Journal of Electromyography and Kinesiology 12 (2002) 205212 www.elsevier.

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Consequences of a ligament injury on neuromuscular function and relevance to rehabilitation using the anterior cruciate ligamentinjured knee as model
Eva Ageberg
Department of Rehabilitation, University Hospital and Department of Physical Therapy, Lund University, Lund, Sweden

Abstract The purpose of this article is to survey current knowledge concerning the consequences of a ligament injury on neuromuscular function and its relevance to rehabilitation, in relation to clinical practice. Although it deals with the ACL-injured knee, these views may also apply to other joints. The effects of a ligament injury on neuromuscular function are rst considered i.e., proprioception, postural control, muscle strength, functional performance, movement and activation pattern, central mechanisms, motor control and learning. The treatment and effects of rehabilitation on neuromuscular function are then discussed. The survey is concluded by discussing the clinical signicance. 2002 Elsevier Science Ltd. All rights reserved.
Keywords: Anterior cruciate ligament; Lower extremity; Neuromuscular; Performance; Rehabilitation; Training

1. Introduction The anterior cruciate ligament (ACL) is the commonest ligament injured in the knee, and several studies have evaluated the consequences of such an injury. Rehabilitation programs formerly focused mainly on restoration of muscle strength, but during the last 10 years, the sensory function of ligaments in relation to functional joint stability has been regarded as important in rehabilitation after a ligament injury. Even though this review deals with the lower extremity and knee, the views expressed here may apply to other joints as well and should be of interest for treatment of a ligament injury.

a motor response. Sensory receptors are present in the skin, muscles, joints, ligaments and tendons. Since a ligament injury causes a disturbance in the somatosensory system it may affect the central programs and motor response. 2.1. Proprioception The threshold for detecting passive motion (TTDPM) is the most established and probably the most sensitive test for measuring proprioception [29]. The knee is passively moved into exion or extension and the subject responds as soon as the movement is felt. Many authors have reported defective proprioception after an ACL injury or ACL reconstruction, measured with TTDPM [4,9,10,14,26,3033,54,61,65,79], despite rehabilitation. Signicantly higher threshold values have been found in injured and uninjured knees than in uninjured knees of controls, indicating bilateral proprioceptive defects [65]. Friden et al. [32] reported that in the near-extended knee position the basis for weightbearing during stance, patients with symptomatic ACL-decient knees were less able to detect a passive movement. They also noted signicant correlations between the patients proprioceptive ability and associated chondral and meniscal lesions, as well as the subjective rating of knee function [31]. Patients with symptomatic ACL-decient knees have

2. Consequences of a ligament injury on neuromuscular function The visual, vestibular and somatosensory systems contribute afferent information to the central nervous system (CNS) regarding body position and balance [71]. This neural input is integrated by the CNS to generate
Corresponding address: Department of Physical Therapy, Lund University, Lasarettsgatan 7, SE-221 85 Lund, Sweden. Tel.: +46-4630-30-96; fax: +46-46-222-42-02. E-mail address: eva.ageberg@sjukgym.lu.se (E. Ageberg).

1050-6411/02/$ - see front matter 2002 Elsevier Science Ltd. All rights reserved. PII: S 1 0 5 0 - 6 4 1 1 ( 0 2 ) 0 0 0 2 2 - 6

