- Email: [email protected]
Cryotherapy does not impair shoulder joint position sense1
1241
Cryotherapy Does Not Impair Shoulder Joint Position Sense Geoffrey Dover, MS, CAT(c), ATC, Michael E. Powers, PhD, ATC, CSCS ABSTRACT. Dover G, Powers ME. Cryotherapy does not impair shoulder joint position sense. Arch Phys Med Rehabil 2004;85:1241-6. Objective: To determine the effects of a cryotherapy treatment on shoulder proprioception. Design: Crossover design with repeated measures. Setting: University athletic training and sports medicine research laboratory. Participants: Thirty healthy subjects (15 women, 15 men). Intervention: A 30-minute cryotherapy treatment. Main Outcome Measures: Joint position sense was measured in the dominant shoulder by using an inclinometer before and after receiving 30 minutes of either no ice or a 1-kg ice bag application. Skin temperature was measured below the tip of the acromion process and recorded every 5 minutes for the entire 30 minutes and immediately after testing. Three different types of error scores were calculated for data analyses and used to determine proprioception. Results: Separate analyses of absolute, constant, and variable error failed to identify changes in shoulder joint proprioception as a function of the cryotherapy application. Conclusions: Application of an ice bag to the shoulder does not impair joint position sense. The control of proprioception at the shoulder may be more complex than at other joints in the body. Clinical implications may involve modifying rehabilitation considerations when managing shoulder injuries. Key Words: Cryotherapy; Kinesthesis; Proprioception; Rehabilitation; Shoulder. © 2004 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation HERRINGTON FIRST DEFINED proprioception in 1906 and is credited with some landmark proprioception experS iments. Since then, many researchers have continued his work 1
in an attempt to determine peripheral control mechanisms. Sherrington1 originally defined proprioception as afferent information traveling to the central nervous system (CNS). More recently, the term proprioception has evolved to include measures of joint position sense (JPS), threshold to detection of passive movement, and force reproduction.2,3 Because measuring proprioceptive control is difficult, researchers have traditionally confined their work to observing motor output and inferring the underlying control processes.4 The most common methods used to quantify proprioception attempt to alter or perturb the afferent information during joint motion. The resultant change in motor output is then used to infer control processes.5-15 The goal of the modification tech-
From the Department of Exercise and Sport Sciences, University of Florida, Gainesville, FL (Dover); and Division of Athletic Training, Shenandoah University, Winchester, VA (Powers). No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors(s) or upon any organization with which the author(s) is/are associated. Reprint requests to Geoffrey Dover, MS, CAT(c), ATC, 160 FL Gym, PO Box 118207, Gainesville, FL 32611-8207, e-mail: [email protected]. 0003-9993/04/8508-8781$30.00/0 doi:10.1016/j.apmr.2003.11.030
nique is to affect the afferent information while not disturbing the mechanical properties of the muscles being tested.4 For example, in 3 different studies11,12,14 examining the effects of fatigue on force reproduction, the authors suggested a similar mechanism for proprioceptive control: afferent feedback, efferent signals, and some central mechanism. Despite these and other studies, the neural mechanisms of proprioception remain unclear. Most proprioception research has examined the elbow, wrist, knee, and ankle. Some authors5,6,8,9,11,12,14,16-20 have attempted to generalize their findings to other joints; however, proprioceptive control may differ depending on the joint tested. The exact mechanism of proprioceptive control remains unclear, particularly in the shoulder. Shoulder proprioception is indispensable because the glenohumeral joint (GHJ) relies primarily on dynamic restraint of the rotator cuff to maintain stability. Proprioception also may affect injury predisposition and rehabilitation. Several studies7,15-27 suggest that shoulder proprioception is impaired after fatigue, injury, and in overhand athletes. Lephart et al28 showed the relations among injury, proprioceptive deficits, and instability of the shoulder. Although the exact relation between proprioception and the cause of injury is unclear, clinicians commonly use proprioception exercises during rehabilitation of the shoulder because the rotator cuff is vital for GHJ stability.29-31 Cryotherapy is commonly used in the clinical setting to decrease pain and to reduce inflammation during injury management.32 Moreover, cryotherapy influences neuromuscular properties, including nerve conduction velocity and muscle contraction.33-40 This change in muscle electrophysiologic activity may be caused by a reduction of sodium, potassium, and calcium diffusion in nerves and at the motor endplate.38 Cryotherapy has become a common tool for disrupting afferent signals and modifying neuromuscular control while measuring proprioception. For example, 3 studies16-18 report the use of cryotherapy to disrupt afferent signals while measuring proprioception of the knee and the ankle. Two of these studies17,18 noted an impaired JPS after cryotherapy. Although cryotherapy is commonly used in the rehabilitation setting, the effects of cryotherapy on shoulder proprioception are unknown. Thus, the purpose of the present study was to assess shoulder JPS after a 30-minute cryotherapy session in healthy subjects. METHODS Participants Thirty volunteers from the university setting, 15 men (mean age ⫾ standard deviation [SD], 23.7⫾5.5y; height, 180.0⫾6.4cm; mass, 86.7⫾18.6kg) and 15 women (mean age ⫾ SD; 20.7⫾1.4y; height, 165.0⫾5.5cm; mass, 58.6⫾6.9kg) participated in the study. Results from a power analysis indicated that 30 subjects were sufficient to identify differences between error scores. Before participating, all subjects signed an informed consent agreement approved by the university’s institutional review board. Subjects were excluded from participation if they had any contraindications to cryotherapy, including areas of decreased sensation, areas of decreased blood flow, Raynaud’s disease, or any previous cold allergies or reactions. Subjects also were excluded if they participated in Arch Phys Med Rehabil Vol 85, August 2004
1242
CRYOTHERAPY AND SHOULDER JOINT POSITION SENSE, Dover
Fig 1. The inclinometer.
