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( J N ~ uo!lel!l!3ej ) ~ e l n ~ s n w o ~ nan!ldaso!~doJd au :jxa)uo3 270 Carter et al at least 1researcher reported that when stretching was incorporated as a component of a fitness program, no attributable benefits were found.ll Researchers agree that proprioceptive neuromuscular facilitation (PNF) stretching techniques elicit maximal improvements in joint range of motion in the shortest amount of tirne.3,78,11,19,20 Three steps occur during PNF stretching techniq~es*,~,~~: The muscle is passively stretched, allowing the stretch receptors of the muscle spindle to get used to the new, increased range of muscle length; in the stretched position, the muscle contracts isometrically against resistance; this contraction activates the Golgi tendon organs more than the passive stretch alone does and causes many of the fast-twitch fibers of the muscle to fatigue. This fatigue makes it more difficult to produce a stretch reflex, and the muscle is passively stretched again through the resulting increased range of motion. This passive stretch inhibits the muscle even more from causing a stretch reflex. Based on the research on PNF stretching, many athletic teams have adopted PNF stretching as part of their precompetition warm-up.21It is believed that PNF stretching diminishes the stretched muscle's ability to produce a stretch r e f l e ~ . ~Thus, , ~ ~it~becomes ,~~ important to determine whether PNF stretching inhibits involuntary movements that can be protective in nature. The purpose of this investigation was to determine how a commonly used PNF stretching technique affects the neuromuscular response of selected posterior thigh musculature during rapid elongation. Materials and Methods Subjects Twenty-four women were recruited for participation (means:height = 167.27 cm; weight = 58.92 kg; age = 21.42 years; percent body fat = 18.41; body mass index = 21.06 kg/m2). After an explanation of the study's purpose, each subject signed an informed consent form approved by The University of Mississippi's Institutional Review Board. Preparatory Protocol The subjects were prepared for electromyography (EMG) electrode placement. Any body hair in the area of electrode placement was removed. Pregelled, silver-silver chloride bipolar surface electrodes (MedicotestA/ S, Rugmaken, Denmark) were placed according to the methods described by Basmajian and D e L u ~ awith , ~ ~ a center-to-center intereledrode distance of 2.5 cm on the skin over the biceps femoris and semitendinosus muscle bellies. A reference electrode was placed at the bony prominence of the wrist. Muscle identification was achieved through manual muscle testing using resistive knee flexion from the supine position. Once positioned PNF and Rapid Muscle Lengthening 271 properly, the electrodes were not removed until the pretest and posttest data had been collected. Subjectswere also fitted with standard stereo headphones, playing music from a radio, and a blindfold. The purpose of the headphones and blindfold was to limit the subjects' awareness of their surroundings and to distract their attention so that the stretching stimulus would be surprising. Instrumentation The analog signalswere converted to digital signals via an analog-to-digital converter interfaced with a desktop computer. Both signals were collected using Run Technologies DataPac 111Version 2.00 software (Laguna Hills, Calif).Two channels of the Noraxon Telemyo (Scottsdale,Ariz) telemetered EMG system (bandwidth = 10-2000 Hz; amplifier impedance < 10 flohm; CMMR = 85 db; gain = 1000)were used to record the activity of the biceps femoris and semitendinosus muscles. The EMG signals were sampled at 1000 Hz and processed, using passive demeaning and root-mean-square smoothing (100-millisecond time constant), and notch filtered at 60 and 110 Hz. A third and separate time-matched channel was used to record when the initiation of the stimulus occurred. Involuntary Movement Assessment As shown in Figure 1,the device used to create involuntary movement of the lower leg was attached to the end of a treatment table. The device consisted of 2 two-by-fours extending the table by 17.25 in. A 1-in dowel rod joined the 2 two-by-fours and could be adjusted at 3-in intervals, depending on each subject's femur length. The dowel rod was padded to assist in subject comfort.An ankle cuff was attached to a cable, which fed through 2 frictionless pulleys and was attached to a circular 5-lb weight. The weight rested in its initial position: