ORIGINAL ARTICLES

Postural Instability in DiabeticNeuropathic Patients at Risk of FootUlcerationE.C. Katoulisa, M. Ebdon-Parryb, S. Hollisc, A.J. Harrisond, L. Vileikytea, J. Kulkarnib,A.J.M. Boultona

aUniversity Department of Medicine, Manchester Royal Infirmary,Manchester, bDisablement Services Centre, Withington Hospital,Manchester, cDepartment of Mathematics and Statistics, LancasterUniversity, Lancaster, and dDepartment of Prosthetics and Orthotics,University of Salford, UK

Diabetic peripheral neuropathy is believed to cause postural instability due to abnormalproprioception. We assessed body sway in four groups, each of 20 subjects, matched forage, sex, and BMI: non-diabetic controls, non-neuropathic diabetic controls, subjects withdiabetic neuropathy and no history of foot ulceration, and subjects with diabetic neuropathyand a history of foot ulceration. Postural sway was assessed on a Kistler force plate usingthe Romberg test, measuring the standard deviation of the centre of pressure in bothsagittal (antero-posterior movement) and frontal (side to side movement) planes with eyesopen and closed. The Romberg test results were log transformed and then analysed usinganalysis of variance followed by Newman-Keuls test. There was no significant differencein body sway between the two control groups and the first group of subjects with diabeticneuropathy. However, in patients with a history of ulceration, values were significantlyhigher (p ,,, 0.05) compared to all other groups in both planes and conditions studied.These results are suggestive of a relationship between impaired body sway control andfoot ulceration. Postural instability may have clinical significance and increase the risk ofminor trauma and ulceration in patients with diabetic neuropathy.

KEY WORDS Body sway Diabetic foot Diabetes mellitus Diabetic neuropathy Footulceration Postural instability

and visual function, if intact, are expected to activateIntroductioncompensatory mechanics.5 However, one can speculatethat not all sensory deficits can be adequately compro-To maintain posture is a complex task which demands

the gathering and integration of sensory (afferent) infor- mised by the remaining and functioning sensory systems.There is currently qualitative6 and quantitative7–9mation to coordinate effectively the neuro-musculo-

skeletal system.1 The peripheral sensory systems involved evidence that body sway is increased in diabetic patients.The increased sway has been attributed to defectsare the vestibular apparatus,2 the visual system,3 and the

kinaesthetic and proprioceptive receptors (e.g. Golgi in proprioception associated with increased vibrationperception threshold (VPT) frequently seen in diabetestendon organs, joint receptors, etc.) which are widely

distributed throughout the body. While complementary, mellitus complicated by neuropathy.10 Increased bodysway could lead to abnormal gait and increased falls11each of these systems serves individually in a unique

functional manner. The somatosensory information (body and thus contribute to the increased risk for ulcerationfound in insensitive feet.segment orientation, joint position, etc.) originates in the

specialized mechano-receptors scattered all over the We therefore sought to investigate the degree ofpostural instability in diabetic patients with neuropathy,body in joint capsules, ligaments, muscles, and the

cutaneous and subcutaneous structures of the skin.4 and investigate the potential relationship between suchinstability and foot ulceration.Somatosensory function has attracted less research and

clinical attention than ocular and vestibular function.Moreover, in the case of a sensory deficit, as is commonly Subjects and Methodsseen in diabetes complicated by neuropathy, vestibular

Sixty subjects with insulin-dependent (Type 1) and non-insulin-dependent (Type 2) diabetes mellitus (IDDM and

Abbreviations: CoP centre of pressure, NDS neuropathy disability NIDDM) were recruited from patients regularly attendingscore, VPT vibration perception threshold the Diabetes Centre, Manchester Royal Infirmary. TheyCorrespondence to: Professor A.J.M. Boulton, University Department

were divided into three groups, each of 20 subjects,of Medicine, Manchester Royal Infirmary, Oxford Rd, Manchester M139WL, UK matched for age, sex, and body mass index (BMI),

