Proprioception and Ankle Injuries

Clin Sports Med 27 (2008) 195217

CLINICS IN SPORTS MEDICINEeccentric training of thigh muscles, proprioceptive training, dynamic stabiliza-tion, and plyometrics with straight leg alignment. The benefits of the programinclude improved performance and injury prevention.

Arnason and colleagues [15] have found that previously sprained ankles ofsoccer players had an increased frequency of lateral instability comparedwith ankles without previous injury. They stated that athletes with formera group of international experts. The exercises focus on core stabilization,

Football Federations (FIFA) medical research center in cooperation within Soccer

Emin Ergen, MD, PhD*, Bulent Ulkar, MD, PhDSports Medicine Department, Ankara University School of Medicine,Cebeci 06590, Ankara, Turkey

Soccer has the highest participation rate in the world with more than 200million players worldwide [1]. It is known to be associated with a rela-tively high injury rate. For some industrial occupations regarded as high

risk, injury level of professional players is shown to be almost 1000 times higher[2]. Ankle sprains are defined as the most common musculoskeletal injuries thatoccur in athletes [3,4]. Several studies have noted that sports requiring suddenstops and cutting movements, such as soccer, cause the highest percentage ofthese injuries [35]. Ankle sprains not only result in significant time lost fromsports participation, they can also cause long-term disability and have a majorimpact on health care costs [4]. According to the results of studies, the mostfrequent injuries of adolescent [6,7] and female [8] soccer players are anklesprains. Some of the intrinsic risk factors involved in ankle injuries have beenidentified as previous sprains, foot type and size, ankle instability, joint laxity,reduced lower extremity strength, and anatomic malalignment [911].

Dvorak and colleagues [12] also supported the observation by Inklaar [10]that the high rate of reinjury suggests that inadequate rehabilitation or incom-plete healing is an important risk factor. Soccer, like most sports, is associatedwith a certain risk of injury for players. Scientific studies have shown, however,that the incidence of football injuries can be reduced by prevention programs[4,13,14].

A prevention program called The 11 was developed by the International*Corresponding author. E-mail address: ergen@medicine.ankara.edu.tr (E. Ergen).

0278-5919/08/$ see front matter 2008 Elsevier Inc. All rights reserved.doi:10.1016/j.csm.2007.10.002 sportsmed.theclinics.com

196 ERGEN & ULKARinjury represented about five times the reinjury risk, indicating the necessity ofa more intensive preventive medical care program.

There are several discussions about the possibilities for prevention of a soccerinjury, such as warm-up with more emphasis on stretching, regular cool-down,adequate rehabilitation with sufficient recovery time, proprioceptive training,protective equipment, good playing field conditions, and adherence to theexisting rules [1]. Among these, proprioceptive or neuromuscular training isstrongly emphasized in the latest reviews and research [4,13,14,16]. Assessingthe best injury prevention strategies for soccer requires a complete understand-ing of the factors that contribute to both the occurrence of these injuries and theuptake of, or compliance with, potential prevention strategies [17].

Long-term injury-prevention strategies, such as introducing proprioceptiveand coordination activities implemented into the training sessions, especially inthe preseasonal preperations, preferably from very early ages are of paramountimportance to reduce not only ankle injuries but also other soccer injuries.

From the sports medicine perspective, the coordination of a movement ismainly the internal organization of optimal control of the motor system andits parts [18]. Coordination can be regarded as an umbrella term embracingthe concept of optimization for intramuscular and intermuscular coordinationand cooperation for a given task including internal and external feedbackmechanisms. These mechanisms are disrupted in case of an injury and the con-tinuation of information processing is ceased, which leads to performancedeteriorations and reinjury. To prevent athletic injuries and program therehabilitation after a joint lesion, understanding the role of proprioception isessential. The terms proprioceptive deficit, proprioceptive training, andproprioceptive (or neuromuscular) rehabilitation are used increasingly insports medicine [19].

DEFINITIONSCoordination is defined as a cooperative interaction between the nervous sys-tem and skeletal muscles [18]. This is particularly important for the preventionof injuries in a risky sports situation, such as cutting, dribbling, jumping, andlanding. Coordination encompasses proprioceptive abilities. With regard toproprioception, many researchers have defined it as the afferent input of jointposition sense (ie, awareness of position or movement), whereas others con-sider proprioception in a broader sense that includes neuromuscular control.Most contemporary authorities define proprioception as a specialized variationof the sensory modality of touch that includes the sensation of joint movement(kinesthesia) and joint position (joint position sense) [20].

Somatosensorial receptors are located in muscles, tendons, joints, and othertissues. Classically, three types of somatic senses are described: (1) pain, (2)thermoreceptivity, and (3) mechanoreceptivity. Proprioception relates primar-

ily to mechanoreceptive sensation, which includes tactile and position sense.Proprioception encompasses two aspects of position sense: static and dynamic.Static sense gives conscious orientation of one body part with respect to

another. Dynamic sense provides the neuromuscular system feedback aboutthe rate and direction of a movement. Proprioception can be thought of asa complex neuromuscular process that involves both afferent input and efferentsignals and allows the body to maintain stability and orientation during bothstatic and dynamic activities [21]. Afferent information for necessary fine tuningof movements is provided by proprioceptive, visual, vestibular, and somatosen-sorial receptors (Fig. 1).

PROPRIOCEPTIVE ORGANS: MECHANORECEPTORSTwo-way communication between sensory and motor systems is crucial fornormal motor control. Visual input is one of the most important aspects in pro-prioception. Information from the vestibular apparatus about head position inrelation to gravity and to head movements is also important. The other impor-tant body sense is obtained through somatosensorial receptors. The sensoryreceptors for proprioception that are found in the skin, muscles, and jointsand in ligaments and tendons all provide input to the central nervous system(CNS) regarding tissue deformation [22].

197PROPRIOCEPTION AND ANKLE INJURIES IN SOCCERSOMATIC JOINT

TOUCH PAIN TEMPERATURE

Receptors

Ruffini endings Paccinian corpuscles Free nerve endings Muscle spindles Golgi tendon organSpecialized nerve endings and proprioceptive mechanoreceptors (paciniancorpuscles, Ruffinis endings, Golgi tendon organlike endings) have been his-tologically identified in the knee joint in the capsule [2325], anterior cruciateligament [26,27], posterior cruciate ligament [28], meniscus [29], lateral collat-eral ligament [30], and infrapatellar fat pad [31].

Mechanoreceptors are specialized neurons that transmit mechanical defor-mation information (eg, joint rotation caused by positional change and motion)

AFFERENT PROPRIOCEPTIVEORGANS AND RECEPTORS

VISUAL ORGAN VESTIBULAR ORGAN SOMATOSENSORIAL RECEPTORSFig. 1. Afferent proprioceptive organs and receptors.

tinuous stimulus. Quick-adapting mechanoreceptors are very sensitive tochanges in stimulation and are considered to mediate the sensation of joint

198 ERGEN & ULKARmotion. Quick-adapting mechanoreceptors may be more important in somesports characterized by sudden directional changes, such as pivoting, shifting,tackling, and so forth. Slow-adapting mechanoreceptors are maximally stimu-lated at certain joint angles, and a continuum of slow-adapting receptors isthought to mediate the sensation of joint position [34,35]. When there is no cap-sule-ligamentous strain (or load) on the joint (midrange of position), afferentneurons are not active and they do not play a role in proprioception.

The muscle spindle receptor is a complex, fusiform, slow-adapting receptorlocated within skeletal muscle. By way of afferents and efferents to intrafusalmuscle fibers, the muscle spindle receptor can detect muscle tension over a largerange of extrafusal muscle length. The monosynaptic stretch reflex involvesmuscle spindle receptor connecting I-a nerve fibers and Golgi tendon organsconnecting to I-b fibers. During rapid perturbation, such as tripping or falling,monosynaptic reflexes are absent and compensation occurs as a result of trans-mission along group II and III afferent fibers from secondary muscle spindles[36].

