- Email: [email protected]
Strength and voluntary activation of the quadriceps femoris muscle at different severities of osteoarthritic knee joint damage
ELSEVIER
Journal of Orthopaedic Research
Journal of Orthopaedic Research 22 (2004) 96-103
www.elsevier.com/locate/orthres
Strength and voluntary activation of the quadriceps femoris muscle at different severities of osteoarthritic knee joint damage Geza Pap *, Andreas Machner, Friedemann Awiszus Neurornusculur Reseurcli Group, Department of Orthopaedrcs, Otto-ron-Guericke University, Leip:lger Street 44, 0-39120 Mugdeburg. Germany Received 19 June 2002; accepted 12 May 2003
Abstract Objective: Improvements of quadriceps motor deficits represent a major therapeutical target in knee osteoarthritis (OA). In the present study, we investigated changes in quadriceps function at different stages of osteoarthritic cartilage damage. A4ethod.s: Measurements of quadriceps voluntary activation (VA) and maximum voluntary contraction (MVC) were performed by a twitch interpolation technique and the total muscular capacity (TMC) was calculated as the ratio of MVC and VA. We assessed 68 patients (56.7 2 9.5 years) with stage I1 and 154 patients (65.6 k 6.0 years) with stage IV chondropathy. As controls, we used 85 age related healthy subjects (58.1 f 8.7 years). Results: While T M C was significantly lower in stage IV (90.6 f 43.7 N rn) than in stage I1 chondropathy (109.6 k 51 .O) there were no differences in the MVCs between both groups. Quadriceps VA was even higher in stage IV (77.2k 13.2%) than in stage I 1 chondropathy (70.8 t 16.0'%). In the controls, MVC, VA and T M C were significantly higher than in both OA groups. Conclusion: We assume that a decrease of T M C might occur within the course of OA and, in consequence, VA increases to maintain quadriceps MVC. 0 2003 Orthopaedic Research Society. Published by Elsevier Ltd. All rights reserved. Keywards: Osteoarthritis; Knee; Cartilage damage; Quadriceps muscle; Voluntary activation; Maximum voluntary contraction
Introduction Osteoarthritis (OA) of the knee is a painful and disabling disease [25]. The joint damage in O A is characterised by progressive loss of articular cartilage [ 101 with the development of cartilage surface defects of different extent [6,32]. In patients with knee OA, quadriceps weakness is a clinical feature that has been described several times before [13,14,36]. It is considered to be an important determinant of disability [25] and should, to a great extent, be due to arthrogenous muscle inhibition (AMI), i.e. an arthrogenous decline in muscle activation [ 13,16, 361. This arthrogenous decline in quadriceps muscle activation is attributed to altered afferent input from the diseased, damaged joint and consequent reduction in efferent motor neuron output to the quadriceps [35]. Thus, AM1 leads to both reduced voluntary activation
*Corresponding author. Tel.: +49-391-67-14035; fax: +49-391-6714006. E-n7rril urldress: [email protected] (G. Pap).
(VA) and maximum voluntary contraction (MVC) in osteoarthritic knees [ 16,201. Several recent studies stress the role of AM1 in OA of the knee, since it is not only considered to be a consequence of OA but even more importantly a risk factor for the initiation and the progression of damage to articular cartilage and other tissues in osteoarthritic knees [20,27,36]. Notably, Hurley and co-workers could demonstrate recently that in osteoarthritic knees AM1 can be reduced by a relatively brief physiotherapeutical exercise regime leading to significant improvement of quadriceps motor and sensory function and consequently to reduced disability in these patients [19]. This is in concordance with other studies reporting on reduction of disability in knee O A by muscle strengthening exercises [ 191. These encouraging reports, however, raise one major question: How does quadriceps motor function change with increasing osteoarthritic knee joint damage? As altered afferent inputs from damaged joints are made responsible for the reduction of quadriceps strength and VA in knee OA, one should suppose that with increasing severity of joint damage there is also an increase in alteration of afferent inputs and subsequently
0736-0266/$ - see front matter 0 2003 Orthopaedic Research Society. Published by Elsevier Ltd. All rights reserved doi: l0.10l6/SO736-0266(03)00128-1
G Pup e f ul. I Journal
of Orthopurdic
a decrease in quadriceps strength and VA. Answering this above question should be of particular importance for determining the optimal time in the onset of treatment in patients with knee OA. However, recent studies on muscle weakness and OA were just comparing OA patients and healthy controls without regard to differences in the severity of OA [13,20,36]. Moreover, in the studies investigating the influence of physiotherapeutical exercises of quadriceps motor function obviously only patients with relatively early stages of knee OA were included [19]. Therefore, in the present study we investigated quadriceps motor function at two distinctly different stages of osteoarthritic knee joint destruction.
