1A

VOLUME 30 NUMBER 5 JUNE 2007

TABLE OF CONTENTS

EDITORIAL 365 Manual Application of Controlled Forces to Thoracic and Lumbar Spine With a Device: Rated Comfort for the 333 Outcome Research Receiver’s Back and the Applier’s Hands Nikolai Bogduk, MD, PhD, DSc Gordon Waddington, PhD, Gordon Lau, BAppSc (Physiotherapy) (Hons), and Roger Adams, PhD JMPT 335 Highlights 374 Effect of Age and Sex on Heart Rate Variability in Healthy Subjects ORIGINAL ARTICLES John Zhang, MD, PhD 336 Preliminary Morphological Evidence That Vertebral 380 A Single-Blind Pilot Study to Determine Risk and Hypomobility Induces Synaptic Plasticity in the Spinal Cord Association Between Navicular Drop, Calcaneal Barclay W. Bakkum, DC, PhD, Charles N.R. Henderson, Eversion, and Low Back Pain DC, PhD, Se-Pyo Hong, DC, PhD, and Gregory D. Cramer, James W. Brantingham, DC, PhD, Katy Jane Adams, DC, PhD MSc Chiropractic, Jeffery R. Cooley, DC, Denise Globe, DC, MS, PhD, and Gary Globe, DC, MBA, PhD 343 Neck Muscle Endurance in Nonspecific Patients With 386 Interexaminer Reliability and Accuracy of Posterior Neck Pain and in Patients After Anterior Cervical Superior Iliac Spine and Iliac Crest Palpation for Spinal Decompression and Fusion Level Estimations Anneli Peolsson, PhD, PT, and Görel Kjellman, PhD, PT Hye Won Kim, MD, PhD, Young Jin Ko, MD, PhD, Won Ihl Rhee, MD, PhD, Jung Soo Lee, MD, 351 Cerebrospinal Fluid Pressure in the Anesthetized Rat Ji Eun Lim, MD, Sang Jee Lee, MD, Sun Im, MD, Brian S. Budgell, PhD, and Philip S. Bolton, PhD and Jong In Lee, MD, PhD

LITERATURE REVIEW 357 Muscular and Postural Demands of Using a Massage Chair and Massage Table 390 Coupling Behavior of the Thoracic Spine: A Systematic Fearon A. Buck, BSc, Usha Kuruganti, PhD, Review of the Literature Wayne J. Albert, PhD, Melanie Babineau, BSc, Phillip S. Sizer Jr., PT, PhD, Jean-Michel Brismée, PT, ScD, Sarah Orser, and Nadine Currie-Jackson, BSc and Chad Cook, PT, PhD, MBA

Full-text online access to JMPT is available for all print subscribers. See page 350 for details. EDITORIAL BOARD Partap Singh Khalsa, DC, PhD Stony Brook, New York Paul B. Bishop, DC, MD, PhD Vancouver, BC, Canada Jennifer Langworthy, MPhil Bournemouth, United Kingdom Jennifer E. Bolton, PhD Bournemouth, United Kingdom Charlotte Leboeuf-Yde, DC, MPH, PhD Odense, Denmark Geoffrey Bove, DC, PhD Boston, Massachusetts Karel Lewit, MUDr, Doc, DSc Prague, Czech Republic EDITOR Alan C. Breen, DC, PhD Bournemouth, England Cynthia R. Long, MS, PhD Claire Johnson, DC, MSEd Davenport, Iowa Jerrilyn A. Cambron, DC, MPH, PhD Lombard, Illinois Christopher Maher, PhD Lidcombe, Australia ASSOCIATE EDITOR J. David Cassidy, DC, PhD, DrMedSc Bart Green, DC, MSEd Toronto, Ontario, Canada Marion McGregor-Triano, DC, MSc, PhD Toronto, Ontario, Canada Pierre Côté, DC, PhD Toronto, Ontario, Canada William C. Meeker, DC, MPH EDITORIAL OFFICES Davenport, Iowa 200 East Roosevelt Road James M. Cox, DC Fort Wayne, Indiana Robert Mootz, DC Lombard, IL 60148-4583 Olympia, Washington E-mail: [email protected] Jeffrey R. Cram, PhD Nevada City, California Craig F. Nelson, MS, DC Minneapolis, Minnesota Vaclav Dvorak, MD PUBLISHER Bonaduz, Switzerland Niels Grunnet-Nilsson, DC, MD, PhD Elsevier Inc. Odense, Denmark Phillip Ebrall, BAppSc(Chiro), PhD Joanne Nyiendo, PhD Bundoora, Australia Brian Arnold, Portland, Oregon Production Editor Christine Goertz,DC, PhD David H. Peterson, DC Bethesda, Maryland Ph. (215) 239-3377 Portland, Oregon E-mail: [email protected] L.G.F. Giles, DC, PhD Reed B. Phillips, DC, PhD Perth, Australia Whittier, California SUBMISSIONS Mitchell Haas, DC Anthony L. Rosner, PhD All manuscripts are submitted Portland, Oregon Arlington, Virginia through the journal website: Scott Haldeman, DC, MD, PhD Charles Sawyer, DC www.Mosby.com/JMPT Santa Ana, California Bloomington, Minnesota Daniel Hansen, DC Gary Schultz, DC Spokane, Washington EDITOR EMERITUS Portland, Oregon Cheryl Hawk, DC, PhD Dana J. Lawrence, DC, MMEd Robert C. Shiel, PhD Kansas City, Missouri Lombard, Illinois Walter Herzog, PhD Kevin P. Singer, PT, PhD Calgary, Alberta, Canada Perth, Western Australia Eric L. Hurwitz, DC, PhD John J. Triano, DC, PhD Los Angeles, California Toronto, Ontario, Canada Jennifer R. Jamison, MBBCh, PhD, EdD Howard T. Vernon, DC, PhD Queensland, Australia Toronto, Ontario, Canada Greg Kawchuk, DC, PhD Terry R. Yochum, DC Edmonton, Alberta, Canada Denver, Colorado Joseph C. Keating, Jr, PhD Kansas City, Missouri

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OUTCOME RESEARCH

Nikolai Bogduk, MD, PhD, DSc

ABSTRACT

This editorial focuses on the topic of outcome research and offers alternate views of what may be important to the practitioner. (J Manipulative Physiol Ther 2007;30:333Q334)

t works. This is what every craft group would like to be would obviate the need for any other health care. said of its interventions. As a referring practitioner, I Reciprocally, if a patient still uses other care, any success Iwould like to know if a treatment works so that I can use could be due to that other treatment and not to yours. Return it for my patients. However, the assertion that it works begs to work is a vexatious measure. It is impressive when return 3 subordinate questions: in what respects, by how much, to work is achieved. Conversely, however, there may be and for how long? reasons why a patient cannot return to work despite Any number of instruments is available by which to successful treatment, such as a hostile economic climate measure outcomes in various domains, such as pain, or hostile employers. So, there can be excuses for not disability, function, and psychologic distress. Most are succeeding in achieving return to work. known by some sort of acronym, for example, Short Form To answer bhow much,Q relief of pain should be 36 (SF-36), Minnesota Multiphasic Personality Inventory quantified. However, research in the past has relied on (MMPI), Beck Depression Inventory (BDI), illness behavior continuous outcome measures. Studies have reported group questionnaire (IBQ), Symptom Checklist 90 Revised (SCL- mean values before and after treatment. This tells me little as 90R), visual analog scale (VAS), and numerical pain rating a consumer. Around every mean value there will be patients scale (NPRS). Research experts would have us use several, if who fare better than the mean value and those who fare not many, of these to verify outcomes. Yet, that advice applies worse than the mean value. But I want to be able to tell my only if we are interested in the particular domains that the patients what their chances are of obtaining a specified specialized instruments measure. For practical purposes, I outcome. For this I need to see categorical data. From a would be satisfied if an investigator told me about pain, study, I want to know how many patients (what proportion) function, use of other health care, and return to work. obtained complete relief of pain, substantial improvement, Pain can be measured by a numerical pain rating scale.1 and other grades of relief, including bworse.Q It is a simple Function can be assessed using patient-specified functional matter to report in a table how many patients in a study outcomes.2-4 For this instrument, the patient nominates obtain 100%, 90%, 80%, etc, relief of their pain. Yet, so few 4 activities of daily living that are impaired by their pain and investigators do this. Cynically, it is my impression that they that most dearly they would want restored by a successful avoid doing so because their outcomes are not impressive in treatment. If those activities are not restored, the treatment these terms. Data on group mean values serve to cover up cannot be held to have been a success. Use of other health mediocre and unimpressive categorical outcomes. care is pivotal to assessing outcomes. A successful treatment Similarly, restoration of function can be quantified and expressed as categorical data. I prefer to know how many Professor, Pain Medicine, Director, Clinical Research, University patients are fully restored, how many are substantially of Newcastle, Newcastle Bone and Joint Institute, Newcastle, rehabilitated, and how many fail to regain function. NSW, Australia. Coupling these data with outcomes on pain, I can determine (e-mail: [email protected]). how successful a treatment is. For me, success is complete Paper submitted April 13, 2007; accepted April 13, 2007. 0161-4754/$32.00 relief of pain (or near complete relief) and complete or Copyright D 2007 by National University of Health Sciences. virtually complete restoration of function. Less than doi:10.1016/j.jmpt.2007.04.010 complete relief and less than complete restoration of

333 334 Bogduk Journal of Manipulative and Physiological Therapeutics Outcome Research June 2007

function is not a success; instead, this amounts to palliation. objective is to determine to what extent nonspecific factors Others may exercise other definitions and value judgments. contribute to the impression that it works. The resultant However, in order for them do so, investigators need to statistic is the number needed to treat.6 This measures the report their categorical data in full. attributable effect of the treatment: the extent to which Use of other health care services requires only a binary outcomes are achieved by components of the intervention measure. The patient either is or is not using other health other than its nonspecific effects. For epidural steroids, for care or is seeking it. Your treatment cannot be a success if example, the number needed to treat is 100.7 This means they are doing so. Your treatment may have bhelped,Q but that for every 100 successful outcomes, only 1 is due to the obviously it did not eliminate the problem if the patient still steroids; the other 99 are due to the nonspecific effects of used other care. Return to work can also be quantified. The having an injection. patient is either working or not, or they may return to part- Knowing the attributable effect is pertinent to education time work or limited duties. and cost. A treatment may work but not because of what is Regarding the question bfor how long,Q investigators have taught as the active ingredient. The same outcomes may be been delinquent or cunning in the past. They have reported achieved by less elaborate interventions that focus on the immediate or short-term outcomes, but not long-term nonspecific effects. The implications could be dire. If back outcomes. Doing so makes the treatment look successful. pain can be adequately treated by explanation, reassurance, This is evident in the literature on drug treatment and on and activation, we do not need elaborate training programs manipulation for back pain,5 where it is not uncommon to to learn 150 different manipulation techniques. If non- have a follow-up measured in days, 1 week, or 2 weeks. Such specific injections work, we do not need fluoroscopy fees data do not inform me as a consumer. These reports are and exorbitant facility fees to achieve the desired outcome. designed to seduce impressionable readers. Maybe the reason why investigators are reluctant to There is no magic number that defines the desirable conduct and publish the appropriate studies is for fear of follow-up period. It is not 3 months, 6 months, or ba year for what they will show. Maybe it is not the specific thrust, nor conservative treatment but 2 years for operative treatment.Q the exercise. Maybe it is not the drug that we prescribe or The operational answer should be follow-up was of inject. Maybe the treatment works simply because we show sufficient duration for results to have stabilized. Immedi- that we care. Yet, to care does not require a 4-year ately after a treatment many patients appear to benefit. postgraduate training program. Nor does it require a Progressively, however, failures emerge. The true measure $2000 facility fee. The threat is that if we discover why it of success appears when the failures cease to emerge. The works, the elaborate and expensive edifices that we have appropriate device is a recovery curve that asymptotes over built to promote the intervention must crumble. time. From such a curve, I can read what the half-life is of a successful outcome and what proportion of patients remains relieved in the long term. If outcomes are confounded by recurrences, then the recurrence rate needs to become an REFERENCES additional outcome measure. If investigators tell me in what respects, by how much, 1. Briggs M, Closs JS. A descriptive study of the use of visual analogue scales and verbal rating scales for the assessment of and for how long, I can determine if I feel that the treatment postoperative pain in orthopedic patients. J Pain Symptom works. Ironically, this does not require a randomized Manage 1999;18:438-46. controlled trial. It requires only a comprehensive audit. An 2. Stratford P, Gill C, Westaway M, Binkley J. Assessing disability audit tells me how many patients obtained different grades and change on individual patients: a report of a patient specific of outcome and for how long. This type of report will tell measure. Physiother Can 1995;47:258-63. b Q 3. Westaway MN, Stratford PW, Binkley JM. The patient- me if it works. specific functional scale: validation of its use in persons In a pragmatic trial, the index treatment is compared with a with neck dysfunction. J Orthop Sports Phys Ther 1998;27: competing treatment. The comparison, however, does not tell 331-8. me if a treatment works. How well each treatment works is 4. Chatman AB, Hyams SP, Neel JM, Binkley JM, Stratford PW, shown by the audit data in each arm of the study. The Schomberg A, et al. The patient-specific functional scale: measurement properties in patients with knee dysfunction. Phys comparison is a little more than a political exercise. It allows Ther 1997;77:82-829. investigators to claim that their treatment is better than 5. Bogduk N, McGuirk B. Medical Management of Acute and someone else’s treatment. But comparisons can be invidious. Chronic Low Back Pain: An Evidence-based Approach. It is no great claim to fame, for example, if 40 hours of Amsterdam7 Elsevier; 2002. p. 83-112. intensive 1-on-1 intervention is shown to be better than a 6. Cook RJ, Sackett DL. The number needed to treat: a clinically useful measure of treatment effect. BMJ 1995;310:452-4. couple of 5-minute consultations from a family practitioner. 7. Valat JP, Giraudeau B, Rozenberg S, et al. Epidural cortico- In an explanatory trial, the index treatment is compared steroid injections for sciatica: a randomised, double blind, with a competitive and credible sham treatment. The controlled clinical trial. Ann Rheum Dis 2003;62:639-43. JMPT HIGHLIGHTS

Testing Chiropractic cular and postural demands Palpation of the PSIS ergonomic handgrip may Theories About of massage therapists per- and Estimation of Spinal be a possible risk control CSF Flow forming on-site massages on Levels measure. a client in a massage chair and on a massage table. Does Age or Gender Their findings help practi- Matter? tioners better understand Zhang (p. 374) investigated postural demands in order the effect of age and gender to avoid work injuries. on the heart rate variability (HRV) analysis and to Testing Chiropractic explore the normal range of Theories About Spinal HRV in different age and Fixation gender group for potential Budgell and Bolton (p. 351) Kim et al (p. 386) found that health care applications. It report on experiments using PSIS palpation used to esti- was found that HRV is more anesthetized rats to isolate mate spinal levels showed affected by advancing age and quantify oscillations in statistically higher interexa- than by gender. cerebrospinal fluid pressure miner reliability than iliac that are linked to the respi- crest level. They recommend Neck Muscle Endurance ratory and cardiac cycles. that clinicians be cautious when applying this method Low Back Pain and as a measurement tool, Flat Feet because PSIS palpation can Brantingham et al (p. 380) be inadvertently influenced assessed the association Bakkum et al (p. 336) present by examiner skill and ana- between flat feet and a preliminary study that sug- tomic variations. mechanical low back pain gests that chronic lumbar (MLBP). They discovered vertebral hypomobility in Avoiding Hand and that compared to controls, rats affects synaptic density Wrist Overuse Injuries there was no significant and morphology in the increased prevalence of flat superficial dorsal horn. feet in subjects with multi- These data offer the first ple episodes (z2) of MLBP. anatomic evidence that Peolsson and Kjellman (p. 343) Ergonomic Postures of altered spinal mechanics measured neck muscle endur- Manual Therapists may produce neuroplastic ance in patients with nonspe- changes in the spinal cord. cific neck pain or cervical disk disease before and after the Coupled Motion of the treatment period. Their results Thoracic Spine were compared to each other Sizer et al (p. 390) performed and to reference values from a systematic review to exam- healthy controls. ine the coupling behaviors of Waddington et al (p. 365) the thoracic spine. They found evaluated hand and back Outcome Research that studies varied in their comfort in asymptomatic Bogduk (p. 333) challenges description of the segmental volunteers during spinal the readers of the JMPT and coupling behaviors, likely mobilization using a manual scientific investigators to due to differences in study therapy tool. They state that rethink how we approach the Buck et al (p. 357) inves- design, measurement method, use of an instrumented use, reporting, and interpreta- tigate the difference in mus- and tissue preparation. mobilization device with an tion of outcome research.

335 PRELIMINARY MORPHOLOGICAL EVIDENCE THAT VERTEBRAL HYPOMOBILITY INDUCES SYNAPTIC PLASTICITY IN THE SPINAL CORD

Barclay W. Bakkum, DC, PhD,a Charles N.R. Henderson, DC, PhD,b Se-Pyo Hong, DC, PhD,b and Gregory D. Cramer, DC, PhDc

ABSTRACT

Objective: A widely accepted theoretical model suggests that vertebral hypomobility can cause pain and abnormal spinal mechanics because of changes in sensory input from spinal and paraspinal tissues. The purpose of this pilot study was 3-fold: (1) to make a preliminary determination if chronic vertebral hypomobility at L4 through L6 in the rat would affect synaptic density and/or morphology in the superficial dorsal horn of the L2 spinal cord level, (2) to identify relevant outcome variables for future studies, and (3) to obtain preliminary data that would permit estimating an appropriate sample size for future studies. Methods: Using an established rat model, we fixed 3 contiguous lumbar segments (L4-L6) for 8 weeks with a specially engineered vertebral fixation device. Electron micrographs were obtained from 2 animals from the experimental (fixed) group and each of 3 control groups (no surgery, surgery but no devices implanted, and devices implanted but not fixed). Synapses were randomly selected using a stereological approach and were analyzed for symmetry, curvature, type of postsynaptic profile, and perforations. The synaptic density was also estimated. Results: There was increased synaptic density and percentage of positively curved synapses in the dorsal horn of experimental animals as compared with controls. Experimental animals had a lower percentage of axospinous synapses, with a concomitant increase in the percentage of synapses on dendritic shafts. Conclusions: These preliminary data suggest for the first time that chronic vertebral hypomobility at L4 through L6 in the rat affects synaptic density and morphology in the superficial dorsal horn of the L2 spinal cord level. More definitive studies are warranted, and the biologic significance of these finding should be investigated. (J Manipulative Physiol Ther 2007;30:336Q342) Key Indexing Terms: Neuronal Plasticity; Synapse; Ultrastructure; Dorsal Horn Neurons; Chiropractic

widely accepted theoretical model suggests that a successful rat model of chronic vertebral hypomobility,3,4 vertebral hypomobility can cause pain and abnor- it should be possible to test this hypothetical link between mal spinal mechanics because of changes in vertebral function and nervous system. A 1,2 sensory input from spinal and paraspinal tissues. Until Activity-dependent plasticity is known to occur in the recently, this hypothesis has been difficult to test because of spinal cord throughout life.5 These neurophysiologic the lack of a suitable animal model. With the introduction of changes appear to be driven by input from the periphery and the brain. They play an important role in the effects of spinal cord injury and other central nervous system a Associate Professor, Department of Basic and Health Sciences, disorders, along with the acquisition and maintenance of Illinois College of Optometry, Chicago, Ill. motor skills. Less is known about the morphological b Associate Professor, Palmer Center for Chiropractic Research, correlates associated with these physiologic adaptations. Davenport, Iowa. Synapses are thought to be primary structures in neuro- c Professor and Dean of Research, Department Research, National University Health Sciences, Lombard, Ill. plastic change undergoing modifications in synaptic density, Submit requests for reprints to: Barclay W. Bakkum, DC, PhD, symmetry, curvature, and perforations of the postsynaptic Illinois College of Optometry, 3241 South Michigan Avenue, density (PSD), as part of this process.6,7 Change in the type Chicago, IL 60616, USA (e-mail: [email protected]). of postsynaptic profile (eg, dendritic spine, dendritic shaft, Paper submitted September 27, 2006; in revised form March 3, or soma) is also thought to play an important role.8 2007; accepted March 26, 2007. 0161-4754/$32.00 Chronic vertebral hypomobility as a cause of neuro- Copyright D 2007 by National University of Health Sciences. plastic change within the spinal cord has not been doi:10.1016/j.jmpt.2007.04.007 previously reported. The purpose of this study was to make

336 Journal of Manipulative and Physiological Therapeutics Bakkum et al 337 Volume 30, Number 5 Hypomobility and Synaptic Plasticity

Fig 1. Three SAUs are shown. The far right SAU is rotated to show the scalloped interior of the saddle that is compressed to attach the unit to a spinous process (Fig 2). The stems of the SAUs project above the skin, permitting subsequent linking to produce fixation and malposition of the vertebrae to which they are attached.

Fig 2. A, This diagram shows SAUs attached to the L4, L5, and 6 a preliminary determination if chronic vertebral hypomo- spinous processes [L5 TP = the L5 transverse process]. B, This is a bility at L4 through L6 in the rat would affect synaptic bnever linked Q control rat (CSAU). C, In this rat, the L4, L5, and L6 density and/or morphology in the superficial dorsal horn of vertebrae are linked in fixation. the L2 spinal cord level. The L2 spinal cord segment receives small-caliber afferent input from the L4-5 and L5-6 stem from each SAU passed through the skin to permit zygapophysial joints in the rat.9-11 The superficial dorsal external interconnection of the 3 SAUs by 2 metal links, horn (Rexed’s laminae I and II) is a primary termination site thus, immobilizing the L4-L6 spine region (Fig 2). for small caliber (Ad and C fibers) associated with pain Two rats were randomly assigned to each of the 4 study mechanisms in both the human and the rat.12-14 Successful groups: experimental (E ), implanted SAUs were linked demonstration of neuroplastic spinal cord changes in this LINK to produce spine fixation; surgical control (C ), a sham pilot study would provide bproof of conceptQ justification SURG SAU surgical procedure; SAU control (C ), SAUs in and sample size data that are necessary for designing a SAU place, but not linked in fixation; and normal control (C ), larger definitive study of vertebral hypomobility as a cause NORM rats without any experimental procedures performed. of morphological changes in dorsal horn synapses. After an 8-week link (fixation) period, or equivalent control period, each animal was anesthetized and trans- cardiallyperfusedwithwarm(408C) isotonic saline, METHODS followed immediately by 300-mL cold (48C) fixative (3% Eight male Sprague-Dawley rats (350-450 g, aged 14- glutaraldehyde-4% paraformaldehyde in 0.1 mol/L cacody- 15 weeks) were obtained (Harlan Laboratories, Indianapolis, late buffer, pH 7.3). Subsequently, a laminectomy was Ind). The animals were housed in individual plastic cages at performed and spinal cord segments L1 through L3 were the vivarium of the Palmer Center for Chiropractic identified by following the dorsal roots from the L1 through Research, Davenport, Iowa. This animal housing facility is L3 intervertebral foramina (referenced from the T13 foramen operated in compliance with the Public Health Service just caudal to the most caudal rib). The spinal cord segments Policy on Human Care and Use of Laboratory Animals. were removed and stored overnight in the fixative solution. Water and Purina Lab Block (Ralston Purina, St Louis, Mo) Each spinal cord segment was cut transversely into 3 slabs, were available ad libitum. Before study implementation, the each approximately 1-mm thick. The caudal slab of each Institutional Animal Care and Use Committee of the spinal cord segment was then cut into quarters by cutting institution reviewed and approved all experiments for along the dorsoventral and transverse midlines. Dorsal compliance with the National Research Council Guide for quarters with the right dorsal horn were placed for 1 hour the Care and Use of Laboratory Animals. in 1% osmium tetroxide in 0.1 mol/L cacodylate buffer (pH In this study, an established animal model was used to 7.3) at 48C. The tissue was then dehydrated and embedded in produce chronic intervertebral hypomobility.4 Spinous Epon according to standard procedures. Semithin (1-lm- attachment units (SAUs) (Fig 1) were surgically implanted thick) sections were obtained in the transverse plane with on each of 3 lumbar spinous processes (L4, L5, and L6). A every fifth section kept and stained with cresyl violet. Serial 338 Bakkum et al Journal of Manipulative and Physiological Therapeutics Hypomobility and Synaptic Plasticity June 2007

Fig 3. Electron micrographs of synapses illustrating the specific parameters measured. A, This axospinous asymmetric synapse (asterisk) shows negative curvature. B, This is a straight, symmetric, axosomatic synapse (asterisk). Arrowheads indicate polyribosomes. C., This axospinous asymmetric synapse (asterisk) shows positive curvature. The dendritic spine, with a spine apparatus (sa), can be seen arising from its parent dendritic shaft. D, Both an asymmetric (1) and a symmetric (2) synapse are seen on a single dendritic spine (sp). The asymmetric synapse shows a perforation (arrowhead) in the PSD (arrows). E, Two axospinous asymmetric synapses (asterisks) show no curvature. F, This is a straight symmetric synapse on a dendritic shaft. Arrows indicate microtubules.

thin sections (pale silver, 75-nm thick) were obtained from 2 These were stained with 5% methanolic uranyl acetate and depths that were at least 3 semithin sections apart within the 4% lead citrate. Therefore, 2 animals were examined in each same block of tissue. Consecutive pairs of sections study group (n = 2), and 2 tissue depths were sampled from (disectors) were mounted on formvar-coated slot grids. the caudal third of the L2 spinal cord segment in each of Journal of Manipulative and Physiological Therapeutics Bakkum et al 339 Volume 30, Number 5 Hypomobility and Synaptic Plasticity

Table 1. Data from the study

CNORM CSURG CSAU ELINK

Density, synapses/lm2 (SEM) 0.057 (0.001) 0.054 (0.001) 0.054 (0.001) 0.062 (0.004) Symmetry (%) Asymmetric (SEM) 68 (9) 65 (2) 66 (3) 71 (12) Symmetric (SEM) 32 (5) 35 (2) 34 (2) 29 (8) Curvature (%) Straight (SEM) 65 (7) 68 (6) 63 (2) 55 (11) Positive (SEM) 22 (4) 19 (5) 22 (2) 31 (6) Negative (SEM) 13 (5) 13 (2) 15 (3) 14 (6) Postsynaptic profile (%) Spine (SEM) 47 (8) 50 (7) 49 (5) 40 (7) Dendrite (SEM) 47 (8) 47 (3) 42 (5) 58 (11) Soma (SEM) 5 (4) 3 (1) 9 (5) 2 (2) Perforated PSD (%) (SEM) 2 (1) 3 (1) 3 (1) 7 (1)

CNORM, Control without any experimental procedures performed; CSURG, control with sham SAU implant surgery; CSAU, control with SAUs in place, but not linked in fixation; ELINK, experimental with implanted SAUs linked to produce spine fixation for 8 weeks. these 2 animals, yielding 4 disectors (pairs of consecutive Synaptic curvature was determined by drawing a straight thin sections) for each group. reference line on the electron micrograph from one edge of Photographic montages (final magnification Â25000) the PSD, or contacting portion of the postsynaptic mem- were made from the medial aspect of the lateral one third of brane in the case of symmetric synapses, to the other edge. Rexed’s laminae I and II using a Hitachi-500 transmission In straight synapses, the postsynaptic membrane and PSD electron microscope (Hitachi, Japan). This region of the were parallel to the reference line. Positively curved dorsal horn receives projections from dorsal primary rami synapses had an invagination of the postsynaptic membrane that carry afferents from spinal and paraspinal tissues.15 and PSD into the presynaptic terminal. In negatively curved Synapses were randomly sampled using an unbiased synapses, the postsynaptic membrane and PSD were stereological approach (physical disector method).16 Phy- invaginated into the postsynaptic process. Synapses were sical disectors (a reference section and a lookup section) categorized as either symmetric or asymmetric based upon were produced by making a montage from each of the 2 the relative thickness of the pre- and postsynaptic special- adjacent thin sections constituting a disector. Consequently, izations.18 Perforated synapses were characterized by one or 4 physical disectors (montage pairs) were produced for more breaks in the PSD with presynaptic vesicles that were each study group, 1 disector for each of the 2 L2 spinal not restricted to the area immediately across from the dense cord level tissue samples for each of the 2 animals in each portion of the PSD. Lastly, synapses were identified as study group. Synapses were identified by the presence of a axosomatic by the presence of a nucleus or Golgi apparatus distinct synaptic cleft or an identifiable PSD and the in the postsynaptic profile, axodendritic by the predom- presence of at least 3 synaptic vesicles in the presynaptic inance of microtubules postsynaptically, or axospinous by terminal.17 An unbiased 2-dimensional sampling frame the lack of microtubules and other organelles, with the with a defined area of 1000 lm2 was randomly super- exception of the spine apparatus or other cisternae, in the imposed on each reference section montage. Synapses postsynaptic process.19,20 were counted if their contact region was observed to be For each study group, synapse density was determined within the sampling frame or intersected the inclusion by adding together the total number of synapses counted for edges, but the synapse was not seen on the lookup section both animals in the group and dividing this sum by the total montage. Therefore, the total area examined in each animal area examined within the counting frames, 4000 lm2 (2 rats  was 2000 lm2. 2000 lm2/rat). Descriptive statistics were calculated for the To assess the effect of spinal hypomobility on synaptic synapse categories, and the data were organized graphically morphology, 5 parameters were measured: (1) synapse for simple trend analysis. Inferential statistics do not density (number of synapses per unit area), (2) the generally reveal statistically significant differences in small percentages of synapses showing positively or negatively pilot studies such as this and are not reported here. Rather, curved or straight contacts, (3) the percentages of synapses trend data were examined for hypotheses that should be with perforated postsynaptic densities, (4) the percentages of tested in later adequately powered studies. Therefore, the synapses with symmetric versus asymmetric contacts, and data were examined to identify outcome (response) varia- (5) the percentages of synapses with somatic (soma), bles for future study, estimate appropriate biologic effect dendritic shaft (dendrite), or dendritic spine (spine) post- sizes, and perform power calculations to determine the synaptic profiles (Fig 3). appropriate sample size for later studies. 340 Bakkum et al Journal of Manipulative and Physiological Therapeutics Hypomobility and Synaptic Plasticity June 2007

Fig 4. Density of synapses (synapses/lm2).

Fig 6. Synapse curvature.

Fig 5. Synapse symmetry.

RESULTS Fig 7. Postsynaptic profile. The data are summarized in Table 1. The density of synapses in the experimental group was greater than that observed in each of the control groups (Fig 4). There was no lent in all study groups, with the experimental group apparent difference in the percentages of synapses that were having at least 25% more positively curved synapses than asymmetric vs symmetric between the experimental and the control groups. control groups (Fig 5). Because the design of the ultramicrograph analysis did In all groups, most synapses were straight, but the not specifically target neuron somas, the counting frames experimental group had proportionately fewer straight did not capture many neuron somas (Fig 7). Therefore, low synapses than the control groups (Fig 6). In all groups, percentages of axosomatic synapses were obtained. With relatively few synapses were negatively curved, and these these low numbers, meaningful quantitative differences were not quantitatively different across groups. By con- were difficult to discern. In the control groups, the trast, positively curved synapses were much more preva- remainder of the synapses were fairly equally divided Journal of Manipulative and Physiological Therapeutics Bakkum et al 341 Volume 30, Number 5 Hypomobility and Synaptic Plasticity

less frequently than synapses in tissue sections. Axoso- matic synapses, by their proximity to the site where action potentials are generated, may be very important in determining neuronal activity. Specific studies to determine the effect of vertebral hypomobility on axosomatic synapse morphology, using unbiased sampling strategies that include at least 200 axosomatic synapses, should be conducted. The relative numbers of perforated synapses identified in this study were either similar to or lower than those percentages of this type of synapse identified in other regions of the central nervous system.8 Follow-up studies, with more power to capture this type of synapse, which has been linked to neuroplasticity, should be conducted.