BRAIN REGIONS INVOLVED IN ANKLE MOVEMENTSCiccarelli and colleagues [37] have investigated defining cortical and subcorticalstructures activated during both active and passive movements of the ankle.Sixteen healthy subjects, all right-foot dominant, were asked to perform a dor-siplantar flexion task of the foot using a custom-made wooden manipulandum,which enabled measurements of the movement amplitude. All subjects were in-volved in a training session, which included surface electromyography, andable to relax completely during passive movements. Patterns of activation dur-ing active and passive movements and differences between functional MRIresponses for the two types of movement were assessed. Common activationsduring active and passive movements have been found in the contralateral pri-into electrical signals [32,33]. Each of the previously mentioned five mechano-receptor types responds to different stimuli and transmits specific afferent infor-mation that modifies neuromuscular function. All receptors need a stimulusto change their membrane potential causing an action potential to travel tothe CNS. Mechanoreceptors can also be stimulated by muscle-length change,including the rate of change in tension and length.

Mechanoreceptors demonstrate different adaptive characteristics related totheir response to a stimulus. Quick-adapting mechanoreceptors (pacinian cor-puscle) decrease their discharge rate to extinction within milliseconds of theonset of a continuous stimulus. Slow-adapting mechanoreceptors (Ruffinisending and the Golgi tendon organ) continue to discharge in response to a con-mary motor and sensory cortices. Additionally, it has been observed that thepremotor cortical regions (eg, the bilateral rolandic operculum and contralat-eral supplementary motor area) and the subcortical regions (eg, the ipsilateral

cerebellum and contralateral putamen) also participate in sensorimotor integra-tion for ankle movements.

CLINICAL IMPORTANCE OF PROPRIOCEPTIONIn any specific situation there are gravity, inertia, and reaction forces creatinga specific external load on musculoskeletal structures. This load is counteractedby the internal forces and the internal forces balance the external. Good propri-oception and coordination means that all the components of musculoskeletalfitness are in balance to overcome any overload on structures, and this isimportant in maintaining dynamic joint stability [38].

Dynamic joint stability can be defined as the ability of appropriately acti-vated muscles to stabilize a joint together with the support of mechanical stabi-lizers. In essence, functional (dynamic) joint stability is the product of theproprioceptive system (Fig. 2) [19]. Trauma to tissues may result in partial deaf-ferentation by causing mechanoreceptor damage, which can lead to propriocep-

199PROPRIOCEPTION AND ANKLE INJURIES IN SOCCERtive deficits. Consequently, susceptibility to reinjury may become a possibilitybecause of this decrease in proprioceptive feedback. The effect of ligamentoustrauma resulting in mechanical instability and proprioceptive deficits contrib-utes to functional instability, which could eventually lead to further microtraumaand reinjury. Achieving functional and sport-specific activities following muscu-loskeletal trauma and rehabilitation can be established if proprioception isaddressed and instituted early in the treatment program [39].

In addition to mechanical disruption of articular structures following injury,the loss of proprioception may have a profound effect on neuromuscular con-trol and the activities of daily living. It seems that neurologic feedback mecha-nisms originating in articular and musculotendinous structures provide animportant component for the maintenance of functional joint stability. Articular

FUNCTIONAL STABILITY

Muscular properties Capsuloligamentous propertiesMECHANICAL STABILITY1-POWER

2-REACTION TIME

POSTURAL CONTROL

PROPRIOCEPTIONFig. 2. Factors effecting functional stability.

200 ERGEN & ULKARdeafferentation results following injury to capsuloligamentous structures. Thiscontributes to alterations in kinesthesia and joint position sense and furtherdegenerative changes in the joint, because the spinal reflexive pathway maybe impaired [40]. Disruptions in the afferent pathway, which are mediatedpartly by articular mechanoreceptors, may also contribute significantly to aninsidious pattern of microtrauma and reinjury [40].

ANKLE PROPRIOCEPTIONFunctional instability of the ankle is one of the most common residual disabil-ities after an acute ankle sprain. Ankle joint instability can be defined as eithermechanical or functional instability. Mechanical instability refers to objectivemeasurement of ligament laxity, whereas functional instability is defined asthe feeling of giving way. Casual factors include a proprioceptive deficit, mus-cular weakness, or absent coordination [41].

Ankle instability as a result of partial deafferentation of articular mechanore-ceptors with joint injury was first postulated by Freeman [42]. It was observedthat a decrease in the ability to maintain a one-legged stance occurred in thesprained ankle versus the contralateral uninjured ankle. Konradsen andRavn [43] attributed the cause of functional instability to mechanical and func-tional causes in stating that functional instability results from damage tomechanical receptors in the lateral ligaments or muscle/tendon with subsequentpartial deafferentiation of the proprioceptive reflex.

Glencross and Thornton [44] reported deficits in the ability actively toreplicate passive ankle and foot positioning while testing the sprained ankle ver-sus the contralateral uninjured ankle. Gross [45] also revealed that an increasedprobability of reinjury occurs as a result of a decrease in sensory input from thejoint.

Konradsen and Ravn [43] found that chronic ankle instability resulted ina prolonged peroneal reaction time in response to a sudden inversion stresswhen compared with age-matched controls. Partial deafferentation resultingin diminished reflex joint stabilization may contribute to these findings.

No increases in postural sway have been observed by Tropp and Odenrick[46] when comparing a group of soccer players with previous ankle sprainswith a control group of uninjured soccer players. Significant increases in pos-tural sway have been observed by Cornwall and Murrell [47], however,when comparing patients with acute ankle sprains with uninjured controls aslong as 2 years after their injuries.

MUSCLE REACTION TIMEPassive restraint is provided by the bones, ligaments, and capsule. Active, ordynamic, restraint is provided by the neuromuscular system. The peronealmuscles are of particular interest at the ankle because they are the primary mus-

cles responsible for everting the foot against an inversion moment. The lengthof reaction time indicates that motor activity cannot be regarded solely in re-sponse to environmental stimuli. The reaction time is the time between

201PROPRIOCEPTION AND ANKLE INJURIES IN SOCCERperturbation and electric activity of the muscle. The electromechanical delay isa measurement of the time lag between muscle activation and the musclesforce production. In terms of lateral foot and ankle perturbations, severalauthors have evaluated the timing and power of neuromuscular response inthe lower leg muscles. A significantly faster reflex time has been found in theperoneal muscles compared with the quadriceps and hamstring [48].

Peroneal reaction time has been found to be significantly shorter in mechan-ically stable ankles [49]. In actions like walking, running, or jumping, however,a considerable preactivation of related muscles before touchdown exists [48].Exercises including perturbations on a wobble board may increase ankle stabil-ity both for preventive and rehabilitative purposes.

Peroneal muscle-reflex characteristics have been largely examined duringsudden inversion. The time and amplitude in which the peroneal musclesfire under static conditions may not reflect what occurs during an actualinjury. Ideally, peroneal muscle function should be assessed during a truedynamic state; however, because of the difficulty in controlling many extrane-ous variables under a true dynamic movement pattern model, the use of inver-sion trapdoors and platforms to simulate an ankle injury has been widelyaccepted.

EFFECT OF FATIGUE ON REFLEX INHIBITIONEndurance training is known to result in neuromuscular adaptations that alterthe production or clearance of metabolic substrates. Soccer is considered anendurance event. It can be speculated that fatigue may well result in lower mus-cular response to inversion. Walton and colleagues [50] determined the extentof reflex inhibition during and after fatigue in endurance-trained individualscompared with sedentary controls. Subjects were found to produce isometricankle plantar-flexion contractions at 30% of maximal voluntary contractionuntil their maximal voluntary contraction torque declined by 30%. H-reflexeswere measured during a brief rest period every 3 minutes and superimposedon the contraction every minute. These experiments demonstrated that theneuromuscular processes associated with fatigue-related reflex inhibitionmust be multifaceted and cannot be explained solely by small-diameter affer-ents responding to the by-products of muscle contraction [50]. Muscular fatiguemay be associated with reflex inhibition of the motoneuron pool. No literatureis available, however, to reveal the possible mechanism explaining the relation-ship between fatigued peroneal muscle and ankle injury.

