Gait & Posture 38 (2013) 518–522

Decreased skin temperature of the foot increases gait variability in healthy youngadults

Ryuichi Sawa a,*, Takehiko Doi b, Shogo Misu c, Kota Tsutsumimoto b,d, Hidemi Fujino d, Rei Ono a

a Department of Community Health Sciences, Kobe University Graduate School of Health Sciences, Kobe, Japanb Section for Health Promotion, Department for Research and Development to Support Independent Life of Elderly Center for Gerontology and Social Science, National Center for

Geriatrics and Gerontology, Obu, Japanc Kobe City Hospital Organization, Kobe City Medical Center West Hospital, Kobe, Japand Department of Rehabilitation Sciences, Kobe University Graduate School of Health Sciences, Kobe, Japan

A R T I C L E I N F O

Article history:

Received 31 May 2012

Received in revised form 10 January 2013

Accepted 29 January 2013

Keywords:

Plantar temperature

Gait

Sensation

Accelerometry

A B S T R A C T

We investigated the effects of reduction in plantar skin temperature on gait. Thirty-four healthy subjects

(20 men and 14 women; mean age 22.2 � 2.5 years; mean height 166.8 � 8.3 cm) walked 16 m under two

different conditions – normal conditions (NC) with the skin at a basal temperature, and cold conditions (CC)

after cooling of the plantar skin to about 15 8C. Wireless motion-recording sensor units were placed on the

back at the level of L3 and on both heels to measure acceleration and angular velocity. Gait velocity and mean

stride, stance and swing times were calculated. The variability of lower limb movement was represented by

the coefficients of variation (CVs) of stride, stance and swing times, and that of trunk movement was

represented by autocorrelation coefficients (ACs) in three directions (vertical: VT; mediolateral: ML; and

anteroposterior: AP). Gait velocity was significantly lower under CC conditions than under NC (p < 0.0001).

None of the temporal parameters were changed by plantar cooling. However, all parameters of gait

variability were significantly worse under CC, and AC-VT, AC-ML, and AC-AP were significantly lower under

CC than under NC, even after adjusting for gait velocity (p = 0.0005, 0.0071, and 0.0126, respectively). Our

results suggest that reducing plantar skin temperature induces gait variability among healthy young adults.

Further studies are now needed to explore the relationship between plantar skin temperature and gait in the

elderly.

� 2013 Elsevier B.V. All rights reserved.

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Gait & Posture

jo u rn al h om ep age: ww w.els evier .c o m/lo c ate /g ai tp os t

1. Introduction

Successful locomotion is supported by rhythmic motor behav-ior that consists of leg movements executed as the primary meansof propulsion and trunk movement helping to maintain bodyequilibrium [1]. Increasing gait variability during walking inducesinstability and implies reduction in the ability to coordinatemovement [2] and thus an increase in fall risk in older adults [3].Rhythmic movement is thought to be generated by a centralpattern generator and is modified by afferent feedback fromvarious sources [4,5]. The gait of people with peripheral sensoryloss is characterized by slow walking velocity, reduced step time,and shortened step length [6,7]. During walking, neuropathicpatients have smaller amplitude of trunk acceleration than controlsubjects owing to peripheral sensory loss [6].

* Corresponding author at: Department of Community Health Sciences, Kobe

University Graduate School of Health Sciences, 7-10-2 Tomogaoka, Suma-ku Kobe,

Hyogo 654-0142, Japan. Tel.: +81 78 792 2555; fax: +81 78 796 4509.

E-mail address: ry-sawa@stu.kobe-u.ac.jp (R. Sawa).

0966-6362/$ – see front matter � 2013 Elsevier B.V. All rights reserved.

http://dx.doi.org/10.1016/j.gaitpost.2013.01.019

The plantar aspect of the foot is the only part of the body that isin direct contact with the external environment. Sensory feedbackoriginating from cutaneous receptors, particularly in the sole,therefore plays a crucial role in walking. The effects of reduced footsensation on gait have been investigated in not only patients withsensory loss but also healthy adults. Experimental reduction inplantar information (i.e. temporary sensory loss) leads to adecrease in gait velocity [8,9], reduced electromyography activityof the muscles of the lower limbs [10], changes in joint movement,and modification of the pressure distribution pattern in walking[8,10,11]. Although gait is believed to be modified by afferentinformation, the effects of reduced plantar sensation on gait –including on trunk movement – during walking are still unclear.We hypothesized that cooling of the foot would reduce footsensation, and that the resulting change in afferent informationwould affect gait, including trunk movement, in the same way asoccurs with sensory loss from disease.