on a pin attached to a solenoid that was stabilized and connected to 2 two-by-fours. The solenoid had a 20-ft-long alternating-current (AC) cord with a flip switch and was fitted with an AC plug. Just below the solenoid was a weight-drop trigger switch; when the 5-lb weight struck this trigger switch, a 5-V signal was sent to the computer. Using free-fall equations of motion, it was determined that the rapid elongation of the posterior thigh muscles would be begin 0.482 seconds after the trigger switch was activated by the falling weight. Protocols Testing consisted of 2 phases: a control group that participated in jerks with no PNF stretching intervention and a treatment group that participated in jerks with the PNF intervention. Each subject in the control group began by lying supine on the treatment table with her ischial tuberosity on the edge of the table. A padded, 272 Carter et a1 - Figure 1 Subject in supine position with the weight supported by the solenoid. adjustable dowel rod attached to an extensionbuilt on the table supported the lower extremities. Both legs were placed over the dowel rod, which was aligned with the popliteal space. The lower legs were then lowered to form a 90" angle with the femur, measured by a handheld goniometer. The ankle cuff was then attached to the subject's right leg. The weight was placed on the pin, and the first trial was executed. After the weight was dropped 30 cm, and 5 seconds of baseline activity were recorded, the weight was replaced on the pin and the procedure was repeated for the second and third trials. The subject then rested approximately5 minutes, or the amount that would be allowed for the treatment group to be stretched, before the second bout of jerks was conducted. The subjects in the treatment group experienced 3 jerks, a contract-relax PNF stretch of the hamstring muscles, and then 3 more jerks. In order to be stretched, each subject remained on the treatment table on which the instrumentation was built. The right leg was placed in a straight-leg knee brace while the hip and left leg were secured to the treatment table using seatbelts. Next, the right hamstring was passively stretched to the endpoint, shown through EMG activity, for 30 seconds to the count of a metronome. The subject was immediately instructed to try to push her leg back to the starting position against resistance for 7 seconds. This procedure was instantaneously repeated 2 more times, with no breaks between repetitions. 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These results are probably best explained using the theories of muscle-spindle desensitization and muscle size. * PNF Group u I I I Pre Test Post Test Figure 2 Average muscle activity of the semitendinosus between groups or across pre- and post- values did not differ (F,,22 = .92; P = .02; +! = .04; P = .15). " 1 0 Pre Test Post Test Figure 3 Average muscle activity of the biceps femoris. decreased as a result of PNF stretching (F,,22 = 4.50; P = .04; +! = .17; P = .53). *Posttest PNF values were lower PNF and Rapid Muscle Lengthening 275 Muscle-Spindle Desensitization In order to understand this neurophysiologicalmechanism, it is important to discuss the 2 proprioceptive bodies in the muscle: the muscle spindles and the Golgi tendon organs (GTOs).Muscle spindles are found within the muscle belly and provide information to the central nervous system (CNS) regarding the absolute length and the velocity of the stretch in the skeletal muscle^."^^,^^ The GTO is located in the tendon, close to the musculotendinous junction. The GTO responds as a feedback monitor and sends irnpulses to the CNS in response to t e n s i ~ n ? ~ , ~ ~ When stimulated, most commonlyvia a rapid stretch, the muscle spindle signals the CNS to send excitatory efferent signals to the corresponding muscle. The resulting contraction halts the intended muscle lengthening. In contrast, via increased muscle tension, when the GTO is stimulated it signals the CNS to send inhibitory signals to the corresponding muscles.10 Muscle spindles are desensitized when a muscle is held in a stretched position for a prolonged period of time. During this time the muscle spindles habituate, signaling is reduced, and a greater muscle length can be obtained during the stretch. When desensitized,the muscle spindles' response to a sudden stretch is diminished, as evidenced by little or no reflexive contraction. This muscle-spindle desensitizationcould be beneficial because it allows for the greatest gains in flexibility. It could also be detrimental because it diminishes the protective stretch-reflex response. Researchers have shown that muscle-spindle desensitizationoccurs during PNF stretching technique^?