N A L A R T I C L E

Postural Instability in
Patients with Diabetic
I t is well known to those who treat pa-
tients with diabetic distal symmetrical
polyneuropathy that these patients will
occasionally complain of instability while
walking or standing (1,2). Instability
Sensory Neuropathy could have many causes (such as central
nervous system [CNS] dysfunction, de-
GUY G. SIMONEAU, PHD MARY B. BECKER, RN creased lower-extremity strength, visual
JAN S. ULBRECHT, MB, BS PETER R. CAVANAGH, PHD deficits, etc.), but in the diabetic patient
JANICE A. DERR, PHD with sensory neuropathy, it is usually at-
tributed principally to the lack of ade-
quate proprioceptive feedback from the
OBJECTIVE — Recent survey evidence suggests that sensory ataxia due to diabetic lower extremities and is labeled sensory
neuropathy may be a more frequent and serious problem than is commonly recog- ataxia (1,2). Although significant anec-
nized. This view is further supported by research that confirms the major contribution dotal evidence of this problem exists (2),
of the somatosensory system to the control of posture. We therefore sought to deter- there is, at present, little quantitative evi-
mine the effects of significant diabetic distal symmetrical polyneuropathy on the con- dence in a well-characterized sample to
trol of posture. determine the magnitude of the effect ( 3 -
RESEARCH DESIGN A N D M E T H O D S — Fifty-one subjects, divided into 5). In addition, clinically significant sen-
three groups, participated in this study. Seventeen had diabetes and significant sensory sory ataxia is thought to be relatively rare
neuropathy, 17 had diabetes and no neuropathy, and 17 had neither diabetes nor (1,2), a perspective that may not be cor-
neuropathy. The subjects were matched across groups, and stringent exclusion criteria rect (4). In this study, therefore, we set
were applied. Postural stability during quiet standing was measured using a force out to measure postural stability among
platform. In addition to electrophysiological and quantitative sensory tests of neurop- patients with diabetic distal symmetrical
athy, a number of physical and functional characteristics were measured for all subjects. polyneuropathy during stance and to de-
termine the physical and sensory charac-
RESULTS— Postural instability was found to be significantly associated with sen- teristics that may be most predictive of
sory neuropathy, but not with diabetes per se. Patients with sensory neuropathy dem- instability in this population. The patients
onstrated between 66 and 117% more instability than did control subjects (depending were not selected for complaints of insta-
on the testing condition). Based on multiple linear regression analyses, the most sig- bility.
nificant correlates of instability were the quantitative sensory measures of neuropathy
and age.
CONCLUSIONS — The loss of sensory perception secondary to diabetic distal RESEARCH DESIGN AND
symmetrical sensory neuropathy has a markedly detrimental effect on postural stabil- M E T H O D S — Fifty-one subjects, di-
ity. The deficit is greatest when visual or vestibular cues are absent or degraded. vided into three groups (n = 17 per
Patients with neuropathy need to be informed of the postural consequences of this group), were studied. Group 1 was se-
condition to limit the potential morbidity caused by falls. lected to have diabetes and neuropathy
(DM-NP), group 2 to have diabetes but no
significant neuropathy (DM-nonNP), and
From the Program in Physical Therapy (G.G.S.), Marquette University, Milwaukee, Wisconsin, group 3 to have neither diabetes nor neu-
and The Center for Locomotion Studies (J-S.U., M.B.B., P.R.C.) and the Department of Statistics ropathy (nonDM). The majority of the
(J.A.D.), Penn State University, University Park, Pennsylvania. subjects with diabetes were recruited
Address correspondence and reprint requests to Peter R. Cavanagh, PhD, The Center for from a specialty diabetes clinic, and a few
Locomotion Studies, Room 10, Intramural Building, Penn State University, University Park, PA
16802. subjects with diabetes and all of the non-
Received for publication 12 December 1993 and accepted in revised form 30 June 1994. diabetic control subjects were recruited
CNS, central nervous system; DM-NP, subjects with diabetes and neuropathy; DM-nonNP, through advertising. Significant periph-
subjects with diabetes and no significant neuropathy; nonDM, subjects with neither diabetes nor eral sensory neuropathy was defined as
neuropathy; VPT, vibratory perception threshold; NIDDM, non-insulin-dependent diabetes the average vibratory perception thresh-
mellitus; IDDM, insulin-dependent diabetes mellitus; SLR, sensory latency response; MNCV,
motor nerve conduction velocity; SW, Semmes-Weinstein; JMPT, joint movement perception old (VPT) for the halluces being equal to,
threshold; VCS, visual contrast sensitivity; ROM, range of movement; CoP, center of pressure; or exceeding, the age-adjusted normal
ANOVA, analysis of variance. VPT values published by Bloom et al. (7)
(the upper limit of normal was defined by