overhand athletics because of a possible effect on proprioception.21,22,27 Finally, subjects who had suffered a previous shoulder injury (including dislocation, subluxation, surgery, or any condition that caused pain during active movement) were excluded because these variables may affect proprioception.23-26 Instrumentation Thermometer and temperature probe. Skin surface temperature was measured by using a SST-1 flexible surface temperature probea with a contact surface area of 0.8cm2. The probe was connected to a thermometera with a range of 0° to 100°C and an accuracy of ⫾0.1°C. Inclinometer. An inclinometer (fig 1) was used for all range of motion (ROM) measurements and JPS testing. The inclinometer resembles a flat goniometer with a weighted arm inside and 360° marked in single-degree increments on its circumference. When the inclinometer is held upright, gravity pulls the inclinometer’s arm inferiorly and the measurement can be made. The angle measured is determined by comparing the location of the inclinometer’s arm with the degree markings around the circumference. We have previously reported41 that this particular inclinometer provides a very reliable (intertester, intratester) and valid method of assessing joint angles. We also reported41 that the inclinometer provides a very reliable measure of JPS. Measurements Joint position sense. All JPS testing was performed with subjects in the standing position. By using a Velcro strap, we secured the inclinometer to the subject’s wrist just proximal to the ulnar styloid process. Then we assessed total internal rotation (IR) and external rotation (ER) ROM while the shoulder and elbow were maintained, respectively, in 90° of abduction and flexion (fig 2). The subjects were instructed to actively rotate the shoulder to the end point of the range in both the IR and ER directions. They were further instructed to hold the end position while the angle was observed and recorded. The repositioning or target angles were then calculated according to the maximum angle each subject achieved. For the present study, the 2 target angles were equivalent to 90% of ER and 90% of IR ROM. Thus, the 2 target angles were 10% short of full IR and ER. These angles ensured that, despite varying Arch Phys Med Rehabil Vol 85, August 2004
ROM values across subjects, the target angle produced similar muscle length and sensations between subjects. To assess JPS, the principal investigator actively assisted the subject’s arm to the target angle and instructed the subject to hold the limb in that position for 3 seconds before returning the arm to the starting position. This time period, which has been used previously,22,41 enables the subject to become aware of the target angle without becoming fatigued. The subjects were blindfolded to eliminate any visual cues and, while the arm was at the target angle, they were told to concentrate on its position “in space.” After returning to the starting point, the subjects were instructed to immediately reposition the arm back to the target angle and inform the tester when they felt the position had been achieved. At this time, the angle observed on the inclinometer was recorded. The measurement was repeated 2 more times for a total of 3 trials and the order of IR and ER testing was randomized. The target angle and the repositioned angles were used to generate 3 types of error scores previously described by Schmidt and Lee42: absolute error, variable error, and constant error. The absolute error score is a measure of overall accuracy in performance and is calculated by measuring the absolute deviation between the target angle and the repositioned angle. Variable error measures the inconsistency and the variability of the participants’ repositioning by comparing the 3 repositioned trials to each other. Constant error represents the amount of deviation or bias of the motor outcome. This error score is the average magnitude of the movement and measures the direction of the errors between the trials and the target angle. Procedures Subjects reported to the testing site on 2 occasions: once for the cryotherapy treatment and once for the no-ice (control) condition. The sessions were separated by a minimum of 48 hours, and the testing order was randomly assigned on arrival. To begin the initial visit, demographic data including height, weight, age, arm dominance, percentage of body fat, and tri-
Fig 2. Subject position during JPS testing.
1243
CRYOTHERAPY AND SHOULDER JOINT POSITION SENSE, Dover
Fig 3. Subject positioning during cryotherapy treatment.
ceps skinfold measurements were measured and recorded. Arm dominance was determined as the arm the subject would naturally use to throw a ball. Only the dominant shoulder was measured in this study. We used a Body Logic Body Fat Analyzer model HBF-301 device and calipersb to evaluate percentage of body fat and measure the triceps skinfold. Following these measurements, subjects’ active IR and ER ROM were assessed by using the inclinometer. Once the target angles were calculated based on the available ROM, JPS testing began. After the initial JPS measurement, the temperature probe was placed on the shoulder and a baseline measure was recorded. Each subject then completed either the cryotherapy or the control condition. In the cryotherapy condition, a 1-kg bag of cubed ice was applied to the shoulder for 30 minutes. The center of the ice bag was applied over the tip of the acromion of the dominant shoulder. The ice bag was 20⫻25cm (surface area, 500cm2) in size and covered the deltoid and lateral portion of the scapula. Each ice bag was prepared in a similar manner and included weighing the bag and removing the air from it as suggested by others.32,43 The ice bag was secured to the shoulder by an elastic bandage. The same type of bandage was used for all subjects during the study, and each time was applied around the upper arm twice followed by once around the chest. After the ice bag was applied, subjects were placed in a supine position where they remained throughout the 30-minute treatment period (fig 3). The surface temperature probe was placed just inferior to the tip of the acromion process, and skin temperature was recorded every 5 minutes during the treatment and immediately after testing. For the control condition, subjects remained in the treatment position for 30 minutes with no ice bag application. Immediately after the cryotherapy or control condition, subjects resumed standing and the JPS testing was repeated. Statistical Analyses To determine a gender effect from the cryotherapy, the surface temperature data were first analyzed using a 2⫻2⫻8 mixed-design analysis of variance (ANOVA) with 1 betweensubjects factor (gender) with 2 levels (male, female) and 2 within-subjects factors: treatment with 2 levels (cryotherapy, control) and time with 8 levels (pre, 5, 10, 15, 20, 25, 30min, post). In addition, 2 independent t tests were used to determine if differences existed between percentage of body fat and skinfold thickness between men and women. After the gender analyses, 3 separate 2⫻2⫻2 (treatment by time by position) repeated-measures ANOVA were performed for absolute, con-
stant, and variable error scores. The designs were similar to the ANOVA above; however, the gender variable was removed and a third within-variable position (IR, ER) was included. An a priori level of significance was set at P less than .05 for all comparisons, and the Tukey honestly significant difference (HSD) test was used for all pairwise comparisons. RESULTS Gender Differences We found no significant differences when we compared male and female skin surface temperatures during the cryotherapy session (F7,196⫽1.75, P⫽.100). After the 30 minutes of cryotherapy, the mean male skin temperature ⫾ SD was 13.3°⫾2.8° and for females skin temperature was 13.0°⫾2.2°. Therefore, we combined the temperature data across the genders for the rest of the analyses. Moreover, no differences were observed between the percentage of body fat (t⫽⫺.798, P⫽.432) and skinfold thickness (t⫽⫺1.359, P⫽.185) between men and women (table 1). Because of the lack of gender differences, we combined the male and female error scores for the rest of the analyses. Surface Temperature A significant treatment by time interaction was observed for surface temperature (F7,203⫽674.28, P⫽.000) because temperature decreased significantly during the cryotherapy treatment, whereas no change occurred during the control condition (fig 4). The Tukey HSD procedure revealed no difference between the baseline temperatures of the cryotherapy and control sessions; however, we found differences when we compared individual time points after 5 minutes of cryotherapy with the baseline measure. Absolute Error Scores No significant differences were observed for absolute error after the cryotherapy session (treatment by time interaction) Table 1: Male and Female Body Composition Gender
% Body Fat
Skinfold (mm)
Male Female
15.9⫾7.4 17.8⫾5.4
11.9⫾4.3 13.6⫾3.6
NOTE. Values are mean ⫾ SD.
Arch Phys Med Rehabil Vol 85, August 2004
1244
CRYOTHERAPY AND SHOULDER JOINT POSITION SENSE, Dover
Fig 4. Skin temperatures, in control versus cryotherapy conditions.
(F1,29⫽1.875, P⫽.181) (table 2). Likewise, no other meaningful main effects or interactions were found to be significant.
DISCUSSION The primary finding of this study indicates that 30 minutes of cryotherapy does not impair shoulder JPS because no differences were observed when comparing error scores before and immediately after the ice bag treatment. There was no change in repositioning error after treatment, according to analyses that included direction bias and variability factors. These findings
conflict with the reports of 2 previous studies17,18 that investigated cryotherapy and proprioception in the knee and the ankle. Those authors reported that cryotherapy affected the afferent information from the periphery and altered the resulting motor output. The output, or JPS in the present case, is measured in degrees, and small differences are sufficient for statistical significance. Two previous studies32,44 measuring JPS of the knee reported that a mean difference of 1.7° between error scores was sufficient for statistical significance. They further suggested that conclusions can be inferred from those differences about proprioceptive control mechanisms. A similar difference was found to be statistically significant in the shoulders of overhand athletes.22 Although a small change in error scores is enough to identify a reliable, statistically significant difference, a question of clinical relevance exists. A difference of a few degrees cannot be observed accurately with the naked eye during an assessment. However, several studies16,17,19,22 have shown a significant change in proprioception with small changes in error scores in injured or predisposed populations, suggesting that these small differences may indeed be clinically significant. Despite the small difference in error scores previously shown to be statistically significant, we did not find these small error scores in the present investigation.