Methods Putients
At our department, measurements of quadriceps strength and activation were performed in a total of 367 patients designated for knee surgery for primary OA of the knee. In the present study, we investigated 223 of these patients. The patients were selected retrospectively using the following inclusion criteria: clinical and radioiogicai signs of O A of the knee according to the ACR criteria [2]; intraoperatively visible cartilage damage: either grade I1 damage of the medial femoral and tibial condyle according to Outerbridge [301 but without damage of the lateral compartment or grade IV damage of both the medial and the lateral femoral and tibial condyle according to Outerbridge [30]; operative procedures: either arthroscopy and high tibial osteotomy or knee arthroplasty. According to the intraoperatively visible cartilage damage, patients were retrospectively divided into two groups. Group I included 68 patients with grade I1 damage of the medial femoral and tibial condyle according to Outerbridge [30]but without damage of' the lateral compartment. These patients of group I were designated to be treated by high tibial osteotomy for medial coinpartment knee OA. Prior to the high tibial osteotomy, all of these patients had undergone knee arthroscopy for assessment of the extent of the cartilage damage. Group I1 consisted of 154 patients who showed varus deformity of the same extent as those in group I but had grade I V damage of both the medial and the lateral femoral and tibial condyle according to Outerbridge [30]. Patients of group 11 were designated for bicondylar knee arthroplasty.
Rewrirch 22 (2004) Y6-1113
97
As controls. we used a group of 85 age related subjects who were staff members of our department or their relatives. According t o the criteria of the ACR [2], none of the controls had clinical signs of knee OA. Also, there was no evidence for any other knee damage in either knee in these subjects. and none of them had a history of significant knee trauma. Subjects with lower-extremity-joint replacements, with neuromuscular disorders, or with any other intercurrent illness were excluded from this study. None of the tested subjects showed significant atrophy of the quadriceps muscle of either leg with differences in thigh circumference of more than 1 cm as compared to the contralateral side. This, however. does not necessarily exclude bilateral quadriceps atrophy. At clinical examination, none of the patients had palpabk knee effusions and there were no signs of knee instability. As the contralateral knees of the OA patients of both groups showed osteoarthritic changes ranging between stage I and 111 according to Kellgren and Lawrence [22], they were excluded from the assessments. Demographic data of the OA patients and the controls included in this study are given in Table I . For pain assessment, we used the pain score of an evaluated German version of the WOMAC with a possible range of 0-10 for each of the five questions [38]. In addition, patients were asked to give the duration of knee symptoms in months. According to the duration of symptoms. OA patients were divided into three groups: patients with short-term duration (< 12 months), patients with medium-term duration (12 60 months), patients with long-term duration (>60 months) (Table 2). All experimental procedures were approved by the local ethics committee. and all subjects gave informed consent to the testing procedure. Assessnirnt of srrengtli, V A ~ i n dtrue niusculur cupucifj ( T M C ) qf' the quudricrps niiiscle
Quadriceps strength was assessed during an isometric MVC o n a purpose built chair [4,23,24,43]. The quantification of the maximal voluntary muscle activation (VA) is based on the principle that if the muscle fibres of a muscle can not be fully recruited during a maximal VA, additional force is generated by superimposed electrical muscle stimulation (twitch) [4, I 1.231. Providing over 25% of the MVC, the additional force generated by superimposing electrical stimulation is known t o have a linear relationship to the voluntarily elicited initial force [4,11.29]. The linearity is used to extrapolate the twitch amplitude at 0% MVC ('resting' muscle). Then the VA of the muscle is calculated as:
['"'
1 - twitch amplitude at MVC [N m] x IOO'X~ estimated twitch amplitude at resting muscle [Nnil
Extrapolation of the resting muscle twitch amplitude instead of direct measurement was done as twitches below 25% of MVC have been shown to have an odd relationship to the initial torque [11.29]. Knowing the MVC and the VA, the extension torque was calculated corresponding to 100'%1muscle activation. representing the T M C of the quadriceps muscle: TMC [Nm]=
maximal voluntary contraction [Nm] x voluntary activation ['XI]
loo'%,
Table 1 Demographic data and grouping of the subjects investigated OA patients chondropathy stage 11 Number of subjects Mean age ( f S D ) Gender (malelfemale) Mean height (kSD) Mean weight (+SD) Mean duration of knee symptoms (+SD) Mean WOMAC Pain score ( f S D )