DIABETES CARE, VOLUME 17, NUMBER 12, DECEMBER 1994 1411

Posture and diabetic sensory neuropathy

Table 1—Exclusion criteria measured in the diabetic subjects. Motor

1. Regular use of medications affecting the central or peripheral nervous system or muscular function tests included manual and hand-
function and likely to have an impact on postural stability measurements (medications held dynamometric assessment of
allowed were limited to angiotensin-converting enzyme inhibitors, antiarrhythmics, strength of the lower-extremity muscula-
antibiotics, nonsteroidal anti-inflammatory drugs, calcium channel blockers, cardiac ture together with motor nerve conduc-
glycosides, diuretics, H2 receptor blockers, hormones, lipid-lowering agents, nitrates) tion velocity (MNCV) testing of the pero-
2. Significant weakness of the lower-extremity musculature, including weakness due to neal nerve in the DM groups.
diabetic distal motor neuropathy or disuse
VPT on the plantar surface of both
3. A history of neurological diseases (other than peripheral neuropathy attributed to
halluces was tested using a fixed-fre-
diabetes) likely to affect lower-extremity function or posture, including, but not limited
to, peripheral nerve compression, focal neuropathies, radiculopathies, strokes, and quency (60 Hz) variable amplitude vibro-
Parkinson's disease meter (Biothesiometer, Bio-Medical In-
4. Visual acuity <20/100, loss of binocular vision, or presence of double vision (diabetic strument, Newbury, OH) using the
retinopathy per se was not an exclusion) method of limits protocol (7,9), with an
5. Abnormal clinical evaluation of vestibular function upper limit value of 50 V. The full set of
6. Weight outside - 2 0 to - 3 3 % ideal body weight (46) 20 Semmes-Weinstein (SW) monofila-
7. Inability to abstain from alcohol on the day of testing; history of drug or alcohol ments (ranging from 1.65 to 6.65: these
dependency or of medical treatment for drug or alcohol dependency numbers represent logg of 10 times the
8. Inability to abstain from caffeine for 6 h before testing of postural stability
buckling force in grams; the higher the
9. A history of psychological/psychiatric conditions requiring medical attention
10. Clinically apparent significant abnormalities (deformity, abnormal range of motion, etc.)
number, the worse the neuropathy) was
of the back, hip, knee, ankle, or foot used for evaluating touch-pressure sensa-
11. Any arthritic conditions causing frequent pain, discomfort, and difficulty walking or tion following the protocol of Sosenko et
standing al. (10). For data analysis, the SW rating
12. A history of major surgical procedures, major fractures, or other musculoskeletal and VPT values obtained for the right and
problems likely to affect lower-extremity function and posture left halluces were averaged.
13. Any previous illness, surgery, or other characteristic(s) that might, in the opinion of the To quantify joint movement per-
investigator, interfere with lower-extremity function, postural mechanism, or the subject's
ception threshold (JMPT) at the ankle in a
adequate participation in the study protocol
14. For the nonDM subjects, a blood glucose value >6.72 mmol/1 more than 2 h after a meal
weight-bearing condition, we used a de-
15. Severe exercise-induced claudication vice that was specially designed for this
purpose. The apparatus consisted of two
individually movable foot plates that
could be tilted up (for dorsiflexion) or
Bloom et al. as mean + 2 SD of their dependent diabetes mellitus (NIDDM),
down (for plantarflexion) through the use
healthy subjects at each age). To control and subjects with onset of diabetes when
of an electromagnetic actuator (11). Test-
for possible effects of multiple other char- younger than age 40 years who were ing was performed for plantarflexion and
acteristics on postural stability, the sub- treated with insulin within 2 years of di- dorsiflexion at an angular velocity of
jects were matched across the groups by agnosis were considered to have insulin- 0.25% using the method of limits. For
gender, age (limited to 4 0 - 7 0 years), dependent diabetes mellitus (IDDM). data analysis, JMPTs of the right and left
weight in relationship to height, and du- ankles were averaged after adding plan-
ration of diabetes. Each triplet of subjects Neuropathy assessment tarflexion and dorsiflexion threshold val-
was matched as closely as possible for all It has been suggested that to fully assess ues together.
four characteristics. The exclusion criteria neuropathy, multiple measures of sen- Knee extensor and flexor and an-
applied during subject selection were de- sory and motor function should be used kle plantarflexor and dorsiflexor strength
signed to limit the possible influence of (8). This approach was particularly rele- testing was performed with a hand-held
factors other than diabetes and neuropa- vant in this study because one of the ques- dynamometer (12,13). These measure-
thy on postural stability (Table 1). Diabe- tions being asked was, What measure of ments were converted into torque values
tes type was assigned as follows: subjects neuropathy might best predict instability? by multiplying the force applied (in kg)
with onset of diabetes when older than Somatosensory function tests included and the distance between the point of ap-
age 40 years and those with onset when the evaluation of vibratory, touch-pres- plication and the center of rotation of the
younger than age 40 years who were not sure, and ankle joint movement percep- joint (in cm). In addition, the strength of
treated with insulin within 2 years of on- tion thresholds. The sensory latency re- the ankle evertors and invertors and flex-
set were considered to have non-insulin- sponse (SLR) of the sural nerve was also ors of the toes, including the halluces,

1412 DIABETES CARE, VOLUME 17, NUMBER 12, DECEMBER 1994

 Simoneau and Associates

were tested subjectively using manual

muscle testing (14).
B
Conventional electrophysiologi-
cal methods (15) were used to measure
MNCV and SLR.

