Journal of

Oral Rehabilitation

Journal of Oral Rehabilitation 2014 41; 875--880

Tactile sensory and pain thresholds in the face and tongue of subjects asymptomatic for oro-facial pain and headache I. OKAYASU*, O. KOMIYAMA†, T. AYUSE* & A. DE LAAT‡

*Department of Clinical Physiology,

Graduate School of Biomedical Sciences, Nagasaki University, Nagasaki, †Department of Oral Function and Rehabilitation, Nihon University School of Dentistry at Matsudo, Matsudo, Japan and ‡Department of Oral Health Sciences, KU Leuven and Dentistry, University Hospital Leuven, Leuven, Belgium

SUMMARY The aim of this study was to examine the tactile sensory and pain thresholds in the face, tongue, hand and finger of subjects asymptomatic for pain. Sixteen healthy volunteers (eight men and eight women, mean age 357 years, range 27– 41) participated. Using Semmes–Weinstein monofilaments, the tactile detection threshold (TDT) and the filament-prick pain detection threshold (FPT) were measured at five sites: on the cheek skin (CS), tongue tip (TT), palm side of the thenar skin (TS), dorsum of the hand (DH) and the finger tip (FT). The difference between the tactile sensory and pain threshold (FPT–TDT) was also calculated. Both for the TDT and FPT, TT and DH had the lowest and highest values, respectively. As for the FPT–TDT, there were no significant differences among the measurement

Introduction The functions of the trigeminal sensory and motor systems are very analogous to those of the hand, particularly in relation to the precise manipulation of objects. This is reflected in the exceptional innervation density of the perioral tissues and the hand (1, 2). The innervation of the face and cheeks resembles that of the hairy skin of the hand and arm, whereas the sensory innervation of the tongue tip resembles that of the finger tips (1, 2). Like the hairy skin of the hand, most mechanoreceptors in the facial skin are slowly adapting with small and well-defined receptive fields. In contrast, most mechanoreceptors terminating superficially in the tongue and the lips have © 2014 John Wiley & Sons Ltd

sites. As the difference between FPT and TDT (FPT–TDT) is known to be an important consideration in interpreting QST (quantitative sensory testing) data and can be altered by neuropathology, taking the FPT–TDT as a new parameter in addition to the TDT and FPT separately would be useful for case–control studies on oro-facial pain patients with trigeminal neuralgia, atypical facial pain/atypical odontalgia and burning mouth syndrome/glossodynia. KEYWORDS: oro-facial pain, sensory threshold, pain threshold, mechanoreceptors, somatosensory function Accepted for publication 21 June 2014

extremely small and well-defined receptive fields and adapt quickly to maintained tissue deformation (1–3). These fast-adapting mechanoreceptors also seem to predominate in the finger tip (1, 2). The tongue tip and finger tips serve to manipulate and explore objects in the mouth and by the hand, respectively. In contrast, mechanoreceptors supplying the skin of the face and back side of the hand serve to signal facial and finger movements (1, 2). Quantitative sensory testing (QST) could improve the diagnostic and therapeutic approaches for orofacial pain conditions (4–8). Oro-facial pain is pain perceived in the face and oral cavity, as for instance in trigeminal neuralgia, atypical facial pain/atypical odontalgia and burning mouth syndrome/glossodynia (9–12). Quantitative sensory testing data for both doi: 10.1111/joor.12213

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I . O K A Y A S U et al. facial skin and tongue could be useful for these orofacial pain conditions. So far, we have examined sensory and pain perception in the masseter muscle and facial skin using Semmes–Weinstein monofilaments (13–15), but we have no data on the tongue. Consequently, the aim of this study was to examine the tactile sensory and pain thresholds in the face and tongue of symptom-free subjects. In addition, we examined thresholds of the hand and finger as control sites for the face and tongue, respectively.

