The Relationship of Lower Limb Muscle Strength and Knee Joint Hyperextension during the Stance Phase of Gait in Hemiparetic Stroke Patients

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1 RESEARCH ARTICLE The Relationship of Lower Limb Muscle Strength and Knee Joint Hyperextension during the Stance Phase of Gait in Hemiparetic Stroke Patients Allison Cooper 1 *, Ghalib Abdulllah Alghamdi 2, Mohammed Abdulrahman Alghamdi 2, Abdulrahman Altowaijri 2 & Susan Richardson 2 1 College of Human & Health Science, Swansea University, Swansea, UK 2 Department of Physiotherapy, School of Healthcare Studies, Cardiff University, Cardiff, UK Abstract Background and Purpose. Despite the finding that 40% to 60% of stroke patients suffer from knee joint hyperextension during gait, there is a lack of agreement of the possible causes of this problem. The aim of this study was to determine whether there is a relationship between lower limb muscle weakness and knee joint hyperextension in hemiparetic stroke patients. Methods. This is a cross-sectional observational comparison study. Twenty patients (mean age 66 years) who had suffered a single hemiparetic stroke and were ambulant with no major lower limb joint pathology participated. Muscle strength of the hip extensors, hip flexors, hip abductors, knee extensors, knee flexors, ankle plantarflexors and ankle dorsiflexors of both limbs was measured using a hand-held dynamometer. Computerized and visual gait analysis identified subjects with and without knee hyperextension in loading response and midstance. Subjects were categorized as having weakness of a particular muscle group if the difference in strength between the paretic and non-paretic muscle was greater than 50%. The Pearson s chi-squared test was used to evaluate the association between weakness and knee hyperextension. Results. A strong relationship was found between ankle plantarflexor weakness and knee hyperextension during midstance (p = 0.044). No relationship was found between lower limb muscle weakness and knee hyperextension during loading response (p > 0.05). No relationship was found between any other lower limb muscle groups and knee hyperextension in midstance (p > 0.05). Conclusions. Weak ankle plantarflexors, in particular gastrocnemius, may have an important role in the presence of knee hyperextension. The results of this study did not support a role for weak hamstrings or quadriceps in knee hyperextension during gait. Further research is needed to clarify the role of gastrocnemius during the stance phase and to determine if strengthening weak gastrocnemius reduces knee hyperextension. Copyright 2011 John Wiley & Sons, Ltd. Received 23 June 2011; Revised 5 October 2011; Accepted 16 October 2011 Keywords Stroke; Physiotherapy; Assessment *Correspondence Dr Allison Cooper, Swansea University, Room 309, Vivian Building, Singleton Park, Swansea, SA2 8PP. Allison.cooper@swansea.ac.uk Published online 7 December 2011 in Wiley Online Library (wileyonlinelibrary.com) DOI: /pri.528 Introduction To be able to walk independently is one of the primary goals of a rehabilitation programme for people who have suffered a stroke (Dodd and Morris, 2003). On regaining the ability to walk, patients often do so with abnormal walking patterns that are a result of the underlying neurological impairments and the compensatory strategies that they develop as they attempt to walk (Olney and Richards, 1996; Dodd and Morris, 150 Physiother. Res. Int. 17 (2012) John Wiley & Sons, Ltd.

