A PILOT STUDY COMPARING THE EFFECTS OF SPINAL MANIPULATIVE THERAPY WITH THOSE OF EXTRA-SPINAL MANIPULATIVE THERAPY ON QUADRICEPS MUSCLE STRENGTH Bernd Hillermann, MChiro,a Adrian Neil Gomes, MChiro, MMedSc,a Charmaine Korporaal, MChiro,a and Dennis Jackson, BSa
ABSTRACT Objective: The objective of this study was to assess whether tibiofemoral joint manipulation is as effective as sacroiliac (SI) joint manipulation in increasing quadriceps muscle strength. Design and Setting: Twenty subjects were divided into two groups of 10. After all base measurements of the maximum voluntary force of the quadriceps muscles were taken, subjects in group A received tibiofemoral joint manipulation and those in group B received ipsilateral SI joint manipulation. After these treatments, the maximum voluntary forces of the subjects’ quadriceps muscles were retested. Results: A significant improvement ( P = .05) in quadriceps muscle strength was noted in the subjects who received an SI joint manipulation. Conclusion: This study showed a significant change within the SI joint manipulation group before and after the manipulation but did not show any significant difference between the groups (tibiofemoral joint vs SI joint manipulation) in increasing quadriceps muscle strength. (J Manipulative Physiol Ther 2006;29:145-149) Key Indexing Terms: Musculoskeletal Manipulations; Patellofemoral Pain Syndrome
K
nee joint pathologies, in general, are associated with loss of knee-extensor muscle strength. This weakness has been attributed to arthrogenous muscle inhibition (AMI).1 Arthrogenous muscle inhibition is defined as the inability of a muscle to recruit all motor units of a muscle group to its full extent during a maximal effort voluntary muscle contraction and is a natural response designed to protect joints from further damage.1 Ongoing inhibition of a muscle, with its concomitant decrease in physical activity, can have numerous long-term effects on muscle tissue: there may be type I fiber atrophy, decreased cross-sectional area, and decreased oxidative enzyme activity, all resulting in a decrease in muscle strength.2 Pain and disuse are often blamed for inhibition and muscle atrophy after acquiring joint injury. A change in the afferent input to the spinal cord from joint receptors appears a Department of Chiropractic, Durban Institute of Technology, South Africa. Submit requests for reprints to: Bernd Hillermann, MChiro, 31 The Crescent, Lakepoint Park, Mullingar, County Westmeath, Republic of Ireland (e-mail:
[email protected]). Paper submitted August 8, 2005. 0161-4754/$32.00 Copyright D 2006 by National University of Health Sciences. doi:10.1016/j.jmpt.2005.12.003
to be the most influential factor in the neurophysiologic response associated with AMI.2 The primary receptors involved in AMI are the mechanoreceptors, although nociceptors also play a role.2 These mechanoreceptors act on inhibitory interneurons synapsing on the motor neuron (MN) pool of the joint musculature, decreasing the force of any contraction stemming from that MN pool.2 Arthrogenous muscle inhibition associated with the quadriceps muscles has been shown to originate from structures in and around the knee joint.2-7 Anecdotal evidence suggest that patients who present with patellofemoral pain syndrome (PFPS) associated with lower back and knee joint dysfunction may benefit from manipulation of the sacroiliac (SI) joint. 1,8 The MN pool of the SI joint originates from L2-S4, which overlaps with the origin of the MN pool supplying the quadriceps muscle L2-L4.9 Hence, altered afferent mechanoreceptor activity around the SI joint may contribute to AMI in the quadriceps muscle.1,10 Studies have shown that manipulation to the SI joint is effective in decreasing AMI in the quadriceps muscles associated with knee pain.1,10 The effect of adjusting the knee joint on quadriceps muscle strength, however, has not yet been investigated. The purpose of this pilot study was to assess whether manipulation of the tibiofemoral (knee) joint is as effective 145
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as SI joint manipulation in increasing quadriceps muscle strength in patients with PFPS. For the purpose of this study, a manipulation is defined as a high-velocity, low-amplitude thrust at the end of the elastic barrier of the joint capsule.11
METHODS Subjects A total of 20 subjects (12 men and 8 women) gave written informed consent to participate in this study. This study was limited to patients aged between 18 and 45 years who have PFPS. Subjects who presented with contraindications to manipulative therapy or isokinetic muscle testing were excluded from the study. The institutional review board of the Durban Institute of Technology, South Africa, approved this study.
Assumptions The following assumptions were made: Because AMI is the inability of a muscle to recruit all motor units of a muscle group during a maximal effort voluntary muscle contraction,1 it is assumed that recruitment of an inhibited muscle group does not occur at its full extent. Mechanoreceptor activity plays the primary role in AMI.2 Manipulation of a joint has been proposed to activate mechanoreceptors from structures in and around the manipulated joint. The altered afferent input arising from the stimulation of these receptors is thought to cause changes in MN excitability, with a subsequent decrease in AMI.1,11 This is assumed to influence MN pool recruitment during voluntary muscle contraction.
