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Article history:

Accepted 15 January 2015

Keywords:ProprioceptionMusculoskeletal rehabilitation

Introduction: Proprioception can be impaired in gradual-onset musculoskeletal pain disorders and

for assessment and interventions is of vital importance in musculoskeletal rehabilitation. In Part 1 of this

of the spine and extremities. Reference is made to research whereinterventions have been reported to demonstrate positive effectson proprioception. A special focus is made on exercise therapy.

ia, or force sense-built devices orare frequently

7; Docherty et al.,l., 2002; Dochertyrman et al., 2009),tting. Researcherstests for the spineeveloped for some

and renement of clinical tests is needed.

2.1. Clinical apparatus

Goniometers, inclinometers, pressure sensors, and laser-pointers are affordable and easy-to-use in a clinical context.There is also scope for new affordable and accurate technology thatincludes smartphones with built-in accelerometers and gyros,

* Corresponding author.

Contents lists availab

Manual T

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Manual Therapy 20 (2015) 378e387E-mail address: Nicholas.Clark@stmarys.ac.uk (N.C. Clark).of clinical assessment and intervention methods for proprioception body parts (e.g. cervical spine) than others. Further developmenttrol. Proprioception fullls roles in feedback and feedforwardsensorimotor control and regulation of muscle stiffness, beingspecically important for movement acuity, joint stability, co-ordination, and balance. Cervical proprioception is uniquelyimportant for head-eye co-ordination and movement control.Proprioception can be disturbed in musculoskeletal disorders dueto pain, effusion, trauma, and fatigue. A variety of assessment pro-cedures and interventions have been developed to specically testand enhance proprioception, respectively. We present an overview

measuring joint position sense (JPS), kinesthes(Roijezon et al., 2015). In the laboratory, customexpensive computer-interfaced equipmentemployed (Lephart et al., 1994; Borsa et al., 1991998; Waddington et al., 2000; Callaghan et aand Arnold, 2008; Benjaminse et al., 2009; Leabut are typically impracticable in the clinical seand clinicians have attempted to develop clinicaland extremities, although some tests are more dProprioception is essential for well-adapted sensorimotor con- Clinical assessment of proprioception should employ tests forAssessmentIntervention

1. Introductionhttp://dx.doi.org/10.1016/j.math.2015.01.0091356-689X/ 2015 Elsevier Ltd. All rights reserved.motor control, causes and ndings of altered proprioception in musculoskeletal conditions, and generalprinciples of assessment and interventions.Purpose: The aim of this second part is to present specic methods for clinical assessment and in-terventions to improve proprioception in the spine and extremities.Implications: Clinical assessment of proprioception can be performed using goniometers, inclinometers,laser-pointers, and pressure sensors. Manual therapy, taping, and bracing can immediately enhanceproprioception and should be used to prepare for exercise interventions. Various types of exercise (activejoint repositioning, force sense, co-ordination, muscle performance, balance/unstable surface, plyo-metric, and vibration training) should be employed for long-term enhancement of proprioception.

2015 Elsevier Ltd. All rights reserved.

2. Clinical assessment of proprioceptionReceived in revised form4 January 2015 two-part Masterclass we presented a theory-based overview of the role of proprioception in sensori-Received 6 November 2014 following trauma. Understanding of the role of proprioception in sensorimotor dysfunction and methodsMasterclass

Proprioception in musculoskeletal rehabassessment and intervention

Nicholas C. Clark a, *, Ulrik Roijezon b, Julia Treleavea School of Sport, Health, and Applied Science, St Mary's University, Twickenham, Londob Department of Health Sciences, Lule University of Technology, Lule, Swedenc CCRE Spine, Division of Physiotherapy, SHRS, University of Queensland, Brisbane, Aust

a r t i c l e i n f o a b s t r a c t

journal homepage: witation. Part 2: Clinical

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nited Kingdomle at ScienceDirect

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camera systems such as the Kinect, the Wii Balance Board, andother video-based technology.

2.2. Specic tests

2.2.1. Joint position senseFor the cervical spine, active JPS testing can use a laser-pointer

attached to a headband to determine patients' ability to relocateto the neutral starting position with the eyes closed after per-forming an active head movement (e.g. right rotation) (Fig. 1). Thedifference between the starting and end position can be measuredin millimetres, and the joint position error then calculated in de-grees (Roren et al., 2009; Chen and Treleaven, 2013). This method isreliable and valid when compared to sophisticated laboratoryequipment (Swait et al., 2007; Roren et al., 2009; Chen andTreleaven, 2013). Errors greater than 4.5 are considered to indi-cate abnormal cervical active JPS. Others have used the cervicalrange of motion (CROM) device to measure cervical active JPS andfound this to also be a reliable and valid method (Wibault et al.,2013; Treleaven et al., 2015).