Other subject characteristics

Since it is known that quality of the visual
input can have an impact on stability
(16), a rather extensive evaluation of vi-
sion was performed. These tests included
standard corrected binocular visual acu-
ity. Visual contrast sensitivity (VCS) at
five spatial frequencies (1.5, 3, 6, 12, and
18 cycles/degree of visual angle) was as-
sessed using three Vistech charts (Vistech
Consultants, Dayton, OH). The assess-
ment of VCS has been reported to provide
a better and more comprehensive mea-
surement of visual function than the as-
sessment of visual acuity (17). The aver-
age luminance for the charts was ~40
candelas/m (2). Because it has been sug-
gested that peripheral vision is most rele-
vant to the maintenance of upright pos-
ture (18), visual peripheral field for each
eye of each subject was tested using stan-
dard equipment for every 45° of periph-
eral vision. Clinical evaluation of the ves-
tibular system, the third sensory system
actively involved in the control of pos-
ture, was performed in the laboratory by
using four standard tests of vestibulo-
ocular function (19) and the stepping test
as described by Fukuda (20). Ranges of
movement (ROMs) of the ankle, subtalar
joint, knee, and first metatarsophalangeal
joint were measured using standard go-
niometric techniques (21). All subjects
completed an activity level questionnaire
that also contained questions regarding
their subjective ability to perform various
daily tasks such as walking, getting up
from a chair, and going up and down
stairs. Blood pressure was measured after
3 min of sitting and then after 1 and 3 min
of standing.
Stability measures
Measurements of stability were per-
formed with the subjects standing quietly
Medio-Lateral
Figure 1—A: A subject standing on a force platform during a stability test. Postural stability is tested
here while the subject is standing barefoot and looking straight ahead with her eyes open for a period of
30 s. The structure surrounding the subject provides a standard visual environment. B: A typical CoP
excursion signal output obtained over the 30 s of data collection. One division on both axes represents a
1-cm excursion of the CoP. The length of this path is used to quantify stability. This approach can be
thought of as a quantitative Romberg test.
barefoot and as still as possible for 30 s value, the less stable the individual
(Kistler type 9261A on-line to an SMS (22,23).
minicomputer) (Fig. 1A). This platform, The force platform was located at
which is level with the floor surface, is the center of a volume (6 ft by 16 ft by 10
equipped with force transducers that ft high) specifically built to control the
measure the magnitude and the direction visual environment (Fig. 1A), which con-
of the forces applied to it. The center of sisted of vertical 3-inch gray/white alter-
pressure (CoP) signal (Fig. IB), corre- nating stripes (optimal for the mainte-
sponding to the point of application of the nance of stable posture [241). Lighting
resultant force between the feet and force was constant, with a mean luminance of
platform, can therefore be measured and 20 candelas/m (2). A pure vertical visual
reflects the stability of each subject during cue pattern was obtained using noncor-
stance (22,23). The CoP signal was sam- rective lenses that allowed full peripheral
pled at a rate of 100 Hz for a period of 30 vision with the exception of the white
s. Before analysis, the data were filtered ceiling and black floor. A standard foot
with a 4th-order, zero-phase shift, Butter- position with the heels 15 cm apart and
worth-type low-pass filter with a cutoff the feet toeing-out 10° was used.
frequency of 5 Hz (24). For the purpose For the diabetic subjects, blood
of these experiments, only the total excur- glucose levels were measured before and
sion of the path of the CoP signal was every 30 min during the experiment.
used to quantify stability: the larger this Minimum and maximum acceptable lev-

DIABETES CARE, VOLUME 17, NUMBER 12, DECEMBER 1994 1413

Posture and diabetic sensory neuropathy

Table 2—Subject characteristics used for matching tarsophalangeal joint ROM in extension,
and amount of body rotation and dis-
DM-NP DM-nonNP nonDM placement obtained with the Fukuda test.
Next, a series of multiple linear regression
Number of subjects 17 17 17 models were fit to this set of predictor
Gender (female/male) 4/13 4/13 4/13
variables. The log transform of total CoP
Age (years) 55.0 ± 7.9 54.2 ± 8.1 54.7 ± 8.5
Weight (kg) 91.6 ± 14.5 86.8 ± 11.7 87.3 ± 9.4 excursion was used as the dependent
Height (cm) 180.0 ± 7.5 177.2 ± 5.3 177.5 ± 7.9 variable to stabilize the error variance.
Duration of diabetes (years) 16.0 ± 9.9 13.4 ± 9.8 NA Predictor variables were sequentially ex-
Age at diabetes onset (years) 39.3 ± 16.3 40.8 ± 11.1 NA cluded from the model using a criterion
Data are means ± SD. No statistically significant differences were found among the three groups for any of for P values that decreased at every pass
the variables (P > 0.05). through the data from P = 0.30-0.20 to
0.10-0.05.
A second group of linear regres-
sion equations using age and quantitative
els of blood glucose were defined as 4.48 characteristics. Each block in the design sensory measurements as predictor vari-
and 22.40 mmol/1, respectively. Testing was made up of the three matched sub- ables of CoP excursion while standing
was started a maximum of 1 h after a meal jects, one from each group. An ANOVA with eyes open/head forward was calcu-
and lasted ~ 2 h. was also used to estimate differences in lated for the subset of 34 diabetic sub-
the CoP total excursion among the three jects, to provide potentially clinically use-
Experimental conditions groups and among the four experimental ful reference tables from which prediction
To assess the effects on stability of so- testing conditions. For all analyses, the of problems of stability in patients with
matosensory deficits caused by neuropa- ANOVA was followed by post hoc com- various degrees of neuropathy might be
thy in conjunction with deficits in vision parisons among model means when sig- possible, while taking into account the
and/or vestibular function, we tested all nificant differences were found. age of the patients. All sets of prediction
subjects under four conditions: eyes To determine the best-fitting lin- equations were inspected for model R2
open/head straight, eyes open/head back, ear regression model predicting CoP total and significance of coefficients.
eyes closed/head straight, and eyes excursion of all 51 subjects while stand- Finally, because age and sensory
closed/head back. In the head back posi- ing with eyes open/head forward, a statis- functions were the best predictors of in-
tion, which is believed to reduce the ef- tical search was conducted in several stability, possible interactions between
fectiveness of vestibular information for steps. First, the correlation matrix of the these two variables in predicting CoP ex-
the control of posture (25), neck/head ex- full set of predictor variables was in- cursion were investigated within the
tension was standardized to be 45°. For spected. The objective of this inspection ANOVA model and by using the interac-
each trial with eyes open, the subjects was to reduce the number of predictor tion terms in the regression models.
were instructed to fix their gaze on a sta- variables in the search set while including
tionary target in the center of their field of representative measures of vision, neu-
vision. Each subject was tested under all ropathy, joint movement perception, ves- RESULTS
four conditions using a randomized bal- tibular function, and subject demo-
anced design; three trials were averaged graphic characteristics. Sets of highly General subject characteristics
under each condition. correlated and functionally related vari- The physical characteristics of the
ables, such as the several measures of vi- DM-NP (diabetic neuropathic), DM-
Statistical analysis sual acuity, were represented by one vari- nonNP (diabetic not significantly neuro-
The SAS software package (26) on the able per set. The initial set of predictors pathic), and nonDM (neither diabetic nor
mainframe computer of The Pennsylvania included 19 variables: age, weight, neuropathic) groups on which matching
State University was used for data analy- height, gender, diabetes, retinopathy, of the subjects was based are shown in
sis. An analysis of variance (ANOVA) for a VPT and an indicator for off-scale read- Table 2. There were no statistically signif-
randomized block design was used to de- ings, SW rating and an indicator for off- icant differences (P > 0.05) among the
termine whether there were any statisti- scale readings, VCS at 1.5 cycles/degree, groups in terms of these attributes. There
cally significant differences among the JMPT, ankle plantarflexion torque, ROM were five subjects with IDDM in the
three groups for all measurements of neu- for ankle dorsiflexion measured with the DM-NP group and six in the DM-nonNP
ropathy as well as for measurements of knee extended, manual muscle testing for group. Of the subjects with NIDDM,
other sensory functions and physical the foot, subtalar joint ROM, first meta- eight in the DM-NP group and seven in

