University of the Pacific Scholarly Commons

School of Pharmacy Faculty Articles Thomas J. Long School of Pharmacy

4-1-2013

Alteration in corticospinal excitability, talocrural range of motion, and lower extremity function following manipulation in non-disabled individuals

Todd E. Davenport University of the Pacific, [email protected]

Stephen F. Reischl University of Southern California

Somporn Sungkarat Chiang Mai University

Jason Cozby University of Southern Claifornia

Lisa Meyer University of Southern California

See next page for additional authors Follow this and additional works at: https://scholarlycommons.pacific.edu/phs-facarticles

Part of the Orthopedics Commons

Recommended Citation Davenport TE, Reischl SF, Sungkarat S, Cozby J, Meyer L, Fisher BE. Alteration in corticospinal excitability, talocrural joint range of motion, and lower extremity function following manipulation in non-disabled individuals. Orthopaedic Practice. 2013;25(2):97-102. © 2013, Orthopaedic Section, APTA, Inc.

This Article is brought to you for free and open access by the Thomas J. Long School of Pharmacy at Scholarly Commons. It has been accepted for inclusion in School of Pharmacy Faculty Articles by an authorized administrator of Scholarly Commons. For more information, please contact [email protected]. Authors Todd E. Davenport, Stephen F. Reischl, Somporn Sungkarat, Jason Cozby, Lisa Meyer, and Beth E. Fisher

This article is available at Scholarly Commons: https://scholarlycommons.pacific.edu/phs-facarticles/136 Alteration in Corticospinal Excitability, Todd E. Davenport, PT, DPT, OCSI Stephen E Reischl, PT, DPT, ocs2 Talocrural Joint Range of Motion, and Somporn Sungkarat, PT, PhD3 Lower Extremity Function Following Jason CozbJG PT, DPT, OCS2 Lisa Meyer, PT, OPT, OCS4 Manipulation in Non-disabled Individuals Beth E. Fisher, PT, PhD5

....· . . . • .· J}/om(f! J Long . . . o]Ph~rmapy and Health Sciences, 2Adju:nct Associate Professor ofClinical Phyfical1herapy, Division oflJitlfei~zesi,oloJrY t.md.RhYs.#'al:YJ~tapy;(iJ(tlle.•!J[e.fr.nit_h; .•.· Dentistry, ·University ofS~uthern. California, Los Ang~les, ·Ctt. . ; 9.ftrsistifnt I!rofossor qnd ,Associate Dean for. Research and lntt.r '1idlrior.ral.4f{t'tirJ.r Rwu.lty,i · Ch4i-zgA{a4: 1hfltil4nd · . . ,:• · .· . · . ... ·.. fAdJu"nctftEtrtt~tor ofClinical Physj(itllfteraP}> Dit~ision · Bit,ki1.iesj,tJlo;~.·

t{tSsfc#J~ Professor ofClinical Physical1herapy ~pirector of thel\.•.. re.. u:' •obirait.icitv a1'1d.l; .· Physical7J;erapy .at the Herman Ostrow School ofDentistry.. T,!niva-sity . (.d.,(ifii,rn.i;.t?,