OA patients chondropathy stage IV
Controls
68
154
56.7 years (k9.5) 40'1/;,/600/;1 164 cm ( i 8 . 7 ) 74 kg (f9.4) 34 months (215) 5.2 (f1.6)
65.6 years (f6.0)
85 58.1 years (f8.7)
41'%1/590/;1
36'%J64'%1
166 cm (f7.2) 76 kg (f11.9) 51 months ( f 1 3 ) 5.5 (k1.7)
173 cm (1-6.8) 75 kg (k9.7) 0
G Pap et ul I Journul of Orthopuedic R e x u r t h 22 (2004) 96-103
98
Table 2 MVC and VA according to the symptom duration
MVC (mean f SD) VA (mean k SD)
Symptom duration < I 2 month ( n = 31)
Symptom duration 12-60 months ( n = 89)
Symptom duration 260 months (n = 102)
80.7 k 40.7 N m 80.9 f 10.3'%1
72.8 k 33.5 N m 74.7 f 13.4%
76.9 38.3 N m 77.7 k 13.6%
Experimental procedure Assessment of MVC and VA was done as described previously [8,23.24,43]. For measurements of MVC and VA, all subjects were seated in an upright position on a purpose-built chair with their hips and knees flexed to 90". The lower legs were fixed to the lever arm of a force-measuring device based on an analogue strain gauge using a noiiextensible leather strap. For electrical muscle stimulation, aluminium plate electrodes of 5 x 10 cm. covered with thin, saline-soaked sponges for better skin contact, were strapped to the middle of the quadriceps muscle (cathode) and to the distal quadriceps muscle 10 cm above the patella (anode). Electrical stimulation of the quadriceps muscle was done using a constant current stimulator (Dantec Counterpoint MK 11) applying single, square-wave stimuli with 100 mA amplitude and 500 11s duration. Self-written software was used for data acquisition and for highly sensitive. automated twitch detection as described by Hales and Gandevia [15]. The sensitivity and reliability of this method had been investigated before [1,1 I]. First, subjects were instructed under intense encouragement to fully extend their knee ( 5 s ) for determination of the MVC and for maximum potentiation of the twitch response [41]. Immediately after twitch potentiation. the subjects performed isometric contractions with 90'%1. 75'%),50'%).25% and 100% of their MVC by matching the visualised torque level to the liiie on the monitor of the desired torque level. When the torque was kept stable three single stimuli were applied to the muscle generating additional force (twitch). During the testing procedure, none of the subjects reported on pain or pain dependent limitation in performing the tests in either knee. On the day of testing. none of the subjects had taken analgesics, muscle relaxants o r psychotropic agents. Tests were performed between 11 am and 3 pm in all patients. In both groups of OA patients, the experimental procedure included testing of the most affected knees that were designated for knee
Y
2I /I
operation one day before the very procedure. In the controls both knees were tested. All subjects were tested by one single, experienced technician, who has done this kind of testing procedure within different studies [4,8,23,24,42,43]. Sfufi.sticu1rmulysis The results are demonstrated as cumulative distribution function. To construct this function, the data points were sorted in ascending order and the function jumps vertically by the reciprocal of the number of data points when scanning the ordered points from left to right. This function allows to visualise the data points without the necessity for the arbitrary choice of a smoothening parameter that is necessary to construct a histogram [ 3 ] . In calculating the cumulative distribution functions, there was no adjustment for age, gender o r BMI of the subjects. In addition, results are given as means and standard deviations. Non-parametric Kolmogorow-Smirnow test was performed to compare MVCs, VAs and TMCs of osteoarthritic and control knees. The level of statistical significance was set to a p-value of p < 0.05.
Results
Fig. 1 shows the cumulative distribution function of the maximum MVCs in the two groups of OA patients and in the controls. It can be seen that in the control knees, MVC values are significantly higher (1 26.8 k 47.3, range 44.1-279 N m ) as compared to both the patients
I
-
c
I
0
. _ -
I
0
50
*
I
I00
I 50 MVC J N m l
, 200
,
250
I
300
Fig. I . Cumulative distribution function of the MVC of the quadriceps femoris muscle. Continuous-line: Group I , OA patients with grade IV chondropathy; dashed-line: Group 11, OA patients with grade 11 chondropathy; dashed-dot-line: controls, without knee joint damage.
G. Pup
0
(If
10
nl. I Journtrl of Ortliopuetlic Resrrircli 22 (2004) 96 103
20
30
40 50 60 voluntarq activation [%]
70
RO
90
99
100
Fig. 2. Cumulative distribution function of the VA of the quadriceps femoris muscle. Continuous-line: Group I, OA patients with grade IV chondropathy; dashed-line: Group 11, OA patients with grade 11 chondropathy; dashed-dot-line: controls, without knee joint damage.