CONCLUSION Fig 8. Perforated synapses. These preliminary data suggest that chronic vertebral hypomobility (fixation) at L4 through L6 in the rat affects between axospinous and axodendritic. In contrast, the synaptic density and morphology in the superficial dorsal experimental group had a lower percentage of axospinous horn of the L2 spinal cord level. Morphological parameters synapses as compared with axodendritic synapses. that appear to be affected include synaptic curvature, type of Like the neuronal somata, relatively few perforated postsynaptic profile, and perforations of the PSD. Additional synapses were observed in the tissue sampled (Fig 8). more definitive studies are warranted, and the biologic Consequently, it was difficult to interpret quantitative significance of these finding should be investigated. differences among the groups, even though this small sample clearly had more perforated synapses in the experimental group as compared with the control groups. Practical Applications ! These preliminary data suggest that chronic DISCUSSION vertebral hypomobility at L4 through L6 in the rat affects synaptic density and morphology These data offer the first anatomical evidence that altered in the superficial dorsal horn of the L2 spinal spinal mechanics may produce neuroplastic changes in the cord level. dorsal horn of the spinal cord. These interesting findings ! Animals with hypomobile lumbar spines appear to suggest the need for larger definitive studies. have an increased density of synapses and an It has been hypothesized that positively curved synapses increased percentage of positively curved synapses are more active synapses, whereas negatively curved 7,21,22 in the superficial dorsal horn. synapses are thought to be less active or inactive. ! The preliminary evidence of these changes is Therefore, the increased percentage of positively curved consistent with increased synaptic activity in the synapses, along with the increased number of synapses, in superficial dorsal horn with lumbar spine hypo- the experimental animals compared with the controls may mobility. indicate an increase in synaptic activity in the dorsal horn of animals with hypomobile (fixated) vertebrae. In addition, previous studies suggest that axospinous synapses are generally excitatory in nature.8 Our small ACKNOWLEDGMENT sample size precludes a definitive determination, but the Support for this study was provided by grant 97-10-18 decreased proportion of axospinous synapses seen in the (principal investigators, Henderson and Cramer) from the experimental animals compared with the controls is National Chiropractic Mutual Insurance Company (Clive, consistent with a decreased amount of excitatory synaptic IA) administered by the Foundation for Chiropractic Educa- activity in the dorsal horn of animals with hypomobile tion and Research. This investigation was conducted at the (fixated) vertebrae. Palmer Center for Chiropractic Research, Davenport, Iowa, Relatively few axosomatic synapses were observed in in a facility constructed with support from Research Facilities this study because the sampling strategy was not designed Improvement Grant C06 RR15433 from the National Center to capture cell bodies, the profiles of which occur much for Research Resources, National Institute of Health. 342 Bakkum et al Journal of Manipulative and Physiological Therapeutics Hypomobility and Synaptic Plasticity June 2007

REFERENCES 12. Mollander C, Xu Q, Grant G. The cytoarchitectonic organ- 1. Henderson CNR. Three neurophysiological theories on the ization of the spinal cord in the rat. I. The lower thoracic and chiropractic subluxation. In: Gatterman MI, editor. Foundations lumbosacral cord. J Comp Neurol 1984;230:133-41. of chiropractic: subluxation, 2nd ed St Louis7 Elsevier Mosby; 13. Kandel ER, Schwartz JH, Jessel TM. The perception of pain. 2005. p. 296-303. Principles of neural science. 4th ed. New York7 McGraw-Hill, 2. Leach RA, Pickar JG. Segmental dysfunction hypothesis: joint Health Professions Division; 2000. p. 472-91. and muscle pathology and facilitation. In: Leach RA, editor. 14. Woolf CJ, Salter MW. Plasticity and pain: role of the dorsal The chiropractic theories, 4th ed. Philadelphia7 Lippincott horn. In: McMahon SB, Koltzenburg M, Wall PD, editors. Williams & Wilkins; 2005. p. 137-206. Wall and Melzack’s textbook of pain. 5th ed. Edinburgh7 3. Henderson CNR, Cramer GD, Zhang Q, DeVocht JW, Fournier Elsevier Churchill Livingstone; 2005. p. 91-106. JT. Introducing the external link model for studying spine 15. Ygge J, Grant G. The organization of the thoracic spinal nerve fixation and misalignment: part 2, biomechanical features. J projection in the rat dorsal horn demonstrated with trans- Manipulative Physiol Ther 2007;30:279-94. ganglionic transport of horseradish peroxidase. J Comp Neurol 4. Henderson CNR, Cramer GD, Zhang Q, DeVocht JW, Fournier 1983;216:1-9. JT. Introducing the external link model for studying spine 16. Geinisman Y. Perforated axospinous synapses with multiple, fixation and misalignment: part 1, need, rationale, and completely partitioned transmission zones: probable struc- applications. J Manipulative Physiol Ther 2007;30:239-45. tural intermediates in synaptic plasticity. Hippocampus 1993; 5. Wolpaw JR, Tennissen AM. Activity-dependent spinal cord 3:417-34. plasticity in health and disease. Annu Rev Neurosci 2001;24: 17. Bakkum BW, Benevento LA, Cohen RS. The effects of light- 807-43. and dark-rearing on the synaptogenesis of the superior 6. Bertoni-Freddari C, Fattoretti P, Paoloni R, Caselli U, colliculus and visual cortex of the rat. J Neurosci Res Galeazzi L, Neier-Ruse W. Synaptic structural dynamics 1991;28:65-80. and aging. Gerontology 1996;42:170-80. 18. Colonnier M. Synaptic patterns on different cell types in the 7. Marrone DF, Petit TL. The role of synaptic morphology in different laminae of cat visual cortex. An electron microscope neural plasticity: structural interactions underlying synaptic study. Brain Res 1968;9:268-87. power. Brain Res Rev 2002;38:291-308. 19. Peters A, Feldman ML, Saldanha J. The projection of the 8. Calverley RKS, Jones DG. Contributions of dendritic spines lateral geniculate nucleus to area 17 of the rat cerebral cortex. and perforated synapses to synaptic plasticity. Brain Res Rev II. Termination upon neuronal perikarya and dendritic shafts. 1990;15:215-49. J Neurocytol 1976;5:85-107. 9. Chung K, Langford A, Applebaum A, Coggeshell RE. Primary 20. Chung SK, Pfaff DW, Cohen RS. Estrogen-induced alterations afferent fibers in the tract of Lissauer in the rat. J Comp Neurol in synaptic morphology in the midbrain central gray. Exp Brain 1979;184:587-98. Res 1988;69:522-30. 10. Budgell B, Noda K, Sato A. Innervation of posterior structures 21. Dyson SE, Jones DG. Quantitation of terminal parameters and in the lumbar spine of the rat. J Manipulative Physiol Ther their interrelationships in maturing central synapses: a per- 1997;20:359-68. spective for experimental studies. Brain Res 1980;183:43-59. 11. Suseki K, Takahashi K, Chiba T, Tanaka K, Morinaga T, et al. 22. Wesa JM, Chang F-LF, Greenough WT, West RW. Synaptic Innervation of the lumbar facet joints: origins and functions. contact curvature: effects of differential rearing on occipital Spine 1997;22:477-85. cortex. Dev Brain Res 1982;4:253-7. NECK MUSCLE ENDURANCE IN NONSPECIFIC PATIENTS WITH NECK PAIN AND IN PATIENTS AFTER ANTERIOR CERVICAL DECOMPRESSION AND FUSION

Anneli Peolsson, PhD, PT,a and Go¨rel Kjellman, PhD, PTa,b

ABSTRACT

Objective: The purpose of this study was to investigate differences in ventral and dorsal neck muscle endurance (NME) among men and women with nonspecific neck pain (NP) or cervical disk disease (who had anterior cervical decompression and fusion [ACDF]) and healthy controls (C). Another purpose was to investigate changes in NME after intervention. Methods: Neck muscle endurance was measured in patients with NP (n = 78) and ACDF (n = 25) before and after the treatment period, and their results were compared to each other and to sex-specific reference values from controls (n = 116) at both the individual and group levels. Results: Patients had significantly decreased ( P b .01) NME compared with control subjects, except for ventral NME in female patients with NP before treatment and male patients with ACDF after treatment. Female patients with ACDF had lower ventral NME than female patients with NP ( P b .01). Among the patients, 35% to 100% had NME disability, with most of them having a lower rate than the 95% confidence interval of controls. Female patients with NP and male patients with ACDF showed improvement ( P b .05) after treatment. Flexion/extension ratio in patients with NP ( P = .36), but not in patients with ACDF ( P b .0001), returned to normal levels after treatment. There was a significant negative correlation ( P b .02) between NME and Neck Disability Index in both patient groups, except for ventral NME in patients with NP before treatment. Conclusion: Many patients had impairment in NME before and after treatment. This suggests that additional exercise of specific training for NME should be incorporated into the rehabilitation program, which may improve treatment outcome. (J Manipulative Physiol Ther 2007;30:343Q350) Key Indexing Terms: Spine; Neck muscles; Physical endurance; Treatment; Disability

here are indications that physical activity with process.3-6 In the Philadelphia panel’s guidelines for patients different forms of exercise may reduce pain and with nonspecific neck pain (NP), neck muscle strength and improve function for patients with neck disor- endurance exercises were recommended.7 T1,2 8-10 ders. Training for neck muscle endurance (NME) has In several studies, Lee et al found that individuals been shown as an important component in the rehabilitation with both treated and untreated NP had lower dorsal NME in comparison to those without neck complaints. Harris et al11 and Jordan et al12 found people with NP to have both lower ventral and dorsal NME compared to those without aSenior University Lecturer, Department of Health and Society, NP. In addition, other studies have shown that patients with f Division of Physiotherapy, Faculty of Health Sciences, Link ping osteoarthritic changes in the cervical spine or who had NP University, Linkfping, Sweden. 13,14 b ¨ had greater neck muscle fatigability, poorer propriocep- R&D Department of Local Health Care, County of Ostergo¨tland, 15 16-19 Sweden. tion, and an altered activation pattern compared to Neck muscle endurance was measured in patients with non- healthy subjects. specific neck pain or cervical disk disease before and after the When measuring NME, it is important to take sex into treatment period. Their results were compared to each other and to consideration, both when using the test procedure and when reference values from healthy controls. comparing the obtained results with reference values.20 Submit requests for reprints to: Anneli Peolsson, PhD, Depart- 8-12,21,22 ment of Health and Society, Division of Physiotherapy, Faculty of Earlier studies of NME in patients with NP have not Health Sciences, Linkfping University, SE-58183 Linkfping, considered sex perspective. Sweden (e-mail:[email protected]). Today, there is no knowledge of the proportion of patients Paper submitted January 29, 2007; in revised form March 3, with decreased NME either before or after treatment, either 2007; accepted March 23, 2007. 0161-4754/$32.00 in patients with nonspecific NP or in patients with cervical Copyright D 2007 by National University of Health Sciences. disk disease proceeding to anterior cervical decompression doi:10.1016/j.jmpt.2007.04.008 and fusion (ACDF). Furthermore, it is not known if there are

343 344 Peolsson et al Journal of Manipulative and Physiological Therapeutics Neck Muscle Endurance June 2007

Table 1. Pretreatment characteristics of 78 patients with non- the 3 treatment options. Therefore, in further analysis, they specific NP, 25 patients with cervical disk disease (ACDF), and were treated as 1 group, the NP group. 116 healthy volunteers (C) These patients participated in a previous published 24 NP ACDF C study, but results from the NME have never been presented. The population and treatments are described in 24,25 Age (y), mean (SD) 45 (11) 47 (10) 43 (12) further detail by Kjellman and O¨ berg. Sex, % women 78 32 48 Pain intensity (mm VAS), 35 (22) 59 (22) 0.8 (3) mean (SD) Patients with Cervical Disk Disease (ACDF) NDI (%), mean (SD) 32 (16) 44 (15) 2 (3) Thirty-three patients with magnetic resonance imaging- VAS indicates visual analog scale; NDI, Neck Disability Index. verified cervical disk disease with neck/arm pain and a neurologic deficit were included in the study before surgery 26 differences in NME between patients with NP and those with (ACDF with a cervical intervertebral fusion cage ), after ACDF. The purpose of this study was to investigate giving informed consent. Twenty-five of the patients differences in ventral and dorsal NME among men and (17 men and 8 women) completed the NME tests both women with nonspecific NP, individuals with cervical disk before surgery and at the 6 months follow-up (mean age, disease, and healthy controls. Another purpose was to 47 years; SD, 10) (Table 1). investigate changes in NME after intervention. Exclusion criteria were as follows: earlier fracture or luxation of the cervical vertebrae, spinal tumor, previous surgery of the cervical spine, diagnosed mental disease, and a lack of familiarity with the Swedish language. METHODS The postoperative treatment included a Philadelphia Subjects collar for 6 weeks; after removal of the collar, most patients The study sample comprised 2 different groups of received conventional (not designed for the study) physi- patients with neck disorder: patients with NP in primary otherapy in primary care facilities. Six months after ACDF, care and ACDF from a spine center, and a control group of there were usually no contraindications for physical activity healthy volunteers. The local ethics committee at Faculty of (except for bextremeQ sports for the neck such as wrestling) Health Sciences approved the study protocols, and the and they were regarded as having no further need of experiments were in compliance with current Swedish laws. treatment, that is, at 6 months follow-up. The patients participated in a previous published study, Nonspecific Patients with NP in Primary Care and were reported to show improvement in ventral, but not 27 After giving informed consent, 78 primary health care in dorsal, NME. Remaining disability, sex differences, and patients with NP were included in a prospective, randomized ventral/dorsal ratio have not been presented. The population and the treatment given are described in further detail by clinical trial and randomly assigned to general exercise, 27 McKenzie treatment,23 or a control group. Seventy patients Peolsson et al. completed the treatment and 65 responded at 2 months follow-up. Seventy-eight (17 men, 61 women; mean age, Control group 45 years; SD, 11) patients participated in the NME test at Reference values of NME were obtained from 116 (60 men entry and 63 patients (14 men, 49 women) when the treatment and 56 women) randomly selected healthy volunteers aged was ended, that is, at 2 months follow-up (Table 1). 24 25 to 64 years (mean age, 43 years; SD, 12) (Table 1). The Inclusion criteria in the study were patients (1) seeking volunteers had different work with different physical care for NP (neck pain origin verified by several tests by an demands and were randomized from the employee records experienced physiotherapist) with or without radiation, and at a university hospital and from a university. The population (2)agerangingfrom18to65years,at3different is described in further detail by Peolsson et al.20 physiotherapy units in primary care and from a private Age and body size have been shown to be of minor physical therapy clinic. Individuals were excluded if they: importance in the NME test performed20 and were not taken (1) received physiotherapeutic or chiropractic treatment in into consideration. In the present study, patients and controls the past 3 months; (2) showed evidence of an affected nerve were matched according to sex. root, and exhibited a symptomatic whiplash-associated disorder within the past 6 months; (3) were involved in an accident less than 10 days previously; (4) had other Measurements diseases; (5) lacked familiarity with the Swedish language. The healthy controls were measured only once. Patients Factorial analysis of variance (ANOVA) with Bonferroni/ were measured both before and after the treatment, with a Dunn posthoc test showed that there were no significant follow-up at 2 months for the NP group and at 6 months for differences in NME either before or after treatment among the ACDF group. Journal of Manipulative and Physiological Therapeutics Peolsson et al 345 Volume 30, Number 5 Neck Muscle Endurance

Pain Intensity Current pain intensity in the neck was registered on a 100-mm (0 = no pain, 100 = worst imaginable pain) horizontal VAS28 before and after every test.

Neck-Specific Disability Disability was measured using the NDI. The 10 sections (pain intensity, personal care, lifting, reading, headaches, concentration, work, driving, sleeping, and recreation) are scored from 0 to 5, added together, and then transformed to percentages with 0% being equivalent to no pain or difficulties, and 100% being the highest score for pain and difficulty on all NDI items.29

Neck Muscle Endurance Measurement of endurance was performed in the same way in all 3 populations and was standardized as follows.20,27 The test position was carefully monitored by the test leader (well trained in the procedure) and immediately corrected if the standardized test position was not maintained. Before the test, the subjects were instructed in the performance of the endurance tests (a test trial was performed in each position). They were instructed to maintain the test position for as long as possible, stopping at exhaustion, pain in the neck, or pain radiating into the arms. During measurements, the test leader reminded the subjects about the correct test position, but did not offer encouragement. The ventral procedure was always per- formed before the dorsal. When ventral NME was measured, the subject was in a supine position with legs straight and the arms positioned alongside the body. The subject was instructed to flex the upper cervical spine, being told bdo a small nod of the head and hold your chin against your chestQ and to raise their head just above the examination table until exhaustion20,27 (Fig 1A). The endurance was measured in seconds with a stopwatch. In the endurance measurement of dorsal neck muscles, the subject was in a prone position with legs straight, arms positioned at the sides, and a load (2 kg for women and 4 kg for men) applied around the head just above the ears. The subject then extended and raised the head just above the examination table (the tip of the chin pointing Fig 1. Test position: ventral NME test (A); dorsal NME test (B). In 20,27 against the floor) as shown in Figure 1B. The this photo, the head of the examination table is tipped for endurance measurement of dorsal neck muscles was photographic reasons. During the actual test procedure, the measured until exhaustion, and was measured in seconds examination table was in a horizontal position. with a stopwatch.20,27 The intra- and intertester reliability for the ventral and Statistical Methods the dorsal NME test procedures used in the present study Differences in mean values among the 2 patient groups have been reported to be good (intraclass correlation and the control group were analyzed for statistical signifi- coefficient z0.80) both for healthy people and patients cance by factorial ANOVA with the Bonferroni/Dunn with NP.20,30 posthoc test. For paired and unpaired 2-group comparisons, 346 Peolsson et al Journal of Manipulative and Physiological Therapeutics Neck Muscle Endurance June 2007

Table 2. Mean values and SD of ventral and dorsal NME (seconds) in patients with nonspecific NP in primary care, patients with cervical disk disease (ACDF), and healthy controls (C)

NP ACDF Control P (NP-C) P (ACDF-C) P (NP-ACDF)

All Test 1 Ventral 33 (28) 53 (68) 97 (94) b.001* .008* .25 Dorsal 110 (109) 54 (75) 461 (350) b.0001* b.0001* .36 Test 2 Ventral 40 (29) 70 (86) 97 (94) b.0001* .12 .10 Dorsal 173 (161) 92 (101) 461 (350) b.0001* b.0001* .22

Men Test 1 Ventral 49 (30) 75 (72) 153 (103) b.0001* b.002* .39 Dorsal 86 (81) 71 (85) 417 (310) .0001* b.0001* .87 Test 2 Ventral 55 (34) 102 (91) 153 (103) .003* .05 .17 Dorsal 174 (148) 130 (109) 417 (310) .003* .0002* .65

Women Test 1 Ventral 28 (25) 6 (8) 37 (11) .03 b.0001* .002* Dorsal 118 (117) 18 (28) 507 (386) b.0001* b.0001* .33 Test 2 Ventral 35 (26) 8 (7) 37 (11) .69 b.0001* .0002* Dorsal 173 (165) 24 (25) 507 (386) b.0001* b.0001* .19

Patients were measured twice, before (test 1) and after treatment (test 2). Controls were measured only once. P values of less than .0167 were considered statistically significant. * Statistically significant.

the differences between means were analyzed for statistical .0001), except for ventral NME in patients with ACDF after significance by the paired or unpaired 2-tailed Student t test, treatment ( P = .12) (Table 2). When the analysis was respectively. classified by sex, patients had lower ventral and dorsal NME Disability in individuals’ NME was defined as values lower than controls ( P b .01), except for ventral NME in female than the 10th percentiles for the sex-specific dorsal and ventral patients with NP and ventral neck muscle endurance in male NME of the control group, and was analyzed by comparison of patients with ACDF after treatment (Table 2). Female patients each individual to sex- and direction-specific values.20 The in the ACDF group had significantly lower ventral NME than cutoff values for subnormal dorsal and ventral NME were 157 female patients with NP before and after treatment ( P b .01) and 56 seconds for men, and 173 and 23 seconds for women.20 (Table 2). There were no other significant differences Disability in NME was analyzed by comparison of each between the 2 patient groups (Table 2). individual to sex- and direction-specific cutoff values. Mean In the NP group, 40% to 82% of patients had disability values of each patient group were compared with the 95% (lower than the 10th percentile of the sex-specific mean confidence interval (CI) obtained from control subjects and value) in NME before and after treatment. Except for were noted to be within or lower than the 95% CI. women’s ventral NME after treatment, the mean value of Pearson correlation coefficient analysis was used to patients with NP was lower than the 95% CI of controls investigate the respective relationships of pain intensity (Table 3). In the ACDF group, 35% to 100% had NME and NDI to NME. disability, and all sex-specific mean values were lower than P values less than .0167 were considered statistically the 95% CI of controls either on group comparison or when significant in the factorial ANOVA with Bonferroni/Dunn classified by sex (Table 3). posthoc test. Otherwise, P b .05 was considered statisti- The mean ventral/dorsal ratios were 1.16 before and 0.87 cally significant. after treatment ( P = .36) in patients with ACDF; this could be compared with 0.52 before treatment ( P = .0001) and 0.33 afterward ( P b .0001) in patients with NP and 0.28 in RESULTS control subjects ( P b .0001). Patients with NP had a Comparison Between Patients and Controls significantly higher ( P = .005) flexion/extension ratio Both before and after treatment, the 2 patient groups had before treatment than the controls, but were normalized lower ventral and dorsal NME than healthy controls ( P b afterward ( P = .36). Journal of Manipulative and Physiological Therapeutics Peolsson et al 347 Volume 30, Number 5 Neck Muscle Endurance

Table 3. Disability in ventral and dorsal NME (seconds) in with ACDF had lower ventral NME than female patients patients with nonspecific NP in primary care and patients with with NP ( P b .01) both before and after treatment. Neck cervical disk disease (ACDF) before (test 1) and after treatment 8-12,21 (test 2) muscle endurance in people with nonspecific NP, as well as in patients with whiplash-associated disorders,22 has ABbeen shown as altered compared with healthy controls, but in none of the studies were the results analyzed with regard to NP, ACDF, NP, ACDF, sex. Peolsson et al27 reported patients with ACDF to be n (%) n (%) 95% CI 95% CI improved in ventral but unchanged in dorsal NME 1 year Men after ACDF; however, they did not analyze men and women Test 1 separately, and there were no comparisons with healthy Ventral 12 (71) 9 (53) lower lower controls. Other comparisons of NME among patients with Dorsal 14 (82) 13 (76) lower lower nonspecific NP and ACDF have not been reported earlier, Test 2 and we expected patients with ACDF to have far lower NME Ventral 9 (64) 6 (35) lower lower Dorsal 9 (64) 10 (62) lower lower compared to patients with NP. That seems true for ventral NME in women, but not for men. In dorsal NME, there were Women no significant differences between the patient groups. In Test 1 power analysis with 20% b error (power = 1 À b = 80%) and Ventral 30 (51) 8 (100) lower lower an a error of .05, 43 patients (10 for women and 137 for men) Dorsal 44 (61) 8 (100) lower lower Test 2 in each of the NP and ACDF groups would be enough to Ventral 19 (40) 8 (100) within lower detect statistically significant differences in dorsal NME Dorsal 32 (65) 8 (100) lower lower between the patient groups. After this analysis, one could Patients are matched to sex-specific reference values obtained from conclude that women in the ACDF group have lower NME randomly selected volunteers (controls). Disability is presented in (A) than those in the NP group. individuals (number and percentages) lower than the 10th percentile of the Neck muscle endurance in female patients with NP ( P b mean value of controls, and as (B) the mean value of the patient group .05) and male patients with ACDF ( P b .05) improved after within or lower than the 95% CI of controls. treatment. For male patients with NP in dorsal NME, 29 men would be enough, and for male patients with NP in ventral Effect of Treatments NME and for female patients with ACDF more than Neck muscle endurance in female patients with NP 200 individuals are needed from 80% power analysis to (ventral P = .04, dorsal P = .001) and male patients with detect significant differences between test occasions. Wang ACDF (ventral P = .01, dorsal P = .003) improved after et al31 had earlier reported patients with nonspecific NP to treatment, compared with pretreatment values. be improved in their ventral NME, with higher physical There was an improvement in pain intensity and NDI in function and lowered pain intensity after an individualized the NP group ( P b .0001) and in NDI ( P = .0005) in the physical intervention. In the present study this was true for ACDF group at follow-up compared with pain and NDI female patients with NP, and with a larger study sample of before treatment. Neck Disability Index both before ( P = men it would have also been true for male patients with NP. .0001) and after treatment ( P b .0002), and pain intensity Ylinen et al4,5 reported that pain intensity and disability after treatment ( P = .006) were worse in the ACDF group decreased and pressure pain threshold increased in women compared to the NP group. with chronic nonspecific NP after neck muscle strength and Correlations Between Pain Intensity or NDI and NME endurance training. Similar to what we have observed in In patients with ACDF, there was a significant correlation NME in our patient group with ACDF, earlier studies on objective variables in patients with cervical disk disease between NME and pain intensity both before treatment and at 27,32-34 follow-up (r = À0.54 to À0.66, P b .01), except for dorsal have shown rather poor treatment outcomes. In a prospective randomized study between surgery, physiother- NME (r =0.39,P = .06) at follow-up. In patients with NP, 32 dorsal NME before treatment was significantly correlated with apy, and a cervical collar, Persson et al reported hand and pain intensity (r = À0.30, P = .01) and otherwise uncorrelated. arm strength to be equal among the treatment groups at a There was a significant correlation between NME and 15-month follow-up, with improvements in some of the NDI (ACDF, r = À0.56 to À0.68, P b .01; NP, r = À0.31 to muscles studied. There were some improvements in the b affected side compared to the nonaffected side in the surgery À0.38, P .02), except for ventral NME before treatment in 32 patients with NP (r = À0.23, P = .07). and physiotherapy groups. In the same study, but with regard to cervical range of motion and shoulder mobility, there were no significant differences among groups at the DISCUSSION 15-month follow-up.33 Except for decreased cervical active Patients with NP and those with ACDF had mainly range of motion (AROM) in the physiotherapy group, decreased NME compared with controls, and female patients mobility was unchanged compared with that before treat- 348 Peolsson et al Journal of Manipulative and Physiological Therapeutics Neck Muscle Endurance June 2007

ment.33 Ylinen et al34 reported that 2 years after cervical Patients had lower NME compared with controls, and disk surgery, patients had decreased cervical AROM and their considerable remaining NME disability after treat- neck strength compared to matched healthy controls. ment may be an indication that the rehabilitation process The different follow-up times for the NP and ACDF was unsatisfactory with regard to NME and that, perhaps, groups resulted from the fact that the follow-up was done the rehabilitation was ended too early. Specific, low- when the treatment was ended. Six months after ACDF loaded NME exercises to increase NME and propriocep- there are usually no contraindications for activity, but the tion, as recommended in recent studies,6,16,18 may fusion is not regarded as healed until 1 year after surgery. improve NME outcomes and should be considered in Neck muscle endurance did not improve in the ACDF future rehabilitation. group between the 6- and 12-month follow-ups ( P = .20- Jull et al16 and Falla et al18,19 found that patients with NP .24). It would have been an advantage with a 1-year put higher demands on their superficial neck muscles than follow-up also for patients with NP; however, we have no do healthy people, to compensate for atrophy and fatty reasons to believe that they will improve in NME after infiltration of the deep muscles. We tested only neck intervention ended. muscles in general. After treatment, the ventral/dorsal ratio in the NP group The load applied during the dorsal neck muscle became equal compared with controls ( P = .36), but was procedure was adjusted for sex, but not for the neck still higher in the ACDF group ( P b .0001). Earlier studies strength of the particular individual. Thus, we may have on ventral/dorsal ratio in NME in patients with neck measured a maximal strength performance for some subjects disorders are lacking, but healthy women have been and a submaximal endurance performance for other reported to have lower flexion/extension ratios than subjects, in both the dorsal and ventral neck muscle men.20 The neck muscles’ flexion/extension strength ratio procedures. If the load applied had been individually has been reported as both higher35 and lower36 in patients adjusted after a maximal voluntary contraction, the distri- with a whiplash-associated disorder compared with people bution may have been smaller. However, because of the risk without a neck disorder. The very high NME ventral/dorsal of causing pain, it is often not preferable to use maximal ratio in patients with ACDF we observed may be a reason tests in pain patients in clinical practice. for their higher pain and disability compared with the NP Here, as well as in the studies by Grimmer,38 Ljunquist group at 12 months follow-up and for the ACDF group’s et al,21,39 Lee et al,8-10 and Peolsson et al,20,27 NME was high degree of remaining disability after treatment.27,37 measured with the patient lying down. From a functional We found that 40% to 65% of patients with NP and perspective, it might have been better if NME had been 35% to 100% of patients with ACDF had NME disability measured in an upright position, but it is difficult to find one at follow-up. Percentages of patients with neck disorders position that is stable. The function of the neck muscles is with remaining NME disability have not been previously static when carrying the head and dynamic during the reported, but our results can be compared to the results of hundreds of daily movements of the head. Consequently, it Peolsson et al,27 who found that approximately one half of is debatable as to whether it is better to measure NME their patients had lingering disability in neck strength and statically or dynamically. In the present study, we measured about one third in hand strength and AROM 1 year after static endurance in stable and comfortable positions that are ACDF. Except for female patients with ACDF, the easy to apply in daily clinical practice. numbers of patients with disability were almost the same Another factor that can cause error when measuring as reported for other variables by Peolsson et al27,37 and NME is the test subject’s ability to understand the verify the finding that many patients have remaining instructions and the test leader’s behavior, for example, disability after treatment. the ability to give instruction before and during the The 10th percentile as recommended by Peolsson procedure.40 Boredom could also be a cause of error, et al20 is one way to calculate values that can be used especially in extension and in those individuals with the to identify subnormal NME; the deficit rate will, of highest performance. Our test leader carefully supervised course, be altered with the use of other cutoff points. The the procedure, and tested persons were informed of the advantage of using 10th percentiles in the present study is importance of doing their best. that the analysis is not so sensitive to outliers. When the Some individuals may be reluctant to perform their best specificity and sensitivity of 10th percentiles used as a because of discomfort or pain, and this is a factor to cutoff point were calculated, the specificity was 91% and consider when measuring physical performance (eg, NME). the sensitivity was 56% to 84% for patients with ACDF The NME of patients with ACDF was mainly moderately to and 45% to 74% for patients with NP, before and after substantially correlated with both pain and NDI (r = À0.54 treatment. Because some people without neck disorders to À0.68, P b .001) on both test occasions. As reported by could have low NME and because neck disorders can Ylinen et al41 for neck muscle strength in patients with NP, have several reasons of origin other than low NME, the the NME of the NP group was mainly not correlated with specificity and sensitivity seem reasonable. pain. However, in contrast to the report Ylinen et al,41 NDI Journal of Manipulative and Physiological Therapeutics Peolsson et al 349 Volume 30, Number 5 Neck Muscle Endurance

was weakly but significantly correlated with NME. Chiu 2. Kay TM, Gross A, Goldsmith C, et al. Exercises for et al42 found a weak correlation between pain intensity and mechanical neck disorders. Cochrane Database Syst Rev 2005;CD004250. both cervical AROM and neck strength. The higher values 3. RandlbvA,astergaard M, Manniche C, et al. Intensive of correlation between NME and pain and disability in dynamic training for females with chronic neck/shoulder pain. patients with ACDF compared with patients who had NP A randomized controlled trial. Clin Rehabil 1998;12:200-10. may have resulted from patients with ACDF having a 4. Ylinen J, Takala E-P, Nyk7nen M, et al. Active neck muscle specific diagnosis and higher pain and disability and training in the treatment of chronic neck pain in women: a randomized controlled trial. JAMA 2003;289:2509-16. therefore more anxious abut their NME performance. 5. Ylinen J, Takala E-P, Kautiainen H, et al. Effect of long-term Another explanation is that their low NME performance neck muscle training on pressure pain threshold: a randomized impaired pain and disability. The weak to moderate controlled trial. Eur J Pain 2005;9:673-81. correlations between pain and NME in patients with NP 6. Falla D, Jull G, Hodges P, Vicenzino B. An endurance-strength and ACDF, respectively, and the slightly higher values of training regime is effective in reducing myoelectric manifes- tations of cervical flexor muscle fatigue in females with chronic correlation between NME and NDI compared with pain, neck pain. Clin Neurophysiol 2006;117:828-37. lead us to believe that we measured muscle function, at least 7. Philadelphia panel evidence-based clinical practice guidelines to some extent. on selected rehabilitation interventions for neck pain. Phys Ther 2001;81:1701-11. 8. Lee H, Nicholson LL, Adams RD. Cervical range of CONCLUSIONS associations with subclinical neck pain. Spine 2003;29:33-40. 9. Lee H, Nicholson LL, Adams RD. Neck muscle endurance, We conclude that many patients with NP and ACDF have self-report and range of motion data from subjects with treated impaired NME compared with healthy controls before and and untreated neck pain. J Manipulative Physiol Ther also after rehabilitation. This suggests that additional 2005;28:25-32. 10. Lee H, Nicholson LL, Adams RD, Bae S-S. Body chart pain exercise of specific training for NME should be incorpo- location and side-specific physical impairment in subclinical rated into the rehabilitation program, which may improve neck pain. J Manipulative Physiol Ther 2005;28:479-86. treatment outcome. 11. Harris KD, Heer DM, Roy TC, Santos DM, Whitman JM, Wainner RS. Reliability of a measurement of neck flexor muscle endurance. Phys Ther 2005;85:1349-55. 12. Jordan A, Mehlsen J, Ostergaard K. A comparison of physical Practical Applications characteristics between patients seeking treatment for neck pain and age-matched healthy people. J Manipulative Physiol Ther 1997;20:468-75. ! Patients with neck disorder had significantly 13. Gogia PP, Sabbahi MA. Electromyographic analysis of neck decreased NME compared with healthy controls. muscle fatigue in patients with osteoarthritis of the cervical ! Women who had undergone surgery for cervical spine. Spine 1994;19:502-6. disk disease had lower ventral NME than women 14. Falla D, Rainoldi A, Merletti R, Jull G. Myoelectric manifestations of sternocleidomastoid and anterior scalene with nonspecific NP. muscle fatigue in chronic neck pain patients. Clin Neuro- ! Thirty-five percent to 100% of the patients had physiol 2003;114:488-95. disability in NME when the treatment was ended. 15. Revel M, Andre-Deshays C, Minguet M. Cervicocephalic That suggests that additional exercise of specific kinesthetic sensibility in patients with cervical pain. Arch Phys training for NME should be incorporated into the Med Rehabil 1991;72:288-91. 16. Jull G, Kristjansson E, DallA` lba P. Impairment in the cervical rehabilitation program. flexors: a comparison of whiplash and insidious onset neck ! Women with nonspecific NP and men who had pain patients. Man Ther 2004;9:89-94. undergone surgery for cervical disk disease 17. Falla D. Unravelling the complexity of muscle impairment in improved in NME after treatment. chronic neck pain. Man Ther 2004;9:125-33. 18. Falla D, Jull G, Edwards S, Koh K, Rainoldi A. Neuro- muscular efficiency of the sternocleidomatoid and anterior scalene muscles in patients with chronic neck pain. Disabil Rehabil 2004;26:712-7. 19. Falla D, Rainoldi A, Jull G, Stavrou G, Tsao H. Lack of ACKNOWLEDGMENTS correlation between sternocleidomastoid and scalene muscle fatigability and duration of symptoms in chronic neck pain This study was supported by the Faculty of Health patients. Neurophysiol Clin 2004;34:159-65. Sciences of Linkfping University. 20. Peolsson A, Almkvist C, Dahlberg C, Lindqvist S, Pettersson S. Age- and sex-specific reference values of a test of neck muscle endurance. J Manipulative Physiol Ther 2007;30:171-7. 21. Ljungquist T, Fransson B, Harms-Ringdahl K, Bjfrnham 2, REFERENCES Nygren 2. A physiotherapy test package for assessing back 1. Gross AR, Hoving JL, Haines TA, et al. Manipulation and and neck dysfunction—a discriminative ability for patients mobilisation for mechanical neck disorders. Cochrane Data- versus healthy control subjects. Physther Res Int 1999;4: base of Syst Rev 2004;CD004249. 123-40. 350 Peolsson et al Journal of Manipulative and Physiological Therapeutics Neck Muscle Endurance June 2007