Table 2: JPS Absolute Error Scores
Table 3: JPS Variable Error Scores
Constant Error Scores Further analysis revealed no significant differences in constant error after the cryotherapy session (F1,29⫽.410, P⫽.527) (table 3). No other significant main effects or interactions were observed. Variable Error Scores No significant differences in variable error scores were observed after the cryotherapy treatment (F1,29⫽1.505, P⫽.230) (table 4). In addition, no other main effects or interactions were found to be significant.
Test Condition and Position
Control IR ER Cryotherapy IR ER
Pre (deg)
Post (deg)
4.5⫾2.5 3.4⫾1.9
3.9⫾1.9 3.1⫾1.7
4.5⫾2.8 2.9⫾1.6
4.1⫾2.1 3.8⫾2.2
NOTE. Values are mean ⫾ SD.
Arch Phys Med Rehabil Vol 85, August 2004
Test Condition and Position
Control IR ER Cryotherapy IR ER NOTE. Values are mean ⫾ SD.
Pre (deg)
Post (deg)
3.3⫾2.3 2.4⫾1.7
2.7⫾1.5 1.9⫾1.1
2.9⫾1.8 2.5⫾1.6
2.7⫾1.2 2.5⫾2.0
CRYOTHERAPY AND SHOULDER JOINT POSITION SENSE, Dover Table 4: JPS Constant Error Scores Test Condition and Position
Control IR ER Cryotherapy IR ER
Pre (deg)
Post (deg)
1.7⫾3.9 ⫺0.2⫾3.5
1.4⫾3.6 ⫺0.2⫾3.3
1.7⫾4.6 0.3⫾2.7
0.8⫾4.5 0.2⫾3.8
NOTE. Values are mean ⫾ SD.
In contrast to the 2 previously mentioned studies investigating cryotherapy and proprioception in the knee and the ankle,17,18 our subjects’ shoulder proprioception was not altered after a standard clinical application of cryotherapy. Previous studies11,12,14 have suggested that motor control is a combination of afferent and efferent information and some central mechanism. The afferent information from the GHJ may have been affected by the cryotherapy, but subjects were able to use peripheral information from other areas to modifying the motor response. Perhaps what little afferent information travels to the CNS is enough for the efferent or central command information to correct the JPS, despite the alteration caused by the cryotherapy in this experiment. Because the shoulder did not react to the cryotherapy in a manner similar to that of the knee or ankle, comparing JPS between joints would be useful in future research. The present study used 3 types of error scores to obtain comprehensive outcome measures on the repositioning task. Other studies12,14,19 have used multiple error scores for a similar reason. In studies in which researchers suspect a bias in a certain direction of error scores, constant error scores should be used because this measurement accounts any difference in direction.41 For example, when using a vibration stimulus, the limb is repositioned short of the target because of the “illusion” created that the limb is being stretched.8,9,20 In this example, constant error would be a useful measure because there is a direction of interest for the error in the repositioning. In addition, when using fatigue to alter proprioception in the elbow, there may be a resultant increase in the variable error in reproducing force.12,14 After fatigue, force reproduction trials increase in variability around the target. No study to date has reported a bias in proprioception or an increase in variable error after cryotherapy, so all 3 error scores were used in the analysis. No increase in bias or variability has been noted in shoulder JPS after cryotherapy. Previous research on the shoulder and cryotherapy has been conducted postoperatively. From those studies,45,46 researchers suggested that the GHJ is difficult to cool. For example, when glenohumeral and subacromial temperatures have been measured postoperatively, changes of only 1°C, on average, have been observed.45 Those authors used continuous cryotherapy for 23 hours with cold water flowing through a cuff around the shoulder postoperatively. Although a small temperature difference existed between the cold group and the control, the difference was still statistically significant. This finding suggests that the temperature within the GHJ may be difficult to lower to a level of clinical significance. In the present study, the shoulder may not have been cooled enough to measure a difference in the motor output. However, the skin surface temperatures (mean ⫾ SD, 14.5°⫾2.1°C) were lower than that (32°C) in the previously mentioned study.45 Thus, the deeper tissues may have cooled more than those previously reported. Both studies45,46 suggest that the subacromial space cools to a
1245
greater extent than the GHJ after cryotherapy. This finding has clinical importance because the tendons from the rotator cuff musculature (the muscle group of interest in the present study) travel through this space.47 Although we standardized the weight of the ice bag, we did not standardize the relative area of ice bag coverage for each subject. Thus, our smaller subjects might have had a greater application area than our larger subjects. However, we do not believe that this would confound our results because the subacromial space and glenohumeral areas were included for all subjects. Previous research48 suggests that differences in body fat percentage may affect cooling rate. Because body fat and skinfold thickness may be greater in women than in men, the rate of cooling might differ between genders. In the current study, percentage of body fat and skinfold thickness measurements were slightly higher in women; yet, these differences were not statistically significant (see table 1). This lack of difference between the male and female subjects may explain the similarity in cooling. CONCLUSIONS The present findings did not support the hypothesis that cryotherapy impairs shoulder JPS. Clinicians should be aware of this information in making decisions during rehabilitation of shoulder injuries. Acknowledgment: We thank James Cauraugh for his invaluable contributions revising the manuscript. References 1. Sherrington CS. On the proprio-ceptive system, especially in its reflex aspect. Brain 1906;29:467-82. 2. Jones LA. Peripheral mechanisms of touch and proprioception. Can J Physiol Pharmacol 1994;72:484-7. 3. Riemann BL, Lephart SM. The sensorimotor system, Part I: The physiologic basis of functional joint stability. J Athl Train 2002; 37:71-9. 4. Kelso JA, Holt KG, Flatt AE. The role of proprioception in the perception and control of human movement: toward a theoretical reassessment. Percept Psychophys 1980;28:45-52. 5. Brockett C, Warren N, Gregory JE, Morgan DL, Proske U. A comparison of the effects of concentric versus eccentric exercise on force and position sense at the human elbow joint. Brain Res 1997;771:251-8. 6. Burgess PR, Jones LF. Perceptions of effort and heaviness during fatigue and during the size-weight illusion. Somatosens Mot Res 1997;14:189-202. 