New Results

Vibrotactile perception in the sole of the foot in people with normal glucose tolerance and type 2 diabetes

Magnus Peterson, Ronnie Pingel, Olov Rolandsson, Lars B. Dahlin
doi: https://doi.org/10.1101/522706

Abstract

Aim To evaluate vibrotactile perception thresholds in people with normal glucose tolerance (NGT) and type 2 diabetes (T2DM) in relation to other sensory tests.

Methods Nerve function was evaluated in 36 and 42 participants with NGT and T2DM, respectively [mean age 70.0 (1.2) years; males n=40, females n=38]. The mean duration of T2DM was 12.3 (7.3) years. Vibration perception thresholds were measured at four frequencies (8, 16, 32 and 125 Hz) bilaterally on the sole of the foot at first and fifth metatarsal heads using Multifrequency vibrametry and compared to vibration perception thresholds using Biothesiometer (128 Hz) bilaterally (medial malleolus and distal dorsal bony surface of great toes), touch sensation with Semmes-Weinstein monofilament bilaterally (10 g) at three sites on the sole of foot (distal great toe and 1st and 5th metatarsal heads), electrophysiology (amplitude and conduction velocity of sural nerve; right side) and thermal sensory testing (i.e. small diameter nerve fibers; method of limits using Thermotest®).

Results Vibration perception and temperature thresholds in the foot and sural nerve function were different between the NGT and T2DM categories. Measuring vibration perception thresholds at lower frequencies with Multifrequency vibrametry, compared to Biothesiometer, both provided similar correlations to the amplitude of the sural nerve. Temperature thresholds did also correlate with vibration perception thresholds and with sural nerve function. Only 4/42 participants with T2DM showed pathology by monofilament test, none with NGT.

Conclusions Vibration perception thresholds have a fair correlation to amplitude of the sural nerve, even when measured at a non-tactile surface. Thus in the present study, measuring vibration perception threshold at a tactile surface does not seem to provide any clear advantage over the traditional way of measuring vibration perception on the medial malleolus. In people with T2DM, both large and small diameter nerve fibers seem to be affected.

Introduction

Vibrotactile perception at tactile surfaces on the feet are important for somatic function [1,2] and may be affected early in various neuropathies [3]. In diabetes type 2 (T2DM), peripheral neuropathy is a well-known long-term complication, occurring in up to 50% of people with T2DM [4,5]. Symptoms of neuropathy are often present even at the time of diagnosis. [4,6,7,8,9]. Combined with reduced blood flow, neuropathy in the feet promotes the risk of foot ulcers, infection, and at times even the need for limb amputation [10,11]. Loss of sensation and decreased balance can lead to increased risk of falls and tissue injury [10] and more than a third of those with T2DM and diabetic sensory-motor polyneuropathy develop neuropathic pain, which significantly impairs their quality of life [4]. In Sweden, screening examination for retinopathy and neuropathy, the latter using monofilament test and vibrating tuning fork, are recommended annually in people with T2DM [12] and is efficient in view of health economy [13,14,15,16]. However, the sensitivity of the screening examination is low and will only screen out those with a manifest neuropathy or with a painful neuropathy [17]. At an early stage, neuropathic changes may be reversible and with a more sensitive instrument for screening examination, the risk for complications could be reduced by early detection [18,19,20]. With invasive methods, such as electrophysiological assessment, neuropathic changes are detectable even in the pre-diabetic stage e.g., impaired glucose tolerance [18,21]. A simple and non-invasive method for more sensitive everyday clinical diagnosis of peripheral neuropathy is warranted.

Vibrotactile perception depends on the function of Pacinian corpuscles, responding to frequencies > 80 Hz (in particular at 250 Hz [22]) and on Meissner’s corpuscles, which are most sensitive at 30 Hz [23,24]. Vibration perception thresholds (VPTs) at different frequencies, reflecting dysfunction in subsets of receptors and their connected axons, may be a useful tool for detecting early signs of peripheral neuropathy. In clinical practice, vibrotactile perception is by tradition investigated by bone contact through the skin, at the pre-tibia, at the medial malleolus and at the big toe at an arbitrarily pragmatic frequency of 128 Hz to detect neuropathy [25,26]. However, tactile surfaces may be more appropriate sites to examine with respect to function [26,27,28]. For example, disturbed vibrotactile perception in finger pulps has been reported in vibration-induced neuropathy and in carpal tunnel syndrome [3,29]. Vibrotactile perception in the foot at different frequencies in a population with T2DM has previously not been examined and compared to normative data in people with normal glucose tolerance (NGT) [30], but has recently been reported in children with type 1 diabetes, showing early signs of neuropathy [31]. Thus, our aim was to evaluate VPTs at tactile surfaces on the sole of the foot bilaterally and to compare them with previously used techniques to evaluate sensory nerve function in people with NGT and in people with T2DM