22. Kumbhare DA, Balsor B, Parkinson WL, et al. Measurement physiotherapy or cervical collar: a prospective, controlled of cervical flexor endurance following whiplash. Disabil study. Eur Spine J 1997;6:256-66. Rehabil 2005;27:801-7. 33. Persson LCG, Moritz U. Pain, muscular tenderness, cervical 23. McKenzie R. The cervical and thoracic spine. Mechanical and shoulder mobility in patients with cervical radiculopathy diagnoses and therapy. Waikane, New Zealand7 Spinal randomly treated with surgery, physiotherapy or a cervical Publications; 1990. collar. Pain Clin 1998;11:51-67. 24. Kjellman G, O¨ berg B. A randomized clinical trial comparing 34. Ylinen JJ, Savolainen S, Airaksinen O, Kautiainen H, Salo P, general exercise, McKenzie treatment and a control group in H7kkinen A. Decreased strength and mobility in patients after patients with neck pain. J Rehabil Med 2002;34:183-90. anterior cervical discectomy compared with healthy subjects. 25. Kjellman G. Neck pain: analysis of prognostic factors and Arch Phys Med Rehabil 2003;84:1043-7. treatment effects. PhD thesis. Faculty of Health Sciences, 35. Prushansky T, Gepstein R, Gordon C, Dvir Z. Cervical muscles Linkfping University, Sweden; 2001. weakness in chronic whiplash patients. Clin Biomech 2005; 26. Peolsson A, Vavruch L, Hedlund R. Long-term randomised 20:794-8. comparison between a Carbon fibre cage and the Cloward 36. Vernon HT, Aker P, Aramenko M, et al. Evaluation of neck procedure in the cervical spine. Eur Spine J Eur Spine J muscle strength with a modified sphygmomanometer dyna- 2007;16:173-8. mometer: reliability and validity. J Manipulative Physiol Ther 27. Peolsson A, Vavruch L, O¨ berg B. Disability after anterior 1992;15:343-9. decompression and fusion for cervical disc disease. Adv 37. Peolsson A, Vavruch L, O¨ berg B. Can the results six month Physther 2002;4:111-24. after anterior cervical decompression and fusion identify 28. Scott J, Huskisson EC. Graphic representation of pain. Pain patients who will have remaining deficit at a long-term? 1976;2:175-84. Disabil Rehabil 2006;28:117-24. 29. Vernon H, Mior S. The neck disability index: a study of 38. Grimmer K. Measuring the endurance capacity of the cervical reliability and validity. J Manipulative Physiol Ther 1991;14: short flexor muscle group. Aust Physiother 1994;40:251-4. 409-15. 39. Ljungquist T, Harms-Ringdahl K, Nygren 2, Jensen I. Intra- 30. Peolsson A. Functional analysis of the cervical spine: and inter-rater reliability of an 11-test package for assessing reliability, reference data and outcome after anterior cervical dysfunction due to back or neck pain. Physther Res Int decompression and fusion. PhD thesis. Faculty of Health 1999;4:214-32. Sciences, Linkfping University, Sweden; 2002. 40. Krebs D. Measurement theory. Phys Ther 1987;67:1834-9. 31. Wang WT, Olson SL, Campbell AH, Hanten WP, Gleeson 41. Ylinen J, Takala E-P, Kautiainen H, et al. Association of neck PB. Effectiveness of physical therapy for patients with pain, disability and neck pain during maximal effort with neck neck pain: an individualized approach using a clinical muscle strength and range of movement in women with decision-making algorithm. Am J Phys Med Rehabil 2003; chronic non-specific neck pain. Eur J Pain 2004;8:473-8. 82:203-18. 42. Chiu TT, Lam T-H, Hedley AJ. Correlation among physical 32. Persson LCG, Moritz U, Brandt L, Carlsson C-A. Cervical impairments, pain, disability, and patient satisfaction in radiculopathy: pain, muscle weakness and sensory loss in patients with chronic neck pain. Arch Phys Med Rehabil patients with cervical radiculopathy treated with surgery, 2005;86:534-40.

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Personal subscriptions to Journal of Manipulative and Physiological Therapeutics Online are for individual use only and may not be transferred. Use of Journal of Manipulative and Physiological Therapeutics Online is subject to agreement to the terms and conditions as indicated online. CEREBROSPINAL FLUID PRESSURE IN THE ANESTHETIZED RAT

Brian S. Budgell, PhD,a and Philip S. Bolton, PhDb,c

ABSTRACT

Objective: The primary aims of this study were to determine the major frequencies and powers of oscillations in cerebrospinal fluid (CSF) pressure in the anesthetized rat, and determine whether the CSF pressure oscillations correlated with the major oscillation frequencies in the cardiovascular and respiratory systems as proposed by some chiropractic theories. Methods: The cardiac and ventilatory cycles, and CSF pressure were simultaneously recorded during spontaneous and positive-pressure mechanical ventilation in the anesthetized rat. Power spectra were generated from the raw data to identify the major oscillation frequencies in cardiorespiratory and CSF data sets. Entrainment of CSF pressure with ventilation was tested by mechanically pacing the ventilation over a range of frequencies. Results: The most powerful oscillation in CSF pressure was coincident with ventilatory chest movement during both spontaneous and mechanically paced ventilation. In 22 of 26 trials, there was also a very weak oscillation in CSF pressure that was entrained to heart rate. In addition, in 21 of 26 trials, it was possible to identify a low-frequency oscillation (b0.25 Hz) in CSF pressure that was coincident with a low-frequency oscillation in the power spectrum of the cardiac cycle. Conclusions: This study suggests oscillations in CSF pressure in the anesthetized rat are entrained to and driven by ventilation. The arterial pulse pressure makes little contribution to oscillations in CSF pressure in the immobile, anesthetized rat. This study provides normative, quantitative data on which to develop studies concerning the effects of vertebral movements and spinal posture on CSF dynamics. (J Manipulative Physiol Ther 2007;30:351Q356) Key Indexing Terms: Rat; Cerebrospinal Fluid; Chiropractic

he clinical application of manual therapies such as Among theories at the core of certain manual therapies cranial and spinal manipulation is guided by are hypotheses that altered motion or malposition of the certain fundamental clinical hypotheses and theo- cranial bones or vertebrae interfere with normal neurologic T 1-3 ries concerning the causes of disease and the physiologic function and thus result in disease. Different iterations of impact of the involved treatments. Indeed, at times such these core theories may evoke somewhat different and hypotheses and theories may seem to hold more importance perhaps complementary pathologic mechanisms such as than objective and quantitative measures of clinical effects. direct pressure on neural structures, tension on meninges, or Many of these clinical hypotheses and theories remain to be disturbances in normal cerebrospinal fluid (CSF) move- rigorously tested. ment.3-5 With regard to the latter, it has been proposed that rhythmic oscillations, both normal and abnormal, in CSF a Associate Professor, School of Health Sciences, Faculty of pressure may result in palpable movements of the cranial Medicine, Kyoto University, Kyoto, Japan. and vertebral bones, sometimes termed the cranial rhythmic b Associate Professor, School of Biomedical Sciences, Faculty of impulse (CRI), and that this CRI may therefore have some Health, University of Newcastle, Callaghan, NSW 2308, Australia. application to diagnosis. However, little data exist concern- c Hunter Medical Research Institute, New Lambton, NSW ing the normal frequencies of the CRI, and it is uncertain Australia. whether oscillations of CSF pressure actually result in a CRI Submit requests for reprints to: Philip S. Bolton, PhD, Associate 6,7 Professor, School of Biomedical Sciences, Faculty of Health, that is palpable on manual examination. University Drive, Callaghan, NSW 2308, Australia Previously, it has been possible to measure lumbar CSF (e-mail: [email protected]). pressure in anesthetized rats,8 and to demonstrate large Paper submitted September 12, 2006; in revised form February absolute pressure changes associated with cerebral hemor- 20, 2007; accepted March 27, 2007. 0161-4754/$32.00 rhage. However, it is unclear whether relatively small Copyright D 2007 by National University of Health Sciences. changes in CSF pressure at the cervical level (or higher) doi:10.1016/j.jmpt.2007.04.002 might be detectable at the lumbar level given the normal

351 352 Budgell and Bolton Journal of Manipulative and Physiological Therapeutics CSF Pressure June 2007

oscillations in CSF pressure at this level. In other words, good physiologic condition, to be returned to spontaneous there may be too much noise in the normal lumbar CSF ventilation. The electrocardiogram (EKG) was recorded pressure recording to permit detection of a subtle pressure from subcutaneous electrodes on each side of the chest. The signal from the more rostral spine or cranium. Furthermore, EKG served as a backup for monitoring the cardiac cycle in even in the prone animal, pressure measures at the lumbar the event, as sometimes happens in prolonged experiments, level may be affected by, for example, small changes in that the carotid cannula became obstructed. Body temper- head position,9 and hence, in absolute terms, lumbar CSF ature was monitored via a rectal probe (Model 43TA; pressure cannot be equated with intracranial pressure. Thus, Yellow Springs Instrument Company, Yellow Springs, in the absence of quantitative data on normal oscillation Ohio) and maintained at 378Cto37.58C by using a heating frequencies, it would be difficult to identify changes in CSF blanket (K-20-D, American Pharmaseal Company, Valencia, fluid dynamics associated with vertebral movement or static Calif) and infrared lamp. Adequacy of anesthesia was malposition at any spinal level, and no conclusions can be judged by stability of heart rate and BP, and by periodically made about any relationship between lumbar CSF oscil- checking for the absence of withdrawal and corneal reflexes. lations and the putative CRI. A catheter (PE10, Atom Medical, Tokyo) was intro- Although animal models have been developed to study duced into the subarachnoid space of the lower lumbar the effects of spinal joint fixation on vertebral morphol- spine via a partial laminectomy of the L5 vertebra by using ogy,10 and the effects of vertebral motion and manipulation an established protocol.8 Specifically, the caudal half of the on paravertebral muscle spindle behavior,11 there are L5 lamina was surgically exposed and removed along with currently no available animal models to study the effects the yellow ligament, leaving the dura mater intact. A small of vertebral movement or position on CSF dynamics. The incision was made in the dura mater, and through this aim of this study was to quantify the frequencies and incision a 25-gauge needle was inserted and used to make relative strengths (powers) of oscillations in CSF pressure in a small puncture in the arachnoid mater caudal to the the anesthetized rat as a first step in developing a model to termination of the spinal cord. Under direct visualization investigate the effects of vertebral displacements and with a dissecting microscope (OPMI-11, Carl Zeiss, manipulations on CSF dynamics. Sydney, Australia), approximately 5 mm of PE10 tubing was fed into the subarachnoid space, and the incision in the arachnoid mater was sealed with tissue adhesive (Quick Fix, Shelley Pty Ltd Padstow, NSW, Australia). METHODS The catheter was filled with artificial CSF (aCSF)12 from a Experiments were performed on 8 urethane-anesthetized reservoir in a side port and connected to a pressure adult male Wistar rats aged 8 to 12 weeks and weighing 360 transducer for continuous measurement of lumbar CSF to 430 g. All procedures were performed in accordance with pressure. The EKG, BP, CSF pressure, ventilatory flow, protocols approved by the University of Newcastle animal and chest excursion were recorded on a computer (G3 care and ethics committee, and conformed to the Australian Apple Macintosh) and analyzed by using a dedicated data National Health and Medical Research Council Code for acquisition system (MacLab 8S, ADInstruments). Mean Practice for the use of animals in experiments. arterial pressure and mean CSF pressure were computed by Anesthesia was induced by an intraperitoneal injection of using the data acquisition system and displayed in real- urethane (1.3 g/kg). Animals were then tracheotomized and time to monitor the stability of the preparation. intubated, and initially allowed to ventilate spontaneously. Data were sampled at a rate of 2000 Hz (EKG, BP, and A carotid artery was catheterized for the continuous CSF pressure) or 200 Hz (chest excursion and ventilatory measurement of blood pressure (BP) and heart rate (World flow), and analyzed using a dedicated software data analysis Precision Instruments, BP-1, Sarasota, Fla), and a jugular system (Chart ver 4.1.1, ADInstruments). Data were vein was catheterized for administration of supplementary obtained from a total of 26 trials performed in 8 animals. anesthetic and fluids as necessary. Respiratory rate was Each trial consisted of a 4-minute recording period with monitored by a pressure transducer (MP100, PowerLab, ventilation at a stable rate, during which time systolic BP ADInstruments, Castle Hill, Australia) placed under the remained higher than 80 mm Hg and a stable anesthetic chest to measure chest excursion. In trials involving plane was maintained. Twelve trials were performed with positive-pressure mechanical ventilation (see later), animals spontaneous breathing and 14 trials were performed in were ventilated at rates of between 65 and 100 breaths per animals that were mechanically ventilated (see above) at minute using a small animal ventilator (Small Animal rates of between 65 and 100 breaths per minute. Hence, in Ventilator Model 683, Harvard Apparatus, South Natick, all animals, recordings were obtained during both sponta- Mass) with a spirometer (MLT1L Spirometer, ADInstru- neous and mechanical ventilation, and in some animals, it ments) placed in series with the ventilator to monitor was possible to obtain records during more than 1 rate of ventilatory flow. No paralyzing agent was used in these mechanical ventilation. Four-minute blocks of data were experiments. This allowed some animals, which remained in recorded for analysis of power spectra to capture a minimum Journal of Manipulative and Physiological Therapeutics Budgell and Bolton 353 Volume 30, Number 5 CSF Pressure

of 260 respiratory cycles even at the slowest rate of mechanical ventilation. Power spectra were generated using 64K or 128K fast Fourier transforms with a Hamming window (Chart ver 4.1.1, ADInstruments). Data were analyzed as follows: peak frequencies in CSF pressure, revealed by power spectrum analysis, were examined for correlation with peak frequencies in the power spectra of the respiratory and cardiac cycles, thus including, but not limited to, the mean respiratory rate and mean heart rate. Furthermore, simultaneous recordings of CSF pressure waves and either chest excursion or BP were averaged (n = 500 ventilatory or cardiac cycles) using commercial soft- ware (Scope ver 3.0, ADInstruments) to determine the phase relationship between these waves. In 6 of 8 animals, after paced respiration, the upper cervical vertebrae were exposed, a 26-gauge needle was introduced into the subarachnoid space at the occiput-C1 level, and the entry site was then sealed with surgical adhesive (Quick Fix, Shelley’s). Discrete volumes (range, 0.05-0.31 mL) of aCSF were introduced at the occipital-C1 level while concurrently measuring the lumbar CSF pressure. The purpose of this protocol was to confirm that pressure changes at the upper cervical level were detectable via the lumbar catheter. In 3 rats, at the conclusion of the experiment, blue food dye was mixed (1% Solution) with aCSF and injected (typically 0.25 mL) at the occipital-C1 level to determine if the lumbar cannular was placed in the subarachnoid space. Fig 1. Power spectra of simultaneously recorded 4-minute epochs of CSF pressure (A), BP (B), and chest excursion (C) in a RESULTS spontaneously breathing anesthetized rat. The insets, top right of each panel, show 8-second epochs of raw data for the CSF In all 6 of 8 animals tested, injection of small volumes of pressure, BP, and chest excursion, respectively. The dashed line aCSF into the cisterna magna resulted in essentially marks the time of peak inspiration. The principal peaks in the CSF instantaneous increases in CSF pressure measured at the pressure spectrum occur at 0.122 and 1.251 Hz. Principal peaks in lumbar level, indicating that the lumbar catheter was patent. the BP spectrum occur at 1.251 Hz (average instantaneous In all 3 rats in which dye was injected into the cisterna respiratory rate) and 6.042 Hz (average instantaneous heart rate). The larger CSF power spectrum peak (A) clearly coincides with magna, dye was found to track in the subarachnoid space at the larger peak power spectrum of chest excursion (C). There is the level of the lumbar cannula and could be aspirated with also a second (harmonic) peak at 2.5 Hz in the spectral analysis the lumbar catheter, demonstrating that the catheter was chest excursion (C). In this animal, the CSF peak at 0.122 Hz (A) within the subarachnoid space. correlated with a very small peak in the BP power spectrum, which cannot be discerned in this figure.

Frequencies of CSF Pressure Oscillations At the commencement of data collection, the mean Powers of CSF Pressure Oscillations (FSD) CSF pressure for all spontaneously breathing rats The CSF power spectra were reanalyzed with 8K fast (n = 8) was 4.18 F 2.49 mm Hg. All 8 rats exhibited Fourier transforms, effectively creating bins of 0.25 Hz in pressure waves in the CSF (Fig 1A, inset). The power width. This second analysis, using a broader bin width, does spectra of CSF pressure, in both spontaneously ventilating not allow as precise an identification of peak frequency, but and mechanically ventilated rats, showed peaks within pools power over the bin width for a more efficient 3 frequency ranges: 0.006 to 0.24 Hz (7/8 rats—in 9 of comparison of powers within the ranges sampled. In 25 of 12 trials with spontaneous breathing, and 12 of 14 trials with 26 trials, the largest peak in the power spectrum of CSF mechanical ventilation); 0.98 to 1.95 Hz (8/8 rats); 5.37 to pressure was that peak within the frequency range of 0.98 to 8.06 Hz (8/8 rats) (Fig 1A). The mean (FSD) of the peaks 1.95 Hz. The powers of the 3 peaks in each CSF pressure in each of the frequency ranges, for all rats, was 0.18 F spectrum were normalized to the power of the major peak in 0.07, 1.53 F 0.36, and 6.99 F 0.08 Hz, respectively. the 0.98 to 1.95 Hz range. Within the same trials, the peaks 354 Budgell and Bolton Journal of Manipulative and Physiological Therapeutics CSF Pressure June 2007

Fig 3. Frequency of the most powerful oscillation in the CSF pressure (CSF) plotted against the frequency of ventilation (Resp) of both spontaneous and mechanically ventilated rats (26 trials in 8 rats; some data points overlap) in this study. The blinearQ regression line (solid line) and 95% confidence intervals (dashed lines) have been plotted. The blinearQ correlation (coefficient of determination = r2) was 0.271.

range of 1.068 to 1.648 Hz. The BP power spectra Fig 2. This figure shows averaged records (n = 500) of chest invariably included more bnoiseQ than the EKG power excursion (upper panel) and CSF pressure (lower panel) over 2 spectra, and the major peaks in the BP power spectra were cycles of spontaneous breathing (A) and mechanical ventilation relatively wide compared to the coincident peaks in the (93 breaths/min) (B). Averages (n = 500) of BP (upper panel) and CSF pressure (lower panel) are shown during spontaneous EKG spectra because of this noise. In 21 of 26 trials, it was breathing (C). These data are from the same animal and clearly possible to resolve a relatively small, low frequency peak show that CSF pressure waves are entrained to ventilatory below 0.25 Hz in the EKG power spectra. movement. With spontaneous ventilation the peak pressure in The power spectra of chest excursion invariably revealed CSF occurs at peak expiration (Exp), whereas minimum pressure a single major peak within the range of 1.076 to 1.648 Hz, occurs at peak inspiration (Insp) (A). Note that the phase of CSF pressure shifts 1808 with mechanical ventilation (B) and is greatest with minor peaks at successive, higher harmonic frequen- with positive pressure ventilation (+ve) and least with negative cies (Fig 1C). There were no lower frequency peaks in the (Àve) pressure ventilation. There was no apparent entrainment of chest excursion records in any spontaneously breathing or CSF pressure (lower panel) with BP (upper panel) in this rat (C). mechanically ventilated animals. In mechanically ventilated animals the frequencies of the major peaks in the power spectra of chest excursion were, within the limits of in the power spectra of CSF pressure within the 5.37 to 8.06 accuracy of the equipment, coincident with the major peaks Hz range had less than 1% of the power of the peaks in the in the power spectra of the spirometer and reflected the rate 0.98 to 1.95 Hz range. Similarly, in 21 of 26 trials, the low of ventilation set by the ventilator. frequency peak (below 0.25 Hz) in CSF pressure had a In 22 trials collected from 6 animals, simultaneous power of less than 8% of the power of the major peak in the recordings of chest excursion and CSF pressure, averaged 0.98 to 1.95 Hz range. In the remaining 3 trials, the powers more than 500 respiratory cycles, showed that CSF pressure of these low frequency peaks (below 0.25 Hz) were 27%, was phase-locked to chest excursion (Fig 2). In sponta- 37%, and 285% of the power of the major peak in the 0.98 neously ventilating animals, CSF pressure and intrathoracic to 1.95 Hz range. pressure were in phase, with the maximum CSF pressure coincident at the peak of expiration. In mechanically Entrainment of CSF Pressure Oscillations to Cardiac and Respiratory Cycles ventilated animals, however, CSF pressure peaked at the Power spectra analysis of the EKG and BP demonstrated point of maximal chest expansion. In both spontaneous and coincident major peaks within the frequency ranges of 5.402 mechanically ventilated rats the frequency of the most to 8.392 Hz. Minor peaks also occurred at successive, powerful oscillation in the CSF pressure had a weak blinearQ higher harmonic frequencies (Fig 1B). In 4 animals, there correlation (r2 = 0.27) with rate of ventilation (Fig 3). In was also a small peak in the BP power spectra within the 9 trials in 5 animals, simultaneous recordings of BP and Journal of Manipulative and Physiological Therapeutics Budgell and Bolton 355 Volume 30, Number 5 CSF Pressure

CSF pressure failed to demonstrate any phase locking of was at or very close to the major peak in the power spectrum these pressure waves. of chest excursion (Fig 1). In 25 of 26 trials, this was far and away the most powerful peak in the CSF spectrum. In mechanically ventilated animals, this major CSF power DISCUSSION spectrum peak was perfectly coincident with the rate of Kusaka et al8 had reported rhythmic variations in lumbar ventilation as determined from power spectrum analysis of CSF pressure in anesthetized rats that they took to be the spirometer placed in series with the tracheal cannula. entrained to the respiratory cycle. Furthermore, Barth et al13 Hence, in both spontaneously ventilating and mechanically reported variations in CSF pressure, measured at the cisterna ventilated animals oscillations in CSF pressure were magna, which they took to be coincident with respiration entrained to ventilation. This was confirmed by averaging and the cardiac cycle. In neither instance, however, were of simultaneous recordings that showed phase-locked waves quantitative data reported and there was no attempt to in CSF pressure and chest excursion. Furthermore, with determine CSF pressure oscillation frequencies. Similar positive-pressure mechanical ventilation, wherein maximum rhythmic oscillations in CSF pressure have also been intrathoracic pressure occurs at the peak of chest excursion, reported in other species.14,15 the phase of entrainment shifted 1808. This strongly In addition to rhythmic oscillations in CSF pressure, suggests that not only are CSF pressure oscillations strongly apparently coincident with the cardiac and respiratory entrained to ventilation, but that they are also driven by cycles, there are numerous reports of low-frequency intrathoracic pressure changes. oscillations, the B waves or Lundberg waves, in humans. In 22 of 26 trials, the power spectra of CSF pressure also These waves have been identified in patients with intra- displayed a small peak, between 5.37 and 8.06 Hz, which cranial pathology, and have been attributed to the low- was at or very close to the major peak of the cardiac cycle, frequency oscillations in respiratory rate that characterize and so reflected an association with heart rate. The power of brain injury.16,17 However, these waves have also been this peak in the CSF pressure power spectrum was described in artificially ventilated patients and in healthy invariably less than 1% of the power of the major peak, volunteers, and so cannot be causally attributed solely to between 0.98 and 1.95 Hz, which was coincident with the pathologic respiratory rhythms.17,18 ventilatory rate. Others have reported oscillations in CSF Because of the superimposition of nonharmonic rhythms, pressure that appeared to be entrained to the cardiac cycle.14 including those associated with the respiratory and cardiac However, our results suggest that in anesthetized rats the cycles, any given oscillation in intracranial pressure is likely arterial pulse exerts only a very minor influence over to have a complex waveform,19 and it may be difficult to oscillations in CSF pressure at the lumbar level. recognize component CSF pressure waves without mathe- In 21 of 26 trials, it was also possible to resolve a low- matical processing of the raw signal (see, eg,20,21). Hence, frequency oscillation, between 0.006 and 0.24 Hz, in CSF in this study, we used power spectrum analysis to search for pressure. This peak occurred in both spontaneously breath- component waves within the CSF oscillations. We partic- ing rats and in rats mechanically ventilated at a fixed rate. ularly sought entrainment to the cardiac and respiratory This oscillation did not correspond to any detectable peak in cycles, but also searched at lower frequencies for phenom- the power spectra of the ventilatory cycle. Rather, it was ena such as Lundberg waves. In this regard, we note that in entrained to a low-frequency oscillation in the power spectra human beings and other animals, low-frequency oscillations of the EKG. in BP, sometimes called Mayer waves, have been identified and attributed to an intrinsic slow rhythm in sympathetic output.22 In humans, Mayer waves have a duration in the CONCLUSION order of 10 seconds. No coincident oscillation has pre- The results of this study suggest that, in the anesthetized viously been reported in CSF pressure. However, if Mayer rat, oscillations in CSF pressure are most strongly entrained waves were to entrain oscillations in CSF pressure, the to the ventilatory cycle and are driven by intrathoracic effect in humans should be distinguishable from B waves, pressure. The major frequency of the cardiac cycle (heart which have wavelengths of 0.5 to 2 minutes. Furthermore, if rate) contributes little power to oscillations in CSF pressure, B waves are attributable to oscillations in the respiratory suggesting that arterial pulse pressure has only a weak rhythm,16 they should be effaced by paced respiration, influence on oscillations in CSF pressure at the lumbar whereas Mayer waves should be relatively unaffected. level. On the other hand, in some animals oscillations in In the current study, 3 peaks were consistently found in CSF pressure are entrained to a low-frequency oscillation in the CSF pressure power spectrum, suggesting that pressure the cardiac cycle, and in a small minority of animals this oscillations at 3 different frequencies were present. In both rivals the influence of the ventilatory cycle. spontaneously ventilating and mechanically ventilated Changes in CSF pressure induced by injections of small animals, the power spectrum of CSF pressure invariably volumes of aCSF at the cisterna magna were immediately displayed a major peak, between 0.98 and 1.95 Hz, which detectable at the lumbar level, suggesting that this model 356 Budgell and Bolton Journal of Manipulative and Physiological Therapeutics CSF Pressure June 2007

may be useful in studies of the effects of vertebral position nervous system—part II: spinal cord strains from postural and motion on CSF fluid dynamics. However, the signal loads. J Manipulative Physiol Ther 1999;22:322-32. 5. Harrison DE, Cailliet R, Harrison DD, Troyanovich SJ, from CSF pressure at the lumbar level is complex, involving Harrison SO. A review of biomechanics of the central nervous at least 3 nonharmonic waves. Consequently, although system—part III: spinal cord stresses from postural loads and pressure changes may be transmitted from the upper cervical their neurologic effects. J Manipulative Physiol Ther 1999;22: region to the lumbar subarachnoid space, a single pressure 399-410. pulse might be obscured by background noise. On the other 6. Moran R, Gibbons P. Intraexaminer and interexaminer reliability for palpation of the cranial rhythmic impulse at hand, sustained changes in CSF dynamics and manifesting the head and sacrum. J Manipulative Physiol Ther 2001;24: as a shift in the frequency or power of a component 183-90. oscillation may well be detectable by power spectrum 7. Hartman S. Cranial osteopathy: its fate seems clear. Chiropr analysis even if not evident on cursory inspection of the raw Osteopat 2006;14:10. CSF pressure signal. 8. Kusaka G, Calvert JW, Smelley C, Nanda A, Zhang JH. New lumbar method for monitoring cerebrospinal fluid pressure in This study has quantified the frequencies and relative rats. J Neurosci Methods 2004;135:121-7. strengths (powers) of oscillations in the lumbar CSF 9. Klarica M, Rados M, Draganic P, Erceg G, Oreskovic D, pressure in the anesthetized rat and identified a clear Marakovic J, et al. Effect of head position on cerebrospinal association with the ventilatory cycle. It has also identified fluid pressure in cats: comparison with artificial model. Croat constraints in the measurement and interpretation of lumbar Med J 2006;47:233-8. 10. Cramer GD, Fournier JT, Henderson CNR, Wolcott CC. CSF pressure in the rat that need to be considered when Degenerative changes following spinal fixation in a small investigating the effects of vertebral displacements and animal model. J Manipulative Physiol Ther 2004;27:141-54. manipulations on CSF pressure dynamics. 11. Pickar J, Wheeler J. Response of muscle proprioceptors to spinal manipulative-like loads in the anesthetized cat. J Manipulative Physiol Ther 2001;24:2-11. Practical Applications 12. McNay EC, Gold PE. Extracellular glucose concentrations in the rat hippocampus measured by zero-net-flux: effects of microdialysis flow rate, strain and age. J Neurochem 1999;72: ! CSF pressure in rats fluctuates in a deterministic 785-90. fashion. 13. Barth K, Onesti S, Krauss W, Solomon R. A simple and ! In the anesthetized rat, CSF pressure fluctuation reliable technique to monitor intracranial pressure in the rat. involves superimposition of oscillations at 3 or Neurosurgery 1992;30:138-40. 14. Hamer J, Alberti E, Hoyer S, Wiedemann K. Influence of more distinct frequencies. systemic and cerebral vascular factors on the cerebrospinal ! Most often, the most powerful influence on CSF fluid pulse waves. J Neurosurg 1977;46:36-45. pressure oscillation is ventilation. CSF pressure 15. Shapiro K, Fried A, Takei F, Kohn I. Effect of the skull and waves are entrained to and driven by the respira- dura on neural axis pressure-volume relationships and CSF tory cycle. hydrodynamics. J Neurosurg 1985;63:76-81. ! 16. Steinmeier R, Bauhuf C, Hubner U, et al. Slow rhythmic Most often, a less powerful influence on CSF oscillations of blood pressure, intracranial pressure, micro- pressure is a low-frequency oscillation in the circulation, and cerebral oxygenation. Stroke 1996;27: cardiac cycle. 2236-43. ! The arterial pulse wave has only a minor influence 17. Lescot T, Naccache L, Bonnet MP, Abdennour L, Coriat P, on the oscillation of CSF pressure. Puybasset L. The relationship of intracranial pressure Lund- berg waves to electroencephalograph fluctuations in patients with severe head trauma. Acta Neurochir 2005;147:125-9. 18. Friese S, Hamhaber U, Erb M, Klose U. B-waves in cerebral and spinal cerebrospinal fluid pulsation; measurement by ACKNOWLEDGMENT magnetic resonance imaging. J Comput Assist Tomogr 2004; This work was supported by grant LG 2005-5 from the 28:255-62. Australian Spinal Research Foundation. 19. Morgalla MH, Stumm F, Hesse G. A computer-based method for continuous single pulse analysis of intracranial pressure waves. J Neurol Sci 1999;168:90-5. 20. Czosnyka M, Pickard J. Monitoring and interpretation of REFERENCES intracranial pressure. J Neurol Neurosurg Psychiatry 2004;75: 1. Richards DM. The Palmer philosophy of chiropractic—an 813-21. historical perspective. Chiropr J Aust 1991;21:63-8. 21. Stephensen H, Andersson N, Eklund A, Malm J, Tisell M, 2. Bolton SP. The bwet specimenQ. Chiropr J Aust 1994;24: Wikkelso C. Objective B wave analysis in 55 patients 147-50. with non-communicating and communicating hydrocephalus. 3. Pederick FO. Cranial adjusting—an overview. Chiropr J Aust J Neurol Neurosurg Psychiatry 2004;76:965-70. 1993;23:106-12. 22. Montano N, Cogliati C, da Silva VJD, Gnecchi-Ruscone T, 4. Harrison DE, Cailliet R, Harrison DD, Troyanovich SJ, Malliani A. Sympathetic rhythms and cardiovascular oscilla- Harrison SO. A review of the biomechanics of the central tions. Auton Neurosci 2001;90:29-34. MUSCULAR AND POSTURAL DEMANDS OF USING A MASSAGE CHAIR AND MASSAGE TABLE

Fearon A. Buck, BSc,a Usha Kuruganti, PhD,b Wayne J. Albert, PhD,c Melanie Babineau, BSc,d Sarah Orser,d and Nadine Currie-Jackson, BSce

ABSTRACT

Objective: The aim of this study was to determine the difference in muscular and postural demands of performing manual therapy using a massage chair and a massage table. Methods: Twelve female senior massage therapy students performed two 10-minute regional back massages on a fully clothed client using both a massage chair and massage table. The root mean square was used to determine the mean activation from the electromyographic signal collected from 8 upper extremity muscles. Integrated electromyography was used to compare activation between the 14 massage techniques used. Eight electromagnetic motion capture sensors were attached: the head, trunk, and upper arm, forearm, and hand bilaterally to track segment kinematics and determine total time spent in different postures. Results: There was higher activation in lumbar erector spinae when using the table and anterior deltoid when using the chair. The anterior deltoid showed a significant condition  period interaction for mean muscle activation for 6 of the 14 massage techniques. The therapists spent significantly more time in mild trunk flexion when using the massage table and significantly more time in severe radial deviation and mild shoulder flexion when using the massage chair. Conclusions: The chair and table were more demanding of the anterior deltoid and lumbar erector spinae, respectively. Therapists adopted trunk and wrist postures that would increase the risk of upper extremity injury while using either the massage chair or table. (J Manipulative Physiol Ther 2007;30:357-364) Key Indexing Terms: Massage Therapy; Massage Chair; Massage Table; Physical Therapy Modalities; Posture; Muscle Activity; Ergonomics

he physically demanding nature of many health professionals. Studies investigating nurses,1-3 physiothera- care jobs has revealed an increasing prevalence in pists,4 dentists,5,6 and chiropractors7 have all shown high Tmusculoskeletal injuries among many health care prevalence of low back injury. Studies addressing the musculoskeletal injuries of chiropractors, for example, found that the back, neck, and wrist were the most at risk for injury.7 Unlike the musculoskeletal demands a Graduate Student, Human Performance Lab, Faculty of Kinesiology, University of New Brunswick, Fredericton, NB, associated with patient handling in the nursing profession, Canada. the risk of injury in the dental and chiropractic professions b Assistant Professor, Human Performance Lab, Faculty of is associated with postural demands and static muscle Kinesiology, University of New Brunswick, Fredericton, NB, activity.5,8 Previous research investigating these profes- Canada. 5,9 c sions propose that poor sitting posture, workstation Associate Professor, Human Performance Lab, Faculty of 10 5,11 Kinesiology, University of New Brunswick, 2 Peter Kelly Dr. design, long periods of static trunk and neck flexion, Fredericton, NB Canada. excessive trunk twisting, unnatural static postures, and d Senior Student, Atlantic College of Therapeutic Massage, high compressive and shearing forces on the spine11 are Fredericton, NB, Canada. also major contributors to low back pain and other e President and Instructor, Atlantic College of Therapeutic musculoskeletal disorders (MSDs). For example, Mior Massage, Fredericton, NB, Canada. 8 Submit requests for reprints to: Wayne J. Albert, PhD, Associate and Diakow reported that 41% of chiropractors in their Professor, Human Performance Lab, Faculty of Kinesiology, study felt the postural demands created by treatment University of New Brunswick, 2 Peter Kelly Dr. Fredericton, techniques and patient positioning were key factors in NB, Canada E3B 5A3 (e-mail:[email protected]). their development of low back pain. Paper submitted September 12, 2006; in revised form To date, the physical demands on massage therapists January 22, 2007; accepted March 25, 2007. 0161-4754/$32.00 have received little attention in the research literature. Copyright D 2007 by National University of Health Sciences. Rather, research has focused on providing empirical evi- doi:10.1016/j.jmpt.2007.04.003 dence for the benefits of massage therapy as a treatment.12,13

357 358 Buck et al Journal of Manipulative and Physiological Therapeutics Ergonomic Assessment of Massage Therapy June 2007

Fig 1. Setup for study of massage done on a massage chair (A) and massage table (B).

