Measuring vibration threshold with a graduated tuning fork in normal aging and in patients with polyneuropathy
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Downloaded from http://jnnp.bmj.com/ on March 17, 2015 - Published by group.bmj.com J Neurol Neurosurg Psychiatry 1998;65:743–747 743 Measuring vibration threshold with a graduated tuning fork in normal aging and in patients with polyneuropathy I S J Martina, R van Koningsveld, P I M Schmitz, F G A van der Meché, P A van Doorn, for the European Inflammatory Neuropathy Cause and Treatment (INCAT) group Abstract devices have been developed, such as the Objective—To provide clinically useful Biothesiometer, the Optacon, and the compu- vibration threshold normal values. ter assisted sensory examination.3–5 Although Methods—The graduated Rydel-SeiVer these instruments are useful in experimental tuning fork was evaluated in 198 healthy studies, they are of little use in daily practice. controls and 59 patients with a polyneu- The size of the apparatus, the duration of ropathy. The measures were done in trip- examination, the demand on patients’ coopera- licate at four locations: the distal tion, and their cost are in sharp contrast with interphalangeal joint of the index finger, the needs of a simple and valid instrument for ulnar styloid process, interphalangeal use in routine neurological investigation. With joint of the hallux, and internal malleolus. the introduction of the 64 Hz graduated tuning The values obtained with this tuning fork fork by Rydel and SeiVer (Martin, Tuttlingen, in healthy controls and patients with Germany) in 1903 it seemed as if all the needs polyneuropathy were compared with the were fulfilled in providing an instrument which values of an electronic device, the Vi- was easy to apply, inexpensive, and reliable for brameter. quantifying impairment of vibration sense.6 Results—Vibration sense was better per- However, this tool has been largely neglected ceived in the arms compared with the legs. by neurologists and thus far, only a few papers There was a significant age related decline have reported on its use.7–14 Clinically useful of vibration sense at all locations. The normal values for vibration sense using this values from the Rydel-SeiVer tuning fork tuning fork were provided by one study only.7 and the Vibrameter were significantly These values were obtained by examining 73 correlated in both groups. The sensitivity healthy controls only at the hallux, which ham- of these two instruments for the four sites pers their general applicability. Other studies examined in the polyneuropathy group acquired their own normal vibration values, ranged from 29–76% and 31–73%, respec- but unfortunately from only a few healthy tively and was the highest at the hallux for controls.8 11 No study has provided normal both instruments. values for the arms. The primary aim of this Department of Conclusion—This study provides clinical study was to obtain specific normal vibration Neurology, University useful normal values of vibration thres- threshold values for the Rydel-SeiVer tuning Hospital Rotterdam, fork at four examination sites in a large number dr Molewaterplein 40, hold for the Rydel-SeiVer tuning fork. 3015 GD, Rotterdam, This is a simple and easily applicable of healthy controls. In addition, the values The Netherlands instrument that assesses vibration sense achieved using the device in healthy controls I S J Martina semiquantitatively and should therefore and in patients with a polyneuropathy were R van Koningsveld have a place in routine neurological compared with those obtained with an elec- F G A van der Meché examination. tronic device, the Vibrameter.15 P A van Doorn (J Neurol Neurosurg Psychiatry 1998;65:743–747) Department of Statistics, Daniel den Keywords: vibration sense; graduated tuning fork; aging Participants and methods Hoed Cancer Centre, HEALTHY CONTROLS University Hospital Healthy controls were recruited from hospital Rotterdam, Groene Abnormalities in sensory qualities are frequent personnel, companions (relatives, friends) of Hilledijk 301, 3075 EA, complaints of patients with peripheral neu- patients visiting our outpatient clinic, and from Rotterdam, The ropathies. Impairment of vibration sense, espe- homes for elderly people. Two hundred and Netherlands P I M Schmitz cially starting distally in the limbs, may be a fourteen potential controls were interviewed sign of peripheral nerve dysfunction.1 Tra- and examined. Those with sensory symptoms, Correspondence