296 CCC 0742–3071/97/040296–05 Accepted 24 November 1996 1997 by John Wiley & Sons, Ltd. DIABETIC MEDICINE, 1997; 14: 296–300

ORIGINAL ARTICLESaccording to the presence or absence of diabetic disease; visual acuity , 6/18 of any aetiology; history of

excessive alcohol intake (. 30 u/week); regular use ofneuropathy, and, in the neuropathic patients, those withand without a history of foot ulceration. The three centrally acting medications; BMI . 30; any minor/major

amputation and any previous illness or operations thatdiabetic groups were therefore:could interfere in any way with the measurements.

1 diabetic control subjects (DC): no neuropathy, noAll 80 subjects were assessed for postural sway control

history of foot ulceration;on a Kistler force plate (Model 9284, Kistler Instruments

2 diabetic neuropathy subjects (DN) without ulceration;AG Winterthur, Switzerland) of our gait analysis system

3 subjects with diabetic neuropathy and a history of(Vifor System, LIC Orthopaedics, Stockholm, Sweden)

foot ulceration (DNU).using a Romberg test. This force plate is a piezoelectrictransducer being able to measure the standard deviationAnother 20 non-diabetic volunteers, most of them being

relatives of the diabetic participants with no history of (STD) of the movement of the centre of pressure (CoP).The latter is defined as the point on the ground throughdiabetes in their own family, served as a further control

group (NC). In summary, we studied 80 subjects allocated which a single resultant ground reaction force appearsto act, although in reality the total force is made up ofin four groups, NC, DC, DN, and DNU.

The presence of neuropathy was evaluated through innumerable small force vectors.The Romberg test is an established balance testthe assessment of the neuropathy disability score (NDS)12

and the vibration perception thresholds (VPT). The NDS12 which gives a quantitative assessment of body sway bycalculating the STD of the movement of CoP while theis the product of scoring ankle reflexes plus vibration,

pin-prick and temperature (cold tuning fork) sensation subject is standing. The STD of CoP in both sagittal(antero-posterior movement) and frontal (side to sideat the great toe. The maximum NDS is 10, and scores

of 3–5, 6–8, and 9–10 were defined as evidence of mild, movement) planes was expressed in millimetres for allthe subjects under two conditions, i.e. subjects standingmoderate, and severe signs, respectively.12 Secondly,

VPT was assessed using the Biothesiometer (Biomedical for 30 seconds on the force plate with their eyes open(fixing their gaze on a stationary target) and then anotherInstrument Company, Newbury, Ohio, USA) on the tip

of the great toe. If the patient could not feel the vibration 30 seconds with their eyes closed.All subjects gave written informed consent. The studyat the maximum amplitude of 50 V, the value of 50 V

was recorded and used for the statistical analysis. VPT protocol was approved by Research Ethics Committeeof Central Manchester Health Authority. The reportedvalues greater than 25 V are strongly associated with

increased risk of foot ulceration13 and were, therefore, investigations have been performed in accordance withthe principles of the Declaration of Helsinki.used as indicative of the presence of neuropathy.

For the purposes of this study, the presence ofneuropathy in the participating diabetic subjects was Statistical Analysisdefined by an NDS . 5 and a VPT . 25 V. All subjectsin the diabetic control group had NDS # 4 and VPT Comparisons of neuropathy tests were made between

the two control groups and between the two diabetic, 25 V. Those with any history of previous neuropathicfoot ulcers up to 3 months prior to study were included neuropathy groups using t-tests for normally distributed

data (VPT) or Mann-Whitney U tests for non-normallyin the DNU group.There were no significant differences between groups distributed data (NDS). Statistical comparisons of NDS

and VPT between the control groups and the diabeticfor sex ratio, age, and BMI. Diabetes duration was longerin group DNU. The participating subjects characteristics neuropathy groups were not made since these are used

to define neuropathy and they are, therefore, expectedare summarized in Table 1.Exclusion criteria included: age over 65 years; history to be different.