For the extremity joints, goniometers (universal, bubble, digital)can also be used tomeasure active JPS. The sequence of events is thesame as that described for laboratory measurement of active JPS(see Masterclass Part 1) (Roijezon et al., 2015). Depending on the

N.C. Clark et al. / Manual Thedevice used and the extremity joint measured, reliability andmeasurement error of active movement goniometry can rangewidely (Gabbe et al., 2004; Lephart et al., 2007; Dickson et al., 2012;Kolber and Hanney, 2012; Hamid et al., 2013), and this should becarefully considered if goniometry is used to measure active JPS ofextremity joints. For the shoulder joint, laser-pointer active JPStests have also been developed and showpromise in thosewith andwithout shoulder injury (Balke et al., 2011). There is potential forusing the laser-pointer to measure JPS in other joints but, to date,there is limited research.

2.2.2. KinesthesiaFor the cervical spine, kinesthesia can be assessed by following a

trace or intricate pattern as accurately as possible. This can be avisual trace (e.g. gure-of-eight, zig-zag pattern) (Woodhouse et al.,

Fig. 1. Cervical Joint Position Sense Assessment. The patient is seated with the laserpointer attached to a headband, 90 cm from the target. The target is adjusted so thatthe laser projects to the centre of the target. They are asked to concentrate on thisresting head position and then close the eyes. They then perform an active movementto comfortable limits and return to the resting head position as accurately as possible.

The difference between the initial and end position can be measured in millimetresand then converted to degrees.2010) or by following a computer generated marker that is movingin a more unpredictable pattern (e.g. the y) (Kristjansson et al.,2004). Outcome variables usually used here are the meandisplacement or time on target. Advances in smart phone sensorshavemade the y technologymore readily accessible to clinicians(Kristjannson, 2014), although recent work has also been con-ducted to investigate the feasibility of a low cost quantitativemethod using video analysis of the patient tracing a pattern with ahead-mounted laser (Pereira et al., 2015).

2.2.3. Force senseForce sense can be measured by the accuracy of reproducing a

specic target force. For example, the pressure biofeedback deviceused for assessing the cranio-cervical exion test could beconsidered a method of assessing force sense in the cervical spine(Jull, 2000). The ability to hold steadily or the accuracy in achievingand maintaining a desired pressure can be used. Others have alsoused custom-made dynamometry placed at the mandible to mea-sure precision and accuracy of maintaining low load upper cervicalexor force levels (O'Leary et al., 2005).

2.3. Non-specic tests

2.3.1. Balance testsBalance tests, such as timed single-leg stance tests, have his-

torically been used to measure lower extremity (e.g. ankle) pro-prioception. As discussed previously (see Masterclass Part 1)(Roijezon et al., 2015), these tests are not specic tests of proprio-ception since balance is a product of integrating sensory, centralnervous system (CNS), and motor functions (Macpherson andHorak, 2013). Nevertheless, balance tests could potentially give anindication of improvement following proprioceptive training. Bal-ance tests can be modied to try to bias proprioception by, forexample, closing the eyes, adding neck torsion, or using unstablesurfaces (Roijezon et al., 2015).

2.3.2. Oculomotor and eye-head coordination testsOculomotor and eye-head co-ordination assessment in people

with neck pain is important as cervical spine afferents have aunique and important role in maintaining eye and head movementcontrol (Corneil et al., 2002; Peterson, 2004). At present, clinicaltests incorporate qualitative assessment of the ability to: 1) main-tain gaze while moving the head; 2) co-ordinate eye and headmovement; 3) eye follow while keeping the head still in neck tor-sion compared to neck neutral positions (Fig. 2). Recent researchhas found these clinical tests to be reliable and able to discriminatebetween chronic neck pain and asymptomatic individuals (DellaCasa et al., 2014), and are described in detail elsewhere(Treleaven, 2008; Grip et al., 2009; Treleaven et al., 2011).