1414 DIABETES CARE, VOLUME 17, NUMBER 12, DECEMBER 1994

 Simoneau mid Associates

Table 3—Neuropathy characteristics ity, visual contrast sensitivity at higher

frequencies, and peripheral visual field
DM-NP DM-nonNP NonDM testing. The differences in retinopathy
were reflected by a statistically significant
VPT (Vs) 47.4 ± 3.3 13.9 ± 6.4 11.8 ± 4 . 7
reduction (P < 0.05) in visual contrast
Touch-pressure perception (SW rating) 4.6 ± 1.4 3.3 ± 0.5 2.9 ± 0.5
JMPT (degrees) 3.8 ± 3.6 1.5 ± 1.0 1.8 ± 1.4
sensitivity at the low spatial frequencies
SLR of sural nerve (ms) 6.3 ± 2.0 4.7 ± 1.1 NA (Table 4).
MNCV of peroneal nerve (m/s) 36.1 ±8.3 42.3 ± 5.1 NA No statistically significant differ-
Strength ences were found among the three groups
Ankle dorsiflexion (kg • cm) 305 ± 109 317 ± 122 397 ± 117 for passive knee ROM, ankle dorsiflexion
Ankle plantarflexion (kg • cm) 301 ± 98 312 ±97 370 ± 91 measured with the knee at 90°, ankle
Knee flexion (kg • cm) 551 ± 225 523 ± 207 576 ± 246
plantarflexion and metatarsophalangeal
Knee extension (kg • cm) 1324 ± 541 1282 ± 443 1544 ± 490
joint flexion. The two groups with diabe-
Data are means ± SD. In the DM-NP group there were 6 off-scale measures for VPT (50 V), 4 for SW rating
(6.65), and none for JMP; these values are included in the data in the table. In four subjects in the DM-NP tes were found to have significantly less (P
and one in the DM-nonNP groups, SLR could not be measured; they are not included in the data in this table. < 0.05) first metatarsophalangeal joint
Differences between the DM-NP and the other two groups for VTP, touch-pressure perception, and JMPT are extension (DM-NP = 76.6 ± 19.6°; DM-
statistically significant (P < 0.01). Difference between the DM-NP and the DM-nonNP group for SLR of sural nonNP = 83.7 ± 11.2°; nonDM = 92.0
nerve and MNCV of peroneal nerve is statistically significant (P < 0.05). Differences between the nonDM and
the two DM groups for ankle dorsiflexion and ankle plantarflexion are statistically significant (P < 0.05).
± 12.4°) and ankle dorsiflexion when
measured with the knee extended (DM-
NP = 5.6 ± 4.0°; DM-nonNP = 5.9 ±
3.3°; nonDM = 8.6 ± 4.8°) than the
the DM-nonNP group were being treated mal strength (4/5 in one case), and the nonDM group. A significant difference
with insulin at the time of the study. nonDM subjects all had normal strength. was also found between the two diabetic
groups for subtalar joint mobility (DM-
Measures of neuropathy Other subject characteristics NP = 25.1 ± 5.8°; DM-nonNP = 29.7 ±
The values for VPT, touch-pressure sen- Four subjects in the DM-NP group had 6.2°; nonDM = 28.1 ± 3.8°). These dif-
sation perception threshold (SW rating), background retinopathy and four others ferences in joint mobility were expected
ankle JMPT, MNCV of the peroneal had prior laser surgery, compared with because others have shown that limited
nerve, and SLR of the sural nerve are one subject with background retinopathy joint mobility is a feature of diabetes
shown in Table 3. There were statistically and one subject with prior laser surgery in (27,28).
significant differences between the the DM-nonNP group (Table 4). There All subjects had normal vestibulo-
DM-NP group and the two control were no statistically significant differences ocular function based on the clinical and
groups, such that the DM-NP group had a (P > 0.05) among groups for visual acu- the Fukuda tests (data not shown). Based
significant amount of neuropathy com-
pared with the control groups. There
were no statistically significant differences Table 4—Visual function characteristics
(P > 0.05) between the DM-nonNP and
nonDM groups in terms of neuropathy.
DM-NP DM-nonNP nonDM
Torque values for the ankle and
knee musculature are also listed in Table Retinopathy (background/laser) 4/4 1/1 NA
3. Strength at the knee was not signifi- Corrected visual acuity (X/20) 25.4 ± 11.6 21.8 ± 7.8 21.2 ± 5.3
cantly different among the groups (P > Visual field (degrees)
0.05). At the ankle, both DM groups were Left eye 63.3 ± 4.6 63.5 ± 3.9 63.8 ± 4.5
significantly weaker than the nonDM Right eye 65.4 ± 5.9 66.7 ± 5.6 66.5 ± 3.0
Visual contrast sensitivity
group (P < 0.05), but the two DM groups
1.5 cycles/degree 62.1 ± 24.9 78.2 ± 22.0 81.9 ± 23.5
were not statistically significantly differ-
3 cycles /degree 102.6 ± 45.8 136.8 ± 36.3 138.6 ± 40.0
ent from each other (P > 0.05). Of the 17 6 cycles /degree 91.3 ± 51.4 121.6 ±38.2 126.8 ± 59.4
DM-NP subjects, 4 had minimal weak- 12 cycles /degree 45.4 ± 29.5 58.4 ± 33.2 55.4 ± 30.7
ness (manual muscle rating of 4/5) of the 18 cycles/degree 13.9 ± 9.2 15.8 ± 10.3 17.5 ± 12.8
hallux or toe flexors of either foot. All but Data are means ± SD. Differences between the DM-NP and the other two groups for visual contrast sensi-
one of the DM-nonNP subjects had nor- tivity at 1.5, 3, and 6 cycles/degree are statistically significant (P < 0.05)