with stage I1 chondropathy (75.9 k41.7, range 15.7216.1 N m ) and to the patients with stage IV chondropathy (70.3 36.9, range 13.0-290.9 N m ) (p < 0.001 for both OA groups). In contrast, cumulative distribution functions of the MVCs in patients with stage I1 and stage IV chondropathy were comparable, with no significant differences between these two groups of OA patients (p = 0.635). Evaluation of the cumulative distribution functions of quadriceps muscle VA revealed different results (Fig. 2). In the control knees, the VA values were significantly higher VA (89.3k8.0, range 55.4-98'1/0) than in both groups of OA patients 0, < 0.001). Surprisingly, in knees with chondropathy stage IV, however, VA values were significantly higher (77.2 13.2, range 37.5-97.5'56) than in knees with stage I1 chondropathy (70.8k 16.0, range 4.5-97.3'%1) (p = 0.004). Fig. 3 shows the cumulative distribution function of the total muscular capacities (TMCs) in OA patients and in the controls. Again, TMC values of the control knees were significantly higher (141.8 k 50.6, range 56.9-293.4 N m) than in both groups of OA patients (p < 0.001). In contrast to the above findings with MVC and VA, measurements yielded significantly lower TMCs in stage IV chondropathy (90.6k43.7, range 19.8-331.1 N m ) than in the knees with chondropathy stage I1 (109.6 51.O, range 37.2-352.1 N m) (p = 0.026). Analysis of symptom duration revealed significantly shorter knee symptoms in patients with chondropathy stage I1 (mean k SD: 50.8 k 43.4 months) than in patients with chondropathy stage IV (mean ? SD: 97.5 85.3 months) (p = 0.001). In contrast, there was no
*
*
* *
difference in both the MVC and the VA between patients with short-term, medium-term and long-term symptom duration, although in patients with short-term symptom duration both parameters were slightly higher as compared to patients with middle and long-term duration of symptoms (Table 2).
Discussion In the present study, we determined quadriceps muscle function at different severities of osteoarthritic cartilage damage. The assessment of osteoarthritic knee damage was performed on the basis of visualisation of the joint surface which has been estimated the golden standard for the classification of cartilage destruction in knee OA by different authors [5,9] especially because it is considered to be more sensitive than other methods of evaluating joint surface integrity as e.g. plain radiographs, computerised tomography and magnetic resonance imaging [6,9,12]. Thus, in the present investigation, evaluation of the extent of osteoarthritic joint damage and subsequent grouping of the patients according to the visible severity of cartilage destruction is probably more exact than in previous studies in which radiographs were used to asses the severity of joint damage [14,36,40]. However, it has to be considered that the patients with Outerbridge grade 11 or Outerbridge grade IV changes represent a specific subset of OA patients and are not necessarily representative of those with mild or severe OA as a whole. Therefore, our observations concerning MVC and VA changes refer only to
100
G. Pop et al. I Journcrl
of
Orrlicipaedic Rrsearcll 22 (2004) 96-103
Fig. 3. Cumulative distribution function of the TMC of the quadriceps femoris muscle. Continuous-line: Group I. OA patients with grade 1V chondropathy; dashed-line: Group 11, OA patients with grade 11 chondropathy: dashed-dot-line: controls, without knee joint damage.
differences in cartilage damage and not necessarily to differences in OA stages in general. Measurements of quadriceps activation by twitch superimposition technique, as used in this study, have been established by several groups for the evaluation of muscle function in different joints [4,20,35,43]. In particular, assessment of MVC and VA of the quadriceps muscle has been shown to be highly reliable and reproducible both in our hands [4,8,23,24,42,43] and in those of other groups (1). This good reproducibility has also been shown for subjects with OA by our group (8) [23,24]. The present study demonstrates that in comparison to healthy controls, patients with osteoarthritic cartilage damage are widely suffering from a significant loss of strength and VA of the quadriceps muscle. This is consistent with previous studies, reporting on quadriceps muscle weakness in knee OA [lo], although correlations between radiographic severity of OA and quadriceps strength have not been strong [20]. Previous studies describe quadriceps weakness in knee OA as characterised by both reduction of the MVC and the VA of the quadriceps muscle [20]. Hereby, the articular damage is supposed to stimulate articular mechanoreceptors-e.g. located in the joint capsule-evoking abnormal afferent information, which in turn decreases the excitability of 01motoneurons and thus leads to a reduced VA of the quadriceps [20]. Although there is much evidence for a complex inter-relationship between sensorimotor dysfunction of muscle, joint damage and disability [17], according to the theory of arthrogenous muscle inhibition in OA it seems to be rather likely that differences in the