Materials and Methods

Examinations were performed as part of a 10-year follow-up of a cohort originally from the population-based Västerbotten Intervention Programme (VIP) [32], with participants recruited from November 2004 until April 2007; the original study population has been described elsewhere [33]. At the 2014 follow-up, six of the original 119 participants were deceased, and 26 declined further participation. The remaining 87 participants with 36, 9, and 42 participants in the NGT, IGT, and T2DM categories, underwent examination of vibratory perception thresholds (VPTs). Due to the small sample size in the impaired glucose tolerance group, these were excluded from further analyses. Thus, 78 participants were analyzed (Table 1). The glycemic status of individuals with NGT and IGT was verified by two standardized oral glucose tolerance tests (OGTT) [34,35]. NGT was defined as a capillary fasting plasma glucose <6.1 mmol/l and a 2-hour plasma glucose <7.8 mmol/l; IGT as fasting plasma glucose < 7.0 mmol/l and a 2 hour plasma glucose ≥7.8 and <11.1 mmol/l. Lastly, T2DM was defined as a fasting plasma glucose level of ≥7.0 mmol/l and/or a 2 hour plasma glucose ≥11.1 mmol/l as defined by the 1999 WHO criteria [34,35]. Glomerular filtration rate was calculated according to the Cockroft-Gault formula where creatinine clearance= [(140-age) x mass (kg) x constant) / serum creatinine (in μmol/l)]. The constant is 1.23 for men and 1.04 for women.

Examination methods

Electrophysiological assessment

An experienced neurophysiologist, blinded to group identity for all participants, performed a standardized nerve conduction assessment at the clinical neurophysiology laboratory at Umeå University, Sweden. All measurements were conducted on the right leg, and included the amplitude and conduction velocity of the sural nerve [17]. The conduction velocity of the peroneal nerve was also measured, but was not analyzed further as it contains a larger proportion of motor neurons than the sural nerve, which was thus deemed the most appropriate target for evaluation of sensory nerve function.

Vibration perception thresholds

VPTs were measured with two different methods: 1) VibroSense Meter and 2) Biothesiometer. 1) VPTs using VibroSense Meter were measured bilaterally on the sole of the foot at two different locations, i.e. the first and fifth metatarsal head [31]. The sites were selected to mirror the function of the median plantar branch of the tibial (first metatarsal head) and the lateral plantar branch of the tibial (fifth metatarsal head). Measurements were performed with a modified VibroSense Meter adopted for measurement on the feet [36]. The thresholds were measured at four frequencies (8, 16, 32 and 125 Hz) at each site. The foot VibroSense Meter comprised of a modified hand device with an extended vibrating probe and a special footplate with a hole, which was placed over the modified device as described (for details, see Ising et al [31] and Dahlin et al [36]). The measuring procedure for the foot was identical with the previously reported examination of the fingers; i.e. according to ISO13091-1 [36]. The examination sequence on the sole of the foot was: 1) first metatarsal head, and 2) fifth metatarsal head. The examination time was approximately 3 min/site; i.e. in total 6 min/foot. Prior to the examination, the temperature was measured with the internal temperature probe on the VibroSense Meter, which is a standard procedure for the VibroSense Meter device at each investigated extremity to secure an appropriate interval of 27°-35° Celsius according to ISO 13091–1 [37,38,39]. The room temperature was between 20°-22°C (requirement according to ISO 13091–1).

2) VPT using a hand-held biothesiometer (Bio-Medical Instrument Co, ROVA Company Inc, Newbury, OH) was tested according to previously described procedure [17]. The VPTs, using the biothesiometer, were measured bilaterally at the medial malleolus and at the distal dorsal bony surface of both great toes. The measured unit is decibel (dB).

Monofilament

The pressure/touch sensation was examined bilaterally on the sole of the foot with a Semmes-Weinstein 10-g monofilament (Gertab AB, Stockholm, Sweden) at three standard sites; i.e. the plantar surface of the distal hallux and the 1st and 5th metatarsal heads [40]. Pathological monofilament test was defined as the absence of sensation at one or more sites on either foot [17,41].

Thermal testing

Thermal sensory testings were performed with the method of limits using Thermotest® equipment (Somedic AB, Hörby, Sweden) as previously described [17]. The limb temperature was kept above 31 °C.

Statistical Analysis

Participant characteristics in the NGT group and the T2DM group were described with counts and proportions for categorical variables and means and standard deviations for quantitative variables. Chi-square tests and Student’s t-tests were used to test for statistically differences in characteristics between the NGT and T2D group.