to: ditionally, a non-graduated tuning fork, which sensory signs including absent vibration sense, Dr ISJ Martina, Department was invented in 1711 and introduced by a history of alcohol misuse, using drugs which of Neurology, University Hospital Rotterdam, Dr Bonnafont as a diagnostic test in general medi- may cause a polyneuropathy or influence their Molewaterplein 40, 3015 cine, is used for the evaluation of the vibration cooperation, and those with a disease which GD Rotterdam, The sense.2 This simple instrument measures the might induce a polyneuropathy, were excluded Netherlands. Telephone 0031 10 4639222; fax 0031 presence or absence of vibration, but unfortu- from the study. The selected participants had a 10 4633208. nately does not quantitatively provide the lucid consciousness and their history did not degree of dysfunction of vibration sense. It is of show any mental or psychological illness. Received 2 December 1997 clinical importance that the vibration sense Standard neurological examination was per- and in revised form 1 April 1998 should be measured quantitatively and consist- formed with special interest in the sensory Accepted 6 April 1998 ently. For this purpose several electronic qualities. Six age groups (
Downloaded from http://jnnp.bmj.com/ on March 17, 2015 - Published by group.bmj.com 744 Martina, van Koningsveld, Schmitz, et al of about 35 participants. Sixteen subjects (nine 8 8 men; seven women; mean age 81 (SD 8.5) years; range 65–93 years) were excluded from 7 analysis, based on absent vibration perception 6 6 in at least one region tested. Eight had an absent vibration sense at the hallux and the internal malleolus, seven only at the hallux, and 4 4 4 one only at the internal malleolus. Nine subjects had absent and four decreased (−3/ −3) ankle jerks. The ankle reflexes were normal 2 2 in the remaining three patients. These patients were considered to have subclinical disease. The problem of the selection of participants for 0 0 normal vibration threshold values is discussed later. A B C D E F PATIENTS WITH POLYNEUROPATHY Figure 1 Extremities of the graduated tuning fork at rest (A) and during vibration (B→F). Intersection between lower and upper triangles moves from 0 (minimum score) to 8 Fifty nine ambulatory patients from our outpa- (maximum score) with decreasing vibration amplitude (↔). tient clinic (31 men; 28 women; mean age 56.8 (SD 15.9) years; range 14–87 years) with a 8.0 clinical and electrophysiologically supported polyneuropathy were enrolled in this study. 7.0 They were stratified into age group, as I described above, and sex. Each age group con- 6.0 sisted of about 10 participants. These patients II had a mild polyneuropathy with limited Tuning fork values 5.0 sensory disturbances and walking problems. The aetiologies of the polyneuropathies were 4.0 diabetes mellitus (11 cases), hereditary motor sensory neuropathy type I (five cases), and type 3.0 II (two cases), systemic disease (three cases), amyloidosis (three cases), drug induced (two 2.0 cases), thyroid dysfunction (one case) and vita- I Mean min B12 deficiency (one case). Fourteen 1.0 II 5% Lower limit patients had a chronic idiopathic axonal polyneuropathy. In 17 cases no cause was 0.0 determined. 10 20 30 40 50 60 70 80 90 100 Age (y) ASSESSMENT TOOLS Figure 2 Vibration threshold values obtained by the Rydel-SeiVer tuning fork at the index The Rydel-SeiVer tuning fork is a graduated finger. Residual standard deviation (SDres = residual standard deviation around the mean fork which determines the ability of subjects to regression line)=0.62. y mean=7.69−0.01 × age; y 5%=6.67−0.01 × age. discriminate various vibration intensities. The 8.0 two arms of this tuning fork bear calibrated weights at their extremities (fig 1).6 8 A triangle 7.0 and an arbitrary scale from 0 (minimum score) I to 8 (maximum score) imprinted on the 6.0 weights allow assessment of vibration thresh- II old. Once the arms are swinging, the fork Tuning fork values 5.0 vibrates at 64 Hz and the triangles on the weights appear double. The intersection of 4.0 these two virtual triangles moves from 0 to 8 in an exponential way with decreasing vibration 3.0 amplitude of the arms. The vibration extinc- tion threshold is considered as the nearest 2.0 value to the apparent point of intersection of the virtual triangles when the subject indicates I Mean that vibration is no longer perceived. The 1.0 II 5% Lower limit Vibrameter (Somedic, Stockholm, Sweden, 0.0 Type III) is a device which