EFFECT OF TAPINGIt has been postulated that ankle tapinginduced prophylaxis is associated withsensory feedback. By uniting the skin of the leg with the plantar surface of thefoot, Robbins and colleagues [51] suggested that the sensory cues to plantar

surface of the foot are increased, thereby allowing a more accurate foot place-ment and reducing the changes of excessive ligamentous strain. Karlsson andAndreasson [49] concluded that tape may help patients with unstable ankles

202 ERGEN & ULKARby facilitating proprioceptive and skin sensory input to the central nervoussystem. Taping or using a lace-up brace may contribute proprioception withsensory stimulation. There are some studies emphasizing that ankle tapingrapidly loses its initial level of resistance; nevertheless, the restraining effect onextreme ankle motion has not been eliminated by prolonged activity [52,53].

EFFECT OF ORTHOSIS AND BRACESThe various forms of ankle support (orthosis and braces) available are gener-ally considered effective in providing mechanical stability while restricting jointrange of motion. Improvement in proprioception and sensorimotor functionhas been shown to occur through stimulation of cutaneous mechanoreceptorsnear and around the ankle through the application of ankle support [54] andtape [55].

In Sweden, 25 teams with 439 adult male soccer players were randomizedinto three groups: (1) those offered a semirigid ankle orthosis (seven teamswith 124 players); (2) those offered an ankle disk training program (eight teamswith 144 players); and (3) 10 control teams with 171 players [14]. None of the439 players were allowed to use taping. Sixty of the 124 players who wereoffered elected to use the orthosis. The rate of sprains was found to be higheramong those with previous history of sprains (25% versus 11%; P

203PROPRIOCEPTION AND ANKLE INJURIES IN SOCCERMEASUREMENT OF PROPRIOCEPTIONThe assessment of neuromuscular control includes the measurement of corti-cal, spinal reflex, and brainstem pathways. The evaluation of this complexneuromuscular system as different components allows a more detailed explana-tion of afferent control mechanisms [20]. Numerous variables (proprioception,postural control, electromyography, kinetics-kinematics, dynamic stability pro-tocols) have been measured to understand better how the body maintains jointstability during a wide range of activities from static standing to dynamiccutting or landing from a jump [58].

Kinesthesia and joint position sensibility are the two major assessmentmethods of joint proprioception. Kinesthesia is assessed by measuring thresh-old to detection of passive motion, whereas joint position sense is assessedby measuring reproduction of passive positioning and reproduction of activepositioning. These tests are performed at slow angular velocities (0.52.5 de-grees per second) to stimulate selectively Ruffini or Golgi-type mechanorecep-tors, and because the test is performed passively, it is believed maximally tostimulate joint receptors while minimally stimulating muscle receptors [40].

Several researchers used position testing devices similar in action and design[5962]. These devices have moving arms rotating the limbs through the axisof the joint. A rotational transducer interfaced with a digital microprocessorcounter provides the angular displacement values. Pneumatic compressioncuffs are placed on each limb distal to the tested joints to reduce cutaneous in-put. The subjects are blindfolded to eliminate visual cues, and headphones withwhite noise are used to eliminate auditory cues. The subjects hold an on-offswitch to press when they detect the threshold of passive motion or the preposi-tioned angle [59,61,62].

Position testing devices, however, may have some limitations. De Jong andcolleagues [63] evaluated the performance in different proprioceptive tests andfound that these do not correlate well in ankles with recurrent sprain. The au-thors argue that proprioception is often discussed as a generic sensation, con-sisting of various subsets of sensations, with an implicit assumption of therebeing a relation between the sensations. In particular, sensations about move-ment, even though tested in different ways, are generally assumed to be related.The lack of relation in performance found in their study is crucial to clinicalpractice because it shows that proprioception is affected in specific ways; reha-bilitation should be directed at the specific deficit and not at a general proprio-ceptive deficit. For example, sprains occasionally damage the common peronealnerve or the peroneal muscles in addition to the anterior and lateral portions ofthe lateral ligament. Removal or distortion of input from these different struc-tures may affect each task differently.

The abilities of position replication on subjects joints also are performed byusing isokinetic dynamometers [61,6466]. Some researchers use modifiedisokinetic devices to record the changes in positioning. Active reproduction

of joint position was another way of assessing joint position sense using anelectromagnetic tracking device and an isokinetic dynamometer [61,66].

204 ERGEN & ULKARIn recent years, motion analysis systems have been used to record targetjoint angles; calculate reproduced angles (eg, angle velocity reproductiontest); and to test dynamic sensorimotor abilities of joints [61,6769]. For thedetermination of the combination of peripheral, vestibular, and visual contri-butions to neuromuscular control postural sway and balance are evaluated.Functional assessment of the combined peripheral, vestibular, and visualcontributions to neuromuscular control is best accomplished through the useof balance and postural sway measurements for the lower extremity. The avail-ability of stabilometric methods and instrumentation can provide a relativelyaccurate index for these measures [7073].

Balance stabilometry provides a specialized mode of assessment for the over-all contribution of these various neural afferent signals to maintain uprightstanding posture. Postural balance and sway measurements are conducted us-ing various types of force platform devices. Postural control is assessed by mea-suring changes in the center of pressure signal provided by a forceplate duringtests of limb standing balance [72,7478].

Assessment of the spinal reflex pathway is conducted to determine thelatency of muscular activation to involuntary perturbations. Electromyographicanalysis has been used extensively to examine the role of this neuromuscularpathway during movements that place functional loads on the ankle andknee joint [40]. The assessment of reflex capabilities is usually performed usingelectromyogram interpretation of firing patterns of those muscles crossing therespective joint.

The delay between the initiating stimulus and the onset of the peroneal mus-cle reflex response is defined as the peroneal latency. Electromyographystudies that investigate muscle onset latency alterations that develop after anankle sprain have typically used a simulated inversion ankle sprain perturba-tion in association with surface electromyogram to record peroneal muscleonset latencies. The electromechanical delay was defined as the time intervalbetween the onset of the peroneus longus electromyogram detected by surfaceelectrodes and the onset of the lateral ground reaction force measured on a for-ceplate. Mora and colleagues [79] investigated ankle instability by measuringthe electromechanical delay of the peroneal muscles (foot pronators).

Noninstrumented, clinically applicable tests to assess neuromuscular andfunctional deficits are reliable and valid for both research and clinical purposes[80]. Limb matching tasks are examples to evaluate proprioception without us-ing an electromechanical device. Providing different angles of joint movements,patients are asked to reproduce the given angle with the other limb [81].Although various hop tests have been used to measure the lower limb powerand functional ability of the athletes, they are assumed to be useful in the eval-uation of proprioceptive status of the injured athlete at the end of the rehabil-itation period. These tests are performed either for distance or time to evaluate

lower extremity symmetry [81,82]. Some examples are single limb hoppingcourse, one-legged and triple-legged hop for distance, and six and cross sixmeter hop for time [83].

205PROPRIOCEPTION AND ANKLE INJURIES IN SOCCERKynsburg and colleagues [84] stated that Ashton-Miller [85] defined verystrict requirements for researchers of ankle proprioception in his book. In hisopinion, measurements without weight-bearing cannot reproduce and modelthe real situation. Regarding primary injuries and recurrent sprains the landingphase of walking, running, and jumping is the most important phase. A perfectmodeling of landing forces subjects to land suddenly on the surface of unex-pected inclination and direction on single leg. Because of the high risk of injury,this can be modeled only approximately at a lower speed in research setting.