The Romberg test results were log transformed toof vestibular, peripheral vascular, neurological (otherthan diabetic aetiology), musculo-skeletal or rheumatic achieve normality. Results were analysed initially by

Table 1. Baseline patient characteristics

NC DC DN DNU

n 20 20 20 20Sex (M/F) 15/5 14/6 14/6 16/4Age (yr)a 50.6 ± 8.6 47.6 ± 10.7 52.9 ± 8.8 54.1 ± 7.1BMIa 25.5 ± 2.4 25.1 ± 2.7 27 ± 1.9 27 ± 1.8Duration of diabetes (yr)b – 11 (6,20) 14 (7,22) 20 (11,35)NDSb 0 0 7.5 (6, 8) 8 (7, 9)cVPTa 11.8 ± 3.6 12.1 ± 4.60 32 ± 5.6 36.7 ± 8.3d

aMean ± SD; bmedian (IQ range); cp = 0.033; dp = 0.04.

297POSTURAL INSTABILITY IN DIABETIC PATIENTS

ORIGINAL ARTICLESanalysis of variance using group and within subject the values produced by the effect of closed eyes in thecomparisons of plane (frontal/sagittal) and eyes control groups. This difference reached significance in(open/closed). Comparisons within each combination of the frontal but not in the sagittal plane. These resultsplane and eyes were then made across the four groups can be explained by the fact that recordings made inusing one-way analysis of variance followed by post hoc the frontal plane measure side to side movement. Thistests adjusted for multiple comparisons (Newman-Keuls is thought to be impaired in advanced neuropathy whentest). The ratio of results with eyes closed to eyes open the small muscles of the feet are affected. It is likely thatwithin the same plane were analysed in a similar manner. the overall increased instability in foot ulcer patients isValues are expressed as geometric means with 95 % related to a proprioceptive deficit related to the neuro-confidence intervals. pathy, as vestibular and visual function were normal in

Moreover, a paired t-test was performed on the our subjects.collected data under eyes open vs eyes closed in each For the purposes of this study neuropathy was definedplane for each group individually. A Bonferroni correction by the assessment of NDS and VPT. This mode ofwas applied to adjust for multiple comparisons (n = 4). evaluation was previously validated by both the Manches-

ter12 and the Mayo group.14 Patients with neuropathyResults were then distinguished by the presence or absence of

a history of foot ulceration. Diabetic patients in the groupThere was no significant difference between the two with a history of foot ulceration showed significantlycontrol groups for NDS and VPT. When subjects with a increased body sway compared with the two controlhistory of foot ulceration were compared (DN vs DNU), and neuropathic groups. These findings are in accordanceNDS and VPT were slightly higher in the DNU group with recently published data,7–9 but previous studies(Table 1). However, the neuropathy in either group was have not specifically looked at the association with footclassified as moderate and severe. ulceration. Was the link in our patients a reflection of

The Romberg test results are shown in Table 2 and more severe neuropathy? Although the neuropathy inFigure 1. In summary, statistical analysis of the parameters our foot ulcer patients was more marked when assessed bystudied revealed significant differences mainly in the NDS and vibration perception, this statistically significantgroup of neuropathic patients who had a history of foot finding is unlikely to be clinically relevant as both groupsulceration (Table 2). Across all conditions there was a had a neuropathy that would be assessed as moderatesignificant difference in the STD of CoP between the

or severe according to previously published criteria.12,13

groups (F3,76 = 17.5, p , 0.0001). Having closed eyesThus, our observations offer an explanation for why

consistently increased body sway (overall estimatedpatients with a foot ulcer history or moderate to severe

increase in STD of CoP of 24 % (95 % CI 14 % to 35 %),neuropathy may be at particular risk of minor traumaF1,76 = 28.3, , 0.0001). These effects did not vary acrossand falls.the groups (two-way interactions between group and

