Effects of Short-Term Cycling on Knee Joint Proprioception in Healthy Young Persons

8/12/2019 Effects of Short-Term Cycling on Knee Joint Proprioception in Healthy Young Persons

1/6

http://ajs.sagepub.com

MedicineAmerican Journal of Sports

2003; 31; 990Am. J. Sports Med.David Roberts, Eva Ageberg, Gert Andersson and Thomas Fridn

Effects of Short-Term Cycling on Knee Joint Proprioception in Healthy Young Persons

http://ajs.sagepub.com/cgi/content/abstract/31/6/990The online version of this article can be found at:

Published by:

http://www.sagepublications.com

On behalf of:

American Orthopaedic Society for Sports Medicine

can be found at:American Journal of Sports MedicineAdditional services and information for

http://ajs.sagepub.com/cgi/alertsEmail Alerts:

http://ajs.sagepub.com/subscriptionsSubscriptions:

http://www.sagepub.com/journalsReprints.navReprints:

http://www.sagepub.com/journalsPermissions.navPermissions:

http://ajs.sagepub.com/cgi/content/abstract/31/6/990#BIBLSAGE Journals Online and HighWire Press platforms):

(this article cites 29 articles hosted on theCitations

2003 American Orthopaedic Society for Sports Medicine. All rights reserved. Not for commercial use or unauthorized distribution.at Liverpool John Moores University on February 8, 2008http://ajs.sagepub.comDownloaded from
http://www.aossm.org/http://ajs.sagepub.com/cgi/alertshttp://ajs.sagepub.com/cgi/alertshttp://ajs.sagepub.com/subscriptionshttp://ajs.sagepub.com/subscriptionshttp://ajs.sagepub.com/subscriptionshttp://www.sagepub.com/journalsReprints.navhttp://www.sagepub.com/journalsReprints.navhttp://www.sagepub.com/journalsReprints.navhttp://www.sagepub.com/journalsPermissions.navhttp://www.sagepub.com/journalsPermissions.navhttp://ajs.sagepub.com/cgi/content/abstract/31/6/990#BIBLhttp://ajs.sagepub.com/cgi/content/abstract/31/6/990#BIBLhttp://ajs.sagepub.com/http://ajs.sagepub.com/http://ajs.sagepub.com/http://ajs.sagepub.com/http://ajs.sagepub.com/cgi/content/abstract/31/6/990#BIBLhttp://www.sagepub.com/journalsPermissions.navhttp://www.sagepub.com/journalsReprints.navhttp://ajs.sagepub.com/subscriptionshttp://ajs.sagepub.com/cgi/alertshttp://www.aossm.org/


2/6

Effects of Short-Term Cycling on KneeJoint Proprioception in HealthyYoung Persons

David Roberts,* MD, Eva Ageberg, RPT, MSc, Gert Andersson, MD, PhD, andThomas Friden,* MD, PhD

From the Departments of *Orthopedics, Rehabilitation, and Neurophysiology, UniversityHospital Lund, Lund, Sweden

Background: Criteria are needed for measuring the effects of exercise and fatigue on proprioception.Purpose: To measure knee joint proprioception in healthy subjects before and after exercise and to establish a reference forfurther comparisons of patients with knee injuries.Study Design: Controlled laboratory study.Methods:We tested proprioception in the knees of 24 healthy subjects with a mean age of 24 years and median Tegner scoreof 5. Subjects were tested to estimate their thresholds for detecting slow passive motion, from starting positions of 20and 40before and after cycling on an ergometer bicycle until the pulse rate reached a steady state level and they reached a score of14 to 17 on Borgs Ratio of Perceived Exertion scale.Results:After cycling, significantly higher threshold values were found for perception of movement toward flexion from both 20and 40. No significant differences were seen in measurements of movement toward extension.Conclusions: Knee joint proprioception seems to be impaired by exercise or training.Clinical Relevance: This impairment may lead to defective dynamic stabilization of the joint, leading to an increased risk ofinjuries.