The slope-box test provides a good model for the real situation of landing,with subjects putting full weight on the tested leg. The inclination and thedirection of the slope are unexpected, but the surface is even and slip-proof, re-ducing the risk of injury. This method is also a compromise, however, becausethere is no forward movement and the speed is also less compared with the realsporting situation [51].

DOES PROPRIOCEPTIVE TRAINING PREVENT ANKLEINJURIES?In Sweden, a study of 12 soccer teams (15 men each), in which the teams wererandomized into an intensive season-long prevention program or a standardtraining program, found that intensive sustained conditioning reduced theoccurrence of ankle sprains over the course of a 6-month season [29]. In thisstudy, all players with previous ankle sprains were forced to have their anklestaped and to participate in a specific rehabilitative program. The Swedish studydescribed previously also showed that ankle disk training significantly loweredinjury rates [86].

Junge and colleagues [87] discussed the effectiveness of preventive interven-tions by studying a program (prospective controlled intervention study) on theincidence of soccer injuries in male youth amateur players. Seven soccer teamswere observed in a prevention program that focused on education and super-vision of coaches and players, whereas seven other teams were instructed totrain and play soccer as usual. Over 1 year all injuries were documentedweekly by physicians. Complete weekly injury reports were available for 194players. The incidence of injury per 1000 hours of training and playing soccerwas reduced by 6.7 in the intervention group and 8.5 in the control group,which equates to 21% fewer injuries in the intervention group. The greatesteffects were observed for mild injuries, overuse injuries, and injuries incurredduring training. The authors concluded that the incidence of soccer injuries canbe reduced by preventive interventions, especially in low skill level youthteams, and the coaches and players need better education regarding injury pre-vention strategies and should include such interventions as part of their regulartraining.

A prospective randomized intervention study performed on 221 female soc-

cer players showed contradictory results that there are no significant differencesbetween the intervention and control groups with respect either to the number,incidence, or type of traumatic injuries of the lower extremities [13]. During the

Following several studies regarding preventive programs, the FIFA medicalcommittee developed an every-day routine for players. The 11 comprises 10

206 ERGEN & ULKARevidence-based or best-practice exercises focusing on core stabilization, eccen-tric training of hamstrings, proprioceptive training, and straight leg alignment.

INTERVENTION STUDIES AND METHODOLOGICCONSIDERATIONSIntervention studies should be handled carefully because of inherent limitingfactors. Verhagen and colleagues [89] critically reviewed the current datafrom papers published between 1980 and December 1998 concerning the effi-cacy of preventive measures on the incidence of lateral ankle ligament injuries.These studies dealt not only with soccer but also other sports disciplines. Over-all, all studies reported a significant decrease in incidence of ankle sprains usingthe preventive measure. The use of either tape or braces reduces the incidenceof ankle sprains. Braces seem to be more effective in preventing ankle sprains,however, than tape. It is not clear which athletes benefit more from the use ofpreventive measures: those with or those without previous ankle sprains. Theefficacy of shoes in preventing ankle sprains is unclear. Proprioceptive trainingreduces the incidence of ankle sprains in athletes with recurrent ankle sprains tothe same level as subjects without any history of ankle sprains.

Reductions in the incidence of ankle injuries, sprains, strains, operations, andabsences from practices and games were also reported for the interventionteams. Several important factors must be considered in performing interventionseason, the players in the intervention group performed a special trainingprogram consisting of 10 to 15 minutes of balance board training in additionto their standard soccer practice and games.

McHugh and colleagues [88] studied the risk factors for noncontact anklesprains in high school athletes by evaluating the role of hip strength andbalance ability. One hundred sixty-nine high school athletes including soccerplayers (101 male athletes and 68 female athletes from football, mens basket-ball, mens soccer, womens gymnastics, womens basketball, and womenssoccer) were observed for 2 years. Balance in single-limb stance on an instru-mented tilt board and hip flexion, abduction, and adduction strength (handhelddynamometer) were assessed in the preseason. Body mass, height, generalizedligamentous laxity, previous ankle sprains, and ankle tape or brace use weredocumented. The results showed that the balance as measured on a balanceboard and hip strength were not significant indicators for noncontact anklesprains. The apparent high injury risk associated with the combination of a his-tory of a previous ankle sprain and being overweight in male athletes warrantsfurther examination for those who would like to participate in competitivesoccer.studies. Before the study a statistical power analysis must be performed todetermine the sample size needed to detect a certain reduction in the injuryfrequency. In the investigation of the authors, a statistical power analysis

1. Reflexes at the spinal level mediate movement patterns that are received from

207PROPRIOCEPTION AND ANKLE INJURIES IN SOCCERhigher levels of the nervous system. This action provides reflex for jointstabilization during conditions of excessive stress around the articulationand has significant implications for rehabilitation.

2. The second level of motor control, located within the brainstem, receivesinformation from joint mechanoreceptors, vestibular system, and visual inputfrom the eyes to maintain posture and balance of the body. Reactivatedneuromuscular actions allowing this pathway to process input from the afore-mentioned forms of afferent stimuli can be used to enhance brainstemfunction.

3. The highest level of CNS function (motor cortex, basal ganglia, and cerebel-lum) obtains cognitive awareness of body position and movement in whichmotor commands are initiated for voluntary movements. Use of the corticalpathway allows movements that are repeated and stored as central com-indicated the need for a sample size of 95 players in each group to detect a re-duction in injury frequency from 30% to 15% to achieve a power of 80%.

The limitations in a sport setting can be compliance, injury awareness, andcontamination. Concrete information on how the coaches and players complywith the intervention program is not always readily available. Injury awarenessis generally believed to be a major confounding factor in sports injury researchbecause it causes players to adjust their sports behavior. Contamination shouldbe controlled and reduced by means of the randomization procedure. Random-ization by player or team greatly reduces control over contamination (and com-pliance) and imposes practical logistical problems. Intervention studies dealingwith proprioceptive neuromuscular training effect on reducing ankle injuriesshould be carefully designed to overcome such limitations [90].

PROPRIOCEPTIVE (NEUROMUSCULAR) EXERCISESIN REHABILITATIONImprovement of ankle proprioception through physiotherapy (ankle proprio-ceptive training) is a widely accepted conservative treatment modality ofchronic functional lateral ankle instability [84]. It was considered that becausemechanoreceptors are located in ligaments, an injury to a ligament would alterafferent input. Training after an injury is needed to restore this altered neuro-logic function. Neuromuscular conditioning techniques have also been advo-cated for injury prevention. Increased postural and movement accuracyincreases the consistency with which activities can be performed safely [38].

Proprioceptive or kinesthetic awareness is one aspect of rehabilitationobtained through specific exercises. The objectives of proprioceptive rehabilita-tion are to retrain altered afferent pathways to enhance the sensation of jointmovement. Proprioceptively mediated neuromuscular control of joints comesinto action at three distinct levels of motor activation within the CNS [36].mands to be performed without continuous reference to consciousness. Kines-thetic and proprioception training are such types of activity that can developthis function.

208 ERGEN & ULKARIncorporating the three levels of motor control into activities to addressproprioceptive deficiencies should be started in the early phases of a rehabili-tation program. Encouraging maximum afferent discharge to the respectiveCNS level should be the target in stimulating joint and muscle receptors. Tostimulate reflex joint stabilization, which emanates from the spinal cord, activ-ities must focus on sudden changes in joint positioning that necessitate reflexneuromuscular control. Development of motor function at the brainstem levelcan be gained by performing balance and postural activities, both with andwithout visual input. Maximally stimulating the conversion of conscious tounconscious motor programming can be achieved by performing joint posi-tioning activities, especially at joint end ranges. Simple tasks, such as balancetraining and joint repositioning, should begin early in the rehabilitation pro-gram and should become increasingly more difficult as the patient progresses[91].