extent of osteoarthritic cartilage damage should lead to differences in the abnormal afferent information and subsequently to differences in the extent of quadriceps muscle weakness and in the reduction of VA [37]. The results of the present study give strong support for this hypothesis showing that VA of the quadriceps muscle is significantly different not only between normal subjects and OA patients but also within the two groups of patients with different severities of osteoarthritic knee joint damage. However, the way VA differed between the two groups of OA patients was rather surprising. While in the control knees quadriceps VA was quite comparable to the values published for non-arthritic knees before [19,20], in the OA knees quadriceps VA did not decrease with increasing severity of osteoarthritic knee damage as one would have expected. Instead, quadriceps VA was significantly higher in knees with stage IV than in those with stage I1 cartilage damage and thus increasing with greater severity of knee OA. In addition, while-in concordance with literature-MVC in the control knees was significantly higher than in OA knees [20], comparison of quadriceps MVC between the two groups of OA patients revealed no differences. In other words, in the present study we did not find any signs of decreasing quadriceps strength with increasing severity of osteoarthritic cartilage damage. This is not necessarily in contrast to previous studies which found decreasing MVC being associated with greater disability in knee OA [20], since these studies did not assess the severity of osteoarthritic cartilage damage by evaluation of the joint surface itself but compared
G. Pup rf ul. I Journal of Orthopacdic Resc~tirch22 (2004) 96-103
different degrees of disability according to scoring systems [20] which do not necessarily correlate directly with the extent of joint damage [21,26]. In contrast to the findings with VA and MVC, the TMC showed a significant decline with increasing severity of osteoarthritic cartilage damage and was significantly inferior to that in the control knees. As the TMC:, as determined in the present study, is independent from the actual a-motoneuron activity, the decrease in TMC with greater cartilage damage reflects a loss in total strength of the entire quadriceps muscle with progression of this disease. Interestingly, despite this reduction of quadriceps TMC with progression of joint destruction, MVC was equal between the two different stages of cartilage damage. This is obviously due to the observed increase in VA of the quadriceps muscle in severe osteoarthritic joint destruction. As TMC is calculated as the ratio of MVC/VA, at lower TMC an increase in the VA is necessary to keep the MVC constant. In other words, the reduction of quadriceps TMC which takes place with progression of osteoarthritic joint damage might be compensated by an increase in the voluntarily achievable muscle activation, enabling patients with more severe forms of osteoarthritic joint damage to widely maintain quadriceps MVC as compared to patients with lesser extent of knee cartilage damage. The reasons for this phenomenon are not completely clear, yet. Since the mean age of the subjects both in the two OA groups and in the controls were slightly different, age dependent changes in quadriceps muscle function as described in previous studies [ 18,28,34] might contribute to our findings. However, as age dependent decline in quadriceps muscle strength has mostly been compared between young, middle-aged and elderly patients [ 18, 33,341, the extent to which ageing influences the changes of quadriceps muscle function in a subgroup of elderly patients with knee OA remains elusive. Moreover, as in the present study MVC remains unchanged and VA even increases with greater severity of osteoarthritic cartilage damage (and thus also with increasing age of the patients), ageing alone cannot be made responsible for the changes in quadriceps motor function observed here. This seems to be even more likely as in different studies no age dependent change of the quadriceps VA was found [18,31,33]. As in the present study only two distinct stages of chondropathy were compared, for final prove of a decline of TMC with increasing severity of OA cartilage damage (i.e. a proportional relationship) further studies including patients with different degrees of OA cartilage damage will be needed. As articular cartilage itself is aneural, arthrogenous decline in muscle activation cannot originate in cartilage but should be due to consequent changes of receptor-rich intra-articular structures such as the knee joint capsule. Characterisation of such capsular changes, e.g. by means of histological and ini-
101