ABSTRACT to the talocrural joint in nondisabled indi­ joint mobility, which may occur as either a Background: Clinical outcomes of viduals. These results establish comparative cause or consequence ofankle . Limited procedures, including values with which to compare the cortico­ ankle dorsiflexion has been documented as a 2 27 manipulation, have been studied. However, spinal responses to manual therapy interven­ major short-term sequel to ankle sprain. 6· mechanisms underlying observed improve­ tion in individuals with pathology. In addition, several studies have identified ments remain unclear. Objective: To limited talocrural joint dorsiflexion range of determine the effect of ankle joint manipu­ Key Words: ankle, manipulation, motion (OF ROM) as an important predis­ 28 30 lation on corticospinal excitability, ankle transcranial magnetic stimulation, posing factor to ankle . - Limited dorsiflexion range of motion (OF ROM), functional testing ankle OF ROM will position the talocru­ and lower extremity functional behavior ral joint in plantar flexion during weight in nondisabled individuals. Method: Six INTRODUCTION bearing activities. This position is notable nondisabled individuals (age range: 31-50 Ankle sprains are the most common because the most common mechanism of years) received the main outcomes measure­ injury to the ankle joint, affecting up to 2 injury for ankle sprains involves plantar flex­ ments of this study, before and after long million people and approximately 53 per ion and inversion of the ankle and foot. The 1 2 axis distraction manipulation of the talc­ 10,000 individuals per year. • Ankle sprains injury mechanism places excessive load on crural joint. Main outcomes measures were are common in younger and active individu­ the anterior talofibular ligan1ent (ATFL). motor evoked potential (MEP) amplitude als.H Certain sports and work activities may With failure of ATFL, secondary restraint of gastrocnemius (GN) and tibialis anterior result in an even higher incidence and risk to inversion occurs by way of the calcaneo­ 15 (TA) using transcranial magnetic stimula­ for injury. 9- Ankle sprains are a clinically fibular and posterior talofibular ligaments, tion, ankle OF ROM with the knee Hexed important problem because they result in placing them at similar risk for injury. Thus, and extended using standard goniometric a substantial number of missed work days8 limited ankle OF ROM may result in injury 3 5 techniques, and unilateral anterior squat and participation in sports activity, • as well and consequent structural and functional reach (ASR) distance. All subjects received as lead to potential early arthritic changes compromise of the ankle lateral collateral the main outcomes measures. Results: Sig­ in the talocrural joint. 16 The prognosis for ligaments. nificant increase in GN MEP amplitude (P functional recovery following ankle sprain Physical therapists use mobilization and < .05), but not TA MEP amplitude, were typically includes a rapid clinical improve­ manipulation to improve ankle OF ROM documented following intervention. Sig­ ment within the first rwo weeks after following ankle sprains. Despite the intui­ nificant improvements also were noted in injury.17 However, a series of recent srudies tive appeal of applying these procedures to ankle OF ROM with knee extended and indicate a subgroup of individuals appears promote parallel improvements in talocru­ ral OF ROM and functioning in individu­ Hexed (P< .001) andASRdistance (P< .05) predisposed to continued pain, functional als following ankle sprains, this notion has Significant correlations were found berween deficits, and prolonged risk for additional been the focus of relatively few prospective standardized change in GN MEP amplitude rein jury berween 6 weeks and 3 years postin­ srudies.31 Pellow and Brantingham32 were and ankle dorsiflexion with knee flexed (p = jury.t7-25 The prolonged disability associated among the first to report reduced and .582, p2 = .339, P < .01), and standardized with ankle sprains represents the possibility improved function in individuals with ankle changes in GN MEP amplitude and ASR of increased direct and indirect sprains receiving an ankle mortise distrac­ distance (p = .601, p2 .361, P< .01). Con­ costs associated with ankle sprains, and may tion technique. Whitman and colleagues" clusions: Increased corticospinal excitability be reduced through identification of optimal reported rapid functional improvement appears to mediate improvements in ankle approaches to clinical management. OF ROM and lower extremity function fol­ One reason for continued pain and ele­ after talocrural manipulation in a competi­ lowing long axis distraction manipulation vated risk for reinjury may be limited ankle tive volleyball player with a mild unilateral