Some authors believe that adaptations that occur during rehabilitation aremediated by feed-forward processing and are less a function of enhanced affer-ent pathways [20]. This theory suggests that fast movements are controlled byadvanced information known about the task, whereas concurrent propriocep-tive feedback is relatively less important. Feedback is used primarily at the cor-tical level to determine the success or failure of that movement and to a lesserextent at the subcortical level for directing the movement. With repetition, thecerebral cortex can determine the most effective motor pattern for a given task,based on the proprioceptive information of previous attempts. Biofeedbacktraining seems to use the feed-forward learning process [92].

The following progression of activities is conducted to allow an athlete toreturn to functional levels [93]:

1. Joint position sense and kinesthesia2. Dynamic joint stabilization3. Reactive neuromuscular control4. Functionally specific activities

Such a progression allows the rehabilitation program to integrate spinalreflex, cognitive, and brainstem pathways focusing on stabilization, motion,and neuromuscular control. Position sensibility activities are designed to re-store joint position sense and kinesthesia. These exercises stimulate cognitivelevel processing through the use of such an exercise as articular repositioningboth with and without visual input and proprioceptive neuromuscular facilita-tion patterns performed with manual resistance. Dynamic stabilization activitiesare designed to stimulate muscular coactivation. In the ankle, such activities in-clude axial loading of the talotibial joint to promote coactivation of the forcecouples around the joint. Ultimately, plyometrics can be used for the integra-tion of both spinal and cognitive levels. Ankle plyometric exercises stimulate

reflexive activity through the facilitation of the myotatic reflex by the releaseof stored elastic energy. Such activities stimulate reflex joint stabilization, whichare critical to the overhead athlete. Once joint sensibility and dynamic muscle

209PROPRIOCEPTION AND ANKLE INJURIES IN SOCCERjoint stabilization are restored, functionally specific activities can be accom-plished [92].

In the past several years, there also has been a heightened awareness of theneed for preseason sport conditioning to focus on lower extremity balance andconditioning to diminish the incidence of knee ligament injuries. Neuromuscu-lar training incorporating plyometrics and agility drills and stressing the needfor proper technique for pivoting, shifting, and landing has been advocatedto decrease the incidence of ankle injuries. Griffis (quad-cruciate interaction),Henning Sportsmetrics (a three-part prevention consisting of stretching,plyometrics, and strengthening drills), Caraffa (a five-phase progressive skillacquisition program), and Santa Monica by Mandelbaum (a five-part programdesigned to improve strength, flexibility, injury awareness, plyometrics, andagility skills) are some of the program examples successfully implemented inrehabilitation [94].

After ankle injury, several investigators [46,95] have reported the use of pos-tural control strategies that rely more heavily on proximal joint (hip) muscleactivation. Collectively, all of these investigations have been found to supportthe premise of higher central motor control changes after orthopedic injury.The stimulus for these changes remains debatable: afferent changes from thearticular receptors, loss of mechanical stability, or both [96].

In an editorial, Eriksson [97] argues, based on studies by Ashton-Miller [85]and coworkers, that there is no proof that training increases proprioception ofthe ankles. Although it may increase coordination and balance, as the authorspoint out, this is not the same thing as proprioception. The issue becomes evenmore complicated when one reads studies about the effect of so-called propri-oceptive training, or what should be called balance training or coordina-tion training.

PROPRIOCEPTIVE TRAINING FOR THE ANKLEFreeman [42] has first recognized the importance of afferent input in neuromus-cular coordination and the significant consequences that result when such inputis disrupted. He analyzed previously injured patients following a trainingperiod and revealed that such exercises can help to achieve less functional in-stability than patients not trained in this manner.

Tropp [98] found that 10 minutes daily wobble board training during a10-week period could improve pronator muscle strength in patients with func-tional instability. Further training has not been found to give any added effect.Wester and colleagues [99] conducted a similar study on 48 patients (24 trainingand 24 no-training group) with residual functional instability caused by grade IIankle sprain. Compared with the no-training group, the 12-week training groupshowed significantly fewer recurrent sprains in a 230-day follow-up period. Eilsand Rosenbaum [41] studied the effects of a 6-week multistation proprioceptive

exercise program. Joint position sense, postural sway, and muscle reaction timesshowed significant improvements following this multistation training programconsisting of 12 different exercises (on mat, swinging platform, air squab,

was

n to

210 ERGEN & ULKAROne major category of proprioceptive exercise is balance training. These exer-cises help to train the proprioceptive system in a mostly static activity. In thelower extremities, activities can include one-legged standing balance exercises;progressive use of wobble board exercises; and tandem exercises in whicha postural challenge (eg, perturbations) can be applied to the individual bythe therapist.

Plyometric ExercisesPlyometric exercises incorporate an eccentric preload (a quick eccentric stretch)followed by a forceful concentric contraction. This exercise technique isthought to enhance reflex joint stabilization and may increase muscle stiffness.It has become increasingly popular as an example of a neuromuscular controlexercise that integrates spinal and brainstem levels and has been an effectiveaddition to upper and lower extremity conditioning and rehabilitation pro-grams [38]. As with the ankle and knee, plyometric exercises are added afternear-normal strength in all targeted muscles has been achieved. In the shoulder,plyometrics are performed using the balls with known weight, thrown orbounced and caught at various angles using stable and unstable reboundingboards or tossed in various and at varying speeds by a physiotherapist [94].

Isokinetic ExercisesBalance Traininginitiate reflex, subconscious muscle contraction. In injury, pain free doesnot necessarily mean completely treated or rehabilitated and unless the fullproprioceptive ability is restored, rehabilitation has not been accomplished.In addition, correction of a damaged static restraint (eg, surgical correctionof mechanically disrupted tissue) may not be sufficient to maximize the afferentneuromuscular input needed to enhance dynamic joint stability.deliberately, and sudden, externally applied perturbations of joint positioconducted in a way that each exercise was performed for 45-seconds followedby a 30-second break where subjects move to the next station.

PROPRIOCEPTIVE EXERCISESAlthough many companies sell fairly complex computerized equipment to helpimprove proprioceptive input and balance, such training can also be accom-plished through various simple drills done on various surfaces with eyesopen and shut, progressing from a double to a single limb stance. If available,however, such technologically advanced devices can also be used in proprio-ceptive trainings and rehabilitation programs. Exercises should include repeti-tive, consciously mediated movement sequences performed slowly andeversion-inversion boards, ankle disk, mini trampoline, step, uneven walkhanging and swinging platforms, and with exercise bands). The programway,Isokinetic exercises can be performed to enhance joint position sense using iso-kinetic devices. The athlete places his or her extremity in a predeterminedposition and is asked to reproduce this position, initially with the eyes open

euro-

cular

211PROPRIOCEPTION AND ANKLE INJURIES IN SOCCERcontraction to the point where contraction offsets injury, but not overreact tothe stimulus, causing injury. There are, however, some limitations of theselaboratory settings to measure the peroneal muscle activity because they doby contractile elements.Another possible mechanism is to increase the magnitude of the musmuscular training program on the electromechanical delay and reaction time ofthe peroneus longus muscle. The authors recruited 36 healthy, physicallyactive, college-age subjects for this study, and 26 completed the study. The elec-tromechanical delay of the peroneus longus was determined by the onset offorce contribution after artificial activation, as measured by electromyographicand forceplate data. Reaction time was measured after a perturbation duringwalking. It was found that a 6-week training program significantly reduced re-action time of the peroneus longus muscle in healthy subjects. Neuromusculartraining may have a beneficial effect on improving dynamic restraint duringactivity. According to the authors, one possible mechanism with which toachieve these goals is to improve the timing of the dynamic restraint mecha-nism, to increase the speed with which support is provided to the joint complextime [38].Linford and colleagues [100] have examined the influence of a 6-week nand then with eyes shut to block visual cues that might aid in neuromuscularcontrol. This exercise can be performed with and without eccentric or concen-tric loads.

