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eBooks Proprioception: The Forgotten Sixth Sense Chapter: Hip Problems and Proprioception Edited by: Defne Kaya Published Date: July, 2015 Published by OMICS Group eBooks 731 Gull Ave, Foster City, CA 94404, USA Copyright © 2015 OMICS Group All book chapters are Open Access distributed under the Creative Commons Attribution 3.0 license, which allows users to download, copy and build upon published articles even for commercial purposes, as long as the author and publisher are properly credited, which ensures maximum dissemination and a wider impact of our publications. However, users who aim to disseminate and distribute copies of this book as a whole must not seek monetary compensation for such service (excluded OMICS Group representatives and agreed collaborations). After this work has been published by OMICS Group, authors have the right to republish it, in whole or part, in any publication of which they are the author, and to make other personal use of the work. 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A free online edition of this book is available at www.esciencecentral.org/ebooks Additional hard copies can be obtained from orders @ www.esciencecentral.org/ebooks I eBooks Hip Problems and Proprioception Sevgi Sevi Subaşi Yeşilyaprak* Assistant Professor, School of Physical Therapy and Rehabilitation, Dokuz Eylul University, Izmir, Turkey *Corresponding author: Sevgi Sevi Subaşi Yeşilyaprak, PT, PhD, Assistant Professor, School of Physical Therapy and Rehabilitation, Dokuz Eylul University, Izmir, Turkey, Tel: +902324124926; E-mail: sevgi.subasi@deu.edu.tr Abstract Proprioceptive information concerning the status of joint and muscle receptors is essential for neuromuscular control and functional joint stability [1,2]. The hip joint has an important role in lower extremity kinetic chain and compromised function of the trunk and hip stabilizers may underlie the mechanism of leg injuries. Poor proprioception of the hip may diminish neuromuscular control of the leg and is related to decreased control of hip joint stability [3]. Deterioration of proprioception is acknowledged as a risk factor for falls [4]. There is limited number of researches examining proprioception of the hip in the literature. Reliable and precise hip proprioception measurement techniques are still being developed [3]. Hip proprioception declines with age [5]. It is correlated with dynamic balance [5,6]. Increased hip proprioception error is related to decreased gait velocity in Cerebral Palsy (CP) [6]. Researchers mostly interested in whether hip proprioception impairs due to fractures/hip replacement [7-10] and the effects of rehabilitation on proprioception [11]. There is almost no information of the effects of specific proprioceptive training on hip proprioception and few studies investigated the hip proprioception in sports [12], healthy young people [3,13] or children with CP [6,14]. In this chapter, definitions and basic neurophysiology of proprioception; interactions with balance, coordination, and agility; hip proprioception, neuromuscular control and functional stability; factors influencing hip proprioception; measurement of hip proprioception; hip and lower extremity injuries, prevention; hip proprioception and problems involving hip joint, healthy people vs. patients; physical activity, sports, exercise and hip proprioception; hip proprioception exercises are discussed in detail. Keywords: Hip; Neuromuscular Control; Proprioception; Proprioceptive Test Definitions Proprioception was first defined by Sherrington in 1906 as “the perception of joint and body movement as well as position of the body, or body segments, in space” [15]. At present, proprioception is defined as the cumulative input to the Central Nervous System (CNS) from mechanoreceptors [16]. It’s a complex sense that utilizes inputs from somatosensory, vestibular, and visual afferent systems. Neural inputs to the CNS are provided from specialized nerve endings called mechanoreceptors located in skin, muscles, tendons, joint 1 capsules, joint ligaments and fascia [16-18]. The somatosensory system includes two types of mechanoreceptors as Quick-Adapting (QA) and Slow-Adapting (SA) mechanoreceptors. If a joint is stimulated continuously by pressure or motion, the QA’s decrease their signaling of the CNS, while the SA’s maintain signaling. Joint motion sense is mediated primarily by QA’s, receptors detecting sudden changes in speed and movement, whereas SA’s giving information to the CNS about joint position, slow changes in position, and sensation [19,20]. Proprioception reflects body’s ability to transmit a sense of position, analyze the information and react consciously or unconsciously to the stimulation with the proper movement and posture, including balance, coordination and agility [20]. Sub modalities of the proprioception are; a. Tension/Force (resistance) Sense (FS)-ability to reproduce the same force, b. Sense of body or joint movement-the ability to appreciate joint movement, including the duration, direction, amplitude, speed, acceleration and timing of movements and kinesthesia-ability to detect the initiation and direction of passive joint movement. c. Joint Position Sense (JPS)-the ability to reproduce the same joint position actively or passively, d. Velocity Sense (VS)-ability to reproduce the same velocity [1,3,21]. Proprioception can be appreciated consciously or unconsciously, contributing to automatic control of movement, balance, and joint stability, and thus being essential to carry out activities of daily living, work and sports activities [1]. Neurophysiology of Proprioception Mechanoreceptors, act as mechanical transducers during the deformation of the related tissue that contains them, in transmitting neural signals to the CNS via afferent sensory pathways [1,20,21]. The main receptors contributing to proprioception are located in muscle, tendon, ligament and capsule. Receptors in skin and fascia are supplementary sources [20,21]. Muscle spindle afferents respond to stretch of a muscle [17-20]. These SA receptors, located within skeletal muscle, maintain a symbiotic relationship with articular receptors to result in sensations of joint motion, joint acceleration and joint position [19]. Current knowledge indicates that proprioception is primarily signaled by muscle receptors, muscle spindles [17,18,22]. Muscle spindle activity results in contraction of a muscle and they are considered as able to provide potent afferent information across the entire range of motion [23]. Golgi Tendon Organs (GTO) detect tension in the muscle and respond not only stretching but also contraction of a muscle [18,20,22]. GTO activity results in relaxation of a muscle [20]. Articular mechanoreceptors play a minor role in proprioception through the midranges of a motion, whereas they can sufficiently stimulated in the end ranges of motion [24]. Similarly, cutaneous receptors have been hypothesized to respond at the end ranges of motion [24] and don’t have a major impact on proprioception in normal people [19,20]. However, Callaghan et al., pointed out that injured body segments more rely on cutaneous receptors in injured subjects [25]. Once afferent nerves of somatosensory, vestibular and visual systems sent the input to the CNS, motor response is determined by three distinct levels to react the stimuli: the spinal level; the brain stem; and the higher brain centers such as cerebral cortex or cerebellum [19-21,26]. The spinal level provides for dynamic muscular stabilization and synchronization of muscle activation patterns based upon spinal reflexes to respond in its simplest form as well as activity received from higher levels of the CNS. Articular mechanoreceptors, muscle spindles and GTOs work together to produce a reflex response and joint stabilization during conditions of abnormal stress in order to prevent injury [27]. 