Similar to chiropractic and osteopathy, the massage that as workstation table height was changed, sagittal therapist uses his or her body as the tool to provide flexion, disk compression force, and ligament strain changed treatment to the client. While treating clients, therapists use significantly. Low table height put the most strain on the low their own musculature to apply sufficient pressure and back, regardless of the task being performed. For cervical repetitive movements, increasing their susceptibility to manipulation, high table height put the least amount of stress repetitive strain injuries. on the low back, and medium table height was best for Our research group recently completed a survey of lumbar and thoracic manipulation.10 Newell and Kumar5 massage therapists from across Canada.14 Most therapists found that an instantaneous load measured for jobs with (68%) indicated working 10 to 30 hours per week. They also smaller loads does not give an accurate picture of the job’s indicated using moderate or deep pressure 44% and 49% of cumulative stress. Static postures and smaller loads experi- the time, respectively, during their treatments. Of the 507 enced by orthodontists over the course of the day could still therapists who responded, 65% reported low back pain, be a risk factor for low back pain because tissues do not have 62% with shoulder pain, and 83% with wrist and thumb a chance to repair themselves. The cumulative stress pain directly related to working. Of those with shoulder experienced by massage therapists may also be a factor pain, 25% now use a massage aid to prevent injury or related to reports of pain. Our research group found that the reinjury. Aids are also used by 31% of those reporting wrist daily cumulative back loads experienced by massage and thumb pain and 33% of those reporting back pain. therapists conducting five 45-minute therapeutic massages Threshold limits have been established for peak spinal in a day16 equaled that of values reported for automotive loading, but many jobs, including massage therapy, would be assembly line workers.17 deemed dsafeT because they do not exceed those limits. More In addition to the biomechanical variables that must be recently, cumulative loading has been recognized as a risk considered, there has been little work that has observed factor for low back pain, taking into account loading over a the neuromuscular function of the muscles involved period and also its effect on other parts of the worker’s during the massage. One method to observe neuro- body.5,15 A study of chiropractors’ low back loading found muscular function is through the use of surface electrodes Journal of Manipulative and Physiological Therapeutics Buck et al 359 Volume 30, Number 5 Ergonomic Assessment of Massage Therapy

Table 1. Massage protocol

Time (min) Quadrant Techniquea Direction

1.0 1 and 2 Muscle squeezes (upper traps) N/A 1.0 1 Fingertip kneading (around scapula) Medial to lateral (moving superiorly) 1.0 2 Fingertip kneading (around scapula) Medial to lateral (moving superiorly) 0.5 All Deep effleurage to entire back Inferior to superior 1.0 3 Palmar kneads (lumbar erectors) Inferior to superior 1.0 3 Thumb kneads (sacral area) Medial to lateral 1.0 4 Palmar kneads (lumbar erectors) Inferior to superior 1.0 4 Thumb kneads (sacral area) Medial to lateral 0.5 All Deep effleurage to entire back Inferior to superior 1.0 1 Muscle stripping (mid traps) Medial to lateral (and return) 1.0 2 Muscle stripping (mid traps) Medial to lateral (and return) 1.0 3 Palmar kneads (lumbar area) Medial to lateral (moving superior to inferior) 1.0 4 Palmar kneads (lumbar area) Medial to lateral (moving superior to inferior) 0.5 All Bilateral compressions Superior to inferior The time for each technique is an approximate time. A diagram of the quadrants is provided in Figure 1. The technique column describes the techniques being used as well as the specific area within the quadrant to be massaged. a The techniques are defined as follows: (1) compressions: a force oriented in a manner to shorten or compact a tissue; (2) effleurage: a group of general guiding manipulations performed with centripetal pressure and varying pressures; (3) kneading: a gliding neuromuscular technique, performed in circles or ellipses, which repeatedly compresses and releases muscle; (4) muscle stripping: a slow, specific, gliding neuromuscular technique that is applied from the origin of the muscle to its insertion for the purpose of reducing the activity of trigger points.29 to record myoelectric signals (MES) from contracting METHODS muscles. The MES measure the result of the neural Participants commands sent to the muscle and provide evidence of the Twelve senior female massage therapy students from the neural mechanisms responsible for the deficit including Atlantic College of Therapeutic Massage (New Brunswick, agonist/antagonist cocontraction. The amplitude of the Canada) volunteered for the study. All participants were MES depends on the muscle fiber membrane properties as right-handed and had a mean age of 22.8 years (SD, well as the timing of the motor unit action potentials and 3.7 years; range, 18-32 years), mean height of 164.6 cm therefore reflects both peripheral and central properties of (SD, 5.6 cm), and mean weight of 74.2 kg (SD, 18.2 kg). As the neuromuscular system.18 The surface MES has been part of the practicum experience for the students, the college used successfully to provide information regarding muscle subscribes to a corporate massage program in the commun- activity, the relative timing of muscles during a move- ity, and therefore all participants had training and experience ment, and to assess antagonist muscle coactivation and in performing on-site massages. All participants gave muscle cocontraction during various movements. This informed consent before beginning the study, which was allows investigators to determine which muscles are used approved by the university’s research ethics board. during a movement and can provide valuable information regarding muscle function. Traditionally, a massage therapy treatment for medical Protocol and rehabilitative therapy, relaxation, or stress relief is Each massage therapist was asked to perform separate conducted in a private clinic, spa, or a private home. More 10-minute on-site massages on a bclientQ using a massage recently, there is increasing support for massage in the chair and massage table (Fig 1A and B). The order of workplace as a means of stress relief that can be adapted to condition (table and chair) was randomized. Each massage address individual complaints, such as low back pain. To therapist had a 5-minute break between massages while the accomplish this on-site massage, the therapist must bring condition was switched. The massage table was adjusted to the massage therapy clinic to the client, which has led to the proper height for each therapist, and the massage chair the increase use of a massage chair in lieu of the was adjusted for both the proper height for the therapist and traditional massage table. The massage table is still the the comfort of the client. The therapists applied 14 different most common piece of equipment used in Canada, but techniques in a sequence of 14 set periods, with each one chairs may be favored when the therapist is traveling to being either 30 or 60 seconds long. Instructions of the different locations. massage protocol were provided on an audio tape to cue the The purpose of this study was to determine the difference therapist to the details of the next period (ie, the technique to in muscular and postural demands of performing an on-site be used, the duration of the technique, the area of the back (corporate) massage to a client in a massage chair and a [quadrants] to be massaged, and direction of the technique massage table. motion) (Table 1). A sign was posted in the massage area as 360 Buck et al Journal of Manipulative and Physiological Therapeutics Ergonomic Assessment of Massage Therapy June 2007

50% between the medial border of the scapula and the spine, at the level of T3. The lumbar erector spinae was measured with electrodes at 2 finger width lateral from the L1 spinous process. For the lateral triceps, electrodes were placed at 50% on the line between the posterior crista of the acromion and the olecranon at 2 finger widths lateral to the line. Electrodes were also placed over the flexor and extensor carpi radialis. The ground electrode was placed on the boniest part of the acromion. The electrodes were not moved during the entire testing session. Myoelectric signals were collected for the entire massage with markers placed at the beginning of each technique change (period). The amplitude of the MES was quantified using the root- mean-square calculation. Because the MES was collected during dynamic con- tractions, it is possible that if the data were collected at a later date, the activity pattern could change. However, the purpose of this study was to examine which muscles were active during the massage and if there were differences between the 2 techniques (chair vs table). The system used to collect the data weighs approximately 1 lb, and no subject indicated that the equipment inhibited them. The therapist’s posture was tracked using electromag- netic motion tracking system (Fastrak, Polhemus Inc, Fig 2. Quadrants of the back massaged in the study. Vermont), which recorded the 3-dimensional position of electromagnetic sensors placed on the center of gravity of a reminder of the 4 quadrants (Fig 2). The techniques the body segment of interest. The Fastrak uses a low- chosen were to replicate the fundamental modalities used frequency magnetic field to determine 3 rectangular during a relaxation massage over fully clothed client most coordinates (x, y, z) and 3 angular coordinates (azimuth, commonly used in an on-site setting. The 10-minute period elevation, and roll) of each sensor in relation to a fixed also reflects a typical on-site massage session. source. The Fastrak motion analysis system has been used extensively in kinesiological studies to investigate lumbar motions,20,21 shoulder girdle motions,22,23 and numerous Data Collection occupational biomechanics studies to model the entire body The MES data were recorded using a wireless tele- during lifting activities.24,25 Electromagnetic device posi- metered electromyography (EMG) (Noraxon, City, State, tions and angular errors have been reported as less than USA) system sampled at 1500 samples per second. Eight 1.8 cm and 1.28, respectively.26 channels of MES were collected, right side only, from the The motion of the following upper extremity segments anterior deltoid, posterior deltoid, upper trapezius, middle was recorded: neck, trunk, right and left upper arm, right trapezius, lumbar erector spinae, lateral triceps, flexor carpi and left forearm, and right and left wrist. To obtain head radialis, and extensor carpi radialis. Bipolar surface posture, the sensor was attached to an elastic headband electrodes (Duotrode silver-silver chloride electrodes, and placed so that the sensor was at the same level as the Myo-tronics, Inc, Kent, WA; interelectrode spacing = ear. The sensor on the trunk was secured using a heart rate 21.0 F 1 mm) were placed over the muscle belly monitor strap and surgical tape (when needed). With the according to the Surface ElectroMyoGraphy for the Non- therapist standing in anatomical position, the remaining Invasive Assessment of Muscles group.19 The skin surface sensors were placed using double-sided tape. The sensors was prepared using alcohol swabs, light abrasion, and a used for wrist posture were placed directly proximal to the very thin layer of ultrasound gel to increase conductivity. third knuckle of each hand using surgical tape with the For the anterior deltoid, the electrodes were place 1 finger wire from the sensor strapped down using a thin Velcro width distal and anterior to the acromion, for the posterior strap proximal to the wrist so as not to obstruct move- deltoid, the electrodes were centered in the area approx- ment. Sensors on the upper arms and forearms were imately 2 fingerbreadths behind the angle of the acromion. strapped down using thick Velcro straps. These straps also For the upper trapezius, the electrodes were placed at 50% stabilized the wires running up the arm from the distal on the line from the acromion to the spine on vertebra C7. sensors. All wires were grouped together behind the For the middle trapezius, the electrodes were placed at therapist and taped together to allow them to move freely Journal of Manipulative and Physiological Therapeutics Buck et al 361 Volume 30, Number 5 Ergonomic Assessment of Massage Therapy

throughout the massage. This was less of an issue during the chair massage but was important during the table massage where the therapist needed to move freely around the table. Due to the dynamic nature of the collection and the required processing time required to save the Fastrak data, collection occurred for half of each technique period in order for the collection system to be ready to collect the next period.

Data Analysis Root mean square was used to calculate the amplitude of the signal to obtain the average activation of the muscles during each movement (period) over the entire massage and used to compare the muscle activation between conditions. Custom software was developed to analyze the posture data using Matlab 6.1 (The MathWorks, Inc). Because the posture data were captured for half of the technique time, it was first extrapolated to the full length to determine the amount of time the participant spent in specific postures. The postures for each segment were sorted into neutral, Fig 3. The mean activation for all technique periods for a) anterior mild, and severe based on the work by Punnett et al,27,28 deltoid and b) erector spinae (the two muscles where signifi- who developed odds ratios for developing musculoskeletal cant differences between conditions occured) for each subject in injury as a function of percent time spent in mild and both conditions. severe postures. The segment angles associated with each posture category are as follows: (1) neck flexion—neutral (08-108), mild (118-308), severe (N308); (2) neck exten- RESULTS N sion—neutral (08-108), severe ( 118); (3) trunk flexion— Electromyography N neutral (08-158), mild (168-458), severe ( 468); (4) trunk Mean activation of each muscle by technique period for N extension—mild (08-158), severe ( 158); (5) shoulder both conditions is presented in Figures 3 and 4. The effect flexion—neutral (08-208), mild (218-458), moderate size was 0.256 for condition, 0.081 for period, and 0.057 for N (468-908), severe ( 908); (6) shoulder extension—neutral condition  period. Significant differences were found in N (08-208), severe ( 208); (7) shoulder abduction—neutral mean activation between conditions for the anterior deltoid (08-458), mild (468-908), moderate (918-1358), severe ( P b .001) and lumbar erector spinae ( P b .001) shown in N ( 1368); (8) elbow flexion—neutral (08-808), mild (818- Figure 3. No significant differences were found for the other N 1208), severe ( 1218); (10) wrist flexion—neutral (08-158), muscles. There was also a significant condition  period N mild (168-308), severe ( 318); (11) wrist extension—neutral interaction for the anterior deltoid ( P b .001), in which 6 of N (08-258), mild (268-408), severe ( 418); (12) wrist radial the 14 technique periods showed significant differences in N deviation—neutral (08-158), mild (168-208), severe ( 218); muscle activation between conditions (Fig 4). They were (13) wrist ulnar deviation—neutral (08-158), mild (168- muscle squeezes (upper trapezius), palmar kneads (lumbar N 208), severe ( 218). area) in quadrant 3, and palmar kneads (lumbar erectors) and thumb kneads (sacral area) for both quadrants 3 and 4. No significant condition  period interactions were found Statistical Analysis for any other muscles. Analyses were performed using SPSS 10.0 for Windows (SPSS Inc, Chicago, Ill). A multivariate analysis of variance was performed to determine differences in muscle activity Posture by period, condition, and period by condition. The muscle There was a significant condition effect for trunk in mild activation of the 8 muscles was the dependent variable, with flexion, trunk in neutral posture, right hand severe radial period and condition as the fixed factors. A univariate deviation, right hand neutral posture, right shoulder mild general linear model was used to determine significant flexion, and right shoulder in neutral flexion. The effect size differences in mean time spent in postures based on was 0.302 for condition. Therapists spent significantly more condition, with Tukey HSD as the post hoc test. Statistical time in a neutral trunk posture when using the massage chair significance was set at an a level of .05. as compared to the table ( P b .05), 65.6% and 51.5%, 362 Buck et al Journal of Manipulative and Physiological Therapeutics Ergonomic Assessment of Massage Therapy June 2007

The right side was chosen because each therapist was right- handed. It is not believed that the left side would have shown any difference from the right side based on the observation that it was used primarily for stabilization of the right hand during the massage. There were 3 periods where the left hand was not a stabilizer; however, these were bilateral techniques where the right and left side performed the same movements together. Overall, the anterior deltoid for each therapist had higher mean activation when using the chair. With the exception of one therapist, the lumbar erector spinae Fig 4. Mean muscle activation of anterior deltoid pooled for all showed higher mean activation when therapists used the F participants (n = 12), by period for both chair (SD 1297.43 table. The activation differences between conditions are uV*s) and table (SD F 669.50 uV*s). Asterisks (*) denote significance between conditions. related to the therapist’s posture to reach the required area of the back. For instance, more time was spent in trunk flexion when using the table as compared to the chair, respectively. They also spent significantly more time in mild which coincides with the higher lumbar erector spinae trunk flexion when using the massage table ( P b .05), activity. Similarly, the shoulders were in mild flexion when almost half of the massage (47.8%). The right hand was in a using the chair, which corresponds to the higher anterior neutral position 45.5% of the time when using the massage deltoid activation. table, which is significantly more than the 26.6% when The anterior deltoid was the only muscle with a using the chair ( P b .05). When using the massage chair, significant interaction between condition and period. however, 61.2% of the massage was spent with the right During these periods, the muscle activity was 1.5 to 3.5 hand in severe radial deviation, significantly more when times greater during massages conducted with the chair. using the table ( P b .05). Therapists spent significantly Of the 6 periods showing significance, one was muscle more time in neutral right shoulder flexion when using the squeezes to the upper trapezius and the other 5 were palmar table as compared to the chair ( P b .05), 82.3% and 66.7%, and thumb kneads, 4 of which are back-to-back, minute- respectively. The participants’ right shoulder spent signifi- long periods. cantly more time in mild shoulder flexion when using the When performing muscle squeezes, the therapist is chair (29.3%), whereas 16.5% of the massage was spent in squeezing the upper trapezius on both the right and left mild shoulder flexion when using the table ( P b .05). sides simultaneously with the entire hand for the duration of There was a significant condition and period interaction the period. When using the massage chair, the therapist is for the following as revealed by the Tukey HSD post hoc standing behind the client with the elbows flexed and test: left hand severe flexion ( P = .020), left arm mild shoulders only slightly flexed, corresponding to the lower flexion ( P = .013), right hand mild flexion ( P = .001), right mean activation during this period when using the chair. hand mild radial deviation ( P = .009), and right arm mild When using the massage table, the therapist tended to stand flexion ( P = .009). to the side of the client, reaching over the client’s back to squeeze the muscle. The therapist’s elbows were extended, whereas the shoulders were flexed to reach the client’s trapezius on the opposite side. The therapists always stood DISCUSSION on the left side of the client and reached across to the right As expected, the muscular and postural demands of side, signified by the higher activation seen in the anterior conducting on-site massages were found to be dictated by deltoid being tested. the massage technique being performed as well as whether When performing palmar and thumb kneading, the the massage was being conducted while the client sat in the therapist used her palm or thumb, moving it in a circular massage chair or was lying on the massage table. However, motion to knead the muscles of the lumbar and sacral area this is the first time, to the authors’ knowledge, that the of the back, one quadrant at a time. When using the muscular and postural demands of massage therapists have massage table, the therapist was able to use gravity and been reported. The following sections will discuss each their body weight to exert pressure. There was little demand separately. shoulder flexion needed during this technique, leading to lower anterior deltoid activity. When switching to quad- rant 4 (lower back; right side), the therapist would walk Muscular Demands around to the other side of the client to work directly in Only 8 channels were available to collect MES, and as a front of themselves. In contrast, when using the massage result, unilateral placement was deemed most appropriate. chair, the therapists tended to stand in one place for both Journal of Manipulative and Physiological Therapeutics Buck et al 363 Volume 30, Number 5 Ergonomic Assessment of Massage Therapy

quadrants. Gravity would not help the therapist in this data were collected. Although this provided previously case, requiring her to exert more force to get the desired undocumented information regarding which muscles are pressure. Because there was no significant increase from active during this type of activity, we were able to the flexor carpi radialis, extensor carpi radialis, or triceps, distinguish differences in activation; however, a longer-term the increased force seems to come primarily from the study would allow for the investigation of spectral changes anterior deltoid. and the presence of muscular fatigue. Furthermore, this At the moment, it is not possible to conclude on possible study highlights the specific muscles that should be the harm using these findings, based on the lack of literature focus of an investigation of fatigue effects. addressing occupational muscle activity or a suggested To avoid an ordering effect, the typical methodological threshold limit. It is possible, however, that if a muscle does process would be to randomize the order in which the not get sufficient rest (ie, back-to-back periods that have the techniques were performed. The decision was to have the same muscles activated), the therapists may fatigue, leading therapists all perform the same on-site massage protocol as to an increased risk of injury. they were trained, as this would be more realistic in practice. To assess whether the 10-minute massage resulted in muscle fatigue, we would have required a longer collection time to Postural Demands monitor the changes in median frequency; however, given Static and awkward postures are well-accepted risk that the therapists conduct massages for a couple of hours factors related to MSDs and repetitive strain injuries.27,28 each day, it is unlikely that this protocol resulted in In 2000, Punnett et al27 provided odds ratios that related significant muscular fatigue. upper extremity postures to the risk of developing MSDs. For example, the odds ratio for low back concerns was 6.1, when the back was in mild flexion (208-458) for greater than 10% of the time. The odds ratio increased to 8.9, when CONCLUSION severe trunk flexion (N458) is required for as little as 10% of The following conclusions are derived from this the work time.15 Similarly, they report the risk of shoulder preliminary investigation of the muscular and postural injury increases by 1.4 for each 10% increase in work time demands of massage therapists performing a 10-minute spent in severe shoulder abduction (N908).27 Given that the on-site massage. There was significantly more anterior therapists adopted a mild trunk flexion for over 30% and deltoid use during the chair massage and significantly 45% of the time for the chair and table massages, more lumbar muscle activation during the table massage. respectively, it suggests that there is an increased risk the Future studies should examine longer durations of activity therapists could develop low back pain. Although odds (eg, therapists performing several massages in 1 day) to ratios for risk of wrist disorders based on nonneutral examine the impact of fatigue on these muscles. Both the postures have not been reported, we can assume that the chair and table massages resulted in nonneutral trunk greater time spent in nonneutral wrist postures, the greater flexion postures for greater than 30% of the massage the risk of wrist injury. The wrist postures used by the time, which significantly increases the risk of low back therapists, therefore, may lead to wrist injury in the future as injury. The table massages required a significantly longer they are placed in a severe posture for greater than 80% of percentage of time (~50%) in a nonneutral posture and the massage time. consequently a larger injury risk. Both the chair and table massages resulted in severe wrist postures for greater than 80% of the massage time, which places the Limitations wrist at risk of injury. These results suggest that manual This study provides a preliminary investigation to the therapist training needs to include education on good muscular activity associated with performing on-site mas- body posture and muscular fatigue as a means of self-care sages. The study was conducted on massage therapy and injury avoidance. students, and there is a possibility that experienced therapists could have distinctly different patterns of muscle Practical Applications usage and position. However, the students were well practiced in the tested techniques, and being that they are ! Massages performed with client in the chair accustomed to having their postures monitored during required greater anterior deltoid muscular activity. supervised clinics, it is conceivable that they would adopt ! Massages performed with client on the table the most ergonomic postures. required greater erector spinae muscular activity. The collection of MES data from one side of the body ! Chair and table massages required trunk postures only was determined due to limitations in the number of and wrist postures that increase the risk of injury to available channels and because all therapists were right- the massage therapists. handed. In addition, a relatively short period of time of MES 364 Buck et al Journal of Manipulative and Physiological Therapeutics Ergonomic Assessment of Massage Therapy June 2007

REFERENCES 15. Godin CA, Andrews DM, Arnold TA. 3-Dimensional peak and cumulative shoulder loads during non-occupational tasks. 1. Marras WS, Davis KG, Kirking BC, Bertsche PK. A Proceedings at the Association of Canadian Ergonomists comprehensive analysis of low-back disorder risk and Annual Conference; 2004 Oct 19-21; Windsor, Canada. spinal loading during the transferring and repositioning of 16. Albert WJ, Duncan C, Currie-Jackson N, Gaudet V, Callaghan patients using different techniques. Ergonomics 1999;42: JP. Biomechanical assessment of massage therapists. Occup 904-26. Ergon 2006;6:1-11. 2. Schibye B, Hansen F, Hye-Knudsen CT, Essendrop M, 17. Norman RW, Wells RP, Neumann P, et al. A comparison of Bfcher M, Skotte J. Biomechanical analysis of the effect of peak vs. cumulative physical work exposure risk factors for the changing patient-handling technique. Appl Ergon 2003;34: reporting of low back pain in the automotive industry. Clin 115-23. Biomech 1998;13:561-73. 3. Skotte J, Essendrop M, Hansen AF, Schibye B. A dynamic 18. Farina D, Merletti R, Enoka RM. The extraction of neural 3D biomechanical evaluation of the load on the low back strategies from the surface EMG. J Appl Physiol 2004;96: during different patient-handling tasks. J Biomech 2002;35: 1486-95. 1357-66. 19. SENIAM [homepage on the internet]. [cited 2007/01/15] 4. Rugeli D. Low back pain and other work-related musculoske- Available from: http://www.seniam.org. letal problems among physiotherapists. Appl Ergon 2003;34: 20. Adams MA, Dolan P. A technique for quantifying the bending 635-9. moment acting on the lumbar spine in vivo. J Biomech 5. Newell TM, Kumar S. Comparison of instantaneous and 1991;24:117-26. cumulative loads on the low back and neck of orthodontists. 21. McGill SM, Cholewicki J, Peach JP. Methodological consid- Clin Biomech 2005;20:130-7. erations for using inductive sensors (3SPACE ISOTRAK) to 6. Lehto TU, Helenius HY, Alaranta HT. Musculoskeletal monitor 3-D orthopaedic joint motion. Clin Biomech 1997;12: symptoms of dentists assessed by a multidisciplinary approach. 190-4. Community Dent Oral Epidemiol 1991;19:38-44. 22. Culham E, Peat M. Functional anatomy of the shoulder 7. Homack DMJ. Occupational injuries to practicing chiroprac- complex. J Orthop Surg Phys Ther 1993;18:342-50. tors in New York State. J Chiropr Educ 2005;19:117. 23. Albert WJ, Stevenson JM, Dumas GA, Wheeler RW. Effects 8. Mior SA, Diakow PRP. Prevalence of back pain in chiroprac- of shoulder translation on lumbar moment for two dimen- tors. J Manipulative Physiol Ther 1987;10:305-9. sional modeling strategies during lifting. Occup Ergon 1998; 9. Michalak-Turcotte C. Controlling dental hygiene work-related 1:173-87. musculoskeletal disorders: the ergonomic process. J Dent Hyg 24. Stevenson JM, Weber CL, Smith JT, Dumas GA, Albert WJ. A 2000;74:41-8. longitudinal study of the development of low back pain in an 10. Lorne KJ, Naqvi SA. Comparative analysis of low-back industrial population. Spine 2001;26:1370-7. loading on chiropractors using various workstation table 25. Wrigley AT, Albert WJ, Deluzio KJ, Stevenson JM. Differ- heights and performing various tasks. J Manipulative Physiol entiating lifting technique between those who develop low Ther 2003;26:25-33. back pain and those who do not. Clin Biomech 2005;20:254-63. 11. Marras WS, Lavender SA, Leurgans SE, et al. Biomechanical 26. Day JS, Duncan DJ, Dumas GA. Calibration of position and risk factors for occupationally related low back disorders. angular data from a magnetic tracking device. J Biomech Ergonomics 1995;32:377-410. 2000;33:1039-45. 12. Moyer CM, Rounds J, Hannum JW. A meta-analysis of 27. Punnett L, Fine LJ, Keyserling WM, Herrin GD, Chaffin DB. massage therapy research. Psychol Bull 2004;130:3-18. Shoulder disorders and postural stress in automobile assembly 13. Field T, Diego M, Cullen C, Hernandez-Reif M, Sunshine W, work. Scand J Work Environ Health 2000;26:283-91. Douglas S. Fibromyalgia pain and substance p decrease and 28. Punnett L, Fine LJ, Keyserling WM, Herrin GD, Chaffin sleep improves after massage therapy. J Clin Rheumatol 2002; DB. Back disorders and nonneutral trunk postures of 8:72-6. automobile assembly workers. Scand J Work Environ Health 14. Albert WJ, Currie-Jackson N. Musculoskeltal injuries amongst 1991;17:337-46. massage therapists: a cross-Canada survey. Bodywork and 29. Andrake CK, Clifford P. Outcome-based massage. Lippincott Movement Therapies 2007; [in press]. Williams & Wilkins; 2000. MANUAL APPLICATION OF CONTROLLED FORCES TO THORACIC AND LUMBAR SPINE WITH A DEVICE: RATED COMFORT FOR THE RECEIVER’S BACK AND THE APPLIER’S HANDS

Gordon Waddington, PhD,a Gordon Lau, BAppSc (Physiotherapy) (Hons),b and Roger Adams, PhDc

ABSTRACT

Purpose: High volumes of manual therapy work can lead to overuse hand and wrist injuries. This study evaluated hand and back comfort in asymptomatic volunteers during spinal mobilization carried out with an instrumented manual therapy tool. Methods: This crossover design study examined 36 asymptomatic physiotherapy students that were tested in pairs. One participant assumed the role of the simulated therapist and the other the simulated patient, before reversing roles. Posteroanterior mobilization conditions formed by using 2 spinal segments (thoracic/ lumbar), 2 force application methods (hands/device), and 3 grades of mobilization were applied in a random order. After each combination, both participants in each pair rated hand or back comfort, respectively, on a 100-mm visual analogue scale. Data were analyzed by analysis of variance. Results: Rated back comfort was greater for hands than for the device and decreased with greater applied force. When the original hard rubber device tip was changed to one of soft molded rubber, both back and hand comfort improved significantly. Although tool mobilization was still rated as significantly less comfortable than mobilization with hands only, this difference was approximately half the discomfort experienced as the grade of mobilization increased from grade I to grade III. For hand comfort when using the softer device tip, the method of force application was no longer a significant determinant of comfort. Conclusions: The mobilizing tool with a molded rubber tip was acceptably comfortable in use with asymptomatic backs and hands. Further research is indicated in manual therapy settings with therapists who have experienced hand pain. (J Manipulative Physiol Ther 2007;30:365-373) Key Indexing Terms: Manual Therapy; Spinal Manipulation; Hand Injuries; Equipment Design

igh volumes of manual therapy work increase the loskeletal areas.4,7,8 Such injuries can be debilitating and risk of hand and wrist work-related musculoske- can ultimately force some therapists to leave the profession.3 Hletal disorders in physical therapists.1-4 This It has been established that the use of spinal mobilizations problem has been reported to affect up to 25% of therapists has been supported as an appropriate treatment of back in all domains of physical therapy5,6 and as many as 79% of pain.9 As back pain is a common problem in the those working in private practices and specialist muscu- population,10 it is probable that manual therapists are going to be at risk of overuse injury unless effective risk control measures are identified and implemented. a Associate Professor, Physiotherapy, School of Health Sciences, Suggested solutions for preventing overuse injuries in University of Canberra, Canberra, Australia. manual therapists have included ergonomic measures that b Post-Graduate Student, School of Physiotherapy, Faculty of entail taking rest breaks, performing upper limb exercises,11 Health Sciences, University of Sydney, Sydney, Australia. and using manual therapy tools. However, a recent c Senior Lecturer, School of Physiotherapy, Faculty of Health Cochrane Review found only limited evidence to support Sciences, University of Sydney, Sydney, Australia. 12 Submit requests for reprint to Gordon Waddington, PhD, Physi- rest breaks and exercises for injury prevention. Further- otherapy, School of Health Sciences, University of Canberra, more, a research study on 2 manual therapy tools found Canberra, Australia (e-mail: [email protected]). them to be significantly less comfortable for both the Paper submitted November 27, 2006; in revised form February patients’ backs and the therapists’ hands.13 These tools are 2, 2007; accepted February 20, 2007. 0161-4754/$32.00 not currently in use, possibly for this reason but perhaps also Copyright D 2007 by National University of Health Sciences. because the role of touch in manual therapy is unclear; so doi:10.1016/j.jmpt.2007.04.006 the problem of hand and wrist injury remains unaddressed.