All measurements of sensory perception were summarized using means and standard deviations. Statistical differences between the left and the right side of the body regarding sensory perception were explored by studying standardized differences in means, i.e. t-values from paired samples Student’s t-tests. Differences in means between the NGT and T2D group were studied using t-values from independent samples Student’s t-tests. Standardized differences allow for comparisons of the different methods for studying sensory perception.

All tests were two-sided and the significance level was set to 5% for all the analyses, i.e. approximately a t-value of 2. Spearman’s correlations were calculated between all sensory measurements, stratified by NGT and T2D group. The statistical analyses were done using R 3.4.3 (R Core Team, 2017) [42] and the package “corrplot” [43].

Results

Demographics of participants

The characteristics of the participants are presented in Table 1. Out of the 78 participants in the study, 77 completed vibrametry, 78 biothesiometer, 74 electrophysiological assessments (amplitude and CV of sural nerve), 78 monofilament test and 73 thermal testing. For the VibroSense Meter, there was missing data for the left MT1, 16 Hz and left MT5, 125 Hz in one (though not the same) subject. The mean duration of diabetes was 12.3 years in the T2DM group (Table 1). As expected, participants with diabetes had a higher BMI than those with normal glucose tolerance as well as higher HbA1c levels. Serum cholesterol was lower and serum triglycerides higher among participants with diabetes (Table 1). Monofilament testing was pathological in 4 participants with T2DM and in none of those with normal glucose tolerance.

View this table:
Table 1. Baseline characteristics of the study population

Participants with normal glucose tolerance (NGT) and type 2 diabetes (T2DM).

Vibration perception and thermal thresholds

Vibration perception thresholds were higher with both methods (VibroSense Meter and Biothesiometer) in the soles of the feet in participants with T2DM compared to participants with normal glucose tolerance (Table 2, Fig 1). There were no clear within-group differences between the right and left side of the feet (Table 2, Fig 1). In a similar way, temperature thresholds for both heat and cold were higher among participants with T2DM compared to participants with normal glucose tolerance. Neither were there any within-group differences between the right and left side of the feet regarding temperature thresholds (Table 2, Fig 1).

View this table:
Table 2. Means and standard deviations for different methods of measuring nerve function in the foot, stratified by group and extremity

Normal glucose tolerance = NGT, type 2 diabetes = T2DM. N.B. Standardized differences between means of groups and extremities are indicated in Fig 1.

Fig 1.
Fig 1. Standardized differences between means of groups and extremities

Correlations between methods of nerve assessment

Correlations between the vibration perception thresholds and amplitude of sural nerve were generally higher in the participants with diabetes than in those with normal glucose tolerance, which had correlations close to zero (Fig 2). There were similar correlations between the amplitude of the sural nerve and vibration perception thresholds at all frequencies.

In participants with diabetes, the biothesiometer had in the present study a tendency to slightly higher correlation to the sural nerve amplitude than the multifrequency vibrametry, but in the normal glucose tolerance the correlations were close to zero. Using biothesiometer, there were similar correlations between the amplitude and vibration perception at both locations of testing, i.e. the medial malleolus and greater toe. Multifrequency vibrametry had a tendency to stronger correlation to amplitude of the sural nerve at the medial plantar examination site (MT1>MT5).

The correlations between amplitude of the sural nerve and temperature thresholds were similar to the correlations between sural nerve amplitude and vibration perception thresholds. There were similar correlations between the amplitude of the sural nerve and laterality (i.e. the right and left extremity) concerning both vibration perception thresholds and thermal thresholds. The correlation was generally weak between conduction velocity of the sural nerve and both vibration perception and thermal thresholds (Fig 2).

Fig 2.
Fig 2. Correlations (Spearman) between different methods for the examination of peripheral nerve function in the foot

The units of measurement for the methods displayed are the same as in Table 2.

Discussion

The present study show that vibration perception and temperature thresholds on the sole of the foot are different in older people with NGT and long-standing T2DM. Measuring vibration perception thresholds at lower frequencies compared to the current standard of 128 Hz both provided similar correlations to amplitude of the sural nerve. Evaluating vibration sense on a tactile area provided similar correlation to amplitude of the sural nerve, as compared to a non-tactile area such as the medial malleolus.

