3 20.0 20.0
19.5
PRU
After the release of force
4.2 4.6 4.9 4.9
23.0 23.4 24.6 25.0 28.8
0 5.2 9.6 9.6
0 1.2 2.0 2.0
23.3 24.5 22.8 22.8
4.2 4.0 4.3 4.3
350 700 900 1050
6.8
FLOW
6.5 6.4 6.1 6.0 5.2
15.7
%
3.0
DPRU
22.0
PRU
6.0
FLOW
During force application
900
Force (N)
350 500 700 900 1050
150 150 150 150 150
24 ‘
B4M
23.3 23.3 20.8 20.8
4.2 4.2 4.7 4.7
98 98 98 98
18
83b
19.0
PRU
7.0
FLOW
133
MAP
19
Wt (kg)
B2F
-
Before force application
Table 1. The peripheral vascular resistance before, during and after occlusal force application
194
G. C. Ng et al.
Percentage
14
force
increase in PRU during
opplicotion
12
T
st 6
I
4 i
2I 300
0
I 500
+
f
Occlusol force (N) I I1 I s 700 900 1100
-IO
_,2
Percentage
++
force
decrease PRU after
release
Fig. 5. Mean changes (and 95 per cent confidence limits) in vascular resistance produced by the application and release of forces of various magnitudes.
105ON). The resistance did not return to normal when load was removed, but dropped below the steady-state value. As Fig. 5 indicates this decrease exceeded the initial increase by as much as 8.5 f 4.5 per cent (at 105ON). Periodontal
pulsation
When the pneumatic loading device was used for tooth intrusion, a fluctuation in the load output signal, of approx. 0.5 N peak-to-peak, synchronized with the blood pressure pulse and thought to be caused by the periodontal pulsation (Korber, 1970), was observed. The magnitude of the pulsation was not seen to vary with the application of forces up to 35 N. A typical waveform is shown in Fig. 4c. DISCUSSION
The technique for exposing and cannulating the mandibular artery we have developed offers a useful method for the study of the isolated periodontium (i.e. periodontal ligament, gingiva and alveolar bone) in situ. Its use will facilitate future studies of the effects of drugs, hormones and surgical procedures on the periodontal vasculature. The values of mandibular arterial pressure, volumetric blood flow and peripheral vascular resistance obtained are comparable to those presented by Bishop et al. (1959), which is the only other study of pressure and flow in this region. It is surprising that the heavy forces we used produce a change in vascular resistance of 10 per cent or less. This may mean that the vessels of the periodontal ligament are well protected from occlusion, or it may indicate only that the blood flow to the periodontal ligament is but a small fraction of the measured flow, the remainder going to the pulp and the gingiva. The question may be resolved by the observation that, on the removal of force, the flow resistance consistently dropped to a level significantly
below the steady-state. This, plus the fact that flow resistance returned, slightly toward the steady-state condition while load was maintained, is highly suggestive of the occurrence of reactive hyperaemia in the periodontal ligament. This implies that functional tooth loading can compromise blood flow to the point of making the periodontal ligament ischaemic. This affirms that only a portion of the measured flow passes through the ligament, but suggests an extremely strong connection between the periodontal vasculature and the tooth supporting system. To look at only the flow through the periodontal ligament, one must cut off the flow to the gingiva, alveolar bone and pulp. This can only be accomplished by more extensive surgery which causes a more radical departure from the physiological state. A mathematical model might be constructed to subtract the flow through these paths from the measured flow, but the apportionment of the flow among these vascular beds must first be established. The extent of the participation of the periodontal vasculature in tooth support is implied by the observations of periodontal pulsation we recorded. Birn’s (1966) observation that the vascular density of the periodontal ligament increases posteriorly implies that, if the blood vessels play a major role in tooth support, the threshold force which stops pulsation should also increase posteriorly. Our findings indicate that this may be true, although the fact that the force required to stop the pulsation of the canine 4th premolar is greater than 35 N, or more than 200 times Parfitt’s (1960) observation, is surprising. The cause of this huge difference may lie in the normal functional forces seen by the respective teeth. The functions and shapes of the individual teeth suggest that the functional load on each tooth may increase posteriorly. Taken with Birn’s findings, this implies a correlation between functional loading and periodontal vascularity. Difference in diet between dog and man could also result in the premolars of dog encountering much larger functional loads than those applied to human molars. The difference from incisor to premolar in vascularity and in the force required to obliterate the periodontal pulsation may well be disproportionately magnified by the change in species between Parfitt’s work and our own. This does, however, imply that the force necessary to stop the periodontal pulsation may be determined by the vascular density which may, in turn, be a product of functional loading. This supports the idea that the vasculature participates directly and significantly in the support of the teeth. In our opinion, further work should be directed toward the measurement of the flow and pressure in localized areas of the periodontal vasculature. Although this approach presents numerous technical problems with respect to gaining access to the periodontal ligament, it will offer more direct evidence as to the exact mechanisms through which the vascular supply to the periodontal ligament participates in tooth support. REFERENCES Bien S. M. 1966. Fluid
dynamic mechanisms which regulate tooth movement. Adu. oral Biol. 2, 173200. Birn H. 1966. The vascular supply of the periodontal membrane. J. periodont. Res. 1, 5146.
Effects of toatb loading on the periodontal vasculature Bishop J. G., Matthews J. L., Dorman II. L. and Moore E. E. 1959. Blood flow and blood pressure in the mandibutar artery. J. derrr. Res. 38,244252. Castehi W. A. and Dempster W. T. 1964. The ~rj~onta~ vasculature and its responses to experimental pressures. J, Am.
dent. Ass. 70. 1194-905.
Ganong W. F. l969.‘1;!evlew of Medical Physiology. 4th edn, Lange, Los Altos, Cahf. Giannelly A. 1969. Force induced changes in the vascularity of the periodomal tigament. rim. J. Orthod. 55, 5-11. GStze W. 1965. Ueber ~~ternsverander~ge~ des Parodon-
195
tiums. Dt. Zahniirzt[. Z. 15,4655470. Kiirber K. Ii. 1970. Periodontal pulsation. J. Periudont. 41, 382-390. Par&t G. 1960. Measurement of the physiological mobility of individual teeth in an axial direction J. denr. Res. 39, 608-618.
Slatter J. and Picton D. C. A. 1972. The effect on intrusive tooth mobility of noradrenaline iniected locallv in monkeys. J. Periohont. Res. 7, 144150: Wills D. 3, P&on D. C, A. and Davies W. I. I976 A study of the fiuid systems of the periodontium in macaque monkeys. Archs oraf Biol. tl, 175-185.