2 A. Cooper et al. Hyperextension and Weakness during Stroke Gait 2003). Abnormal walking patterns are undesirable as they reduce the ability to balance, increase energy expenditure and can lead to deformity and muscle wasting (Edwards, 2002). The challenge for physiotherapists is to determine the causes of an individual patient s abnormal walking pattern to provide the most appropriate and effective treatment. Knee hyperextension is a common kinematic problem in the gait of people with hemiplegic stroke (Knutsson and Richards, 1979; Lehmann et al., 1987; Pinzur et al., 1987; Morris et al., 1991). Knee hyperextension is defined as extension of the affected knee beyond the neutral anatomical position during the stance phase of gait, instead of the normal flexion of the knee joint that is important for shock absorption (Morris et al., 1991). It may be rapid and abrupt or occur slowly, and the degree of hyperextension depends on the mobility of the knee (Perry, 1992). Knee hyperextension may be advantageous in providing a mechanism to control an otherwise unstable limb during the stance period of the gait cycle. However, the concern is that hyperextension may place the capsular and ligamentous structures of the posterior aspect of the knee at risk of injury. Injury to these tissues can cause pain, ligamentous laxity or bony deformity. Such problems may lead to functional gait deficits and require management with expensive aids and orthoses, or surgery may even become necessary (Morris et al., 1991). Studies have shown that the peak angle of knee hyperextension can be as high as 22 degrees in stroke patients (Knutsson and Richards, 1979; Hogue and McCandless, 1983). Despite the finding that 40% to 60% of stroke patients suffer from knee hyperextension (Knutsson and Richards, 1979; Chin et al., 1982), there is a current lack of agreement of the possible causes of this problem. Lower limb muscle weakness, particularly quadriceps, hamstring and gastrocnemius muscle weakness, has been suggested as a possible cause (Moseley et al., 1993). This is inferred from knowledge of normal kinematics and gait control rather than extensive investigation of the gait patterns of stroke patients. In a previous study, patients with knee hyperextension were more likely to have hamstring muscle weakness than those without knee hyperextension and no relationship of knee hyperextension with quadriceps, or gastrocnemius muscle weakness was found in the patients studied (Cooper, 2006). Further research is needed to specifically investigate the relationship between knee hyperextension and lower limb muscle weakness in a further group of stroke patients. The aim of this study therefore was to determine whether a relationship exists between muscle weakness of the lower limb and knee hyperextension in hemiparetic stroke patients. It was decided to extend the definition of knee hyperextension to include patients whose knee showed an abnormal extension pattern during stance rather than only patients whose knee extended beyond the neutral anatomical position. The degree of knee extensionseeninpatientsisdependentonthepassive structures on the posterior aspect of the knee that is, muscles, joint capsule and ligaments. Actual genu recurvatum or knee hyperextension frequently occurs later post-stroke because of progressive stretching of these posterior structures. The term hyperextension therefore, for the purposes of this study, indicates the presence of an abnormal extension pattern following initial contact rather than the normal knee flexion pattern that should occur. Methods Subjects Twenty patients with hemiparesis following stroke were recruited from the rehabilitation wards and outpatient rehabilitation units of a large National Health Service Wales Trust. All fulfilled the following inclusion criteria: hemiparesis due to a unilateral single clinical stroke, no major lower limb joint pathology (such as joint replacements or rheumatoid arthritis), able to walk independently with or without a walking aid and able to give informed consent. The local research ethics committee approved the study, and all participants gave their informed consent. Procedure Muscle strength of both the paretic and non-paretic limbs was measured with a hand-held dynamometer (Commander PowerTrak II, JTech Medical; Salt Lake, Utah, USA) using a standard protocol and testing positions (Table 1). Hip extension, hip flexion, knee extension, knee flexion, ankle dorsiflexion and ankle plantarflexion strength were recorded. Each subject was required to perform three maximum voluntary isometric contractions for each requested test movement. Subjects were instructed to build the force up over 2 seconds and then hold that maximum Physiother. Res. Int. 17 (2012) John Wiley & Sons, Ltd. 151