Orthopaedic Practice \ml 25;2: 13 97

~------·- ankle sprain. More recently, Whitman and and potential alteration in functional behav­ Transcranial magnetic stimulation coworkers34 documented favorable clinical ior using valid and reliable measurements. measurement outcomes in approximately 75% of their The purpose of this pilot study was to deter­ All the TMS assessments were carried sample with post-acute ankle sprains fol­ mine the effect of talocrural manipulation out with a single-pulse magnetic stimulator 2 lowing two sessions of mobilization and on gastrocnemius and tibialis anterior MEP, (Magstim 200 ). A Double Cone 110 mm manipulation directed at distal to the ankle DF ROM, and unilateral anterior coil was used to generate the TMS pulse. knee. Although initial results are promising, squat reach (ASR) distance in nondisabled This pulse provides stimuli of sufficient mechanisms underlying the clinical effects individuals. depth of penetration to activate the corti­ of manual therapy in individuals with ankle cal representational areas of lower extrem­ sprains remain unclear. METHOD ity muscles. The skin over the designated Through further study of the poten­ Subjects muscles of the right lower extremity was tial role for neuroplasticity to mediate the Participants prepared with cleansing gel and alcohol to relationship between brain activity and Six nondisabled individuals (2 females, decrease impedance for applying surface behavior in people with ankle sprains, it 4 males) ranging in age from 30-51 years electromyography (EMG) electrodes. Sur­ may be possible to better understand those participated in this study. Subjects were face EMG electrodes (Ag-AgCl, 12 mm mechanisms that result in a symptomatic excluded if they experienced a lower extrem­ diameter, interelectrode distance: 17 mm) and behavioral benefit. Various central and ity injury in the past 12 months, a history of were attached over the muscle belly of TA spinal sensorimotor mechanisms of manual lower extremity or low back , lower and GN, and the ground electrodes were therapy procedures recently have been inves­ extremity neuropathy, vestibular dysfunc­ placed over the medial and lateral femoral tigated. Inhibition of the Hoffman reflex tion, diabetes or active arthritis, or if there epicondyle, respectively for each muscle. following and increased were any contraindications to undergo­ The electrodes remained in place between lower extremity muscle strength have been ing talocrural joint manipulation (ie, gross the two TMS test sessions. The EMG signals observed following manual therapy directed mechanical instability, history of connective were filtered with 1-1000 Hz bandwidth to the lumbopelvic.3'-39 Manual therapy pro­ tissue disease). Based on the TMS safety filter, amplified, and digitized at 2000 Hz. cedures may facilitate descending inhibitory guidelines,« other exclusion criteria include The data were displayed and stored with cus­ inputs to local spinal circuits that cause the neurological disorders; psychological prob­ tomized MATLAB module (dwaq; dataWiz­ observed H-reflex depression, suggesting a lems; history of significant head trauma; ard acquisition, ADW) in 600-ms samples broader effect on the central nervous system any electrical, magnetic, or metal device beginning 100 ms before TMS stimulus. (CNS).40 Dishman and colleagues41 identi­ implanted in the body (ie, cardiac pacemak­ To determine the optimal TMS stimu­ fied a short-term increase in motor evoked ers or intracerebral vascular clip); pregnancy; lus point ("hotspot"), the participants were potential (MEP) amplitude for the lumbar history of seizures or unexplained loss of required to wear a swim cap with 1 em x paraspinals in healthy volunteers following consciousness; immediate family member 1 em grid. The coil was initially placed on . manipulation of the lumbar spine, using with epilepsy; use of seizure threshold low­ a potential spot for the target muscle, and single-pulse transcranial magnetic stimula­ ering medication; current use of alcohol or then systematically moved in 1 em incre­ tion (TMS) directed to contralateral motor drugs; history of schizophrenia; or history of ments in each direction to find the point cortex. Haavik-Taylor and Murphy42 also hallucinations. that induced the most consistent and promi­ documented a significant muscle-specific nent motor evoked potentials (MEPs) with pattern of effects following cervical spine Procedure the shortest latency.46 To control TMS coil manipulation on short interval intracortical The Institutional Review Board of the positioning variability, a stereotactic image facilitation, short interval intracortical inhi­ University of Southern California Health guidance system (Brainsight™ Frameless) bition, and cortical silent period of abductor Sciences Campus approved the study proto­ was used. The hotspot of each muscle was pollicis brevis and extensor indicis without col. The protocol is described in detail else­ marked on a 3D reconstruction of a stan­ significant change in F wave in asymptom­ where.45 The following paragraphs include dard magnetic resonance image of the brain atic individuals with a history of recurrent a brief description of the protocol. Afrer an in the first test session, and the same point neck pain. These results suggest a potentially intake screening interview and informed ofstimulation was used for the postinterven­ broad effect of manual therapy on the neu­ consent was obtained, all subjects then tion test session. For TMS data collection, romotor processing of functional behavior received preintervention measurements, pulses were delivered as participants actively bytheCNS. intervention, and postintervention measure­ contracted TA and GN by performing ankle Our collective understanding of the role ments. Pre- and postintervention measure­ dorsiflexion and plantar flexion, respec­ for neuroplasticity to explain short-term ments included corticospinal excitability, tively, through a small, consistent amount of symptomatic and behavioral changes in ankle DF ROM, and anterior reaching dis­ range. Ten TMS pulses at 100% ofMT were response to ankle manipulation is hampered tance achieved during a single leg squat (ASR delivered with an inter-stimulus interval of I by shortcomings in the current literature. distance). The right lower extremity was approximately 5 to 10 seconds, also during For example, the study of manual therapy tested in all subjects. Afrer postintervention closed chain active ankle plantar flexion (ie, directed to the spine potentially jeopardizes testing, all subjects were discharged from the "seated heel raise") to mid-range. the specificity of conclusions that can be study. Completion of all study took up to I drawn, since spinal manipulation is poorly two hours per subject during one day. Ankle dorsiflexion range of motion localized even in skilled and,. experienced measurement practitioners.43 In addition, no correlation Following the TMS hotspot location has been made between neuromotor changes and MT measurement, all subjects received