Peripheral neuropathy is one of many potential multi-factorial complications in T2DM [44]. In combination with reduced blood flow, neuropathy in the feet increases the risk of foot ulcers, infection, and sometimes even the need for limb amputation [11]. Early detection of disturbed sensory perception in T2DM is important, in order to avoid further complications [19,20,45]. During the early stages of T2DM, plasticity of the nervous system remains, and metabolic corrections have the potential to reverse symptoms [20,46]. In the present study, with long follow up of the participants we used a variety of methods to detect neuropathy, where vibration sense, detected by two different methods, was evaluated in an age-matched sample of individuals with NGT and T2DM. In most previous studies, the Biothesiometer, using a single frequency (128 Hz), has been used to detect vibrotactile perception applied at non-tactile surfaces [17]. This may seem an odd site of approximating peripheral sensory perception as tactile sensation on the sole of the foot or on the glabrous skin in the hand is considered to be more relevant for function of the lower extremity and the hand, respectively. Along with decreasing balance at higher age, reduced tactile sensation increases the risk of falls [10]. This suggests that measuring peripheral sensory perception at a tactile surface may be more relevant than measuring at a non-tactile surface area. However, the present study indicates measurement of vibration sense with the two techniques at a tactile or non-tactile area had a similar correlation to the amplitude of the sural nerve and thus a similar correlation to neuropathy. Measuring vibration perception thresholds at lower frequencies than the current standard of 128 Hz provides no clear advantage judging by the correlation to the amplitude of the sural nerve in the present study in older people with a long-standing T2DM. The current practice of measuring vibration perception on the bony surface of the medial malleolus seems to be as fair an approximation to amplitude of the sural nerve as vibration perception on the tactile surface of the foot, indicating loss of myelinated nerve fibers. Furthermore, temperature thresholds had similar correlations to sural nerve amplitude as vibration perception thresholds, indicating involvement to a similar degree of both myelinated and non-myelinated nerve fibers. Thus, in older people with long-standing T2DM, large and small diameter nerve fibers seem to be affected equally. In contrast, the correlation was generally weak between conduction velocity of the sural nerve and both vibration perception and thermal thresholds. This is likely due to the fact that demyelination of nerves is less apparent than the loss of nerve fibers in early stages of neuropathy[47]. Previous results suggest an association between blood glucose level and the severity of peripheral neuropathy, measured as amplitude of the sural nerve [18]. Thus, finding and evaluating sensitive methods of detecting reduced function of peripheral nerve function in various nerve fibers is an important task. As expected, there were differences between participants with NGT and the those with T2DM. VPTs in men and women are differently affected by diabetes with a higher risk for neuropathy in males with diabetes [48], but in the present study analysis of gender differences was not to possible due to the limited number of participants.

At present, monofilament testing, using the 10 gram monofilament, and vibration perception thresholds, measured with 128 Hz tuning fork, are used the everyday clinical setting in Sweden [41]. Lack of sensation for monofilament and vibration has high specificity, however, sensitivity is quite low [41,49]. Accordingly, the 10 gram monofilament test indicated very few of the pathological values in the present study.

The strength of the present study was that both people with T2DM and age- and gender-matched subjects were examined. This is relevant since vibration perception thresholds are age-dependent and appropriate cut-off values for judging between pathological and non-pathological values are different across different age categories [31]. Sensory perception in the foot was measured with different methods and at different sites on the lower extremities and vibration perception thresholds were measured with two different methods. The temperature of the foot was carefully measured before the examination, as this influences vibrotactile perception. A limitation is that the vibration threshold at each site was only measured once with each method in each participant. However, good test-retest reliability has been shown for VPT which decreases the need for repeated measurements [50]. Also, it is less likely that repeated measurements would influence results and conclusions due to the fair number of participants.

Conclusions

Vibration perception and temperature thresholds on the sole of the foot are different in older people with NGT and long-standing T2DM. Measuring vibration perception threshold at lower frequencies compared to the current standard of 128 Hz, or evaluating vibration sense on a tactile area compared to a non-tactile area provided similar correlation to amplitude of the sural nerve. Thus, measuring vibration perception thresholds at a tactile surface did not in the present study seem to provide any clear advantage over the traditional way of measuring vibration perception threshold at 128 Hz on the medial malleolus. In people with neuropathy due to long-standing T2DM, large (myelinated) and small (non-myelinated) diameter nerve fibers seem to be equally affected.

Acknowledgements

Our sincerest gratitude to Dr Sigbritt Rasmark, RN Karin Nilsson, and biomedical scientist Anette Broberg for their skillful assessment of the participants. We thank Tony Speidel, Vibrosense Dynamics for help with technical issues. We are indebted to the late Professor Göran Sundqvist, who was one of the initiators of the study. We would also like to thank all the participants who made this study possible. The work was supported by grants from Västerbotten County Council, and Umea University, Sweden (to O.R.)., funds from Skåne University Hospital, Lund University, the Diabetes Association in Malmö and the Swedish Diabetes Foundation (to L.D.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Posted January 16, 2019.
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Vibrotactile perception in the sole of the foot in people with normal glucose tolerance and type 2 diabetes
Magnus Peterson, Ronnie Pingel, Olov Rolandsson, Lars B. Dahlin
bioRxiv 522706; doi: https://doi.org/10.1101/522706
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