365 366 Waddington et al Journal of Manipulative and Physiological Therapeutics Back and Comfort When Using a Mobilizing Device June 2007

Recently, a new manual therapy tool with instantaneous redesigned version of the original mobilizing dynamometer force measurement and an ergonomic handle (MobDyn, and was manufactured by Metron Pty Ltd. In phase 1, this Metron Pty Ltd, Churrum Downs, Victoria, Australia) has version of the mobilizing device maintains the ergonomi- been described.14 Current research suggests this tool is cally designed, molded plastic walking-stick handle and acceptably comfortable for the hands, and use of the readout the circular, hard rubber tip; but the hydraulic force on the tool can almost eliminate the variability of spinal transducer in the original tool (JAMAR handgrip dyna- mobilization forces.15 Potentially, such a tool could provide mometer; JAMAR Technologies, Inc, Horsham, Pa) has a measure of patient progress, as the force that could be been replaced with an electronic force transducer. In phase applied at a symptomatic spine level before pain response, 2, the working tip of the device was changed to one made as well as help the therapist control mobilization forces and of a softer molded rubber with a cupped section in the avoid injury.14-16 However, the size of the prototype center of the tip for the spinous process (Fig 1A). This tool MobDyn was not optimal for use. Accordingly, a new was labeled MobDyn IIb. As no other part of the version of the tool (MobDyn II) has been manufactured. mobilizing dynamometer was changed, the MobDyn IIb First, this tool must be tested to determine if it is acceptably was used in the same way; and it had the same modes and comfortable for backs and hands when applied. Hence, the function as MobDyn II. aim of the current study was to evaluate hand and back Because use of the force readout was not required for the comfort in simulated therapists and patients to establish present study on hand and back comfort, the readout screen whether the tool is suitable for testing in the clinical that was built for testing purposes was located on the side of environment as a hand/wrist injury risk control measure. the device. To use the tool, the therapist placed the device tip on the target vertebrae. By holding the molded handle with one hand and applying overpressure with the other, METHODS downward mobilizing forces were exerted onto the patient’s Participants back (Fig 1B). This version of the tool can be set to display A group of 36 asymptomatic, physiotherapy students (15, the peak force on the LCD screen or to give auditory male; 21, female; mean age, 21.9 years F 2.9 years) feedback when a preset force is reached. volunteered to participate in the study and give hand and An instrumented plinth was used to standardize the back comfort ratings, made on 100 mm visual analogue forces delivered with each grade of spinal mobilization scales (VAS) labeled highly uncomfortable on the left and (Fig 2). The height-adjustable plinth contained 7 load cells highly comfortable on the right. Comfort rating was done to measure forces applied in all directions to an error of 17 both after mobilization by hand and after mobilization using 2%. Only forces in the vertical plane were considered the device. Participants were recruited via advertisements here. As the side-mounted LCD screen on the tool was not posted on notice boards around the Faculty of Health visible when the tool was in use, participants were instructed Science, University of Sydney. All volunteers had passed to use the force meter on the computer monitor to the relevant courses where spinal mobilization was taught. standardize their PA pressures. The grades of mobilization One of the manual therapy techniques taught was a and associated forces were as follows: grade I = 50 N, grade 2-handed posture: the Maitland bpisiform gripQ where the II = 100 N, and grade III = 150 N. These definitions of mobilizing force is applied through the pisiform of the lower forces were obtained from studies concerning posterior 18-22 hand. Participants were excluded if they had experienced anterior forces applied in spinal mobilizations. hand or back pain in the 3 months before the study and were recruited over time as 2 groups, labeled phase 1 and phase 2. The first 18 participants (8, male; 10, female; mean age, Protocol 22.4 years F 3.4 years) who volunteered were allocated to Participants worked in pairs; and in the first half of the phase 1. A second group of 18 asymptomatic, physiotherapy study, one participant was randomly assigned to the role of students (7, male; 11, female; mean age, 21.4 years F the simulated therapist and the other to the role of the 2.3 years) was tested in phase 2. Before commencement, the simulated patient. In the second half of the study, participants read an information sheet and signed informed participants swapped roles and testing was repeated. All consent. Participants worked in pairs and attended one possible combinations of spinal segment (T6 or L3), force testing session lasting for an hour. Conduct of the study was application method (hand mobilization with the pisiform grip23 or tool mobilization with the MobDyn II), and grade approved by the Human Research Ethics Committee, 23 University of Sydney. of mobilization (I, II, or III) were arranged to form 12 mobilization combinations. The dependent variables were rated simulated-therapist hand comfort and rated simulated- Instrumentation patient back comfort. A purpose-built tool, the MobDyn II, was constructed The participant randomized to the role of the simulated for the conduct of this study. The MobDyn II is a therapist practiced using MobDyn II for approximately Journal of Manipulative and Physiological Therapeutics Waddington et al 367 Volume 30, Number 5 Back and Comfort When Using a Mobilizing Device

Fig 2. Instrumented plinth used to control the level of mobilization forces on the spine. Forces measured by the instrumented plinth are displayed in a force meter on the computer monitor.

mobilization combinations were drawn randomly by the investigator, alternating between the spinal levels to allow adequate rest between each set of mobilizations (30 sec- onds). Each mobilization combination was announced, and the plinth was calibrated before the commencement of each mobilization combination to standardize the forces (Fig 2). After each set of mobilizations, both the simulated therapist and the simulated patient reported their hand and back comfort, respectively, on a 100-mm VAS (where 0 mm was highly uncomfortable and 100 mm was highly comfortable). This procedure was repeated until all 12 mobilization combinations had been tested. At this point, the participants reversed roles; and the protocol was repeated until they had individually rated both their hand and back comfort for each Fig 1. A, The MobDyn II device with the circular hard rubber tip mobilization combination. used in phase 1 and the contoured, soft rubber tip used in phase 2 for MobDyn IIb. B, Application of the MobDyn IIb version of the instrumented manual therapy tool. Data Analysis Data on back and hand comfort from the 100-mm VAS were measured with a ruler to the closest millimeter to 10 minutes, as the investigator marked the spinal levels on obtain scores on the comfort continua. Condition mean the exposed back of the simulated patient. The simulated values are presented in Figure 3. To determine the effect of patient then lay prone on the instrumented plinth as spinal segment, force application method, and grade of 368 Waddington et al Journal of Manipulative and Physiological Therapeutics Back and Comfort When Using a Mobilizing Device June 2007

Fig 3. Mean VAS ratings of back comfort and hand comfort for the use of hand in a pisiform grip and use of the MobDyn II and MobDyn IIb versions of the mobilization device, applied to different spinal segments and across 3 grades of mobilization. Error bars represent 1 SEM.

mobilization on back and hand comfort, a 2 Â 2 Â 3 Back Comfort analysis of variance (ANOVA) was used. Post hoc ANOVA According to those receiving the force, the VAS ratings and paired t tests were used to further explore significant from the 18 participants in phase 1 demonstrated a values and generate the 95% CIs. A P b .05 was considered significant difference in back comfort when comparing the to be statistically significant. All collected data were 2 force application methods. The pisiform grip was rated as processed and analyzed using SPSS version 13 for Windows significantly more comfortable than the use of the MobDyn (SPSS Inc, Chicago, Ill). II (mean, 32 mm on the 100-mm VAS; CI 25.2-39.2 mm; P b .001). This difference in comfort was also dependent on the spinal level, where mobilizations in the thoracic region RESULTS were more uncomfortable than those in the lumbar region Phase 1 (mean, 9 mm; CI 2.5-15.1 mm; P = .009). Together, these The mean rating values of simulated-therapist hand results generated a significant interaction between the spinal comfort and simulated-patient back comfort for the different level and the force application method ( P = .039), whereby grades and methods of force application are presented on the the mean difference between pisiform and MobDyn II left side of Figure 3. This information is expressed as mobilization applied to the thoracic spine was 37 mm millimeters on the VAS scale. (CI 27.6-46.4 mm) and that to the lumbar spine was 27 mm Journal of Manipulative and Physiological Therapeutics Waddington et al 369 Volume 30, Number 5 Back and Comfort When Using a Mobilizing Device

(CI 20.5-34.5 mm). Thus, the difference in back comfort Table 1. Difference between the comfort rating mean values at the when using the pisiform vs the MobDyn II was larger on the back and at the hands, with associated P values, showing that the use of a contoured, soft rubber device tip in phase 2 significantly more sensitive thoracic spine than on the lumbar spine. The reduced the amount of difference between pisiform and tool final significant result was expected. Mobilizing force at mobilization in terms of back comfort grade III was more uncomfortable than that at grade I, which was consistent in both spinal segments. Here, the mean Phase 1 Phase 2 P difference between grades I and III was 26 mm (CI 17.3- b Back comfort Thoracic 37.0 17.6 .002 35.6 mm; P .001), suggesting back comfort decreased as Lumbar 27.5 10.8 .001 the grade of mobilization increased. Hand comfort Thoracic 11.5 3.2 .146 Lumbar 14.3 8.4 .375 Hand Comfort In terms of those applying the force, significant values addition, there was no longer an interaction between spinal were only obtained from the force application method and level and the force application method ( P = .053). Although the grade of mobilization. That is, the pisiform grip was the greater difference in thoracic spine comfort still suggests significantly more comfortable than the MobDyn II on the this region remained the more sensitive—mean difference of simulated therapists’ hands (mean, 13 mm on the 100-mm 18 mm in the thoracic (CI 9.8-25.5 mm) vs 11 mm in the VAS; CI 4.7-21.2 mm; P = .004). Like simulated-patient lumbar spine (CI 3.7-17.9 mm)—both mean values obtained back comfort, hand comfort when performing grade III in phase 2 were less than half of those in phase 1. This mobilization was significantly lower than that obtained from difference can be attributed to the use of the softer tip in grade I (mean, 18.8 mm; CI 12.9-24.7 mm; P b .001); MobDyn IIb, as this feature was the only change between hence, the trend of increased discomfort with increased the phases. grades of mobilization also held for hand comfort. Hand Comfort When considering hand comfort, the grade of mobiliza- RESULTS tion was the only variable that remained significantly Phase 2 different in phase 2 (mean, 20 mm; CI 13.5-27.2 mm; P b Data in phase 2 were collected following the same .001), suggesting that grade III was more uncomfortable procedure and analyzed in the same way as in phase 1. As in than grade I. As a result, hand comfort still decreased with phase 1, the mean values plotted demonstrate back and hand increased grade of mobilization. This difference was again comfort for the force application method, grade of mobi- comparable to that obtained from phase 1. However, in lization, and the 2 spinal levels tested. phase 2, the method of force application was no longer significant (mean, 6 mm; CI 3.4-15 mm; P = .199). Therefore, comfort in performing pisiform mobilization Back Comfort was not significantly different to MobDyn IIb mobilizations. According to those receiving the force, the VAS ratings This change can also be attributed to the softer tip on the from the 18 participants in phase 2 demonstrated a MobDyn IIb. significant difference in back comfort when comparing the force application methods. This showed that mobilizations with the pisiform grip were still significantly more Combined Results comfortable than those with the MobDyn IIb. However, When the data from all the participants from both phases the mean difference here was 14 mm (CI 7.6-20.8 mm; P b of the study were pooled, ANOVA was used to examine the .001), which was approximately half of the difference in difference in back and hand comfort between phase 1 and phase 1. This improvement can be attributed to the use of a phase 2 to establish the effect of the modification. The softer tip on the MobDyn IIb. The other significant result difference in pisiform and tool mobilization on back comfort was the grade of force application, where grade III was was significant between the phases in both spinal regions significantly less comfortable than grade I (mean 27 mm; CI (Table 1). 19.5-34.5 mm; P b .001). This difference was comparable to This effect can be attributed to the soft tip on the that of phase 1. Therefore, as expected, back comfort still MobDyn IIb, which significantly improved simulated- decreased as grades of mobilizations increased. patient comfort. Although the mean difference in hand Although the variable, force application method, was still comfort between the use of the pisiform and tool significant in phase 2, there was no longer a significant mobilization also seemed to be reduced, this change was difference between the spinal levels (mean, 2 mm; CI 2.5- not significant between the 2 phases because it is difficult 6.3 mm; P = .369); thus, back comfort was not significantly to further reduce the small difference in hand comfort in different between the thoracic and the lumbar spine. In phase 1. Because the difference between the hand and the 370 Waddington et al Journal of Manipulative and Physiological Therapeutics Back and Comfort When Using a Mobilizing Device June 2007

tool mobilization was approximately half the discomfort region,26 only a weak correlation was found in the caused as the grade of mobilization was increased from thoracolumbar region,27 which suggests the limited role of grade I to grade III, this difference in comfort was deemed adiposity in protecting the more cephalic regions of the to be acceptable. spine. Less adipose tissue over the spinous process equates to a lesser ability of the region to absorb mobilizing forces. Therefore, the use of a softer tip to improve comfort is most indicated for the thoracic spine. DISCUSSION Another possibility is that thoracic sensitivity could be Mobilization forces were applied in the current study linked to anatomical structures that increase the stiffness in with a purpose-built, instrumented tool (the MobDyn II) that this region. PA pressures have been observed to increase was one third the size of the original prototype MobDyn. In thoracic extension.16,28 However, because the thoracic spine terms of both simulated-therapist hand comfort and simu- is stabilized by the ribcage anteriorly, rib compressibility lated-patient back comfort, this study showed significant would contribute significantly to the stiffness in this improvements from using the softer tip on a modified region.29 Furthermore, the anterior translation movements version, the MobDyn IIb. Compared with the MobDyn II, would be blocked by the orientation of the facet joints and the MobDyn IIb reduced the degree of both hand and spine the natural anterior wedging of the thoracic vertebrae that sensitivity initially observed (Table 1). In both phases, there forms the kyphosis.30,31 Therefore, stiffness in the thoracic was an expected decrease in hand and back comfort with an region is increased. This evidence is consistent with findings increase in grade of mobilization such that greater applied from a study that identified the midthoracic region as the forces were rated as less comfortable by both participants. least compliant region in the spine in a sample of young, Because the final difference in back comfort between the healthy participants with asymptomatic spines.32 use of hand and tool mobilization was half of the difference In comparison, because of the anatomical structure in the that occurred from an increase in the grade of mobilization lumbar spine, this region is not as stiff as the thoracic spine. (from grade I to grade III), the mobilizing tool now can be Variables such as adiposity26 and other factors such as considered to be acceptably comfortable to progress to sagittal rotation of the pelvis have been found to influence research into its clinical use. measures of lower lumbar stiffness, but not that of the The reason for the improvements in hand and back midlumbar region33 as tested in the present study. Therefore, comfort, as observed from the comparison of results from it can be assumed that the possible confounding variables, the 2 phases, can be attributed to the use of the softer tip of adiposity and instability of the pelvis, did not affect the the MobDyn IIb. Although the ergonomically designed validity of this study. walking-stick handle has been found in the past to be Although back discomfort was much greater in the comfortable for the hands of the elderly15 and simulated thoracic than that in the lumbar spine, it was evident in both therapists who tested the original MobDyn,24 results here regions. Because this cannot be explained by anatomical still showed otherwise. Mobilization with the tool was still discrepancies, this back discomfort was most likely linked significantly more uncomfortable than hand mobilization in to a failure to relax when the simulated patient was anxious phase 1, especially so at the thoracic spine (Fig 3). However, or perceived the method of force application as undesirable. this problem was solved with the use of the softer tip. The This was a limitation of the crossover design used in the effectiveness of this change can be explained via the present study. That is, if the simulated therapists identified a bsprings in seriesQ theory,24 whereby the yielding properties mobilization combination as undesirable, their perception of of the softer tip helped dissipate the posteroanterior forces discomfort would be carried through when they assume the applied. Hence, the transfer of mobilization forces was less role of the simulated patients. Thus, they may contract their abrupt on the simulated therapists’ hands; and thus, hand back muscles in response and reduce the compliance of their comfort was improved, as was back comfort (Fig 3). spine.34 This is a further reason for the use of the softer tip When considering the role of the softer tip on back to improve initial comfort. comfort, the sensitivity of the different spinal regions was an Another explanation relevant to findings in both the important factor. Although the thoracic spine region is not as thoracic and the lumbar regions would be an absence of the frequently researched as the lumbar and cervical regions of usual indications for spinal mobilization. Because spinal the spine, the sensitivity of the thoracic spine identified here mobilizations are not required in healthy participants, the is consistent with reports in the available literature.23 A higher grades of mobilization would stress the spinal study on the different regions of the spine showed that the structure and result in increased discomfort.31 This is also pain-pressure threshold increases caudally. Therefore, the the reason for the linear relationship between increased back magnitude of back discomfort would be greater in the more discomfort and increased grades of mobilization. Therefore, sensitive thoracic spine than that in the lumbar spine.25 the finding that back comfort was no longer different Furthermore, although a strong correlation was identified between spinal regions strongly supports the use of the between adiposity and spinal stiffness in the lower lumbar softer tip on the device. Journal of Manipulative and Physiological Therapeutics Waddington et al 371 Volume 30, Number 5 Back and Comfort When Using a Mobilizing Device

Apart from the compressibility of the patient-tool contact material, the literature also suggests that the area of the working tip of any tool used in applying forces to the spine is a major determinant of comfort. For this reason, although the use of the softer tip on MobDyn IIb significantly decreased the btool-comfort-costQ in simulated-patient back comfort, mobilizations with the pisiform grip remained more comfort- able in both phases of the study. In spinal mobilization, a smaller contact area on the patient’s back equates to more concentrated PA pressures.24,35 The contact area of the flat hard rubber tip on the original MobDyn II (Fig 1A) was smaller (573 mm2) than that of an average pisiform grip (1600 mm2).13 Because of the nonconforming properties of the firm rubber indenter head, the effective patient-tool contact area would have been limited to the patient’s spinous process. Consequently, by changing to the softer, contoured rubber tip of the MobDyn IIb (Fig 1B), the effective patient- tool contact area was increased (706 mm2). Thus, forces were less concentrated and a more acceptable level of back comfort was achieved (Table 1). Back comfort is likely to be related to both the size and the compressibility of the indenter head on any mobilizing device. Higher grades of mobilization were also associated with increased hand discomfort. The hand discomfort experi- enced is consistent with the literature concerning work- related musculoskeletal disorders of the hand.7,8,11 During mobilizations, the hands absorb a force equivalent in magnitude to that applied to the patient’s back. Because forces are focused in the small joints of the hand and wrist, they are amplified. Furthermore, because these joints were not designed to function as pseudo–weight-bearing surfaces, they are at risk of biomechanical overload; and both active and passive structures are consequently stressed.36 Some researchers have advocated the use of thumb splints as a risk control measure because they act by correcting the align- ment of thumb joints in mobilization.8,37,38 However, because forces would still be transferred through the thumbs when wearing a splint, all the thumb joints would still be at Fig 4. A, Version of the device (MobDyn III) with the force readout risk. Therefore, other risk control measures such as the use display located to the front, in the user’s line of vision. B, Visual of a mobilization tool to reduce exposure of hands to manual display on the MobDyn III showing the capacity to set a maximum force that would result in an audible signal from the device if the forces are indicated. specified amount is exceeded. Two reservations that many therapists have regarding the use of manual therapy tools are, firstly, the tool’s possible effect on stiffness discrimination and, secondly, the possible IIb.24,39 Indeed, the Kneeshaw device, already tested for elimination of touch from the therapeutic interaction. Both stiffness discrimination and not found to be different to the of these factors are seen as important in manual therapy. use of the hands,13 has a similar molded rubber tip to that on From past studies, the therapists’ ability to discriminate the MobDyn IIb. Hence, the tool should be equally capable elastic stiffness has not been found to be affected by the use of measuring force, quantifying patient progress, and of manual therapy tools.13,15 However, such studies have minimizing the high variability of force application with also found previous manual therapy tools to be relatively the softer tip.14,15 uncomfortable for both the therapists’ hands and the Although touch is considered to be an important part of patient’s backs.13 Data here suggest that the solution for manual therapy,40-42 there remains the risk of overuse this problem is the use of a softer tip. Furthermore, based on injuries from performing high volumes of manual therapy the bWorking Point Theory,Q the softer tip would not work.4,6,36 With the current version of the device, where the interfere in stiffness perception when using the MobDyn readout screen is faced toward the therapist (Fig 4A and B), 372 Waddington et al Journal of Manipulative and Physiological Therapeutics Back and Comfort When Using a Mobilizing Device June 2007

a compromise is possible—the hands could be used during Confederation for Physical Therapy; Barcelona Spain WCPT assessment, whereas the tool could be used during treat- 7th-12th June, 2003. 5. Caragianis S. The prevalence of occupational injuries among ment. Its function here would be as a risk control measure to 14,15 hand therapists in Australia and New Zealand. J Hand Ther reduce the exposure of hands to mobilization forces. 2002;15:234-41. This pattern allows the inclusion of the role that touch plays 6. West DJ, Gardner D. Occupational injuries of physiotherapists in the therapist-patient relationship while exposing the in North and Central Queensland. Aust J Physiother 2001; therapist’s hands to less concentrated forces when they are 47:179-86. 7. Reglar P, James G. Thumb pain in physiotherapists: a performing mobilizations. preliminary study. Br J Ther Rehabil 1999;6:505-9. 8. Wajon A, Ada L. Prevalence of thumb pain in physical therapists practicing spinal manipulative therapy. J Hand Ther CONCLUSION 2003;16:237-44. 9. Bronfort G, Haas M, Evans RL, Bouter LM. Efficacy of spinal The modified spinal mobilization tool, MobDyn IIb, was manipulation and mobilization for low back pain and neck found to be acceptably comfortable at the back and the pain: a systematic review and best evidence synthesis. Spine J hands. With a contoured soft rubber tip, the tool-comfort- 2004;4:335-56. 7 cost was no longer significant between the sensitive thoracic 10. Waddell G. The back pain revolution. 2nd ed. China Churchill Livingstone; 2004. spine and the lumbar spine. Furthermore, hand comfort was 11. Snodgrass SJ, Rivett DA. Thumb pain in physiotherapists: not significantly different between the tool and the pisiform potential risk factors and proposed prevention strategies. grip. Because there is a potential benefit in the use of the J Manipulative Physiol Ther 2002;10:206-17. MobDyn IIb in the prevention of hand injury, further 12. Verhagen AP, Karels C, Bierma-Zeinstra SMA, et al. Ergo- research is warranted in the clinical setting involving nomic and physiotherapeutic interventions for treating work- related complains of the arm, neck or shoulder in adults. therapists with a history of hand pain and patients with a Cochrane Database Syst Rev 2006;3:CD003471. history of back pain. 13. Maher CG, Latimer J, Starkey I. An evaluation of Superthumb and the Kneeshaw device as manual therapy tools. Aust J Physiother 2002;48:25-30. 14. Waddington G, Diong J, Adams R. Development of a hand Practical Applications dynamometer for the control of manually applied forces. J Manipulative Physiol Ther 2006;29:297-304. ! Simulated patients rated back comfort and simu- 15. Waddington G, Adams R. Initial development of a device for lated therapists rated hand comfort of a device as controlling manually applied forces. Man Ther 2006; [Sept 11: Electronic publication]. lower than when using the hands when the device 16. Sran MM, Khan KM, Zhu Q, McKay HA, Oxland TR. Failure had a hard rubber tip. characteristics of the thoracic spine with a posteroanterior load: ! Comfort was improved by the use of a soft molded investigating the safety of spinal mobilization. Spine rubber tip on the instrumented mobilizing device. 2004;29:2382-8. ! Comfort for both hands and backs of asymptomatic 17. Chiradejnant A, Maher C, Latimer J. Forces applied during central posteroanterior mobilization treatment of patients with subjects decreased with greater applied force. low back pain. Proceedings of the 7th Scientific Conference ! The thoracic spine was more sensitive to applied of the International Federation of Orthopaedic Manipulative forces than the lumbar spine. Therapists in conjunction with the 11th Biennial Conference of the Manipulative Physiotherapists Association of Aus- tralia. Perth; Australian Physiotherapy Association November 6th-10th, 2000. 18. Chiradejnant A, Latimer J, Maher CG. Forces applied during manual therapy to patients with low back pain. J Manipulative REFERENCES Physiol Ther 2002;25:362-9. 1. Bork E, Cook TM, Rosecrance JC, et al. Work-related 19. Chiradejnant A, Maher CG, Latimer J. Objective manual musculoskeletal disorders among physical therapists. Phys assessment of lumbar posteroanterior stiffness is now possible. Ther 1996;76:827. J Manipulative Physiol Ther 2003;26:34-9. 2. Holder NL, Clark HA, Di J, Blasio M, et al. Cause, 20. Chester R, Swift L, Watson MJ. An evaluation of therapists’ prevalence, and response to occupational musculoskeletal ability to perform graded mobilization on a simulated spine. injuries reported by physical therapists and physical Physiother Theory Pract 2003;19:23-34. therapist assistants (statistical data included). Phys Ther 21. Harms MC, Bader DL. Variability of forces applied by 1999;79:642-58. experienced therapists during spinal mobilization. Clin Bio- 3. Cromie JE, Robertson VJ, Best MO. Work-related muscu- mech 1997;12:393-9. loskeletal disorders in physical therapists: prevalence, severity, 22. Snodgrass SJ, Rivett DA, Robertson VJ. Manual forces risks, and responses. Phys Ther 2000;80:336-51. applied during posterior-to-anterior spinal mobilization: a 4. Branton A, Egan K, Conroy R, Horgan F. A study examining review of the evidence. J Manipulative Physiol Ther 2006; the prevalence of thumb signs and symptoms among 29:316-29. physiotherapists working in private practice in Ireland. 23. Maitland GD, Hengeveld E, Banks K, English K. Vertebral Proceedings of the 14th international WCPT. The World manipulations. Butterworth7 Heinemann; 2005. Journal of Manipulative and Physiological Therapeutics Waddington et al 373 Volume 30, Number 5 Back and Comfort When Using a Mobilizing Device

24. Nicholson L, Maher C, Adams R. Hand contact area, force bourne (Victoria)7 Australian Physiotherapy Association; 1987. applied and early non-linear stiffness (toe) in a manual stiffness p. 367-76. discrimination task. Man Ther 1998;3:212-9. 33. Chansirinukor W, Lee M, Latimer J. Contribution of pelvic 25. Keating L, Lubke C, Powell V, Young T, Souvlis T, Jull G. rotation to lumbar posteroanterior movement. Man Ther Mid-thoracic tenderness: a comparison of pressure pain 2001;6:242-9. threshold between spinal regions, in asymptomatic subjects. 34. Shirley D, Lee M, Ellis E. The relationship between Man Ther 2001;6:34-9. submaximal activity of the lumbar extensor muscles and 26. Viner A, Lee M, Adams R. Posteroanterior stiffness in the lumbar posteroanterior stiffness. Phys Ther 1999;79:278-85. lumbosacral spine: the correlation between adjacent vertebral 35. Squires MC, Latimer J, Adams RD, Maher CG. Indenter levels. Spine 1997;22:2724-9. head area and testing frequency effects on posteroanterior 27. Chansirinukor W, Lee M, Latimer J. Contribution of ribcage lumbar stiffness and subjects’ rated comfort. Man Ther 2001;6: movement to thoracolumbar posteroanterior stiffness. J Manip- 40-7. ulative Physiol Ther 2003;26:176-83. 36. Snodgrass SJ, Rivett DA, Chiarelli P, Bates AM, Rowe LJ. 28. Sran MM, Khan KM, Zhu Q, Oxland TR. Posteroanterior Factors related to thumb pain in physiotherapists. Aust J stiffness predicts sagittal plane midthoracic range of motion Physiother 2003;49:243-50. and three-dimensional flexibility in cadaveric spine segments. 37. Blizzard P. Save our thumbs. Physiotherapy 1991;77:573-4. Clin Biomech 2005;20:806-12. 38. Wajon A, Ada L, Refshauge K. Work-related thumb pain in 29. Edmondston S, Allison G, Althorpe B, McConnell D, Samuel physiotherapists is associated with thumb alignment during K. Comparison of ribcage and posteroanterior thoracic spine performance of PA pressures. Man Ther 2007;12:12-6. stiffness: an investigation of the normal response. Man Ther 39. Gibson JJ. The sense considered as perceptual systems. 1999;4:157-62. London7 George Allen & Unwin Ltd; 1968. 30. Goh S, Price R, Leedman P, Singer K. The relative influence of 40. Roger J, Darfour D, Dham N, Hickman O, Shubach L, Shepard vertebral body and intervertebral disc shape on thoracic K. Physiotherapists’ use of touch in inpatient settings. kyphosis. Clin Biomech 1999;14:439-48. Physiother Res Int 2002;7:170-86. 31. Edmondston S, Singer K. Thoracic spine: anatomical and 41. Hargreaves S. The relevance of non-verbal skills in physi- biomechanical considerations for manual therapy. Man Ther otherapy. Physiotherapy 1987;73:685-8. 1997;2:132-43. 42. Petitpas A, Cornelius A. Practitioner-client relationships: 32. Minucci A. Palpation of the thoracic spine T1-T8. In: Dalziel building working alliances. In: Kolt G, Anderson M, editors. BA, Snowsill JC, editors. Fifth Biennial Conference of Psychology in the physical and manual therapies. London7 the Manipulative Therapists Association of Australia. Mel- Churchill Livingstone; 2004. p. 57-70. EFFECT OF AGE AND SEX ON HEART RATE VARIABILITY IN HEALTHY SUBJECTS

John Zhang, MD, PhD

ABSTRACT

Objective: The study aimed to investigate the effect of age and sex on the heart rate variability (HRV) analysis and to explore the normal range of HRV in different age and sex groups for potential health care applications. Method: Baseline HRV, age, and sex data were collected from 470 subjects without cardiovascular conditions. Short-term HRV was recorded using Biocom Active ECG units (Biocom, Seattle, Wash). Subjects were divided by age into 10-year intervals and by sex for HRV analysis. Results: Total power, representing the overall autonomic activity, decreased consistently from the age groups 10+ to 80+ years ( P b .001). Both the low frequency (sympathetic activity) and high frequency (parasympathetic activity) declined ( P b .05) as age increased. Sex had a significant effect on heart rate, R-R interval, high frequency, normalized low frequency, normalized high frequency, and low frequency–high frequency ratio. Sex did not seem to affect the SD of the normal-to-normal heartbeats and total power ( P N .05) despite the significant heart rate changes ( P b .05). Conclusion: This study demonstrated that age had a greater impact on HRV than sex. The older age group had consistently lower HRV than younger people. The values generated in this study may be useful in health care settings to determine abnormal ranges of HRV under different clinical and experimental conditions. (J Manipulative Physiol Ther 2007;30:374Q379) Key Indexing Terms: Heart Rate; Age Factors; Sex

he chiropractic profession has become increas- simplicity, accuracy, and noninvasive application.3,4 How- ingly aware of the value of heart rate variability ever, a normal range of HRV in the healthy asymptomatic (HRV) analysis with increased research activities population has still not been identified. When HRV is T 1,2 in recent years. Some research evidence has suggested compared to blood pressure measurements in perceived that autonomic nervous system activities may be affected by normal or abnormal readings, even untrained people normal and diseased conditions.3,4 Modern physiologic recognize a blood pressure reading of more than 140/90 investigations of the impact of somatosensory input on mm Hg as higher than normal (120/80 mm Hg). Similarly, a autonomic functions have been reviewed by Sato et al3 with heart rate measurement of 110 beats per minute suggests an 750 basic scientific articles cited. There is a growing need increased heart rate (tachycardia). However, the perceived for a clearly defined normal range of HRV in different age normal range is not clear for HRV measurements. Without a and sex groups to make HRV a useful clinical assessment normal range, changes in HRV are difficult to interpret and tool in chiropractic and other health care professions. use in evaluating chiropractic adjustments. Heart rate variability analysis has been used for many Recent studies on the effect of age and sex on HRV years to measure autonomic nervous system activities for its focused on certain stimulations to change the short-term HRV. Sato and Miyake4 found that the male subjects were more sympathetic dominant than the female subjects. Carter a Associate Professor, Associate Director of Research, Logan et al5 reported an increase in total power in all age groups after College of Chiropractic, Chesterfield, MO. endurance training programs. Bonnemeier et al6 investigated This study was funded internally by the Logan College of Chiropractic, Chesterfield, MO. the circadian profile of cardiac autonomic nervous modu- Submit requests for reprints to: John Zhang, MD, PhD, Logan lation in healthy subjects and concluded that normal aging College of Chiropractic, Chesterfield, MO 63017, USA was associated with a constant decline of cardiac vagal (e-mail: [email protected]). modulation due to a significant decrease in nocturnal para- Paper submitted April 7, 2006; in revised form February 22, sympathetic activity. The significant sex-related difference of 2007; accepted March 25, 2007. 0161-4754/$32.00 HRV decreased with aging. These findings emphasize the Copyright D 2007 by National University of Health Sciences. need to determine age- and sex-dependent normal ranges for doi:10.1016/j.jmpt.2007.04.001 HRV assessment. Normal HRV in the healthy population is

374 Journal of Manipulative and Physiological Therapeutics John Zhang 375 Volume 30, Number 5 Heart Rate Variability

Table 1. Relationship of sex to HRV

Sex n Mean SD Minimum Maximum tP

Mean RR Male 167 825.379 126.588 511.6 1162 6.957 .009 Female 303 799.368 121.98 525.2 1221 RM-SSD Male 167 38.598 28.558 4.7 186 2.225 .136 Female 303 43.46 45.311 4.7 550.3 Total power Male 167 697.117 847.911 14.9 6918.6 0.066 .798 Female 303 706.263 883.162 10.4 7665.8 VLF Male 167 274.23 350.867 8.8 2749.9 0.596 .44 Female 303 254.688 425.437 2.1 5872.3 LF Male 167 291.263 472.27 2.2 4741.8 0.377 .539 Female 303 258.919 339.015 3.5 2557.5 HF Male 167 132.08 225.481 1.3 2266 6.461 .011 Female 303 191.372 333.216 1.6 3176.1 LF NORM Male 167 68.308 19.946 14.3 98.2 17.204 .0001 Female 303 60.867 19.947 13 96.8 HF NORM Male 167 31.604 19.907 1.8 85.7 16.525 .0001 Female 303 38.469 20.031 3.2 87 LF/HF ratio Male 167 4.37 5.86 0 53 16.542 .0001 Female 303 2.77 3.33 3 30 RR, R-R interval; RM-SSD, square root of the mean squared differences of successive normal-to-normal intervals; VLF, very low frequency; NORM, normalized.