98 Orthopaedic Practice Vol. 2.5:2:13 ankle OF ROM measurements. In the first tintervention value - preintervention value)/ RESULTS measurement, subjects laid prone on a preintervention value x 100. These calcula­ No significant differences were observed padded table. A single blinded and standard­ tions were completed in order to standard­ in median MEP amplitude for GN or TA ized examiner measured ankle OF ROM ize the data to the starting value for each across the 4 TMS intensities, so MEP with the knee fully extended using a 15.24 subject. data was pooled for analysis. Following em goniometer in a standard manner.47 Ihe Distribution of the data was then sum­ intervention, median GN MEP increased measurement was repeated with the knee marized by visual inspection of histograms 23.8% from .504pV (interquartile range fully flexed. Ibis measurement of ankle OF and the Shapiro Wilk test of data normaliry. [IQR]: .488) to .624pV (IQR: .375; Table). ROM demonstrates strong test-retest reli­ Nonparametric statistical tests were used for Median ankle DF ROM with knee extended abiliry with knee both Hexed (ICC .97) analysis, because the data was non-normally increased 130.8% from -6.5" (IQR: 7.0) to r and extended (ICC .98).47 distributed. For analysis of unstandardized 2.0° (IQR: 4.5) and median ankle OF ROM measurements, the Wilcoxon signed-rank with knee flexed increased from 5.0° (IQR: Anterior squat reach test test was used to assess the significance of 9.0) to 14.0° (IQR: 6.3) following interven­ Following the ankle OF ROM measure­ pairwise between-group median differences, tion. Median ASR distance also increased ment, all subjects completed the ASR mea­ and the Kruskal-Wallis test was used for 7.2% from 32.1 em (IQR: 7.4) to 34.4 surement. 'Jhis test is a component of the comparison of group medians among mul­ em (IQR: 4.8). No significant change in star balance excursion test, which has been tiple independent variables. Spearman's rho TA MEP was noted after intervention. Per­ 2 described as a clinical test of dynamic bal­ (p) and explained variance (p ) were calcu­ cent change in GN MEP amplitude dem­ ance.48 Subjects assumed unilateral stance lated for bivariate correlations among stan­ onstrated significant moderate correlations on the right lower extremiry in the center dardized changes in MEP amplitude, ankle with percent change in ankle OF ROM with of a grid marked circumferentially in 45o OF ROM, and ASR performance. Strength knee flexed (p = .582, p 2 = .339, P < .01) increments. Subjects then assumed a single of the association among the variables was and ASR distance (p = .601, p2 = .361, P < leg squat and reached with the left lower interpreted using Munro's'3 criteria: very .01), and percent change in ankle DF ROM extremiry, tapping the heel on the ground low = .15-.24, low = .25-.49, moderate with knee flexed showed significant high anterior to the stance limb as far as possible. .50-.69, high .70-.89, and very high = correlation with percent change in ASR dis­ After a brief learning period consisting of 6 .90-1.00. tance (p .700, p2 = .490, P .001) . trials,4 9 subjects completed 3 repetitions of ASR standing on the right lower extrem­ iry. Repetitions were excluded if the subject (I) was unable to maintain weight bearing during the trial, (2) lifted the stance foot, (3) lost balance, or (4) did not maintain the hold or start positions for one second. The mean of the 3 trials was taken as the ASR measurement. This test demonstrates good test-retest reliabiliry (ICC .67-.97).485°