Materials and methods Subjects Sixteen healthy volunteers (eight men, eight women, age range 27–41 years) were recruited from Nagasaki University staff. All were asymptomatic for pain in the head and neck. As a previous study indicated that pain thresholds were lower in the menstrual phase (16, 17), women were not tested during their menstrual phase and smokers were excluded. Informed consent was obtained from all participants. The institutional Ethics committee of Nagasaki University Graduate School of Biomedical Sciences approved the study (No. 1181). The subjects were seated comfortably upright in a dental chair. The tactile detection threshold (TDT) and the filament-prick pain detection threshold (FPT) were measured on the right and left cheek skin (CS), tongue tip (TT), palm side of thenar skin (TS), dorsum of the hand (DH) and the finger tip (FT) of the right hand. The sequence of the measurement sites was randomised. Semmes–Weinstein monofilaments with 20 different diameters were used*. The number of the filaments (165–665) corresponds to a logarithmic function of the equivalent forces of 00045–447 g (18, 19). Each filament size is marked with the resultant force, and these values are used in the descriptive statistics, which enables easier comparison of thresholds as reported previously (13, 14, 20, 21).

procedure and to raise their hand as soon as they felt the stimulus on the test site. The filament was applied vertically to the test site and slowly the pressure was increased until the filament bowed. The time needed to bow the filament was standardised to approximately 15 s. The stimulus was maintained for approximately 15 s and then removed in 15 s. Quick applications and bouncing of the filaments against the skin were avoided. At each site, the test started with the number (No.) 474 filament. If the subject raised his/her hand, this was considered a positive response, and the next filament applied was one step lower (No. 4.56). This procedure was repeated with decreasing filament diameters until the subject no longer felt the pressure. This was considered a negative answer. Again, the filament with a higher pressure was applied. This procedure continued until five positive and five negative peaks were recorded, and the threshold (TDT) was calculated as the average of these values. If the subject still had a positive response while applying the lowest fibre (No. 1.65), this pressure was considered the threshold. Two ‘blank’ (placebo) trials were performed after peaks 5 and 10. During these control trials, the filament did not make contact with the tissue. If the subject reported a positive answer, the test was discontinued and the subject was questioned about what kind of stimulus was perceived. The whole procedure was explained again to the subject and afterwards the test was restarted. Filament-prick pain detection threshold After the TDT measurements, the FPT was examined. The stimuli were applied in the same way as for the TDT, but the subjects were instructed to keep their eyes open and to raise their hand as soon as they felt not only pressure but also pain in the test area. If the subject had no positive response for the thickest fibre (No. 6.65), this value was recorded as the threshold. No placebo stimuli were applied. There was a time lag of 3 min between the measurements on a same site to avoid sensitisation.

Tactile detection threshold At first, TDT was examined. The subjects were instructed to close their eyes during the whole test

*Premier Products, Kent, WA, USA.

Statistical analysis The mean values and standard error of the mean of TDT and FPT were calculated. The difference between the tactile sensory and pain threshold (FPT–TDT) was also calculated. The differences in mean threshold © 2014 John Wiley & Sons Ltd

TACTILE SENSORY AND PAIN THRESHOLDS values between various sites were analysed using Wilcoxon–Mann–Whitney test. The significance was accepted at P < 005. As there were no side differences between left CS and right CS regarding TDT, FPT and the FPT–TDT, we selected the right CS as a single value for the CS.

Results Depending on the test area, the TDT ranged from 208  014 to 339  044. The TDT was lowest at the TT (208  014), followed by the CS (268  043), the FT (290  044) and the TS (300  029), while the TDT at the DH (339  044) was highest (Table 1). The TT had a significantly lower threshold compared with the other test sites (P < 005), and the DH had a significantly higher threshold compared with the other test sites (P < 005) (Fig. 1). The FPT ranged from 509  031 to 629  031. The FPT was lowest at the TT (509  031), followed by the CS (581  053), the FT (596  027) and the TS (611  044), while the FPT at the DH (629  031) was highest (Table 1). Also for FPT, the TT had a significantly lower threshold compared with the other test sites (P < 005), and the DH had a significantly higher threshold compared with the CS, TT and FT (P < 005) (Fig. 2). The FPT–TDT ranged from 289  059 to 314  049 (Table 2). The FPT was significantly higher than the TDT but there were no significant differences in the FPT–TDT among the measurement sites (Fig. 3).

