Archives of Gerontology and Geriatrics 51 (2010) 64–67
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Archives of Gerontology and Geriatrics
journal homepage: www.elsevier.com/locate/archger
Effect of physical exercise and age on knee joint position sense
Fernando Ribeiro a,b,*, José Oliveira a
a
b
Research Centre in Physical Activity, Health and Leisure, Faculty of Sport, University of Porto, Rua Dr. Plácido Costa, 91, P-4200.450 Porto, Portugal
Physiotherapy Department, Health School of Vale do Sousa, Rua Central de Gandra, 1317, P-4585.116 Gandra PRD, Portugal
A R T I C L E I N F O
A B S T R A C T
Article history:
Received 3 April 2009
Received in revised form 17 July 2009
Accepted 20 July 2009
Available online 27 August 2009
This study aimed to test the hypotheses that knee position sense declines with age and that regular
exercise can attenuate that decline. This cross-sectional study encompassed 69 older and 60 young
adults divided in four groups (exercised-old, N = 31; non-exercised-old, N = 38; exercised-young, N = 35;
non-exercised-young, N = 25) according to chronological age and exercise practice in the past year. Knee
position sense was measured by open kinetic chain technique and active positioning and is reported as
the absolute and relative angular error. Knee angles were determined by computer analysis of videotape
images using the Ariel Performance Analysis System. Compared to their non-exercised counterparts,
exercised-young and -old showed lower absolute and relative angular errors. The absolute (1.62 0.718)
and relative errors (0.02 1.658) for exercised-young were lower than all other groups (p < 0.001). The
absolute and relative errors of exercised-old (4.27 2.498 and 5.51 3.428) were similar to non-exercisedyoung (4.74 2.678 and 4.18 3.408). The non-exercised-old exhibited higher absolute (9.35 4.348) and
relative errors (9.73 5.158) than all other groups (p < 0.001). The present data indicates that age has
deleterious effects on knee position sense although regular exercise can attenuate that age-related decline.
ß 2009 Elsevier Ireland Ltd. All rights reserved.
Keywords:
Proprioception
Older adults
Exercise
Knee position
1. Introduction
The aging process is accompanied by a decline in neuromuscular control, motor coordination, balance and consequently
increasing the risk to falls (Shaffer and Harrison, 2007). The
proprioceptive acuity is a central piece of the above-mentioned
abilities. Proprioception is the afferent information to the central
nervous system provided by specialized nerve endings called
mechanoreceptors that contributes to the conscious and unconscious sensation, automatic control of movement, posture, and
balance. Regarding balance, proprioception is paramount to its
sensory control (Ribeiro and Oliveira, 2007); for instance, the
balance of old aged subjects relies more on proprioception than on
vision (Colledge et al., 1994). In older adults, the decline in lower
limb proprioception is of great concern since it has been related to
balance deficits, which consequently increase the susceptibility to
fall (Sorock and Labiner, 1992; Lord et al., 1999). In addition, the
decrease of joint proprioception could lead to abnormal joint
biomechanics during functional activities which could lead to, over
a period of time, degenerative joint disease (Skinner, 1993). Hence,
it is important to develop and implement strategies to attenuate
* Corresponding author at: Research Centre in Physical Activity, Health and
Leisure, Faculty of Sport, University of Porto, Rua Dr. Plácido Costa, 91, P-4200.450
Porto, Portugal. Tel.: +351 225 074 773; fax: +351 225 500 689.
E-mail address: [email protected] (F. Ribeiro).
0167-4943/$ – see front matter ß 2009 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.archger.2009.07.006
the age-related decline in proprioception. So far, the only strategy
that seems to retain/regain joint proprioception in old age subjects
is regular physical exercise. However, the beneficial effect of
regular exercise on lower limb proprioception of older adults is not
consensual (Tsang and Hui-Chan, 2003; Xu et al., 2004; Schmitt
et al., 2005; Li et al., 2008). It seems that only the regular practice of
forms of exercise emphasizing awareness of joint position and
movement, such as tai chi, and not the most common exercises
practiced in the Western society, such as swimming and running,
improves proprioception. The purpose of the present study is to
examine the effects of age and regular exercise on knee
proprioception assessed through measurement of joint position
sense.