Intervention With the subject in a seated position on a treatment table and the lower extremiry of interest stabilized to the table with a belt, a standardized licensed physical therapist grasped the foot of interest with the thenar eminences on the plamar surface of the sub­ ject's foot. A thrust was delivered parallel to the long axis of the subject's lower leg after the treating therapist induced passive ankle 4 1 dorsiflexion to end range (Figure). '·'

Data Analysis Transcranial magnetic stimulation data were analyzed off-line with a customized MATLAB (Mathworks, Natick, MA) soft­ ware, dataWizard (version 08.11, A.D.W, Figure. Intervention under study: long axis talocrnral joint. .··. ·.· ...... USC) by the same rater. 12 The average of (A) With the subject in a seated position on a treatment table ...... ·· .··· I 0 trials for each stimulus intensiry was ahiliz d to the table with a belt, the treating investigator grasped the foot calculated and used for data analysis. Per­ st'th th: thenar eminences on the foot's plantar surface. (B) After inducing passive cent change in GN MEP, TA MEP, ankle :kle dorsiflexion (open arrow), a thrust was then delivered parallel to the long axis DF ROM, and ASR test performance were of the subject's lower leg (hatched arrow). calculated according to the fOrmula: (pos-

Orthopaedic Practice Hd 25;2: 1.3 99 Table. Effect ofTalocrural Joint Manipulation on MEP Amplitude, Ankle DF ROM, ROM in response to manual therapy with­ and ASR Measurements out corresponding change in pressure or thermal pain thresholds. A follow-up study Preintenention Postintervention Percent change P-value by this group found a significant association measurement" measurement change between improvement in a clinical measure GN MEP (!lV) .504 (.488) .624 (.375) 23.8% .037' of talocrural posterior glide and improve­ ment in talocrural DF ROM. 55 Overall TAMEP(!lV) .771 (1.05) .767 (1.04) -0.5% .695 these findings suggest a primarily mechani­ cal effect of treatment. However, the mag­ Ankle OF ROM, knee extended (") -6.5 (7.0) 2.0 (4.5) 130.8% <.OOJS nitude, time, and speed of loading that Ankle OF ROM, characterize manipulation seem inadequate knee flexed n 5.0 (9.0) 14.0 (6.3) 180.0% <.001§ to reverse maladaptive fibrosis that has been hypothesized to result in arthrokinematic ASR distance (em) 32.1 (24.7- 39.5) 34.4 (29.6- 39.2) 7.2% .04?1 and osreokinematic ankle mobility limita­ 49 56 * Values expressed as median (incerquartile range) tions following sprains. · Significant mod­ t - Statistically significant, P < .05 erate to high correlations between changes §-Statistically significant, P < .001 in GN MEP amplitude, ankle DF ROM, and ASR distance that were identified in Abbreviations: GN, gastrocnemius; TA, tibialis anterior; MEP, motor evoked potential; OF ROM, dorsiflexion range of motion; ASR, anterior squat reach this study suggest the potential mechanistic importance of short-term neuromotor adap­