^,^^ Beyond that, Prentice1°demonstrated a reduced musclespindle response during the contract-relax PNF technique. This reduced response is thought to be chiefly responsible for the immediate increase in muscle length that is common during PNF stretches. The decrease in muscle activity during the stretch reflex after a bout of contract-relax PNF found in the current study is also indicative of muscle-spindle desensitization and is congruent with these findings. Other researchers have shown that average EMG muscle activity produced during PNF stretching techniques decreases, as we11.10,19,29,30 For example, researchers have assessed the H (Hoffman) and T (tendon tap) reflex responses after the isometric contractions of various PNF stretching techniques and found diminished EMG activity during both response^.^,^^,^^ This body of research indicates that PNF causes a decreased excitability of both the muscle spindle and the motor neurons immediately after an isometic contraction that lasts for approximately 10 seconds. Furthermore, the depression of the reflexes is similar for voluntary contractions that vary in duration from 1to 30 seconds.31 There is reason to believe that PNF stretching changes the functioning of the intrafusal fibers.31There are 2 types of fiber that can modulate the sensitivity of the muscle spindle. The dynamic fibers (primary effect on Ia afferents) are larger and more prevalent in the muscle, transmit impulses 276 Carter et a1 quickly, and are strongly sensitized to dynamic stret~h.3~ These fibers are called on when reflexive types of actions are req~ired.3l.~~ The static (types Ia and 11)fibers regulate background Ia discharge and reduce the sensitivity of types Ia and I1fibers to dynamic stretch.32Assuming no independent fusimotor activation, the 30-second passive stretch of the PNF technique performed in this study should primarily alter the sensitivity of the static However, because response to a stretch reflex depends on the dynamic fibers and a reduction in muscle activity was found, we conclude that dynamic fibers were desensitized, as well?= Muscle Size The hamstrings, as a collective group of posterior thigh muscles, are capable of producing large amounts of force because they have long fibers and intermediate physiologic cross-sectional Nonetheless, the muscles that make up the hamstrings are not all the same size. The long head of the biceps femoris has a mass of 128zk 28 g and a length of 342 f 14 mm. The semitendinosus has a mass of 76.9 f 7.7 g and a length of 312 f 4 mm.33In addition, the biceps femoris has a greater cross-sectional area, a smaller fiber length, and a lower fiber-length-to-muscle-lengthratio than the semitendinosus does.33Depending on the size of a muscle, it can contain anywhere from 6 to 1300 muscle ~pindles.3~ There are more muscle spindles to influence per unit area in the biceps femoris, because it is a larger muscle than the ~emitendinosus.3~ Therefore, there is reason to believe that the sigrufrcant decrease in muscle activity between groups by time shown in the biceps femoris and not the semitendinosus was because the spindle desensitization had a greater effect. Conclusion The results of this study suggest that contract-relax PNF stretching techniques reduced the average EMG activity of the biceps femoris muscle associated with a stretch reflex. Explanations for these findings are rooted in the process of muscle-spindle desensitization and the overall size of the biceps femoris muscle. The desensitization of the muscle spindle that occurs during the contract-relax PNF stretching technique can allow for a greater risk of muscle and tendon injury to occur. Because the biceps femoris is a larger muscle than the semitendinosus, there are more muscle spindles to influence per unit area. This allows for greater effects of muscle-spindle desensitization. This information is importantbecause it shows that stretching a large muscle, such as the biceps femoris, using the contract-relax PNF stretching technique precompetition can be problematic, especially if a reflexive adivity is warranted. PNF and Rapid Muscle Lengthening 277 Acknowledgment This research was part of the lead author's Master's thesis project, which was completed at The University of Mississippi. References 1. Godges J, MacRae H, Longdon C, Tinberg C , MacRae P. The effects of two stretching procedures on hip range of motion and joint economy. J Orthop Sports Pkys Ther. 1989;10:350-357. 