Study Protocol Convenience purposive sampling was used to allocate the subjects into two treatment groups. Subjects in group A received a long-axis distraction manipulation of the tibiofemoral joint whereas those in group B received an SI joint manipulation. Both manipulations were performed on the ipsilateral side of the knee pain. At the first appointment, subjects underwent a full case history taking and physical, lumbar spine, as well as knee regional examinations. Subjects accepted into the study were given a covering letter that explained the study. Subjects in group B also needed to present with a symptomatic SI joint to be included in the study. At the second consultation, subjects were screened using lower back and knee regional examinations for any change in their condition. If no change was noted, then subjects underwent isokinetic testing of the quadriceps muscle. A baseline measurement of the subjects’ maximum voluntary quadriceps muscle forces was established. Within 1 minute of the initial muscle testing, the subjects received the relevant manipulation (depending on which group each subject was in). The maximum voluntary quadriceps force was then
Fig 1. Protocol used for the isokinetic testing procedure. retested. Only the ipsilateral thigh underwent isokinetic testing because previous studies found that changes in knee-extensor strength in the contralateral legs of both treatment patients and control subjects after SI joint manipulation did not reach a level of statistical significance.1
Muscle Testing The Cybex Orthotron II Isokinetic Rehabilitation System (Cybex Division of Lumex, Bayshore, NY) was used to perform the isokinetic testing of the thigh. This machine is designed to measure the voluntary force output (isometric contractibility) of a muscle group. The quadriceps muscle group was tested in this study. Several authors have agreed on the reliability and validity of this instrument.12-14 Before the isokinetic testing was performed, subjects completed a 5-minute warm-up cycle, which was followed by 3 sets of a 20-second hamstring and quadriceps stretch. Subjects were placed in a comfortable upright-seated position, had their back rested at 858, and were secured using thigh, pelvic, and torso straps to minimize extraneous body movements. Their knee rested at a 908 angle from full extension. The lateral femoral condyle was used as the bony landmark for matching the axis of rotation of the knee joint with that of rotation of the dynometer resistance adaptor. Subjects were given verbal encouragement while they were performing the test.1,12,13,15-17 The testing procedure is outlined in Fig 1. Approximately 3 readings, before and after manipulation, were taken to ensure an accurate measurement of the isometric contractibility of the quadriceps muscle.
Interventions Only the symptomatic knee or SI joints were manipulated. If subjects complained of bilateral PFPS, then they were asked to make a subjective judgment as to which knee was worse. That knee was then manipulated. If subjects complained of bilateral lower back pain, then only the SI joint on the ipsilateral side of their symptomatic knee was manipulated. An audible cavitation was not required to indicate a successful manipulation.18 Restrictions in the knee and SI joints were identified by using dynamic palpation techniques, as described by Schafer and Faye.19 A long-axis distraction manipulation was used on the tibiofemoral joint fixation to stimulate mechanoreceptors around the knee joint.19 The SI joint was
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Fig 3. Maximum voluntary force readings before and after the manipulation. Once all the joint slack had been removed, the researcher then performed a body drop and applied a high-velocity, low-amplitude thrust in an inferior line of drive.21 Fig 2. Positioning of patient for SI manipulation. manipulated according to the restriction palpated. Restrictions in the SI joint occur in either the upper or the lower area of the joint. These joints may be restricted in flexion or extension. The standing flexed knee–raising test was used to identify the restriction present in the SI joint.19 The tibiofemoral joint was manipulated by having the subjects lie supinely. The researcher contacted his hands bilaterally just distal to the tibiofemoral joint space. Each subject’s leg was secured at approximately the malleolus level, between the researcher’s knees. Each subject’s knee was placed into slight flexion, by elevating the researcher’s hands, while the researcher performed a partial deep knee bend. The manipulation was achieved by allowing the subject’s knee to drop into extension and by exerting a longaxis distraction through an inferior line of drive.19,20 For the SI joint manipulation, subjects were positioned according to the direction of the fixation present (Fig 2). If the SI joint was fixated in a flexed position, then the subjects were placed in the side-lying posture with the lesion side up. If the SI joint was fixated in an extended position, then the subjects were placed in the side-lying posture with the lesion side down. Once the subjects were in a side-lying position, their lower arm was pulled toward the researcher until they were in a comfortable position. The lower arm was then folded over the top of the shoulder and stabilized with the researcher’s cephalad hand. The lower limb not in contact with the table was slightly flexed at the hip and knee. The foot of this leg was then placed in the popliteal space of the other leg, ensuring that the pelvis was at a 908 angle to the table.21 The researcher stood alongside the subjects in a fencer stance. The subjects’ flexed lower limb was supported between the researcher’s upper thighs. The researcher then took a pisiform contact with his caudal hand over the involved area of the SI joint (superior or inferior). The researcher then removed the joint slack by applying a cephalad traction force with his indifferent hand and an anterior rotation of the pelvis with his contact hand.
