145

Pain, 1(1977) 115-152 @ ElsevieriNorth-Holland

SENSATION IN MAN

J. AZERAD

(Accepted

EVOKED

* and

Laboratcire (France)

Biomedical

March

BY BIPOLAR

A. WODA

de Physiologic

29th,

Press

INTRAPULPAL

STIMULATION

**

des C’cntres Scrrvzrs.

-1, aLvnue Gordon-Bennett,

75016-Paris

1977)

SUMMARY

Bipolar intrapulpal stimulation was applied to human teeth using the same procedure as in animal experiments. The effects of variation of stimulus parameters on the quality of sensation were studied. A prepain sensation exists which cannot be explained by diffusion of the stimulus to periodontal tissues. When the intensity of stimulation is increased, the prepain sensation is gradually replaced by a pinprick sensation. With long, high intensity stimulation, an acute long lasting very painful sensation appears. To evoke a pinprick sensation the best stimulation seems to be a 50 msec train (0.5 msec, 300 Hz, 0.5 mA). Longer train duration and a higher intensity of current are necessary to evoke a long lasting, acute very painful sensation. Since the exclusively A6 and C nerve fiber content of the dental pulp is well documented and since it is possible to avoid current diffusion outside the dental pulp cavity, the tooth pulp implantation seems to be a good technic for studying pain, as long as the investigator uses adequate stimulation.

INTRODUCTION

Electrical stimulation of the dental pulp is now widely used in animals as an experimental painful stimulation. Indeed dental pulp offers to experiments an exclusively small nerve fiber content (A6 and C) [7,10,13,18,25, 301 and the possibility to confine the stimulation to a well localized area [ 14,201. Moreover, it is generally believed that pain is the only sensation elicited by pulp stimulation [2,3,8,9,11,20 and others]. In the experiments carried out up till now by different research workers, only pain has been evoked by suprathreshold electrical stimulation of the * Assistant ** Assistant

-

Faculte Faculte

de Chirurgie de Chirurgie

Dentaire, Dentaire,

Paris VII. Paris V.

146 human tooth. I~fowever, when a near-threshold stimulus is delivered, a nonpainful sensation is generally described. In these experiments the stimulus was generally monopolar and always applied to the crown surface; tooth pulp was then stimulated through enamel and dentine whose high electrical resistance is well known [22]. The question then arises whether this nonPainful sensation results from the diffusion of current to neighboring soft tissues or from a threshold stimulation of the pulp nerve fibers. In the experiment we are presenting here, the dental pulp of a human subject was electrically stimulated through a bipolar electrode inserted into the pulp by the same procedure as in animal experiments [ 4,9,28,34]. \Ve investigated the effect, on the quality and threshold of the sensation, of variations in stimulus parameters. The results will be of practical use in the future in animal experiments and will give an idea of what sensation is evoked in man by the stimulations currently applied during animal experiments. METHODS Eight testing procedures were performed on 6 healthy third molars. These teeth were fully erupted and normally innervated [6]. They belong to 4 young dental practitioners, two of whom were the present authors. The tooth vitalities were checked before an anesthetic block of the superior or inferior dental nerves. Two steelwires (diameter: 0.2 mm) were directly implanted into the dental pulp through two holes drilled in the enamel and dentine. The wires were then secured with dental acrylic resin and radiographic control of their position was made. Six hours after the anesthetic block, the subject sat in a dental chair and was acoustically isolated during the testing procedure. Before each trial, the subject was warned by a signal from the investigators. Stimulation was delivered in the following 5 set, and the trials were separated by about 15 sec. The subject estimated stimulation intensity on a 3-point scale: 0 = no sensation; 1 = first perception (Sl); 2 = painful sensation (S2). Monophasic square wave pulses were generated by a digitimer with constant voltage through an isolated stimulation unit, and the electrode resistance was systematically measured and remained constant throughout the course of the experiments, with values ranging between 15 and 25 kfl. For the study of one stimulus parameter, each value of the parameter was tested in several ascending and descending series of increasing or decreasing intensity. In each series we considered as threshold the first intensity of current which led to a shift in the subject answer (for example, from 0 to 1 in an ascending series, or from 1 to 0 in a descending series). Thresholds obtained in different series were averaged. Parameters of stimulation were tested and their effect on threshold sensations were determined. The first parameter was pulse duration, the second was frequency of 0.5 msec pulses in a 10 msec duration tram, and the third, pulse train of variable duration. These trains were composed of 0.5 msec pulses at a frequency of 300 Hz. In two cases, the wires remained in place for one night and the following day the full testing procedure was repeated. The results are derived from S testing procedures.

