Measuring vibration threshold with a graduated tuning fork in normal aging and in patients with polyneuropathy

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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 (
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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
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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
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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
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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
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                              ister clinically relevant information. Long term          157–61.
                                                                                    19 Merchut MP, Toleikis SC. Aging and quantitative sensory
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                                                                                    22 Steinberg FU, Graber AL. The eVect of age and peripheral
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                                                                                    23 Thomson FJ, Masson EA, Boulton AJM. The clinical diag-
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                      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

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