'i tation to promote improvements in ankle DF ROM and lower extremity functional behavior. Additional work is necessary to 1:1.. •. DISCUSSION ble empirical examination of the relationship elucidate the nature and time course of these

\.: The talocrural JOlfit long-axis trac­ between short-term CNS neuroplasticity neuromotor changes in individuals with \ ll I r tion manipulation has been described as and the changes in functional behavior that lower extremity disablement. '. ' a procedure to improve ankle DF ROM have been elucidated by clinical studies. .,jI' 32 33 45 1 • • .5 t l: following ankle sprain. This study In this study, GN MEP amplitude was ACKNOWLEDGEMENT ll documented the effect of talocrural joint II observed to increase significantly following This work was supported by a grant to I long-axis traction manipulation on cortico­ talocrural long-axis traction manipulation, Todd E. Davenport from the Orthopaedic spinal excitability and lower extremity func­ which indicates increased corticospinal tract Section, APTA, Inc. tional behavior in nondisabled individuals. excitability involving this muscle group. To date, the literature regarding neuromo­ Treatment effects seem unique to GN, REFERENCES tor effects of manual therapy has involved because significant increases in TA MEP 1. Beynnon BD, Renstrom PA, Alosa DM, 41 42 procedures directed to the spine. • How­ amplitude were not observed. Studies to Baumhauer JF, Vacek PM. Ankle liga­ ever, spinal manipulation is poorly localized date using TMS methodology to determine ment injury risk factors: a prospective even in the hands of skilled and experienced the effect of manual therapy procedures study of college athletes. J Orthop Res. practitioners.43 1hus, the emphasis on spinal on corticospinal excitability have not mea­ 2001;19(2):213-220. manual therapy procedures in research sured the effect of intervention on opposing 2. Bridgman SA, Clement D, Down­ designs of studies to date potentially inhib­ muscle groups. Thus, the discrepant effect of ing A, Walley G, Phair I, Maffulli N. its the specificity of conclusions that can be manipulation on antagonist muscle groups Population based epidemiology of ankle drawn from these studies about the effect of observed in this study represents a new find­ sprains attending accident and emer­ manual treatment procedures. ing in the literature that requires additional gency units in the West Midlands of This study provides support for using replication in studies of the spine and upper England, and a survey of UK practice the talocrural joint to study the neuromotor extremity. This finding also indicates the for severe ankle sprains. Emerg Med]. effects of manipulation in individuals with need to assess the potential for differential 2003;20(6):508-51 0. lower extremity pathology. The talocrural effects of treatment on antagonist muscle 3. Bahr R, Reeser JC. Injuries among joint is a promising body region to elucidate groups in the ankles of individuals with world-class professional beach volleyball the potential neuromotor effects of manual symptoms. players. The Federation Internationale de therapy for a number of reasons.'5 The talo­ In addition to significant increase of Volleyball beach volleyball injury study. crural joint is relatively large, so interven­ GN MEP amplitude, parallel significant Am] SportsMed. 2003;31(1):119-125. tion may be more specifically localized to improvements in ankle DF ROM and ASR 4. Fong DT, Hong Y, Chan L, Yung PH, the talocrural joint than smaller joints of the distance were observed following long­ Chan K. A systematic review on ankle spine. Muscle groups crossing the talocru­ axis traction talocrural joint manipulation. injury and ankle sprain in sports. Sports ral joint are relatively large, which provide These findings confirm observations from Med. 2006;37(1):73-94. for reliable placement of EMG 'electrodes prior studies and clinical experience with 5. Fernandez WG, Yard EE, Comstock with minimal cross-talk. Valid .and reliable manual therapy of relatively rapid improve­ RD. Epidemiology of lower extremity behavioral measurements for talocrural joint ment in symptoms and ankle DF ROM injuries among U.S. high school athletes. range of motion and lower extremity func­ following manipulation. Collins and col­ AcadEmergMed. 2007;14(7):641-645. tional behavior already exist, making possi- leagues54 found an increase in ankle DF 6. Fordham S, Garbutt G, Lopes P.