2 At the brain stem, the second level of motor control and primary proprioceptive correlation center, afferent information from mechanoreceptors is integrated with visual and vestibular inputs via the cerebellum nuclei. It sends excitatory or inhibitory efferent stimulation in order to control automatic and stereotypical movement patterns and to maintain posture and balance [19,20]. Proprioceptive information travels to the supraspinal regions of the CNS via 1. The dorsal lateral tracts (terminating in the somatosensory cortex) which are responsible for the conscious perception of proprioception, and 2. The spinocerebellar tracts that exhibit fastest transmission velocity for nonconscious proprioception [1]. The higher brain centers of the CNS, the motor cortex, basal ganglia and cerebellum, are responsible for cognitive programming of musculoskeletal motion in which motor commands are initiated for voluntary movements, and for the cognitive awareness of proprioception. Cortical pathway allows movements that are repeated and stored as central commands to be performed without continuous reference to consciousness that means more automatically [19,26,27]. Integration of the proprioceptive information results in conscious awareness of joint position and motion sense for motor programming and unconscious joint stabilization to protect body from injuries via spinal reflexes and to maintain balance and appropriate posture [19]. With this integration of proprioception, body stability ahead of movement execution (feedforward) can be coordinated and velocity or timing errors can be corrected (feedback) [17,18,28]. Interactions with Balance, Coordination and Agility Balance is “the body’s ability to maintain equilibrium by controlling the body’s center of gravity over its base of support” in both static and dynamic activities [20]. Strength and proprioception as well as visual system and vestibular system are important to maintaining good balance and posture. Proprioception input from the lower extremities is arguably the most important contributor to standing balance [29]. If proprioceptors are damaged following an injury or surgery, balance can be impaired [17,18,20]. Coordination, a proprioceptive function, means a smooth pattern of combination of muscle activities with appropriate intensity and timing. Strength, appropriate activity perception and feedback mechanism via proprioceptors, repetition and proper inhibition of undesired muscle activity are the key components for the coordination [20]. Agility is a highly advance skill that can be defined as the ability to control the direction of body or body segments during rapid movements which requires flexibility, strength, power, speed, balance and coordination. Agility also involves sudden stopping and starting the activity [20]. Although a person must have muscle strength, endurance and flexibility to able to perform various activities, agility to change the direction of movement very quickly and correctly cannot be expected without proprioception. Additionally, balance is needed to establish and to maintain stability, so is coordination to produce the activity correctly and consistently. Proprioception seems very important not only for the rehabilitation process after an injury but also as a routine part of a therapeutic exercise program for improvement and to prevent injuries [20]. Hip Proprioception Muscle spindles are the major mechanoreceptor involved in proprioception [22]. Proprioception changes following physical activity seem to be related at peripheral level with muscle spindle adaptations [16]. There are sensory nerve end organs, such as, Pacinian 3 corpuscles, Golgi-Mazzoni corpuscles, Ruffini endings and articular corpuscles (Krause corpuscle) in acetabular labrum of the hip [30]. Free nerve endings have been found in the labrum and ligamentum capitis femoris [31]. Free nerve endings may help to prevent excessive joint motion that may damage to the acetabular rim and/or adjacent cartilage. Traumatic or degenerative lesions of the ligamentum capitis femoris can damage free nerve endings and their ability to transmit a mechanical stimulus as a correct efferent impulse can be deteriorated. The absence of the muscular reflex might impair the protective function of the joint with ensuing micro- and/or macro trauma. There was a lack of information about the distribution of mechanoreceptors in the capsule and other ligaments of the human hip in the past; furthermore presence of mechanoreceptors in the labrum was questionable. Since mechanoreceptors are exclusively present in the loose tissue between the mechanical relevant collagen bundles, high density of collagen bundles in the area of the labrum was believed eliminating the possibility of the presence of mechanoreceptors in it. In terms of joint protection; when there is excessive stress on the ligamentum capitis femoris, it may give afferent signals to prevent further joint excursion with reflexive muscular response. Moraes et al., [32] recently identified and quantified mechanoreceptors and free nerve endings in the femoral head ligament, labrum, and capsule joint in the hip serving to stabilize hip joints. The density of Pacinian corpuscles is significantly more than densities of Golgi corpuscles and Ruffini endings while free nerve endings are found with similar density in healthy subjects’ hips. Neuromuscular control and functional stability Motor control is a plastic process that undergoes constant review and modification (i.e., feed forward and feedback) based upon the integration and analysis of sensory input, efferent motor commands, and resultant movements. Riemann et al., [2] defined neuromuscular control as unconscious activation of dynamic restraints occurring in preparation for and in response to joint motion and loading to maintain and restore functional joint stability of both the entire body (postural stability) and the segments (joint stability). Proprioceptive information concerning the status of the joint and muscle receptors is essential for neuromuscular control and maintaining functional joint stability [1,2]. Muscle spindles were found to be more important in proprioception, with the active contraction of the muscles can provide more afferent feedback for the joint position than do the passive movement. Changes of proprioception are mainly rely on morphological changes in the muscle spindles [33]. The afferents that signal hip-joint position come mainly from muscles around the hip. Simple stretch and cutaneous reflexes might be involved in compensating for irregularities and in adapting to ground conditions [17]. After mechanoreceptor stimulation, increased activity of γ motor neurons increase muscle activity [34]. Inputs arising from cutaneous or muscle sources and descending supraspinal commands increase γ motor neuron activity which increases muscle spindle sensitivity. This sensitivity is controlled by the fusimotor system, which can vary the strength of activation of intrafusal muscle fibres in muscle spindles by γ motor neurons [17]. Increased muscle spindle sensitivity improves the ability to resist a perturbation and assists α motor neuron activation in decreasing the chance of an injury, simply due to muscle stiffness decreasing the electromechanical delay. Enhanced muscle stiffness, of which muscle spindles are important component, is argued to be an important characteristic for dynamic joint stability. Articular mechanoreceptors are attributed instrumental influence over γ motor neuron activation, and indirectly influence muscle stiffness [2]. Stiffer muscles should potentially resist sudden joint displacements more effectively [35]. This may be essential in maintaining functional stability when mechanical stability is deficient. Additionally, stiffer muscles could transmit loads