Closed and Open Kinetic Chain ExercisesClosed kinetic chain exercises challenge the dynamic and reflexive aspects ofproprioception in the legs and feet. During a closed-chain movement at one jointa predictable movement at other joints is produced, usually involving axialforces. The lower extremities function in a closed-chain manner during sportsand daily life activities, so these exercises aid in regaining proper neuromuscularpatterns. Leg press, squat, circle running, figure eights, single-leg hops, verticaljumps, lateral bounds, one-legged long jumps, and carioca (crossover walking)are some examples. In the upper extremities, physiotherapist application ofgraded, multidirectional manual resistance can provide proprioceptive feedbackin a closed-chain fashion. Open-chain manual resistance exercises with rhythmicstabilization (rapid change in direction of applied pressure) are also consideredproprioceptively useful. In either case, resistance can be modified, dependingon pain tolerance, as the patient progresses.

Reaction TimeTo prevent injuries, a stored set of muscle commands is necessary. This motorprogramming allows the initiation of activity on exposure to unfolding events.The repetition of such exercises also allows the cerebral cortex to determine themost effective motor pattern for that task and potentially decrease the responsenot resemble the actual movement pattern. To mimic more closely the dynamicmechanism of an ankle sprain injury and the motor patterns active during gait,some authors have developed a runway with built-in trapdoors. This makes

possible measurement of reaction time of the ankle evertors while walking,taking into consideration sensorimotor factors that are only present duringmovement. In the past, electromechanical delay was determined in a partialor nonweight-bearing position [2527,30]. Recently, however, Mora andcolleagues [79] have tested electromechanical delay by electrically stimulatingthe common peroneal nerve and measuring the resultant force in a weight-bear-

212 ERGEN & ULKARSoccer is the most popular sport worldwide with more than 200 million activeplayers, according to FIFA, and ankle injuries are common. The ankle sprain isone of the most common injuries in athletes, particularly in sports in which

Box 1: Exercise prescription for proprioceptive training

Number of exercises: 25Number of repetitions of exercises: 1015Number of sets: 13Duration of total proprioceptive training: 515 minutes (shorter for prevention,SUMMARYing position. A 6-week training program used in that study significantly re-duced reaction time while marginally increasing the electromechanical delayof the peroneus longus muscle in healthy subjects.

Sport-Specific ManeuversThe final phase of any functional rehabilitation or conditioning program mustinclude exercises that mimic those the athlete does in daily sport activities. Thisspecificity of training improves feed forward mechanism and reflex and con-sciously controlled motor functions [93]. Sport-specific exercises serve to hard-wire the proprioceptive pathways and solidify a neuromuscular engram specificto these activities. Rehabilitation is then completed as maneuvers specific to thesport and the athletes position in the sport can be performed maximally andwithout pain or loss of function. These skills should be tested in the clinic,laboratory, or field before the patient returns to competition.

For constructing programs with the aim of conditioning and rehabilitation,one should incorporate exercises that improve joint motion sense, increaseawareness of joint motion, enhance dynamic joint stability, and improve reac-tive neuromuscular control.

In light of the present literature, an exercise prescription for proprioceptivetraining is as follows (Box 1):

It is generally recommended to continue such a program for at least 6 to10 weeks to improve proprioceptive abilities, especially during preseason. Itshould also be remembered that proprioceptive exercises should incorporateother specific training items, such as strength, flexibility, and agility, duringworkouts [39].longer for rehabilitative purposes), preferably every training day (at least 35days a week).

ectivestudy in the German National League. Am J Sports Med 2005;33:1694700.

213PROPRIOCEPTION AND ANKLE INJURIES IN SOCCER[9] Barker HB, Beynnon BD, Renstrom PAFH. Ankle injury risk factors in sport. Sports Med1997;23:6974.

[10] Inklaar H. Soccer injuries. II. Aetiology and prevention. Sports Med 1994;18:8193.[11] Giza E, Fuller C, Junge A, et al. Mechanisms of foot and ankle injuries in soccer. Am J

Sports Med 2003;31:5504.[12] Dvorak J, Junge A, Chomiak J, et al. Risk factor analysis for injuries in football players

possibilities for a prevention program. Am J Sports Med 2000;28:S6974.[13] Soderman K, Werner S, Pietila T, et al. Balance board training: prevention of traumatic

injuries of the lower extremities in female soccer players? A prospective randomized inter-vention study. Knee Surg Sports Traumatol Arthrosc 2000;8(6):35663.

[14] Tropp H, Askling C, Gillquist J. Prevention of ankle sprains. Am J Sports Med 1985;13(4):25962.

[15] Arnason A, Sigurdsson SB, Gudmundsson A, et al. Risk factors for injuries in football. Am JSports Med 2004;32:5S16S.

[16] Surve I, Schwellnus MP, Noakes T, et al. A fivefold reduction in the incidence of recurrentankle sprains in soccer players using the Sport-Stirrup orthosis. Am J Sports Med[8] Faude O, Junge A, Kindermann W, et al. Injuries in female soccer players: a prospparticipants frequently jump and land on one foot or are expected to makesharp cutting maneuvers, such as soccer. Because soccer attracts many partic-ipants and leads to a substantial number of injuries, especially of the lower ex-tremities, it is important to study possibilities for injury prevention and properrehabilitation to return safely to activities. Ankle sprains can be prevented byexternal ankle supports and proprioceptive-coordination training, especiallyin athletes with previous ankle sprains.

Proprioception is a broad concept that includes balance and postural controlwith visual and vestibular contributions, joint kinesthesia, position sense, andmuscle reaction time. Proprioceptive feedback is crucial in the conscious andunconscious awareness of a joint or limb in motion. Enhancement of functionaljoint stability by proprioceptive (or neuromuscular) training is important bothin prevention and rehabilitation of athletic injuries.

References[1] Junge A, Dvorak J. Soccer injuries: a review on incidence and prevention. Sports Med

2004;34(13):92938.[2] Hawkins RD, Hulse MA, Wilkinson C, et al. The Association Football Medical Research

Programme: an audit of injuries in professional football. Br J Sports Med 2001;35:437.[3] Garrick JG. The frequency of injury, mechanism of injury, and epidemiology of ankle

sprains. Am J Sports Med 1977;5:2412.[4] McGuine TA, Keene JS. The effect of a balance training program on the risk of ankle sprains

in high school athletes. Am J Sports Med 2006;34:110311.[5] Barrett J, Bilisko T. The role of shoes in the prevention of ankle sprains. Sports Med

1995;20:27780.[6] Emery CA, Meeuwisse WH, Hartmann SE. Evaluation of risk factors for injury in adolescent

soccer implementation and validation of an injury surveillance system. Am J Sports Med2005;33:188291.

[7] Peterson L, Junge A, Chomiak J, et al. Incidence of football injuries and complaints in dif-ferent age groups and skill-level groups. Am J Sports Med 2000;28:S6974.1994;22(5):6016.[17] Olsen L, Scanlan A, MacKay M, et al. Strategies for prevention of soccer related injuries:

a systematic review. Br J Sports Med 2004;38:8994.

214 ERGEN & ULKAR[18] Tittel K. Coordination and balance. In: Dirix A, Knuttgen HG, Tittel K, editors, Encyclope-dia of sports medicine, vol. 1. London: Blackwell Scientific Publ; 1988. p. 194211.

[19] Laskowski ER, Newcomer-Aney K, Smith J. Refining rehabilitation with proprioceptiontraining: expediting return to play. Phys Sports Med 1997;25:89102.