determines 10 20 30 40 50 60 70 80 90 100 vibration sense electronically. It has been Age (y) extensively described by Goldberg and Lindb- lom and consists essentially of a hand held Figure 3 Vibration threshold values obtained by the Rydel-SeiVer tuning fork at the ulnar vibrating probe which vibrates at 100 Hz.15 The styloid process. Residual standard deviation (SDres = residual standard deviation around the mean regression line)=0.55. y mean=7.60−0.0079 × age; y 5%=6.68−0.0079 × age. vibration amplitude of this probe increases from zero to a maximum of 399.9 µm. 60–69, 70–79, >80 years) were formed. One hundred and ninety eight healthy controls (93 TEST PROCEDURES men; 105 women; mean age 55.1 (SD 18.0) All participants gave informed consent before years; range 19–93 years) stratified for sex were the study. All measurements were performed enrolled in this study. Each age group consisted by one investigator (RvK) and the vast majority
Downloaded from http://jnnp.bmj.com/ on March 17, 2015 - Published by group.bmj.com Measuring vibration threshold with a graduated tuning fork 745 8.0 women; total n=100), and all patients with polyneuropathy. Vibration threshold was 7.0 measured according to the method of limits.15 The subjects were asked to indicate when the 6.0 vibration stimulus was felt for the first time (perception threshold) and when this stimulus Tuning fork values 5.0 I disappeared again (disappearance threshold). The average of these three paired measure- 4.0 ments was considered the vibration threshold at the location investigated. The Vibrameter II 3.0 was applied resting on its own weight and its equilibration was electronically controlled. 2.0 Each cycle of measurement included catch I Mean trials with a resting probe. 1.0 II 5% Lower limit STATISTICS 0.0 Vibration threshold reference values for the 10 20 30 40 50 60 70 80 90 100 Rydel-SeiVer tuning fork were calculated for Age (y) the four sites examined, depending on age and Figure 4 Vibration threshold values obtained by the Rydel-SeiVer tuning fork at the sex, using linear and quadratic regression hallux. Residual standard deviation (SDres = residual standard deviation around the analysis at a chosen specificity of 95%. The 5% mean regression line)=0.99. y mean=7.38−0.026 × age; y 5%=5.75−0.026 × age. lower limits for the Rydel-SeiVer tuning fork were estimated for each site of examination as 8.0 the mean−1.65*Sres. The mean was defined as the mean vibration threshold for a certain age 7.0 (and sex) and Sres was considered the residual 6.0 standard deviation around the regression line. Tuning fork values The 95th percentile vibration threshold values Ia 5.0 for the Vibrameter were also calculated. The Ib obtained limits were estimated and further 4.0 used to determine new specificities and sensi- IIa 3.0 tivities for both instruments. A vibration sense IIb was considered to be abnormal if the corre- I Mean sponding value was below the 5% lower limit 2.0 II 5% Lower limit when examined with the tuning fork or above a Female 1.0 the 95th percentile vibration value when investi- b Male gated with the Vibrameter at the same site of 0.0 examination. The correlation between the two 10 20 30 40 50 60 70 80 90 100 instruments was analysed by Spearman’s rank Age correlation test. All analyses were performed Figure 5 Vibration threshold values obtained by the Rydel-SeiVer tuning fork at the using Stata 5.0 for Windows 95 (Stata Statisti- internal malleolus. Residual standard deviation (SDres = residual standard deviation cal Software: Release 5.0. 702 University Drive around the mean regression line)=0.89; sex = 1 (male); sex = 0 (female). y East, College station, TX: Stata Corporation mean=6.80−0.51 × sex−0.0002 × age × age; y 5% (female)=5.33−0.0002 × age × age; y 5% (male)=4.82−0.0002 × age × age. 1997). A p value
Downloaded from http://jnnp.bmj.com/ on March 17, 2015 - Published by group.bmj.com 746 Martina, van Koningsveld, Schmitz, et al Table 1 Normal vibration threshold values (5% lower cificity of 80% and a sensitivity of 83%. The limit) in healthy controls (with the Rydel-SeiVer tuning specificity and sensitivity for the Vibrameter fork) were 86% and 78%, respectively. The corre- For the upper extremities For the lower extremities sponding specificity and sensitivity when at least two sites investigated showed an abnormal Age (y) Values Age (y) Values vibration sense was 94% and 63% for the tun- 6.5 4.5 ing fork, and 98% and 61% for the Vibrameter. 