2003 American Orthopaedic Society for Sports Medicine

Stability of the knee joint depends on passive soft tissuerestraints, joint geometry, compressive forces, cartilagefriction, and tension in the surrounding muscles.15 It hasbeen shown that activity in the muscle spindles is influ-enced, via gamma motoneurons, by joint and ligamentreceptors.15,16,29,32 These receptors are located in differ-ent joint structures, such as the capsule, menisci, collat-

eral ligaments, and cruciate ligaments and contribute tothe overall proprioception of the knee.1417,32 The aim isto maintain balance and control of limb movements toattain optimal stability and minimize the risk of injury inany situation.12,16 This balance and control also requiresinput from receptors in other joints, muscles, and skin, aswell as from visual and vestibular information.8,15 Fatigu-ing exercise increases joint laxity24,31,33,34,36 and modi-

fies the afferent information from the muscles via chemi-cal agents such as lactic acid, which may affect jointstability.5,8,15,25,26

Skinner et al.30 found a significantly poorer ability toreproduce a given change in joint angle after fatigue, asdid Lattanzio et al.20 However, Marks and Quinney23

noted no change in subjects ability to reproduce angles

after exercise. Skinner and colleagues

30

reported that thethreshold for detection of passive movement in the kneejoint did not change significantly after fatigue. Exercise,without fatigue, has been shown to improve the positionsense in active positioning measurements.3

As in studies of proprioception in ACL-deficient knees,the lack of criteria for measurements makes the resultsdifficult to interpret and compare.811,27,28 Therefore,more studies are needed to determine possible effects ofvarious types of exercise and fatigue on proprioceptionand to arrive at standardized measurements for estimat-ing knee joint proprioception. The aims of this study wereto 1) measure knee joint proprioception in healthy personsbefore and after a short period of exercise with methods

Address correspondence and reprint requests to David Roberts, MD,Department of Orthopedics, University Hospital Lund, S-221 85 Lund,Sweden.

No author or related institution has received any financial benefit fromresearch in this study. See Acknowledgments for funding information.

0363-5465/103/3131-0990$02.00/0THEAMERICANJOURNAL OFSPORTSMEDICINE, Vol. 31, No. 6

2003 American Orthopaedic Society for Sports Medicine

990

http://ajs.sagepub.com/http://ajs.sagepub.com/http://ajs.sagepub.com/http://ajs.sagepub.com/


3/6

that have been shown in our previous studies to be both

sensitive and reproducible,811,27,28 and 2) establish a

reference point for further comparisons of patients with

knee injuries.

MATERIALS AND METHODS

Twenty-four healthy young persons, mainly students at

the University Hospital in Lund, were tested. Their mean

age was 24 years (range, 20 to 32), and 13 were women.

Most of them participated in various sports. Their median

score on the Tegner activity scale was 5 (range, 2 to 9),

equal to strenuous work or leisure time sports such as

running on uneven ground about twice a week.35 The

subjects had no history of major orthopaedic lesions or

general diseases that would interfere with peripheral pro-

prioception. The Research Ethics Committee at Lund Uni-

versity Hospital approved the study, and all subjects gave

their written informed consent to participate.

Proprioception Test

Before exercise we measured proprioception on a specially

designed apparatus consisting of a platform on the floor

(Fig. 1). Mounted at one end was an electric motor with a

wire connected to a movable T-shaped sled with a plastic

splint attached to it for fixation and positioning of the

lower limb and foot. A metal bar in the center of the

platform fixed the sled, and a pull by the wire in either

direction made it turn like the hand of a clock along the

natural arc of extension or flexion of the knee. The arrow-

shaped tip of the sled pointed to an analog scale to record

movements in increments of 0.25. The use of ball bear-

ings allowed movements with little friction. The subjectlay in the lateral decubitus position, with the lower foot in

the plastic splint. The splint supported the posterolateral

part of the lower leg but also had a slight anterior curve.