Discussion Recently, we used Semmes–Weinstein monofilaments to measure tactile sensory and pain thresholds in the oro-facial region of symptom-free men and women and of patients with myofascial pain of the jaw

muscles (13, 14). We reported that in symptom-free subjects, not only sensitivity to pain but also habituation of sensory perception was higher in women than men (13). Furthermore, our case–control study clarified that sensitivity to pain was more pronounced in patients with temporomandibular disorders (TMD) (14). Next to TMD, trigeminal neuralgia, atypical facial pain/atypical odontalgia and burning mouth syndrome/glossodynia are less common oro-facial pain conditions (22–28). No diagnostic tests have sufficient specificity and sensitivity for trigeminal neuralgia; so, its diagnosis remains largely based on clinical history, signs and symptoms (29). Atypical facial pain/ atypical odontalgia and burning mouth syndrome/ glossodynia are chronic oro-facial pain conditions that have less clear diagnostic signs than trigeminal neuralgia and are even more problematic in their management (29). Consequently, QST data for both facial skin and tongue could be useful for the assessment and diagnosis of these oro-facial pain in clinical practice. In the present study, we evaluated the tactile sensory and pain thresholds at multiple measuring points in the oro-facial region and corresponding control sites of symptom-free subjects. The most common intra-individual reference when testing with von Frey filaments is provided by stimulation at the corresponding contralateral and supposedly unaffected location (30). We selected the hand and finger as the extra-oral corresponding control site of face and tongue, respectively, as the characteristics in mechanoreceptors and functional property of face and tongue are similar to those of hand and finger (1–3). First, we compared the TDT at five different sites: CS, TT, TS, DH and FT. The TDT was lowest at the TT, followed by the CS, the FT and the TS, while the TDT at the DH was highest. Rath and Essick (31) examined spatial variations in the two-point discrimination threshold as well as TDT. According

Table 1. Descriptive data of the tactile detection threshold (TDT) and the filamentprick pain detection threshold (FPT)

TDT FPT

CS

TT

TS

DH

FT

268  043 581  053

208  014 509  031

300  029 611  044

339  044 629  031

290  044 596  027

Data are expressed as mean values  standard error of the mean. CS, cheek skin; TT, tongue tip; TS, palm side of the thenar skin; DH, dorsum of the hand; FT, finger tip. © 2014 John Wiley & Sons Ltd

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Fig. 1. Figure shows the mean values and standard error of the mean of tactile detection threshold (TDT). The TDT was measured at five sites: on the cheek skin (CS), tongue tip (TT), palm side of the thenar skin (TS), dorsum of the hand (DH) and the finger tip (FT). *P < 005, showing a significant difference between sites.

Fig. 2. Figure shows the mean values and standard error of the mean of filament-prick pain detection threshold (FPT). The FPT was measured at five sites: on the cheek skin (CS), tongue tip (TT), palm side of the thenar skin (TS), dorsum of the hand (DH) and the finger tip (FT). *P < 005, showing a significant difference between sites.

to their study (31), the tongue tip is the most tactually sensitive area of the body with the testing of two-point discrimination (1 mm) followed by the