7. Carpenter JE, Blasier RB, Pellizzon GG. The effects of muscle fatigue on shoulder joint position sense. Am J Sports Med 1998; 26:262-5. 8. Cordo P, Gurfinkel VS, Bevan L, Kerr GK. Proprioceptive consequences of tendon vibration during movement. J Neurophysiol 1995;74:1675-88. 9. Goodwin GM, McCloskey DI, Matthews PB. Proprioceptive illusions induced by muscle vibration: contribution by muscle spindles to perception? Science 1972;175:1382-4. 10. Jones LA, Hunter IW. Effect of fatigue on force sensation. Exp Neurol 1983;50:640-50. 11. McCloskey DI, Ebeling P, Goodwin GM. Estimation of weights and tensions and apparent involvement of a “sense effort”. Exp Neurol 1974;42:220-32. 12. Saxton JM, Clarkson PM, James R, et al. Neuromuscular dysfunction following eccentric exercise. Med Sci Sports Exerc 1995;27: 1185-93. 13. Stevens JC, Cain WS. Effort in isometric muscular contractions related to force level and duration. Percept Psychophys 1970;8: 240-4. 14. Vincent HK, Carlson C, Hyatt JP, Yihua L, Vincent KR. Alterations in bilateral force judgment following strenuous eccentric exercise. Res Q Exerc Sport 2000;71:340-8. Arch Phys Med Rehabil Vol 85, August 2004
1246
CRYOTHERAPY AND SHOULDER JOINT POSITION SENSE, Dover
15. Voight ML, Hardin JA, Blackburn TA, Tippett S, Canner GC. The effects of muscle fatigue on and the relationship of arm dominance to shoulder proprioception. J Orthop Sports Phys Ther 1996;23: 348-52. 16. Thieme HA, Ingersoll CD, Knight KL, Ozmun JC. Cooling does not affect knee proprioception. J Athl Train 1996;31:8-11. 17. Uchio Y, Ochi M, Fujihara A, Adachi N, Iwasa J, Sakai Y. Cryotherapy influences joint laxity and position sense of the healthy knee joint. Arch Phys Med Rehabil 2003;84:131-5. 18. Hopper D, Whittington D, Davies J, Chartier JD. Does ice immersion influence ankle joint position sense? Physiother Res Int 1997;2:223-36. 19. Feuerbach JW, Grabiner MD, Koh TJ, Weiker GG. Effect of an ankle orthosis and ankle ligament anesthesia on ankle joint proprioception. Am J Sports Med 1994;22:223-9. 20. Calvin-Figuiere S, Romaiguere P, Gilhodes JC, Roll JP. Antagonist motor responses correlate with kinesthetic illusions induced by tendon vibration. Exp Brain Res 1999;124:342-50. 21. Allegrucci M, Whitney S, Lephart S, Irrgang J, Fu F. Shoulder kinesthesia in healthy unilateral athletes participating in upper extremity sports. J Orthop Sports Phys Ther 1995;21:220-6. 22. Dover GC, Kaminski TW, Meister K, Powers ME, Horodyski M. Assessment of shoulder proprioception in the female softball athlete. Am J Sports Med 2003;31:431-7. 23. Lephart SM, Myers JB, Bradley JP, Fu FH. Shoulder proprioception and function following thermal capsulorraphy. Arthroscopy 2002;18:770-8. 24. Warner JJ, Lephart S, Fu FH. Role of proprioception in pathoetiology of shoulder instability. Clin Orthop 1996;Sep(330):35-9. 25. Machner A, Merk H, Becker R, Rohkohl K, Wissel H, Pap G. Kinesthetic sense of the shoulder in patients with impingement syndrome. Acta Orthop Scand 2003;74:85-8. 26. Smith RL, Brunolli J. Shoulder kinesthesia after anterior glenohumeral joint dislocation. Phys Ther 1989;69:106-12. 27. Safran MR, Borsa PA, Lephart SM, Fu FH, Warner JJ. Shoulder proprioception in baseball pitchers. J Shoulder Elbow Surg 2001; 10:438-44. 28. Lephart SM, Pincivero DM, Giraldo JL, Fu FH. The role of proprioception in the management and rehabilitation of athletic injuries. Am J Sports Med 1997;25:130-7. 29. Wilk KE, Arrigo C. Current concepts in the rehabilitation of the athletic shoulder. J Orthop Sports Phys Ther 1993;18:365-78. 30. Hayes K, Callanan M, Walton J, Paxinos A, Murrell GA. Shoulder instability: management and rehabilitation. J Orthop Sports Phys Ther 2002;32:497-509. 31. Kibler WB, McMullen J, Uhl T. Shoulder rehabilitation strategies, guidelines, and practice. Orthop Clin North Am 2001;32:527-38. 32. Knight KL. Cryotherapy in sport injury management. Champaign: Human Kinetics; 1995.
Arch Phys Med Rehabil Vol 85, August 2004
33. Abramson DI, Chu LS, Tuck S Jr, Lee SW, Richardson G, Levin M. Effect of tissue temperatures and blood flow on motor nerve conduction velocity. JAMA 1966;198:1082-8. 34. Bell KR, Lehmann JF. Effect of cooling on H-reflexes and Treflexes in normal subjects. Arch Phys Med Rehabil 1987;68: 490-3. 35. De Jesus PV, Hausmanowa-Petrusewicz I, Barchi RL. The effect of cold on nerve conduction of human slow and fast nerve fibers. Neurology 1973;23:1182-9. 36. Halar EM, DeLisa JA, Brozovich FV. Nerve conduction velocity: relationship of skin, subcutaneous and intramuscular temperatures. Arch Phys Med Rehabil 1980;61:199-203. 37. Krause BA, Hopkins JT, Ingersoll CD, Cordova ML, Edwards J. The relationship of ankle temperature during cooling and rewarming to the human soleus H reflex. J Sport Rehabil 2000;9:253-62. 38. Rutkove SB. Effects of temperature on neuromuscular electrophysiology. Muscle Nerve 2001;24:867-82. 39. Bergh U, Ekblom B. Influence of muscle temperature on maximal muscle strength and power output in human skeletal muscles. Acta Physiol Scand 1979;107:33-7. 40. Sargeant AJ. Effect of muscle temperature on leg extension force and short-term power output in humans. Eur J Appl Physiol Occup Physiol 1987;56:693-8. 41. Dover G, Powers ME. Reliability of joint position sense and force-reproduction measures during internal and external rotation of the shoulder. J Athl Train 2003;38:304-10. 42. Schmidt RA, Lee TD. Motor control and learning. 3rd ed. Champaign: Human Kinetics; 1999. p 18-35. 43. Merrick MA, Knight KL, Ingersoll CD, Potteiger JA. The effects of ice and compression wraps on intramuscular temperatures at various depths. J Athl Train 1993;28:236-45. 44. Adachi N, Ochi M, Uchio Y, Sumen Y. Anterior cruciate ligament augmentation under arthroscopy. A minimum 2- year follow-up in 40 patients. Arch Orthop Trauma Surg 2000;120:128-33. 45. Osbahr DC, Cawley PW, Speer KP. The effect of continuous cryotherapy on glenohumeral joint and subacromial space temperatures in the postoperative shoulder. Arthroscopy 2002;18:748-54. 46. Levy AS, Kelly B, Lintner S, Speer KP. Penetration of cryotherapy in treatment after shoulder arthroscopy. Arthroscopy 1997; 13:461-4. 47. Wilk KE, Arrigo CA, Andrews JR. Current concepts: the stabilizing structures of the glenohumeral joint. J Orthop Sports Phys Ther 1997;25:364-79. 48. Otte JW, Merrick MA, Ingersoll CD, Cordova ML. Subcutaneous adipose tissue thickness alters cooling time during cryotherapy. Arch Phys Med Rehabil 2002;83:1501-5. Suppliers a. Physitemp Industries Inc, 154 Huron Ave, Clifton, NJ 07013-2999. b. Omron Healthcare Inc, 300 Lakeview Pkwy, Vernon Hills, IL 60061.