to muscle spindles more readily, reducing some of the lag time associated with initiation of reflexive activity [2]. The hip plays an important role in the kinetic chain of the lower extremity. Compromised function of the trunk and hip stabilizers may underlie the mechanism of lower extremity 4 injuries. Poor proprioception or proprioceptive deficits of the hip may diminish neuromuscular control of the lower extremity, therefore is related to decreased control of hip joint stability [3]. Relationship of Hip and Lower Extremity Injuries Weakness and/or imbalances of the hip muscles could lead difficulties in hip control especially during dynamic movements [36]. In case of poor hip control due to weak gluteus medius muscle, the hip will tend to move into adduction when loaded. If the hip moves into adduction, the femur internally rotates and the knee is placed into a valgus position [37]. Leetun et al., found significantly higher hip abduction and external rotation strength in athletes with no previous injury concerning lower extremity [38]. Diminished proprioception and core stability of the hip may also has influence on controlling knee movements leading to valgus angulation and increased strain on the ligaments of the knee [36]. ACL injury is one of the lower extremity injuries that hip proprioception and neuromuscular control could likely involve. Hip neuromechanical characteristics effects knee angles and moments. Risk factors for ACL injuries are multifactorial; and possible intrinsic factors are anatomical, hormonal, neuromuscular and biomechanical characteristics, previous injury, prior, reconstruction of the ACL, and genetics [39,40]. Female athletes have been identified at increased risk of ACL injuries during certain sports with the greater injury rates than men. Several sex-based differences were also identified and there is an important underlying mechanism in terms of hip proprioception. It’s found that females land from a jump and perform cutting-pivoting maneuvers with less knee and hip flexion, increased knee valgus, increased internal rotation of the hip coupled with increased external rotation of the tibia, and increased quadriceps muscle activation. These movement patterns has been hypothesized to increase the strain in the ACL during activity or sport, it’s also hypothesized that the difference in injury incidence rates between males and females may be attributed to neuromuscular differences and resultant mechanics [40]. Deficits in hip neuromuscular control in different planes of movement could be involved in the ACL injury mechanism [41]. Kinematic analyses of the hip and investigations on muscle recruitment related to the position of the whole lower extremity indicated that females have difficulty controlling the hip during dynamic movement, revealing the possibility that females may be more vulnerable to external forces on the lower extremity and has poor control at the hip leading an increased ACL injury risk. Hip abduction weakness with combination of increased hip internal rotation, could increase knee valgus [42] resulting in higher ACL injury risk [40]. Further investigation is still warranted to understand the contribution of hip proprioception to functional knee stability. Measurement of Hip Proprioception There are several methods to assess joint proprioception with its sub modalities [3,21,43]. The measurement of proprioception is divided into four modalities: 1) JPS-the ability to reproduce the same joint position, 2) Kinesthesia is measured by (a) Threshold to Detect Passive Motion (TTDPM)-ability to detect the initiation of passive joint movement, and (b) Threshold to Detection of Movement Direction (TTDMD)-ability to detect motion and in which direction the motion is occurring, 3) VS-ability to reproduce the same velocity and 4) FS-ability to reproduce the same force [3]. These proprioceptive testing methods rely on conscious appreciation of the mechanoreceptor input. The differences of the results reported in the literature could be related to several factors such as testing device (e.g. open vs. closed chain testing or position of the patient with respect to gravity leading to different muscular actions), the assessment procedures (e.g. joint angles, active vs. passive testing, direction and speed of the movement, 5 ipsilateral vs. contralateral matching responses), and the study design (e.g. experimental group compared with control group or bilateral comparison). Seeing the position and the targets or hearing the noise coming from the test device may give clues to person who is being tested. Therefore, subjects are usually wear blindfold and headphones, and pneumatic cuff to eliminate confounding cues. Isokinetic dynamometers, goniometers, electromagnetic tracking devices, 3D optoelectronic analysis, video analysis, potentiometers, custom-made jigs, manually controlled or motor-driven proprioception testing devices are used as testing devices [43]. Joint position sense assessment JPS assessment measures the accuracy of position replication and can be conducted actively or passively in both open, and closed kinetic chain positions [43]. The accuracy of JPS is often measured by goniometers and video analysis systems. The testing protocols usually comprise the definition of a target position that is identified and appreciated by the subject, with no vision. Then, the target position is reproduced passively or actively to the best of subjects’ ability. Active JPS testing is mostly influenced by muscle spindles and cutaneous information. Mechanoreceptors are sensitive to the joint position. Ruffini corpuscles detect joint limits. If a joint is moved into its limits, capsule stress increases, and Ruffini afferents are excited proportionally to the stress. The Golgi tendon organs are sensitive to joint position, tension and movement, measuring ligament and tendon tension and sensing active tension within the myotendinous unit. In extreme positions they fire through their Ib-afferents, thereby inhibiting the α-motor neurons [44]. The test position, Range of Motion (ROM) and the degree of generalized laxity of a person will affect the sensitivity of the mechanoreceptors. Procedure of the proprioception test is essentially similar [3,5-9,11-14,43,45,46]. First; target angle is familiarized by the participant. In target angle, the participant holds the position for 3-5 sec and remembers what the position feels like at the hip. Then the patient returns to the starting position passively with the help of the examiner or actively by him/herself. After a short rest for a few seconds, test angle is reproduced in the same leg passively or actively. Participant acknowledges verbally or presses a manual trigger (stop button) when he/she believes that the angle is achieved. The “replicated angle” is noted. Either active or passive testing results are reported as the Absolute Angular Error (AAE), defined as the absolute difference between the target position and the estimated position, the Relative Angular Error (RAE), defined as the signed arithmetic difference between a test and response position, and the Variable Angular Error (VAE), commonly represented by the standard deviation from the mean of a set of response errors [21]. Hip JPS can be assessed in weight bearing standing position and in open chain activity. Closed chain activity is convenient because it mimics activities of daily life [3]. After active teaching the target angels of the ROM, test is performed for five to ten times for each leg. Average of multiple measures is more reliable then only one measure [11]. However repetitions should be limited because fatigue experienced by the subject from the high repetition may adversely alter joint proprioception results. The discrepancy in start and stop angles is recorded as the error. Benjaminse et al., found only hip adduction JPS testing as a