41–85 >6.0 41–60 >4.0 >85 >5.5 61–85 >3.5 >85 >3.0 Discussion Sites of examination: dorsum of the distal interphalangeal joint The present study provides clinical useful nor- of the index finger, the ulnar styloid process, dorsum of the interphalangeal joint of the hallux ,and the internal malleolus. mal values for the vibration sense using the Values are 0–8; the vibration threshold values are presented in graduated Rydel-SeiVer tuning fork at four rounded numbers. sites of examination. These normal values are diVerent from those provided by the literature. tion sense were better in the arms than in the Claus et al stated that subjects up to 40 years legs. In addition, there was a significant should score at least 6/8 and those older than (p
Downloaded from http://jnnp.bmj.com/ on March 17, 2015 - Published by group.bmj.com Measuring vibration threshold with a graduated tuning fork 747 distal regions, possibly due to a metabolic this tuning fork. We propose to incorporate this abnormality leading to failure of axonal pocket sized instrument in the routine neuro- transport and subsequent degeneration.27 logical examination. The sensitivity of the Rydel-SeiVer tuning fork for patients with a polyneuropathy is We thank professor KV Toyka for advising us to use the gradu- highly dependent on the selection of patients. ated Rydel-SeiVer tuning fork in the INCAT studies. This study In patients with predominantly motor signs was part of the Biomed-project number BMH4-CT96 0324. and those with only small size myelinated/ unmyelinated nerve disturbances it might be 1 Schaumburg HH, Berger AR, Thomas PK. Anatomical expected that the sensitivity for detecting classification of peripheral nervous system disorders. In: Disorders of peripheral nerves, 2nd ed. Philadelphia: FA Davis, vibration sense abnormalities using this tuning 1992:10–24. fork will be low. The vast majority of the 2 Bickerton RC, Barr GS. The origin of the tuning fork. J R Soc Med 1987;80:771–3. patients with a polyneuropathy in the present 3 Bloom S, Till S, Sönksen P, et al. Use of a biothesiometer to study had limited sensory disturbances and measure individual vibration thresholds and their variation in 519 non-diabetic subjects. BMJ 1984;288:1793–5. hardly ambulatory problems. These findings 4 Arezzo TC, Schaumburg HH. The use of the Optacon as a might explain the low sensitivity that was found screening device. J Occup Med 1980;22:461–4. 5 Dyck PJ, Karnes J, O’Brien PC, et al. Detection thresholds at the sites examined in the arms and the of cutaneous sense in humans. In: Dyck PJ, Thomas PK, somewhat higher sensitivity for the two loca- GriYn JW, et al, eds. Peripheral neuropathy, 3rd ed. Philadelphia: WB Saunders, 1993:706–28. tions investigated in the legs. 6 Rydel A, SeiVer W. Untersuchungen über das vibrationsge- The vibration threshold values obtained with fühl oder die sog. “Knochensensibilität” (Pallästhesie). Archiv für Psychiatrie und Nervenkrankenheiten 1903;37: the Rydel-SeiVer tuning fork showed a signifi- 488–536. cant correlation with those of the Vibrameter. 7 Claus D, Carvalho VP, Neundörfer B, et al. Zur unterzuc- hung des vibrationsempfindens. Nervenarzt 1988;59:138– This correlation was, however, moderate and 42. was probably due to an increasing variability 8 Thivolet C, El Farkh J, Petiot A, et al. Measuring vibration sense with graduated tuning fork. Diabetes Care 1990;13: between the values obtained with the Vibram- 1077–80. eter in participants 50 years and older. A con- 9 Liniger C, Albeanu A, Bloise D, et al. The tuning fork revis- ited. Diab Med 1990;7:859–64. siderable variability when applying the Vibram- 10 Crausaz FM, Clavel S, Liniger C, et al. Additional factors eter in elderly people has also been reported associated with plantar ulcers in diabetic neuropathy. Dia- bet Med 1988;5:771–5. earlier.15 23 28 A significant correlation between 11 Bergin PS, Bronstein AM, Murray NMF, et al. Body sway these two instruments has been shown by and vibration perception thresholds in normal aging and in others.9–11 Hotta et al found a good correlation patients with polyneuropathy. J Neurol Neurosurg Psychiatry 1995;58:335–40. between a variant of the graduated Rydel- 12 Hilz MJ, Claus D, Rösl G, et al. Besserung des temperatur- SeiVer tuning fork and the Vibrameter and und vibrationsempfindens bei chronischer urämie nach einzeldialyse. Fortschr Neurol Psychiatr 1995;63:264–9. stated that the tuning fork provided objective 13 Hilz MJ, Zimmerman P, Rösl G, et al. Vibrameter testing and reliable measurements of