3 Hyperextension and Weakness during Stroke Gait A. Cooper et al. Table 1. Positions for muscle groups tested (Bohannon, 1990) Muscle group Patient position Limb positions Manually stablized body part Dynamometer placement Hip extensors Supine Hip flexed to 90, knee relaxed Trunk Just proximal to the knee on flexor surface of thigh Hip flexors Supine Hip flexed to 90, knee relaxed Trunk Just proximal to the knee on extensor surface of thigh Knee Sitting Hip and knee flexed to 90 Thigh Just proximal to ankle on anterior surface of leg extensors Knee flexors Sitting Hip and knee flexed to 90 Thigh Just proximal to ankle on posterior surface of leg Ankle dorsiflexors Supine Hip and knee extended Lower limb proximal to ankle Just proximal to metatarsophalangeal joints on dorsal surface of foot Ankle plantarflexors Supine Hip and knee extended Lower limb proximal to ankle Just proximal to metatarsophalangeal joints on plantar surface of foot contraction for another 3 seconds. The average of the maximum level of force for each contraction was used for all analyses. Acceptable reliability of the hand-held dynamometer has been established, reporting interclass correlation coefficients of in a single session for lower limb muscles (Riddle et al., 1989). Three reflective markers were placed on the subject s paretic leg by following the strength testing: on the lower end of the fibula over the lateral malleolus, over the lateral femoral epicondyle of the femur and over the greater trochanter of the femur. The subject walked along a 10-m walkway at their self-selected speed, while a video camera, on a tripod perpendicular to the walkway on the subject s paretic side at the level of their knee, recorded their gait pattern. The video was imported into computerized movement analysis software (Siliconcoach Ltd, Dunedin, New Zealand) and pelvic, hip, knee and ankle angles at initial contact and loading response, and midstance were measured using this software. Only one previous study has reported on the reliability of using Siliconcoach (Cronin et al., 2006); therefore, an intrarater reliability study was also undertaken, which found intraclass correlation coefficients of 0.83 for initial contact, 0.89 for loading response and 0.93 for midstance for the knee joint. Knee angle at initial contact was measured when the heel of the foot on the affected side touched the ground, while the knee angle at loading response was measured when the paretic foot was flat on the ground and the non-paretic leg was in the pre-swing phase. The knee angle at midstance was measured when the foot of the paretic leg was completely flat on the ground and the non-paretic leg had moved exactly behind the affected side in midswing phase. A visual gait analysis was also undertaken of all subjects to confirm the presence or absence of an abnormal knee extension pattern. Data analysis For each muscle group, the average strength of the paretic limb was expressed as a percentage of the average strength of the non-paretic limb. Subjects were categorized as having weakness of a particular muscle group if the difference in strength between the paretic and non-paretic muscle was greater than 50%. This threshold was based on previous work examining muscle strength differences between the two limbs of healthy adults (Cooper, 2006). Subjects were categorized as having knee hyperextension during loading response and/or midstance by examining the knee extension angles at initial contact, loading response and midstance. Knee hyperextension was identified if the knee did not show the usual flexion pattern after initial contact (see Table 2). A visual gait analysis was used in addition to the joint angle measures to confirm the hyperextension as the joint angle measures alone did not identify some subjects with obvious excessive knee extension during midstance. A2 2 contingency table for each muscle was completed and a chi-squared test was used to evaluate the association between each muscle strength measure and the dependent variable (knee hyperextension). Fisher s Exact Test was used when the data did not meet the requirements of the chi-squared test. The Statistical Package for Social Sciences for Windows (version 15.0, SPSS Inc, Chicago, IL) statistical software 152 Physiother. Res. Int. 17 (2012) John Wiley & Sons, Ltd.

4 A. Cooper et al. Hyperextension and Weakness during Stroke Gait Table 2. Subject characteristics Subject Age Gender Months since stroke Knee hyperextension Muscle weakness Knee joint angles LR MS ADF APF KE KF HE HF HA IC LR MS 1 58 M F F M M M F M M M M F M M M F M F F M IC = initial contact; LR = loading response; MS = midstance; ADF = ankle dorsiflexors; APF = ankle plantarflexors; KE = knee extensors; KF = knee flexors; HE = hip extensors; HF = hip flexors; HA = hip abductors; + = present; - = absent. was used for all statistical analyses. Significance level was set at a level of Results All 20 stroke patients completed the evaluation (see Table 2). There were 13 male and 7 female subjects. Nine subjects had a right-sided hemiparesis, while 11 had a left sided hemiparesis. The mean (SD) age of the subjects was 66 years (11.1). The median time since stroke was 10 months (range from 1 to 47 months). All subjects were able to achieve plantigrade at the ankle passively and also make initial contact with the heel of the affected leg during gait. All subjects walked independently without the assistance of a walking