3. Clinical interventions to improve proprioception

In Part 1 of this Masterclass (Roijezon et al., 2015), the impor-tance of addressing causes of altered proprioception and rehabili-tation techniques intended to enhance proprioception wereintroduced. Pain, effusion, and fatigue can be common aftermusculoskeletal injury, result in impaired proprioception(Treleaven et al., 2003; Anderson and Wee, 2011; Cho et al., 2011),and, consequently, are barriers against effective interventions forenhancing proprioception and sensorimotor control. Therefore, it isimportant to administer techniques to reduce pain, effusion, andfatigue in order to facilitate the implementation of effective in-terventions to enhance proprioception. Augmentation of somato-sensory information via passive techniques such as manual

rapy 20 (2015) 378e387 379therapy, soft tissue techniques, and taping or bracing can be

Some researchers have reported that specic soft tissue techniquescan signicantly and positively affect extremity joint propriocep-tion dened by measures of active JPS (Henriksen et al., 2004).

3.2. Taping and bracing

Taping and bracing techniques are adjunct interventions used toobtain specic clinical effects including, for example, pain relief,swelling control, and protect injured anatomical structures(Macdonald, 2004). Another clinical goal of applying athletic tape(Fig. 3) and different types of brace is to enhance proprioception(Macdonald, 2004) via stimulation of mechanoreceptors respond-ing to skin stretch and compression during joint motion (Martinand Jessell, 1991; Rothwell, 1994). Authors have reported that theapplication of selected athletic taping techniques, elastic bandages,and neoprene sleeves can immediately and signicantly enhancespinal and extremity proprioception in uninjured and injured in-dividuals (Lephart et al., 1992; Jerosch et al., 1995; Jerosch andPrymka, 1996; Simoneau et al., 1997; McNair and Heine, 1999;Newcomer et al., 2001; Callaghan et al., 2002; Chu et al., 2002;Chang et al., 2010).

Therapy 20 (2015) 378e387N.C. Clark et al. / Manual380important. Exercise therapy is a vital component in enhancingproprioception and will be considered in detail. In order to deducethat a clinical intervention yields a proprioceptive effect, one of thespecic modalities of proprioception (JPS, kinesthesia, force sense)must be measured before and after the intervention. The followingsections will, therefore, refer only to research where this hasoccurred.

3.1. Manual therapy

Joint mobilisation/manipulation can create a controlled stretchto capsuloligamentous tissue (Kaltenborn, 1999; Greenman, 2003),which is populated with multiple types of mechanoreceptors(Kennedy et al., 1982; McLain and Raiszadeh, 1995; Michelson andHutchins, 1995; Steinbeck et al., 2003; Moraes et al., 2011), therebyaffecting proprioceptive feedback to the CNS. Authors have re-ported that joint passive movement techniques can have an im-mediate and signicantly benecial effect on spinal and extremityproprioception (Heikkila et al., 2000; Vicenzino et al., 2005;Palmgren et al., 2006; Learman et al., 2009; Ju et al., 2010; Haavikand Murphy, 2011). Similarly, soft tissue techniques including awide variety of body segment massage and localized connectivetissue techniques mechanically affect the skin, connective tissue(e.g. fascia), and muscles (Goats and Keir, 1991; Goats, 1994;Greenman, 2003), which are also richly innervated with mecha-noreceptors (Yahia et al., 1992; Rothwell, 1994; Stecco et al., 2007).

Fig. 2. Eye Follow in Neck Torsion. The patient keeps the head still while followingwith the eyes as accurately as possible a moving target (e.g. or a pen) with the eyes.The target is moved slowly side to side (20 per second through a visual angle of 40).The test is repeated with the neck in torsion (head still but with the trunk rotated up to45) then repeated on the opposite side. Any difference noted in smooth eye follow(quick catch up eye movements) in these positions compared to the neutral position isnoted.Fig. 3. Proprioception Knee Taping Technique (Modied from Callaghan et al., 2002).Copyright Nicholas Clark. Reproduced with permission.

3.3. Exercise therapy

Any active exercise can be considered proprioceptive trainingbecause it will generate a barrage of afferent impulses to the CNSfrom joint and muscle-tendon mechanoreceptors (Clark andHerrington, 2010; Clark and Lephart, 2015). Thus, active exerciseswould seem a vital component in augmenting proprioception(Perez et al., 2004; Lagerquist et al., 2012; Clark and Lephart, 2015).There is, however, much overlap across the potential purposes,goals, and clinical uses for any single exercise. Terminology used inexercise therapy (e.g. proprioceptive training, strength training)can mean different things to different clinicians and researchers. Asingle exercise can result in multiple different physiological andphysical adaptations in several body systems. In general, exercisetherapy refers to the performance of repeatedmovements as part ofa goal-directed training programme to improve a physiological orphysical characteristic (Clark and Lephart, 2015). For the purpose ofthis paper we offer simplistic denitions according to the primarycharacteristics of the exercise task, introduce basic concepts, offerselected clinical examples, and present research reports on theeffect of an exercise type on proprioception.