Cryotherapy Does Not Impair Shoulder Joint Position Sense Geoffrey Dover, MS, CAT(c), ATC, Michael E. Powers, PhD, ATC, CSCS ABSTRACT. Dover G, Powers ME. Cryotherapy does not impair shoulder joint position sense. Arch Phys Med Rehabil 2004;85:1241-6. Objective: To determine the effects of a cryotherapy treatment on shoulder proprioception. Design: Crossover design with repeated measures. Setting: University athletic training and sports medicine research laboratory. Participants: Thirty healthy subjects (15 women, 15 men). Intervention: A 30-minute cryotherapy treatment. Main Outcome Measures: Joint position sense was measured in the dominant shoulder by using an inclinometer before and after receiving 30 minutes of either no ice or a 1-kg ice bag application. Skin temperature was measured below the tip of the acromion process and recorded every 5 minutes for the entire 30 minutes and immediately after testing. Three different types of error scores were calculated for data analyses and used to determine proprioception. Results: Separate analyses of absolute, constant, and variable error failed to identify changes in shoulder joint proprioception as a function of the cryotherapy application. Conclusions: Application of an ice bag to the shoulder does not impair joint position sense. The control of proprioception at the shoulder may be more complex than at other joints in the body. Clinical implications may involve modifying rehabilitation considerations when managing shoulder injuries. Key Words: Cryotherapy; Kinesthesis; Proprioception; Rehabilitation; Shoulder. © 2004 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation HERRINGTON FIRST DEFINED proprioception in 1906 and is credited with some landmark proprioception experS iments. Since then, many researchers have continued his work 1
in an attempt to determine peripheral control mechanisms. Sherrington1 originally defined proprioception as afferent information traveling to the central nervous system (CNS). More recently, the term proprioception has evolved to include measures of joint position sense (JPS), threshold to detection of passive movement, and force reproduction.2,3 Because measuring proprioceptive control is difficult, researchers have traditionally confined their work to observing motor output and inferring the underlying control processes.4 The most common methods used to quantify proprioception attempt to alter or perturb the afferent information during joint motion. The resultant change in motor output is then used to infer control processes.5-15 The goal of the modification tech-
From the Department of Exercise and Sport Sciences, University of Florida, Gainesville, FL (Dover); and Division of Athletic Training, Shenandoah University, Winchester, VA (Powers). No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors(s) or upon any organization with which the author(s) is/are associated. Reprint requests to Geoffrey Dover, MS, CAT(c), ATC, 160 FL Gym, PO Box 118207, Gainesville, FL 32611-8207, e-mail: [email protected]. 0003-9993/04/8508-8781$30.00/0 doi:10.1016/j.apmr.2003.11.030
nique is to affect the afferent information while not disturbing the mechanical properties of the muscles being tested.4 For example, in 3 different studies11,12,14 examining the effects of fatigue on force reproduction, the authors suggested a similar mechanism for proprioceptive control: afferent feedback, efferent signals, and some central mechanism. Despite these and other studies, the neural mechanisms of proprioception remain unclear. Most proprioception research has examined the elbow, wrist, knee, and ankle. Some authors5,6,8,9,11,12,14,16-20 have attempted to generalize their findings to other joints; however, proprioceptive control may differ depending on the joint tested. The exact mechanism of proprioceptive control remains unclear, particularly in the shoulder. Shoulder proprioception is indispensable because the glenohumeral joint (GHJ) relies primarily on dynamic restraint of the rotator cuff to maintain stability. Proprioception also may affect injury predisposition and rehabilitation. Several studies7,15-27 suggest that shoulder proprioception is impaired after fatigue, injury, and in overhand athletes. Lephart et al28 showed the relations among injury, proprioceptive deficits, and instability of the shoulder. Although the exact relation between proprioception and the cause of injury is unclear, clinicians commonly use proprioception exercises during rehabilitation of the shoulder because the rotator cuff is vital for GHJ stability.29-31 Cryotherapy is commonly used in the clinical setting to decrease pain and to reduce inflammation during injury management.32 Moreover, cryotherapy influences neuromuscular properties, including nerve conduction velocity and muscle contraction.33-40 This change in muscle electrophysiologic activity may be caused by a reduction of sodium, potassium, and calcium diffusion in nerves and at the motor endplate.38 Cryotherapy has become a common tool for disrupting afferent signals and modifying neuromuscular control while measuring proprioception. For example, 3 studies16-18 report the use of cryotherapy to disrupt afferent signals while measuring proprioception of the knee and the ankle. Two of these studies17,18 noted an impaired JPS after cryotherapy. Although cryotherapy is commonly used in the rehabilitation setting, the effects of cryotherapy on shoulder proprioception are unknown. Thus, the purpose of the present study was to assess shoulder JPS after a 30-minute cryotherapy session in healthy subjects. METHODS Participants Thirty volunteers from the university setting, 15 men (mean age ⫾ standard deviation [SD], 23.7⫾5.5y; height, 180.0⫾6.4cm; mass, 86.7⫾18.6kg) and 15 women (mean age ⫾ SD; 20.7⫾1.4y; height, 165.0⫾5.5cm; mass, 58.6⫾6.9kg) participated in the study. Results from a power analysis indicated that 30 subjects were sufficient to identify differences between error scores. Before participating, all subjects signed an informed consent agreement approved by the university’s institutional review board. Subjects were excluded from participation if they had any contraindications to cryotherapy, including areas of decreased sensation, areas of decreased blood flow, Raynaud’s disease, or any previous cold allergies or reactions. Subjects also were excluded if they participated in Arch Phys Med Rehabil Vol 85, August 2004
1242
CRYOTHERAPY AND SHOULDER JOINT POSITION SENSE, Dover
Fig 1. The inclinometer.