DIABETES CARE, VOLUME 17, NUMBER 12, DECEMBER 1994 1415

Posture and diabetic sensory neuropathy
on the activity profile questionnaire, the
groups were well matched in terms of ac-
tivities and abilities to perform routine
daily tasks.
The average blood glucose levels
during postural testing were 10.70 and
11.20 mmol/1 for the DM-NP and DM-
nonNP groups, respectively. These values
were 10.98 and 11.48 mmol/1 at the start
of the experiments and 10.19 and 10.98
mmol/1 after 90 min, respectively. These
values were not significantly different be-
tween the two groups with diabetes at any
time.
HbAlc values were not obtained
as part of the formal protocol. Clinical re-
sults were available for 13 subjects in the
DM-NP group and for 12 subjects in the
DM-nonNP group. The average values
(mean ± SD) were 8.1 ± 2.2 and 6.9 ±
2.0%, respectively, and these were not
statistically different from each other (P =
0.19). These results do provide some in-
dication of the level of control of diabetes
among our subjects at the time of these
experiments. As has been the case in most
studies of diabetes complications, we did
find a significant positive correlation be-
tween the HbAlc values and neuropathy
measures (r = 0.31-0.43)
Patients receiving antihyperten-
sive therapy during the study were as fol-
lows: six in the DM-NP group (two were
receiving diuretics only); three in the DM-
nonNP; and one in the nonDM group.
Blood pressure values for the three groups
are shown in Table 5. There was a trend
for the systolic blood pressure to be
higher in the diabetes groups when com-
pared with the nonDM group, and this
difference was statistically significant (P
< 0.05, DM-NP versus nonDM and DM-
nonNP versus nonDM) in the 3-min sit-
ting blood pressure. However, when the
two diabetes groups were compared, the
largest difference between them in sys-
tolic blood pressure was only 2 mmHg, so
that these two groups can be considered
well matched in terms of systolic blood
pressure. There were no significant differ-
ences between the groups in diastolic
blood pressure. Most importantly, there
1416
Table 5—Blood pressure by group
3 min 1 min 3 min
sitting standing standing
DM-NP 143V81 141/81 142/82
(20/7) (27/8) (29/8)
DM-nonNP 144V86 139/86 141/86
(22/12) (22/10) (22/11)
nonDM 128/84 127/83 131/85
(15/7) (14/7) (18/7)
Values are averages (SD). * Systolic blood pressure
in the DM group statistically significantly different
from nonDM group; changes from sitting to stand-
ing are not statistically significantly different.
were no significant differences between
the three groups in the change in systolic
and diastolic blood pressure from sitting
to standing after 1 and 3 min. The lowest
recorded standing systolic blood pressure
was coincidentally identical in the three
groups at 104 mmHg. No patients had
CNS symptoms upon standing (symp-
tomatic postural hypotension was an ex-
clusion criterion). Thus, no differences in
postural hypotension existed among the
three groups.
Therefore, with the exception of
small deficits in some aspects of visual
function, minor differences in ankle and
foot mobility, small deficits in ankle and
foot musculature strength, and a differ-
ence in systolic blood pressure after 3 min
of sitting, the three groups of subjects
were considered to have very similar
physical characteristics except for the
quality of somatosensory perception in
the distal end of the lower extremities.
Instability and diabetic neuropathy
The postural stability results for each
group under the four testing conditions
are graphically represented in Fig. 2. The
DM-NP subjects were found to be signif-
icantly less stable (greater CoP excursion)
under all conditions than either the DM-
nonNP or nonDM subjects (P < 0.01).
These differences were large: the DM-NP
group was, on average, between 66 and
DIABETES CARE, VOLUME 17,
117% less stable than the nonDM group.
Note that as visual or vestibular inputs
were degraded or removed (e.g., in the
eyes closed/head back condition) the
neuropathic patients experienced much
greater percentage declines in stability
than did the other groups. No significant
differences were found between the DM-
nonNP and nonDM groups under any of
the test conditions (P > 0.05). Thus, sen-
sory neuropathy had a significant adverse
effect on stability while standing, but dia-
betes per se had no effect.
Association between instability and
sensory and physical characteristics
The influence of sensory deficits as repre-
sented by the different sensory measures,
as well as of all the other physical charac-
teristics on the control of posture were
investigated by grouping all 51 subjects
together and using regression analysis
techniques. Thereby, possible contribu-
tions of measures that were found to be
different among groups (ankle strength
and visual contrast sensitivity at low fre-
quencies) and of variables that although
not different among the groups could in-
fluence control of posture (age, for exam-
ple) could be determined. In a multiple
linear regression model in which all mea-
sures of sensation as well as age, weight,
height, duration of diabetes, retinopathy
status, measures of vision, strength at the
ankle, and range of motion of several
joints of the foot were tested, only mea-
sures of sensory neuropathy and age con-
tributed significantly to the fit of the
model (Eq. 1)
Instability = exp (1.89 + 0.018
age + 0.010 VPT
+ 0.396 SW off-scale) (1)
withR2 = 63.3% (Pearson r = 0.80). (For
Eqs. 1 through 4, coefficients are signifi-
cant at P < 0.05, unless otherwise stated;
instability corresponds to the CoP excur-
sion in cm over 30 s in the eyes open/head
forward condition; the indicator variable
SW off-scale has a value of 0 if the SW
rating is ^6.65 and a value of 1 if it is
NUMBER 12, DECEMBER 1994
 Simoneau and Associates