2. Methods
2.1. Subjects
A total of 69 older male adults (mean age = 72.2 5.0 years) and
60 young male adults (mean age = 20.6 3.0 years) voluntarily
participated in the present study. The older adults were noninstitutionalized, presented no sign of loss of autonomy, were independent in the daily living activities, and had to have chronological age
65 years. All subjects were healthy, with no known pathology of the
central or peripheral nervous system, neuromuscular deficits, or
degenerative joint diseases (e.g., osteoarthritis or rheumatoid
arthritis), and none had had orthopedic disorders of the lower back
F. Ribeiro, J. Oliveira / Archives of Gerontology and Geriatrics 51 (2010) 64–67
Table 1
Participant characteristics, mean S.D.
N
Age (years)
Weight (kg)
Height (cm)
Exercisedyoung
Non-exercisedyoung
Exercisedold
Non-exercisedold
35
20.3 3.2
70.4 5.8
178.0 5.1
25
20.9 2.9
70.4 4.5
176.9 5.3
31
72.1 4.8
72.5 11.8
161.4 8.1
38
72.2 5.2
71.0 10.0
162.0 8.5
or lower limbs during the preceding year. Normal knee range of
motion was observed in all subjects.
Four groups were defined according to the chronological age
and the practice of regular physical exercise in the past year. The
characteristics of the groups are presented in Table 1. Exercisedold subjects were participants in organized exercise programs
mainly composed by aerobic, flexibility and strength exercises.
Exercised-young subjects practiced soccer or volleyball. To be
admitted to one of these two exercised groups, a frequency of three
times a week for at least 45–60 min must be achieved. Nonexercised-old and non-exercised-young subjects had not participated in any organized physical exercise programs, and they were
not involved in any regular self-exercise activities in the past year.
Within each age cohort, no significant difference was observed
concerning mean age, weight and height.
The dominant lower limb was tested on all subjects. Leg
dominance was established by asking the subject which leg they
preferred to use to kick a ball. The subjects were familiarized with
the experimental protocol and apparatus, and they provided written
consent for participation. The experiment was approved by the local
Ethics Committee, according to the Declaration of Helsinki.
2.2. Evaluation of joint position sense
Joint position sense, the ability to replicate a target joint position,
was evaluated using an open kinetic chain technique and active knee
positioning as previously described (Ribeiro et al., 2007, 2008). The
subjects were seated in a comfortable position (with the hip at an
angle of 808 of flexion), with the legs hanging freely, and blindfolded
to block visual input. Four reflective markers were fixed with
double-sided adhesive tape to the skin of the lateral thigh and leg:
over the apex of the greater trochanter, iliotibial tract level with the
posterior crease of the knee when flexed to 808, neck of the fibula,
and prominence of the lateral malleolus. Then, passive positioning
by the examiner was performed by extending the knee, at
approximately 108/s, from the starting position of 908 of flexion
to a flexion angle between 408 and 608. The subject maintained the
position actively for 3 s without manual contact from the examiner
in order to identify the test position. After that, the examiner
replaced the leg to the starting position. The subject was then
instructed (upon the command ‘‘reposition’’) to actively reproduce
the test position. The subject then returned to the position perceived
as the test position and reported ‘‘target’’ to the examiner. This
position was held for 3 s, and on the command ‘‘return’’ the subject
returned to the initial position. One test position was examined. Each
participant performed three consecutive trials trying to reproduce
the test position to obtain a realistic sample of joint position sense
accuracy and reliability for that test position. The test and the
response positions were recorded with a video camera. The tripodmounted video camera was positioned 5 m from the participant, at
the same level of the knee joint, and then manually focused on the
field of view. The camera was in the sagittal plane. The same video
camera was used over the experimental period. Natural vertical and
horizontal lines in the videotaped environment were aligned
parallel to the horizontal and vertical edges of the viewfinder to
minimize camera tilt. Knee angles were determined by computer
65
analysis of the videotape images of the joint using the twodimensional automatic digitizing module of the Ariel Performance
Analysis System software (Ariel Dynamics, CA, USA). Each test or
response position was determined as the average of seven
consecutive knee angles digitized at 50 Hz from the videotape view
of each position.
Knee joint position sense is reported as: the absolute angular
error (defined as the absolute difference between the test position
and the position reproduced by the subject), which represents
accuracy without directional bias, and the relative angular error
(the signed arithmetic difference between a test and response
position), which represents accuracy with directional bias.
The reliability of the chosen method of measuring JPS was
established in 10 subjects (age 21–26 years) tested on two sessions
separated by 5 days. The results demonstrated good to excellent
test–retest reliability with intraclass correlation coefficients = 0.92, ranging from 0.71 to 0.98.