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higher threshold values than controls, but no difference has been observed between asymptomatic patients and controls. These ndings indicate that impairment in knee joint function is related to a reduced proprioception after ACL injury [65]. 2.2. Postural control Several authors have found a disturbed postural control in single-limb stance in the injured and uninjured legs after an ACL injury [35,53,88] or reconstruction [39,40,69], even after rehabilitation. Higher amplitude values [35,53,69,88] and longer reaction time when subjected to perturbations [39,40,53] have been observed among patients compared to controls. Shiraishi et al. [69] reported a correlation between one-leg standing balance and subjective rating and functional performance. 2.3. Muscle strength Despite rehabilitation, persistent quadriceps weakness seems to be common in the ACL-injured leg [25,46,83], although others report that quadriceps strength can be restored after rehabilitation [34,49,68,76]. Weakness of the knee extensors correlate with poor knee function [72,82]. Elmqvist et al. [24] found reductions in quadriceps cross-sectional area (CSA), in strength, and in EMG activity on the affected side in patients with ACL injury, suggesting that these ndings were caused by a change in knee joint receptor afferent inow. Lorentzon et al. [50] found no relationship between CSA and strength of the quadriceps in the ACL-injured leg. Only minor atrophy of the quadriceps was observed, but strength was greatly reduced, indicating that muscle size was not the major determinant of strength. They suggested that the reduction in strength was caused by reduced activation of normally functioning muscle bers due to altered afferent feedback from the mechanoreceptors of the torn ACL [50]. Moreover, bilateral defects in voluntary quadriceps muscle activation after a unilateral ACL injury have been observed [78]. Although quadriceps strength seems to be difcult to restore, several studies report restoration of hamstring muscle strength after an ACL injury [34,46,76,83]. 2.4. Functional performance Several tests of function are used to measure lower extremity performance. One-leg hop tests, such as the one-leg hop test for distance, triple jump and stairs hopple test are determined strenuous activity tests, and two-leg hop tests, like the vertical jump, gure-of-eight, and stairs-running test daily life activity tests [63]. Although an ACL injury causes an increase in anterior tibial translation, the magnitude of this does not correlate with functional outcome after an ACL injury [23,37,73].

The Limb Symmetry Index (LSI) has been used, to calculate the difference between the injured and uninjured sides. An LSI of 85% i.e., a 15% difference between limbs is regarded as satisfactory for one-leg hop tests [3]. Abnormal scores on the one-leg hop tests i.e., less than an LSI of 85% correlate with the patients subjective knee function [3]. It has however, been demonstrated that afferent information has an effect on the neuromuscular function of both the ipsilateral and contralateral limb muscles [43], which may explain why both legs are affected after a unilateral injury [35]. Using the uninjured leg as control is therefore unreliable, and patients should be compared with a control group to ensure detection of impairment. After an ACL injury most patients have reduced functional performance [3,35,56,63,75,87]. However, satisfactory results in function have been reported after rehabilitation [13,28,34,76,87], and improvement in functional tests may occur despite weakness of quadriceps strength [46]. 2.5. Movement and activation pattern Solomonow et al. [74] observed that direct stress on the ACL reduced the EMG activity of the quadriceps, but increased that of the hamstrings. Beard et al. [7] found a reduction in reex hamstring contraction latency in patients with ACL deciency, and thought it might be caused by loss of nerve endings in the ACL. Wojtys and Huston [82] reported that muscle timing and recruitment order in response to anterior tibial translation were affected after ACL injury. They also found that athletes had less anterior translation than nonathletic controls, indicating that training stiffened the knee joint [41]. In subjects who had undergone ACL reconstruction, isokinetic muscle strength and endurance, and neuromuscular function, quantied with simultaneous anterior tibial translation and surface EMG tests, did not return to the level of a control group at follow-ups 6, 12 and 18 months after surgery. In addition, bilateral defects were observed in neuromuscular function. The authors proposed that the central nervous system might reduce the neural drive, inhibiting the quadriceps muscles [83]. Although a normal hop distance can be achieved, Gaufn and Tropp [36] found that the movement and muscular-activation pattern in the one-leg hop test of the injured leg differed from that of the uninjured in patients with ACL injury. This pattern seemed to be adaptive and to reduce load on the knee joint. However, Rudolph et al. [66] reported that patients with complete ACL rupture but no subjective knee instability moved almost similar compared to uninjured persons during single-leg hops. Kalund et al. [48] reported a change in the muscle coordination pattern in patients with ACL deciency, compared to controls. When walking uphill, the patients hamstring muscles were activated signicantly earlier than those of controls, probably in an effort to ensure

