Sensory Adaptation After a 2-Week Stretching Regimen of the Rectus Femoris Muscle

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1 1245 Sensory Adaptation After a 2-Week Stretching Regimen of the Rectus Femoris Muscle Martin Björklund, PT, Jern Hamberg, MD, Albert G. Crenshaw, PhD ABSTRACT. Björklund M, Hamberg J, Crenshaw AG. MUSCLE STRETCHING EXERCISES are commonly Sensory adaptation after a 2-week stretching regimen of the applied as flexibility training in sports activities. 1 In rectus femoris muscle. Arch Phys Med Rehabil 2001;82: Objective: To study the effects of a muscle stretching regimen for the rectus femoris muscle on subjective stretch sensation and range of motion (ROM). Design: A2 2 crossover design comprising 2 treatments and 2 intervention periods. Setting: A military base in Sweden. Participants: A volunteer sample of 29 male military conscripts divided into 2 groups, with each group subjected to both experimental and control treatments at different time periods. Intervention: Two weeks of supervised stretching (4 times/ wk) of the rectus femoris muscle (experimental treatment) and the calf muscles (control treatment). Main Outcome Measures: Subjective rating of the stretch sensation for the anterior aspect of the thigh determined on a category ratio scale. Passive knee flexion ROM determined on each test with the same applied torque, specific for each subject. Results: An additive analysis of variance revealed that the stretch sensation after the experimental treatment was decreased, compared with the control treatment (p.01). The knee flexion, however, remained the same regardless of the treatment. Conclusion: Sensory adaptation seems to be an important mechanistic factor in the effect stretching has on ROM changes. The lack of change in knee flexion suggests that the stretching, as performed in this study, did not influence stiffness of the rectus femoris muscle. Sensory adaptation may also be an underlying mechanism in the alleviating effect of stretching when applied to tired, tender, and painful muscles. Key Words: Knee; Muscles; Range of motion, articular; Rehabilitation by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation From the Centre for Musculoskeletal Research, National Institute for Working Life, Umeå (Björklund, Hamberg, Crenshaw); Stiftelsen Alfta Kurhem, Alfta Rehab Center, Alfta (Björklund, Hamberg); and the Department of Surgical and Perioperative Science, Sports Medicine Unit, University of Umeå, Umeå (Björklund, Hamberg), Sweden. Accepted in revised form September 15, Supported by the Swedish Council for Work Life Research and Stiftelsen Alfta Kurhem. 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 or upon any organization with which the authors are associated. Reprint requests to Albert G. Crenshaw, PhD, Centre for Musculoskeletal Research, National Institute for Working Life, Box 7654, S Umeå, Sweden, albert.crenshaw@niwl.se /01/ $35.00/0 doi: /apmr clinical rehabilitation, they are used to diminish muscle tenderness and tension, as well as to enhance range of motion (ROM). 2,3 Thus, there are many studies aimed at determining the most effective type of stretching, the optimal frequency and duration of stretch, and the placement of stretch exercise within a workout. 4,5 In workplace settings, where workers assume static postures and perform monotonous work tasks, stretching is recommended as a self-administered micropause to prevent and/or alleviate discomfort. To this end, workplace stretching programs as ergonomic interventions have been successfully implemented. 6 Despite its widespread use and the vast research literature, the mechanism behind the effects of stretching remains controversial. A reduction in passive stiffness of the muscle tendon unit is a largely accepted, presumed mechanism for the beneficial effects of stretching. In this regard, Madding et al 7 and Toft et al 8 showed reduced passive tension after stretching of the hip adductors and the calf muscles, respectively. Furthermore, Rosenbaum and Hennig 9 showed reduced stiffness, assessed by Achilles tendon reflex force characteristics, after stretching the calf muscles. Of late, some researchers have challenged the dogma of stretch effects on passive stiffness as the sole mechanistic explanation for the benefits associated with stretching. 1,10 In particular, recent studies involving long-term flexibility stretch training, as well as acute effects of single stretching maneuvers, produced significant increases in ROM but found either no change in stiffness, or only minor short lasting changes. Thus, the authors of these studies attributed their findings to an increased subjective stretch tolerance (ie, the stretch was believed to yield an adaptive or a sensory effect), rather than decreases in passive tension. This study was undertaken to shed light on the controversy about the mechanism behind the effects of stretching. We designed a 2-week stretching regimen and then assessed its effects on ROM and on subjective stretch sensation. Rather than study hamstrings, of which stretching studies are abundant, 11 we chose to study the rectus femoris muscle, which has rarely been the focus of investigations into stretching. This is somewhat surprising, because the rectus femoris muscle is a 2-joint postural muscle that is susceptible to tightness and is often subjected to stretch exercises for sports activities at both the novice and the elite levels. 19,20 In addition, several clinical disorders associated with tight rectus femoris muscles have been reported, 21 and it is suspected that tight rectus femoris muscles contributes to low back pain and alter movement patterns. 16,18,22 Therefore, our objective was twofold: (1) to elucidate the mechanism of the effects of muscle stretching; and (2) to present stretch data for a poorly understood but important muscle group. METHODS Thirty-five male military conscripts volunteered to participate in the study. Subjects received written information about the experiment 2 weeks before its start. Only subjects who regarded themselves as having healthy hips and knees and did