[20] Lephart SM, Pincivero DM, Giraldo JL, et al. The role of proprioception in the managementand rehabilitation of athletic injuries. Am J Sports Med 1997;25(1):1307.

[21] Bunton EE, Pitney WA, Kane AW, et al. The role of limb torque, muscle action and propri-oception during closed kinetic chain rehabilitation of the lower extremity. J Athl Train1993;28:1020.

[22] Grigg P. Peripheral neural mechanism in proprioception. J Sport Rehabil 1994;3:217.

[23] Barrack RL, Skinner HB, Brunet ME, et al. Joint kinesthesia in the highly trained knee. JSports Med Phys Fitness 1983;24:1820.

[24] Barrett DS, Cobb AG, Bentley G. Joint proprioception in normal, osteoarthritic, andreplaced knees. J Bone Joint Surg Br 1991;73:536.

[25] Sojka P, Sjolander P, Johansson H, et al. Influence from stretchsensitive receptors in thecollateral ligaments of the knee joint on the gamma-muscle spindle systems of flexor andextensor muscles. Neurosci Res 1991;11:5562.

[26] Kennedy JC, Alexander IJ, Hayes KC. Nerve supply of the human knee and its functionalimportance. Am J Sports Med 1982;10:32935.

[27] Schutte MJ, Dabezies EJ, Zimny ML, et al. Neural anatomy of the human anterior cruciateligament. J Bone Joint Surg 1987;69A:2437.

[28] Katonis PG, Assimakopoulos AP, Agapitos MV, et al. Mechanoreceptors in the poste-rior cruciate ligament: histologic study on cadaver knees. Acta Orthop Scand1991;62:2768.

[29] Zimny ML, Albright DJ, Dabezies E. Mechanoreceptors in the human medial meniscus.Acta Anat 1988;133:3540.

[30] DeAvila GA, OConnor BL, Visco DM, et al. The mechanoreceptor innervation of the hu-man fibular collatera11igament. J Anat 1989;162:17.

[31] Krenn V, Hofmann S, Engel A. First description of mechanoreceptors in the corpus adipo-sum infrapatellare of man. Acta Anat 1990;137:1878.

[32] Grigg P, Hoffman AH. Properties of Ruffini afferents revealed by stress analysis of isolatedsections of cat knee capsule. J Neurophysiol 1982;47:4154.

[33] Grigg P, Hoffman AH. Calibrating joint capsule mechanoreceptors as in vivo soft tissueload cells. J Biomech 1989;22:7815.

[34] Heetderks WJ. Principal component analysis of neural population responses of knee jointproprioceptors in cat. Brain Res 1978;156:5165.

[35] Johansson H, Sjolander P, Sojka P. Receptors in the knee joint ligaments and their role in thebiomechanics of the joint. Crit Rev Biomed Eng 1991;18:34168.

[36] Guyton AC. Textbook of medical physiology. 6th edition. Philadelphia: Saunders; 1981.p. 12237, 5346, 5624, 58895, 629.

[37] Ciccarelli O, Toosy AT, Marsden JF, et al. Identifying brain regions for integrative sensori-motor processing with ankle movements. Exp Brain Res 2005;166(1):3142.

[38] Tropp H, Alaranta H, Renstrom A. Proprioception and coordination training in injuryprevention. In: PAFH Renstrom, editor. Sports injuries basic principles of preventionand care. London: Blackwell; 1992. p. 27788.

[39] Ergen E, Ulkar B. Proprioception and coordination. In: Frontera WR, Herring SA,Micheli LJ, et al, editors. Clinical sports medicine. Saunders: Elsevier; 2007. p. 23755.

[40] Lephart SM. Proprioception of the ankle and knee. Sports Med 1998;25:14955.[41] Eils E, Rosenbaum D. A multi-station proprioceptive exercise program in patients with ankle

instability. Med Sci Sports Exerc 2001;33:19918.

[42] Freeman MA. Instabilities of the foot after lateral ligament injuries of the ankle. J Bone Joint

Surg 1965;47:66977.

215PROPRIOCEPTION AND ANKLE INJURIES IN SOCCER[43] Konradsen L, Ravn JB. Ankle instability caused by prolonged peroneal reaction time. ActaOrthop Scand 1990;61:38890.

[44] Glencross D, Thornton E. Position sense following joint injury. J Sports Med Phys Fitness1991;21:237.

[45] Gross MT. Effects of recurrent lateral ankle sprain on active and passive judgments of jointposition. Phys Ther 1987;67:15059.

[46] Tropp H, Odenrick P. Postural control in single-limb stance. J Orthop Res 1988;6:8339.[47] Cornwall MW, Murrell P. Postural sway following inversion sprain of the ankle. J Am Po-

diatr Med Assoc 1991;81:2437.[48] Richie DH. Functional instability of the ankle and the role of neuromuscular control: a com-

prehensive review. J Foot Ankle Surg 2001;40:24051.[49] Karlsson J, Andreasson GO. The effect of external ankle support in chronic lateral ankle

joint instability: an electromyographic study. Am J Sports Med 1992;20:25761.[50] Walton DM, Kuchinad RA, Ivanova TD, et al. Reflex inhibition during muscle fatigue in

endurance-trained and sedentary individuals. Eur J Appl Physiol 2002;87(45):4628.[51] Robbins S, Waked E, Rappel R. Ankle taping improves proprioception before and after

exercise in young men. Br J Sports Med 1995;29:2427.[52] Myburgh KH, Vaughan CL, Isaacs SK. The effects of ankle guards and taping on joint mo-

tion before, during, and after a squash match. Am J Sports Med 1984;12:4416.[53] Manfroy PP, Ashton-Miller JA, Wojtys EM. The effect of exercise, prewrap, and athletic tape

on the maximal active and passive ankle resistance of ankle inversion. Am J Sports Med1997;25:15663.

[54] Feuerbach JW, Grabiner MD, Koh TJ, et al. Effect of an ankle orthosis and ankle ligamentanesthesia on ankle joint proprioception. Am J Sports Med 1994;22:2239.

[55] Simoneau GG, Degner RM, Kramper CA, et al. Changes in ankle joint proprioceptionresulting from strips of athletic tape applied over the skin. J Athl Train 1997;32:1417.

[56] Cordova ML, Ingersoll CD. Peroneus longus stretch reflex amplitude increases after anklebrace application. Br J Sports Med 2003;37:25862.

[57] Cordova ML, Christopher D, Ingersoll CD, et al. Efficacy of prophylactic ankle support: anexperimental perspective. J Athl Train 2002;37(4):44657.

[58] Wikstrom EA, Tillman MD, Chmielewski TL, et al. Measurement and evaluation of dynamicjoint stability of the knee and ankle after injury. Sports Med 2006;36(5):393410.

[59] Borsa PA, Lephart SM, Irrgang JJ, et al. The effects of joint position and direction of jointmotion on proprioceptive sensibility in anterior cruciate ligament-deficient athletes. Am JSports Med 1997;25:33640.

[60] Barrack RL, Skinner HB, Buckley SL. Proprioception in the anterior cruciate deficient knee.Am J Sports Med 1989;17:16.

[61] Lephart SM, Myers JB, Bradley JP, et al. Shoulder proprioception and function followingthermal capsulorrhaphy arthroscopy. J Arthroscop Rel Surg 2002;18(7):7708.

[62] Ulkar B, Kunduracioglu B, Cetin C, et al. Effect of positioning and bracing on passive po-sition sense of shoulder joint. Br J Sports Med 2004;38:54952.

[63] De Jong A, Kilbreath SL, Refshauge KM, et al. Performance in different proprioceptive testsdoesnot correlate inankleswith recurrent sprain.ArchPhysMedRehabil 2005;86:21015.

[64] Janwantanakul P, Magarey ME, Jones MA, et al. Variation in shoulder position sense at midand extreme range of motion. Arch Phys Med Rehabil 2001;82:8404.