100 Orthopaedic Practice ~L 25;2:13 Epidemiology of injuries in adven­ afrer medical evaluation. Arch Fam Med. driks EJ, Stomp DJ, Dekker J, de Bie ture racing athletes. Br J Sports Med. 1999;8(2): 143-148. RA Effectiveness of exercise therapy 2004;38(3):300-303. 20. Garrick JG, Requa RK. The epide­ and m.anual mobilisation in ankle Jacobson BH, Hubbard M, Redus B, et miology of foot and ankle injuries sprain and functional instability: a al. An assessment of high school cheer­ in sports. Clin Podiatr Med Surg. systematic review. Aust f Physiother. leading: injury distribution, frequency, 1989;6(3):629-637. 2006;52(1):27-37. and associated factors. f Orthop Sports 21. Kofotolis ND, Kellis E, Vlachopoulos 32. Pellow JE, Brantingham JW The efficacy Phys 1her. 2004;34(5):261-265. SP. Ankle sprain injuries and risk fac­ of adjusting the ankle in the treatment of Grimm DJ, Fallat L. Injuries of the tors in amateur soccer players during subacute and chronic grade I and grade fOot and ankle in occupational medi­ a 2-year period. Am J Sports Med. II ankle inversion sprains. f Manipula­ cine: a 1-year study. f Foot Ankle Surg. 2007;35(3):458-466. tive Physiol1her. 2001;24(1):17-24. 1999;38(2): 102-108. 22. McKay GD, Goldie PA, Payne WR, 33. WhitmanJM, Childs JD, Walker V. The Bahr R, Bahr IA. Incidence of acute Oakes BW. Ankle injuries in basketball: use of manipulation in a patient with volleyball injuries: a prospective cohort injury rate and risk factors. Br f Sports an ankle sprain injury not responding srudy of injury mechanisms and Med. 2001;35(2):103-108. to conventional management: a case risk factors. Scand J Med Sci Sports. 23. Milgrom C, Shlarnkovitch N, Fine­ report. Man 1her. 2005;10(3):224-231. 1997;7(3): 166-171. stone A, et al. Risk factors for lat­ 34. Whitman JM, Cleland JA, Mintken PE, lO. Hickey GJ, Fricker PA, McDonald WA eral ankle sprain: a prospective study et al. Predicting short-term response Injuries of young elite female basketball among military recruits. Foot Ankle. to thrust and nonthrust manipulation players over a six-year period. Clin J 1991; 12(1 ):26-30. and exercise in patients post inversion Sport Med. 1997;7(4):252-256. 24. Tyler TF, McHugh MP, Mirabella MR, ankle sprain. J Orthop Sports Phys 1her. 11. Kirkpatrick DP, Hunter RE, Janes PC, Mullaney MJ, Nicholas SJ. Risk factors 2009;39(3 ): 188-200. Mastrangelo J, Nicholas RAThe snow­ for noncontact ankle sprains in high 35. Herzog W, Scheele D, Conway PJ. boarder's foot and ankle. Am f Sports school fOotball players: the role of previ­ Elecrromyographic responses of back Med. 1998;26(2):271-277. ous ankle sprains and body mass index. and limb muscles associated with 12. Kujala UM, Nylund T, Taimela S. Acute Am] Sports Med. 2006;34(3):471-475. spinal manipulative therapy. Spine. injuries in orienteerers. Int J Sports Med. 25. Anandacoomarasamy A, Barnsley L. 1999;24(2):146-152; discussion 153. 