lating instability to age and SW rating in

the diabetic patients is

Instability = exp (1.46 + 0.023

age + 0.118 SW rating
+ 0.218 SW off-scale) (3)
where R2 = 54.7% (Pearson r = 0.74).
The SW off-scale variable was included in
the model to account for the upper limit
in the measurement despite its P value
being >0.05.
The linear regression equation re-
lating instability to age and ankle JMPT in
the diabetic patients is
Instability = exp (2.07 4- 0.0182
age + 0.0697 JMPT) (4)

Eyes Eyes Eyes Eyes where R2 = 51.9% (Pearson r = 0.72).

open/Head open/Head closed/Head closed/Head Equations for MNCV and SLR are
straight back straight back not shown because MNCV did not pre-
dict sway and SLR did so with an R? value
Testing Conditions
of only 4.4%.
Figure 2—Postural instability for the three groups of subjects under the jour testing conditions. A Tables 6, 7, and 8, developed
statistically significant difference (P < 0.01) was found between the DM-NP group and the two other from Eqs. 2, 3, and 4, provide a simple
groups jor all conditions. No statistically significant difference was found between the DM-nonNP and reference chart to determine the level of
nonDM groups (P > 0.05). Also note the similarity in instability between the DM-NP subjects standing
instability of individuals between 40 and
with eyes openAooking ahead and the nonDM group when standing with eyes closed/head back. The solid
65 years of age with various levels of sen-
line above each bar represents 1 SD.
sory losses measured in different ways.
The shaded areas correspond to the com-
bination of age and sensory loss in an in-
greater and therefore off scale; the indica- ered reasonable to provide an equation dividual with diabetes that would predict
tor variable VPT off-scale has a value of 0 for each sensory measurement technique more instability during stance than ex-
if the VPT is < 50 V and a value of 1 if it is because clinicians, in the absence of a rec- pected when compared with a healthy
greater and therefore off scale. The base of ognized standard measurement of sen- person between the ages of 40 and 60.
the natural logarithm [exp] is ~2.7182.) sory neuropathy, will often limit their as- The criterion value for normal stability
The type of diabetes, treatment sessment of sensory function to any one (determined to be 27.1 cm) is based on
method, and blood glucose level at the of these tests. the average CoP excursion (18.55 cm)
time of the experiment were not signifi- The linear regression equation re- plus 2 SD (8.54 cm) for the 13 nonDM
cantly related to postural stability. lating instability to age and VPT in the subjects between the ages of 40 and 60.
diabetic patients is
Prediction of instability from age CONCLUSIONS
and single measurements of Instability = exp (1.63 + 0.024
neuropathy age + 0.010 VPT Instability and diabetic neuropathy
The individual linear regression models + 0.079 VPT off-scale) (2) The major finding of this study is that di-
to predict instability for the eyes open/ abetic patients with distal symmetrical
head forward condition using age in con- where R2 = 53.6% (Pearson r = 0.73). sensory neuropathy not selected for any
junction with three different quantitative The VPT off-scale variable was kept in the complaint of instability are significantly
sensory tests of neuropathy as predictor model to adjust for the upper limit of VPT less stable during quiet standing than ei-
variables are presented below. These measurement despite its P value being > ther age-matched diabetic patients with-
equations were derived from the data of 0.05. out marked sensory neuropathy or age-
the 34 diabetic subjects. It was consid- The linear regression equation re- matched nondiabetic control subjects.