vibration sense.14 facilitates the diagnosis of uremic and alcoholic polyneu- ropathy. Acta Neurol Scand 1995;92:486–90. The pocket sized Rydel-SeiVer tuning fork 14 Hotta N, Sugimura K, Tsuchida I, et al. Use of the C64 detected slightly more abnormalities in the quantitative tuning fork and the eVect of niceritrol in diabetic neuropathy. Clin Ther 1994;16:1007–15. selected group of patients with a polyneuropa- 15 Goldberg JM, Lindblom U. Standardised method of thy than the Vibrameter. The present study determining vibratory perception thresholds for diagnosing and screening in neurological investigation. J Neurol Neuro- also shows that the Rydel-SeiVer tuning fork is surg Psychiatry 1979;42:793–803. easily applicable, does not require long periods 16 Pearson GHJ. EVect of age on vibratory sensibility. Arch Neurol Psychiatry 1928;20:482–96. of attention, and measures vibration sense 17 De Michele G, Filla A, Coppola N, Bisogno A, et al. Influ- quicker than the Vibrameter. ence of age, gender, height and education on vibration sense. A study by tuning fork in 192 normal subjects. J The clinical relevance of a screening test Neurol Sci 1991;105:155–8. depends not only on its simplicity and validity, 18 Wiles PG, Pearce SM, Rice PJS, et al. Vibration perception threshold: Influence of age, height, sex, and smoking, and but also on its reliability and sensitivity to reg- calculation of accurate centile values. Diabet Med 1991;8: ister clinically relevant information. Long term 157–61. 19 Merchut MP, Toleikis SC. Aging and quantitative sensory follow up of patients with a polyneuropathy will thresholds. Electromyogr Clin Neurophysiol 1990;30:293–7. determine the sensitivity of the Rydel-SeiVer 20 Critchley M. The neurology of old age. Lancet 1931;i:1221– 30. tuning fork to changes in time and will indicate 21 Kokmen E, Bossemeyer Jr RW, Barney J, et al. Neurological whether clinical improvement correlates with manifestations of aging. J Gerontol 1977;32:411–9. 22 Steinberg FU, Graber AL. The eVect of age and peripheral improvement in vibration sense. This is cur- circulation on the perception of vibration. Arch Phys Med rently being evaluated more extensively in a Rehabil 1963;44:645–50. 23 Thomson FJ, Masson EA, Boulton AJM. The clinical diag- group of patients with immune mediated nosis of sensory neuropathy in elderly people. Diabet Med polyneuropathy with various degrees of sever- 1993;10:843–6. 24 Knox CA. Neuroanatomical changes associated with aging ity. Its interobserver and intraobserver reliabil- in the peripheral nervous system. In: Albert ML, Knoefel ity and sensitivity to register changes in time JE, eds. Clinical neurology of aging, 2nd ed. New York: Oxford University Press, 1994:68–78. are under investigation. 25 Howell TH. Senile deterioration of the central nervous In conclusion, our findings indicate that the system: a clinical study. BMJ 1949;1:56–8. 26 Thomas PK. Late life neuropathy: an overview. New Iss Rydel-SeiVer tuning fork is a simple instru- Neurosci 1988;1:85–94. ment which rapidly measures vibration sense in 27 GriYn JW, Watson DF. Axonal transport in neurological disease. Ann Neurol 1988;23:3–13. a semiquantitative way. Clinically useful vibra- 28 Fagius J, Wahren LK. Variability of sensory threshold deter- tion threshold normal values are provided for mination in clinical use. J Neurol Sci 1981;51:11–27.
Downloaded from http://jnnp.bmj.com/ on March 17, 2015 - Published by group.bmj.com Measuring vibration threshold with a graduated tuning fork in normal aging and in patients with polyneuropathy I S J Martina, R van Koningsveld, P I M Schmitz, F G A van der Meché and P A van Doorn J Neurol Neurosurg Psychiatry 1998 65: 743-747 doi: 10.1136/jnnp.65.5.743 Updated information and services can be found at: http://jnnp.bmj.com/content/65/5/743 These include: References This article cites 22 articles, 6 of which you can access for free at: http://jnnp.bmj.com/content/65/5/743#BIBL Email alerting Receive free email alerts when new articles cite this article. Sign up in the service box at the top right corner of the online article. Topic Articles on similar topics can be found in the following collections Collections Neuromuscular disease (1200) Peripheral nerve disease (599) Notes To request permissions go to: http://group.bmj.com/group/rights-licensing/permissions To order reprints go to: http://journals.bmj.com/cgi/reprintform To subscribe to BMJ go to: http://group.bmj.com/subscribe/
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