147 RESULTS

(1) Wire tolerance The implanted wires were well tolerated and of the 6 implantations, 3 were free of pain in the absence of stimulation. In two instances when the wires were in place for 4 and 7 days, pain did not occur unless the wires were moved. This pain was described as a sharp pinprick. In the 3 other teeth a light background of pain was described, which disappeared when there was absence of movement of the wires. (2) Sensation quality During electrical stimulation by a single pulse or by a short train, the first sensation (Sl) was described by all subjects as extremely light, and the quality of sensation was difficult to describe, but was not painful. By increasing the stimulation intensity a painful prick was felt (S2). Moreover a 6-fold increase of S2 threshold did not modify the quality of sensation and the stimulation could be repeated and was well tolerated by all subjects. It was interesting to note that the transition from an Sl response to an S2 response was gradual since the subjects did not detect any sharp change in the quality of sensation when the stimulation intensity was increased. Sensation was generally of short duration and localized to the stimulated tooth. However, in two cases the sensation was referred to a tooth located on the same side but in the other jaw. For long duration trains (1 set or more) of 300 Hz, 0.5 msec pulse duration, a t,hrobbing sensation occurred similar to that described as subpulpitis pain. This pain occurred 1 set after the onset of stimulation and lasted for 2 or 3 sec.

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Fig. 1. Single pulse duration curve. Abscissa = pulse duration in msec. Ordinate = intensity in pA (scale is log-log). Upper curve, S2; lower curve, Sl. Vertical bars of the curve refer to the fiducial limit of 95% probability. The curves of Figs. 1, 2 and 3 represent the mean value of 8 testing procedures.

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Fig. 2. IO mser train of variable frequency curve. Abscissa = number of pukes in the train. Ordinate = int.ensity in pA (scale is lag-log). Upper curve, S2; lower curve, SI \wertiCI\/ itars of the curve refer to the fiducial limit of 95”: probability.

For intermediate lengths of train stimulat.ion, when sensations were elicited, the pinprick sensation was first and was followed by the throbbing. In two cases a second type of stimulation [ 261 was used. It consisted of a ~o~~tinuous train (several seconds) with high intensity (more than 0.3 m-4). The subjects described a long lasting, acute, unbearable pain.

The response variations following modifications of respectively single pulse duration, pulse frequency (number of 0.5 msec pulses in a 10 msec train) and train duration (0.5 msec, 300 Hz) are given in Figs. 1, 2 and 3. In all curves an increase in stimulation parameters affects the S2 threshold

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Fig. 3. Train duration curve (300 Hz, 0.5 mscc). Abscissa = train duration in msec. Ordinate = intensity in PA (scale is log-log). Upper curve, SC!; lower curve, Sl. Vertical bars of the curve refer to the fiducial limit of 95% probability.

149

but increasing pulse frequency (Fig. 2) and train duration (Fig. 3) affect the Sl threshold very little. The pulse duration curve (Fig. 1) indicates that a maximum effect on Sl and S2 is obtained with a 0.5 msec duration pulse. For the frequency curve (Fig. 2), it appears that two pulses in a 10 msec train (200 Hz) give an almost maximal effect on S2. The train duration curve (Fig. 3) indicates that a 50 msec train (300 Hz) is necessary to get the maximal effect on S2. For longer train duration, Sl and S2 tend to overlap (Fig. 3). DISCUSSION