There is evidence that increased instability may beplane or eyes, p . 0.5) and there was no additionalrelated with increased risk of falls in the elderly15,16 andeffect of combining the plane of measurement with eyesthe neuropathic diabetic subjects.6,11 The consequencesclosed (interaction between plane and eyes and three-wayof falls are increasingly recognized among the leadinginteraction between group plane and eyes both p . 0.2).causes of morbidity and mortality in the elderly17 withIn the intergroup comparisons there was a significantsubstantial social and economic impact that should nottrend to increased sway across the four groups asbe neglected. Indeed, a recent study by Young et al.18

compared with non-diabetic controls; DC: +2 % (14 %,has shown the presence of decreased bone mineral+21 %), DN: +22 % (3 %, 45 %), and DNU: +72 %density in the lower limbs of neuropathic patients with(45 %, +105 %), p , 0.0001. In addition, compared toCharcot neuroarthropathy which could well increase theDN, the increase in sway in diabetic foot ulcer patientsrisk of fractures in neuropathic patients.was 41 % (19 %, 67 %), p = 0.0001.

We postulate that postural instability is a silent problemin diabetic neuropathic patients which is under-reportedDiscussionin the literature, and underestimated and overlooked inthe clinical practice. With this study we were able toThe results suggest a significant adverse effect of diabeticshow that diabetic neuropathy in patients with historyneuropathy when associated with foot ulceration onof foot ulcers is associated with increased body swaybody sway control during standing, while diabetes itself,during standing, thus extending the results of previousin the absence of neuropathy, had no effect on posturalstudies. Although longitudinal studies would be neededstability. We have confirmed that the presence ofto confirm it, our findings raise the possibility thatneuropathy is associated with an increase in body swaypostural instability may be causally associated with footsimilar to that produced by closed eyes in the twoulceration, and its consequences in neuropathic diabeticcontrol groups. Moreover, the presence of neuropathypatients deserve further research and increased clinicaland foot ulceration is associated with an additional

increase in body sway with eyes open thus exceeding awareness in diabetes care.

298 E.C. KATOULIS ET AL.

ORIGINAL ARTICLES

Tabl

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299POSTURAL INSTABILITY IN DIABETIC PATIENTS

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control. In: Amblard B, Berthoz A, Clarac F, eds. Postureand Gait.: Development, Adaptation and Modulation.New York: Excerpta Medica, 1988: 95–104.

5. Paulus W, Straube A, Brandt TH. Visual postural perform-ance after loss of somatosensory and vestibular function.J Neurol Neurosurg Psychiatry 1987; 50: 1542–1545.

6. Cavanagh PR, Derr JA, Ulbrecht JS, Maser RE, OrchardTJ. Problems with gait and posture in neuropathic patientswith insulin dependent diabetes mellitus. Diabetic Med1992; 9: 467–474.

7. Simoneau GG, Ulbrecht JS, Derr JA, Becker MB, CavanaghPR. Postural instability in patients with diabetic sensoryneuropathy. Diabetes Care 1994; 17: 1411–1421.

8. Boucher P, Teasdale N, Courtemanche R, Bard C, FleuryM. Postural stability in diabetic polyneuropathy. DiabetesCare 1995; 18: 638–645.

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11. Lord SR, Caplan GA, Colagiuri R, Colagiuri S, Ward JA.Figure 1. Geometric mean STD of the CoP in normal control Sensori-motor function in older persons with diabetes.(P), diabetic control (m), diabetic neuropathy (r), and diabetic Diabetic Med 1993; 10: 614–618.neuropathy with history of ulceration (K) groups. Geometric 12. Young MJ, Boulton AJM, MacLeod AF, Williams DRR,means with 95 % confidence intervals Sonksen PH. A multicentre study of the prevalence of

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This study was partly supported by a grant for diabetic prediction of diabetic neuropathic foot ulceration usingvibration perception thresholds. Diabetes Care 1994; 17:research from the British Diabetic Association and the557–560.Lilian Voudouri Foundation, Athens, Greece.

14. Dyck PJ. Detection, characterization and staging ofpolyneuropathy assessed in diabetics. Muscle Nerve 1988;11: 21–32.

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