2 1246 STRETCHING OF THE RECTUS FEMORIS MUSCLE, Björklund not have a history of rheumatologic, orthopedic, or neurologic disorders were included. During the preliminary interview, 4 subjects were found not to fit the criteria, reducing the study population to 31. The subjects were then arbitrarily divided into 2 groups: 16 subjects in group A and 15 subjects in group B. One subject from each group subsequently dropped out during the study, one because of illness and one because of a lack of interest. The physical characteristics of the study group (n 29) were as follows (mean standard deviation [SD]): age, years; height, cm; weight, kg. There was no significant difference for these anthropometric data between the groups. The range of passive knee flexion and subjective rating of stretch sensation were considered dependent variables, and the independent variable was stretching of the rectus femoris muscle. All measurements were taken by the same physical therapist, who had no knowledge of the subjects groupings. A physical therapist and experimental assistants supervised the stretch training. A questionnaire was used to obtain information on subjects training and stretching habits. Informed consent was given by each subject, and the study was conducted in accordance with the Declaration of Helsinki guidelines. Range of Passive Knee Flexion To obtain a quantitative measure of the stretchability of the rectus femoris muscle, passive knee flexion was determined according to Evjenth and Hamberg 23 (fig 1). This method is reliable and valid and was described in detail previously. 24 The measurement device consisted of an electronic goniometer a and pressure transducer b with a bridge amplifier c for the purpose of measuring the knee flexion and the applied force, respectively. The goniometer and pressure transducer were connected to a computer that registered the knee flexion when a preprogrammed torque was reached (see below). Figure 2 illustrates the placing of the instruments on the subjects. The following sequence describes the measurement procedure. The subject, dressed in shorts, squatted 10 times to limber up. He was then placed in the starting position for measurement of left knee flexion, and the test leader placed a pressure transducer against the cuff of the goniometer, and slowly flexed the subject s knee (approximate rate, 8 /s) until the computer signaled that the preprogrammed torque had been reached. Simultaneously, the knee flexion (in degrees) was automatically registered in the computer, which was not visible to the test leader. The measurements were repeated twice more on the left leg. Then the Fig 2. Placing the instruments on the subject. subject stood, the cuff of the goniometer was shifted to the right leg, and the procedure was repeated. In total, 6 measurements of knee flexion were acquired per subject. From these, a mean was calculated to represent a single knee flexion value per subject and per test occasion. Subjective Rating of Stretch Sensation The subjects rated the stretch sensation at the anterior aspect of the thigh on a category ratio scale 25,26 (table 1). The rating was made at each measurement of knee flexion when the preprogrammed torque was reached, as signaled by the computer. In total, 6 ratings of stretch sensation were acquired per subject on each test occasion, and from these a mean was calculated to represent a single value of rating of stretch sensation per subject and per test occasion. Preprogrammed Torque On the first test occasion, the magnitude of the applied torque with which the subject s knee was flexed by the tester was determined and stored in the computer. This value was designated as the preprogrammed torque. This was accomplished in the following manner. The tester flexed the subject s right knee joint (fig 1), and the subject was asked to say when the stretch sensation at the anterior aspect of the thigh was strong (at 5 on the category scale, table 1). This maneuver was repeated 3 times with the same leg to acquaint the subject with the rating procedure. The force applied in the fourth flexion that elicited a rating of 5 from the subject was registered in the computer. The same procedure was repeated with the left leg, Table 1: Category Scale According to Borg. 25,26 Fig 1. Knee flexion method according to Evjenth and Hamberg Nothing at all 0.5 Extremely weak (just noticeable) 1 Very weak 2 Weak (light) 3 Moderate 4 Somewhat strong 5 Strong (heavy) 6 7 Very strong Extremely strong (almost maximal)