lips and the finger tip (2–3 mm). On the other hand, the perinasal skin is the most tactually sensitive area of the body with TDT as low as 5-milligram (mg) weight (wgt). For comparison, the minimal mechanical stimuli that can be detected on the finger tip are 40- to 100-mg wgt. In either case, the tactile sensitivity of the oro-facial tissues is as high, or higher, than other areas of the body. This can be attributed to both 1) the high density of mechanoreceptors with small and well-defined receptive fields and 2) the high compliance of most oro-facial soft tissues by which even low forces produce deformation and strain of the specialised nerve endings of the mechanoreceptors (1, 2). Second, we also compared the FPT at five different sites: CS, TT, TS, DH and FT. The FPT was lowest at the TT, followed by the CS, the FT and the TS, while the FPT at the DH was highest. These data are consistent with those of a previous study by Mashu et al. (32): the most sensitive area to mechanical pain stimuli is the tongue tip followed by the facial skin, the finger tip and the hand skin. This might be explained by the exceptional innervation density of the orofacial region, and its large areas of sensory and motor cortex that process the sensory information and control the motor activities of these vital areas of the body (1, 2). In addition, another reason why the orofacial region is more sensitive to tactile sensory and pain stimuli than other areas of the body might be the presence or absence of the visual perception: we can observe and see our body by ourselves but not the oro-facial region. So, the sensitivity of the orofacial region might be enhanced as compensation for lack of visual perception. Our data indicated that sensitivity to tactile sensory and pain (TDT, FPT) at the FT was not significantly different from that at the CS. We speculated that the sensitivity of the finger might show some similarity of somatosensory characteristics in the tongue, which is the most sensitive area in the oro-facial region, from

Table 2. Descriptive data of the difference between the tactile detection threshold and the filament-prick pain detection threshold (FPT–TDT)

FPT–TDT

CS

TT

TS

DH

FT

314  049

301  035

311  051

289  059

307  060

Data are expressed as mean values  standard error of the mean. CS, cheek skin; TT, tongue tip; TS, palm side of the thenar skin; DH, dorsum of the hand; FT, finger tip. © 2014 John Wiley & Sons Ltd

TACTILE SENSORY AND PAIN THRESHOLDS control subjects and patients with trigeminal neuralgia, atypical facial pain/atypical odontalgia and burning mouth syndrome/glossodynia could establish more objective diagnostic criteria for these oro-facial pain conditions instead of traditional techniques like electromyography of jaw reflexes (33–37).

Ethical approval

Fig. 3. Figure shows the mean values and standard error of the mean of the difference between the tactile detection threshold and filament-prick pain detection threshold (FPT–TDT). The FPT–TDT was measured at five sites: on the cheek skin (CS), tongue tip (TT), palm side of the thenar skin (TS), dorsum of the hand (DH) and the finger tip (FT).

several aspects: most mechanoreceptors in the tongue are fast-adapting as well as those in the finger (1, 2), and from the viewpoint of functional movements, the tongue and finger serve to manipulate and explore objects in the mouth and by the hand, respectively (1, 2). We speculated that these common points in somatosensory and motor functions between the finger and tongue would reflect in the sensitivity of the FT found in this study. Third, we measured and compared the value of FPT–TDT at five different sites: CS, TT, TS, DH and FT. Although there were no significant differences among the measurement sites, the difference between the sensory and pain threshold (FPT–TDT) is known to be an important consideration in interpreting QST data and can be altered by neuropathology (8, 14). BaadHansen et al. (8) examined intra-oral QST in atypical odontalgia patients using healthy subjects at reference. According to this study (8), compared with control subjects, atypical odontalgia patients had lower FPT and higher TDT. The fact that TDT is higher in the patients than in the normal subjects is in good agreement with our previous case–control study with TMD (14). So, it might be argued that taking the FPT–TDT as a new parameter in addition to the TDT and FPT separately would be useful for case–control studies on oro-facial pain patients. Studying the somatosensory function in the trigeminal region might contribute to a better understanding of the aetiology and improve diagnosis and management of oro-facial pain and dysfunction (13–21). In particular, case–control studies using QST between © 2014 John Wiley & Sons Ltd

The institutional ethics committee of Nagasaki University Graduate School of Biomedical Sciences approved the study (No. 1181).

Funding This study was supported by a Subsidy for dentistry research General Foundation Hojin-kai for 2012.

Competing interests None.