The oversized construction allowed for differences in the

girth of the lower leg. Two bars mounted on the platform

served as guides for placing the thigh and trunk in a

standard position, with the hip joint semiflexed. The knee

joint was carefully positioned in the rotator center. Tape

marks on the surface allowed proper positioning of the

knee in the different starting positions of knee joint flex-

ion: 20 and 40. The upper thigh and hip rested on arubber pillow (which could be adjusted for different

heights, due to more extreme varus/valgus angulations),and pillows were also placed under the back to help the

subject relax during the test. Care was taken to eliminate

any external stimuli to limb movement except those from

the knee joint and surrounding structures. All subjects

wore short pants and thick woolen socks, and the knee had

no contact with the underlying surface to minimize cuta-

neous sensations during the tests. Visual control of the leg

was eliminated by the subjects position, and auditoryimpulses were prevented during the threshold trial by use

of earmuffs and by playing a tape recording that imitated

the sound of a motor.

The threshold measurements were made of movements

of the knee toward extension and flexion from two starting

positions, 20 and 40. The subjects were asked to closetheir eyes, concentrate on their knee, and respond when

they felt any sensation of movement, changed position, or

anything going onin their knee. The tape recorder wasthen turned on, and, with a delay of 5 to 15 seconds, the

motor started to move the leg with a calibrated angular

velocity of 0.5 deg/sec in the knee. When the subjects

responded, the motor was stopped, and the movement was

registered in degrees. The median value of three consec-

utive trials was used for statistical analysis.

The different starting positions were chosen to bewithin the working range of the knee during ordinary

weightbearing activities or training. Because range of mo-

tion may differ between individual subjects, the most ex-

treme joint positions were excluded. Thus, tensions in the

muscles, capsule, and ligaments were kept below high

levels, and more variable tissue tensions between individ-

ual subjects were avoided, so that the subjects could relax

without having their leg forced into maximum extension.

A slow speed was chosen to ensure that the subjects

could not detect a sudden onset of motion and to make

testing more difficult than if a higher speed had been

used.11 Because the subjects had been placed in a lateral

decubitus position, comparisons between flexion and ex-

Figure 1. The setup for proprioception testing.

Vol. 31, No. 6, 2003 Effects of Short-Term Cycling on Knee Joint Proprioception 991



4/6

tension could be made without any uncontrolled effect of

gravity.11

The tests were made on both the left and the right legs

by shifting the apparatus arrangement from one side of

the platform to the other. This type of apparatus has been

used in previous investigations.811,27,28 No statistical

differences were found between two measurements with

an interval of 1 month when subjects in a previous control

group were measured,11 as seen in Table 1. The standard

error of the mean was calculated for all the measurements

and ranged between 0.04 and 0.11.

Exercise Protocol

A bicycle ergometer was used to exercise the subjects. The

aim was not for the subjects to perform strenuous exercise

causing extreme fatigue but to approximate the level of

normal leisure sports such as jogging, aerobics, or tennis.

The subjects wore a heart-rate monitor during the entire

trial. The load on the bicycle was first adjusted to fit the

subjects approximate ability by asking whether it was toolight or too heavy. Subjects were asked to cycle energeti-

cally for 5 to 10 minutes with a constant pedaling speed of

60 revolutions per minute. The median effect was 150 W

(range, 100 to 200), equal to 900 kpm/min. The initial

pulse rate before cycling was a mean value of 98 beats per

minute (range, 61 to 152). Some subjects had rather high

initial pulse rates; this may have reflected high mental

tension and nervousness among them because they were

unused to testing situations, as some commented. When

the clock was started, they began to cycle. Their pulse rate

was taken every minute. They were asked to estimate

their level of exhaustion on Borgs Ratio of Perceived Ex-

ertion (RPE) scale,2

which ranges from 6 to 20; 6 is noexertion at all,13 is somewhat hard,15 is hard,17 isvery hard, and 20 is maximal exertion. This scale isclosely related to physiologic variables affected by exer-