There are various experimental ways of inducing brief sensoryloss. They include induction of ischemia [12], application of localanesthesia [9], or induction of hypothermia [8,11]. Hypothermia isone causes of sensory deficit and is achieved by immersing the feet

Fig. 1. Wireless motion-recording sensor (MVP-RF8; 45-mm width, 45-mm depth,

18-mm height; weight, 60 g).

R. Sawa et al. / Gait & Posture 38 (2013) 518–522 519

in ice-cold water for 15 min [13] or 30 min [8] or until the skintemperature of the plantar surface of the foot drops below 6 8C[14]. However, the conditions achieved by using these methods arefairly unlikely to occur in everyday life: even in winter, foot skintemperature naturally declines to only about 15 8C [15]. Decreas-ing the skin temperature reduces blood flow. Thus the function ofthe cutaneous mechanoreceptors declines and afferent nerveconduction velocity is decreased. Moreover, because the plantaraspect of the foot contacts the external environment – especiallythe floor – almost constantly, it is likely that the supporting surfaceconducts heat away from the foot at cold times of the year or incold regions. However, to our knowledge, there have been nostudies of the effects of the decreases in plantar skin temperatureexpected in everyday life on foot sensation and gait; it maytherefore be useful to determine whether common decreases inskin temperature reduce plantar sensation and thus affect gait. Theaim of this study was to investigate how reducing plantar skintemperature to a level common in cold environments wouldinfluence gait. Our hypothesis was that the decreases in plantarskin temperature expected in everyday life induce declines insensory function and thus increases in gait variability, including intrunk movement.

2. Methods

2.1. Subjects

The study participants were 34 healthy subjects (20 men and 14women; mean age 22.2 � 2.5 years; mean height 166.8 � 8.3 cm).All subjects reported that they were free of neurological dysfunctionor disease, and of pain that might have affected their performance inthe study. Ethical approval for the study was given by the EthicsCommittee of the Kobe University Graduate School of Health Sciences(approval number 113). All subjects were properly informed aboutthe study and signed written consent forms, in accordance with theDeclaration of Helsinki, before their participation.

2.2. Gait measurement procedure

Subjects were instructed to walk at preferred speed along a 16-m smooth, horizontal walkway. A 12-m section of the walkwaywas marked off by two lines, one positioned 2 m from each end, toallow space and time for acceleration and deceleration. Walkingtime over the middle 10 m was measured with a stopwatch (areliable method for measuring time [16,17]), and gait velocity wasexpressed in meters per second. Trunk and lower limb movementduring gait was measured by using three wireless motion-recording sensor units (MVP-RF8; 45-mm width, 45-mm depth,18-mm height; weight, 60 g; MicroStone Co., Ltd., Nagano, Japan;Fig. 1), one fixed to a belt at the level of the L3 spinous process andthe others attached to the posterior surface of each heel withsurgical tape. Acceleration and angular velocity could thus bemeasured without restricting the subject’s movement. All signalswere sampled at 200 Hz and synchronously wirelessly transferredto a personal computer via a bluetooth personal area network.

2.3. Experimental reduction of plantar skin temperature

Plantar skin temperature was monitored with a digitalthermometer (PT-201, Unique Medical Co., Tokyo, Japan) thathad a temperature resolution of 0.1 8C and was equipped with awired thermosensor (PTP-50, Unique Medical Co., Tokyo, Japan).Before data collection the subjects were given a 20-minequilibration period to adjust to the room and floor temperatures(26.9 � 1.4 8C and 28.3 � 1.9 8C, respectively). Plantar skin tempera-ture was measured at three anatomical locations (heel, first

metatarsal head [1st MTH], and hallux) on the plantar aspect ofthe foot to determine the baseline plantar skin temperature. Theconditions after the subject’s plantar skin had adjusted to the floortemperature after removing their shoes were defined as normalconditions (NC). To alter plantar skin temperature, the subject’s feetwere placed on a block of ice with a plate-like surface. Thetemperature at each anatomical location on the foot was checkedevery 3 min to ensure that the skin was cooling. When thetemperature at each anatomical location on the foot was below15 8C, the conditions were defined as cold conditions (CC).