overhand athletics because of a possible effect on proprioception.21,22,27 Finally, subjects who had suffered a previous shoulder injury (including dislocation, subluxation, surgery, or any condition that caused pain during active movement) were excluded because these variables may affect proprioception.23-26 Instrumentation Thermometer and temperature probe. Skin surface temperature was measured by using a SST-1 flexible surface temperature probea with a contact surface area of 0.8cm2. The probe was connected to a thermometera with a range of 0° to 100°C and an accuracy of ⫾0.1°C. Inclinometer. An inclinometer (fig 1) was used for all range of motion (ROM) measurements and JPS testing. The inclinometer resembles a flat goniometer with a weighted arm inside and 360° marked in single-degree increments on its circumference. When the inclinometer is held upright, gravity pulls the inclinometer’s arm inferiorly and the measurement can be made. The angle measured is determined by comparing the location of the inclinometer’s arm with the degree markings around the circumference. We have previously reported41 that this particular inclinometer provides a very reliable (intertester, intratester) and valid method of assessing joint angles. We also reported41 that the inclinometer provides a very reliable measure of JPS. Measurements Joint position sense. All JPS testing was performed with subjects in the standing position. By using a Velcro strap, we secured the inclinometer to the subject’s wrist just proximal to the ulnar styloid process. Then we assessed total internal rotation (IR) and external rotation (ER) ROM while the shoulder and elbow were maintained, respectively, in 90° of abduction and flexion (fig 2). The subjects were instructed to actively rotate the shoulder to the end point of the range in both the IR and ER directions. They were further instructed to hold the end position while the angle was observed and recorded. The repositioning or target angles were then calculated according to the maximum angle each subject achieved. For the present study, the 2 target angles were equivalent to 90% of ER and 90% of IR ROM. Thus, the 2 target angles were 10% short of full IR and ER. These angles ensured that, despite varying Arch Phys Med Rehabil Vol 85, August 2004
ROM values across subjects, the target angle produced similar muscle length and sensations between subjects. To assess JPS, the principal investigator actively assisted the subject’s arm to the target angle and instructed the subject to hold the limb in that position for 3 seconds before returning the arm to the starting position. This time period, which has been used previously,22,41 enables the subject to become aware of the target angle without becoming fatigued. The subjects were blindfolded to eliminate any visual cues and, while the arm was at the target angle, they were told to concentrate on its position “in space.” After returning to the starting point, the subjects were instructed to immediately reposition the arm back to the target angle and inform the tester when they felt the position had been achieved. At this time, the angle observed on the inclinometer was recorded. The measurement was repeated 2 more times for a total of 3 trials and the order of IR and ER testing was randomized. The target angle and the repositioned angles were used to generate 3 types of error scores previously described by Schmidt and Lee42: absolute error, variable error, and constant error. The absolute error score is a measure of overall accuracy in performance and is calculated by measuring the absolute deviation between the target angle and the repositioned angle. Variable error measures the inconsistency and the variability of the participants’ repositioning by comparing the 3 repositioned trials to each other. Constant error represents the amount of deviation or bias of the motor outcome. This error score is the average magnitude of the movement and measures the direction of the errors between the trials and the target angle. Procedures Subjects reported to the testing site on 2 occasions: once for the cryotherapy treatment and once for the no-ice (control) condition. The sessions were separated by a minimum of 48 hours, and the testing order was randomly assigned on arrival. To begin the initial visit, demographic data including height, weight, age, arm dominance, percentage of body fat, and tri-
Fig 2. Subject position during JPS testing.
1243
CRYOTHERAPY AND SHOULDER JOINT POSITION SENSE, Dover
Fig 3. Subject positioning during cryotherapy treatment.
ceps skinfold measurements were measured and recorded. Arm dominance was determined as the arm the subject would naturally use to throw a ball. Only the dominant shoulder was measured in this study. We used a Body Logic Body Fat Analyzer model HBF-301 device and calipersb to evaluate percentage of body fat and measure the triceps skinfold. Following these measurements, subjects’ active IR and ER ROM were assessed by using the inclinometer. Once the target angles were calculated based on the available ROM, JPS testing began. After the initial JPS measurement, the temperature probe was placed on the shoulder and a baseline measure was recorded. Each subject then completed either the cryotherapy or the control condition. In the cryotherapy condition, a 1-kg bag of cubed ice was applied to the shoulder for 30 minutes. The center of the ice bag was applied over the tip of the acromion of the dominant shoulder. The ice bag was 20⫻25cm (surface area, 500cm2) in size and covered the deltoid and lateral portion of the scapula. Each ice bag was prepared in a similar manner and included weighing the bag and removing the air from it as suggested by others.32,43 The ice bag was secured to the shoulder by an elastic bandage. The same type of bandage was used for all subjects during the study, and each time was applied around the upper arm twice followed by once around the chest. After the ice bag was applied, subjects were placed in a supine position where they remained throughout the 30-minute treatment period (fig 3). The surface temperature probe was placed just inferior to the tip of the acromion process, and skin temperature was recorded every 5 minutes during the treatment and immediately after testing. For the control condition, subjects remained in the treatment position for 30 minutes with no ice bag application. Immediately after the cryotherapy or control condition, subjects resumed standing and the JPS testing was repeated. Statistical Analyses To determine a gender effect from the cryotherapy, the surface temperature data were first analyzed using a 2⫻2⫻8 mixed-design analysis of variance (ANOVA) with 1 betweensubjects factor (gender) with 2 levels (male, female) and 2 within-subjects factors: treatment with 2 levels (cryotherapy, control) and time with 8 levels (pre, 5, 10, 15, 20, 25, 30min, post). In addition, 2 independent t tests were used to determine if differences existed between percentage of body fat and skinfold thickness between men and women. After the gender analyses, 3 separate 2⫻2⫻2 (treatment by time by position) repeated-measures ANOVA were performed for absolute, con-
stant, and variable error scores. The designs were similar to the ANOVA above; however, the gender variable was removed and a third within-variable position (IR, ER) was included. An a priori level of significance was set at P less than .05 for all comparisons, and the Tukey honestly significant difference (HSD) test was used for all pairwise comparisons. RESULTS Gender Differences We found no significant differences when we compared male and female skin surface temperatures during the cryotherapy session (F7,196⫽1.75, P⫽.100). After the 30 minutes of cryotherapy, the mean male skin temperature ⫾ SD was 13.3°⫾2.8° and for females skin temperature was 13.0°⫾2.2°. Therefore, we combined the temperature data across the genders for the rest of the analyses. Moreover, no differences were observed between the percentage of body fat (t⫽⫺.798, P⫽.432) and skinfold thickness (t⫽⫺1.359, P⫽.185) between men and women (table 1). Because of the lack of gender differences, we combined the male and female error scores for the rest of the analyses. Surface Temperature A significant treatment by time interaction was observed for surface temperature (F7,203⫽674.28, P⫽.000) because temperature decreased significantly during the cryotherapy treatment, whereas no change occurred during the control condition (fig 4). The Tukey HSD procedure revealed no difference between the baseline temperatures of the cryotherapy and control sessions; however, we found differences when we compared individual time points after 5 minutes of cryotherapy with the baseline measure. Absolute Error Scores No significant differences were observed for absolute error after the cryotherapy session (treatment by time interaction) Table 1: Male and Female Body Composition Gender
% Body Fat
Skinfold (mm)
Male Female
15.9⫾7.4 17.8⫾5.4
11.9⫾4.3 13.6⫾3.6
NOTE. Values are mean ⫾ SD.
Arch Phys Med Rehabil Vol 85, August 2004
1244
CRYOTHERAPY AND SHOULDER JOINT POSITION SENSE, Dover
Fig 4. Skin temperatures, in control versus cryotherapy conditions.
(F1,29⫽1.875, P⫽.181) (table 2). Likewise, no other meaningful main effects or interactions were found to be significant.
DISCUSSION The primary finding of this study indicates that 30 minutes of cryotherapy does not impair shoulder JPS because no differences were observed when comparing error scores before and immediately after the ice bag treatment. There was no change in repositioning error after treatment, according to analyses that included direction bias and variability factors. These findings
conflict with the reports of 2 previous studies17,18 that investigated cryotherapy and proprioception in the knee and the ankle. Those authors reported that cryotherapy affected the afferent information from the periphery and altered the resulting motor output. The output, or JPS in the present case, is measured in degrees, and small differences are sufficient for statistical significance. Two previous studies32,44 measuring JPS of the knee reported that a mean difference of 1.7° between error scores was sufficient for statistical significance. They further suggested that conclusions can be inferred from those differences about proprioceptive control mechanisms. A similar difference was found to be statistically significant in the shoulders of overhand athletes.22 Although a small change in error scores is enough to identify a reliable, statistically significant difference, a question of clinical relevance exists. A difference of a few degrees cannot be observed accurately with the naked eye during an assessment. However, several studies16,17,19,22 have shown a significant change in proprioception with small changes in error scores in injured or predisposed populations, suggesting that these small differences may indeed be clinically significant. Despite the small difference in error scores previously shown to be statistically significant, we did not find these small error scores in the present investigation.
