Allet 2012
Allet 2012
Allet 2012
ABSTRACT: Introduction: Changes occur in muscles and at the hip is of greater importance to equilibrium
nerves with aging. In this study we explore the relationship in the frontal plane than control at the ankle. For
between unipedal stance time (UST) and frontal plane hip and
ankle sensorimotor function in subjects with diabetic neuropa- example, a whole-body inverted pendulum model
thy. Methods: UST, quantitative measures of frontal plane ankle of medial–lateral control during human walking
proprioceptive thresholds, and ankle and hip motor function suggests that the hip exerts the primary influence,
were tested in 41 subjects with a spectrum of lower limb senso-
rimotor function ranging from healthy to moderately severe dia- and that minor errors in hip motion are compen-
betic neuropathy. Results: Frontal plane hip and ankle sated by adjustments at the subtalar joint.12 Simi-
sensorimotor function demonstrated significant relationships larly, a second model demonstrated that foot
with UST. Multivariate analysis identified only composite hip
strength, ankle proprioceptive threshold, and age to be signifi- placement in the frontal plane, which is regulated
cant predictors of UST (R2 ¼ 0.73), explaining 46%, 24%, and by hip abduction/adduction, was the most efficient
3% of the variance, respectively. Conclusions: Frontal plane hip method for controlling frontal plane balance while
strength was the single best predictor of UST and appeared to
compensate for less precise ankle proprioceptive thresholds. walking.13 Other studies have provided experimen-
This finding is clinically relevant given the possibility of strength- tal support for these models and demonstrated the
ening the hip, even in patients with significant peripheral neu- importance of hip frontal plane strength for bal-
ropathy.
Muscle Nerve 45: 578–585, 2012 ance control in elderly subjects when they negoti-
ate obstacles14 and for fall prevention.15,16
However, no study has described the relationship
Quantitative and qualitative changes occur in between lower limb afferent and efferent neuromus-
muscles and nerves with aging.1 These changes
cular capacities relevant to frontal plane control in
include a decrease in the number of alpha moto-
older subjects with a demonstrably significant range
neurons, reduced motoneuron excitability, and loss
of peripheral neurological function. For example,
of type II muscle fibers, leading to decreased muscle
none of the aforementioned biomechanical models
mass and slower muscle response latencies.2 Such
or experimental studies addressed the role of distal
changes, which adversely affect motor control and
balance in older persons, are even more marked afferent function (i.e., ankle proprioception). Simi-
among older persons with peripheral neuropathy larly, evaluations of lower limb neuromuscular
(PN), a common complication of diabetes mellitus. capacities associated with balance deficits in subjects
In such patients, the neuropathy is usually length-de- with PN studied either ankle proprioception5 or
pendent and results in distal sensorimotor dysfunc- ankle joint motor function,17,18 but not both, and no
tion of varied severity. As a result, diabetic patients study has evaluated hip motor function in this high-
have decreased balance,3–6 altered gait,7 and risk population.
increased fall risk,8,9 compared with healthy controls. Unipedal stance time (UST) is a convenient
Control of frontal plane stability is particularly clinical measure of balance that evaluates frontal
important given that lateral falls are associated plane postural control. It is the most challenging
with hip fractures in older adults.10,11 Biomechani- activity within the widely used Berg Balance
cal models and human studies suggest that control Scale.19 Moreover, UST is associated with
frailty,20,21 PN,6,22 activity level,23 and falls in older
Abbreviations: BMI, body mass index; COM, center of mass; MVC, persons with PN24 and without PN,25,26 and
maximum voluntary contraction; MDNS, Michigan Diabetes Neuropathy decreases markedly with age.27,28 Therefore, our
Score; PN, peripheral neuropathy; RTD, rate of torque development; UST,
unipedal stance time objective was to elucidate the relationships
Key words: age, balance, diabetic neuropathy, muscle strength, between UST and lower limb neuromuscular
proprioception
Correspondence to: L. Allet, University of Applied Sciences of Western capacities relevant to frontal plane postural control
Switzerland (HEDS) Dpt of Physiotherapy, Rue des Caroubiers 25, in older subjects with a spectrum of neuromuscu-
CH1227 Carouge, Switzerland; e-mail: [email protected]
lar function. The primary hypothesis was that hip
V
C 2011 Wiley Periodicals, Inc.
Sensorimotor Function and Balance MUSCLE & NERVE April 2012 581
Table 3. Regression model.
95% CI bound
2
Model R R Dependent variable US* Lower Upper t P
1 0.676 0.456 Hip MVC* 460.945 290.881 631.010 5.497 0.000
2 0.834 0.696 Hip MVC* 386.485 254.224 518.745 5.932 0.000
Ankle proprioception 4.179 5.794 2.564 5.254 0.000
3 0.856 0.733 Hip MVC* 339.517 205.974 473.060 5.167 0.000
Ankle proprioception 3.867 5.433 0.300 5.017 0.000
Age 0.265 0.515 .015 2.156 0.038
dorsiflexors),36 whereas mediolateral balance is with previous work5 in which ankle inversion/ever-
controlled via frontal plane motion at the hip.36 sion proprioceptive thresholds explained approxi-
Other studies demonstrated significant correlations mately half the variance in UST (R2 ¼ 0.514) in
between hip abduction RTD and performance of
reactive and voluntary frontal plane balance in
older adults.37 A study of slips noted that older
persons used frontal plane mechanisms for recov-
ery, whereas young subjects did not.38 One way to
interpret the importance of abductor and adductor
muscles with regard to unipedal stance is to sug-
gest that a co-contraction of these muscles allows a
transient, voluntary increase in hip rotational stiff-
ness. Given that an inverted pendulum is a com-
monly used model for human standing balance,
this stiffness creates a longer pendulum, which
requires more time to fall than a shorter pendu-
lum. As a result, there is more time available for
postural adjustments, which renders the task of
one-legged balance less challenging.39 However,
once balance is disturbed, it is likely that the avail-
ability of a rapid rate of strength development
would be more important, given that balance resto-
ration occurs within fractions of a second.34
The independent contribution of ankle pro-
prioception for balancing on one leg is consistent
582 Sensorimotor Function and Balance MUSCLE & NERVE April 2012
older subjects with a range of peripheral neurolog- pensate for distal sensory impairment at the ankle.