2.4. Plantar sensation testing

Before and after the cooling procedure, the plantar cutaneoussensation threshold was determined by using Semmes–Weinsteinmonofilaments (North Coast Medical Inc., San Jose, CA, USA). Eachfilament had a specified diameter and a known buckling force. Eachtest began with the 2.83 filament to evaluate the plantar cutaneoussensation thresholds at the three anatomical locations on theplantar aspect of the foot (i.e. the heel, 1st MTH, and hallux). Eachmonofilament was applied for 1 s perpendicular to the skin of thefoot being tested [18]. Before the test, the testing procedure wasexplained to the subjects and they were instructed to respondverbally when they felt the stimulus; they were also familiarizedwith the sensation produced by being touched with themonofilament. Testing at each anatomical location was repeatedwith monofilaments of increasing diameter until the subjectresponded to the stimulus.

Table 1Difference in the size of monofilaments between conditions.

Locations Condition p-Value

Normal Cold

Heel 4.17 (3.84–5.07) 4.74 (4.17–5.46) <0.0001*

1st MTH 3.84 (3.22–4.17) 4.31 (3.84–5.46) <0.0001*

Hallux 3.84 (3.22–4.31) 4.24 (3.61–5.18) <0.0001*

* Compared between conditions, p < 0.05. Differences in all parameters between

normal and cold conditions were compared by using the non-parametric Wilcoxon

signed-rank test.

Table 2Differences in basic gait parameters between conditions.

Parameters Condition p-Value

Normal Cold

Gait velocity (m/s) 1.31 � 0.18 1.25 � 0.17 <0.0001*

Stride time (s) 1.03 � 0.07 1.03 � 0.07 0.4727

Stance time (s) 0.60 � 0.05 0.60 � 0.05 0.5033

Swing time (s) 0.42 � 0.03 0.43 � 0.03 0.6720

* Compared between conditions, p < 0.05. Differences in all parameters between

normal and cold conditions were compared by using a paired t-test.

Table 3Condition-related differences in gait variability.

Parameters Condition p-Value Adjusted

p-value*

Normal Cold

Stride time CV (%) 1.79 � 0.67 2.07 � 0.50 0.0278y 0.1266

Stance time CV (%) 2.68 � 0.71 3.06 � 0.81 0.0156y 0.0579

Swing time CV (%) 2.93 � 0.91 3.42 � 1.02 0.0106y 0.2545

AC-VT 0.88 � 0.07 0.81 � 0.10 0.0001y 0.0005z

AC-ML 0.69 � 0.15 0.61 � 0.19 0.0041y 0.0071z

AC-AP 0.87 � 0.07 0.82 � 0.10 0.0011y 0.0126z

CV, coefficient of variation; AC, autocorrelation coefficient; VT, vertical; ML,

mediolateral; AP, anteroposterior.* Adjusted for gait velocity.y Compared between conditions, p < 0.05. Differences in all parameters between

normal and cold conditions were compared by using a paired t-test.z Compared between conditions after adjusting for gait velocity, p < 0.05.

Differences in all parameters between normal and cold conditions were compared

by using a paired t-test.