3.3.1. Active joint repositioning trainingObservation of injury mechanisms suggests that there are spe-

head to a pre-determined target angle, or returning the head asclosely as possible to the initial position after movement, checkingaccuracy by opening the eyes (Revel et al., 1994). For the extrem-ities, both open (Fig. 4) and closed kinetic chain exercises can beemployed with emphasis on repositioning training occurringwithin the specic range-of-motion associated with a specicinjury type (Borsa et al., 1994; Lephart and Henry, 1996). Headrepositioning training with eyes open and eyes closed has beendemonstrated to improve cervical JPS patients with chronic neckpain (Revel et al., 1994; Jull et al., 2007). For peripheral joints,including the shoulder and knee, the addition of a low externalload to a limb segment (5e10% bodyweight) signicantly improvedthe accuracy of joint repositioning tasks in uninjured individuals(Lamell-Sharp et al., 2002; Brindle et al., 2006; Suprak et al., 2007).

3.3.2. Force sense trainingPerception of force and effort can be trained by activating a

muscle or muscle group to a predetermined amount of force, ormaintaining the same amount of force for a dened period-of-time(e.g. 10 s) (Jull et al., 2007). Cranio-cervical exor training using thepressure biofeedback unit (Fig. 5) has demonstrated improvedprecision for maintaining a low level upper cervical exion force inpeople with neck pain (O'Leary et al., 2007), and improved forcepressure levels achieved in people with cervicogenic headache (Jull

ointioce

N.C. Clark et al. / Manual Therapy 20 (2015) 378e387 381cic points in a joint's range-of-motion at which a joint is at risk ofinjury. For example, non-contact injuries occur between 9 and 22

plantarexion in the ankle (Mok et al., 2011), 10 and 60 exion inthe knee (Koga et al., 2010), and at extremes of external rotation inthe shoulder (Wassinger and Myers, 2011). This suggests there maybe a position of vulnerability in a joint's range-of-motion that maybe related to proprioceptive decits (Myers and Lephart, 2000).Active joint repositioning training involves a similar procedure tothat used in JPS testing: a starting positon/angle and target posi-tion/angle are selected, and training involves moving from oneposition to another as closely as possible, holding each for a shortduration (e.g. 5 s) (Myers and Lephart, 2000; Suprak et al., 2007). Adifference between JPS testing and training is that visual feedbackcan be permitted for how accurately the task is performed. For thecervical spine, training can be performed by actively moving the

Fig. 4. Shoulder Joint Active Repositioning Training. A target angle that lies at a specic protation). A low external load is added to the limb (e.g. 1 kg dumb-bell) to enhance propr0 external rotation, and then eccentrically externally rotate as closely as possible to the tar

and then concentrically return to the start position. This can be performed with eyes openet al., 2002).

3.3.3. Co-ordination trainingCo-ordination is the process of controlling the activation of

many different muscles so that they act together simultaneously asa single functional unit (Gordon, 1991), and the process of inte-grating different body parts in specic movement patterns (Kent,2006). Co-ordination training has a different connotationcompared to movements in other types of exercise therapy. Weconsider co-ordination training to have primary emphasis oncueing an individual to specically concentrate on very ne aspectsof sequencing and linking multiple muscles and/or body-parts. Co-ordination training, thus, requires precise verbal cueing for theclinician and a high cognitive demand for the patient. Examples ofco-ordination training are preferential activation of one muscle

within the range-of-motion associated with shoulder injury is chosen (e.g. 80 externalption via increased mechanoreceptor stimulation. The individual is instructed to start at

get angle, isometrically hold for up to ve seconds, concentrate on feeling the position,or eyes closed. Copyright Nicholas Clark. Reproduced with permission.

in uninjured military cadets (Rogol et al., 1998). General ankleanisometric elastic resistance strength training was reported tosignicantly enhance ankle inversion and plantarexion active JPSin athletes with functional ankle instability (Docherty et al., 1998),

Fig. 6. Side-Lying Loaded Ankle Eversion. An external load is added to the foot (e.g. 2kg ankle-weight). The individual is then instructed to perform dynamic eversionagainst gravity. Traditional resistance training programme design methods are applied(e.g. 3 sets 10 repetitions, 3 sessions per week). Copyright Nicholas Clark.Reproduced with permission.