Table 2: JPS Absolute Error Scores
Table 3: JPS Variable Error Scores
Constant Error Scores Further analysis revealed no significant differences in constant error after the cryotherapy session (F1,29⫽.410, P⫽.527) (table 3). No other significant main effects or interactions were observed. Variable Error Scores No significant differences in variable error scores were observed after the cryotherapy treatment (F1,29⫽1.505, P⫽.230) (table 4). In addition, no other main effects or interactions were found to be significant.
Test Condition and Position
Control IR ER Cryotherapy IR ER
Pre (deg)
Post (deg)
4.5⫾2.5 3.4⫾1.9
3.9⫾1.9 3.1⫾1.7
4.5⫾2.8 2.9⫾1.6
4.1⫾2.1 3.8⫾2.2
NOTE. Values are mean ⫾ SD.
Arch Phys Med Rehabil Vol 85, August 2004
Test Condition and Position
Control IR ER Cryotherapy IR ER NOTE. Values are mean ⫾ SD.
Pre (deg)
Post (deg)
3.3⫾2.3 2.4⫾1.7
2.7⫾1.5 1.9⫾1.1
2.9⫾1.8 2.5⫾1.6
2.7⫾1.2 2.5⫾2.0
CRYOTHERAPY AND SHOULDER JOINT POSITION SENSE, Dover Table 4: JPS Constant Error Scores Test Condition and Position
Control IR ER Cryotherapy IR ER
Pre (deg)
Post (deg)
1.7⫾3.9 ⫺0.2⫾3.5
1.4⫾3.6 ⫺0.2⫾3.3
1.7⫾4.6 0.3⫾2.7
0.8⫾4.5 0.2⫾3.8
NOTE. Values are mean ⫾ SD.
In contrast to the 2 previously mentioned studies investigating cryotherapy and proprioception in the knee and the ankle,17,18 our subjects’ shoulder proprioception was not altered after a standard clinical application of cryotherapy. Previous studies11,12,14 have suggested that motor control is a combination of afferent and efferent information and some central mechanism. The afferent information from the GHJ may have been affected by the cryotherapy, but subjects were able to use peripheral information from other areas to modifying the motor response. Perhaps what little afferent information travels to the CNS is enough for the efferent or central command information to correct the JPS, despite the alteration caused by the cryotherapy in this experiment. Because the shoulder did not react to the cryotherapy in a manner similar to that of the knee or ankle, comparing JPS between joints would be useful in future research. The present study used 3 types of error scores to obtain comprehensive outcome measures on the repositioning task. Other studies12,14,19 have used multiple error scores for a similar reason. In studies in which researchers suspect a bias in a certain direction of error scores, constant error scores should be used because this measurement accounts any difference in direction.41 For example, when using a vibration stimulus, the limb is repositioned short of the target because of the “illusion” created that the limb is being stretched.8,9,20 In this example, constant error would be a useful measure because there is a direction of interest for the error in the repositioning. In addition, when using fatigue to alter proprioception in the elbow, there may be a resultant increase in the variable error in reproducing force.12,14 After fatigue, force reproduction trials increase in variability around the target. No study to date has reported a bias in proprioception or an increase in variable error after cryotherapy, so all 3 error scores were used in the analysis. No increase in bias or variability has been noted in shoulder JPS after cryotherapy. Previous research on the shoulder and cryotherapy has been conducted postoperatively. From those studies,45,46 researchers suggested that the GHJ is difficult to cool. For example, when glenohumeral and subacromial temperatures have been measured postoperatively, changes of only 1°C, on average, have been observed.45 Those authors used continuous cryotherapy for 23 hours with cold water flowing through a cuff around the shoulder postoperatively. Although a small temperature difference existed between the cold group and the control, the difference was still statistically significant. This finding suggests that the temperature within the GHJ may be difficult to lower to a level of clinical significance. In the present study, the shoulder may not have been cooled enough to measure a difference in the motor output. However, the skin surface temperatures (mean ⫾ SD, 14.5°⫾2.1°C) were lower than that (32°C) in the previously mentioned study.45 Thus, the deeper tissues may have cooled more than those previously reported. Both studies45,46 suggest that the subacromial space cools to a
1245
greater extent than the GHJ after cryotherapy. This finding has clinical importance because the tendons from the rotator cuff musculature (the muscle group of interest in the present study) travel through this space.47 Although we standardized the weight of the ice bag, we did not standardize the relative area of ice bag coverage for each subject. Thus, our smaller subjects might have had a greater application area than our larger subjects. However, we do not believe that this would confound our results because the subacromial space and glenohumeral areas were included for all subjects. Previous research48 suggests that differences in body fat percentage may affect cooling rate. Because body fat and skinfold thickness may be greater in women than in men, the rate of cooling might differ between genders. In the current study, percentage of body fat and skinfold thickness measurements were slightly higher in women; yet, these differences were not statistically significant (see table 1). This lack of difference between the male and female subjects may explain the similarity in cooling. CONCLUSIONS The present findings did not support the hypothesis that cryotherapy impairs shoulder JPS. Clinicians should be aware of this information in making decisions during rehabilitation of shoulder injuries. Acknowledgment: We thank James Cauraugh for his invaluable contributions revising the manuscript. References 1. Sherrington CS. On the proprio-ceptive system, especially in its reflex aspect. Brain 1906;29:467-82. 2. Jones LA. Peripheral mechanisms of touch and proprioception. Can J Physiol Pharmacol 1994;72:484-7. 3. Riemann BL, Lephart SM. The sensorimotor system, Part I: The physiologic basis of functional joint stability. J Athl Train 2002; 37:71-9. 4. Kelso JA, Holt KG, Flatt AE. The role of proprioception in the perception and control of human movement: toward a theoretical reassessment. Percept Psychophys 1980;28:45-52. 5. Brockett C, Warren N, Gregory JE, Morgan DL, Proske U. A comparison of the effects of concentric versus eccentric exercise on force and position sense at the human elbow joint. Brain Res 1997;771:251-8. 6. Burgess PR, Jones LF. Perceptions of effort and heaviness during fatigue and during the size-weight illusion. Somatosens Mot Res 1997;14:189-202. 