(1) Dental pulp stimulation technique Recordings of pulp and non-pulp fibers in the inferior dental nerve were made by Wagers and Smith [34] in the dog, and by Greenwood et al. [14] in the cat. These studies showed that monopolar intrapulpal stimulation also recruits large nerve fibers belonging to surrounding tooth tissues. The results of both groups of workers indicated that a monopolar stimulation results in an overlapping of threshold of pulp and non-pulp units. In these experiments, when on the contrary bipolar stimulation was used, it was not possible to excite non-pulp fibers, even with a 90 V stimulus. However, Matthews et al. [20] showed that a monopolar stimulation when delivered with limited intensity values could be successfully applied. -Another approach first described by Kerr et al. [19] was to stimulate in close proximity to the pulp through two wires sealed in place in dentine with dental amalgam (intradentinal stimulation). Many workers still use this technique [12,17,36 and others]. However the risk of current spread to periodontal tissues seems to be increased. Indeed using this kind of stimulation the threshold of the jaw-opening reflex in cats is high and fluctuating when compared to the threshold obtained with direct intrapulpal stimulation [27]. Moreover, Nord [ 241 comparing intradentinal and intrapulpal stimulation techniques found units activated by an intradentinal stimulation which could not be fired by an intrapulpal stimulation. Some of these units could also be activated by a gingival stimulation. On the contrary with a bipolar intradentinal stimulation at intensity below 10 V, Horiuchi and Matthews [17] were able to limit current spread to the tooth pulp. But these authors did not show that with higher intensities there is no current spread to the surrounding tissues. Finally, if the goal is to exclusively stimulate the dental pulp of the cat using a full intensity range [21], it seems safer to use a bipolar intrapulpal stimulation. Moreover this technique proved during these experiments and in the past ones [ 1,271 that damage to the pulp is within acceptable limits since both sensory and reflex thresholds remained constant for at least one week. (2) Sensation quality Various stimuli (mechanical, thermic, chemical) have been applied to dentine or pulp in man. They evoke only painful sensations (see articles of Anderson et al. [ 31, Brannstrom and Astrom [8], Hensel and Mann [ 151). So

150 far Only a few experiments have been specifically concerned with the quality evoked by electrical stim~llation of the human tooth pulp. Among these experiments two groups of results can be distin~ished: Van Hassel and Harrington [31] used transenamel monopolar stimulation and their patients described an unpleasant sensation only. Chatrian et al, [ 121 used intradentinal, amalgam sealed, bipolar electrodes; all their subjects described the sensation “as sharp pain of very brief duration, strictly confined to the individu~ tooth stimulated”. However, one cannot conclude from these results that pain is the only sensation evoked by tooth stimulation since the authors applied only suprathreshold stimuli. On the contrary, Vargas [32], Shimizu [29], Mumford [23] and Matthews et al. [20] reported other sensations for near-threshold stimulation, although increasing intensity evoked painful sensations. In our experiments we never found cold, warm, hot or mechanical sensations, such as were described in Mumford’s experiments [23]. Neither did Vargas 1321, Shimizu [29] or Matthews et al. [ 201, who called the first sensation respectively “a pure prick which is not painful”, “prepain” or “pricking throbbing or pulsating but not as painful”. Our results are in agreement with those obtained with extracoronal stimulation and show that a prepain sensation exists and cannot be accounted for by diffusion of the current to surrounding structures. This of course does not mean that neurons activated with this stimulation intensity and responsible for the prepain sensation are not related to pain mechanisms. On the contrary we would like to emphasize that our subjects did not report any sharp distinction in quality between Sl and S2. En experiments of Matthews et al. [20], for a S-fold increase in the threshold of the first sensation, a pain sensation sometimes appeared. This result is very close to the 4-fold increase necessary in our study to get an S2 sensation, This sensation (S2) was like a pinprick and was perfectly tolerable to all our subjects. This would seem to justify the observation [1,33] that an awake chronic cat can withst~d single pulse tooth pulp stimulation, evoking a jaw opening reflex, without any apparent discomfort. Moreover, it might be useful to recall that the threshold of the jaw opening reflex in man [ 201, the threshold of the first sensation (Sl) measured by Matthews et al. [20] and by us in this study and the threshold of the jaw opening reflex in acute 151 or chronic cats [27f are of the same order of magnitude. This line of evidence would mean that in animal experiments, when dental pulp stimulation is used for the study of pain, we are working: on a prepain sensation if stimulation intensity is near the threshold of the jaw opening reflex; on a pinprick sensation if a nearly 4-fold threshold intensity is used. No other kind of sensation can be expected if single pulses or short trains of pulses are used. However, these conclusions must be carefully considered since it is always difficult to infer an animal sensation from a human report; moreover, anatomical differences between cat and human teeth obviously exist which result in differences in current spread [ 17 I. of sensation