2. Hartley-O'Brien S. Six mobilization exercises for active range of hip flexion. Res Q Exerc Sport. 1980;51:625-635. 3. Holt L, Travis T, Okita T. Comparative study of three stretching techniques. Percept Motor Skills. 1980;31:611-616. 4. Prentice W. TherapeuticModalities for Allied Health Professionals. New York, NY: McGraw-Hill Health Professions Division; 1998. 5. Hartig D, Henderson J. Increasing hamstring flexibility decreases lower extremity overuse injuries in military basic trainees. Am J Sports Med. 1999;27:173-176. 6. Lustig S, Ball T, Looney M. A comparison of two proprioceptive neuromuscular facilitationtechniques for improving range of motion and muscular strength. Isokinet Exerc Sci. 1992;2:154-159. 7. Osternig L, Robertson R, Troxel RPH. Differential responses to proprioceptive neuromuscular facilitation stretch technique. Med Sci Sports Exerc. 1990;22:106111. 8. Prentice W. A comparison of static and PNF stretching for improvement of hip joint flexibility. Athletic Training. 1983;18:56. 9. Prentice W, Kooima E. The use of PNF techniques in rehabilitation of sportrelated injury.Athletic Training. 1986;21:26-31. 10. Prentice W. Rehabilitation Techniques in Sports Medicine. 2nd ed. St. Louis, Mo: Mosby Year Book; 1994. 11. Sady J, Wortman M, Blanke D. Flexibility training: ballistic, static, or PNF? Arch Pkys Med Rehabil. 1982;63:261-263. 12. Wang RY, Effect of proprioceptive neuromuscular facilitation on the gait of patients with hemiplegia of long and short duration. Pkys Tker. 1994;74: 1108-1115. 13. Wiktorsson-MollerM, Oberg B, Ekstrand J, Gillquist J. Effects of warming up, massage, and stretching on range of motion and muscle strength in the lower extremity.Am J Sports Med. 1983;11:249-252. 14. Worrell T, Smith T, WmegardnerJ. Effect of hamstring stretching on hamstring muscle performance.J Ortkop Pkys Tker. 1994;20:154-159. 15. Lewit K, S i o n s D. Myofascialpain: relief by post-isometric relaxation. Arch Pkys Med Rehabil. 1984;65:452-456. 278 Carter et al 16. Etnyre BR, Abraham LD. H-reflex changes during static stretching and two variations of proprioceptive neuromuscular facilitation techniques. Electroencephalogr Clin Neurophysiol. 1986;63:174179. 17. Lewit K. Manipulative Therapy in Rehabilitation of the Motor System. London, England: Butterworth & Co; 1985. 18. Vujnovich A, Dawson H. The effect of therapeutic muscle stretch on neural processing. J Orthop Sports Phys Ther. 1994;20:145-153. 19. Moore M, Hutton R. Electromyographicinvestigation of muscle stretchingtechniques. Med Sci Sports Exerc. 1980;12:322-329. 20. Osternig L, Robertson R, Troxel R, Hansen P. Muscle activation during proprioceptive neuromuscular facilitation (PNF) stretching techniques. Am J Phys Med. 1987;66:298-307. 21. Arnheim D, Prentice W. Principles of Athletic Training. 8th ed. St. Louis, Mo: Mosby Year Book; 1993. 22. Basmajian J, DeLuca C. Muscles Alive, Their Functions Revealed by Electromyography. 5th ed. Baltimore, Md: Williams & Wilkins; 1985. 23. McArdle W, Katch F, Katch V. Exercise Physiology: Energy, Nutrition, and Human Performance. Philadelphia, Pa: Lea & Febiger; 1991. 24. Thibodeau G, Patton K. Anatomy and Physiology. St. Louis, Mo: Mosby; 1993. 25. Astrand P, Rodahl K. Textbook of Work Physiology. New York, NY. McGraw-Hill; 1986. 26. Gregor R. Neurology, kinesthesia, and servomotor control. In: Rasch P, ed. Kinesiology and Applied Anatomy. Philadelphia, Pa: Lea & Febiger; 1989:62-77. 27. Enoka R, Hutton R, Eldred E. Changes in excitability of tendon tap and Hoffmann reflexes following voluntary contractions. Electroencephalogr Clin Neurophysiol. 1986;48:664-672. 28. Matthews P. The human stretch reflex and the motor cortex. Trends Neurosci. 1991;14:88. 29. Moore M, Kukulka C. Depression of Hoffmann reflexes following voluntary contraction and implications for proprioceptive neuromuscular facilitation therapy. Phys Thm. 1991;71:321-333. 30. Knott M, Voss D. Proprioceptive Neuromuscular Facilitation: Patterns and Techniques. 2nd ed. Evanston, Ilk Hoeber Medical Division; 1968. 31. Enoka R. Single joint system operations. Neuromechanical Basis of Kinesiology. 2nd ed. Champaign, J L Human Kinetics; 1994. 32. Adrian M, Cooper J. Biomechanics of Human Movement. 2nd ed. Dubuque, Iowa: Brown & Benchmark; 1995. 33. Lieber R. Skeletal Muscle Structure and Function: Implications for Rehabilitation and Sports Medicine. Baltimore, Md: Williams & Wilkim; 1992.