R. Sawa et al. / Gait & Posture 38 (2013) 518–522520

2.5. Data analysis

Signal processing was performed with MATLAB (The Math-Works Co., Release 2008, Cybernet Systems Co., Ltd., Tokyo, Japan).Before the analysis, all acceleration and angular velocity data werelow-pass filtered with a cutoff frequency of 20 Hz. To computetemporal gait parameters we analyzed heel acceleration and heelangular velocity data. On the basis of pilot testing to determinetemporal parameters by using heel acceleration and heel angularvelocity data, a heel contact event was identified as a verticalacceleration peak and a toe-off event was identified as themaximum heel angular velocity in the sagittal plane. These eventswere used to calculate the timing of the stride-, stance- and swing-phase intervals. The stride, stance, and swing times were thencalculated by using the mean duration of each phase. Theconcurrent validity of this method was good to excellent in youngsubjects in comparison with that of a standardized method usingforce-sensitive resistors (ICC: 1.0, 0.95, and 0.89, respectively). Thecoefficients of variation (CVs) of the stride, stance and swing timeswere also computed to estimate the variability of lower limbmovement. CV was calculated by using the formula: CV = (stan-dard deviation/mean) � 100. Trunk acceleration data for eachdirection, namely vertical (VT), mediolateral (ML), and anteropos-terior (AP), were analyzed to evaluate the variability of trunkmovement, as computed by using an unbiased autocorrelationprocedure [19]. An unbiased autocorrelation coefficient (AC) is anestimate of the regularity of a time series by cross-correlation withitself at a given time shift; it is independent of the length of themanaged data. Perfect stride-regularity of trunk movementreturned an AC of 1; if there was no association between trunkmovement and stride, the AC was 0.

2.6. Statistical analysis

Plantar sensation under the two conditions was compared byusing the non-parametric Wilcoxon signed-rank test, because thesensation data did not have a normal distribution. A paired t-testwas used to compare differences in gait parameters betweenconditions. It was further performed after adjustment of the valuesin the results to differences in gait velocity, because the values ofCV and AC were potentially dependent on gait velocity [19–22]. Allanalyses were performed with JMP7.0J software (SAS InstituteJapan, Tokyo, Japan) for Windows XP. The level of significance wasset at p < 0.05.

3. Results

3.1. Sensation before and after reduction of plantar skin temperature

We tested the sensation at each anatomical location before andafter cooling of the plantar surface to about 15 8C. All subjectsreported that the plantar aspect of the foot was less sensitive underCC than under NC; this was confirmed by a significant increase inthe size of the monofilament required to elicit sensation aftercooling. The size of the first monofilament that could be feltincreased significantly at all three locations (Table 1).

3.2. Comparison of gait parameters between conditions

Cooling did not change any mean gait parameters other thangait velocity (Table 2). Subjects walked about 4.5% slower under CC(gait velocity: p < 0.0001), but the mean stride, stance and swingtimes did not differ between conditions. Cooling did, however, leadto significant changes in all parameters associated with gaitvariability (Table 3). In the unadjusted analyses, CVs of stride,stance, and swing time increased significantly (CV of stride time:

p = 0.0278; CV of stance time: p = 0.0156; CV of swing time:p = 0.0106) and AC-VT, -ML, and -AP worsened by about 8.0%,11.6%, and 5.7%, respectively (AC-VT: p = 0.0001; AC-ML:p = 0.0041; AC-AP: p = 0.0011). The differences in the CVs of stride,stance and swing time between conditions were not significantafter adjustment for gait velocity, but AC-VT, AC-ML, and AC-APdecreased significantly after cooling, even after adjustment (AC-VT: p = 0.0005; AC-ML: p = 0.0071; AC-AP: p = 0.0126).

4. Discussion

Our results revealed that decreasing the plantar temperature toabout 15 8C in healthy young people caused a reduction in plantarcutaneous sensation and affected gait. The significant reduction inplantar cutaneous feedback was confirmed at all plantar testregions (heel, 1st MTH, and hallux). Mean stride, stance and swingtimes did not differ significantly between conditions. After footcooling, the subjects walked more slowly and there were changesin the parameters associated with gait variability. The significantdifferences between conditions were confirmed in ACs represent-ing trunk movement variability, even after adjustment for gaitvelocity.

The reduction in information input from the plantar surfacereduced gait velocity and increased variability of stride, stance and