Theversus another muscle within a synergistic muscle group (Jull et al.,2007), specic eye-head-neck co-ordination during neck move-ments (Revel et al., 1994; Humphreys and Irgens, 2002), and foot-shank-thigh co-ordination on an elliptical training device (Leeet al., 2014). Different types of co-ordination training haveenhanced proprioception of the spine and extremities. Cranio-cervical exor training focusing on use of the deep upper cervicalexors versus the supercial cervical exors can signicantlyenhance cervical active JPS in people with neck pain (Jull et al.,2007). Eye head neck co-ordination exercises demonstratesimproved JPS in people with neck pain (Humphreys and Irgens,2002). Fine foot orientation training during external perturba-tions on an elliptical training device has been shown to signicantlyimprove passive foot kinesthesia during full weight-bearingmovements in uninjured adults (Lee et al., 2014). Whole body co-ordination exercises including yoga and tai chi have also demon-

Fig. 5. Force sense training using the pressure biofeedback unit (PBU) in cranio-cervical exion training (CCFT). The patient is given feedback of the force appliedduring the incremental stages of CCFT (22e30 mmHg) from the PBU. Patients closetheir eyes during the task and then open them to check they have reached theappropriate level.

N.C. Clark et al. / Manual382strated improvements in proprioception (Tsang and Hui-Chan,2003; Cramer et al., 2013).

3.3.4. Muscle performance trainingThe terms muscle performance and muscle strength both

broadly refer to the ability of a muscle to produce force, regardlessof the action (isometric vs. anisometric), load (body segment vs.free-weight), or intensity (low load vs. high load) (Mayhew andRothstein, 1985; Sapega, 1990; Clark, 2001). Muscles must rstpossess inherently sufcient muscle strength before they caneffectively control the mass, orientation, and alignment of bodysegments (Borsa et al., 1994; Hodges and Moseley, 2003;Macpherson and Horak, 2013). Muscle performance training usu-ally involves the repeated activation of skeletal muscle around aprimary axis-of-rotation and in a single plane-of-motion, typicallyagainst some resistance (body segment or an added external load),with the primary intent of modifying muscle force generatingcharacteristics. Examples are side-lying loaded shoulder externalrotation, double-leg bodyweight squats, and side-lying loadedankle eversion (Fig. 6). Muscle performance training has been re-ported to benecially modify proprioception. In the spine,controlled head lift exercise in people with neck pain demonstratedimproved force sense (O'Leary et al., 2007). Scapular and gleno-humeral anisometric bodyweight and dumb-bell strength traininghas been reported to signicantly improve glenohumeral active JPSrapy 20 (2015) 378e387and ankle invertor and evertor isokinetic strength training has alsobeen reported to signicantly improve ankle inversion passive JPSin recreational athletes with functional ankle instability (Sekir et al.,2007).

3.3.5. Balance/unstable surface trainingBalance is the process of maintaining the body's center of mass

within its base of support via appropriate internal momentsresisting destabilizing external moments acting on the body(Macpherson and Horak, 2013). Balance is the result of feedbackand feed-forwards corrective movements at multiple joints tomaintain the position and orientation of one body segment relativeto another over the base-of-support (Macpherson and Horak,2013). Balance training typically involves performing exercises onan unstable surface (e.g. rocker-board, inatable devices) (Clark andHerrington, 2010). Examples of balance training exercises arestanding balance tasks on soft surfaces or wobble-boards (Beinertand Taube, 2013), performing cervical movements whilst chal-lenging balance (Gatti et al., 2011), press-ups on a Swiss-ball (Myersand Lephart, 2000), and single-leg squats on a rocker-board (Fig. 7)(Clark and Herrington, 2010). Single-leg stance, tandem stance, anddouble-leg stance on a wobble-board has enhanced cervical spineactive JPS in a group of people with sub-clinical neck pain (Beinertand Taube, 2013). Lower extremity wobble-board training hasenhanced ankle active kinesthesia (active movement