tion, such as heart rate and blood lactate concentration.2

When subjects reached a steady state of pulse rate, with

no difference in heart rate exceeding 5 beats per minute

between measurements at 1-minute intervals, and a level

of exertion of 14 to 17 on the RPE scale, the subjects

immediately lay down on the apparatus for measurement

of proprioception. The pulse rate after cycling was 163

beats per minute (range, 138 to 196) and after the meas-

urement was 93 beats per minute (range, 63 to 121). The

median cycling time was 6 minutes (range, 5 to 8), long

enough to increase blood lactate levels.18

Statistical Analysis

Because there seemed to be no proprioceptive difference

between the left and right legs,11 the mean of both legs

(right left/2) was used for the analyses. Comparisons

between the measurements were performed by using pair-

wise t-tests. The significance level was set at P 0.05.

Statistical analyses were performed with the Minitab 10

(Minitab, State College, Pennsylvania), SAS 6.10 (SAS,

Cary, North Carolina), and SPSS 11.0 (SPSS, Inc., Chi-

cago, Illinois) program packages.

RESULTS

When the measurements for each starting position were

analyzed before and after cycling, comparisons showed no

significant effect on threshold of perception of movement

toward extension from 20 and 40. Toward flexion, sig-nificantly higher threshold values, indicating poorer pro-

prioception, were found from both starting positions (P

0.025 for 20 and P 0.003 for 40) (Table 2).

DISCUSSION

A matter of concern when these results are discussed is

the small magnitude of observed differences, in mean val-

ues, between the measurements and the clinical relevance

of these possible changes. Within the limitations of what

is currently known, we cannot establish using our meas-

urement method how much proprioception may be de-

creased before the result is clinically relevant. However, it

is important to note that group comparisons may show

discrete, but statistically significant, differences in

threshold values, whereas comparisons between individ-

ual subjects may show large differences.811,27,28 It

should also be emphasized that the estimated conscious

proprioceptive ability, in this case the threshold to detec-

tion of movement value, likely is the tip of the iceberginthe complex conscious and unconscious neuromuscular

TABLE 1Difference between Initial Measurement and after 1 Month in a

Previous Normal Population

Type of test Difference

(deg)95% confidence

interval

20 toward extension 0.13 0 to 0.3840 toward extension 0.25 0 to 0.6320 toward flexion 0.13 0 to 0.2540 toward flexion 0.00 0 to 0.13

TABLE 2Comparison of Threshold Values (in Degrees) before and after Exercise

Starting position Before exercisea After exercisea Before vs. after cycling

20 toward extension 0.61 0.22 0.66 0.30 P 0.39840 toward extension 0.85 0.33 0.96 0.40 P 0.12520 toward flexion 0.84 0.85 1.02 0.51 P 0.025b

40 toward flexion 0.54 0.14 0.66 0.22 P 0.003b

a Mean standard deviation.b Significant difference.

992 Roberts et al. American Journal of Sports Medicine



5/6

system controlling balance, joint movement, and stability.

It is very difficult to estimate to what degree the observed

changes reflected the status of the whole system.

The results of the present study indicate that short-

term cycling may reduce knee joint proprioception. This

result is supported by a previous experimental study that

showed primary muscle spindle afferents, which contrib-

ute to proprioception, have reduced capability to discrim-

inate between different muscle lengths after fatigue.26

Gamma motoneurons that innervate the muscle spindles

and affect the spindle outflow are often referred to as the

fusimotor system.12 The activity in the fusimotor system

is increased because of fatigue, and the effect seems to be

reflex-mediated by chemosensitive group III and IV mus-

cle afferent fibers.21,22 Metabolic products of fatigue, such

as bradykinin, 5-hydroxytryptamine, and lactic acid, are

thought to cause this effect. A resultant, mainly excita-

tory, effect on the primary and secondary muscle spindle

afferents has been observed in both heteronymous, hom-

onymous, ipsilateral, and contralateral muscles.4,5 The

effect on proprioception is suggested to be negative be-cause of an increased similarity in the fusimotor drive on