3 STRETCHING OF THE RECTUS FEMORIS MUSCLE, Björklund 1247 Figure 3. Schematic description of the experimental design and a mean value of the applied forces for the 2 legs was calculated and used as the preprogrammed torque for that subject. This same value was used at each test occasion for that particular subject. To convert the force measurements to torque, the distance between the lateral epicondyle of the femur and the lower border of the lateral malleolus of the fibula of the subject was measured and stored into the computer program and represented the lever arm for the force. Also, the torque acting on the subject s knee joint, because of the weight of his lower leg, was calculated according to Dempster s data. 27 Thus, compensation for the weight of the lower leg was included in the computer program. Experimental Design Figure 3 provides a schematic description of the experimental design. Data were acquired on 5 test occasions extending over 9.5 weeks. The measurements from test occasions 1 and 2 were used to assess the test-retest reliability. The study was arranged as a 2 2 crossover design comprising 2 treatments (experimental and control, sham treatment) and 2 intervention periods. The intervention periods were separated by a wash-out period of 3 weeks. In the first intervention period (between test occasions 2 and 3), group A was allocated the experimental treatment and group B the control treatment. In the second intervention period (between test occasions 4 and 5), group B received the experimental treatment and group A the control treatment. The experimental treatment consisted of stretching the rectus femoris muscle 4 times a week during the intervention period of 2 weeks. Control treatment consisted of stretching the superficial and deep calf muscles with the same frequency and duration as the experimental treatment. Experimental Treatment The experimental treatment, performed as supervised group training, consisted of the following steps during 1 training session: (1) a 3-minute warm-up by jogging; (2) performing 10 squats; and (3) stretching the rectus femoris muscle according to Evjenth and Hamberg 20 (fig 4). This procedure requires 5 seconds of isometric contraction of the knee extensors, 2 to 3 seconds of relaxation, 20 seconds of stretching, and a repeat of the same sequence without returning to standing position. The procedure is then repeated with the opposite leg. Once more, each leg undergoes the stretching sequence. In all, each leg is stretched twice (2 20s each time), resulting in a total stretch duration of 80 seconds per leg at each training session. Control Treatment The control (sham) treatment, performed as supervised group training, consisted of the following steps during 1 training session: (1) a 3-minute warm-up by jogging; (2) performing 10 squats; and (3) stretching the superficial and deep calf muscles, again, according to Evjenth and Hamberg. 20 The procedure starts with the superficial calf muscles: 5 seconds of isometric contraction of the plantarflexors, 2 to 3 seconds of relaxation, 20 seconds of stretching, and a repeat of the same sequence for the deep calf muscles. The procedure is repeated with the opposite leg, and then both legs again undergo the stretching sequence. In all, each leg is stretched twice, with both the superficial and deep calf muscles stretched 1 20 seconds, resulting in a total stretch duration of 80 seconds per leg in each training session. Data Handling and Statistical Analyses A program designed in-house, d running on an IBM compatible personal computer, was used to collect knee flexion data. The stretch sensation ratings were collected manually and subsequently stored in the computer. Data analysis was based on each subject s mean range of passive knee flexion and mean rating of stretch sensation per test occasion (right and left legs grouped together). To determine test-retest reliability, paired t tests and Pearson s product-moment correlation coefficient were calculated from the measurements obtained from tests 1 and 2. An additive 3-way analysis of variance (ANOVA), using the statistical program MINITAB 12 e for Windows, was used to determine differences before and after the intervention periods. The 3 factors of the ANOVA were treatment (experimental, control), intervention period (first, second) and subject (n 29). For all analyses, the level of significance was set at p less than.05. Fig 4. Stretching of the rectus femoris muscle according to Evjenth and Hamberg. 20

4 1248 STRETCHING OF THE RECTUS FEMORIS MUSCLE, Björklund Table 2: Subjective Rating of Stretch Sensation on a Category Scale Treatment Before After Control Experimental NOTE. Values are means SDs. ANOVA detected a significant decrease after the experimental treatment compared with the control treatment (p.01). RESULTS There was no systematic variation of the ratings of stretch sensation from test occasion 1 to 2 (p.21), and the data between occasions correlated well (r.71, p.001). The range of passive knee flexion decreased 2.3 from test occasion 1to2(p.01) and the data between occasions correlated highly (r.97, p.001). Subjective Rating of Stretch Sensation Table 2 shows the average category scale ratings before and after control and experimental treatments. The 3-way ANOVA revealed a significantly decreased category scale rating after experimental treatment when compared with the control treatment (p.01). No difference was seen for results obtained in the first intervention period as compared with the second intervention period (p.83, factor intervention period), or for differences between subjects in their responses to treatments (p.06, factor subject). Range