munohistochemical examinations should be included in further studies to gain further insights into the contribution of this factor to the phenomenon of AMI. In addition, as cross-sectional studies like the present one have certain limitations, in these further studies longitudinal analyses will be necessary to confirm this hypothesis. Hereby, consideration of factors such as pain, duration of pain, BMI, activity limitation, joint alignment and the influence of pharmacologic agents etc. should be included to elucidate how the extent of visible cartilage damage relates to other signs and symptoms of OA and thus to disease severity as a whole. In particular, duration of symptoms seems to be a very important factor. It is well known that even terrible locking X-rays of knees can have very little symptoms. Therefore, a hyposthesis that is just as reasonable as articular damage being the source of inhibition would be the duration of symptoms. In the present study, patients with short-term duration of knee symptoms seemed to have a greater MVC and a higher VA than patients with middle and long-term symptom duration. This difference, however, was statistically not significant. This might be related to the fact that the present study did not primarily focus on this relationship. Thus, the parameter symptom duration was assessed only retrospectively on the basis of the patients reports at preoperative examination. In order to comprehensively investigate this interesting aspect, further studies will have to be conducted including standardized self assessment questionnaires capable of recording the parameter symptom duration more precisely. Moreover, there are some other possible confounding factors which might have influenced the results of this study. First, this concerns the contralateral knees of the OA patients in which radiographic signs of OA ranging between stage I and I11 according to Kellgren and Lawrence [22] were found. Although adjustment for this factor would have been rather useful, assessment of cartilage damage should be done with the same accuracy as for the involved knees. As visualisation of the cartilage of the contralateral knees was not possible, adjustment for the cartilage damage of these knee was not done in the present study, but should possibly be included in further studies. Second, although day to day variability and diurnal variation have been found to be rather low in normal subjects [8,23,24,42,43] it has to be considered that in patients with knee OA pain and functional impairment often increase as the day progresses. In order to minimise that possible variable, all patients were tested between 11 am and 3 pm, however, this parameter should be seen as a possible confounding factor. Third, it has to be considered that because all the testing was performed at 90" of knee flexion, results at other, functionally important, angles of knee flexion are unknown and could be very different from those presented here [7,39]. Also, in the present study the criterion
I02
G. Pup rt ul. I Journul of Orthopedic Rrsrurch 22 (2004) 96-103
for quadriceps atrophy was only a difference of more than 1 cm in the circumference of the two thighs. Therefore, more sophisticated methods for the measurement of muscle atrophy should be included in further studies to see in how far more distinct degrees of quadriceps atrophy affect the leg strength of OA patients. This is also important as differences in preoperative physical therapy and training to strengthen the quadriceps could certainly cause differences quadriceps MVC. Although rather difficult to exactly determine, in the present study there was no evidence that patients with advanced OA had more P.T. and training to strengthen the quadriceps than patients with mildmoderate OA. In conclusion, however, from the present study it seems that not MVC but TMC is the parameter of muscle function that decreases with greater severity of osteoarthritic knee joint destruction. Although speculative, we assume that a decrease of TMC might occur with increasing severity of osteoarthritic cartilage damage and, in consequence, VA increases to maintain quadriceps MVC. Further studies will have to prove this hypothesis and should study the role of other possible confounders such as symptom duration.
Acknowledgements This work was supported by Deutsche Forschungsgemeinschaft AW 512-2, AW 512-4 and NE 50514-2. The authors thank Brigitte von Specht for her technical assistance in performing the measurements. References [I] Allen GM, Gandevia SC, McKenzie DK. Reliability of measurements of muscle strength and voluntary activation using twitch interpolation. Muscle Nerve 1995;18:593400. [2] Altman R, Asch E, Bloch D, Bole G, Borenstein D, Brandt K, et al. Development of criteria for the classification and reporting of osteoarthritis. Classification of osteoarthritis of the knee. Diagnostic and Therapeutic Criteria Committee of the American Rheumatism Association. Arthritis Rheum 1986;29:103949. 131 Awiszus F. Spike train analysis. J Neurosci Meth 1997;74:155-66. [4] Awiszus F, Wahl B, Meinecke I. Influence of stimulus cross talk on results of the twitch-interpolation technique at the biceps brachii muscle. Muscle Nerve 1997;20:1187-90. [5] Ayral X . Diagnostic and quantitative arthroscopy: quantitative arthroscopy. Baillieres Clin Rheumatol 1996;10:477-94. [6] Ayral X, Gueguen A, Ike RW, Bonvarlet JP, Frizzier0 L, Kalunian K. et al. Inter-observer reliability of the arthroscopic quantification of chondropathy of the knee. Osteoarthr Cartilage 1998;6:160-6. [7] Becker R, Awiszus F. Physiological alterations of maximal voluntary quadriceps activation by changes of knee joint angle. Muscle Nerve 2001;24:667-72. [8] Berth A, Urbach D, Awiszus F. Improvement of voluntary quadriceps muscle activation after total knee replacement. Arch Phys Med Rehab 2002:10:1432.