References 1. Trulsson M, Essick GK. Mechanosensation. In: Miles TS, Nauntofte B, Svensson P, eds. Clinical oral physiology. Copenhagen: Quintessence; 2004:165–198. 2. Morimoto T, Yamada Y, eds. Basic physiology for dental students, 5th ed. Tokyo: Ishiyaku; 2008. 3. Johansson RS, Trulsson M, Olsson KA, Westberg K-G. Mechanoreceptor activity from the human face and oral mucosa. Exp Brain Res. 1988;72:204–208. 4. Svensson P, Baad-Hansen L, Thygesen T, Juhl GI, Jensen TS. Overview on tools and methods to assess neuropathic trigeminal pain. J Orofac Pain. 2004;18:332–338. 5. Eliav E, Gracely RH, Nahlieli O, Benoliel R. Quantitative sensory testing in trigeminal nerve damage assessment. J Orofac Pain. 2004;18:339–344. 6. Pigg M, Baad-Hansen L, Svensson P, Drangsholt M, List T. Reliability of intraoral quantitative sensory testing (QST). Pain. 2010;148:220–226. 7. Baad-Hansen L, Arima T, Arendt-Nielsen L, Neumann-Jensen B, Svensson P. Quantitative sensory tests before and 11/2 years after orthognathic surgery: a cross-sectional study. J Oral Rehabil. 2010;37:313–321. 8. Baad-Hansen L, Pigg M, Ivanovic SE, Faris H, List T, Drangsholt M et al. Intraoral somatosensory abnormalities in patients with atypical odontalgia-a controlled multicenter quantitative sensory testing study. Pain. 2013;154:1287– 1294. 9. Okayasu I, Oi K. Case report of orofacial pain-Burning mouth syndrome and neuropathic pain. J Jpn Soc Stomatognath Funct. 2012;18:204–205.

879

880

I . O K A Y A S U et al. 10. Okayasu I, Oi K. Case report of orofacial pain 2-Atypical facial pain and migraine. J Jpn Soc Stomatognath Funct. 2012;19:52–53. 11. Okayasu I, Ayuse T, Oi K. Case report of orofacial pain 3Cracked tooth syndrome (CTS) and atypical odontalgia (AO). J Jpn Soc Stomatognath Funct. 2013;19:196–197. 12. Okayasu I, Ayuse T. Case report of orofacial pain 4-Glossodynia. J Jpn Soc Stomatognath Funct. 2013;20:48–49. 13. Okayasu I, Oi K, De Laat A. The effect of tooth clenching on the sensory and pain perception in the oro-facial region of symptom-free men and women. J Oral Rehabil. 2009;36:476–482. 14. Okayasu I, Oi K, De Laat A. The effect of nonfunctional tooth contact on sensory and pain perception in patient with myofascial pain of the jaw muscles. J Prosthodont Res. 2012;56:87–92. 15. Okayasu I, Komiyama O, Yoshida N, Oi K, De Laat A. Effects of chewing efforts on sensory and pain thresholds in human facial skin: a pilot study. Arch Oral Biol. 2012;57:1251–1255. 16. Isselee H, De Laat A, Bogaerts K, Lysens R. Long-term fluctuations of pressure pain thresholds in healthy men, normally menstruating women and oral contraceptive users. Eur J Pain. 2001;5:27–37. 17. Isselee H, De Laat A, De Mot B, Lysens R. Pressure-pain threshold variation in temporomandibular disorder myalgia over the course of the menstrual cycle. J Orofac Pain. 2002;16:105–117. 18. Jacobs R, Wu C-H, van Loven K, Desnyder M, Kolenaar B, van Steenberghe D. Methodology of oral sensory tests. J Oral Rehabil. 2002;29:720–730. 19. Michelotti A, Farella M, Stellato A, Martina R, De Laat A. Tactile and pain thresholds in patients with myofascial pain of the jaw muscles: a case–control study. J Orofac Pain. 2008;22:139–145. 20. Komiyama O, De Laat A. Tactile and pain thresholds in the intra- and extra-oral regions of symptom-free subjects. Pain. 2005;115:308–315. 21. Komiyama O, Gracely RH, Kawara M, De Laat A. Intraoral measurement of tactile and filament-prick pain threshold using shortened Semmes-Weinstein monofilaments. Clin J Pain. 2008;24:16–21. 22. Lewis M, Sankar V, De Laat A, Benoliel R. Management of neuropathic orofacial pain. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2007;103(Suppl 1):S32.e1–S32.e24. 23. Patton LL, Siegel MA, Benoliel R, De Laat A. Management of burning mouth syndrome: systematic review and management recommendations. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2007;103(Suppl 1):S39.e1–S39.e13. 24. Baad-Hansen L. Atypical odontalgia: pathophysiology and clinical management. J Oral Rehabil. 2008;35:1–11.