individual afferents in ensembles of muscle spindle affer-

ents, producing a decrease in the response variability.26

We have no evidence that we actually caused fatigue in

the study setup, but earlier findings imply that an in-

crease in blood lactate is likely to occur during these

circumstances.18

Thus, it seems to be well established that local muscular

effects occur during fatigue that may negatively affect

proprioception,4,5,13,21,22,25,26 but little is known about

joint receptors during exercise. No biochemical changes in

the synovial fluid associated with muscular fatigue that

may affect joint receptors have, to our knowledge, beendescribed. However, a direct effect on the knee joint re-

ceptors may occur because fatigue increases joint lax-

ity,24,31,33,34,36 which, by changing the elastic properties

of the ligaments containing collagen, may modify the re-

sponse of the receptors.

Clinically, we have found three studies evaluating the

effects of fatigue on knee joint proprioception20,23,30 and

one on the joint position sense during nonfatiguing exer-

cise.3 The findings of Lattanzio et al.,20 who reported a

reduction in proprioception after fatigue, support the re-

sults of our study to some extent.

Skinner et al.30 reported that healthy subjects had more

difficulty in reproducing a knee joint angle after fatiguebut showed no significant change in threshold. They in-

terpreted their findings as supporting the view that mus-

cle receptors play a significant role in the conscious ap-

preciation of joint position.

In contrast, Marks and Quinney23 detected no effect of

muscle fatigue on knee joint position sense. However, they

induced fatigue by having the subject contract the quad-

riceps muscle 20 times, which likely was less fatiguing

than the exercise used by Skinner et al. This exercise also

mainly affected the anterior structures of the thigh.

Therefore, the posterior structures, which are of afferent

importance during extension, were probably less affected

by fatigue. Moreover, Marks and Quinney used active

positioning and active reproduction, whereas Skinner et

al.30 used passive positioning and active reproduction,

which may also explain the difference in results. In the

study by Bouet and Gahery,3 the participants improved

their joint position sense (active reproduction) after a

warm-up exercise, cycling on the ergometer bicycle for 10

minutes at their own pace. With regard to the results of

Marks and Quinney23 and Skinner et al.,30 this raises the

question of whether an initial improvement is followed by

afatigue threshold,above which muscles perform worse,functionally and proprioceptively.

The lack of difference in threshold before and after

fatigue in the study by Skinner et al.30 does not conflict

with our findings because they measured the threshold

only toward extension; we also did not detect differences

between before and after exercise of perception of motion

toward extension. Our measurements showed a signifi-

cant reduction in thresholds only for motion toward flex-

ion, which again may underline the role of the muscle

spindles. Our fatigue test was cycling, which, in our setup

without toe clips, can be thought to activate the quadri-ceps muscle more than the hamstring muscles.6,7 The

measurements of flexion, which stretch the quadriceps

muscle, may therefore be more affected if muscles play a

significant or dominant proprioceptive role. In the study of

Skinner et al.,30 the fatigue protocol, including running,

probably affected the hamstring muscles more, which was

one of their aims, and they ascribed their intact threshold

values after fatigue to an enhancement of capsular receptors

due to inadequate muscle receptor function. Even though the

lack of knowledge about joint receptor characteristics during

exercise is obvious, as mentioned earlier, some authors seem

to believe in reduced activity of these receptors during

fatigue, rather than an enhancement.1,19,20

In the present study, an effect of laxity on the knee joint

receptors was unlikely. Fatigue-induced laxity may not

have occurred; Nawata et al.24 have shown that laxity

does not occur until after 20 minutes of running, and no

subject in the present study cycled more than 8 minutes.

Theoretically, fatigue may increase the time of reaction,

which, in the present setup, would be seen as higher

threshold values. However, this would presumably affect

both flexion and extension measurements, which was not

seen.

In conclusion, we found that a short period of moderate

exercise can reduce proprioception, which may affect the

neuromuscular control of the knee joint and, thus, maymake it more susceptible to injuries. No conclusions re-

garding the origin of the proprioceptive loss can be drawn

from the results in this study, nor about the effect of

fatigue on subconscious reflective afferent information.