reliable method with an intersession ICC (SEM) of 0.753 (0.248). Intersession ICC’s of other directions of hip movements varied between 0.070 and 0.737. Intrasession ICC’s were even lower in all directions and ranged between 0.159 and 0.319. Further investigation is warranted to develop reliable and precise measurement methods for active JPS of the hip [3]. Mendelsohn et al., used “passive-to-active” reproduction technique (passive teaching, active replication) in open chain activity with electrogoniometer in patients after hip fracture [11]. The mean AAE was calculated. In terms of test–retest reliability, when more trials were performed proprioception testing produced more reproducible results with ICCs varying from 0.510 to 0.690, whereas the ICCs of single measurements were lower. Authors recommended the use of non-injured side as the control in the assessment of hip proprioception. This finding can guide other researchers or clinicians planning to measure 6 hip flexion [11]. Proprioceptive testing in the closed-chain model allows partial body weight bearing during test [12]. Additionally, in the close chained testing, there might be additional afferent inputs from receptors of lower extremity muscles. The input from muscle would integrate with the hip proprioceptive information, resulting in more accurate perception. Lin et al., [12] declared that the AE could be considered as the representative of accuracy of overall performance. The VE represents the inconsistency in each performance (response). These two variables demonstrated the validity (AE) and reliability (VE) of the repositioning test [12]. Functional squat system is another option for close chained proprioceptive testing [47]. This system is reliable and valid for assessment of motor coordination and proprioception and mimics the movement-coordination pattern of a squat jump under the control of external load throughout the concentric and eccentric phases. Although this test position for a whole lower extremity is more like a real life activity, researchers pointed out that these sorts of tests that includes weight-bearing procedures can provide extra sensations that may directly affect joint receptors [47]. Electromagnetic tracking motion analysis system [13] and potentiometer was also used to measure hip JPS proprioception [8,9]. It has been suggested that the velocity of angular displacement is of considerable importance in perception of joint position, and that initial limb position has no effect on joint position recognition [9]. However, there is no reliability information of these methods, neither is of hip JPS assessment during internal and external rotation [6,14]. Kinesthesia Sense of limb movement is assessed by measuring the TTDPM and TTDMD. These tests quantifies a subject’s ability to consciously detect movement, as well as, its direction and is often performed on some type of proprioception testing device such as an isokinetic dynamometer [3,21,43]. Testing speeds are slow, ranging from 0.5 to 2°/s, in order to target the slow-adapting mechanoreceptors such as Ruffini endings or Golgi-type organs while minimally stimulating muscle receptors [43]. In shutting down muscle activity, TTDPM is often chosen to assess afferent activity following ligament pathology [3]. While the examiner passively move the leg, subject indicates (usually stops the device by pressing a “hold” button) when the passive movement is detected and the examiner records the amount of movement occurring before detection [21]. Benjaminse et al., indicated a reliable and precise method of measuring hip TTDPM [3]. Participant’s hip was moved passively at a rate of 0.25°/s using an isokinetic dynamometer. The participant was instructed to focus on their hip position and press a stop button as soon as motion was perceived and the direction of movement could be identified. The displacement between the initiation of motion and the subject’s perception of motion and direction was recorded in degrees. Sagittal plane testing was done in supine position with the knee extended. The test started with the hip in 45° of flexion. Frontal plane testing was done in side-lying position with the knee extended. The test started with the hip in 15° of abduction. Five repetitions for each direction were performed in a randomized order. Good intra-session reliability was shown for hip abduction, and adduction with ICCs between of 0.825 and 0.765, respectively. Good intersession reliability was shown for hip flexion, extension, abduction, and adduction with the ICCs ranged between 0.777 and 0.810 [3]. Wingert et al., [14] assessed hip kinesthesia with goniometer and limb positioning device. Participants immediately reported movement direction on detecting passive hip rotation of approximately 0.5°/s with a maximum displacement of 4°. Movement was imposed passively using a control rod attached to the back of the goniometer. Direction was pseudorandomly selected per trial. Performance accuracy was the number of correct responses in 10 trials for each limb. However, there is no reliability information regarding this methodology [14]. Force sense Sense of tension is assessed with measuring the ability to reproduce torque magnitudes produced by a group of muscles [43]. The force-matching protocols are conducted without 7 vision and with low load, as the ability to reproduce force is associated with the recruitment of motor units and its firing frequency. The difference between the target force and the torque produced is used to quantify the accuracy of sense of tension [21]. Benjaminse et al., measured FS by assessing the ability to reproduce a reference torque in hip joint. FS is thought to have two sources: the sense of tension generated by afferent feedback from the muscle, and the sense of effort generated centrally. FS reproduction should provide information regarding the integrity of muscle spindles and Golgi tendon organs per given effort. Further investigation is needed to develop reliable techniques for FS measurements of the hip [3]. Velocity sense Currently, there is no study on the ability to reproduce the same velocity in hip joint that is the last sub modality of the proprioception. Hip Proprioception and Age There is limited number of researches examining proprioception of the hip in the literature. Most of the studies have been conducted on middle aged or older adults [79,11,18,32,46,47], whereas few studies focused on younger populations [3,6,12-14]. Pickard et al., investigated the effect of age on hip JPS and declared no difference between young and older subjects’ active or passive JPS. It’s known that people who exercise regularly have greater strength and shorter reaction times. Therefore, the reason of that they were unable to show a difference of proprioception between age groups might have been that their older group included active people. In both age groups, hip JPS were more accurate when performed actively than passively, especially when performed in the inner range of the hip abductor muscles. As the muscle spindles are regarded as more important in proprioception, active contraction of the hip abductors that requires contribution of the muscle spindles might provide more afferent feedback regarding joint position than do the passive movement [13]. Wingert et al., were the first researchers showing that hip proprioception declines with age. They determined that older and middle aged adults had significantly increased JPS error compared to younger adults. Kinesthesia was deteriorated in older adults compared to younger and middle aged adults. Correlation between age and proprioception was also found. Moreover, hip proprioception was correlated with dynamic balance whereas no correlation was found in postural sway during static stance [5]. Two strategies were stated in maintaining dynamic postural control: a hip strategy and an ankle