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knee stability. Some authors have reported quadriceps avoidance gait as a gait adaptation in patients with ACL deciency [8,16], but others have not [64,77]. It has also been suggested that hip or ankle extensors may compensate for the knee extension moment decit during the performance of functional tests, such as a vertical jump and a lateral step-up [25]. 2.6. Central mechanisms Proprioceptive information is integrated by the CNS to orient the body and maintain balance control [45]. Di Fabio et al. [17] reported that a reex response involving the hamstring muscles was found selectively in an ACLdecient extremity. Hamstring activity was signicantly faster in the ACL-decient extremity, than in the uninjured and their study showed that postural responses could be unilaterally restructured and pre-programmed to compensate for joint laxity. Valeriani et al. [79,80] suggested that loss of knee mechanoreceptors could lead to modications in the central nervous system, in patients with ACL deciency or with ACL reconstruction. They also suggested that some patients can compensate for loss of ACL inputs by inputs from other knee and muscle proprioceptors, since they do not develop central somatosensory abnormalities or impairment in knee position sense [80]. 2.7. Motor control and learning Motor control is dened as control of posture, balance, and movement, involving interaction between the individual, the task, and the environment. Motor learning is the process of acquisition and/or modication of movement [71]. Feedback is essential in relearning motor programs [55,71], and since the sensory feedback from the joint is affected after ligament injury, it has been suggested that motor programs have to be modied [43]. Neuromuscular rehabilitation can largely be viewed as motor learning, where the patient has to regain coordinated movements or learn new coordinated movement patterns [55].

adequate positioning of the center of gravity in relation to the supporting area of the foot [86]. Closed kinetic chain (CKC) exercises have gained recognition over more traditionally-used open kinetic chain (OKC) exercises in the last 15 years for use after ACL injury or reconstruction, since they are believed to be safer and more functional [12,27]. Compared to OKC exercises, CKC exercises produce less shear forces and thereby minimize strain on passive structures [51,60,81,84,85], produce greater compressive forces [51,81], increase joint stiffness [47], and increase muscular coactivation [47,51,81]. Muscular coactivation can unload the knee ligaments [58], ensures that the pressure on the articular surface is evenly distributed and joint congruency is achieved [2,70], and is important in maintaining joint stability [2,20]. Recently, Dietz and Duysens [19] reported that load receptors in the feet contribute signicantly to legmuscle activation. Some authors propose the use of both open and closed kinetic chain exercises in ACL rehabilitation programs [27,81]. However, knee extensor strength can be improved by functional training, and training the knee extensors selectively may not be necessary [87]. A crucial point is, that not only the mechanical aspects, but also sensorimotor integration through motor learning are believed to be important in functional training, to effectively use afferent neural input [57], and to improve overall extremity function [6,28,87]. 3.1. Neuromuscular problems in relation to time after injury A range of factors have been suggested to contribute to the functional capacity of an injured knee, such as anatomic, kinematic, physiologic and treatment [21,22]. The envelope of function, a concept developed by Dye [21,22], is a load and frequency distribution that denes a safe range of loading the envelope of function for a given joint. Loads within its envelope of function is compatible with tissue homeostasis, but loads beyond this physiologic capacity lead to overload and can result in structural tissue failure, such as a rupture of the ACL. The limits of this safe range of loading are narrower in an injured knee, and maximum envelope is reached about 1 year after injury/reconstruction and rehabilitation, but will not be restored to the preinjury level. Signs that a joint is being loaded beyond its envelope of function include discomfort, warmth, swelling and functional instability. It has been shown that knee pain and effusion decrease muscle strength [42,59]. The signs of overload are important to consider throughout the rehabilitation period, and patients who have these ndings are recommended to decrease, at least temporarily, the loading of the symptomatic joint [21,22]. It has been reported that muscle function improves up to 18 months after ACL reconstruction [83]. Muscle

3. Relevance to rehabilitation The development of rehabilitation programs after an ACL injury or reconstruction is based on theoretical models and clinical experience, and the aims are to restore joint motion, regain muscle strength and function to the preinjury level or a modied level of activity. Some authors report that active rehabilitation is performed for 58 months after an ACL injury [38,86] and up to 1 year after an ACL reconstruction [38,52]. An efcient function of the leg, hip and trunk muscles is needed to stabilize the body segments and give an