ACKNOWLEDGMENTS

We thank Mats Christensson, of the Department of Med-

ical Technology, for his construction of the apparatus

used, all of the subjects who volunteered to take part in

the study, and statistician Per-Erik Isberg. Funding for

this study was received from Medicinska forskningsrdet,projekt 09509, Stockholm; Stiftelsen for Bistnd t Van-

Vol. 31, No. 6, 2003 Effects of Short-Term Cycling on Knee Joint Proprioception 993



6/6

fora i Skne, Sweden; Syskonen Perssons Donationsfond,Sweden; Svenska Sallskapet for Medicinsk Forskning,

Stockholm; Thyr och Thure Stenemarks Fond, Sweden;

Centrum for Idrottsforskning, Stockholm; the Swedish So-

ciety of Medicine, Stockholm; the National Board of

Health and Welfare, Stockholm; and the Faculty of Med-

icine, University of Lund, Lund, Sweden.

REFERENCES

1. Barrack RL, Skinner HB, Cook SD: Proprioception of the knee joint.Paradoxical effect of training. Am J Phys Med 63:175181, 1984

2. Borg G: Psychophysical scaling with applications in physical work and theperception of exertion.Scand J Work Environ Health 16 (Suppl 1):5558,1990

3. Bouet V, Gahery Y: Muscular exercise improves knee position sense inhumans. Neurosci Lett 289:143146, 2000

4. Djupsjobacka M, Johansson H, Bergenheim M, et al: Influences on thegamma-muscle spindle system from muscle afferents stimulated by in-creased intramuscular concentrations of bradykinin and 5-HT. NeurosciRes 22:325333, 1995

5. Djupsjobacka M, Johansson H, Bergenheim M, et al: Influences on thegamma-muscle-spindle system from contralateral muscle afferents stim-ulated by KCl and lactic acid. Neurosci Res 21:301309, 1995

6. Ericson M: On the biomechanics of cycling. A study of joint and muscleload during exercise on the bicycle ergometer. Scand J Rehabil Med(Suppl) 16:143, 1986

7. Ericson MO, Nisell R, Arborelius UP, et al: Muscular activity during er-gometer cycling. Scand J Rehabil Med 17:5361, 1985

8. Friden T, Roberts D, Movin T, et al: Function after anterior cruciateligament injuries. Influence of visual control and proprioception. ActaOrthop Scand 69:590594, 1998

9. Friden T, Roberts D, Zatterstrom R, et al: Proprioceptive defects after ananterior cruciate ligament rupturethe relation to associated anatomicallesions and subjective knee function. Knee Surg Sports Traumatol Ar-throsc 7:226231, 1999

10. Friden T, Roberts D, Zatterstrom R, et al: Proprioception after an acuteknee ligament injury: A longitudinal study on 16 consecutive patients.J Orthop Res 15:637644, 1997

11. Friden T, Roberts D, Zatterstrom R, et al: Proprioception in the nearlyextended knee. Measurements of position and movement in healthy indi-viduals and in symptomatic anterior cruciate ligament injured patients.

Knee Surg Sports Traumatol Arthrosc 4:217224, 199612. Gordon J, Ghex C: Modality coding in the somatic sensory system, in

Kandel ER, Schwartz JH, Jessel TM (eds): Principles of Neural Science.Third edition. New York, Elsevier, 1991, pp 564581

13. Hutton RS, Nelson DL: Stretch sensitivity of Golgi tendon organs infatigued gastrocnemius muscle. Med Sci Sports Exerc 18:6974, 1986

14. Johansson H, Lorentzon R, Sjolander P, et al: The ACL. A sensor actingon the gamma muscle spindle systems of muscles around the knee joint.Neuro-Orthop 9:123, 1990

15. Johansson H, Sjolander P, Sojka P: Receptors in the knee joint ligamentsand their role in the biomechanics of the joint. Crit Rev Biomed Eng 18:341368, 1991