aid during the gait recordings. Thirteen subjects (65%) had knee hyperextension during the loading response and/or midstance phases of gait (see Table 2). Nine subjects (45%) had knee hyperextension during loading response, which persisted through to midstance. The remaining four subjects (20%) presented with knee hyperextension as they progressed to midstance. Of the subjects who had no knee hyperextension during stance, only three had any significant lower limb muscle weakness. Lower limb muscle weakness was common where there was knee hyperextension during stance (see Table 3). However, the only significant association found was between ankle plantarflexor weakness and knee hyperextension during midstance (p = Fisher s Exact Test, contingency coefficient = 0.016). The findings also suggest an association between ankle dorsiflexion weakness and knee hyperextension; however, this did not achieve significance (p = 0.051). Knee joint hyperextension in midstance was not related to weakness in any other lower limb muscle groups. No significant relationships were found between weakness of any of the lower limb muscle groups and knee joint hyperextension during loading response. Discussion This study explored the relationship between lower limb muscle weakness and the presence of knee joint hyperextension during the stance phase of gait in a Physiother. Res. Int. 17 (2012) John Wiley & Sons, Ltd. 153

5 Hyperextension and Weakness during Stroke Gait A. Cooper et al. Table 3. Relationship between muscle group weakness and knee hyperextension during loading response and midstance Loading response knee hyperextension Midstance knee hyperextension Muscle group weakness Absent n (%) Present n (%) Association (FET) Absent n (%) Present n (%) Association (FET) Ankle dorsiflexors Weak 1 (5%) 5 (25%) p = (0%) 6 (30%) p = No weakness 10 (50%) 4 (20%) 7 (35%) 7 (35%) Ankle plantarflexors Weak 2 (10%) 5 (25%) p = (0%) 7 (35%) p = No weakness 9 (45%) 4 (20%) 7 (35%) 6 (30%) Knee extensors Weak 1 (5%) 2 (10%) p = (0%) 3 (15%) p = No weakness 10 (50%) 7 (35%) 7 (35%) 10 (50%) Knee flexors Weak 2 (10%) 5 (25%) p = (5%) 6 (30%) p = No weakness 9 (45%) 4 (20%) 6 (30%) 7 (35%) Hip extensors Weak 1 (5%) 4 (20%) p = (0%) 5 (25%) p = No weakness 10 (50%) 5 (25%) 7 (35%) 8 (40%) Hip flexors Weak 1 (5%) 3 (15%) p = (0%) 4 (20%) p = No weakness 10 (50%) 6 (30%) 7 (35%) 9 (45%) Hip abductors Weak 1 (5%) 4 (20%) p = (0%) 5 (25%) p = 114 No weakness 10 (50%) 5 (25%) 7 (35%) 8 (40%) FET = Fisher s Exact Test. group of ambulant stroke patients. A relationship was found between ankle plantarflexor weakness and knee joint hyperextension during the midstance phase of gait. The gastrocnemius muscle produces knee flexor activity during midstance that acts to prevent knee hyperextension, so weakness of this muscle could allow the knee to hyperextend in midstance (Moseley et al., 1993). It is also suggested that shortening of the ankle plantarflexors could limit dorsiflexion range, which could impair movement of the tibia over the foot during loading response and midstance; however, all subjects were able to achieve plantigrade, so this was unlikely to be a contributing factor in this study. It has been suggested previously that knee hyperextension during stance could occur as a compensation for an inability to produce adequate knee extensor activity during stance; the knee hyperextends to prevent collapse of the knee during single leg stance (Moseley et al., 1993). These results, however, do not support a relationship between weakness of knee extensor muscles and knee hyperextension during stance in the stroke patients studied. These findings also do not support a relationship between hamstring weakness and knee hyperextension, as found previously by Cooper (2006). However, a different muscle strength testing protocol was used (load cell and muscle testing chair rather than a hand-held dynamometer) and almost three quarters of the subjects in the Cooper (2006) study had ankle plantarflexor contracture, and these factors could account for the differences in findings. Ankle dorsiflexor weakness was close to having a significant association with knee hyperextension (p = 0.051). The ankle dorsiflexors are active during early stance to control the loading response and lowering of the foot to the floor. The loss of control that would occur with weakness of this muscle together with the fact that all but one subject with ankle dorsiflexor weakness also had ankle plantarflexor weakness, may account for this finding. The limitations of this study are determined by the number of cases investigated (n = 20). This meant that the groups of subjects for comparison with and without knee hyperextension were small (n = 13 and n = 7, respectively); therefore, the possibility of a type II error means that the findings should be viewed with caution. This study was aiming for a sample size of 48, but because of problems with time and the recruitment process, only 20 subjects were recruited. The study was therefore under-powered. Additionally, this study 154 Physiother. Res. Int. 17 (2012) John Wiley & Sons, Ltd.