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strength of the quadriceps did not increase at follow-up 6 months after reconstruction, but improvements were seen at follow-ups 12 and 18 months after surgery. A slowing of muscle reaction time and time needed to reach peak muscle torque was observed in these patients compared to uninjured controls [83]. Patients with acute ACL injury (less than 6 months from injury) used a different muscle recruitment order compared to noninjured subjects, but in those with semi-acute (618 months from injury) or chronic (more than 18 months from injury) ACL injury the muscle recruitment order was normal. Muscle timing remained slower in individuals with chronic ACL injury. The authors suggested that muscle timing and recruitment order changed with time from injury [82]. In a prospective study on patients with ACL injury, proprioception was measured repeatedly up to 8 months after injury and rehabilitation [33]. The proprioceptive defects found initially improved with time, but whether this was due to an effect of training or a change with time from injury, or both, require further studies [33]. 3.2. Effects of rehabilitation on neuromuscular function Although rehabilitation is normally included in the treatment after injury or reconstruction of the ACL, few studies specically evaluate the effects of rehabilitation on neuromuscular function [5,6,13,15,28,34,67,68,76,87, 88]. Knee muscle strength is frequently evaluated [5,13, 15,28,34,67,68,76,87], while other measurements of neuromuscular function, such as functional performance [13,28,34,76,87], postural control [88], proprioception [13], and muscle reaction time [6] are not as often included in the evaluation. Increased quadriceps muscle strength and a reduced difference in strength values between the injured and uninjured legs, have been reported after various training programs [5,13,15,28,34,67,68,76,87]. Strength of the injured leg compared to the uninjured has been found to be about 70% [5,15,68] to 90% [34] at a 3-month followup, about 75% [5,15,68] to 90% [28,34] at a 6-month follow-up, and 80%-85% [15,76] to 90% [34,67,68] at a 1-year follow-up, without deterioration at follow-up after 3 years [34] and 29 years [67]. Muscle strength of the injured leg compared to the uninjured was only slightly reduced pretreatment [28,87], but functional performance was greatly reduced [87]. Improvements in functional tests have been observed at follow-ups ranging from 1 month to 1 year [13,28,34,76,87], with persistent effect after 3 years [34]. Normal values in postural control were found in the uninjured leg after 3 months training and after 12 months in the injured one, with persistent effect at follow-up after 3 years [88]. Carter et al. [13] reported that no improvement in joint position sense (JPS) was seen after

a 4-week training program. Beard et al. [6] observed improved reex hamstring contraction latency after 12 weeks training. 3.2.1. Neuromuscular training Lund training concept [86,87,89,90] This training method, developed by Zatterstrom, based on biomechanical and neuromuscular principles, aims to improve sensorimotor control and obtain compensatory functional stability. These principles apply not only to patients with ACL injury or reconstruction, but also to those with other diagnoses, since the training aims to resemble conditions in daily life and physical activities. Shortly after an ACL injury, active movements in synergies of the joints in an injured extremity [62] are encouraged to improve mobility of the injured knee. The patients are told not to make any movement if it causes pain so that the injured structures will have time to heal. They are also asked to do exercises daily at home, to improve joint mobility and functional stability. The latter can be improved by movements performed in closed kinetic chains [51,60], aiming at obtaining congruency of joint surfaces [2,70] by muscular coactivation [2]. This training model emphasizes the enhancement of antigravity postural functions of weightbearing muscles, and provoking postural reactions in the injured leg by using voluntary movements in the other lower extremity, trunk and arms [11,18]. The training model is divided into four levels, according to function. The training usually starts on an individual basis and continues in groups, all under supervision to ensure that the movements are correctly done while gradually increasing individual activity levels. The level of training and progression are determined by the patients neuromuscular function, and not by time from injury. Strength, coordination, balance and proprioception are all included in the movements. These start with the uninjured extremity, initiating the normal movement, applying the bilateral transfer effect of motor learning to the injured leg [18,44]. The goal is to obtain equilibrium of the loaded segments in static and dynamic situations without unwanted compensatory movements. Thus, the quality of the performance in each exercise is very important. To achieve the desired requirement of postural activity, the patients perform the exercises on sloping boards, to obtain axial loading of joint surfaces by muscular coactivation. Progression is provided by varying the angles of the sloping board in relation to the gravity line, by varying the number, direction and velocity of the voluntary movements, and also by training more complex functions, cardiovascular endurance and sport-specic skills. The training stops when muscular postural reactions, provoked by voluntary movements, are clinically evaluated as occurring without delay and are the same as those on the uninjured side (based on visual inspection and palpation).