Fig 2. Relationship of sex to SDNN. Fig 1. Relationship of sex to heart rate. strongly affected by 2 factors: age and exercise. Young people short term are unlikely to be effective. For example, by (b30 years) tend to have higher HRV because of active asking an individual to run for 10 minutes, a temporary autonomic modulations. With aging, the heart rate changes increase in heart rate will be observed; when the individual less because of increasingly sedentary lifestyle. The only rests, his heart rate will return to the resting level. This is proven method for older people (N50 years) to increase their true with HRV recording. Exercise and sympathomimetic HRV is engaging in regular exercise. drugs can change short-term HRV, but once drug and Decreased HRV is caused by disease processes such as exercise effects are gone, HRV returns to the set point.9 stress, anxiety, diabetes, heart disease, hypertension, and However, if drug and exercise are applied daily over a many other conditions.7,8 However, the normal range of period, the HRV set point becomes reset at higher or lower HRV is one of the most important factors in the application levels. Therefore, studies of short-term HRV changes should of HRV analysis to any medical condition. To observe a take into account these limitations. This is the reason why treatment effect on HRV, an overlooked factor is the bset long-term HRV changes are more reliable than short-term pointQ of the normal HRV, regulated by the body’s negative HRV changes.11 feedback mechanism to maintain homeostasis. The set point It is important that normative HRV data are collected for is not changed by short-term heart rate fluctuations except studying the effects of chiropractic manipulation on HRV. by trauma. The set point is established and modulated by This study gathered HRV data from many studies to lifestyle and physiologic processes of the internal organs generate baseline HRV readings evaluating effects of age over the years.9,10 Attempts to change the set point in the and sex on HRV. 376 John Zhang Journal of Manipulative and Physiological Therapeutics Heart Rate Variability June 2007

Table 2. Relationship of age to HRV

Age n Mean SD Minimum Maximum F P

Mean RR 10+ 15 793.753 117.979 647.6 1075.2 3.955 0 20+ 63 760.975 132.274 511.6 1125 30+ 83 799.894 123.606 527.6 1147.1 40+ 115 809.617 116.823 540 1163.1 50+ 92 811.529 119.539 562.8 1221 60+ 68 854.382 123.774 614.8 1162 70+ 27 813.526 126.171 583.8 1058.1 80+ 7 853.986 120.001 595.5 942.5 RM-SSD 10+ 15 49.06 28.639 19.2 98.3 1.34 .229 20+ 63 43.825 26.802 9.2 147.1 30+ 83 45.454 30.699 6.4 179.4 40+ 115 35.988 24.975 5.4 162.7 50+ 92 48.895 70.896 4.7 550.3 60+ 68 35.266 25.264 7.4 186 70+ 27 41.474 36.578 8.3 136.9 80+ 7 27.129 24.318 4.7 79.1 Total power 10+ 15 1627.073 1796.028 240.5 6918.6 7.561 .000 20+ 63 872.468 695.091 56.2 3317.3 30+ 83 913.537 950.546 43 5330.1 40+ 115 688.602 900.373 32.8 7665.8 50+ 92 676.824 884.743 10.4 6262.7 60+ 68 344.572 310.673 30.9 1624.3 70+ 27 308.87 272.382 46.1 1112.3 80+ 7 284.814 432 14.9 1240.4 VLF 10+ 15 532.347 586.369 120.5 2293.1 3.37 .002 20+ 63 313.632 252.518 31.4 1310.6 30+ 83 321.453 435.591 15.2 2749.9 40+ 115 278.683 572.404 12.7 5872.3 50+ 92 245.017 299.597 5 1637.4 60+ 68 149.713 164.68 2.1 951.9 70+ 27 116.581 87.156 16.6 364.7 80+ 7 89.129 63.616 11.4 169.1 LF 10+ 15 809.2 1250.543 36.7 4741.8 10.049 0 20+ 63 346.77 305.004 10.7 1445.4 30+ 83 371.096 460.525 13.5 2557.5 40+ 115 257.496 277.373 10.3 1352.2 50+ 92 241.704 302.285 3.8 1490.6 60+ 68 110.119 108.97 3.5 502.9 70+ 27 87.722 92.576 8.5 456.5 80+ 7 86.071 155.614 2.2 431.6 HF 10+ 15 285.5 272.219 36.4 828.7 2.312 .025 20+ 63 216.022 300.328 5.5 1717.6 30+ 83 218.568 246.408 3 997 40+ 115 150.475 262.752 1.7 1915.6 50+ 92 191.24 458.585 1.6 3176.1 60+ 68 81.459 135.945 1.3 961.9 70+ 27 104.015 183.424 1.6 758.2 80+ 7 109.071 234.448 1.3 639.7 LF NORM 10+ 15 66.267 20.417 26.4 85.6 1.177 .314 20+ 63 64.967 17.265 16.6 92.5 30+ 83 63.576 19.808 13 93.1 40+ 115 65.247 18.735 14.3 96 50+ 92 64.082 22.234 13.1 96.9 60+ 68 59.641 21.212 15.7 98.2 70+ 27 61.907 24.619 15.7 94.4 80+ 7 51.5 18.474 15 65.8 HF NORM 10+ 15 33.733 20.417 14.4 73.6 1.108 .357 20+ 63 34.594 17.448 7.5 83.4 30+ 83 36.249 19.794 6.9 87 40+ 115 34.447 18.581 4 85.7 50+ 92 35.075 21.927 3.1 86.9 Journal of Manipulative and Physiological Therapeutics John Zhang 377 Volume 30, Number 5 Heart Rate Variability

Table 2. continued Age n Mean SD Minimum Maximum F P

HF NORM 60+ 68 39.663 21.659 1.8 84.3 70+ 27 37.689 24.764 5.6 84.3 80+ 7 48.129 18.823 32 85 LF/HF ratio 10+ 15 2.95 1.92 0 6 0.88 .522 20+ 63 2.78 2.3 0 12 30+ 83 2.91 2.66 0 14 40+ 115 3.27 3.6 0 24 50+ 92 4.27 5.9 0 31 60+ 68 3.5 6.91 0 53 70+ 27 3.44 3.82 0 17 80+ 7 1.29 0.66 0 2

Fig 4. Relationship of age to SDNN. Fig 3. Relationship of age to heart rate (N = 470).

digital signal-processing software. This scanner records MATERIALS AND METHODS electrocardiographic (ECG) signals, computing the instanta- neous changes of HRV after each session. A Biocom Active Design ECG unit connected the unit to the subjects through 3 small This retrospective study gathered baseline HRV data electrodes that attach to the left arm, right arm, and left leg. from studies in the past 4 years that involved HRV data. No additional gels were needed. If the ECG signal was weak, Subjects in the original studies were required to read and the skin surface was cleaned to improve skin conductance. sign institutional review board–approved informed consent documents before undergoing any study-related procedures. All study data collections were approved by an institutional Statistical Analysis review board. From existing studies, only baseline HRV, Subjects were divided by age and sex for final data age, and sex were used. analysis. Age groups were divided by 10-year intervals, producing a total of 8 age groups from 10+ to 80+ years old. All continuous data were expressed in mean values F SD. Inclusion Criteria The paired t test was used for comparisons of continuous Subjects were selected from different racial, sex, and age variables measured in the study. Analysis of variance was groups. used for comparison of 3 or more groups. Correlation was analyzed using SPSS 12 (SPSS Inc, Chicago, Ill). P b .05 Exclusion Criteria was considered significant. Individuals with coronary heart diseases, serious and uncontrolled hypertension, or other overt diseases were RESULTS excluded from the study. Data on HRV from 470 subjects (303 females) were included. The average patient age was 44 F 16 years. Sex Measurement had a significant effect on heart rate, R-R interval, high Biocom’s Heart Rhythm Scanner (Active ECG, Biocom, frequency (HF, represents some parasympathetic activity), Seattle, Wash) was used in the HRV data collection with normalized low frequency (LF, represents some sympathetic 378 John Zhang Journal of Manipulative and Physiological Therapeutics Heart Rate Variability June 2007

activity), normalized HF, and LF/HF ratio (Table 1, Fig 1). gradual decline to the 80+ age group. The reason for this Sex did not seem to affect the SD of the normal-to-normal large drop at 2 critical ages was not clear. It was postulated heartbeats (SDNN, Fig 2), total power ( P N .05), or the LF that the significant decrease in HRV resulted from the component despite the significant heart rate changes ( P b transition from postpubertal growth spurt to adulthood and .05). Both the SDNN and the total power were higher in the overall decline in physical activities and possibly health females than in males but did not reach statistically in the 60+ age group. Further study may include neonates to significant levels. Age groups from 10+ to 80+ years extend the range of the age groups. It has been reported that showed significant differences on HRV response (Table 2, increasing postnatal age was accompanied by a significant Figs 3 and 4). Total power, representing the overall ( P b .05) elevation of HRV parameters.11 autonomic activity, decreased consistently in age groups This study is significant because it used a relatively large 10+ to 80+ years ( P b .001). The age groups 20+ to 50+ database to determine the distribution of HRV in varying years had narrow ranges of total power readings. The age and sex groups. The numbers in Tables 1 and 2 may be biggest change of total power was found between the age helpful in determining normal ranges for HRV comparisons groups 10+ to 20+ and 50+ to 80+ years. The SDNN also under different clinical and experimental conditions. How- decreased ( P b .05) as age increased (Fig 4). Both the LF ever, the database needs to expand to cover wider age and HF declined ( P b .05) as age increased (Table 2). groups and include more subjects. Although it was known that long-term exercise exerts significant effects on the HRV, it was not part of the study because of the limitation of the study design. The effect of DISCUSSION exercise on HRV needs to be investigated and compared to Since the first study on the effect of mechanical stimulation the data in the current study. on the autonomic nervous system activities,12 many studies have investigated the effects of spinal stimulation on autonomic or visceral function.13-19 A recent study by Budgell CONCLUSION and Polus20 demonstrated improvement of HRVafter thoracic Age was the most considerable factor affecting HRV in chiropractic adjustments. Our own studies also showed a this study. Sex did not seem to significantly affect the positive effect of chiropractic adjustment on HRV.21,22 These resting HRV. Further studies will compare this normal range efforts affect the long-term use of HRV in the chiropractic of HRV with the HRV in patients with a variety of illnesses profession. There is a great need for establishing the normal and physical conditions. Final establishment of reference HRV ranges in age and sex groups to provide guidance in the HRV ranges based on patient age could be used to evaluate clinical application of HRV analysis. the effect of chiropractic manipulation on the autonomic Two important issues were addressed in the current nervous system. study: the influence of sex on subjects’ HRV and the effect of age on subjects’ HRV. This study demonstrated that age had a greater impact on the HRV than sex. Interestingly, the mean values of the female subjects’ heart rate (76.9 beats per minute) was slightly higher than that of male subjects (74.5 beats per minute), but the total power was also higher Practical Applications in the female subjects. ! Heart rate variability decreases with advancing age The heart rate sex differences were significant, whereas in healthy subjects. the total power difference was not statistically significant. ! Heart rate variability is less affected by sex. Women throughout the world enjoy higher life expectancy ! Heart rate variability may be useful in health compared to men for varying reasons. Could higher total care settings to determine abnormal ranges of power, an increased parasympathetic activity, play a role in HRV under different clinical and experimental their longevity? Because the total power in this study was conditions. not significantly higher in the female sex, no conclusion could be drawn on the effect of sex on the HRV. The effect of age on HRV demonstrates the most striking differences. Subjects in the 10+ age group had much higher total power of 1627 compared with 284 in the 80+ age REFERENCES group. The other age groups presented themselves in 1. Eingorn AM, Muhs GJ. Rationale for assessing the effects of descending order (Table 2). Total power was lower from manipulative therapy on autonomic tone by analysis of heart rate variability. J Manipulative Physiol Ther 1999;22:161-5. the 10+ to the 20+ age groups and stayed fairly flat from the 2. Driscoll D, Dicicco G. The effects of metronome breathing on 20+ to 50+ age groups. The HRV total power of the 60+ age the variability of autonomic activity measurements. J Manip- group showed another marked drop before continuing a ulative Physiol Ther 2000;23:610-4. Journal of Manipulative and Physiological Therapeutics John Zhang 379 Volume 30, Number 5 Heart Rate Variability

3. Sato A, Sato Y, Schmidt RF. The impact of somatosensory 13. Budgell B, Sato A. Modulations of autonomic functions by input on autonomic functions. Rev Physiol Biochem Pharma- somatic nociceptive inputs. Progress in brain research 1996;vol col vol 130. Berlin7 Springer-Verlag; 1997. 113. Amsterdam7 Elsevier; 1996. p. 525-39. 4. Sato N, Miyake S. Cardiovascular reactivity to mental stress: 14. Budgell B, Hotta H, Sato A. Spinovisceral reflexes evoked relationship with menstrual cycle and gender. J Physiol by noxious and innocuous stimulation of the lumbar spine. Anthropol Appl Human Sci 2004;23:215-23. J Neuromusculoskelet Syst 1995;3:122-31. 5. Carter JB, Banister EW, Blaber AP. The effect of age and 15. Budgell B, Sato A, Suzuki A, Uchida S. Responses of adrenal gender on heart rate variability after endurance training. Med function to stimulation of lumbar and thoracic interspinous Sci Sports Exerc 2003;35:1333-40. tissues in the rat. Neurosci Res 1997;28:33-40. 6. Bonnemeier H, Richardt G, Potratz J, et al. Circadian profile of 16. Budgell B, Hotta H, Sato A. Reflex responses of bladder cardiac autonomic nervous modulation in healthy subjects: motility following stimulation of interspinous tissues in differing effects of aging and gender on heart rate variability. the anesthetized rat. J Manipulative Physiol Ther 1998;21: J Cardiovasc Electrophysiol 2003;14:791-9. 593-9. 7. Hoyer D, Friedrich H, Zwiener U, Pompe B, Baranowski R, 17. Bolton PS, Kerman IA, Woodring SF, Yates BJ. Influences of Werdan K, Muller-Werdan U, Schmidt H. Prognostic impact of neck afferents on sympathetic and respiratory nerve activity. autonomic information flow in multiple organ dysfunction Brain Res Bull 1998;47:413-9. syndrome patients. Int J Cardiol 2006;14:359-69. 18. Fujimoto T, Budgell B, Uchida S, Suzuki A, Meguro K. 8. Sato A, Sato Y, Schmidt RF. Changes in blood pressure and Arterial tonometry in the measurement of the effects of heart rate induced by movements of normal and inflamed knee innocuous mechanical stimulation of the neck on heart rate joints. Neurosci Lett 1984;52:55-60. and blood pressure. J Auton Nerv Syst 1999;75:109-15. 9. Antelmi I, de Paula RS, Shinzato AR, Peres CA, Mansur AJ, 19. Kimura A, Ohsawa H, Sato A, Sato Y. Somatocardiovascular Grupi CJ. Influence of age, gender, body mass index, and reflexes in anesthetized rats with the central nervous system functional capacity on heart rate variability in a cohort of intact or acutely spinalized at the cervical level. Neurosci Res subjects without heart disease. Am J Cardiol 2004;93:381-5. 1995;22:297-305. 10. Tuomainen P, Peuhkurinen K, Kettunen R, Rauramaa R. 20. Budgell B, Polus B. The effects of thoracic manipulation on Regular physical exercise, heart rate variability and turbulence heart rate variability: a controlled crossover trial. J Manipu- in a 6-year randomized controlled trial in middle-aged men: the lative Physiol Ther 2006;29:603-10. DNASCO study. Life Sci 2005;77:2723-34. 21. Zhang JQ, Dean D, Nosco D, Strathopulos D, Floros M. Effect 11. Longin E, Schaible T, Lenz T, Konig S. Short term heart rate of chiropractic care on heart rate variability and pain in a variability in healthy neonates: normative data and physio- multisite clinical study. J Manipulative Physiol Ther logical observations. Early Hum Dev 2005;81:663-71. 2006;29:267-74. 12. Sato A, Swenson RS. Sympathetic nervous system response to 22. Zhang JQ. Short-term power spectrum analysis of heart rate mechanical stress of the spinal column in rats. J Manipulative variability of chiropractic students in college. Chiropr Res J Physiol Ther 1984;7:141-7. 2000;7:70-7. ASINGLE-BLIND PILOT STUDY TO DETERMINE RISK AND ASSOCIATION BETWEEN NAVICULAR DROP, CALCANEAL EVERSION, AND LOW BACK PAIN

James W. Brantingham, DC, PhD,a Katy Jane Adams, MSc Chiropractic,b Jeffery R. Cooley, DC,c Denise Globe, DC, MS, PhD,d and Gary Globe, DC, MBA, PhDe

ABSTRACT

Objective: Syndromes causing mechanical low back pain (MLBP) continue to plague the US health care system. One hypothesis is that flatfeet are a risk factor for MLBP. This pilot study evaluated whether subjects with flatter feet are at greater risk for MLBP than subjects without flatter feet. Methods: Fifty-eight subjects (16-70 years old) were allocated to a group diagnosed with 2 or more episodes of MLBP or with no history of MLBP. A blind assessor measured navicular drop (ND) using navicular height (NH) and calcaneal eversion (CE). Based on a range of reported data, flatfoot was defined as a possible risk factor for MLBP with ND greater than 3, 8, and/or 10 mm, and/or greater than 68 CE. Results: According to v2 analysis, risk of MLBP appeared similar between groups ( P N .05). There was no significant difference ( P N .05) between continuous variables (t tests, Pearson r and r2) with one exception, correlation of increasing CE with increasing ND ( P = .0001). Power was generally low (b0.80). Likelihood ratios and Fisher exact tests supported the v2 analysis. Conclusions: In this study, flatfeet did not appear to be a risk factor in subjects with MLBP. However, small sample size, low power, broader age range, low prevalence of flatfeet (N10 mm ND), and lesser back pain severity make these data tentative. Further research is needed. (J Manipulative Physiol Ther 2007;30:380-385) Key Indexing Terms: Chiropractic; Low Back Pain; Flatfoot; Etiology

he impact of mechanical low back pain (MLBP) is lation, rehabilitation, and physical therapy modalities.3 significant with increasing costs for health care, However, despite treatment, some MLBP conditions do T industry, and society.1,2 Many MLBP conditions not resolve or recur with unacceptable frequency.1 are effectively managed by general medical care, manipu- There exist numerous etiologic theories for the develop- ment and perpetuation of MLBP.4,5 One theory holds that a

a flatfoot or flatfeet is a risk factor for, cause of, or perpetuator of Associate Professor, Cleveland Chiropractic College Los 6,7 Angeles, Los Angeles, Calif 90004, USA. MLBP. Because of this belief, and evidence that bilateral b Associate Chiropractor, Windsor Remedy Centres, Windsor, foot alignment and range of motion should be roughly Berkshire SL4 3HU, United Kingdom. equivalent,8-10 one posited mechanism is that a single flatfoot c Senior lecturer, School of Chiropractic, Murdoch University, may cause an unleveling or malalignment of the pelvis, leading South Street, Murdoch 6150, Western Australia. d to MLBP; others speculate that loss of shock absorption from Director, Global Health Economics, Amgen Inc, Thousand 6,7,11 Oaks, Calif 91320, USA. flatfeet will cause MLBP. Although these theories remain e Provost and Academic Dean, Cleveland Chiropractic College hypothetical, and no fully agreed normative data exist defining Los Angeles, 590 South Vermont Avenue, Los Angeles, Calif level, ranks, or severity of flatfeet (see the succeeding 90004, USA. data),12,13 many practitioners clinically apply these theories Submit requests for reprints to: James W. Brantingham, DC, and dispense foot orthotics to treat MLBP.6,7,11 PhD, Associate Professor, Cleveland Chiropractic College Los Although greater than 3 mm of navicular drop (ND) has Angeles, 590 South Vermont Avenue, Los Angeles, CA 90004, 14 USA (e-mails: [email protected], chirokate@ been suggested as a risk factor for MLBP, studies have hotmail.co.uk, [email protected], [email protected], gary. suggested that 10 mm or less should be considered normal [email protected]). (11 mm of ND was reported abnormal).15,16 Literature Paper submitted October 26, 2006; in revised form March 23, review using navicular height (NH) to assess reliability of 2007; accepted March 25, 2007. ND conservatively suggests that normal ND is on average at 0161-4754/$32.00 15 Copyright D 2007 by National University of Health Sciences. least 6 to 8 mm. In specific disorders, there is commonly a doi:10.1016/j.jmpt.2007.04.004 larger ND, 13 to 15 mm being typical and correlating with

380 Journal of Manipulative and Physiological Therapeutics Brantingham et al 381 Volume 30, Number 5 Foot Position and Low Back Pain

increased risk of foot injury or weakness.15 Indeed, in might obscure measurements,21,22 and anterior cruciate assessing patients with rheumatoid arthritis (with docu- ligament rupture significantly increase ND and were there- mented flattening of the medial longitudinal arch due to fore exclusion factors.23-25 ligament damage), Shrader et al15 found an average ND 15 drop of approximately 10 mm. Thus, as a compromise, Z this study has assessed risk for MLBP associated with Inclusion Criteria Group 2 greater than 3, 8, or 10 mm ND. On the other hand, Inclusion criteria for group 2 were the same as group 1, abnormal weight-bearing calcaneal eversion (CE) as a cause except subjects were asymptomatic or with a musculoske- of flatfeet or hyperpronation has been reported from 58 to letal complaint that did not include LBP, as defined in 138, but literature presently suggests that normal weight- the study. bearing CE is 68 or less; therefore, increased risk for MLBP 6,17 was defined as greater than 68. Exclusion CriteriaZGroup 2 With increasing emphasis on evidence to support clinical The same criteria were used as in group 1, except practice, it is important to systematically investigate the subjects were excluded if they had experienced a single potential relationship between flatfeet and low back pain episode of LBP, as revealed by history and examination. (LBP). Roncarati and McMullen18,19 studied more than 674 patients with LBP and found (using the Feiss line—a variant of ND) no association between flatfeet and LBP. Blinding Only one controlled study (using ND) has attempted to This was a single-blind study. An experienced podiatrist, measure such a relationship and found no correlation blind to group designation, performed measurements for between flatfeet in 100 patients with and 104 patients ND in millimeters and degrees of CE (in relaxed calca- 16 without MLBP. This present study, using a more reliable neal stance). modified ND test and additional CE measurement, inves- tigates their association with the presence of MLBP. In conjunction with the previous research,16,18 this study may Measurements help to determine if subjects with flatter feet are at greater The methods used in this study have extended use as risk than subjects without flatter feet for MLBP. common and acceptable measurements for determination of the presence of flatfeet.12,17,21,26 The ND test and CE range of motion were measured. If done carefully, increased ND or METHODS increased CE (or both) suggests a flatter medial longitudinal arch and flatter feet. Measurement of NH by ruler (used with Subjects were recruited directly from the University of ND) is valid and reliable for showing flattening of the Surrey Chiropractic Clinic (Guildford, Surrey, GU2 7XH) as medial longitudinal arch (representing the position of the well as through poster and leaflet advertisements placed navicular tuberosity and sagittal plane angular relationships around the university and local city area. Group 1 was made 12 up of 30 subjects diagnosed with 2 or more episodes of of the calcaneus and first metatarsal). Measurement of calliper-based relaxed calcaneal bisection eversion or valgus current or past MLBP. Group 2 was made up of a control stance in degrees is reliable and accurate17 and correlates population of 28 subjects with no history of MLBP. well with the radiographic malleolar valgus index.27,28 Normal eversion by this method is 68 or less.17 Inclusion CriteriaZGroup 1 Nevertheless, depending on the methodology used for Subjects were required to read and sign an informed measurement, and with up to moderate intratester reliability consent document with the understanding that this study for the ND and CE test, there has been controversy received prior institutional review board approval from the regarding the ND test because previous initial height b Q Research Ethics Committee of the University of Surrey. measurements were taken using the subtalar neutral position, the reliability and validity of which is now Diagnosis of MLBP and exclusion of non-MLBP followed 21,22,29,30 guidelines and algorithms as written by Souza.20 Subjects questioned. Therefore, we did not use the subtalar were 16 to 70 years old, required to undergo a full case neutral position in this study. history and relevant physical and orthopedic examination, Using a marked wooden plank platform (with spirit level), we obtained ND (using NH technique) and CE and with 2 or more episodes of LBP, defined as pain around 31 or over L1/L5, the sacrum and/or sacroiliac joints. measurements. The subject sat in a chair with the knee flexed and the foot resting on the floor. The midpoint of the navicular tubercle was marked, and the distance from the Exclusion CriteriaZGroup 1 tubercle to the floor (measured in mm with a ruler) was Previous or present pathologic LBP and inability to stand noted as the first or initial measurement. Next, the subject and walk unassisted, foot and ankle trauma or fractures that stood up with full weight bearing on the feet, and the 382 Brantingham et al Journal of Manipulative and Physiological Therapeutics Foot Position and Low Back Pain June 2007

Fig 1. Assessment of ND in the non–weight-bearing position. Fig 2. Assessment of ND in the weight-bearing position.

distance was remeasured from the floor to the midpoint of For intergroup statistical analysis, the parametric t test the navicular bulge (with remarking if the bulge moved was used for percentage ND test and CE in degrees, NH off under the skin). This measurement determined if the weight bearing (mm), and difference in ND test (weight navicular bulge lowered, and if it did get lower, it was bearing, mm) and CE in degrees. considered to be a flattening of the medial longitudinal arch To date, there is no criterion standard test to diagnose a (Figures 1 and 2).12,32 flatfoot. Demonstration of intertest reliability will provide For measurement of CE, or calliper-based relaxed an enhanced understanding of the interpretability of ND and calcaneal bisection-based eversion, the heel was bisected CE test. To determine if there was an association between with the patient prone using calliper technique, and a line the ND test and CE range of motion, we calculated a was drawn perpendicular to these points6,17,33 Then, a Pearson product-moment correlation coefficient (Pearson r) protractor was used to measure the bisected calcaneus in and a coefficient of determination (r2). comparison to 08. Total degrees were noted for each foot.33 Several different criteria have been reported in the literature to define a flatfoot from ND, ranging from greater than 3- to RESULTS 10-mm drop. We assessed the association between flatfeet Subject Characteristics and MLBP using each of these definitions (N3-, N8-, or N10-mmND).Wealsoassessedtheassociationof Of the 58 subjects (30 with MLBP and 28 with no MLBP) flatfeet and MLBP, defining a flatfoot as one with greater who agreed to participate in this study, 55% (n = 32) were than 68 CE.19-34 female and 45% (n = 26) were male, and the mean age was 44 years. No statistically significant differences were evident between the MLBP and control groups. The overall preva- Outcome Measures lence of flatfeet in the study sample ranged from 13.8% to There were 6 outcome measures: (1) initial NH measure- 87.9% right foot, 19.0% to 87.9% left foot, and 5.2% to ments both seated and weight bearing, (2) ND test (weight 79.3% bilateral depending on the criterion used to define a bearing), (3) percentage ND test (weight bearing), (4) flatfoot (ND N10, N8, or N3 mm, or CE N68). Not surprisingly, degree of CE (weight-bearing range of motion), (5) differ- the highest percentage of subjects were classified as having a ence in ND test and CE bilaterally, and (6) CE correlated to flatfoot when the ND greater than 3-mm criterion was used percentage ND test. (87.9% right, 87.9% left, and 79.3% bilateral).

Analysis v2, Fisher Exact Tests, Likelihood Ratios, and Associated Correlations a was set at .05 at a 95% confidence level. To determine The proportion of subjects in each group with a flatfoot if ND greater than 3, 8, and 10 mm, and CE greater than 68 varied by the definition used. For instance, using the greater could be considered a risk factor for MLBP, we calculated than 8-mm ND criterion to define a flatfoot, 25% of those v2 for each definition of flatfoot. Some definitions of without MLBP had a flatfoot on the right, whereas 37% of flatfoot resulted in too few observations of flatfeet (eg, those with MLBP were categorized as flat-footed on the N10 mm ND), violating v2 assumptions. Therefore, Fisher right. Similarly, using the definition of greater than 8-mm exact test and likelihood ratios were included. Parametric ND, 32% without MLBP and 40% of those with MLBP had t tests, Pearson r (correlation coefficient), and the coef- a flatfoot on the left. Using this definition to classify ficient of determination (r2) were performed to determine subjects into categories of flatfeet or normal arch, there was association between groups. Power was calculated at 0.80. no statistically significant association between the presence Journal of Manipulative and Physiological Therapeutics Brantingham et al 383 Volume 30, Number 5 Foot Position and Low Back Pain

Table 1. Results of v2 analysis

Total No MLBP (n = 28), n (%) MLBP (n = 30), n (%) v2 statistic P

Right foot ND N10 mm 12 6 (21.4) 6 (20.0) 0.018 .893 ND N8 mm 15 7 (25.0) 8 (27.7) 0.921 .337 ND N3 mm 51 26 (92.9) 25 (83.3) 1.28 .241 CE N68 11 4 (14.3) 7 (23.3) 0.771 .390

Left foot ND N10 mm 13 7 (25.0) 6 (20.0) 0.208 .648 ND N8 mm 17 9 (32.1) 8 (27.7) 0.387 .534 ND N3 mm 51 24 (85.7) 27 (90.0) 0.251 .460 CE N68 8 4 (14.3) 4 (13.3) 0.011 .916 There was no statistically significant increased risk ( P V .05, increased risk) between the presence of a flatfoot and MLBP.