to mid-stance of gait, lower extremity extensors use eccentricmuscle actions to decelerate the body, followed by very brief iso-metric muscle actions, before transitioning to concentric muscleactions to accelerate the body from mid-stance to push-off (Komi,1992; Chu, 1998). Plyometric training uses the SSC as a keyfeature during the execution of exercise drills. Plyometric trainingmust be executed rapidly with meticulous technique withemphasis on the transition between eccentric and concentricmuscle actions being as fast and short duration as possible (Chu,1998). Examples of plyometric training exercises are kneeling 90-90 shoulder internal-external rotations against elastic resistance(Swanik et al., 2002) (Fig. 8), double-leg barrier jumps (Chu, 1998)(Fig. 9), and single-leg in-place (vertical) hops (Clark andHerrington, 2010). Plyometric training can benecially modifyproprioception of the extremities. Kneeling 90-90 shoulder inter-nal-external rotations against elastic resistance and ball throwing

Therapy 20 (2015) 378e387 383N.C. Clark et al. / Manualdiscrimination) in uninjured, elite rugby league players(Waddington et al., 1999), Australian Rules Football players(Waddington et al., 2000), and independent older people(Waddington and Adams, 2004). Swiss-ball training was shown tosignicantly improve knee passive JPS in uninjured students (Cuget al., 2012). Upper extremity wobble-board training has been re-ported to signicantly enhance shoulder active kinesthesiafollowing shoulder dislocation (Naughton et al., 2005). A lowerextremity exercise programme including a rocker-board, wobble-board, mini trampoline, tilted platform, and uneven walkway hasalso been reported to signicantly improve ankle passive JPS inadults with functional ankle instability (Eils and Rosenbaum, 2001).

3.3.6. Plyometric trainingMany functional tasks demonstrate an eccentric-isometric-

concentric sequence of muscle actions termed the stretch-shortening cycle (SSC) (Chu, 1998). For example, from foot-strike

drills against a mini-trampoline have been reported to signicantlyimprove glenohumeral active JPS and passive kinesthesia in unin-jured elite swimmers (Swanik et al., 2002). Jump-landing andjump-landing with change-of-direction training has been reportedto signicantly improve knee active kinesthesia in uninjuredAustralian Rules Football players (Waddington et al., 2000).

Fig. 7. Single-Leg Rocker-Board Squat. Copyright Nicholas Clark. Reproduced withpermission.Fig. 8. Kneeling 90-90 Plyometric Shoulder Internal-External Rotation (From Swaniket al., 2002). The individual is instructed to perform concentric shoulder internalrotation to 90 , hold the position for two seconds, and then release the isometric holdso that the tubing rapidly recoils and pulls the shoulder into external rotation. As soonas the desired amount of external rotation is achieved, the individual is instructed tostop the external rotation recoil and again perform concentric internal rotation to 90 .Traditional plyometric training programme design methods are applied (e.g. 3 sets

15 repetitions, 2 sessions per week). Copyright Nicholas Clark. Reproduced withpermission.

3.3.7. Vibration training

Fig. 9. Double-Leg Barrier Jumps. Copyright Ni

N.C. Clark et al. / Manual The384Vibration is a mechanical event that demonstrates rapid oscil-latory movements and is a powerful stimulus for the musclespindle (Goodwin et al., 1972; Roll and Vedel, 1982). Vibrationtraining involves exercising with a device that produces a vibrationstimulus (e.g. vibration platform), where the combination of mus-cle activationwith the rapid small amplitude change in direction ofjoint motion becomes a powerful stimulus for the muscle spindle(Cardinale and Bosco, 2003). The intensity of the vibration isdetermined by the amplitude and frequency of the oscillations(Cardinale and Bosco, 2003), and devices vibrating from 5 to 50 Hzare typically used in training (Fontana et al., 2005; Moezy et al.,2008; Tripp et al., 2009). Examples of vibration training includeFig. 10. Modied push-ups on a vibration platform.modied push-ups (Hand et al., 2009) (Fig.10), bodyweight double-leg squats and bodyweight lunges onto a vibration platform (Moezyet al., 2008). Vibration training can alter proprioception of the spineand extremities. Isometric neck extension using a sling systemwithsuperimposed vibration stimuli signicantly enhanced force sense(steadiness) of the cervical spine in chronic neck pain (Muceli et al.,2011). Postural exercise involving lumbar hyperlordosis isometricholds while standing on a vibration platform signicantly improvedsingle-session lumbar spine active JPS (Fontana et al., 2005), andisometric elbow exion holding a vibrating dumb-bell has beenreported to signicantly enhance elbow active JPS within in a singletraining session (Tripp et al., 2009). Isometric and anisometricdouble-leg and single-leg balance, squat, and lunge exercises on avibrating platform has also shown improvement in knee active JPSafter anterior cruciate ligament reconstruction (Moezy et al., 2008).cholas Clark. Reproduced with permission.