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The effects of this training concept on neuromuscular function have been studied in consecutive patients with an acute ACL injury who were followed during 3 years [1,86,89,90]. The patients were randomized into two training models: neuromuscular supervised training or traditional self-monitored training. Isometric and isokinetic muscle strength of the knee extensors and exors were signicantly greater or tended to be greater in the injured and uninjured legs in the neuromuscular supervised group than in the traditional self-monitored group. Functional performance was measured with the one-leg hop test for distance. The hop distance was signicantly longer or slightly longer in the neuromuscular supervised group than in the traditional self-monitored group. Six weeks rehabilitation was found to be too short a time period from original injury to obtain normal mobility and restored neuromuscular function. Improvements in muscle strength and functional performance were found at the 12-month compared to the 3-month follow-up, with persistent effect at the 36-month followup. Compared to a control group of noninjured subjects, functional performance was restored to the level of the control group at the 12-month follow-up in the neuromuscular supervised training group and was still normal after 36 months. In the traditional self-monitored group, however, the hop distance was shorter in the injured and uninjured legs throughout the study. Postural control was measured with stabilometry in single-limb stance on a force platform. In both training groups, center of pressure amplitude was consistently higher in both legs during the 3-year follow-up, but average speed was less affected or unaffected, than in a control group of uninjured subjects. A decrease in variance of the values over time was observed, which may reect learning and improvement by training, or a biological adaptation. These results indicate that although functional performance can be restored, the sensory system for maintenance of postural control is persistently disturbed in patients with ACL injury compared to noninjured subjects.

4. Conclusions An ACL injury causes changes in neuromuscular function. Several studies show persistent weakness of the quadriceps and a reduction in functional performance, but others report that quadriceps strength and performance is restored. Strength of the hamstring muscles can be restored. Several studies report persistent impairment of proprioception or postural control, while few report normal values. The increase in knee joint laxity after an ACL injury does not correlate with functional outcome, indicating that the degree of anterior tibial translation does not reect the complexity of the injury or extremity function. A different movement and activation pattern in

the injured leg, such as a delayed muscle response, a change in muscle timing and recruitment order, an altered coordination pattern, and compensations by muscle groups other than the quadriceps have been found, compared to the uninjured leg or to a control group. Bilateral defects after a unilateral injury have been reported in proprioception, postural control, voluntary quadriceps muscle activation, and in functional performance, which stresses the importance of comparing patients with a control group to ensure detection of impairment. Feedback is essential in the process of relearning motor programs. Since the sensory feedback from the injured joint is persistently disturbed, the existing motor programs may need to be modied by regaining coordinated movements or learning new coordinated movement patterns. The development of rehabilitation programs is based on theoretical models and clinical experience. The aims of these programs are to restore joint motion, regain muscle strength and function to the preinjury level or a modied level of activity. CKC exercises are believed to be safer and more functional than OKC exercises. However, both CKC and OKC can be modied to minimize shear forces, and may be useful for simulating functional activities. Muscle coactivation maintains joint stability and aims at obtaining congruency of joint surfaces. A voluntary movement is preceded by anticipatory postural adjustment and produces postural reactions. These principles are used in functional training programs, aiming to obtain improvements in functional stability and neuromuscular function. Discomfort, warmth, swelling and functional instability show that a joint is being loaded beyond its physiologic capacity, which should be avoided throughout the rehabilitation period. The neuromuscular function may change with time from injury. Few studies specically evaluate the effects of rehabilitation on neuromuscular function after an ACL injury or reconstruction. Improvements in muscle strength and functional performance have been reported after various training programs, and at various follow-ups after the training period, with persistent effect at long-term follow-up. On the basis of present knowledge, it seems unlikely that complete recovery of neuromuscular function can be achieved after an ACL injury or reconstruction, although improvements are obtained during rehabilitation. However, the effects of rehabilitation on neuromuscular function need to be further studied, to improve the overall treatment after an ACL injury. References
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Eva Ageberg graduated from Lund University, Sweden in 1992. From 1994 she has worked at the Physical Medicine Unit, Department of Rehabilitation, Lund University Hospital. She has specialized in Physiotherapy in Orthopedics, and received her MSc in Physical Therapy in 1998. Her postgraduate studies at the Institute for Musculoskeletal Diseases, Department of Physical Therapy, Lund University, involve assessment of neuromuscular function, mainly postural control, and effects of rehabilitation in individuals with anterior cruciate ligament injury in the knee.