[9] Blackburn-WD J, Bernreuter WK, Rominger M, Loose LL. Arthroscopic evaluation of knee articular cartilage: a comparison with plain radiographs and magnetic resonance imaging. J Rheumatol 1994;21:675-9. [lo] Brandt KD. Putting some muscle into osteoarthritis. Ann Intern Med 1997;127:154-6. [I 11 Bulow PM, Norregaard J, Mehlsen J, Danneskiold-Samsoe B. The twitch interpolation technique for study of fatigue of human quadriceps muscle. J Neurosci Meth 1995;62:103-9. [12] Fife RS, Brandt KD, Braunstein EM, Katz BP, Shelbourne KD, Kalasinski LA, et al. Relationship between arthroscopic evidence of cartilage damage and radiographic evidence of Joint space narrowing in early osteoarthritis of the knee. Arthritis Rheum 1991;34:377-82. [13] Fisher NM, Pendergast DR. Reduced muscle function in patients with osteoarthritis. Scand J Rehabil Med 1997;29:213-21. [I41 Fisher NM, White SC, Yack HJ, Smolinski RJ, Pendergast DR. Muscle function and gait in patients with knee osteoarthritis before and after muscle rehabilitation. Disabil Rehabil 1997; 19:47-5 5. [15] Hales JP, Gandevia SC. Assessment of maximal voluntary contraction with twitch interpolation: an instrument to measure twitch responses. J Neurosci Meth 1988;25:97-102. [I61 Hurley MV. Quadriceps weakness in osteoarthritis. Curr Opin Rheumatol 1998;10:246-50. [17] Hurley MV. The role of muscle weakness in the pathogenesis of osteoarthritis. Rheum Dis Clin North Am 1999;25:283-98. [IS] Hurley MV, Rees J, Newham DJ. Quadriceps function, proprioceptive acuity and functional performance in healthy young, middle-aged and elderly subjects. Age Ageing 1998;27:55-62. [I91 Hurley MV, Scott DL. Improvements in quadriceps sensorimotor function and disability of patients with knee osteoarthritis following a clinically practicable exercise regime. Br J Rheumatol 1998;37:1181-7. [20] Hurley MV, Scott DL, Rees J, Newham DJ. Sensorimotor changes and functional performance in patients with knee osteoarthritis. Ann Rheum Dis 1997;56:641-8. [21] Jewel1 FM, Watt I, Doherty M. Plain radiographic features of osteoarthritis. In: Brandt KD, Lohmander LS, Doherty M, editors. Osteoarthritis. Oxford, New York, Tokyo: Oxford University Press; 1998. p. 217-37. [22] Kellgren JH, Lawrence JS. Radiological assessment of osteoarhrosis. Ann Rheum Dis 1957;16:494-501. [23] Machner A, Pap G, Awiszus F. Evaluation of quadriceps strength and voluntary activation after unicompartmental arthroplasty for medial osteoarthritis of the knee. J Orthop Res 2002;20: 10811. [24] Machner A, Pap G, Krohn A, Rohkohl K, Awiszus F. Quadriceps muscle function after high tibia1 osteotomy for osteoarthritis of the knee. Clin Orthop 2002;399: 177-83. [25] McAlindon TE, Cooper C, Kirwan JR, Dieppe PA. Determinants of disability in osteoarthritis of the knee. Ann Rheum Dis 1993;52:258-62. [26] McAlindon TE, Wilson PW, Aliabadi P, Weissrnan B, Felson DT. Level of physical activity and the risk of radiographic and symptomatic knee osteoarthritis in the elderly: the Framingham study. Am J Med 1999;106:151-7. [27] Minor MA. Exercise in the treatment of osteoarthritis. Rheum Dis Clin North Am 1999;25:397415. [28] Murray MP, Duthie EH, Gambert SR, Sepic SB, Mollinger LA. Age related difference in knee muscle strength in normal women. J Gerontol 1985;40:280. [29] Norregaard J, Lykkegaard JJ, Bulow PM, Danneskiold-Samsoe B. The twitch interpolation technique for the estimation of true quadriceps muscle strength. Clin Physiol 1997;17:523-32. [30] Outerbridge RE. The ethiology of chondromalacia patellae. J Bone Joint Surg [Br] 1961;43-B:752-7.
G. Pup et ul. I Journal
of
Orthopuedic Reseurch 22 (2004) 96-103
[31] Phillips SK, Bruce SA, Newton D, Woledge RC. The weakness of old age is not due to failure of muscle activation. J Gerontol 1992;47:M45-9. [32] Pritzker KPH. Pathology of osteoarthritis. In: Brandt KD, Doherty M, Lohmander LS, editors. Osteoarthritis. Oxford, New York, Tokyo: Oxford University Press; 1998. p. 5&61. [33] Roos MR, Rice CL, Connelly D M , Vandervoort AA. Quadriceps muscle strength, contractile properties, and motor unit firing rates in young and old men. Muscle Nerve 1999;22:1094103. [34] Rutherford OM, Jones D. The relationship between muscle and bone loss and activity levels with age in women. Age Ageing 1992;21:286-93. [35] Rutherford OM, Jones DA, Newham DJ. Clinical and experimental application of the percutaneous twitch superimposition technique for the study of human muscle activation. J Neurol Neuro Surg Psychiat 1986;49:1288-91. [36] Slemenda C, Brandt KD, Heilman DK, Mazzuca S, Braunstein EM, Katz BP, et al. Quadriceps weakness and osteoarthritis of the knee. Ann Intern Med 1997;127:97-104. [37] Stokes M, Young A. The contribution of reflex inhibition to arthrogenous muscle weakness. Clin Sci 1984;67:7-14.