25. Zakrzewska JM. Trigeminal neuropathic pain. In: Mogil J, ed. Pain 2010: an updated review, Refresher course syllabus. Seattle: IASP Press; 2010:137–146. 26. De Laat A. Pain associated with temporomandibular disorders. In: Tracey I, ed. Pain 2012: refresher courses. 14th World Congress on Pain. Seattle: IASP Press; 2012:251–256. 27. Komiyama O, Obara R, Uchida T, Nishimura H, Iida T, Okubo M et al. Pain intensity and psychosocial characteristics of patients with burning mouth syndrome and trigeminal neuralgia. J Oral Sci. 2012;54:321–327. 28. Komiyama O, Nishimura H, Makiyama Y, Iida T, Obara R, Shinoda M et al. Group cognitive-behavioral intervention for patients with burning mouth syndrome. J Oral Sci. 2013;55:17–22. 29. Sessle BJ. Orofacial pain. In: Merskey H, Loeser JD, Dubner R, eds. The paths of pain 1975–2005. Seattle: IASP Press; 2005:131–150. 30. Lindblom U. Sensory quantification and pain. In: Merskey H, Loeser JD, Dubner R, eds. The paths of pain 1975–2005. Seattle: IASP Press; 2005:253–270. 31. Rath EM, Essick GK. Perioral somesthetic sensibility: do the skin of the lower face and the midface exhibit comparable sensitivity? J Oral Maxillofac Surg. 1990;48:1181– 1190. 32. Mashu S, Shibaji T, Zeredo JL, Toda K, Suzuki N. Comparison of mechanical pain thresholds among various orofacial areas in human. Pain Res. 2004;19:123–131. 33. Yamada Y, Ash MM. An electromyographic study of jaw opening and closing reflexes in man. Arch Oral Biol. 1982;27:13–19. 34. Yamada Y, Stohler CS, Shimada K, Ash MM. Short and long latency jaw-opening reflex responses elicited by mechanical stimulation in man. Arch Oral Biol. 1985;30:197–200. 35. Yamada Y, Haraguchi N, Oi K, Ash MM. Human jaw-opening muscle responses elicited by multiple-site electrical stimulation. J Oral Rehabil. 1990;17:15–23. 36. van Steenberghe D, van der Glas HW, De Laat A, Weytjens J, Carels C, Bonte B. The masseteric poststimulus EMG complex (PSEC) in man: methodology, underlying reflexes and clinical perspectives. In: van Steenberghe D, De Laat A, eds. Electromyography of jaw reflexes in man. Leuven: University Press; 1989:269–288. 37. De Laat A, Svensson P, Macaluso GM. Are jaw and facial reflexes modulated during clinical and experimental orofacial pain? J Orofac Pain. 1998;12:260–271. Correspondence: Ichiro Okayasu, Department of Clinical Physiology, Graduate School of Biomedical Sciences, Nagasaki University, 1-7-1 Sakamoto, Nagasaki 852-8588, Japan. E-mail: [email protected]

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Tactile sensory and pain thresholds in the face and tongue of subjects asymptomatic for oro-facial pain and headache.

The aim of this study was to examine the tactile sensory and pain thresholds in the face, tongue, hand and finger of subjects asymptomatic for pain. S...
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