2.3. Statistical analysis
All data were analyzed using SPSS version 16.0 (SPSS Inc.,
Chicago, IL) statistical software. Descriptive statistics were used to
calculate the mean and standard deviation. One-way analysis of
variance was performed to compare the mean values of age,
weight, height, absolute angular error, and relative angular error
for the four groups. Post hoc comparisons were performed with the
Bonferroni test. Statistical significance was set at a = 0.05 for all
statistical comparisons.
3. Results
Mean performances from all three reposition trials of the testing
session are shown in Table 1. Compared to their non-exercised
counterparts, both exercised-young and -old subjects showed lower
absolute and relative angular errors. The mean absolute and relative
angular errors for exercised-young subjects were significantly lower
than all other groups. In contrast, non-exercised-old subjects
showed higher absolute and relative angular errors than the other
three groups. Interestingly, the mean absolute and relative angular
errors for the exercised-old group were not different from the group
of non-exercised-young subjects. The relative error showed directional bias into the extension movement. With the exception of
exercised-young group, in all the other groups there was a trend to
overestimate the test position. The subjects showed a trend,
significantly higher in the non-exercised-old group, to reproduce
lower knee flexion angles than the pre-selected flexion angle
determined by the examiner (Table 2).
4. Discussion
This study compared knee joint position sense between
younger and older groups of exercised and non-exercised subjects.
Table 2
Comparisons of joint position sense values in the four groups, mean S.D.
Exercised-young
Non-exercisedyoung
Exercised-old
Non-exercisedold
Absolute angular
error (8)
1.62 0.71
4.74 2.67*
4.27 2.49*
9.35 4.34*,#
Relative angular
error (8)
0.02 1.65
4.18 3.40*
5.51 3.42*
9.73 5.15*,#
*
Significantly different from exercised-young (p < 0.001).
Significantly different from non-exercised-young and
(p < 0.001).
#
exercised-old
66
F. Ribeiro, J. Oliveira / Archives of Gerontology and Geriatrics 51 (2010) 64–67
The results of the present study point out (i) a significant
deterioration in knee position sense with age and (ii) an
attenuation of the age-related decline in knee position sense by
regular physical exercise.
4.1. Knee position sense and age
Previous studies reported that aging is related to the decline of
several aspects of proprioceptive sensitivity, namely the decrease
of joint position sense and the increase of movement detection
threshold. Collectively the studies that assessed knee proprioception, despite using different methodologies, found evidence to
support the hypothesis that knee position sense declines with age
(Pai et al., 1997; Petrella et al., 1997; Hurley et al., 1998). Our
results are in agreement with the results of those studies, as our
data indicates that the acuity of knee position sense is two times
higher in young subjects comparatively to their old counterparts.
Indeed, older adults showed a reduced ability to discriminate static
knee angles combined with a larger variation in discriminative
ability (Table 2).
Since proprioception involves peripheral and central components, the observed age-related deterioration in joint position
sense may be elucidated by age-related changes in both central
and peripheral components. The relative contribution of each
component is not established. At peripheral level the aging process
induces several modifications within articular, cutaneous and
muscle receptors (for Ref.: Ribeiro and Oliveira, 2007). One should
focus the rationalization in the muscle spindles modifications, as
position sense acuity is, to a large extent, dependent upon muscle
spindle activity (Proske, 2005) and the reproduction tests used to
assess joint position sense in our study were actively performed in
the intermediate range of knee flexion where the input of muscle
spindles is thought to be the major source mediating sense of knee
position. Several studies had shown anatomical and physiological
changes in muscle spindle with age, namely a decrease in the
dynamic response of the muscle spindle primary afferents to ramp
stretch (Miwa et al., 1995), a decrease in the total number of
intrafusal muscle fibers and nuclear chain fibers per spindle, and an
increase in spindle capsule thickness (Miwa et al., 1995; Liu et al.,
2005). Additionally, aging leads to deficits in the processing of
sensory input due to myelin abnormalities, axonal atrophy and
declined nerve conduction velocity (Verdu et al., 2000).