strategy. Generally, the ankle strategy is most often used by healthy individuals whereas the hip strategy is used by elderly individuals. Positive correlation between hip proprioception and dynamic balance can be explained by the findings of two researchers. Shumway-Cook and Horak suggested that stance on pliant surfaces caused an increased reliance on a hip strategy [48]. It’s stated that the ankle is of primary importance during single-leg stance on firm, foam, and multiaxial surfaces, whereas proximal joints having an increased role in more challenging conditions [49,50]. Hip Proprioception and Problems Involving Hip Joint, Healthy People vs. Patients Hip fracture in older people is a major public problem causing disability, mortality and morbidity [11]. Deterioration of joint proprioception was declared to be one of the risk factors for falls because errors in proprioceptive acuity can lead to faulty or delayed corrective reactions [4]. Thus, researchers interested in hip proprioception whether proprioception impairs due to fractures, treatment methods such as hemiarthroplasty or total hip replacement and also the effects of rehabilitation on proprioception. Studies investigating hip proprioception in older adults agree that people with hip fracture or total hip replacement or hemiarthroplasty have no proprioceptive deficit [7,8,10]. Ishii et al., 8 determined that hip joint proprioception of people with hip fracture was not found to be diminished compared to age-matched normal controls. Moreover proprioception in patients treated with hemiarthroplasty wasn’t deteriorated when compared with patients treated by osteosynthesis [7]. They pointed out that the surgical capsulotomy and replacement of femoral head didn’t affect the ability to detect joint position. The physiologic implication of that study is that substantial extracapsular components such as stretch receptors in the adjacent tendons and muscles influence hip joint proprioception, rather than capsule and femoral head. It’s stated that a decline in lower limb proprioception may contribute to abnormal balance responses and increased falls in the older population. Skinner et al., defended that a decrease in proprioception could lead to abnormal joint biomechanics during functional activities such as walking so that, over a period of time, degenerative joint disease may occur [51]. Pain was found as an important factor for impaired postural balance. Pain-induced neural muscle inhibition or altered proprioceptive feedback from a painful body part can negatively affect the motor responses needed to control balance [50]. However, to date there is no study on the relationship between pain and hip proprioception. Moraes et al., identified mechanoreceptors and free nerve endings in the femoral head ligament, labrum, and capsule joint in hip serving to stabilize hip joints [32]. Reduction in the number of collagen fibers and vessels was found in the hips with arthrosis. Morphology of mechanoreceptors was similar in the hips with or without arthrosis. The density of Pacinian corpuscles was significantly more than densities of Golgi corpuscles and Ruffini endings while free nerve endings were found with similar density in healthy subjects’ hips. In the hips of the patients with arthrosis, there was a significant reduction of Golgi corpuscles when compared with Pacinian corpuscles and free nerve endings. Total density of mechanoreceptors in the hip without arthrosis was found to be more pronounced and a decrease determined in the number of the nerve endings observed in hips with arthrosis. These findings demonstrate the evidence of the significant role of these structures in the proprioceptive system and stability of the joints. Authors stated that their findings are valuable to help to develop an efficient rehabilitation program, and they recommend performing studies to clarify the functions of the mechanoreceptors in the hip joints, as the treatment of most orthopedic diseases is beginning to include programs for proprioceptive rehabilitation [32]. It’s been aforementioned that only few studies focused on role of hip proprioception in the young population [3,6,12-14]. Benjaminse et al., [3] aimed to establish the intrasession and intersession reliability and precision of TTDPM, FS, and active JPS tests for the hip in healthy individuals between the ages of 18 and 30 years. A reliable and precise method of measuring hip TTDPM was established. However, they stated that further study is needed to develop reliable measurement methods for FS and active JPS of the hip and to identify if TTDPM is related to hip kinematics, hip kinetics, and muscle activation about the hip during functional activities [3]. Other studies including young population were on children with CP [6,14]. Proprioception impairment in the lower extremity can directly impact balance and gait [17]. People with CP has balance problems and tend to rely disproportionately on visual input to maintain posture and to position their limbs during gait or other functional activities, which may be due to deficits in proprioception. Wingert et al., assessed active JPS and kinesthesia of hip joint internal/external rotation bilaterally in patients with hemiplegic and diplegic CP (both have milder impairment) and an age-matched group without disability [14]. They found bilateral joint-position sense deficits in the lower extremities of both CP groups, whereas kinesthesia was rather similar. There was no proprioceptive error when the participant was able to see his/her leg and targets. It’s suggested that patients with CP use visual input as a compensatory mechanism for activities involving JPS. Researchers indicated that internal rotation errors reflect common lower extremity musculoskeletal alignment in CP. Patients with CP have increased internal femoral torsion and hip 9 adduction during standing and walking compared to people without disability. Abnormal biomechanical alignment, muscle weakness or imbalance, and/or increased muscle tone related to CP cause internally oriented joint-position errors. Additionally, muscle changes related to spasticity also might impair joint-position sense over time by shortening and stiffening muscle tissue, altering the muscle-joint relationship and disrupting the sensitivity of muscle spindles, which contribute to proprioception [14,17]. It’s known that ankle strategy is typically utilized for Anterior–Posterior (AP) balance and a hip strategy is typically utilized for Medial-Lateral (ML) balance [52]. Largest contributor to ML balance in both healthy and CP children was found as transverse body rotation and this was proportionately even greater in patients with CP perhaps as a consequence of compensation for poor ankle control [53]. Cherng et al., showed that CP patients don’t differ from healthy ones in their static balance abilities whereas there are certain deficiencies in dynamic balance [54]. In the light of these information Damiano et al., investigated the contribution of hip joint proprioception to static and dynamic balance in milder diplegic and hemiplegic CP [6]. They believed that measurement of hip proprioception is relevant in CP because patients tend to rely disproportionately more on this joint in their balance strategies compared to healthy people. They have found that increased hip proprioception error was related to increased postural sway and decreased gait velocity, especially in children with hemiplegic CP, whose dominant side hip proprioception error was an important determinant of gait velocity. Patients with CP had greater differences from control values in the center of pressure in ML direction than in the AP direction, possibly due to both biomechanical and neurological changes seen in CP. Physical Activity, Sports Participation, Exercise and Hip Proprioception Favorable effects of regular physical activity or