DIABETES CARE, VOLUME 17, NUMBER 12, DECEMBER 1994 1417

Posture and diabetic sensory neuropathy

Table 6—Prediction of instability for diabetic individuals standing with eyes open and symptoms, and some had a history of foot
looking forward based on VPT and age ulceration. Even though they did not
complain of instability, we found them to
VPT (Vs) be quite unstable. In a survey of younger
patients with neuropathy, we found re-
Age (years) 10 20 30 40 50 cently that similar patients did report
40 14.49 16.00 17.67 19.52 21.55 problems when questioned directly (6).
45 16.30 18.00 19.88 21.96 24.25 Therefore, we suspect that this is a clinical
50 18.34 20.26 22.37 24.71 27.29 problem that is underreported, perhaps
55 20.64 22.80 25.18 27.80 30.71 because patients consider it to be a part of
60 23.23 25.65 28.33 31.29 34.55 normal aging. Instability may also not be
65 26.14 28.86 31.88 35.21 38.88 as disturbing as neuropathic pain or as
Instability = exp(1.63 4- 0.024 age + 0.010 VPT + 0.079 VPT-offscale). A value of 27.1 cm represents the visible as ulceration. We suggest, how-
upper 95% confidence interval for stability in healthy adults between 40 and 60 years of age (mean + 2 SD
ever, that clinicians must consider insta-
[18.55 + 2 X 4.27]). All values in excess of 27.1 cm are shaded, indicating that individuals with these
combinations of age and sensory losses are outside the normal 95% confidence interval. Therefore, this table bility in dealing with their patients with
can be used clinically to establish the level of instability of patients based solely on VPT testing and age, neuropathy.
eliminating the need to perform a test of stability with sophisticated equipment.

Consequences of instability
Diabetes per se has no effect on postural tually be much worse than what we have There is, in fact, additional circumstantial
stability. While the results have implica- observed in this study. In the clinical set- evidence in the literature to suggest that
tions for posture control theory, there are ting, neuropathic patients are likely to be instability may be clinically important
a number of potentially significant clini- encountered with a variety of conditions, among patients with diabetic neuropathy.
cal consequences of these findings. e.g., medications that act on the CNS, sig- Heath et al. (31) reported an increased
With eyes open/head straight the nificant weakness and/or other lower- incidence of leg/ankle fractures in dia-
patients with sensory loss were found to extremity dysfunction, uncorrected vi- betic women compared with age-
sway 66% more than did the healthy con- sual deficits, or obesity (29,30), that matched nondiabetic control subjects (al-
trol subjects. This is approximately the would cause additional instability. though neuropathy was not measured in
same degree of instability seen in healthy As noted, these neuropathic pa- their study). Selby (32), based on a review
people of a similar age when standing tients were not selected based on any of several publications, indicated that the
with their eyes closed/head back (Fig. 2). complaints of instability, but simply on incidence of diabetes among patients with
In the eyes closed/head back position the basis of having neuropathy. A few femoral neck fractures is greater than ex-
(such as might be encountered by a per- were experiencing painful dysesthetic pected based on the incidence of diabetes
son with cataracts in poor lighting look-
ing up to reach a high shelf), the patients
with sensory neuropathy were found to Table 7—Prediction of instability for diabetic individuals standing with eyes open and
be approximately twice as unstable as an looking forward, based on SW rating and age
average healthy person under the same
circumstances (Fig. 2). Semmes-Weinstein monofilament (SW rating)
Because of the rigorous exclusion
criteria used in this study, we were able to Age (years) 1.65 3.22 4.31 5.18 6.65
recruit neuropathic patients with no 40 13.34 16.05 18.26 20.23 24.06
likely reason for instability other than 45 14.99 18.05 20.52 22.74 27.05
neuropathy. Specifically, patients with all 50 16.86 20.29 23.07 25.57 30.41
the other known clinically important con- 55 18.95 22.80 25.93 28.74 34.18
tributors to instability (29,30) were ex- 60 21.30 25.64 29.15 32.31 38.42
cluded. In addition, the visual environ- 65 23.94 28.82 32.77 36.32 43.19
ment was optimized for the maintenance Instability = exp (1.46 + 0.023 AGE + 0.118 SW-rating + 0.218 SW-offscale). A value of 27.1 cm
of posture in our experiments. This im- represents the upper 95% confidence interval for stability in healthy adults between 40 and 60 years of age
(mean + 2 SD [18.55 + 2 X 4.27]). All values in excess of 27.1 cm are shaded, indicating that individuals
plies that in clinical situations, the degree
with these combinations of age and sensory losses are outside the normal 95% confidence interval. There-
of postural instability among patients fore, this table can be used clinically to establish the level of instability of patients based solely on SW
with diabetic sensory neuropathy may ac- monofilament testing and age, eliminating the need to perform a test of stability with sophisticated equipment.