The central component of proprioception, e.g. the integration of
the sensory input, is also affect by the aging process. The
conductive function of the central somatosensory pathways is
impaired by the progressive loss of the dendrite system in the
motor cortex (Scheibel et al., 1975; Nakamura et al., 1985), the
decrease in the number of neurons and receptors, and the
neurochemical modifications in the brain (Masliah et al., 1993;
Pakkenberg and Gundersen, 1997; Strong, 1998). Additionally, the
decrease in muscle spindle sensitivity can also result from
supraspinally mediated changes in the gamma drive to the
spindles themselves (Mynark and Koceja, 2001).
not different from their non-exercised counterparts and it is
inferior than proprioception of tai chi practitioners. The present
data suggests that ‘‘usual’’ exercise and not only exercise that puts
a great emphasis on the awareness of joint position and direction,
such as tai chi, is effective to preserve joint proprioception.
It is very important to note that the proprioceptive acuity of
exercised-old subjects was identical to the non-exercised-young
subjects and significantly superior to non-exercised-old subjects,
suggesting that regular exercise may attenuate the age-related
proprioceptive decline. Our data is similar to the results observed
by Pickard et al. (2003) at the hip joint. The authors did not find
significant differences in hip position sense between nonexercised-young subjects and exercised aged subjects.
Several mechanisms by which exercise ameliorates joint
proprioception can be point towards based on the best evidence
available. Since central and peripheral components of proprioception are implicated in the proprioceptive age-related decline, it is
not surprising that they are also both involved in the improvement
of proprioception observed in result of engagement in regular
physical exercise.
At peripheral level exercise induces morphological adaptations
in the muscle spindle. There are adaptations on a microlevel, the
intrafusal muscle fibers could show some metabolic changes, and
on a more macrolevel, the latency of the stretch reflex response
decrease and the amplitude increase (Hutton and Atwater, 1992).
At central level, exercise can modify proprioception through the
modulation of the muscle spindle gain and the induction of plastic
modifications in the central nervous system. During physical
exercise there is an increase in the muscle spindle output through
the g route, hence enhancing proprioception by facilitating its
cortical projection. Thus, regular exercise can increase the muscle
spindle output, which could induce plastic changes in the central
nervous system, such as increased strength of synaptic connections and/or structural changes in the organization and numbers of
connections among neurons (Ashton-Miller et al., 2001). The
demands of regular exercise and more specifically regular and
repetitive afferent inputs from the mechanoreceptors could be able
to induce plastic changes in the cortex hence modifying the cortical
maps of the body over time (increasing the cortical representation
of the joints leading to enhanced joint proprioception) (AshtonMiller et al., 2001).
5. Conclusions
The results from this study suggest that: (i) regular physical
exercise has a positive impact on knee joint position sense both in
younger and older subjects; (ii) age has a deleterious effect on knee
position sense; and (iii) regular physical exercise can attenuate the
age-related decline in knee position sense.
Conflict of interest statement
None.
4.2. Effect of regular physical exercise on knee position sense
References
It is widely acknowledged that regular physical exercise
promotes beneficial effects in many physiologic systems. Regarding proprioception our results support the valuable role of physical
exercise performed on a regular basis in the attenuation of the agerelated decline of knee position sense.
Our results are in agreement with the conclusions drawn by
Petrella et al. (1997), who reported better knee joint proprioception in exercised-old subjects than in non-exercised-old subjects,
and in disagreement with the findings of Xu et al. (2004), who point
towards that knee proprioception of older swimmers/runners is
Ashton-Miller, J.A., Wojtys, E.M., Huston, L.J., Fry-Welch, D., 2001. Can proprioception really be improved by exercises? Knee Surg. Sports Traumatol. Arthrosc. 9,
128–136.
Colledge, N.R., Cantley, P., Peaston, I., Brash, H., Lewis, S., Wilson, J.A., 1994. Ageing
and balance: the measurement of spontaneous sway by posturography. Gerontology 40, 273–278.
Hurley, M.V., Rees, J., Newham, D.J., 1998. Quadriceps function, proprioceptive
acuity and functional performance in healthy young, middle-aged and elderly
subjects. Age Ageing 27, 55–62.
Hutton, R.S., Atwater, S.W., 1992. Acute and chronic adaptations of muscle proprioceptors in response to increased use. Sports Med. 14, 406–421.
Li, J.X., Xu, D.Q., Hong, Y., 2008. Tai chi exercise and proprioception behavior in old
people. Med. Sport Sci. 52, 77–86.