specific exercise programs on physiologic systems are acknowledged. Regular proprioceptive activities allow retaining an excellent response to somatosensory inputs, which may be useful for maintaining proper balance in everyday life [55]. However, there is limited information on the effects of proprioceptive exercises on hip proprioception and there are few studies showing the effects of physical therapy exercise programs on hip proprioception. After a hip fracture progressive gain of the range of motion, strengthening and functional drills, proprioceptive, balance-related and postural drills, are usually used when bone union process is satisfactory and/or the surgical procedure assures protection and stiffness to the injured part and partial or total load is allowed to the affected limb. Yet, it seems there is no evidence for specific proprioceptive exercises to improve proprioception. Generally, physical therapy programs consisting strength and endurance exercises and/or balance and gait drills were used [11,56]. Hip proprioception improvement was found following rehabilitation of hip fracture [11]. Mendelsohn et al., tested proprioception first within 48 hrs of admission to the rehabilitation unit and again within 48 hrs of discharge. A complex program composed of range of motion, flexibility, and strengthening exercises; balance, gait, and stair retraining; and activities of daily living training were performed. It was stated that this rehabilitation program improved proprioception indirectly related to other variables, gait, isometric muscular strength since they depend on the full integrity of proprioceptive sensations to be regarded as satisfactory and appropriate for each individual [11,18]. This improvement probably due to induced morphological changes in the muscle spindles [33] because physical activity doesn’t change the amount of the mechanoreceptors [57]. Modulation of the muscle spindle gain and the induction of plastic modifications in the CNS by regular physical activity and exercise are able to change proprioception [57]. Beneficial effects of physical therapy and kinesitherapy on postural stability in men with hip osteoarthritis were shown previously [58] but no direct measurement for proprioception was performed. Ozer Kaya et al., examined lower extremity proprioception after calisthenics and pilates exercise training in sedentary adult women in their randomized controlled trial [47]. They measured not the pure hip or knee joint proprioception, but rather they followed a multijoint approach in a squat position. 10 Neither calisthenics nor pilates exercise trainings improved proprioception after 6 months, but improved lower extremity coordination [47]. One study investigated the hip and knee proprioception in elite, amateur, and novice healthy young men tennis players [12]. Joint angle duplication in closed chained position test was used to determine proprioception. Matching error was smaller in the stance-dominant leg, possibly due to more practicing stance-dominant leg because the adjustment of the height of center of gravity before a stroke might more depend on the stance leg in tennis. The elite tennis players had the less amount of error in the position-matching test than the amateur and novice groups. Proprioceptive sensitivity of healthy people can depend on their activity and skill level. Supporting this statement, people with intensive training, like professional athletes, have better performance in proprioception testing. Researchers pointed out the need of prospective design using a proprioception testing apparatus with accurate velocity control to determine the causality between proprioception and training [12]. Injury/Re-Injury Prevention Three systems work together to maintain postural control: The somatosensory system, the vestibular and the visual system. The vestibular system, gathers information from the vestibules and semicircular canals of the inner ear for overall body posture and balance. The visual system helps to maintain balance. If the eyes are closed, help of the visual system is removed. Some of the imbalances within the athletes are not recognized and are therefore not modified until an injury occurs. When an injury occurs in a joint, the joint loses its ability to gauge stresses placed upon it and react to it appropriately [59]. In case of an injury muscle, tendon, and ligament are damaged. In the mean time, mechanoreceptors are also damaged leading decreased neural afferent input and diminished kinesthetic acuity and, therefore, neuromuscular control. The coupling effect of ligamentous trauma resulting in mechanical instability and proprioceptive deficits contributes to functional instability. This could cause to further microtrauma and re-injury. Deteriorated proprioception may play a more significant role than pain impulses in preventing injury. Re-injury rates and the cause of chronic injuries may be attributed, to a greater extent, to proprioceptive deficits [27]. Peroneal muscles assist maintaining balance in the ankle strategy, which is most often used by healthy individuals. Ankle strategy is used when perturbation is slow and low amplitude. The hip strategy is used when the perturbation is fast and large amplitude. Interestingly, hip strategy that is used by elderly individuals is also adopted by individuals who have sustained an ankle sprain. In this strategy, gluteus medius muscle is used to correct posture and keep an individual balanced and erect [60]. Leavey et al., investigated the effects of 6 weeks gluteus medius strength training, proprioception training, and a combination of those on dynamic postural control measured with The Star Excursion Balance Test [61]. Use of exercises for proprioception, gluteus medius strength, or a combination program was found as beneficial to improve dynamic postural control in healthy, active individuals [61]. Proprioceptive system could have a role for this improvement. Nevertheless, the specific contribution of the systems was not known since the authors didn’t use discriminative measurements for each system. These findings may be valuable for elderly people and athletes who tend to injure certain joints repeatedly. For the lower extremity, mechanoreceptors located within the joints are most functionally stimulated in closed-kinetic chain positions with perpendicular axial loading of the joint. These exercises are recommended at various positions throughout the full range of motion because of the difference in the afferent response that has been observed at different joint positions [27]. Improved hip proprioceptive function may potentially reduce the risk of injury and even may improve performance as it has been shown for other joints such as knee, ankle and shoulder [27]. However, there is a lack of information on the relationship between hip proprioception and lower extremity injuries. Furthermore the preventive effects of good hip proprioception or the effects of specific hip proprioception training on injury/re-injury prevention are still unknown. Studies 11 using direct proprioception measurement methods to understand the pure effect of proprioception instead of the information derived from multiple systems (somatosensory, visual and vestibular) in maintaining postural control are also needed. Hip Proprioception Exercises Although very little is known about the effects of proprioceptive exercises on hip proprioception, still there are proprioceptive exercises that can be performed based on the proposed effects of them and mechanisms of the possible improvement of proprioception. Proprioceptive exercises stimulate the nervous system promoting muscle responses that encourage neuromuscular control. Goals of the proprioceptive training are; increasing the frequency of muscle unit stimulation, the synchronicity of motor unit firing and proprioceptive and kinesthetic awareness. For