1995; 16(2): 122-125. Long term outcomes of inversion ankle 36. Murphy BA, Dawson NJ, Slack JR. Sac­ 13. Linko PE, Blomberg HK, Frilander injuries. Brf Sports Med. 2005;39(3):el4; roiliac joint manipulation decreases the HM. Orienteering competition injuries: discussion e) 4. H-reflex. Electromyogr Clin Neurophysiol. injuries incurred in the Finnish Jukola 26. Cross KM, Worrell Tw, Leslie JE, Van 1995;35(2):87-94. and Venia relay competitions. Br J Sports Veld KR. The relationship between self­ 37. Symons BP, Herzog W, Leonard T, Med. 1997;31(3):205-208. reported and clinical measures and the Nguyen H. Reflex responses associated 14. McGaughey I, Sullivan P. The epi­ number ofdays to return to sport follow­ with activator treatment. f Manipulative demiology of knee and ankle inju­ ing acute lateral ankle sprains. f Orthop Physiol1her. 2000;23(3):155-159. ries on Macquarie Island. Injury. Sports Phys 1her. 2002;32(1):16-23. 38. Bulbulian R, Burke J, Dishman JD. 2003;34(11):842-846. 27. Denegar CR, Hertel J, Fonseca J. The Spinal reflex excitability changes afrer 15. Verhagen EA. VanderBeek AJ, Bouter effect of lateral ankle sprain on dorsi­ lumbar spine passive flexion mobili­ LM, Bahr RM, Van Mechelen W. A flexion range of motion, posterior ralar zation. f Manipulative Physiol 1her. one season prospective cohort study glide, and joint laxity. f Orthop Sports 2002;25(8):526-532. of volleyball injuries. Br J Sports Med. Phys 1her. 2002;32(4):166-173. 39. Suter E, McMorland G, Herzog W, 2004;38(4):477 -481. 28. de Noronha M, Refshauge KM, Herbert Bray R. Decrease in quadriceps inhi­ ;. 16. Larsen E, Jensen PK, Jensen PR. Long­ RD, Kilbreath SL, Hertel J. Do volun­ bition afrer sacroiliac joint manipu­ i term outcome of knee and ankle injuries tary strength, proprioception, range of lation in patients with anterior knee in elite football. Scand f Med Sci Sports. motion, or postural sway predict occur­ pain. f Manipulative Physiol 1her. 1999;9(5):285-289. rence of lateral ankle sprain? Br J Sports 1999;22(3): 149-153. 17. van Rijn RM, van Os AG, Bern­ Med. 2006;40(10):824-828; discussion 40. Dishman JD, Ball KA, Burke J. First sen RM, Luijsterburg PA, Koes BW, 828. Prize: Central motor excitability changes Bierma-Zeinstra SM. What is the clini­ 29. Pope R, Herbert R Kirwan J. Effects afrer spinal manipulation: a transcranial cal course of acute ankle sprains? A of ankle dorsiflexion range and pre­ magnetic stimulation study. f Manipula­ systematic literature review. Am J Med. exercise calf muscle stretching on injury tive Physiol1her. 2002;25(1):1-9. 2008;121(4):324-331 e326. risk in Army recruits. Aust J Physiother. 41. Dishman JD, Greco DS, Burke JR. 18. Gerber JP, Williams GN, Scoville 1998;44(3):165-172. Motor-evoked potentials recorded CR, Arciero RA, Taylor DC. Persis­ 30. Willems TM, Witvrouw E, Delbaere from lumbar erector spinae muscles: tent disability associated with ankle K, Mahieu N, De Bourdeaudhuij I, a study of corticospinal excitability sprains: a prospective examination of De Clercq D. Intrinsic risk factors for changes associated with spinal manipu­ an athletic population. Foot Ankle Int. inversion ankle sprains in male subjects: lation. f Manipulative Physiol 1her. 1998;19(10):653-660. a prospective study. Am J Sports Med. 2008;31 (4):258-270. 19. Braun BL. Effecrs of ankle sprain in a 2005;33(3):41 S-423. 42. Taylor HH, Murphy B. Altered senso- general clinic population 6 to 18 months 31. van der Wees PJ, Lenssen AF, Hen-

Orthopm:dic Practiu W.L 25;2:13 101