of Passive Knee Flexion Table 3 shows the average range of passive knee flexion before and after control and experimental treatments. The 3-way ANOVA showed no significant change in knee flexion after the experimental treatment compared with the control treatment (p.42). Also, no difference existed between results obtained in the 2 intervention periods (p.73) or between subjects in their responses to treatments (p.32). DISCUSSION This study showed a decreased sensation to stretching for the anterior aspect of the thigh after a 2-week stretching regimen of the rectus femoris muscle. This was revealed by measuring knee flexion with a preprogrammed torque (the same value used for all test occasions for a particular subject), and the subject concomitantly rating the stretch sensation. To our knowledge, this study is the first to show sensory adaptation after stretching of this muscle. Other studies of the rectus femoris muscle present data showing an increased ROM but without regard to stiffness or stretch sensation Therefore, such studies contribute little toward understanding the mechanisms behind the acquired increase in ROM after stretching. Our findings suggest that sensory adaptation may be an important mechanistic factor. Studies of the hamstrings by Halbertsma and Göeken 11 and Magnusson et al, 15 via increased stretch tolerance, also provide evidence of sensory adaptation from stretching. In these studies, the stretch regimens were appreciably more intensive than were ours, both in the length of training periods and the frequency of stretching sessions. Hardy, 31 however, showed gains in hip flexion comparable to gains reported by Magnusson 15 after only 1 week with a total stretch time of 360 seconds. Hardy s results induced Magnusson to postulate that a considerably smaller amount of stretch stimuli would be needed to bring about the changes in stretch tolerance that they found. In our study, the 2-week intervention period, comprising a total stretch time of 320s/wk, corroborates this notion. The mechanistic explanation for the demonstrated sensory adaptation (ie, which receptors were responsible for the reduced stretch sensation), is not readily apparent. Magnusson 15 speculated about nociceptive nerve endings in the joint and muscle as possible structures accounting for the increase in stretch tolerance. Other candidates might be mechanoreceptors and proprioceptors that show reduced firing after single stretch maneuvers. 32 In our laboratory, direct measurements of muscle spindle afferents showed reduced activity immediately after large amplitude stretching of the cat hindlimb muscle (unpublished data). The effect of a stretch training regime on proprioceptors, however, has not been established. No increase in range of passive knee flexion was found in this study, which can be interpreted to mean that the passive stiffness of the muscle was unaffected by the stretch regimen. This is not to say, however, that a change in the muscle stiffness would not have occurred had we used a more intense stretching protocol. It may be assumed that sensory adaptation precedes changes in stiffness. Our finding of a lack of change in stiffness contradicts other studies that report reduced stiffness after single stretch sessions, 7-9 as well as after a long-term stretching regimen. 8 Discrepancies between studies may partially result from the different muscle groups studied. The studies that reported reduced stiffness involved the hip adductors 7 and calf muscles, 8,9 whereas our results, and the studies cited that support sensory adaptation, involved the quadriceps and hamstrings. Cross-sectional area, shortening velocity, and pennation angles are reported to be important factors for the passive properties of a muscle. 33 The design of the study may also be a factor that gives preference to data interpretation as either sensory adaptation or a change in passive stiffness. In our experimental design, we used the preprogrammed torque as the end-point criterion during passive knee flexion while recording the sensation to stretching. Had we used stretch sensation as the definitive criterion (ie, passive knee flexion until reaching the same magnitude of sensation after the stretching regimen as that recorded before), it would be reasonable to assume an increase in ROM. To test this assumption, we selected a subgroup of 12 of our subjects who had rated consistently lower stretch sensation at the posttest. The subgroup was then retested, but this time with stretch sensation as the end-point criterion (ie, the same magnitude of stretch sensation as that rated before the experimental treatment), instead of the predetermined torque. The outcome of this test showed a significantly increased ROM of about 15. This magnitude corresponds well with the mean increase of 17 reported by Magnusson 15 for the hamstrings. We used a reliable and validated stretchability test for the rectus femoris muscle, 24 and the test-retest reliability for the studied group was high (r.97). Therefore, the changed knee flexion between tests 1 and 2 is somewhat perplexing. It may be related to the fact that the time interval between tests 1 and 2 was 2.5 weeks and the subjects activities Table 3: Range of Passive Knee Flexion Treatment Before After Control Experimental NOTE. Values are means SDs. ANOVA showed no significant change after the experimental treatment compared with the control treatment (p.42).