Statistical Analysis Nonparametric testing was used to analyze the data. Intragroup comparisons were made, testing for a significant change as a result of the intervention, using the Wilcoxon signed rank test for matched pairs. Intergroup comparisons were made using the Kruskal-Wallis H test, testing for a significant difference between the treatment groups in terms of the maximum voluntary quadriceps force. The a level of significance was set at .05, and all data were analyzed using SPSS Package 12.0 (SPSS Inc, Chicago, Ill).
RESULTS The maximum voluntary force readings before and after manipulation are shown in Fig 3. There was a significant increase in the quadriceps force in group B ( P = .05) after the manipulation. The quadriceps force increased in group A ( P = .415) after the manipulation, but this increase did not reach a statistically significant level. The mean scores before the manipulation were not similar between the groups, which may indicate an error in the sampling procedure and allocation of the subjects. The mean scores before the manipulation should ideally be similar between the treatment groups. When the data were statistically analyzed, there was no statistically significant difference in the quadriceps force before the manipulation between treatment groups ( P = .083). Group B (SI joint manipulation) was the only group to improve significantly ( P = .05) after the manipulation. The Kruskal-Wallis H test showed that there was no significant difference between both treatment groups ( P = .174) after the manipulation.
DISCUSSION This study aimed to compare the effectiveness of tibiofemoral (knee) joint manipulation with that of SI joint
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manipulation in increasing quadriceps muscle strength. The presence of AMI can only be accurately assessed using more sensitive measuring techniques such as the interpolated twitch technique or Hoffman’s reflex.2 Therefore, this study used two assumptions to hypothesize on the presence and reduction of AMI. It was hypothesized that the recruitment of all motor units of a muscle group does not occur in the presence of AMI. The presence of AMI in a muscle group results in a decrease in the maximum voluntary contraction of that muscle group.2 Furthermore, AMI could be decreased by altering the aberrant afferent information from the affected joint, through mechanoreceptor stimulation, after manipulative therapy.1,11 The resultant decrease in AMI would lead to an increase in the maximum voluntary contraction of the affected muscle group. Studies have shown that manipulation of the SI joint can decrease AMI in the quadriceps muscles with a subsequent increase in quadriceps muscle strength.1,10 The results of this study are in line with those of previous studies,1,10 showing that quadriceps muscle strength increased significantly after SI joint manipulation ( P = .05). Manipulation of the knee (tibiofemoral) joint showed no significant increase in quadriceps muscle strength ( P = .415). Although these results suggest that SI joint therapy is more effective than tibiofemoral (knee) joint manipulative therapy in increasing quadriceps muscle strength, statistical analysis revealed no significant difference between the two treatment groups. The effectiveness of tibiofemoral joint manipulation in stimulating the MN pool of the quadriceps muscle is, however, still questionable. Clinical observations suggest that the treatment area should be over the dermatomal level of the femoral nerve when trying to reduce quadriceps muscle inhibition because this might alter the afferent mechanoreceptor information of the quadriceps MN pool more effectively than if the treatment area were over the knee.6 The results of this pilot study are intriguing but require further investigation. Limited funding for this study prevented the testing of a larger sample population. Results obtained from such a small sample population (N = 20) cannot be extrapolated onto an entire population because the results obtained from such a small group rarely provide results better than chance. A larger and more uniform sample group, along with a more sensitive measurement tool for determining the presence and extent of AMI, may have produced more significant results. This pilot study was designed as a clinical outcome study. This study design— although clinically relevant—may have contained experimental bias or placebo effects. A randomized, controlled, and double-blinded clinical trial is required to establish a scientifically tenable relationship comparing the efficacy of spinal with that of extraspinal manipulative therapy in reducing quadriceps AMI.
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Being able to reduce AMI in patients recovering from joint injuries is important to the rehabilitation process.22 Exercise is another important factor in joint rehabilitation. Clinicians are often able to help a patient regain range of motion and general fitness, but one factor that often eludes clinicians is functional, bilateral strength.2 This study measured the force of the MN pool output before and after manipulation and explained the findings by hypothesizing on the presence and elimination of AMI in the quadriceps muscle group. Measuring the voluntary force output of an MN pool has some limitations when assessing a pathologic population; the maximum voluntary contraction measurement must be reproducible, and this maximum contraction may not be possible or could cause more damage in the presence of a joint injury. A more sensitive measuring tool is needed to draw more accurate conclusions on the presence and elimination of AMI and its subsequent effect on muscle strength. The interpolated twitch technique and Hoffman’s reflex are two other measurement tools that could be used for future research in this field. Hoffman’s reflex is a more sensitive measurement but requires great control.2 This method of analysis can also be used on a pathologic population because no voluntary effort is required.2 This study was designed as a clinical outcome study; therefore, it may have contained experimental bias. The results obtained from such a small sample population rarely provide results better than chance. Hence, more advanced studies with larger population samples should be performed.