7. Carpenter JE, Blasier RB, Pellizzon GG. The effects of muscle fatigue on shoulder joint position sense. Am J Sports Med 1998; 26:262-5. 8. Cordo P, Gurfinkel VS, Bevan L, Kerr GK. Proprioceptive consequences of tendon vibration during movement. J Neurophysiol 1995;74:1675-88. 9. Goodwin GM, McCloskey DI, Matthews PB. Proprioceptive illusions induced by muscle vibration: contribution by muscle spindles to perception? Science 1972;175:1382-4. 10. Jones LA, Hunter IW. Effect of fatigue on force sensation. Exp Neurol 1983;50:640-50. 11. McCloskey DI, Ebeling P, Goodwin GM. Estimation of weights and tensions and apparent involvement of a “sense effort”. Exp Neurol 1974;42:220-32. 12. Saxton JM, Clarkson PM, James R, et al. Neuromuscular dysfunction following eccentric exercise. Med Sci Sports Exerc 1995;27: 1185-93. 13. Stevens JC, Cain WS. Effort in isometric muscular contractions related to force level and duration. Percept Psychophys 1970;8: 240-4. 14. Vincent HK, Carlson C, Hyatt JP, Yihua L, Vincent KR. Alterations in bilateral force judgment following strenuous eccentric exercise. Res Q Exerc Sport 2000;71:340-8. Arch Phys Med Rehabil Vol 85, August 2004
1246
CRYOTHERAPY AND SHOULDER JOINT POSITION SENSE, Dover
15. Voight ML, Hardin JA, Blackburn TA, Tippett S, Canner GC. The effects of muscle fatigue on and the relationship of arm dominance to shoulder proprioception. J Orthop Sports Phys Ther 1996;23: 348-52. 16. Thieme HA, Ingersoll CD, Knight KL, Ozmun JC. Cooling does not affect knee proprioception. J Athl Train 1996;31:8-11. 17. Uchio Y, Ochi M, Fujihara A, Adachi N, Iwasa J, Sakai Y. Cryotherapy influences joint laxity and position sense of the healthy knee joint. Arch Phys Med Rehabil 2003;84:131-5. 18. Hopper D, Whittington D, Davies J, Chartier JD. Does ice immersion influence ankle joint position sense? Physiother Res Int 1997;2:223-36. 19. Feuerbach JW, Grabiner MD, Koh TJ, Weiker GG. Effect of an ankle orthosis and ankle ligament anesthesia on ankle joint proprioception. Am J Sports Med 1994;22:223-9. 20. Calvin-Figuiere S, Romaiguere P, Gilhodes JC, Roll JP. Antagonist motor responses correlate with kinesthetic illusions induced by tendon vibration. Exp Brain Res 1999;124:342-50. 21. Allegrucci M, Whitney S, Lephart S, Irrgang J, Fu F. Shoulder kinesthesia in healthy unilateral athletes participating in upper extremity sports. J Orthop Sports Phys Ther 1995;21:220-6. 22. Dover GC, Kaminski TW, Meister K, Powers ME, Horodyski M. Assessment of shoulder proprioception in the female softball athlete. Am J Sports Med 2003;31:431-7. 23. Lephart SM, Myers JB, Bradley JP, Fu FH. Shoulder proprioception and function following thermal capsulorraphy. Arthroscopy 2002;18:770-8. 24. Warner JJ, Lephart S, Fu FH. Role of proprioception in pathoetiology of shoulder instability. Clin Orthop 1996;Sep(330):35-9. 25. Machner A, Merk H, Becker R, Rohkohl K, Wissel H, Pap G. Kinesthetic sense of the shoulder in patients with impingement syndrome. Acta Orthop Scand 2003;74:85-8. 26. Smith RL, Brunolli J. Shoulder kinesthesia after anterior glenohumeral joint dislocation. Phys Ther 1989;69:106-12. 27. Safran MR, Borsa PA, Lephart SM, Fu FH, Warner JJ. Shoulder proprioception in baseball pitchers. J Shoulder Elbow Surg 2001; 10:438-44. 28. Lephart SM, Pincivero DM, Giraldo JL, Fu FH. The role of proprioception in the management and rehabilitation of athletic injuries. Am J Sports Med 1997;25:130-7. 29. Wilk KE, Arrigo C. Current concepts in the rehabilitation of the athletic shoulder. J Orthop Sports Phys Ther 1993;18:365-78. 30. Hayes K, Callanan M, Walton J, Paxinos A, Murrell GA. Shoulder instability: management and rehabilitation. J Orthop Sports Phys Ther 2002;32:497-509. 31. Kibler WB, McMullen J, Uhl T. Shoulder rehabilitation strategies, guidelines, and practice. Orthop Clin North Am 2001;32:527-38. 32. Knight KL. Cryotherapy in sport injury management. Champaign: Human Kinetics; 1995.
Arch Phys Med Rehabil Vol 85, August 2004
33. Abramson DI, Chu LS, Tuck S Jr, Lee SW, Richardson G, Levin M. Effect of tissue temperatures and blood flow on motor nerve conduction velocity. JAMA 1966;198:1082-8. 34. Bell KR, Lehmann JF. Effect of cooling on H-reflexes and Treflexes in normal subjects. Arch Phys Med Rehabil 1987;68: 490-3. 35. De Jesus PV, Hausmanowa-Petrusewicz I, Barchi RL. The effect of cold on nerve conduction of human slow and fast nerve fibers. Neurology 1973;23:1182-9. 36. Halar EM, DeLisa JA, Brozovich FV. Nerve conduction velocity: relationship of skin, subcutaneous and intramuscular temperatures. Arch Phys Med Rehabil 1980;61:199-203. 37. Krause BA, Hopkins JT, Ingersoll CD, Cordova ML, Edwards J. The relationship of ankle temperature during cooling and rewarming to the human soleus H reflex. J Sport Rehabil 2000;9:253-62. 38. Rutkove SB. Effects of temperature on neuromuscular electrophysiology. Muscle Nerve 2001;24:867-82. 39. Bergh U, Ekblom B. Influence of muscle temperature on maximal muscle strength and power output in human skeletal muscles. Acta Physiol Scand 1979;107:33-7. 40. Sargeant AJ. Effect of muscle temperature on leg extension force and short-term power output in humans. Eur J Appl Physiol Occup Physiol 1987;56:693-8. 41. Dover G, Powers ME. Reliability of joint position sense and force-reproduction measures during internal and external rotation of the shoulder. J Athl Train 2003;38:304-10. 42. Schmidt RA, Lee TD. Motor control and learning. 3rd ed. Champaign: Human Kinetics; 1999. p 18-35. 43. Merrick MA, Knight KL, Ingersoll CD, Potteiger JA. The effects of ice and compression wraps on intramuscular temperatures at various depths. J Athl Train 1993;28:236-45. 44. Adachi N, Ochi M, Uchio Y, Sumen Y. Anterior cruciate ligament augmentation under arthroscopy. A minimum 2- year follow-up in 40 patients. Arch Orthop Trauma Surg 2000;120:128-33. 45. Osbahr DC, Cawley PW, Speer KP. The effect of continuous cryotherapy on glenohumeral joint and subacromial space temperatures in the postoperative shoulder. Arthroscopy 2002;18:748-54. 46. Levy AS, Kelly B, Lintner S, Speer KP. Penetration of cryotherapy in treatment after shoulder arthroscopy. Arthroscopy 1997; 13:461-4. 47. Wilk KE, Arrigo CA, Andrews JR. Current concepts: the stabilizing structures of the glenohumeral joint. J Orthop Sports Phys Ther 1997;25:364-79. 48. Otte JW, Merrick MA, Ingersoll CD, Cordova ML. Subcutaneous adipose tissue thickness alters cooling time during cryotherapy. Arch Phys Med Rehabil 2002;83:1501-5. Suppliers a. Physitemp Industries Inc, 154 Huron Ave, Clifton, NJ 07013-2999. b. Omron Healthcare Inc, 300 Lakeview Pkwy, Vernon Hills, IL 60061.