Table 2. Symmetry of feet

Right flatfoot

Left flatfoot Absent % (of total sample) Present % (of total sample) P

ND N10 mm Absent 70.7 8.6 .000 Present 6.9 13.8 ND N8 mm Absent 55.2 13.8 .000 Present 8.6 22.4 ND N3 mm Absent 3.4 8.6 .196 Present 8.6 79.3 CE N68 Absent 72.4 8.6 .167 Present 13.8 5.2

Discordant pairs represent the respective proportions of subjects with unilateral flatfoot (asymmetry). of a flatfoot and MLBP (v2 = 0.387 left, 0.337 right; P N.05). independent t tests ranging from P = .20 to P = .774) further These findings were consistent across the 4 different supporting v2 results. definitions: ND greater than 3, 8, and 10 mm, and CE There was evidence of fair to good intertest reliability greater than 68 (Table 1). The 3-mm ND cutoff reflects between ND and CE. With Pearson correlation coefficient (r) nonpublished guidelines. However, this cutoff is sometimes and coefficient of determination (r2), increasing CE corre- used in clinical practice as a criterion to recommend the use lated with increasing ND ( P V .0001), supporting the of arch support through foot orthotics.14 commonly held assumption that CE and ND are likely to Although some asymmetry (presence of unilateral flat- occur together in the flatfoot (Table 3). This was further foot in an individual subject) was suggested in groups with supported by percentage intertest reliability (Table 4).12 v2 8- and 10-mm NDs, the overall comparison between left and analysis supported this association between flatfeet as defined right feet for both groups showed that one foot was not in the literature as ND of either greater than 8- and/or 10-mm significantly flatter than the other (v2 = 2.043, P = .153). ND correlated with greater than 68 CE. Power was generally Although the v2 assumption of 5 observations per cell was low (b0.80.) violated, likelihood ratios and Fisher exact tests ( P = .196) support the findings calculated with v2.34 Comparing flat- footedness by different definitions (Table 2) showed that DISCUSSION asymmetry was limited. Measurement approaches, current at the time of this study, were standardized and practiced by an experienced Parametric t Tests, Pearson r (Correlation Coefficient), Coefficient of podiatrist before the trial.31 No unblinding of subjects Determination (r2) occurred. In addition, it is posited that measurement Regarding the parametric t tests, there was no significant reliability was more robust secondary to using initial difference or correlation between groups in all measures: resting NH, rather than subtalar neutral position (followed initial NH off weight bearing, mm ND, % ND, CE, by full weight-bearing ND) as the first and higher asymmetry in ND, or asymmetry in CE ( P N .05 with measurement.12 Navicular height by ruler is reliable and 384 Brantingham et al Journal of Manipulative and Physiological Therapeutics Foot Position and Low Back Pain June 2007

Table 3. Pearson correlation coefficient (r) and coefficient of Table 4. Intertest reliability between ND and CE determination (r2) CE N68, % agreement Variables P4 rr2 Â 100% Right foot Left % ND-left % CE .000 0.451a 20% ND N10 mm 74.1 Right % ND-right %CE .000 0.626b 39% ND N8 mm 70.7 N a Fair to moderate relationship. ND 3mm N b Moderate to good relationship. CE 68 4 P value was considered statistically significant at P V .05. Left foot ND N10 mm 84.4 significantly correlated with NH obtained by radiography ND N8 mm 74.1 (r = 0.792, P b .01).12 Neither this nor any other previously ND N3mm N published study has shown increased ND greater than 8 or CE 68 10 mm or CE greater than 68 as significant risk factors in Percentage agreement is the number of feet categorized by both tests as MLBP.16,18 This study showed no statistically significant either flatfoot or normal arch divided by the total number of subjects. For differences between subjects with and without MLBP in example, when assessing the agreement between flatfoot defined as ND N8 mm and CE N68 for the right foot, 35 subjects were categorized as terms of ND, degrees of CE, or asymmetry of foot having a normal arch by both tests, and 6 subjects were categorized as alignment within or between groups (supported by compar- having a flatfoot by both measures. The agreement was 70.7% for the ison of percentage symmetry and intertest reliability). 58 subjects. Nevertheless, regarding asymmetry, we did not measure and correlate actual pelvic height with ND or CE; thus, no conclusions should be drawn regarding these particular data in clinical practice. There was a statistically significant at this time. association between CE and ND as defined in the literature N N Although small sample size (n = 58) and low power (with ND 10 and 8 mm), but not between CE and flatfeet, N (power b0.80; range, 0.20-0.774) suggest the possibility of a as sometimes used in clinical practice (ND 3 mm). type II error, these findings should not be discounted Defining greater than 3-mm ND as a risk factor increases because of previous similar and supportive research.16,18 the number of subjects with flatfeet up to 87.9% in our Consideration of these findings may help in clinician sample; however, we were not able to show an association decision making. with either CE or MLBP. Future research may help us to This research should be repeated with a larger sample better understand the relevance of this criterion. size (particularly using as a risk factor the often cited N10 mm ND) and repeated with different and developing measurement techniques such as the arch index, foot posture CONCLUSIONS index, and navicular drift. Subjects with more episodes and In this study, flatfeet did not appear to be a risk factor in greater chronicity of MLBP should also be included.15 subjects with multiple episodes (z2) of MLBP ( P N .05). Future analyses should assess risk for and association with No statistically significant difference in ND or CE between MLBP controlling for these indices.12,35,36 subjects with and without MLBP was detected ( P N .05). In Interestingly, there are now similar questions as to why addition, asymmetry (or unilateral flatfoot) may be of less foot orthotics dispensed for foot, knee, or lower extremity etiologic significance in causation or aggravation of MLBP disorders relieve pain (as they may for MLBP), with than previously believed, but further larger studies are researchers postulating that (in addition to lifting a flatfoot) required to evaluate this definitively. Finally, because of the pain-relieving effects may occur through altered sensory small sample size and power, broader age range, and lesser information, proprioception, and gait.37 Flatfeet (or severe back pain severity, these data remain tentative. These flatfeet), in association with other risk factors (knee or hip preliminary research findings suggest the need for further osteoarthritis, athletic activity, age, etc), may combine to in- research to determine the role and/or risk factor flatfeet play crease overall risk for development of LBP, but such speculation as an etiology or aggravator in causation and perpetuation requires further research. Prospective longitudinal studies using of MLBP. an odds ratio to determine flatfeet as a risk factor in MLBP should be included in future statistical analyses.38 Further research is also needed to assess the sensitivity Practical Applications and specificity of the different methods for assessing the ! In this preliminary study, flatfeet were not integrity of the arch and classifying the foot as flat. In this more common in mechanical patients with study, we used 2 different tests to assess arch integrity (ND MLBP. and CE) and 4 different classification methods cited in the literature (ND N10, N8, and N3 mm, and CE N68) and used Journal of Manipulative and Physiological Therapeutics Brantingham et al 385 Volume 30, Number 5 Foot Position and Low Back Pain

values in children and adults. J Am Podiatr Med Assoc ACKNOWLEDGMENT 1999;89:258-64. This research dissertation was designed, funded, and 18. Roncarati A, McMullen W. Correlates of low back pain in a completed as part of a Masters in Science (chiropractic) general population sample: a multidisciplinary perspective. degree for Dr Adams in the Institute of Health and Medical J Manipulative Physiol Ther 1988;11:158-64. 19. Magee D. Orthopedic physical assessment. 3rd ed. Phila- Sciences, University of Surrey. We thank Dr Richard Frost delphia7 W.B. Saunders Company; 1997. p. 636-8. for his contribution as the podiatrist, Dr Cheryl Hawk for 20. Souza TA. Differential diagnosis and management for the her suggestions for revision, and Dr Jennifer Price for her chiropractor, 2nd ed. Gaithersburg, MD7 Maryland Aspen assistance with editing and revision of the manuscript. Publishers; 2001. p. 47-8. 21. Weiner-Ogilvie S, Rome K. The reliability of three techniques for measuring foot position. J Am Podiatr Med Assoc 1998; 88:381-6. REFERENCES 22. Mueller M, Host JV, Norton BJ. Navicular drop as a composite 1. Kent PM, Keating JL. The epidemiology of low back pain in measure of excessive pronation. J Am Podiatr Med Assoc primary care. Chiropr Osteopat 2005;13:13. 1993;83:198-202. 2. Hansson TH, Hansson EK. The effects of common medical 23. Beckett ME, Massie DL, Bowers KD, Stoll DA. Incidence of interventions on pain, back function, and work resumption in hyperpronation in the ACL injured knee: a clinical perspective. patients with chronic low back pain: a prospective 2-year J Athl Train 1992;27:58-62. cohort study in six countries. Spine 2000;25:3055-64. 24. Loudon J, Jenkins W, Loudon K. The relationship between 3. Assendelft WJ, Morton SC, Yu EI, Suttorp MJ, Shekelle PG. static posture and ACL injury in female athletes. J Orthop Spinal manipulative therapy for low back pain. Cochrane Sports Phys Ther 1996;24:91-7. Database Syst Rev 2004;CD000447. 25. Woodford-Rogers B, Cyphert L, Denegar CR. Risk factors for 4. Saidoff D, McDonough A. Critical pathways in therapeutic anterior cruciate ligament injury in high school and college intervention. Extremities and spine. St Louis, MI7 Mosby, Inc., athletes. J Athl Train 1994;29:343-6. 2002. p. 871-1097. 26. Menz HB, Munteanu SE. Validity of 3 clinical techniques 5. Haldeman S. Principles and practice of chiropractic. 3 ed. New York: for the measurement of static foot posture in older people. McGraw-Hill Medical; 2005. p. 473-5, 911-49, J Orthop Sports Phys Ther 2006;36:179. 6. Michaud T. Foot orthoses and other forms of conservative foot care. 27. Lamm B, Mendicino R, Catanzariti A, Hillstrom H. 2nd ed: Thomas Michaud; 1997. p 56-70, 89, 114-17 Static rear foot alignment: a comparison of clinical and 7. Dananberg HJ, Guiliano M. Chronic low-back pain and its radiographic measures. J Am Podiatr Med Assoc 2005; response to custom-made foot orthoses. J Am Podiatr Med 95:26-33. Assoc 1999;89:109-17. 28. LaPointe S, Peebles C, Nakra A, Hillstrom H. The reliability 8. Brantingham J, Wood T, Parkin-Smith G, Van der Muelen A, of clinical and caliper-based calcaneal bisection measure- Weston P. The inter-examiner reliability of the circumduction ments. J Am Podiatr Med Assoc 2001;91:121-6. test for general foot mobility/joint dysfunction. J Am Chiropr 29. Sell K, Verity T, Worrell T, Pease B, Wigglesworth J. Two Assoc 2003;40:32-9. measurement techniques for assessing subtalar joint posi- 9. Ridola C, Palma A, Cappello F, et al. Symmetry of healthy tion: a reliability study. J Orthop Sports Phys Ther 1994; adult feet: role of orthostatic footprint at computerized 19:162-7. baropodometry and of digital formula. Ital J Anat Embryol 30. Picciano AM, Rowlands MS, Worrell T. Reliability of 2001;106:99-112. open and closed kinetic chain subtalar joint neutral positions 10. Sforza C, Michielon G, Fragnito N, Ferrario VF. Foot and navicular drop test. J Orthop Sports Phys Ther 1993;18: asymmetry in healthy adults: elliptic Fourier analysis of 553-8. standardized footprints. J Orthop Res 1998;758-65. 31. Cowan D, Robinson J, Jones B, Polly D, Berrey H. 11. Larsen K, Weidich F, Leboeuf-Yde C. Can custom-made Consistency of visual assessments of arch height among biomechanic shoe orthoses prevent problems in the back and clinicians. Foot Ankle Int 1994;15:213. lower extremities? A randomized, controlled intervention trial 32. Vinicombe A, Raspovic A, Menz HB. Reliability of navicular of 146 military conscripts. J Manipulative Physiol Ther 2002; displacement measurement as a clinical indicator of foot 25:326-31. posture. J Am Podiatr Med Assoc 2001;91:262-8. 12. Menz HB, Munteanu SE. Validity of 3 clinical techniques for 33. Lorimer D, French G, O’Donnell M, Burrow JG. Neale’s the measurement of static foot posture in older people. J common foot disorders diagnosis and management, 6th ed Orthop Sports Phys Ther 2005;35:479-86. New York7 Churchill Livingstone; 2002. p. 128-31. 13. Manek NJ, MacGregor AJ. Epidemiology of back disorders: 34. Haneline M. Evidence-based chiropractic practice. Sudbury, prevalence, risk factors, and prognosis. Curr Opin Rheumatol Massachusetts7 Jones and Bartlett Publishers, Inc; 2007. 2005;17:134-40. p. 131-5. 14. Postural stability indicator ADPS-0206. Roanoke7 Foot Lev- 35. Menz HB. Alternative techniques for the clinical assessment of elers, Inc; 2006. foot pronation. J Am Podiatr Med Assoc 1998;88:119-29. 15. Shrader JA, Popovich JM, Gracey GC, Danoff JV. Navicular 36. Portney L, Watkins P. Foundations of clinical research: drop measurement in people with rheumatoid arthritis: applications to practice, 2nd ed New Jersey7 Prentice-Hall; interrater and intrarater reliability. Phys Ther 2005;85:656-64. 2000. p. 317-37. 16. Brantingham JW, Gilbert J, Shaik J, Globe G. Sagittal plane 37. Hertel J, Sloss BR, Earl JE. Effect of foot orthotics on quadriceps blockage of the foot, ankle and hallux and foot alignment— and gluteus medius electromyographic activity during selected prevalence and association with low back pain. J Chiropr Med exercises. Arch Phys Med Rehabil 2005;86:26-30. 2006;5:123-7. 38. Domholdt E. Physical therapy research: principles and 17. Sobel E, Levitz S, Casell MA, et al. Reevaluation of the applications, 2nd ed. Philiadelphia7 WB Saunders Company, relaxed calcaneal stance position. Reliability and normal 2000. p. 179-80. INTEREXAMINER RELIABILITY AND ACCURACY OF POSTERIOR SUPERIOR ILIAC SPINE AND ILIAC CREST PALPATION FOR SPINAL LEVEL ESTIMATIONS

Hye Won Kim, MD, PhD, Young Jin Ko, MD, PhD, Won Ihl Rhee, MD, PhD, Jung Soo Lee, MD, Ji Eun Lim, MD, Sang Jee Lee, MD, Sun Im, MD, and Jong In Lee, MD, PhD

ABSTRACT

Objective: The purpose of this study was to compare the posterior superior iliac spine (PSIS) and the iliac crest as accurate anatomical landmarks for identifying spinal level. Methods: This study was conducted in 2 stages. First, 4 examiners examined 60 patients and blindly identified iliac crest and PSIS levels, and the interexaminer reliability of PSIS and iliac crest palpation were then analyzed. Second, 4 examiners attached a radio opaque marker at presumed PSIS and iliac crest levels in 72 patients, and posteroanterior lumbar radiographs were then taken. Four examiners then confirmed PSIS and iliac crest levels after radiographically identifying the marker levels and checked the spinal level at which the spinous process or interspace was crossed by drawing a horizontal line drawn between radio opaque markers. Results: The interexaminer reliability of palpation was significantly greater for PSIS level than for the iliac crest ( P b .05). Spinal levels of estimated PSISs identified by palpation ranged from the L5-S1 interspace to the S2 spinous process, and the spinal levels of estimated iliac crest ranged from the L2-3 interspace to the L5 spinous process. Conclusions: Although PSIS palpation showed statistically higher interexaminer reliability than iliac crest level, clinicians should be cautious when applying this method as a measurement tool because estimated spinal level by palpation can be influenced inadvertently by examiner skill and anatomical variations. (J Manipulative Physiol Ther 2007;30:386-389) Key Indexing Terms: Spine; Reproducibility of Results; Palpation

he accurate identification of spinal level is a between the palpated points by different examiners, and prerequisite for the success and safety of spinal accuracy means the extent of concordance between the T procedures, such as epidural block, cerebrospinal palpated point by an examiner and the anatomical location fluid tapping, electromyographic examination, and manip- confirmed by x-ray. Tuffier’s line (defined by drawing a ulative and physiologic therapeutics. The detection of spinal horizontal line across the highest points of the iliac crests) is levels by x-ray examination is more accurate than the now the most widely used anatomical landmark during palpation of surface anatomical landmarks, but in the lumbar spine surface palpation and has been proven to outpatient setting, it is difficult to order radiologic exami- correlate with the L4-5 interspace or L4 spinous process.1 nations on a routine basis, and thus, there is a need for an However, this technique has its limitations because, accurate, reliable, and easy clinical method for identifying although Tuffier’s line crosses the spinal level with a spinal level. Reliability means the extent of concordance maximal incidence at the L4 spinous process, this varies from the L5-S1 interspace to the L3-4 interspace.1 This method is also limited by the technical difficulty associated with manually palpating the iliac crest.2,3 Department of Rehabilitation Medicine, College of Medicine, In electromyographic examinations, the posterior supe- The Catholic University of Korea, Korea. rior iliac spine (PSIS) is often used as an anatomical Submit requests for reprints to: Jong In Lee, MD, PhD, 4 Department of Rehabilitation Medicine, College of Medicine, landmark to estimate spinal level. The spinal level of the The Catholic University of Korea, 505 Banpo-Dong, Seocho-Gu, PSIS is known to be at the midpoint between S1 and S2 Seoul 137-701, Korea (e-mail: [email protected]). foramen by cadaver study.5,6 However, formal clinical Paper submitted October 24, 2006; in revised form January 24, studies have yet to be carried out to ascertain its reliability 2007; accepted February 20, 2007. 0161-4754/$32.00 as a surface marker for determining spinal level. Copyright D 2007 by National University Health Sciences. The 2 main objectives of this study were to determine doi:10.1016/j.jmpt.2007.04.005 which of these 2 anatomical landmarks is more statistically

386 Journal of Manipulative and Physiological Therapeutics Kim et al 387 Volume 30, Number 5 Interexaminer Reliability of the PSIS

Fig 1. Method of measurement by manual palpation. A and B, Fig 2. Method of measurement on x-ray. A and B, estimated upper upper margin of iliac crest. C and D, Posterior superior iliac margin of iliac crest. C and D, estimated PSIS. E and F, real upper spine. a, midpoint of A-B. b, midpoint of both dimple (C-D). margin of iliac crest. reliable and accurate for palpation purposes, and to second examiner as aV and bV. Four other examiners with determine whether PSIS palpation predicts spinal level in no prior information concerning this study or of the a uniform manner. volunteer distribution recorded the location of the cross points. The examiners were unaware of each other’s results, and all data were kept confidential until the end METHODS of the study (Fig 1). After approval by the research ethics committee of the College of Medicine, The Catholic University of Korea, Spinal Level Estimation With Radio Opaque Markers Seoul, Korea, patients were enrolled in this study after To avoid data being influenced by variations due to providing written informed consent. examiners’ personal styles, we divided 72 volunteers randomly into 4 groups, and they were examined by one Interexaminer Reliability of Palpation of the examiners. Volunteers with a spinal operation history, Four examiners with at least 3 years of clinical lumbarization of sacral vertebrae, or sacralization of lumbar experience in musculoskeletal medicine were divided into vertebra were excluded, as were those with a lumbar area 2 separate groups. Sixty volunteers were randomly divided that was too painful to allow easy examination by palpation into 2 groups each with 30 volunteers, and 2 examiners or with marked lumbar spinal deformity. performed the palpation. Any volunteer with a lumbar area With the volunteer in the same prone position as in the that was too painful to allow examination by palpation or previous group, examiners palpated both iliac crests (A who had undergone previous spinal surgery was excluded and B) and PSIS (C and D), and attached radio opaque from this study. Volunteers were placed in a prone position, markers to these points. Lumbar anteroposterior view and a pillow was placed below the abdomen to allow back radiographs were obtained, with the x-ray source placed muscle relaxation. A 100-cm ruler was then attached to the 40 in away from the patient. All the examiners were vertebral midline as a reference line. unaware of each other’s observations and were not Two examiners from each group then separately allowed to view any of the lumbar x-ray images or to identified the estimated level of the PSIS (C, D) and iliac be reeducated until the completion of this study. Four crest (A, B) for both right and left side of each volunteer other examiners marked the level at which the spinous by manual palpation, marked the level, and connected both process or interspace was crossed by drawing a horizontal sides of the PSIS (C, D) and iliac crest (A, B) by a straight line drawn between radio opaque markers and then transverse line. The most upper part of the iliac crest was radiographically confirmed the level of the iliac crest (E palpated, and the most prominent and superficial part of and F) (Fig 2). the PSIS from the skin was palpated. The points where To avoid uncertainty due to abnormal sacralization, these lines intersected the 100-cm ruler were identified (a spinal levels were counted down from the most caudal for the iliac crest and b for the PSIS). Crossing points for thoracic vertebra, which was confirmed by rib position on the first examiner were defined as a and b, and for the lumbar x-ray.1,7 388 Kim et al Journal of Manipulative and Physiological Therapeutics Interexaminer Reliability of the PSIS June 2007

Table 1. Patient characteristics

Group 1 (n = 60) Group 2 (n = 72)

Male (30) Female (30) Male (19) Female (53)

Age (y) 26.6 (6.3) [19-46] 39.2 (15.6) [20-63] 25.4 (6.5) [20-38] 36.2 (11.6) [20-68] Body mass index (kg mÀ2) 23.9 (3.3) [20.3-31.2] 21.6 (2.6) [17.4-27.0] 21.9 (3.0) [18.5-30.5] 20.9 (2.6) [15.6-27.6] Values are mean (SD) [range]. Group 1, group who underwent surface palpation. Group 2, group who took radiologic examination.

Table 2. Discrepancy values of iliac crest and PSIS estimations by Table 3. Estimated spinal level of the PSIS in 72 patients who surface palpation underwent x-ray examination

Examiner group Level of spine Male Female Total (%)

1 and 2 3 and 4 L5-S1 interspace 10 6 16 (22.2) S1 spinous process 7 24 31 (43.1) Iliac crest (cm) 0.92 F 0.68 0.96 F 0.60 S1-2 interspace 2 20 22 (30.5) PSIS (cm) 0.60 F 0.64 0.59 F 0.55 S2 spinous process 0 3 3 (4.2) P .007 .008 Total 19 53 72 (100) Values are means F SD. Values are number of patients (proportions).

crest was correctly identified in only 26 cases (36%), and Statistics there was no significant difference in accuracy among Data analysis was performed using SPSS version 10.0 the examiners. In most cases, it was determined to be (SPSS Inc, Chicago, Ill). To determine interexaminer at a higher level than the radiologically confirmed reliability of iliac crests and PSIS palpation tests, we level (Table 4). calculated differences between examiner-determined values (ie, between a and aV, and b and bV). The reliability between measures based on iliac crests and PSIS by the 2 examiners DISCUSSION was assessed using the Wilcoxon signed rank test, and the Tuffier’s line has been the most popular and widely data between groups were assessed using the Mann-Whitney used landmark for the rapid identification of spinal level. test. The difference in accuracy of palpating iliac crest However, palpating the upper iliac crests and drawing an between the examiners was analyzed with the v2 test. adjoining line is prone to error and may be an unreliable P values of less than .05 were considered significant, and guide for determining precise spinal level. Therefore, when results are expressed as mean values F SD. the iliac crest is used as an anatomical surface marker to identify accurate spinal levels, clinicians should be aware that this method has its limitations. Moreover, the position RESULTS of Tuffier’s line was found to vary from the L5-S1 The mean age of volunteers who underwent surface interspace to the L3-4 interspace1 because it is difficult to palpation (group 1) was 32.9 years, and the mean age of palpate surface landmarks correctly in all patients. This volunteers who had radiographic examination (group 2) was was also shown by Broadbent et al2 and Furness et al3 33.3 years (Table 1). who identified the spinal level correctly in only 29% and Based on discrepancies between PSIS and iliac crests 30% of cases, respectively, by using the iliac crest as an measurement, the interexaminer reliability of palpation was anatomical landmark. The present study also showed significantly greater for PSIS than for the iliac crest palpation similar results; iliac crest palpation was only accurate in test ( P b .05) (Table 2). There was no significant difference 36% of cases, which indicates its limitation as an accurate between groups ( P N .05) (Table 2). The estimated level of palpation method. PSISs was located between the L5-S1 interspace and the S2 Based on a previous report,8 which showed that the spinous processes, and the most common level was the S1 PSIS method has moderate interexaminer reliability as a spinous process (31 [43%] of 72 cases) (Table 3). The surface marker, the authors suggested that the use of this estimated level of iliac crests was located between the L2-3 anatomical landmark might reduce interexaminer discrep- interspace and the L5 spinous processes. ancy more successfully compared with the use of the iliac Tuffier’s line, which was confirmed radiologically, was crest method. However, as our results show, although the located from as low as the L5-S1 interspace to as high as discrepancy between examiners was smaller for the PSIS the L4 spinous process (Table 4). Of the 72 cases, the iliac method vs the iliac crest method, the PSIS approach itself Journal of Manipulative and Physiological Therapeutics Kim et al 389 Volume 30, Number 5 Interexaminer Reliability of the PSIS

Table 4. Estimated spinal level of iliac crest compared with its mass index of the volunteers failed to reflect the influence radiologically confirmed level in 72 patients who underwent of obesity on surface anatomy palpation. Despite these x-ray examination limitations, this study is of value because it is one of the Radiologically confirmed level of iliac crest first studies to ascertain and compare the reliability of the PSIS and iliac crests as accurate landmarks. In addition, L4 L4-5 L5 L5-S1 the study showed that PSIS would be located at variable points by surface palpation. Estimated level of iliac crest L2-3 interspace 1 L3 spinous process 2 1 CONCLUSION L3-4 interspace 3 1 L4 spinous process 10 20 8 Although interexaminer reliability may be better for PSIS L4-5 interspace 9 91 than iliac crest palpation, discrepancy values between L5 spinous process 7 examiners showed that although useful, PSIS palpation is Correct identification of the spinal level is indicated by underlined type. still prone to substantial inaccuracies in terms of defining exact spinal level. Therefore, although the PSIS palpation also has discrepancies between each examiner and varied test has the potential to be used as an alternative to, or in as much as 2.5 cm in some cases. In addition, although it combination with, other conventional tests, clinicians should was not true PSIS levels based on radiologic findings, the bear in mind that estimated spinal level by palpation could be result from spinal level estimation by palpation showed influenced by examiner skill and anatomical variations. PSIS levels varied from the L5-S1 interspace to the S2 spinous process. Unlike the iliac crest, which can easily be discerned on REFERENCES lumbar x-rays, accurate identification of the PSIS based on 1. Render CA. The reproducibility of the iliac crest as a marker of radiologic findings is technically difficult, which could be lumbar spine level. Anaesthesia 1996;51:1070-1. proposed by a few references,5,9 and palpation of the most 2. Broadbent CR, Maxwell WB, Ferrie R, Wilson DJ, Gawne- prominent and superficial part of the PSIS from the skin is Cain M, Russell R. Ability of anaesthetists to identify a marked lumbar interspace. Anaesthesia 2000;55:1122-6. even more difficult to be located with x-ray. Therefore, it is 3. Furness G, Reilly MP, Kuchi S. An evaluation of ultrasound not possible to measure accuracy of locating the PSIS by imaging for identification of lumbar intervertebral level. palpation, and also, it is impossible to compare accuracy Anaesthesia 2002;57:277-80. between the examiners, which is one of the shortcomings of 4. Haig AJ, Moffaroid M, Henry S, Haugh L, Pope M. A technique this study. Because there was less discrepancy between for needle localization in paraspinal muscles with cadaveric confirmation. Muscle Nerve 1991;14:521-6. examiners locating the PSIS than the iliac crest, and there 5. Rohen JW, Yokochi C. Color atlas of anatomy. 5th ed. was no difference in accuracy of palpating iliac crests Philadelphia7 Lippincott Williams & Wilkins; 2002. p. 423. between the examiners, it could be proposed that there 6. Atlihan D, Bozkurt M, Turanli S, Dogan M, Tekdemir I, might be no difference in the accuracy of palpating the PSIS Elhan A. Anatomy of the posterior iliac crest as a reference between 4 examiners. However, no difference in accuracy to sacral bar insertion. Clin Orthop 2004;418:141-5. 7. Jung CW, Bahk JH, Lee JH, Lim YJ. The tenth rib line as a new does not mean high accuracy, and considering the accuracy landmark of the lumbar vertebral level during spinal block. of locating the iliac crest by palpation was 36% and Anaesthesia 2004;59:359-63. discrepancies between examiners varied as much as 2.5 cm 8. O’Haire C, Gibbons P. Inter-examiner and intra-examiner in some cases, it could suggest that palpating the PSIS with agreement for assessing sacroiliac anatomical landmarks using accuracy might be difficult. palpation and observation: pilot study. Man Ther 2000;5:13-20. 9. Schildhauer TA, McCulloch P, Chapman JR, Mann FA. Another limiting factor of this study is the young age of Anatomic and radiographic considerations for placement of the volunteers and our failure to make comparisons transiliac screws in lumbopelvic fixations. J Spinal Disord Tech between different age groups. Finally, the low mean body 2002;15:199-205. COUPLING BEHAVIOR OF THE THORACIC SPINE: ASYSTEMATIC REVIEW OF THE LITERATURE

Phillip S. Sizer Jr, PT, PhD,a Jean-Michel Brisme´e, PT, ScD,b and Chad Cook, PT, PhD, MBAc

ABSTRACT

Objective: The knowledge of 3-dimensional spine coupling characteristics is important for treating patients with spinal pain. The purpose of this study was to examine the coupling directional pattern of the thoracic spine by systematic review. This review could help determine the use of coupling knowledge for manual therapy treatment. Methods: A systematic review of studies examining in vivo and in vitro thoracic spine coupled motion was conducted using PubMed and Cumulative Index to Nursing and Allied Health Literature searches (1960-2006), as well as a separate hand-search. Study abstracts were independently reviewed and selected by two investigators based on face validity. The reliability between investigators was established using the Kappa (K) coefficient. A third investigator resolved any inclusion disagreement. Full studies were then evaluated for compliance with inclusion criteria. Coupling patterns from accepted studies were then qualitatively compared. Results: Of the 56 citations originally identified in the searches, the first two investigators reached consensus on 41 citations and required further assistance by the third investigator on 15 citations. The reliability between investigators was rated fair (K = 0.38). Twenty-one citations were deemed acceptable for further review. Of 21 citations, 8 met the inclusion criteria and were fully reviewed. No consistent coupling pattern was observed across the 8 studies, where they exhibited ipsilateral, contralateral, or mixed coupling behaviors. Conclusions: Differences in study design, measurement method, and tissue preparation may have contributed to differences between studies. More quality, in vivo investigations are needed to evaluate thoracic coupling in symptomatic subjects in both a flexed and extended position. (J Manipulative Physiol Ther 2007;30:390-399) Key Indexing Terms: Biomechanics; Movement; Spinal Manipulation; Thoracic Vertebrae

he thoracic spine is considered a transitional zone function.1 The combined flexion and extension range of between the cervical and lumbar spine, yet is unique motion in the thoracic spine is bimodal, from the superior to Tbecause of the size and extent of the region and the the inferior segments.2 The upper thoracic spine shows a articulations with the rib cage. The articulations with the rib total of 38 to 58 of flexion or extension that is reduced to 28 cage lead to regional variations in movement patterns and to 78 at T5 to T6 and further increases to 68 to 208 at T12 to L1. Overall, greater range of motion is available in flexion than in extension.2 a Professor & Program Director, ScD Program in Physical Therapy, Director, Clinical Musculoskeletal Research Lab, Center Several anatomical components control or contribute to for Rehabilitation Research, Texas Tech University Health the available movements of the thoracic spine. The Sciences Center, Lubbock, Tex. intervertebral disk plays a major role in movement control b Assistant Professor, ScD Program in Physical Therapy, of the thoracic spine, a much more significant role than the Faculty, Clinical Musculoskeletal Research Lab, Center for posterior structures.3 With respect to height, the disk in the Rehabilitation Research, Department of Rehabilitation Sciences, thoracic spine shows less height in ratio to the vertebral Texas Tech University Health Sciences Center, Lubbock, Tex. 4 c Assistant Professor, Division of Physical Therapy, Department body than the cervical and lumbar spines. In addition, the of Community and Family Medicine, Duke University, Durham, thoracic disk has a relatively small nucleus pulposus.5 There NC. are variations in the orientation of the zygapophyseal joints Submit requests for reprints to: Phillip S. Sizer Jr, PhD, PT, (facets) throughout the length of the thoracic spine. In Professor & Program Director, ScD Program in Physical Therapy, general, the superior facets face anteriorly but are not Director, Clinical Musculoskeletal Research Lab, Center for 6 Rehabilitation Research, Texas Tech University Health Sciences completely aligned in the frontal plane. This angulation is Center, 3601 4th St., Lubbock, TX 79430, USA reduced as the thoracic spine descends, culminating at T12. (e-mail: [email protected]). At T12, the facets show an orientation similar to lumbar Paper submitted December 1, 2006; in revised form spine facet orientation.6 February 23, 2007; accepted February 25, 2007. 0161-4754/$32.00 Movement analysis is considered an essential element of Copyright D 2007 by National University of Health Sciences. clinical examination, including the biomechanical assess- 1 doi:10.1016/j.jmpt.2007.04.009 ment of multiple planes of movement. Germane to the

390 Journal of Manipulative and Physiological Therapeutics Sizer, Brisme´e, and Cook 391 Volume 30, Number 5 Coupling Behavior of the Thoracic Spine

Table 1. Search strategy to identify thoracic spine coupling Table 2. Reasons for abstract rejection during the initial citation manuscripts and abstract review

No. Search history Resultsa No. of citations in 1 Thoracic vertebrae/ or thoracic spine.mp. 12,151 Reasons for abstract rejection this category 2 Limit 1 to English language 9,516 3 Biomechanics.mp. or Biomechanics/ 50,089 Examination of intermuscular coupling 1 4 Limit 3 to English language 42,854 during a lifting task 5 Coupling.mp. 52,580 Examination of limb coupling in spinal cord lesions 1 6 Limit 5 to English language 50,650 Evaluation of 3-D surface anatomy of 1 7 Models, structural/ or three-dimensional.mp. 80,219 thoracic vertebrae 8 Limit 7 to English language 74,069 A pure 3-D geometric structural reconstruction 1 9 Movement.mp. or Movement/ 174,798 Influence of spine morphology on intervertebral 1 10 Limit 9 to English language 155,707 disk loads 11 2 and 4 610 The consequences of anatomical variation on 1 12 8 and 10 3,780 thoracic kyphosis 13 6 or 12 54,348 Assessment of spine structural attributes 1 14 11 and 13 22 Motion analysis after selective cutting 2 a Numbers of citations produced by search. Relationship of leg-length discrepancy and lateral 2 bending motion during gait Influence of lifting on spine mechanics 1 Response to posteroanterior loads applied to 1 concept of biomechanical movements is spinal coupling bio- the spinous processes mechanics. By definition, coupling biomechanics, or General spinal flexibility measure 1 coupled motion, is the rotation or translation of a vertebral Examination of the effects of the rib cage on thoracic 1 spine flexibility body about or along one axis that is consistently associated 7 Assessment of motion limited to pure segmental 1 with the main rotation or translation about another axis. axial rotation During movement, translation occurs when movement is Motion assessment limited to thoracic cage 2 such that all particles in the body at a given time have the translations same direction of motion relative to a fixed coordinate Assessment of rib mechanics 2 7 Evaluation of scoliosis development and progression 6 system. With movement, rotation occurs as a spinning or Modeling study of scoliotic deformities 1 angular displacement of the vertebral body around a Evaluation of the influence of scoliosis on 1 particular axis of rotation. segmental motion Biomechanical coupling is 3-dimensional (3-D) and Assessment was limited to lumbar coupling 3 takes place within 6 degrees of freedom, where the vertebrae Assessment was limited to cervical coupling 1 7 Paper was a commentary 1 can translate along or rotate about each orthogonal axis. No abstract available 2 The 3-D motions in human vertebral segments correspond Total 35 to flexion/extension, rotation and side-bending (lateral flexion) forces; one specific movement initiation (such as side-bending) theoretically activates movement in the other component motions. This coupling behavior is dependent on The purpose of this study was to review the coupling the first motion of initiation (ie, side-bending), the posture directional pattern of the thoracic spine by systematic of the spine, and the pathology of the segment.8 Because the examination of the literature. Examining the consistency movements are 3-D, measurement should incorporate among biomechanical investigations of thoracic coupling appropriate devices that address the multidimensional nature will help determine the utility of its use in manual of movement. Failure in the use of the appropriate examination and treatment of the spine. Within clinical measurement device may lead to errors and inaccuracies practice, the side-bend and axial rotation initiations of associated with coupling biomechanics. movement are used more frequently than flexion/extension In theory, measurement of coupling motion is useful initiation. Because of the clinical relevance and the lack of to diagnose pathological disorders, such as clinical instability representation in the literature of flexion/extension initia- due to degeneration, disease, or trauma.9,10 It has been sug- tion, only coupling studies associated with initiation of gested that an advanced understanding of spine coupling side-bend and/or axial rotation initiation are investigated biomechanics and kinesiology will result in better compre- within this review. hension of symptoms manifestation and pathogenesis of spinal dysfunction.11-16 If pathological coupling patterns exist, manual therapy practitioners could logically intervene METHODS and appropriately incorporate those movements to improve Language patient outcomes. Studies written in the English language were reviewed. 392 Sizer, Brisme´e, and Cook Journal of Manipulative and Physiological Therapeutics Coupling Behavior of the Thoracic Spine June 2007

Table 3. Description of included studies, including specimen, number of subjects/specimens, status of surrounding tissues, and method for acquiring data

Tissue preparation Author Specimen N Age (y) (if applicable) Ribs and costal joints Data acquisition method

Panjabi, 197618 In vitro 2 females 19-59 Fresh frozen; disk, Ribs in place and CTJ Load cell measures human and 3 males ligaments, and joints and CVJ intact acted upon rigid arms intact. All nonligamentous attached to the cranial tissue removed from the vertebra segment Oxland et al, In vitro 5 females 19-70 Fresh frozen; all Ribs, CTJs, and CVJs Stereoradiophotogram- 199219 human and 3 males nonligamentous dissected metric motion recording tissue removed from the segment Willems et al, In vivo 30 females 18-24 All tissues intact Ribs in place and CTJ 3-Space Fastrak System 19961 human and 30 males and CVJ intact Gregersen and In vivo 7 males 20-26 Steinmann pins Ribs in place and CTJ Pin displacement was Lucas, 196720 human embedded into the and CVJ intact transmitted through a spinous processes flexible extension arm to a relative rotation transducer Stewart et al, In vivo 20 females 18-22 All tissues intact Ribs in place and CTJ 3-Space Fastrak System 199521 human and CVJ intact Theodoridis In vivo 25 females 45-64 All tissues intact Ribs in place and CTJ Electromagnetic and Ruston, human and CVJ intact Tracking System 200222 Schultz et al, Mathematical NR NR Disk, ligaments, and Ribs not represented Mathematical model 197323 model transverse processes with computer program were represented analysis in the model Scholten and Mathematical NA NA Disk, ligaments, and Ribs not represented Mathematical model Veldhuizen, model transverse processes were with computer program 198524 represented in the model analysis CTJ, costotransverse joint; CVJ, costovertebral joint; NR, not reported; NA, not applicable.