16. Johansson H, Sjolander P, Sojka P: A sensory role for the cruciateligaments. Clin Orthop 268:161178, 1991

17. Johansson H, Sjolander P, Sojka P: Activity in receptor afferents from theanterior cruciate ligament evokes reflex effects on fusimotor neurones.Neurosci Res 8:5459, 1990

18. Knuttgen HG, Saltin B: Muscle metabolites and oxygen uptake in short-term submaximal exercise in man. J Appl Physiol 32:690694, 1972

19. Lattanzio PJ, Petrella RJ: Knee proprioception: A review of mechanisms,measurements, and implications of muscular fatigue. Orthopedics 21:

463471, 199820. Lattanzio PJ, Petrella RJ, Sproule JR, et al: Effects of fatigue on knee

proprioception.Clin J Sport Med 7:2227, 199721. Ljubisavljevic M, Anastasijevic R: Fusimotor system in muscle fatigue. J

Peripher Nerv Syst 1:8396, 199622. Ljubisavljevic M, Jovanovic K, Anastasijevic R: Changes in discharge rate

of fusimotor neurones provoked by fatiguing contractions of cat tricepssurae muscles. J Physiol 445:499513, 1992

23. Marks R, Quinney HA: Effect of fatiguing maximal isokinetic quadricepscontractions on ability to estimate knee-position. Percept Mot Skills 77:11951202, 1993

24. Nawata K, Teshima R, Morio Y, et al: Anterior-posterior knee laxity in-creased by exercise. Quantitative evaluation of physiologic changes. ActaOrthop Scand 70:261264, 1999

25. Pedersen J, Ljubisavljevic M, Bergenheim M, et al: Alterations in informa-tion transmission in ensembles of primary muscle spindle afferents aftermuscle fatigue in heteronymous muscle. Neuroscience 84: 953959,1998

26. Pedersen J, Lonn J, Hellstrom F, et al: Localized muscle fatigue de-creases the acuity of the movement sense in the human shoulder. MedSci Sports Exerc 31:10471052, 1999

27. Roberts D, Friden T, Stomberg A, et al: Bilateral proprioceptive defects inpatients with a unilateral anterior cruciate ligament reconstruction: A com-parison between patients and healthy individuals. J Orthop Res 18:565571, 2000

28. Roberts D, Friden T, Zatterstrom R, et al: Proprioception in people withanterior cruciate ligament-deficient knees: Comparison of symptomaticand asymptomatic patients.J Orthop Sports Phys Ther 29:587594, 1999

29. Sjolander P: A sensory role for the cruciate ligaments. Dissertation. Uni-versity of Ume, Ume Sweden, 1989

30. Skinner HB, Wyatt MP, Hodgdon JA, et al: Effect of fatigue on jointposition sense of the knee. J Orthop Res 4:112118, 1986

31. Skinner HB, Wyatt MP, Stone ML, et al: Exercise-related knee joint laxity.Am J Sports Med 14:3034, 1986

32. Sojka P, Sjolander P, Johansson H, et al: Influence from stretch-sensitive

receptors in the collateral ligaments of the knee joint on the gamma-muscle-spindle systems of flexor and extensor muscles.Neurosci Res 11:5562, 1991

33. Steiner ME, Grana WA, Chillag K, et al: The effect of exercise on anterior-posterior knee laxity.Am J Sports Med 14:2429, 1986

34. Stoller DW, Markolf KL, Zager SA, et al: The effects of exercise, ice, andultrasonography on torsional laxity of the knee.Clin Orthop 174:172180,1983

35. Tegner Y, Lysholm J: Rating systems in the evaluation of knee ligamentinjuries.Clin Orthop 198:4349, 1985

36. Weisman G, Pope MH, Johnson RJ: Cyclic loading in knee ligamentinjuries. Am J Sports Med 8:2430, 1980

994 Roberts et al. American Journal of Sports Medicine


Documents

Effects of Short-Term Cycling on Knee Joint Proprioception in Healthy Young Persons