[65] Swanik KA, Lephart SM, Swanik B, et al. The effects of shoulder plyometric training on pro-prioception and selected muscle performance characteristics. J Shoulder Elbow Surg2002;11(6):57986.

[66] Lee HM, Liau JJ, Cheng CK, et al. Evaluation of shoulder proprioception following musclefatigue. Clin Biomech 2003;18:8437.

[67] Hopper DM, Creagh MJ, Formby PA, et al. Functional measurement of knee joint position

sense after anterior cruciate ligament reconstruction. Arch Phys Med Rehabil 2003;84:86872.

216 ERGEN & ULKAR[68] Jerosch J, Brinkmann T, Schneppenheim M. The angle velocity reproduction test (AVRT) assensorimotor function of the glenohumeral complex. Arch Orthop Trauma Surg 2003;123:1517.

[69] Barden JM, Balyk R, Raso JV, et al. Dynamic upper limb proprioception in multidirectionalshoulder instability. Clin Orthop 2004;420:1819.

[70] Berg KO, Wood-Dauphinee SL, Williams JI, et al. Measuring balance in the elderly: vali-dation of an instrument. Can J Public Health 1992;83(Suppl 2):S711.

[71] Hansen MS, Dieckmann B, Jensen K, et al. The reliability of balance tests performed on thekinesthetic ability trainer (KAT 2000). Knee Surg Sports Traumatol Arthrosc 2000;8:1805.

[72] Ageberg E, Roberts D, Holmstrom E, et al. The effect of short-duration sub-maximal cyclingon balance in single-limb stance in patients with anterior cruciate ligament injury: a cross-sectional study. BMC Musculoskelet Disord 2004;5:44.

[73] Arnold BL, Schmitz RJ. Examination of balance measures produced by the Biodex StabilitySystem. J Athl Train 1998;33:3237.

[74] Adlerton AK, Moritz U, Nilssen RM. Force plate and accelerometer measures for evaluat-ing the effect of muscle fatigue on postural control during one-legged stance. Physiother ResInt 2003;8(4):18799.

[75] Fuchs S, Tibesku CO, Frisse D, et al. Clinical and functional comparison of uni- and bicon-dylar sledge prostheses. Knee Surg Sports Traumatol Arthrosc 2004. Available: http://www.springerlink.com. Accessed December 24, 2004.

[76] Gosselin G, Rassoulian H, Brown I. Effects of neck extensor muscles fatigue on balance.Clin Biomech 2004;19:4739.

[77] Madeleine P, Prietzel H, Svarrer H, et al. Quantitative posturography in altered sensoryconditions: a way to assess balance instability in patients with chronic whiplash injury.Arch Phys Med Rehabil 2004;85:4328.

[78] Kovacs EJ, Birmingham TB, Forwell L, et al. Effect of training on postural control in figureskaters a randomized controlled trial of neuromuscular versus basic off-ice training pro-grams. Clin J Sport Med 2004;14(4):21524.

[79] Mora I, Quinteiro-Blondin S, Perot C. Electromechanical assessment of ankle stability. Eur JAppl Physiol 2003;88:55864.

[80] Gribble PA, Hertel J, Denegar CR, et al. The effects of fatigue and chronic ankle instabilityon dynamic postural control. J Athl Train 2004;39(4):3219.

[81] Noyes FR, Barber SD, Mangine RE. Abnormal lower limb symmetry determined by functionhop tests after anterior cruciate ligament rupture. Am J Sports Med 1991;19:5138.

[82] Risberg MA, Ekeland A. Assessment of functional tests after anterior cruciate ligamentsurgery. J Orthop Sports Phys Ther 1994;19:2127.

[83] Sekir U, Yildiz Y, Hazneci B, et al. Effect of isokinetic training on strength, functionality andproprioception in athletes with functional ankle instability. Knee Surg Sports TraumatolArthrosc 2007;15(5):65464.

[84] Kynsburg A, Halasi T, Tallay A, et al. Changes in joint position sense after conservativelytreated chronic lateral ankle instability. KneeSurgSports TraumatolArthrosc2006;14(12):1299306.

[85] Ashton-Miller JA. Proprioceptive thresholds at the ankle: implications for the prevention ofligamentous injury. In: Lephart SM, Fu FH, editors, Proprioception and neuromuscular con-trol in joint stability. Champaign: Human Kinetics; 2000. p. 27989.

[86] Ekstrand J, Gillquist J, Liljedahl SO. Prevention of soccer injuries: supervision by doctor orphysiotherapist. Am J Sports Med 1983;11:11620.

[87] Junge A, Rosch D, Peterson L, et al. Prevention of soccer injuries: a prospective interventionstudy in youth amateur players. Am J Sports Med 2002;30:6529.

[88] McHugh MP, Tyler TF, Tetro DT, et al. Risk factors for noncontact ankle sprains in high school

athletes; the role of hip strength and balance ability. Am J Sports Med 2006;34:46470.

[89] Verhagen E, Van Mechelen W, De Vente W. The effect of preventive measures on the inci-dence of ankle sprains. Clin J Sport Med 2000;10:2916.

[90] Verhagen E, van der Beek A, Twisk J, et al. The effect of a proprioceptive balance boardtraining program for the prevention of ankle sprains. a prospective controlled trial. Am JSports Med 2004;32:138593.

[91] Tyldesling B, Greve JI. Muscles, nerves and movement: kinesiology in daily living. Boston:Blackwell Scientific Publications; 1998. p. 26,34,284.

[92] Dunn TG, Gillig SE, Ponsor SE. The learning process in feedback: is it feed forward or feed-back? Biofeedback Self Regul 1986;11(2):14356.

[93] Lephart SM, Henry TJ. The physiological basis for open and closed kinetic chain rehabili-tation for the upper extremity. J Sport Rehabil 1996;5:7187.

[94] Griffin LYE. Neuromuscular training and injury prevention in sports. Clin Orthop Rel Res2003;409:5360.

[95] Pintsaar A, Brynhildsen J, Tropp H. Postural corrections after standardized perturbations ofsingle limb stance: effect of training and orthotic devices in patients with ankle instability. BrJ Sports Med 1996;30:1515.

[96] Riemann BL, Lephart SM. The sensorimotor system, part II: the role of proprioception in mo-tor control and functional joint stability. J Athl Train 2002;37(1):804.

[97] Eriksson E. Can proprioception be trained? Knee Surg Sports Traumatol Arthrosc 2001;9:127.

[98] Tropp H. Pronator muscle weakness in functional instability of the ankle joint. Int J SportsMed 1986;7:2914.

[99] Wester JU, Jespersen SM, Nielsen KD, et al. Wobble board training after partial sprains of

217PROPRIOCEPTION AND ANKLE INJURIES IN SOCCERthe lateral ligaments of the ankle: a prospective randomized study. J Orthop Sports PhysTher 1996;23:3326.

[100] Linford CW, Hopkins JT, Schulthies SS, et al. Effects of neuromuscular training on thereaction time and electromechanical delay of the peroneus longus muscle. Arch PhysMed Rehabil 2006;87:395401.

Proprioception and Ankle Injuries in SoccerDefinitionsProprioceptive organs: mechanoreceptorsBrain regions involved in ankle movementsClinical importance of proprioceptionAnkle proprioceptionMuscle reaction timeEffect of fatigue on reflex inhibitionEffect of tapingEffect of orthosis and bracesMeasurement of proprioceptionDoes proprioceptive training prevent ankle injuries?Intervention studies and methodologic considerationsProprioceptive (neuromuscular) exercises in rehabilitationProprioceptive training for the ankleProprioceptive exercisesBalance TrainingPlyometric ExercisesIsokinetic ExercisesClosed and Open Kinetic Chain ExercisesReaction TimeSport-Specific Maneuvers

Summary

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