CONCLUSION This study showed a significant change within the SI joint manipulation group before and after the manipulation; however, it did not show any significant difference between the groups (tibiofemoral [knee] joint vs SI joint manipulation) in increasing quadriceps muscle strength. Using a more sensitive measuring tool, testing a larger sample group, and using a randomized, controlled, double-blinded clinical trial are recommended for future research.
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collateral ligaments of the human knee joint. Arch Phys Med Rehabil 1995;76:750-7. 4. Fischer-Rasmussen T, Krogsgaard MR, Jensen DB, DyhrePoulsen P. Muscle reflexes during gait elicited by electrical stimulation of the posterior cruciate ligament in humans. J Orthop Res 2002;20:433-8. 5. Lewek M, Rudolph K, Axe M, Snyder-Mackler L. The effect of insufficient quadriceps strength on gait after anterior cruciate ligament reconstruction. Clin Biomech 2002;17:56-63. 6. Hopkins JT, Ingersoll CD, Krause BA, Edwards JE, Cordova ML. Effect of knee joint effusion on quadriceps and soleus motor neuron pool excitability. Med Sci Sports Exerc 2001;33: 123-6. 7. Sanchis-Alfonso V, Rosello-Sastre E. Immuno-histochemical analysis of neural markers of the lateral retinaculum in patients with isolated symptomatic patellofemoral malalignment: a neuroanatomic basis for patellofemoral pain syndrome. Am J Sports Med 2000;28:725-31. 8. Wood A. Conservative management of patellofemoral pain syndrome. J Sport Chiropr Rehabil 1998;12:1-13. 9. Moore KL. In: Clinically orientated anatomy. 3rd ed. Baltimore: Williams and Wilkins; 1992. p. 387, 423. 10. Suter E, McMorland G, Herzog W, Bray R. Decrease in quadriceps inhibition after sacroiliac manipulation in patients with anterior knee pain. J Manipulative Physiol Ther 1999;22: 149-53. 11. Lewit K. Role of manipulation in spinal rehabilitation. In: Liebenson C, editor. Rehabilitation of the spine: a practitioner’s manualBaltimore7 Williams and Wilkins; 1996 p. 213. 12. Davies GJ. A compendium of isokinetics in clinical usage and rehabilitation techniquesLaCrosse (Wis)7 S&S publishers; 1992. p. 35-44.
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13. Chan KM, Mafulli N. Principles and practice of isokinetics in sports medicine and rehabilitationHong Kong7 Williams and Wilkins Asia Pacific Ltd; 1996. p. 10-23. 14. Callaghan MJ, McCarthy CJ, Al-Olmar A, Oldham JA. The reproducibility of multi-joint isokinetic and isometric assessment in a healthy patient population. Clin Biomech 2000;15: 678-83. 15. Perrin DH. Isokinetic exercise and assessmentChampaign (Ill)7 Human Kinetics Publishers; 1993. p. 7-48. 16. Pincivero DM, Lephart SM, Karunakara RA. Reliability and precision of isokinetic strength and muscular endurance for the quadriceps and hamstrings. Int J Sports Med 1997;18:113-7. 17. Clifton S. The presence and extent of quadriceps femoris weakness in individuals with patellofemoral pain syndrome [dissertation]. Durban Institute of Technology; 2003. 18. Suter E, Herzog W, Conway PJ, Zang YT. Reflex response associated with manipulative treatment in the thoracic spine. J Neuromusculoskel Syst 1994;2:123-30. 19. Schafer RC, Faye LJ. Motion palpation and chiropractic technique. 2nd ed. Santa Monica7 Motion Palpation Institute; 1990. p. 40-398. 20. Meyer JJ, Zachman ZJ, Keating JC, Traina AD. Effectiveness of chiropractic management for patellofemoral pain syndrome’s symptomatic control phase: a single subject experiment. J Manipulative Physiol Ther 1990;13:539-49. 21. Szaraz ZT. Compendium of chiropractic technique. 2nd ed. Toronto7 Vivian, LR Associates Ltd Technical Production; 1990. p. 139-41. 22. Hurley MV, Newham DJ. The influence of arthrogenic muscle inhibition on quadriceps rehabilitation of patients with early, unilateral osteoarthritis of the knee. Br J Rheumatol 1993;33: 127-31.
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