6 A. Cooper et al. Hyperextension and Weakness during Stroke Gait focused on lower limb muscle weakness and the presence of spasticity or changes in muscle activation patterns were not measured. Subjects may have had increased stretch response activity or altered muscle activation patterns during gait that could have contributed to their knee hyperextension. The method of using joint angles generated through the use of computerized video gait analysis software reliably identified subjects with knee hyperextension during loading response. This method, however, missed four subjects where the knee hyperextension occurred in midstance. Observation of the video recordings of these subjects identified abnormal extension of the knee joint during this phase. Further work is needed to develop this method so that it can reliably identify knee hyperextension through all phases of stance. This may require repeated measures through stance or the integration of kinematic data with kinetic measures such as the ground reaction force vector. This study included a wide range of stroke patients in terms of age, time since stroke and walking ability using broad inclusion criteria, and as such, it is likely that the group were representative of stroke patients seen in a rehabilitation unit. Sixty-five per cent of the study subjects had knee hyperextension indicating how common this gait problem is amongst ambulant stroke patients. Greater understanding of the relationship of gastrocnemius weakness with knee hyperextension during stance is needed by further studies of a larger number of stroke patients with this gait problem. The use of electromyography during the gait cycle to measure gastrocnemius activation may give further insight into the muscle s role. A study to measure the effect of gastrocnemius strengthening on the degree of knee hyperextension may also further test the relationship. Implications for practice and research The findings from this study with a limited sample suggest that there may be a relationship between ankle plantarflexor muscle weakness and knee joint hyperextension during the stance phase of gait following stroke. Physiotherapists should consider the activity and function of this muscle when treating stroke patients with this gait problem in clinical practice. Further research is needed to support this relationship and to determine effective interventions to manage knee joint hyperextension. Acknowledgements This research was supported by a grant to Dr Cooper by Gwent Healthcare NHS Trust. Dr Cooper s post was jointly funded by the Wales Office of Research and Development (WORD) and The Stroke Association at the time of this study. The project was completed in partial fulfillment of Mr G.A. Alghamdi, Mr M.A. Alghamdi and Mr A. Altowaijri s Master of Science degree. The authors would like to thank the patients and physiotherapy staff for their time and support of this project, to Dr M Busse for the development of the study and to Dr Robert van Deursen and Dr Sarah Curran for commenting on drafts of the paper. REFERENCES Bohannon RW. Muscle strength testing with handheld dynamometry. In: Amundsen L (ed.), Muscle Strength Testing: Instrumented and Non-instrumented Systems. New York: Churchill Livingstone Inc, 1990; p Chin PL, Rosie A, Irving M, Smith R. Studies in hemiplegic gait. In: Rose FC (ed.), Advances in Stroke Therapy. New York: Raven Press, Cooper A. PhD thesis: The relationship of hemiparetic gait patterns to underlying neurological impairment and its relevance to physiotherapeutic intervention. Department of Physiotherapy, Cardiff University, Cronin J, Nash M, Whatman C. Assessing dynamic knee joint range of motion using siliconcoach. Physical Therapy in Sport 2006; 7(4): Dodd KJ, Morris ME. Lateral pelvic displacement during gait: abnormalities after stroke and changes during the first month of rehabilitation. Archives of Physical Medicine and Rehabilitation 2003; 84(8): Edwards S. An analysis of normal movement as the basis for the development of treatment techniques. In: Edwards S (ed.), Neurological Physiotherapy. London: Churchill Livingstone, Hogue RE, McCandless S. Genu recurvatum: auditory biofeedback treatment for adult patients with stroke or head injuries. Archives of Physical Medicine and Rehabilitation 1983; 64(8): Knutsson E, Richards C. Different types of disturbed motor control in gait of hemiparetic patients. Brain 1979; 102(2): Lehmann JF, Condon SM, Price R. delateur BJ. Gait abnormalities in hemiplegia: their correction by anklefoot orthoses. Archives of Physical Medicine and Rehabilitation 1987; 68(11): Physiother. Res. Int. 17 (2012) John Wiley & Sons, Ltd. 155

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