F. Ribeiro, J. Oliveira / Archives of Gerontology and Geriatrics 51 (2010) 64–67
Liu, J.X., Eriksson, P.O., Thornell, L.E., Pedrosa-Domellof, F., 2005. Fiber content and
myosin heavy chain composition of muscle spindles in aged human biceps
brachii. J. Histochem. Cytochem. 53, 445–454.
Lord, S.R., Rogers, M.W., Howland, A., Fitzpatrick, R., 1999. Lateral stability, sensorimotor function and falls in older people. J. Am. Geriatr. Soc. 47, 1077–1081.
Masliah, E., Mallory, M., Hansen, L., DeTeresa, R., Terry, R.D., 1993. Quantitative
synaptic alterations in the human neocortex during normal aging. Neurology
43, 192–197.
Miwa, T., Miwa, Y., Kanda, K., 1995. Dynamic and static sensitivities of muscle spindle
primary endings in aged rats to ramp stretch. Neurosci. Lett. 201, 179–182.
Mynark, R.G., Koceja, D.M., 2001. Effects of age on the spinal stretch reflex. J. Appl.
Biomech. 17, 188–203.
Nakamura, S., Akiguchi, I., Kameyama, M., Mizuno, N., 1985. Age-related changes of
pyramidal cell basal dendrites in layers III and V of human motor cortex: a
quantitative Golgi study. Acta Neuropathol. (Berl.) 65, 281–284.
Pai, Y.C., Rymer, W.Z., Chang, R.W., Sharma, L., 1997. Effect of age and osteoarthritis
on knee proprioception. Arthritis Rheum. 40, 2260–2265.
Pakkenberg, B., Gundersen, H.J., 1997. Neocortical neuron number in humans: effect
of sex and age. J. Comp. Neurol. 384, 312–320.
Petrella, R.J., Lattanzio, P.J., Nelson, M.G., 1997. Effect of age and activity on knee
joint proprioception. Am. J. Phys. Med. Rehabil. 76, 235–241.
Pickard, C.M., Sullivan, P.E., Allison, G.T., Singer, K.P., 2003. Is there a difference in
hip joint position sense between young and older groups? J. Gerontol. A: Biol.
Sci. Med. Sci. 58, M631–M635.
Proske, U., 2005. What is the role of muscle receptors in proprioception? Muscle
Nerve 31, 780–787.
67
Ribeiro, F., Oliveira, J., 2007. Aging effects on joint proprioception: the role of
physical activity in proprioception preservation. Eur. Ver. Aging Phys. Act. 4,
71–76.
Ribeiro, F., Mota, J., Oliveira, J., 2007. Effect of exercise-induced fatigue on position
sense of the knee in the elderly. Eur. J. Appl. Physiol. 99, 379–385.
Ribeiro, F., Santos, F., Gonçalves, P., Oliveira, J., 2008. Effects of volleyball matchinduced fatigue on knee joint position sense. Eur. J. Sport Sci. 8, 397–402.
Scheibel, M.E., Lindsay, R.D., Tomiyasu, U., Scheibel, A.B., 1975. Progressive dendritic
changes in aging human cortex. Exp. Neurol. 47, 392–403.
Schmitt, H., Kuni, B., Sabo, D., 2005. Influence of professional dance training on peak
torque and proprioception at the ankle. Clin. J. Sport Med. 15, 331–339.
Shaffer, S.W., Harrison, A.L., 2007. Aging of the somatosensory system: a translational perspective. Phys. Ther. 87, 193–207.
Skinner, H.B., 1993. Pathokinesiology and total joint arthroplasty. Clin. Orthop.
Relat. Res. 288, 78–86.
Sorock, G.S., Labiner, D.M., 1992. Peripheral neuromuscular dysfunction and falls in
an elderly cohort. Am. J. Epidemiol. 136, 584–591.
Strong, R., 1998. Neurochemical changes in the aging human brain: implications
for behavioral impairment and neurodegenerative disease. Geriatrics 53, S9–
S12.
Tsang, W.W., Hui-Chan, C.W., 2003. Effects of tai chi on joint proprioception and
stability limits in elderly subjects. Med. Sci. Sports Exerc. 35, 1962–1971.
Verdu, E., Ceballos, D., Vilches, J.J., Navarro, X., 2000. Influence of aging on peripheral
nerve function and regeneration. J. Peripher. Nerv. Syst. 5, 191–208.
Xu, D., Hong, Y., Li, J., Chan, K., 2004. Effect of tai chi exercise on proprioception of
ankle and knee joints in old people. Br. J. Sports Med. 38, 50–54.