ical function. More precise ankle proprioceptive Given the fact that the majority of polyneuropa-
thresholds may reduce the lateral distance that the thies are distal, this strategy can be used in a large
center of mass (COM) can travel prior to detec- proportion of patients with lower limb neuromus-
tion. Early detection of a displaced COM would cular disease. Conversely, persons with PN and
then require only moderate strength that a major- proximal weakness that cannot be improved may
ity of older persons likely possess. In contrast, less be best served by an assistive device, appropriate
precise ankle proprioception would require greater upper limb strengthening, environmental modifi-
intensity of motor function for appropriate reposi- cation, and instruction.44,45 Finally, it should be
tioning of the COM. Supporting this explanation, noted that diminished UST need not be viewed as
healthy subjects demonstrate increased center-of- a natural consequence of aging, despite research
pressure velocities when the plantar aspect of the that has noted an inverse association between the
foot is anesthetized, which is consistent with the two and even one study suggesting age-adjusted
greater motor function requirement.40 norms for UST.27,46 Instead, a decreased UST
Ankle motor function did not show a signifi- should, in the absence of an obvious musculoskel-
cant independent influence on UST, despite the etal and/or central neurological disorder, be con-
fact that ankle inversion and eversion rates of tor- sidered a function of diminished lower limb neuro-
que generation explained approximately 40% and muscular competence.
25%, respectively, of its variance. These findings A recent study47 found that improvements in
are consistent with those of Gutierrez et al.,17 who trunk extension endurance, but not lower limb
found that ankle inversion RTD explained over strength or power, were independently associated
50% of the variance in UST (R2 ¼ 0.575). In con- with clinically meaningful change in balance in
trast, ankle maximum isometric inversion and ever- older adults. However, that protocol measured
sion strengths each explained only 12% of UST. lower limb strength by means of a seated double-
When observing subjects successfully balancing on leg press maneuver, and thus sagittal plane
one foot there are rapid postural adjustments in strength of multiple muscle groups within the
ankle inversion and eversion as the center of pres- lower limbs was simultaneously measured. This
sure is quickly manipulated to control the move- technique contrasts with that of our study, which
ments of the whole-body COM. The rapid speed measured frontal plane sensorimotor functions dis-
with which these changes occur in the subject who cretely at the hip and ankle. Therefore, although
can reliably stand on one foot is consistent with trunk extension endurance may be more impor-
ankle maximum RTD being an important motor tant to balance than to sagittal plane lower limb
function for the maintenance of unipedal stance. strength, the relative importance of trunk endur-
These findings are in line with other studies show- ance and lower limb frontal plane sensorimotor
ing that the ability of the lower limbs to create function with reference to balance has yet to be
force quickly is of greater importance than the explored.
total force a muscle group can generate.41,42 The strengths of this study include the fact that
Although highly correlated with UST, ankle RTD sensory and motor control mechanisms were quan-
had no independent influence on UST in the pres- tified simultaneously in subjects with a spectrum of
ence of ankle proprioception and hip strength. neuromuscular dysfunction. The correlations and
This is of clinical interest, given the challenge of multiple regression analyses were unusually strong.
strengthening distal musculature in PN subjects. Given the complexity of any human behavior it is
Given the established relationships between a remarkable that just two lower limb neuromuscular
diminished UST and frailty, activity level, and falls, characteristics explain nearly 75% of UST. Limita-
strategies to increase UST have clinical relevance. tions include the fact that UST is unlikely to per-
There is no clear evidence that ankle propriocep- fectly reflect a variety of relevant mobility charac-
tive thresholds can be improved by therapeutic teristics, such as gait speed and the ability to
exercise,43 and recent work has shown that an recover from a perturbation while walking. The
ankle orthosis, which decreased the temporal and lower limb sensorimotor function(s) responsible
spatial variability of neuropathic gait on an irregu- for these deserves further attention. In addition,
lar surface, did not improve ankle proprioceptive only frontal plane neuromuscular functions were
thresholds.35 Given these findings, frontal plane evaluated. It is possible that sagittal plane muscle
hip strengthening appears the best strategy for strength also influences UST. It should also be
improving UST. This strengthening should be pur- noted that the measurements of ankle motor func-
sued most aggressively in those with decreased dis- tion assumed the ankle’s center of rotation to be
tal afferent neurological function, as it appears midway between the malleoli. This was an estima-
that increased frontal plane hip strength can com- tion and therefore represents a study limitation,
Sensorimotor Function and Balance MUSCLE & NERVE April 2012 583
but an important one to note given that ankle 12. MacKinnon CD, Winter DA. Control of whole body balance in the
frontal plane during human walking. J Biomech 1993;26:633–644.
motor function was not identified as an independ- 13. Bauby CE, Kuo AD. Active control of lateral balance in human walk-
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14. Chou L, Kaufman K, Brey R. Correlation between muscle strength
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an open chain technique, would have led to an al- 46th annual meeting of the Orthopaedic Research Society, Orlando,
Florida; 2000; p 315.
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