151 The same considerations must be kept in mind if the following statements are to be applied to animal experiments: To elicit a pinprick sensation, a 50 msec train (0.5 msec, 300 Hz) at 0.5 mA seems to be the best stimulus. If short latency cell responses are to be analyzed, then a 10 msec train (0.5 msec, 300 Hz) at 0.7 mA seems to be the best stimulus. During thalamic recording experiments [ 351, this kind of stimulation gave the best cell activation. To elicit a long lasting, very painful sensation, trains of several seconds with very high intensity are needed. REFERENCES 1 .Ube-Fessard,

8 9 10 11 12 13 14

15 16 17 18 19

D., Nashold, B., Pollin, B. and Woda, A., Thalamic and mid-brain responses to dental pulp afferent messages in awake cats. In: Pr. of the symposium lo-11 Sept. 1976, J. Physiol. (Paris), in “Neural Mechanisms of Pain”, Smolenice press. Anderson, D.F., Hannam, A.G. and Matthews, B., Sensory mechanisms in mammalian tooth and their supporting structures, Physiol. Rev., 50 (1970) 171-195. Anderson, D.F. and Matthews, B., Osmotic stimulation of human dentine and the distribution of dental pain threshold, Arch. oral Biol., 12 (1967) 417-426. Anderson, K.V. and Pearl, G.S., Conduction velocity in afferent fibers from feline tooth pulp, Exp. Neurol., 43 (1964) 281-283. Xzerad, J. and Woda, A., Tooth pulp projection to the trigeminal complex and jaw opening reflex in the cat, J. Biol. (Buccale), 4 (1976) 109-115. Bernick, S., Difference in nerve distribution between erupted and non erupted human teeth, J. dent. Res., 43 (1964) 406-411. Bessou, P., Gauthier, J. et Pages, B., Mise en evidence de fibres afferentes du Groupe C innervant la pulpe de la canine chez le chat, C.R. Sot. Biol. (Paris), 164 (1970) 1815-1850. Brlnnstrom, M. and .&striim, A., The hydrodynamics of the dentine; its possible relationship to dentinal pain, Int. dent. J., 22 (1972) 219-227. Brookhart, J.M., Livingston, W.K. and Haugen, F., Functional characteristics of afferent fibers from tooth pulp of cat, J. Neurophysiol., 16 (1953) 634-642. Bueltmann, K.W., Karlsson, V.L. and Edie, J., Qualitative ultrastructure of intra-dental nerve fibers in marmosets, Arch. oral Biol., 17 (1972) 545-660. Chatrian, G.E., Farell, D.F., Canfield, R. and Le Hich, E., Congenital insensitivity of noxious stimuli, Arch. Neurol. (Chic.), 32 (1975) 141-145. Chatrian, G.E., Farell, D.F., Canfield, R. and Le Hich, E., Cerebral responses to electrical tooth pulp stimulation in man, Neurology (Minneap.), 25 (1975) 745-757. Graf, W. and Bjorlin, C., Diameters of nerve fibers in human tooth pulps, J. Amer. dent. Ass., 43 (1951) 186. Greenwood, F., Horiuchi, F. and Matthews, B., Electrophysiological evidence on the types of nerve fibers excited by electrical stimulation of teeth with a pulp tester, Arch. oral Biol., 17 (1972) 701-709. Hensel, H. and Mann, G., Pain in human teeth caused by temperature variations and heat conduction, Stoma (Heidelb.), 9 (1956) 76-85. Horiuchi, H., A study of pulp-nerve excitation through a silver wire electrode, J. dent. Res., 44 (19653 1257-1263. Horiuchi, H. and Matthews, B., Evidence on the origin of impulses recorded from dentine in the cat, J. Physiol. (Lond.), 243 (1974) 797-829. Johnsen, D.C. and Karlsson, V.L., Electron microscopic quantitations of feline primary and permanent incisor innervation, Arch. oral Biol., 19 (1974) 671-678. Kerr, D.I.B., Haugen, F.P. and Melzack, R., Responses evoked in the brainstem by tooth stimulation, Amer. J. Physiol., 183 (1955) 253-258.

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Sensation evoked by bipolar intrapulpal stimulation in man.

145 Pain, 1(1977) 115-152 @ ElsevieriNorth-Holland SENSATION IN MAN J. AZERAD (Accepted EVOKED * and Laboratcire (France) Biomedical March B...
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