1418 DIABETES CARE, VOLUME 17, NUMBER 12, DECEMBER 1994

 Simoneau and Associates

Table 8—Prediction of instability for diabetic individuals standing with eyes open and touch) would have greater instability than
looking forward, based on JMPT and age would a 73-year-old individual with nor-
mal age-adjusted sensory function.
Ankle JMPT (degrees) A major goal of the regression
analysis was to provide the clinician with
Age (years) 0.5 2.25 4 5.75 7.5 a method to predict instability in diabetic
40 16.99 19.20 21.69 24.50 27.68 patients without the use of force plat-
45 18.61 21.03 23.76 26.84 30.32 forms, which are rarely available in a clin-
50 20.39 23.03 26.02 29.39 33.21 ical setting. Equation 1 appears to provide
55 22.33 25.22 28.50 32.19 36.37 such a tool, because a large percentage of
60 24.46 27.63 31.21 35.26 39.84 the variance in the measurement of stabil-
65 26.79 30.26 34.19 38.62 43.63 ity (R2 = 63.3%) is accounted for by age
Instability = exp (2.07 + 0.0182 AGE + 0.0697 JMPT). A value of 27.1 cm represents the upper 95% and only two clinically measurable inde-
confidence interval for stability in healthy adults between the ages of 40 and 60 (mean 4- 2 SD [18.55 + 2
X 4.27]). All values in excess of 27.1 cm are shaded, indicating that individuals with these combinations of
pendent variables: VPT and SW off-scale.
age and sensory losses are outside the normal 95% confidence interval. Therefore, this table can be used The determination of these factors, using
clinically to establish the level of instability of patients based solely on ankle JMPT testing and age, elimi- a vibrometer and a single SW mono fila-
nating the need to perform a test of stability with sophisticated equipment. ment, can be easily performed in the phy-
sician's office and takes ~ 5 min using
simple and affordable equipment.

in the population, although there is some
debate over whether diabetic osteopenia
or diabetic neuropathy is responsible. We
have found radiographic evidence of foot
fractures to be much more prevalent in
neuropathic diabetic patients (33), and,
in the recent interview study already
mentioned, neuropathic patients self-
reported 15 times more injuries during
gait and felt significantly less safe in un-
usual conditions than did non-neuro-
pathic diabetic patients (6). Finally, Rich-
ardson et al. (34) reported that peripheral
neuropathy was significantly associated
with falling and repetitive falls.
Falls have been linked to instabil-
ity by others (35-39), and the awareness
of the problem of falls among the elderly
is presently heightened because the se-
quelae of falls are becoming increasing
causes of morbidity and mortality and an
increasing burden on the health care sys-
tem (29,40-42). Based on our findings, it
is possible that diabetic neuropathic
ataxia is a significant contributing factor
to injuries from falls in the elderly, and
this clearly deserves further investigation.
In this study, we investigated the effects of
distal symmetrical diabetic polyneuropa-
thy on posture in a very simple situa-
tion—quiet stance. It is likely that recov-
ery from a disturbing force (43,44)
during standing would be even more af-
fected and that gait and ability to recover
from slipping or tripping may also be al-
tered.
Association between instability and
sensory and physical characteristics
From the regression analyses performed
on the data, instability observed among
the DM-NP group was largely related to
sensory neuropathy and aging (the com-
bined R2 of Eq. 1 was 63.3%) and not
significantly related to diabetes or any
other physical or functional characteris-
tics assessed in this study (Eq. 1). Specif-
ically, the effects of mild ankle muscle
weakness and vision deficits in the group
with neuropathy did not confound our
results. Among the measures of neuropa-
thy, the best predictors of instability were
the three quantitative sensory tests. It is
noteworthy that stability was very poorly
related to the electrophysiological tests, a
significant point in favor of the continued
use of quantitative sensory tests to assess
sensory neuropathy. The increase in pos-
tural instability related to aging predicted
in Eq. 1 has been previously documented
(45). It is of note, however, that using Eq.
1, a 30-year-old diabetic patient with sig-
nificant neuropathy (off-scale measure-
ment of vibration and perception to
Prediction of instability from age
and single measurements of
neuropathy
A secondary hypothesis for this study was
that a particular measure of neuropathy
may be better associated with instability
than all others. To test this hypothesis and
to further simplify the prediction of insta-
bility, three equations were developed,
each making use of age and a single mea-
sure of neuropathy (Eqs. 2, 3, and 4).
Each of these three equations accounts for
a similar amount of variance, with R? val-
ues of 53.6, 54.7, and 51.9%, respec-
tively. The similarity in the R2 values sup-
ports the use of any one of these three
quantitative sensory tests for prediction
of instability.
Tables 6-8, developed from these
equations, represent an attempt to pro-
vide a quick, clinically useful guide for
prediction of instability based on these
single measures of neuropathy. We recog-
nize that these predictions are based on a
small number of patients, and yet we feel
they are useful. For all three measures of
neuropathy, the general rule appears to
be that at <50 years of age, very severe
neuropathy (such as that represented by
off-scale measurements for both monofil-
ament testing and VPT) is required to
cause significant instability. However,

DIABETES CARE, VOLUME 17, NUMBER 12, DECEMBER 1994 1419

Posture and diabetic sensory neuropathy

above this age, even mild neuropathy will 10. Sosenko JM, Kato M, Soto R, Bild DE:
Acknowledgments—This work was per- Comparison of quantitative sensory-
render the patient's postural stability ab-
formed at the Center for Locomotion Studies threshold measures for their association
normal, and severe neuropathy results in
(CELOS) at Penn State University and was with foot ulceration in diabetic patients.
dramatic deficits in stability. Table 8 is of
partially supported by a grant from the Amer- Diabetes Care 13:1057-1061, 1990
special interest because ankle JMPT is the
ican Diabetes Association.
only test that allows the establishment of 11. Simoneau GG, Ulbrecht JS, Becker MB,
The results were first presented in abstract
an abnormally high level of sway in the Derr JA, Cavanagh PR: Design and pre-
form at the 1992 Annual Meeting and Scien-
younger population. This is no doubt due liminary testing of a device to quantify
tific Sessions of the American Diabetes Associ-
to the fact that it is the only test of neu- ankle joint proprioceptive function dur-
ation, San Antonio, Texas.
ropathy used here that does not have a ing weightbearing. In Posture and Gait:
finite upper limit. Control Mechanisms. Proc Xlth Interna-
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