Inclusion Criteria articles references from those studies collected in the Studies that investigated in vivo (live subjects), in vitro computer-based search and those known to the authors (cadaveric specimens), or modeled (mathematical modeling) was conducted. thoracic spine coupled motion were selected. For inclusion, each study required an experimental analysis for detection of 3-D coupled movements. A report of coupled movement Methods of Review direction was required for inclusion. In addition, the Study abstracts were independently reviewed, and investigators observed for a report of side-bend initiation citations were selected by two authors (P. S. and C. C.) or rotation initiation when evaluating the coupled move- based on face validity. A binary decision (yes vs no) was ments. The analysis did not consider textbook references that used to determine if each citation was suitable for inclusion referred to thoracic spine coupling because the likelihood based on the study’s apparent compliance with the that the reported thoracic coupling patterns were established previously discussed inclusion criteria. Investigators’ pre- through experimental measures was questionable. liminary decisions regarding the suitability for each study’s inclusion were compared, and the reliability between investigators was established using the Kappa (K) coef- Search Strategy for Selection of Studies ficient. Citations that reached consensus between investi- The present study selection strategy was initiated through gators were deemed suitable for inclusion and further the computer-based search engines of PubMed and Cumu- review. For those citations where the two investigators lative Index to Nursing and Allied Health Literature disagreed, a third investigator (J. M. B.) reviewed the (February 1965-November 2006). The search strategy is abstracts for suitability, thus making a tie-breaking decision outlined in Table 1. Each search included the search terms of for those specific citations. Once deemed suitable, the full bthoracic vertebrae or thoracic spine,Qbbiomechanics,Q text of each study was further evaluated to determine if the bcoupling,Qbthree-dimensionalQ or bmodels, structural,Q and study, in fact, met the inclusion criteria and could be bmovement.Q Furthermore, a comprehensive hand-search of all included as a part of the systematic review. Once included, oue3,Nme 5 Therapeutics Number 30, Physiological Volume and Manipulative of Journal Table 4. Composite quality scoring for study compliance with quality standards

Study Total no. of studies complying with a standard Percentage of studies Oxland Willems Gregersen Stewart Theodoridis Schultz Scholten and complying Panjabi, et al, et al, and Lucas, et al, and Ruston, et al, Veldhuizen, with Quality standard 197618 199219 19961 196720 199521 200222 197323 198524 Y totals N totals NA totals standards

Specimens 1. Study specimens or subject Y N Y Y Y Y NA NA 5 1 2 62.5 pathology or status is adequately described 2. Study specimen or subject Y Y Y Y Y Y NA NA 6 0 2 75.0 preparation is adequate 3. Study performed with intact Y Y Y Y Y Y Y(1) Y(1) 8 0 0 100.0 articular tissue (ligaments, capsule, cartilage, disk) 4. Study performed with N N Y Y Y Y N(2) N(2) 4 4 0 50.0 intact adjacent soft tissue (muscle, tendon, fascia) 5. Study is performed without rib Y N Y Y Y Y N(2) N(2) 5 3 0 62.5 structures intact (rib, CVJ, CTJ) Methods 6. Setup is adequately described Y Y Y Y Y Y Y Y 8 0 0 100.0 and reproducible 7. Study identifies the use of 3-D Y Y Y Y Y Y Y Y 8 0 0 100.0 measures of assessment 8. Study identifies single spinal Y Y N Y N Y Y Y 6 2 0 75.0 level of assessment (not multiple levels) 9. Study outlines movement Y Y Y Y Y Y Y Y 8 0 0 100.0 initiation for each measure 10. Study defines a bdirectional Y Y Y Y Y Y Y Y 8 0 0 100.0 coupling patternQ using the Cartesian system Analysis 11. Data variance is reported (eg, N Y Y N Y Y N N 4 4 0 50.0 SD or SEM) 12. Reliability measures are reported N N N N Y Y N N 2 6 0 25.0 when appropriate 13. Experimental error is reported N N Y Y Y Y N N 4 4 0 50.0

14. Study reported instrumentation N NA Y Y Y Y N N 4 3 1 50.0 Spine Thoracic the of Behavior Coupling errors lower than the actual movement measured Application 15. Reported movements are N Y Y Y Y Y N N 5 3 0 62.5 reproducible as clinically ie,Brisme Sizer, important values 16. Study outlines limitations on Y Y Y Y Y Y Y Y 8 0 0 100.0 experimental design Yes grand totals (out of a total of 16 standards) 10 10 14 14 15 16 7 7 Composite quality score (% of total) 62.5 62.5 87.5 87.5 93.8 100 43.8 43.8 Cook and ´e,

Y indicates no; Y, yes; NA, not applicable. (1) Computer model did not include joint capsule. (2) Computer model did not include these tissues. 393 394 Sizer, Brisme´e, and Cook Journal of Manipulative and Physiological Therapeutics Coupling Behavior of the Thoracic Spine June 2007

the reported coupling behaviors of the thoracic spine from segments T1-T2 through T11-T12 during movements while each study were qualitatively evaluated and compared. loads were exerted on rigid arms attached to the cranial-most To further analyze the quality of each study, the vertebra. Similarly, Oxland et al19 evaluated 5 fresh frozen investigators methodologically scored each of the 8 articles cadaveric specimens in a similar age range. However, unlike reviewed. This analysis was based on 16 quality standards Panjabi et al,18 all nonligamentous tissues were dissected, that described the quality of the specimens or subjects, the along with all costal structures. Moreover, this study specifics regarding methodology, the analysis that was documented the coupling behaviors only at T11-T12 and incorporated, and the clinical application of the findings. T12-L1 through a stereophotogrammetric motion recording. The investigators established the percentage of studies that Four studies examined in vivo human coupling behaviors complied with each quality standard. Moreover, a Compo- (Table 3).1,20-22 Willems et al1 evaluated 30 male and 30 site Quality Score was established for each study reflecting female young adult in vivo human subjects, measuring the study’s compliance with the quality standards. This coupling behaviors during active spine movements using a score reflected the total number of standards with which the 3-Space Fastrak system. Gregersen and Lucas20 evaluated study complied, based on a Yes (Y)-No (N) binary decision. coupling behaviors by observing the rotational displacement of Steinmann pins that had been embedded into the subjects’ spinous processes at T1 through L1. Stewart et al21 and Theodoridis and Ruston22 used electromagnetic tracking RESULTS systems to examine thoracic coupling that was initiated The PubMed and Cumulative Index to Nursing and Allied through upper extremity elevation in 20 and 25 female Health Literature searches identified 22 citations and subjects, respectively. Finally, Schultz et al23 and Scholten abstracts using the combined keywords of bthoracic spine,Q and Veldhuizen24 reported coupling behaviors established bthoracic vertebrae,Qbbiomechanics,Qbcoupling,Qbthree- through mathematical modeling. In both studies, the disk, dimensional,Q and bmovementQ (Table 1). A hand-search ligament, and bony processes were represented in the model, identified 34 additional citations and abstracts that were omitting rib mechanism representation from the mathemat- obtained for initial review, creating a total of 56 studies. Of ical analysis. the 56 studies identified in the searches, the first two Composite Quality Scores were established for each investigators (P. S. and C. C.) reached consensus on 41 study to analyze the quality of each study (Table 4). All 8 studies and required further assistance by the third independ- studies reflected intact articular tissue (standard 3), adequate ent investigator on 15 studies. Of the 41 studies reaching description of the investigation setup (standard 6), identi- consensus, the two investigators agreed that 10 studies were fication of a 3-D measure (standard 7), description of acceptable for inclusion (ie, for further review) in the study. movement initiation (standard 9), directional coupling Conversely, 31 studies were deemed unacceptable for further patterns (standard 10), and limits to the study (standard review. Initial citation and abstract review produced a fair 16). Only two studies (Stewart et al21 and Theodoris and intertester reliability for study inclusion between the two Ruston22) reported measures of reliability (standard 12). investigators (K = 0.38).17 The third investigator was Theodoris and Ruston22 showed the highest Composite employed to evaluate 15 studies, of which 11 were deemed Quality Score (100%), complying with all of the 16 quality acceptable and 4 were deemed unacceptable for further standards. Stewart et al21 complied with 15 of the standards evaluation. Table 2 reflects the reasons for abstract rejection. (93.8%), where they only failed to evaluate single segmental The 21 articles that were deemed acceptable by the levels (standard 8). Studies of Shultz et al23 and Scholten distillation process were obtained for review. Of the 21 and Veldhuizen24 each complied with only 7 of the 16 articles, 12 did not define a directional coupling pattern and standards, producing the lowest Composite Quality Scores. did not qualify. One study met the coupling criteria but was Six studies qualified as 3-D analyses of coupling motion conducted on canine cadaveric specimens and was therefore with rotation initiation (Table 5). Coupling behaviors in disqualified. Upon completion of the review, 8 articles were response to rotation initiation varied both between and identified as plausible investigatory analyses of coupling within the previously described studies. Panjabi et al18 motion of the thoracic spine (Table 3).1,18-24 Six of the reported that all segments side-bend (lateral flexion)- articles used thoracic motion initiation (either rotation or coupled in the same direction as the rotation when the side-bend),1,18-20,23,24 whereas two used upper extremity segments were passively rotated to the left, whereas the elevation to initiate the coupling behaviors.21,22 same segments side-bend-coupled left when the segments Two of evaluated studies reported the use of in vitro were passively rotated right. Conversely, Oxland et al19 specimens for analysis (Table 3).18,19 Panjabi et al18 reported side-bend coupling to the same direction as rotation evaluated 5 fresh frozen cadaveric specimens where the when performed to the left or right rotation at the two most majority of segmental support structures remained intact, caudal thoracic motion segments. Similarly, Schultz et al23 including the ribs, costovertebral joints, and costotransversal concluded from mathematical analysis that a side-bend joints. These investigators examined coupling motion in coupling occurs in the same direction as the rotation. Journal of Manipulative and Physiological Therapeutics Sizer, Brisme´e, and Cook 395 Volume 30, Number 5 Coupling Behavior of the Thoracic Spine

Table 5. Coupled thoracic motion with rotation initiation

Spine position Author (F, N, or E) Direction C7T1 T1T2 T2T3 T3T4 T4T5 T5T6 T6T7 T7T8 T8T9 T9T10 T10T11 T11T12 T12L1

Panjabi et al, Neutral (L) rotation NT S S S S S S S S S S S NT 197618 (R) rotation NT O O O O O O O O O O O NT Oxland et al, Neutral Both (L) and NT NT NT NT NT NT NT NT NT NT NT S S 199219 (R) rotation Willems et al, Neutral Both (L) and NT V V V 19961 (R) rotation Gregersen Neutral NT NT NT NT NT NT NT NT NT NT NT NT NT NT and Lucas, 196720 Schultz et al, Neutral NR NT S S S S S S S S S S S S 197323 Scholten and Not NR NT NT NT NT NT NT NT NT NT NT NT NT NT Veldhuizen, applicable 198524 S, axial rotation coupling to the same side as side-bend; O, axial rotation coupling to the opposite side of side-bend; NT, not tested;. V, variable coupling pattern among specimens; NR, not reported; F, flexed; E, extended; N, neutral; (L), left; (R), right.

Table 6. Coupled thoracic motion with side-bend (lateral flexion) initiation

Spine position Author (F, N, or E) Direction C7T1 T1T2 T2T3 T3T4 T4T5 T5T6 T6T7 T7T8 T8T9 T9T10 T10T11 T11T12 T12L1

Panjabi Neutral Both (L) and NTOOOOOOOOOO O NT et al, (R) side-bend 197618 Oxland Neutral Both (L) and NT NT NT NT NT NT NT NT NT NT NT NC (1) NC (1) et al, (R) side-bend 199219 Willems Neutral Both (L) and NT V V V NT et al, (R) side-bend 19961 Gregersen Neutral Both (L) and SSSSSSSSSS S S O and Lucas, (R) side-bend 196720 Schultz Neutral NR NT S S S S S S S S S S S S et al, 197323 Scholten and Flexion NRNTSSSSSSSSSS S S Veldhuizen, and 198524 extension NC indicates no coupling observed.

However, they did not identify the specific rotation the rotation-initiated coupled movements, side-bend–initi- direction. Finally, Willems et al1 reported differences in ated movements produced varying results depending on the coupling directions depending on the regions of the thoracic investigator. Panjabi et al18 reported that all segments spine. When rotation was the primary motion, it was showed rotation coupling in the opposite direction as the accompanied by ipsilateral side-bend coupling in (1) 18% side-bending to either left or right (T1T2 through T11T12), of subjects at segments T1T2 through T3T4; (2) 99% of whereas Oxland et al19 reported no rotation coupling when subjects at segments T4T5 through T7T8; and (3) 93% of the T11T12 or T12L1 segments were passively side-bent. subjects at segments T8T9 through T11T12. The remainder Willems et al1 reported regional differences in rotation of subjects produced contralateral side-bend coupling within coupling in a similar fashion to the previously reported side- each segmental region. bend coupling. When side-bending was the primary motion, Six studies qualified as 3-D analyses of coupling motion it was accompanied by axial rotation in approximately 2:1 with side-bend initiation (Table 6). In a similar fashion to (T1-T4), 1:1 (T4-T8), and 3:1 (T8-T12) ratios. The side- 396 Sizer, Brisme´e, and Cook Journal of Manipulative and Physiological Therapeutics Coupling Behavior of the Thoracic Spine June 2007

Table 7. Coupled thoracic motion with upper extremity initiation, side-bend, or rotation initiation was not reported

Spine Position Author (F, N, or E) Direction C7T1 T1T2 T2T3 T3T4 T4T5 T5T6 T6T7 T7T8 T8T9 T9T10 T10T11 T11T12 T12L1

Stewart NR (R) UE NT V (1) V (2) NT et al, elevated 199521 Theodoridis NR Both (L) NTNTVVVVVNTNTNTNTNTNT and and (R) UE Ruston, elevated 200222

Spine position was not reported. UE indicates upper extremity.

bend movement was accompanied by ipsilateral rotation identified coupling behavior of the thoracic spine. Variations coupling in (1) 47% of subjects at segments T1-T2 through were reported in side-bending and rotation initiation, and no T3-T4; (2) 83% of subjects at segments T4-T5 through T7- consistent pattern was observed when comparing in vivo vs T8; and (3) 68% of subjects at segments T8-T9 through in vitro findings. Coupling motion secondary to upper T11-T12. The remainder of subjects produced contralateral extremity movement resulted in the greatest display of rotation coupling within each segmental region. variation. Taken at face value, the findings suggest that Two studies reported coupled thoracic motion in thoracic spine coupling patterns are inconsistent. Second, response to active upper extremity elevation initiation there was significant variation observed regarding study (Table 7). In both studies, side-bend or rotation initiation designs, measurement methods, and tissue preparation for was not reported, as well as a lack of spine position. each study. Variations in methodology may account for Theodoridis and Ruston22 evaluated the coupled thoracic differences among the findings in each study.25,26 For movements in the T2-T3 through T6-T7 segments during example, tissue preparation ranged from removal of all ribs left and right upper extremity elevation in both the sagittal and corresponding ligaments to maintenance of all anatom- and scapular planes. They reported that 92% of the subjects ical structures. This may have contributed to differences in produced ipsilateral thoracic rotation and side-bending- coupling outcomes. coupled movement during flexion of both the right and left Abnormalities associated with quality and direction of upper extremities, whereas 8% produced contralateral coupling could be construed as pathological and have been coupling. Conversely, elevation in the scapular plane associated with physical variation or dysfunction.12,14 produced ipsilateral coupling in 76% of the subjects, Because many manual therapy clinicians base specific whereas 24% exhibited contralateral coupling. mobilization and manipulation decisions on selected theo- Stewart et al21 examined the coupling behaviors produced ries of coupling, such as Fryette laws,27,28 variations in during active right upper extremity elevation. For segments treatment application are possible as result of inconsisten- T1-T2 through T5-T6, 8 subjects produced ipsilateral cies between theories.28 The feasibility exists, that if thoracic spine coupling, whereas 12 produced contralateral practicing therapists do not share consistent directional coupling. Of those subjects producing ipsilateral coupling, 6 coupling pattern expectations, the results of their assessment subjects coupled to the right, whereas 2 coupled to the left. and treatments may be dissimilar. Of those coupling contralaterally, 7 coupled with right It has been recognized that 2-D analysis of coupling rotation and left side-bending, whereas 5 coupled with left spinal motions are inaccurate at measuring axial rotation and rotation and right side-bending. In segments T6-T7 through may be ineffective at measuring coupling direction and T11-T12, 14 subjects produced ipsilateral coupling, whereas quantity.25 Two-dimensional imagery has been criticized 6 produced contralateral coupling. Of those subjects that because of the potential magnification of errors, projection produced ipsilateral coupling, 4 subjects coupled to the right, of translations as rotations, and misleading results.26,29 To whereas 10 coupled to the left. Of those that produced represent the true accurate motion behavior of the spine, contralateral coupling, 5 subjects coupled with right rotation intervertebral coupling motion is best measured with 3-D 25,30 and left side-bending, whereas 1 coupled left rotation and instrumentation, which allows the calculation of finite right side-bending. movements in multiple planes. Thus, we elected to include only studies that used 3-D imagery. This review found that under controlled in vitro DISCUSSION conditions, variations of the coupling pattern of the thoracic There are two notable findings in this review. First, there spine are present, which indicates variability of thoracic is poor agreement among 3-D biomechanical studies that coupling in controlled conditions both with side-bend Journal of Manipulative and Physiological Therapeutics Sizer, Brisme´e, and Cook 397 Volume 30, Number 5 Coupling Behavior of the Thoracic Spine

initiation and rotation initiation. Although 3-D analyses of the standards creates a foundation for assessing the have shown the greatest degree of accuracy, translating the quality of biomechanical studies at other spinal regions. results of in vitro studies into the clinical setting is Moreover, the standards may suggest a basis for future questionable. In vitro studies involve cadaveric specimens study design when addressing biomechanical behaviors of with selected tissue removed, such as muscles, ligaments, the spine. and/or rib structures. In addition, different investigators test It has been stated that knowledge of spine mobility and different combinations of thoracic segments using different characteristics of coupling direction are important for variations of applied load.18,31 These changes produce understanding and treating patients with spinal pain.18 At alterations in tissue flexibility and resultant coupling present, the evidence to support this view is wanting. The behavior of the spine.18 Nonetheless, in vitro studies can 3-D thoracic movement research using in vivo human be useful because they allow for the control of extraneous subjects tested the coupling of the thoracic spine in neutral variables, such as the load that is applied; the passivity of position with the exception of one investigation.24 Both motion (no muscle activity); prepositioning of the spine in a side-bend– and rotation-initiated results are inconsistent. flexed, neutral, or extended position; and the degree of Most manual, segmental therapeutic techniques that are kyphosis and/or scoliosis,32 which all can influence the based on coupling theory use side-bend initiation. With the coupling behavior of the thoracic spine.24 findings of this review in mind, this approach should be In vivo studies are clinically applicable but lead to questioned, unless preceded by a reliable and valid challenges in controlling extraneous variables that include segmental movement testing procedure. motor and postural control, as well as tissue adaptation33 All 3-D in vivo studies published to date included anatomical and circadian variability; applied preload forces asymptomatic subjects only. The findings have limited 12,18,34,35; the degree of thoracic kyphosis and scoliosis 36; application to a symptomatic patient population with and technical difficulty in measuring spinal coupling.20 For thoracic pain. Thus, the need for additional research example, most of the studies reported in this systematic investigating the coupling pattern of the thoracic spine in review, with the exception of one study, measured the symptomatic subjects is merited, considering that patients coupling of the thoracic spine in its neutral position. This with spinal pain display greater levels of guarding, could create variability in measurement outcomes due to the recruit muscle activity differently, move slower, and have considerable variance in the position that the investigators altered range of motions compared with asymptomatic considers dneutral,T which appears to depend on the degree individuals.40 of thoracic kyphosis. The finding of Scholten and Veldhui- The lack of a common coupling pattern may merit zen24 that coupling is stronger in a flexed position of the individual clinical assessment for each patient examined. thoracic spine supports this notion, which may partially However, the reliability and validity of such clinical explain selected disparities in the findings of this review. measurement must serve as a prerequisite for the use of Further supporting this idea, Stewart et al21 used women manual testing in the clinic. Brismee et al37 examined the aged 18 to 22 years with no excessive kyphosis and found intertester reliability of a passive physiological interverte- no significant pattern of thoracic coupling in a neutral bral motion test of the mid thoracic spine in live position using arm elevation, whereas Theodoridis and asymptomatic subjects. This measure used thoracic motions Ruston22 used an older sample of women aged 45 to 64 and in 3 dimensions, whereas investigators tested the relative found predominance of ipsilateral thoracic coupling. In movements of the spinous processes. These investigators addition, similar findings were identified in a study observed fair to substantial reliability between 3 experi- involving manual palpation of thoracic segmental motion enced manual therapy examiners in evaluating mid thoracic that reported 90% of young men exhibiting an ipsilateral segmental mobility. Although this study could represent a 3-D movement in thoracic spinal extension, whereas a foundation for developing a method for clinical testing, contralateral 3-D movement was reported in 91% of young further investigations are merited to establish the validity of women in a position of thoracic extension.37 These results testing that measures thoracic segmental coupling move- may reflect the interaction of the thoracic kyphosis with sex- ments in symptomatic subjects. In the absence of any related differences in spinal stiffness and segmental behav- available valid test for clinical determination, clinicians iors that have been previously described.38,39 must then reconsider the limited value of coupling This is the first manuscript we are aware of to score the information for the diagnosis and treatment of thoracic quality of manuscripts addressing coupling behaviors of the spine conditions. spine. The results of this scoring provide details regarding the differences observed between the study outcomes. A lack of any reliability measure in most of the evaluated CONCLUSION studies suggests a considerable limitation in the available data to date and implies the need for this consideration in Findings suggest that the coupling of the thoracic spine future studies. The compliance of all 8 studies with several is inconsistent and, if used in clinical reasoning and 398 Sizer, Brisme´e, and Cook Journal of Manipulative and Physiological Therapeutics Coupling Behavior of the Thoracic Spine June 2007

methodology, may merit specific segmental testing. More 14. Gracovetsky S, Newman N, Pawlowsky M, Lanzo V, Davey B, rigorous, in vivo investigations are needed to evaluate the Robinson L. A database for estimating normal spinal motion derived from noninvasive measurements. Spine 1995;20: coupling pattern of the thoracic spine in symptomatic 1036-46. subjects prepositioned in both thoracic flexion and 15. Parnianpour M, Nordin M, Frankel V, Kahanovitz N. Trunk extension. Present studies on coupling behavior may triaxial coupling of torque generation of trunk muscles during yield some useful information, but clinicians need to isometric exertions and the effect of fatiguing isoinertial recognize that not all individuals will display the same movements on the motor output and movement patterns. Spine 1988;13:982-92. mechanical behaviors. 16. Weitz E. The lateral bending sign. Spine 1981;6:388-97. 17. Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977;33:159. 18. Panjabi MM, Brand RA, White AA. Mechanical properties Practical Applications of the human thoracic spine as shown by three-dimensional load-displacement curves. J Bone Joint Surg Am 1976; ! Of 56 identified studies, 8 met the inclusion criteria 58:642-52. and showed variations in coupling behaviors 19. Oxland TR, Lin RM, Panjabi MM. Three-dimensional findings. mechanical properties of the thoracolumbar junction. J Orthop ! Differences in study design, measurement method, Res 1992;10:573-80. 20. Gregersen GG, Lucas DB. An in vivo study of the axial and tissue preparation may have contributed to rotation of the human thoracolumbar spine. J Bone Joint Surg differences between studies. Am 1967;49:247-62. 21. Stewart SG, Jull G, Jg JK-F, Willems JM. An initial analysis of thoracic spine movement during unilateral arm elevation. J Man Manip Ther 1995;3:15-20. 22. Theodoridis D, Ruston S. The effect of shoulder movements on REFERENCES thoracic spine 3D motion. Clin Biomech (Bristol, Avon) 1. Willems JM, Jull G, Ng J. An in-vivo study of the primary and 2002;17:418-21. coupled rotations of the thoracic spine. Clin Biomech 23. Schultz AB, Belytschoki TB, Andriacchi TP. Analog studies of 1996;11:311-6. forces in the human spine: mechanical properties and motion 2. White AA, Panjabi MM. Clinical biomechanics of the spine. segment behavior. J Biomech 1973;6:373-83. 2nd ed. Philadelphia7 JB Lippincott; 1990. 24. Scholten PJM, Veldhuizen AG. The influence of spine 3. Edmondston SJ, Singer KP. Thoracic spine: anatomical and geometry on the coupling between lateral bending and axial biomechanical considerations for manual therapy. Man Ther rotation. Eng Med 1985;14:167-71. 1997;2:132-43. 25. Harrison D, Harrison D, Troyanovich S. Three-dimensional 4. Kapandji I. The physiology of the joints. Vol. 3. The trunk and spinal coupling mechanics. Part one. A review off the the vertebral column. 2nd ed. London7 Churchill Livingstone; literature. J Manipulative Physiol Ther 1998;21:101-3. 1978. 26. Harrison D, Harrison D, Troyanovich S, Hansen D. The 5. Galante JO. Tensile properties of the human lumbar annulus anterior posterior full spine view: the worst radiographic view fibrosis. Acta Orthop Scand 1967;(Suppl 100):1-91. for determination for mechanics of the spine. Chiropr Tech 6. Masharawi Y, Rothschild B, Dar G, Peleg S, Robinson D, Been 1996;8:163-70. E, Hershkovitz I. Facet orientation in the thoracolumbar spine. 27. Fryette H. The principles of osteopathic technique. Carmel CA7 Spine 2004;29:1755-63. Academy of Applied Osteopathy; 1954. 7. Panjabi M, Hult J, Crisco J, White A. Biomechanical studies 28. Cook C. Lumbar coupling biomechanics—a literature review. in cadaveric spines. In: Jayson M, editor. The Lumbar Spine J Man Manip Ther 2003;11:137-45. and Back Pain. 4th ed. London7 Churchill Livingstone; 1992. 29. Olin T, Olsson T, Selvik G, Willner S. Kinematic analysis of p. 133-55. experimentally provoked scoliosis in pigs with Roentgen 8. Panjabi M, Yamamoto I, Oxland T, Crisco J. How does posture stereophotogrammetry. Acta Radiol Diagn (Stockh) 1976; affect coupling in the lumbar spine? Spine 1989;14:1002-11. 1F:107-27. 9. Panjabi M, Oda T, Crisco J, Dvorak J, Grob D. Posture affects 30. Stokes I, Medlicott P, Wilder D. Measurement of movement in motion coupling patterns of the upper cervical spine. J Orthop painful intervertebral joints. Med Biol Eng Comput 1980;18: Res 1993;11:525-36. 694-700. 10. Pearcy M, Tibrewal M. Axial rotation and lateral bending in 31. Cholewicki J, Crisco J, Oxland T, Yamamoto I, Panjabi M. the normal lumbar spine measured by three-dimensional Effects of posture and structure on three-dimensional coupled radiography. Spine 1984;9:582-7. rotations in the lumbar spine. Spine 1996;21:2421-8. 11. Grice A. Radiographic, biomechanical and clinical factors in 32. Beausejour M, Aubin CE, Feldman AG, Labelle H. Simulation lumbar lateral flexion: part 1. J Manipulative Physiol Ther of lateral bending tests using a musculoskeletal model of the 1979;2:26-34. trunk. Ann Chir 1999;53:742-50. 12. Panjabi M, Oxland T, Yamamoto I, Crisco J. Mechanical 33. Hodges PW, Richardson CA. Inefficient muscular stabilization behavior of the human lumbar and lumbosacral spine as shown of the lumbar spine associated with low back pain. A motor by three-dimensional load-displacement curves. J Bone Joint control evaluation of transversus abdominis. Spine 1996;21: Surg Am 1994;76:413-24. 2640-50. 13. Pearcy M, Portek I, Shepherd J. The effect of low back pain on 34. Panjabi M, Krag M, White A, Southwick W. Effects of pre- lumbar spine movements measured b three-dimensional x-ray load on load-displacement curves of the lumbar spine. Orthop analysis. Spine 1985;10:150-3. Clin North Am 1977;8:181-92. Journal of Manipulative and Physiological Therapeutics Sizer, Brisme´e, and Cook 399 Volume 30, Number 5 Coupling Behavior of the Thoracic Spine

35. Vincenzino G, Twomey L. Side-flexion induced lumbar spine 38. Einkauf DK, Gohdes ML, Jensen GM, Jewell MJ. Changes in conjunct rotation and its influencing factors. Aust J Physiother spinal mobility with increasing age in women. Phys Ther 1993;39:299-305. 1987;67:370-5. 36. Pope MH, Stokes IA, Moreland M. The biomechanics of 39. Fon GT, Pitt MJ, Thies AC. Thoracic kyphosis: range in scoliosis. Crit Rev Biomed Eng 1984;11:157-88. normal subjects. AJR Am J Roentgenol 1980;134:979-83. 37. Brisme´e JM, Gipson D, Ivie D, et al. Interrater reliability 40. Dankaerts W, O’Sullivan P, Burnett A, Straker L. Altered of a passive physiological intervertebral motion test in the patterns of superficial trunk muscle activation during sitting in mid-thoracic spine. J Manipulative Physiol Ther 2006; nonspecific chronic low back pain patients: importance of 29:368-73. subclassification. Spine 2006;31:2017-23.