the proprioceptive rehabilitation, retraining of altered afferent pathways to enhance the sensation of joint movement is crucial. Encouraging maximum afferent discharge to the CNS is the goal in stimulating joint/muscle receptors. Activities with sudden alterations in joint positioning that necessitate reflex neuromuscular control stimulates reflex joint stimulation at the level of spinal cord. Balance and postural activities with Eyes Open (EO) or Eyes Closed (EC) enhance motor function at the brainstem. Performing joint positioning activities, especially at joint end ranges with high repetition stimulates the conversion of conscious to unconscious motor programming. Kinesthetic and proprioception training can enhance this function [27]. As it is for any type of exercise training, a proper progression should be followed for proprioceptive exercises too, starting with static balance activities, progressing to dynamic balance activities and finally advancing to coordination and agility training. Training starts with simple exercises and complexity is increased as proprioception improves. The surface, the distance, or the weight of the objects (i.e., medicine ball) used to distract the individual is changed. From EO condition to EC, from the position on two feet to one foot, standing still for a few seconds to 30 sec, simple to complex, focusing to distracting, slow speed to fast movements can be used for the progression. Highlights of the proprioceptive exercise training program Adequate warm up should be performed before proprioception exercises. Training could be three times a week for at least 6-8 weeks. Body weight, age, level of competition and footwear should be considered while planning a proprioceptive training. Children and older adults have higher risk of injury. Children’s CNS is not fully developed and information is not transmitted quickly enough to provide the necessary safeguards against excessive body stresses. Message transmissions to and from the CNS tend to slow with age [62]. Acute inflammation, postoperative conditions, instability should be carefully evaluated. Correct technique is the vital part of the whole training. Good postural alignment during each movement with no compensating with the other parts of the body should be provided during proprioceptive exercises. If the proper technique cannot be maintained during exercises the difficulty level should be decreased to a level that the individual can perform correctly. Feedback is needed to recognize the successful completion of a task. High repetition is also very important for cognitive programming of motor patterns [63]. However, fatigue should be avoided [64]. If proprioceptive exercise training is properly planned and executed, proprioception can be improved and the risk of future injuries can be reduced. Females need special attention when planning these trainings due to particular reasons. They exhibit a wider pelvis and increased genu valgus, generate muscular force more slowly than males, tend to have less developed thigh musculature, exhibit less effective dynamic stabilization, and lose hip control upon landing when performing jumps [65]. 12 Closed chain exercises Most of the physical therapy programs have been developed to take advantage of the force-generation and loading characteristics of closed-chain exercises. Closed chain exercises could be an important part of hip proprioceptive training because, the effect that closed-chain exercise have on the entire kinetic chain is more functionally important than the effect on one joint alone (i.e. ankle or knee). Closed-chain exercises are based on application of a load to the distal end of an extremity that doesn’t move freely due to either positioning or the load type (axially applied load). Subsequent joint motion takes place in multiple planes while the limb is supporting weight [66]. Closed kinetic-chain exercises are very specific to the functional demands placed on the lower extremity during sport or occupational activities [63,66]. During closed chain activities, the body moves over the foot resulting in simultaneous movement of all lower extremity joints and coordinated muscular activity including concentric and eccentric co-contraction of antagonistic muscle groups that are required to control all segments of the kinetic chain [63]. Kinetic-chain segment motions and positions are created by agonist-antagonist muscle activation patterns. Cocontraction of these force couples around a joint occurs to control joint perturbations and to gain stability. Resultant synergistic patterns create postural stability throughout the entire extremity while allowing voluntary muscle activity at the distal segment. It’s highly dependent on joint- and angle-specific proprioceptive feedback [27]. In terms of lower extremity neuromuscular control, hamstring muscles act not only as a part of a lengthdependent force couple to control anterior tibial translation, but also as a part of a forcedependent pattern to coordinate hip and knee motion, stabilize the hip, and transfer loads up and down the leg. Most of the proprioceptive exercise programs use closed chain activities because they simulate biomechanical and physiologic requirements. Mechanically, they initiate joint movements from a base of support, emphasize sequential control of segment position/motion, place the segments in functionally correct positions, and control the load transfer. Physiologically, they utilize both length-dependent and activity-specific forcedependent activation patterns, emphasize position-specific proprioceptive feedback to initiate and control activity. After an injury, activation of the inhibited muscles should be encouraged by “facilitation of muscle activation” with placing the extremity in a closed-chain position, emphasizing the normal activation pattern, and progressively “unmasking” the target muscle by eliminating the substituting muscle. Micro or macro trauma to tissues that contain mechanoreceptors may cause proprioceptive deficits due to partial deafferentation leading possible re-injury. Maintaining neuromuscular control or regaining it after injury or surgery is a necessary prerequisite for the individual in returning daily life or occupation, and for the athlete in returning to sports [27]. Hip proprioception exercise training program In the first stages of the training (Phase I) closed chain exercises and active repositioning of the hip joint can be performed [63]. Initially, proprioceptive exercise training usually begins with two-legged support stance on a flat surface in static conditions, and then is moved into a one-legged support stance as a progression. Early emphasis is placed on achievement and maintenance of a position of 0° of hip extension with neutral pelvic tilt for maximum activation of the hip muscles. Most of the lower extremity exercises proceed from this ideal position [66]. Depending on the individual’s level, standing still on the floor starting from the position on two feet for 30 sec (can be started with 10 sec according to patient’s ability and gradually progressed to 30 sec) with EO is continued with EC. Tandem stance (one foot in front of the other, heel to toe) or standing on one foot (keeping hip and trunk in extension posture) with EO and then EC can be practiced for 30 sec for each [20]. Patient may touch a table, chair or wall for support if she/he doesn’t feel secure, at the very beginning (Figure 1). 