rapy 20 (2015) 378e3874. Summary

Clinical assessment of proprioception can be performed usinggoniometers, inclinometers, laser-pointers, and pressure sensors.These devices can be employed in a clinical context within tests ofactive JPS and kinesthesia, and force sense. Balance tests can also beemployed in a clinical context for measuring integrated sensori-motor control of balance, but it should be remembered that theseare not able to isolate proprioception alone. In the cervical spine,head and eye movement control should also be assessed as one ofthe important roles of proprioception. Following musculoskeletalinjury, pain, effusion, and fatigue can result in impaired proprio-ception, and so these causes of impaired proprioception should betreated alongside the implementation of other interventions.

Manual therapy interventions (joint mobilisations, manipula-tions, soft tissue techniques) taping, and bracing show the ability toimmediately and benecially affect proprioception. Several types ofexercise therapy have also demonstrated long-term improvementsin proprioception in the spine and the extremities. Althoughmanual therapy, taping, and bracing can immediately and bene-cially affect proprioception, concern has been statedwith regards tothe size and duration of therapeutic effects of passive interventions(Cook, 2011). Nevertheless, these passive interventions can beemployed immediately prior to same-session active rehabilitation

Table 1Proposed specic example exercises to benecially affect proprioception of different body parts.

Exercise type Cervical spine Lumbar spine Upper limb Lower limb

Active jointrepositioning (JPS)training visualfeedback

Repositioning head to neutraland other points in ROM usinglaser-pointer (sitting, standing,SLS)

Repositioning spine to neutral,points in range (sitting, standing,four-point kneeling)

OKC and CKC shoulder, elbow,wrist, nger repositioning todifferent points in ROM

OKC and CKC hip, knee, anklerepositioning to different pointsin ROM

Path-of-motion(kinesthesia)training

Following a line or pattern (zig-zag, gure-of-eight, computergenerated) using a laser-pointer on the head or motionsensors

Tracing patterns with laser-pointerMovement acuity exercises of wristand ngers (using smartphone orsurfpad)

Tracing pattern with laser-pointer (letters of alphabet withfoot and ankle)

Force sense training CCFT with PBUForce and effort perceptiontraining using a dynamometerat pre-determined percentageof isometric MVMA (exors,extensors, lateral exors,rotators)

Abdominal muscle training withPBUForce and effort perception trainingusing a dynamometer at pre-determined percentage of isometricMVMA (exors, extensors, lateralexors)

Force and effort perception trainingof hand and ngers with grip/pinchdynamometerForce and effort perception trainingusing a dynamometer at pre-determined percentage of isometricMVMA (shoulder external rotators,elbow exors, wrist extensors)

Force and effort perceptiontraining using a dynamometerat pre-determined percentageof isometric MVMA (hipexternal rotators, knee exors,ankle evertors)

Co-ordinationtraining

Head-eye co-ordinationTrunk-head co-ordinationEye, head, trunk, arm co-ordinationCCFTNeck extension with neutralupper cervical spineGaze stability (eyes still, headmoves into exion, extensionand rotation)Eye follow side to side head stillin head neutral and in torsion

TrA-multidus co-activationUL and LL movement whilemaintaining trunk stability (neutrallumbar spine)Pilates

Scapular inter-muscular co-ordination (scapular upwardrotation force couple)Rotator cuff co-ordination withgross UL movementsWrist, hand, nger ne co-ordination tasks

Gluteus maximus-hamstringsco-ordination during prone SLRGluteus medius-TFL co-ordination during hipabduction variationsPelvis-hip-knee-ankle-footalignment training during CKCtasksKnee valgus-varus movementcontrol during CKC tasksFoot-shank-thigh co-ordinationon elliptical trainerTai Chi

Muscle performancetraining

CCFT low-load enduranceCervical extensor training infour-point kneeling externalloadHead-lifts into exion,extension, lateralexion external load

TrA, multidus enduranceCurl-upsTrunk extensor, front-plank, side-plank isometric holds

Bodyweight strength trainingResistance training machinesFree-weightsElastic resistance training

Bodyweight strength trainingResistance training machinesFree-weightsElastic resistance training