5 STRETCHING OF THE RECTUS FEMORIS MUSCLE, Björklund 1249 during this period were not controlled to the same extent as they were in the intervention periods. However, our use of a crossover design reduced the impact that these changes may have had on our overall results. Because the muscle s electric activity was not measured, we cannot state that the passive knee flexion tests were entirely passive. However, a plethora of data suggests that passive ROM tests to an end point that precedes a pain-eliciting end point will not evoke significant electric activity from the stretched muscle. 14,34 In addition, the velocity with which the subjects were tested for knee flexion was probably well below that needed to stimulate stretch reflexes. 35 The injury-preventing and performance-promoting effects of stretching empirically defend its widespread use in conjunction with sports activities. There is, however, a scarcity of controlled studies and, with regard to the sensory explanation of the mechanism behind stretching, of tenable mechanistic models to support the rationale for stretching before exercise. 1,10,36 A practical consequence of muscle stretching in normal daily situations, as well as in clinical instances, is that people feel suppler and relieved. This may suggest sensory changes, rather than changes in material properties, when the mechanism of sensory adaptation is considered. Myofascial pain patients experienced a decrease in trigger point sensitivity, as assessed by a pressure algometer, after passive stretch. 37 This may imply that a mechanism of sensory adaptation after stretch applies both to normal muscles and to painful muscles, where high threshold mechanoreceptors are believed to be sensitized. 38 CONCLUSION This study showed a reduced stretch sensation after 2 weeks of stretching of the rectus femoris muscle, which indicates that stretching as described here may induce sensory adaptation rather than changes in stiffness. It is suggested that sensory adaptation is important for the ROMenhancing effects of muscle stretching. However, research is indicated to clarify the receptor part of the mechanism and for determining the effect of stretching on different subpopulations of patients. Acknowledgments: The authors thank Bengt Nordgren, Department of Neuroscience, Rehabilitation Medicine, Uppsala University, for scientific support of this work. 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6 1250 STRETCHING OF THE RECTUS FEMORIS MUSCLE, Björklund 33. Gareis H, Solomonow M, Baratta R, Best R, D Ambrosia R. The isometric length-force models of nine different skeletal muscles. J Biomech 1992;25: McHugh MP, Kremenic IJ, Fox MB, Gleim GW. The role of mechanical and neural restraints to joint range of motion during passive stretch. Med Sci Sports Exerc 1998;30: Davidoff RA. Skeletal muscle tone and the misunderstood stretch reflex. Neurology 1992;42: Shrier I. Stretching before exercise does not reduce the risk of local muscle injury: a critical review of the clinical and basic science literature. Clin J Sport Med 1999;9: Jaeger B, Reeves JL. Quantification of changes in myofascial trigger point sensitivity with the pressure algometer following passive stretch. Pain 1986;27: Mense S. Nociception from skeletal muscle in relation to clinical muscle pain. Pain 1993;54: Suppliers a. Orto-Ranger II; MI Tech Inc, Remcat Trade AB, Box 5011, S Vällingby, Sweden. b. Strain gauge type RM-50 KA; Meproel Instrument AB, Box 29016, S Stockholm, Sweden. c. Bridge amplifier type ABA-02; IPM-Electronic AB, Box 6003, S Vällingby, Sweden. d. Data collection card, Burr Brown PCI 20002M-1; Metric Teknik, Box 1494, Solna, Sweden. e. Minitab Inc, 3081 Enterprise Dr, State College, PA