R. Sawa et al. / Gait & Posture 38 (2013) 518–522 521

swing times. Studies of the influence of experimentally inducedplantar insensitivity on gait patterns suggest that reduction ofafferent input may result in slower walking [8,9], decreased peakpressure [8,11], and increased duration of loading during stancephase [8]. In addition, patients with peripheral neuropathy arecharacterized by plantar insensitivity and, unlike healthy adults,have reduced gait velocity [6,7]. Dingwell et al. suggested thatpatients with peripheral neuropathy walk slowly and adjust bysmall perturbations in gait as a way of compensating for thedecrease in afferent feedback from the soles of their feet [23]. Ourresults built on these results and suggested that plantarinsensitivity affected gait. However, the post-cooling changes invariability of the stride, stance and swing times were weakened byadjustment of the results to account for gait velocity. This meansthat these differences between the two conditions were affected bythe change in gait velocity. The relationship between gait velocityand gait variability has been reported elsewhere as strong [21,22].Manor et al. investigated the effects of plantar desensitization ontreadmill walking and showed that reducing plantar sensation didnot lead to a change in variability of stride duration during lowerlimb movement under controlled speed [24]. These findingssupported our results: experimental reduction of foot sensation ledto slower walking in an effort to maintain afferent feedback fromthe sole of the foot, but this was not extended to the mean andvariability of stride, stance, and swing times.

Trunk movement variability increased in all directions underCC. The increase in trunk movement variability in all directionswas significant even after adjustment for gait velocity, althoughtrunk movement variability is influenced by gait velocity [3,17].Trunk movement plays a crucial role in the control of balanceduring walking [1], and sensory feedback contributes to thestability of trunk movement during walking [25]. Menz et al.suggest that the gait of older people with diabetic peripheralneuropathy is characterized by decreased velocity, reduced trunkacceleration during normal walking, and reduced smoothness oftrunk movement during more challenging gait (i.e. walking onirregular surfaces) [6]. Plantar sensation is of particular importancein trunk movement during postural control in experimentalstudies of altered foot sensation. Reduction of afferent inputcauses body sway in standing [26], and increasing sensory input tothe skin of the sole effectively reduces postural sway in quietstanding [27–29]. Our results build on these findings and suggestthat plantar sensation contributes to postural control of not onlystanding balance but also gait. Furthermore, even though ourexperimental alteration of foot sensation was brief, its effects ongait were similar to those of long-term insensitivity in diabeticperipheral neuropathy. A temporary decrease in plantar sensationmight also have the potential to increase trunk movementvariability in older adults, who show functional decline of sensorysystems and physical functions with age. Further studies arerequired to determine the effects of decreased plantar skintemperature on gait in the elderly.

Here, we cooled the plantar aspect of the foot to below 15 8C.Immersing the feet in ice-cold water for a given time [8,13] orplacing them on shaved ice [14] are methods that have been usedto reduce sensation on the sole. Nurse and Nigg placed the feet onshaved ice until the plantar skin temperature dropped below 6 8Cto induce plantar hypothermia [14]. However, even in winter, footskin temperature usually does not drop below about 15 8C [15].Our study is the first to have decreased plantar skin temperature toa level that would likely commonly occur and to then find that thisdecrease was capable of reducing plantar sensation and increasingtrunk movement variability in gait. Increased trunk movementvariability means that locomotor control is disabled, and this inturn is associated with fall risk among older adults [3]. Plantartemperatures that are commonly reached are therefore likely to

increase this fall risk. In fact, seasonal variations in the rates of fallsand fall-related hip fractures among the elderly have been reportedin several studies: their incidence is higher indoors during winter,particularly at low daily ambient temperatures [30–32]. Thereduced temperature of the plantar surface might make gaitunstable and thus be a risk factor for falls.

This study had several limitations. First, an important drawbackof hypothermic protocols is that cooling procedures can affect notonly plantar cutaneous receptors but also intrinsic foot musclesand joint receptors. Second, this study was conducted during theJapanese autumn and the floor surface temperature was higherthan 15 8C. During stance phase, the floor surface therefore mighthave provided the plantar skin with heat and thus warmed theplantar skin during the gait analyses. Ideally we would havemonitored the changes in plantar surface temperature during gait,but such monitoring would have been difficult. Third, it is difficultto generalize our results, because our analysis was limited tohealthy young adults. Further studies are needed to clarify therelationship between plantar skin temperature and gait.

In conclusion, cooling of the plantar skin to a temperature thatcould commonly occur on cold days affected gait velocity,variability in stride, stance and swing time, and variability intrunk movement. Further studies are needed to clarify therelationship between plantar skin temperature and gait in theelderly and to investigate the importance in gait of keeping theplantar aspect of the foot warm.

Acknowledgement

We would like to thank all the subjects who participated in thisstudy.

Conflict of interest statementThere is no conflict of interest.

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