13 Figure 1: Early-stage lower extremity closed chain exercise; standing on one leg. Tools such as soft surfaces (i.e., foam), stability trainer, balance board, disc trainer, BOSU balance trainer, or trampoline fulfill the need of unstable surface throughout the progression [62,66]. It should be noted that standing on an unstable surface is called proprioceptive training, however in fact it is a combined training of proprioceptive, vestibular, and visual systems, since the visual and vestibular systems help the somatosensory system to maintain control and balance on unstable surface. If the eyes are closed, the contribution of the visual system drops out. Standing still on both feet is progressed by calf-raises, multidirectional hip positions, squats, and lunges. Perturbation could be performed. Elastic resistive band can be looped around the body or leg as training progressed. Closed chain exercises can be also performed on floor/exercise mat. Bridging exercise is performed in supine position with palms facing down and feet on the floor in hook-lying position. This exercise can be progressed from two-legged position to one-legged position as one knee is extended and held at the same level as the other kneecap. Side-lying plank exercise with and without knee support can be added the exercise program, respectively [67-69]. Exercise ball is also used to improve neuromuscular control of the trunk and hip [70]. It is a stabilization tool for neuromuscular control using inhibition or facilitation. It facilitates automatic postural reactions and co-contraction ultimately reflex stabilization. Swinging on the ball either facilitates muscle spindle with faster, longer amplitude and more variation in movements or inhibits muscle spindle with slow, short amplitude and rhythmic movements. Bridge knee extension, bridge hip lift stabilization, wall squat, sitting knee extension, sitting hip flexion and pelvic clock exercises can be recommended to improve hip proprioception (Figure 2, 3, 4) [71]. 14 Figure 2A: Bridge knee extension. Figure 2B: Bridge hip lift stabilization. A B C Figure 4: Pelvic clock exercises. 15 In addition, bridging exercise can be performed with positioning of the distal portions of lower limbs in a sling suspension system to add a dynamic stabilization effort [72]. Bridging exercise starts from the supine position with palms facing down and the ankle regions of both lower legs is placed with the feet at shoulder width in the holding straps of the sling system to establish the body suspension point during the exercise. The height of the straps is adjusted in accordance with the knee level in hook-lying position with knee flexed to 90 degree. Bridging exercise is performed using an abdominal drawing-in maneuver. To perform the bridging exercise, pelvis is lifted into the air until the angle of hip flexion reaches 0 degree while maintaining straight alignment of the knees, hips, and shoulders [72,73]. Progression should be arranged considering the fact that hip joint has an increased role in more challenging conditions [49,50]. Progression is first achieved by removing one knee from the sling and holding it at the same level as the other knee, second by having both knees placed in the sling and placing a balance cushion in between the scapulae to provide an unstable proximal surface upon which to perform the bridge, and finally third by placing the ankles in two separate slings and performing the bridge and then abduct the legs one at a time before lowering back to the starting position [72]. Park et al., stated that during dynamic limb movements such as hip abduction and adduction, and particularly bilateral movements proprioceptive system activation might increase [73]. Integration of hip movements may make bridging exercise more challenging because it requires controlling the errors of active repositioning against the destabilizing torque and perturbation force of the trunk during the hip movements [72,73]. Dynamic hip movements can provide a better opportunity to facilitate sensory-motor feedback, leading recruitment of trunk muscles during the bridging exercise to establish efficient motor control strategies [73]. Closed kinetic chain stabilizing exercise of the lumbo-pelvo-hip complex can be performed in the prone position as well with or without a sling [74]. As soon as the static activities are performed properly with good coordination and speed, more dynamic activities should be added the training program (Phase II). Resistive elastic band quick kick exercises in multiple directions of hip movements are also recommended to improve proprioception, strength and stabilization of the stance leg thanks to their closed chain nature (Figure 5). A B C Figure 5: (A) Hip abduction with resistive elastic band “Quick Kick” (B) Hip extension with resistive elastic band “Quick Kick” (C) Hip flexion with resistive elastic band “Quick Kick”. 16 Kicking activity is used to stimulate proprioceptors around the joint in response to positional changes of the body’s center of gravity. Reflex activation and co-contraction of muscles occurs during resistive kick and this activation seems more in kick when compared to other closed chain exercises such as step-up or trampoline [75,76]. Use of proprioceptive exercise tools can also be continued in this phase but in more dynamic fashion such as standing on one foot with repeated multidirectional hip movements, and squats. Progression in perturbation exercises and use of elastic resistive bands looped around the leg while standing on foam could be useful to increase complexity. Sliding board, fitter, or Bongo Board fit in this phase [66]. Playing catches with medicine ball in different weights is a distracting activity that can be used during progression. Dynamic lunges, walking (+cone walking and/or use of sports cord) or running forward, backward and lateral directions can be used increasing speed or complexity in time. Co-contraction lateral slides, mini-tramp hopping and jogging, pogo ball balancing and hopping, advance lateral slide board exercises are performed towards the end of this phase and continued in the last phase if needed [63]. In advanced level (Phase III), agility and coordination exercises such as pivoting, twisting, reaction cutting drills, shuttle run, carioca crossover maneuvers, four-corner running, and/or jumping are performed. Plyometric exercises take place in the program. Sport specific activities both on unstable platforms and in the playing field should also be performed in the athlete’s advance training towards the final stages [20,63]. Cross-training A proprioceptive cross-training (contralateral training) effect was found for ankle [77]. It’s pointed out that the CNS takes the pattern of control established in the trained leg and applies it to the unworked one. Possible mechanism suggested for this is a phenomenon in the nervous system, both at the level of the spinal cord and the motor cortex [78]. If proprioceptive cross-training effects for hip can be determined, that information would be highly valuable and have large implications for the rehabilitation. Rehabilitation protocols could be designed to include proprioceptive training of the sound leg in the very early stages of the rehabilitation when the injured leg is not ready to start training directly. Athlete could return to normal more quickly when training is resumed. Similarly, in neurologic problems involving unilateral extremity, proprioceptive exercises for the sound side of the body could help the contralateral side. More recently, Kim et al., found that short duration isokinetic exercise training of the contralateral hip improves single-limb stance in the interested leg [78]. Further research should be performed to clarify how effective cross-training is in comparison to direct training of the leg to improve proprioception and balance and the exact mechanism of this improvement. In brief, drawing certain conclusions with limited information on hip proprioception in the literature may be difficult. Hip proprioception is still an exciting and promising new area for future research. Future studies are needed to develop reliable measurement techniques for hip proprioception in order to interpret the results precisely. 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