Balance/unstablesurface training

Standing (eyes open or closed;narrow, tandem, SLS on rmthen soft surface (foam) thenunstable surface (rocker board))Perform other exercises whilein unstable positions (JPS, eyeco-ordination)Tandem walk, walking withhead movementNeck resistance training inslingsControl motion of a movingobject with the head and neck(ball on head)

Standing (eyes open or closed;narrow, tandem, SLS on rm thensoft surface (foam) then unstablesurface (rocker board))Sitting on a Swiss-ball ULmovementsStabilising the trunk whileperforming active UL movementswhile controlling an oscillating polePerforming active movements oftrunk while controlling oscillatingpole or Swiss-ball

Press-ups on a Swiss-ball orwobble-boardPress-ups with legs elevated on aSwiss-ballWrist gyroscopic exercise balltrainingActive UL movements whilecontrolling an oscillating poleControl of ball on wall withshoulder and UL

Standing (eyes open or closed;narrow, tandem, SLS on rmthen soft surface (foam) thenunstable surface (rocker board))Standing as above distraction/perturbation from clinician(ball throwing/catching, pelvicgirdle rhythmic stabilisations)Single-leg squats on rocker-boardWobble-board, Swiss-ball,mini-trampoline training

Plyometric training Plyoball sit-upsPlyoball back extensionPlyoball long-sitting side throws

Kneeling 90-90 shoulder internal-external rotations against elasticresistanceClapping press-upsBall throwing/catching against mini-trampoline

Double-leg and single-leg hops,leaps, jumps,bounding barriers, boxes,platformsDepth jumpsSkipping drills

Vibration training Neck extension resistancetraining with vibration added

Lumbopelvic postural exerciseswhile standing of vibrationplatform

Push-ups on vibration platformElbow, wrist movement withvibrating dumb-bellsArm movement with oscillatingpole

Double-leg and single-legsquats on vibration platformLunges on vibration platform

ROM range-of-motion.SLS single-leg stance.OKC open kinetic chain.CKC closed kinetic chain.CCFT cranio-cervical exion training.PBU pressure biofeedback unit.JPS joint position sense.MVMA maximum voluntary muscle action.TrA transversus abdominis.UL upper limb.LL lower limb.SLR straight leg raise.

N.C. Clark et al. / Manual Therapy 20 (2015) 378e387 385

Thewith a view to assisting patients to prepare for specic exercisetherapy interventions and functional movements (Clark andLephart, 2015). Thus, it is likely that a mixed mode interventionapproach is optimal for enhancing proprioception in clinicalpractice.

As discussed in Part 1 of this Masterclass (Roijezon et al., 2015),different exercise types will affect the CNS in different ways. Someexercises will preferentially affect supraspinal levels of the CNS (e.g.cerebrum), while others preferentially affect spinal cord levels and,therefore, inuence different aspects of proprioception in differentfunctional contexts. The types of exercise commonly used toimprove proprioception can vary according to different functionaldemands of the body areas and joints. Exercises (active jointrepositioning, force sense, co-ordination, muscle performance,balance/unstable surface, plyometric, and vibration training)should be used to facilitate long-term benecial adaptations inproprioception and enhance overall sensorimotor control (Clarkand Lephart, 2015). There is also evidence that different exercisetypes can enhance proprioception in asymptomatic individualsand, therefore, may have specic clinical utility for the preventionand rehabilitation of musculoskeletal disorders.

Based on research presented here, examples of exercises tobenecially affect proprioception of different body parts are pro-posed in Table 1. Future directions should consider advances inclinical assessment of proprioception, which is lacking in a numberof areas. This might also direct future research towards identifyingother interventions, or the most appropriate combinations of in-terventions, to improve proprioception in musculoskeletalrehabilitation.

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Proprioception in musculoskeletal rehabilitation. Part 2: Clinical assessment and intervention1. Introduction2. Clinical assessment of proprioception2.1. Clinical apparatus2.2. Specific tests2.2.1. Joint position sense2.2.2. Kinesthesia2.2.3. Force sense

2.3. Non-specific tests2.3.1. Balance tests2.3.2. Oculomotor and eye-head coordination tests

3. Clinical interventions to improve proprioception3.1. Manual therapy3.2. Taping and bracing3.3. Exercise therapy3.3.1. Active joint repositioning training3.3.2. Force sense training3.3.3. Co-ordination training3.3.4. Muscle performance training3.3.5. Balance/unstable surface training3.3.6. Plyometric training3.3.7. Vibration training

4. SummaryReferences