103
[38] Stucki G , Meier D, Stucki S, Michel BA, Tyndall AG, Dick W, et al. Evaluation of a German version of WOMAC (Western Ontario and McMaster Universities) Arthrosis Index. Z Rheuniato1 1996;55:40-9. [39] Suter E, Herzog W. Extent of muscle inhibition as a function of knee angle. J Electromyogr Kinesiol 1997;7: 123-30. [40] Tan J, Balci N, Sepici V, Gener FA. Isokinetic and isometric strength in osteoarthrosis of the knee. A comparative study with healthy women. Am J Phys Med Rehabil 1995:74:364 9. [41] Thomas CK, Johansson RS, Westling G , Bigland-Ritchie B. Twitch properties of human thenar motor units measured in response to intraneural motor-axon stimulation. J Neurophysiol 1990;64:133946. [42] Urbach D, Awiszus F. Effects of transcranial magnetic stimulation on results of the twitch interpolation technique. Muscle Nerve 2000;23:1125-8. [43] Urbach D, Nebelung W, Weiler H-T, Awiszus F. Bilateral deficit of voluntary quadriceps muscle activation after unilateral isolated rupture of the anterior cruciate ligament. Med Sci Sport Exer 1999;3 I :1691-6.
Journal of Orthopaedic Research
Journal of Orthopaedic Research 22 (2004) 96-103
www.elsevier.com/locate/orthres
Strength and voluntary activation of the quadriceps femoris muscle at different severities of osteoarthritic knee joint damage Geza Pap *, Andreas Machner, Friedemann Awiszus Neurornusculur Reseurcli Group, Department of Orthopaedrcs, Otto-ron-Guericke University, Leip:lger Street 44, 0-39120 Mugdeburg. Germany Received 19 June 2002; accepted 12 May 2003
Abstract Objective: Improvements of quadriceps motor deficits represent a major therapeutical target in knee osteoarthritis (OA). In the present study, we investigated changes in quadriceps function at different stages of osteoarthritic cartilage damage. A4ethod.s: Measurements of quadriceps voluntary activation (VA) and maximum voluntary contraction (MVC) were performed by a twitch interpolation technique and the total muscular capacity (TMC) was calculated as the ratio of MVC and VA. We assessed 68 patients (56.7 2 9.5 years) with stage I1 and 154 patients (65.6 k 6.0 years) with stage IV chondropathy. As controls, we used 85 age related healthy subjects (58.1 f 8.7 years). Results: While T M C was significantly lower in stage IV (90.6 f 43.7 N rn) than in stage I1 chondropathy (109.6 k 51 .O) there were no differences in the MVCs between both groups. Quadriceps VA was even higher in stage IV (77.2k 13.2%) than in stage I 1 chondropathy (70.8 t 16.0'%). In the controls, MVC, VA and T M C were significantly higher than in both OA groups. Conclusion: We assume that a decrease of T M C might occur within the course of OA and, in consequence, VA increases to maintain quadriceps MVC. 0 2003 Orthopaedic Research Society. Published by Elsevier Ltd. All rights reserved. Keywards: Osteoarthritis; Knee; Cartilage damage; Quadriceps muscle; Voluntary activation; Maximum voluntary contraction
Introduction Osteoarthritis (OA) of the knee is a painful and disabling disease [25]. The joint damage in O A is characterised by progressive loss of articular cartilage [ 101 with the development of cartilage surface defects of different extent [6,32]. In patients with knee OA, quadriceps weakness is a clinical feature that has been described several times before [13,14,36]. It is considered to be an important determinant of disability [25] and should, to a great extent, be due to arthrogenous muscle inhibition (AMI), i.e. an arthrogenous decline in muscle activation [ 13,16, 361. This arthrogenous decline in quadriceps muscle activation is attributed to altered afferent input from the diseased, damaged joint and consequent reduction in efferent motor neuron output to the quadriceps [35]. Thus, AM1 leads to both reduced voluntary activation
*Corresponding author. Tel.: +49-391-67-14035; fax: +49-391-6714006. E-n7rril urldress: [email protected] (G. Pap).
(VA) and maximum voluntary contraction (MVC) in osteoarthritic knees [ 16,201. Several recent studies stress the role of AM1 in OA of the knee, since it is not only considered to be a consequence of OA but even more importantly a risk factor for the initiation and the progression of damage to articular cartilage and other tissues in osteoarthritic knees [20,27,36]. Notably, Hurley and co-workers could demonstrate recently that in osteoarthritic knees AM1 can be reduced by a relatively brief physiotherapeutical exercise regime leading to significant improvement of quadriceps motor and sensory function and consequently to reduced disability in these patients [19]. This is in concordance with other studies reporting on reduction of disability in knee O A by muscle strengthening exercises [ 191. These encouraging reports, however, raise one major question: How does quadriceps motor function change with increasing osteoarthritic knee joint damage? As altered afferent inputs from damaged joints are made responsible for the reduction of quadriceps strength and VA in knee OA, one should suppose that with increasing severity of joint damage there is also an increase in alteration of afferent inputs and subsequently
0736-0266/$ - see front matter 0 2003 Orthopaedic Research Society. Published by Elsevier Ltd. All rights reserved doi: l0.10l6/SO736-0266(03)00128-1
G Pup e f ul. I Journal
of Orthopurdic
a decrease in quadriceps strength and VA. Answering this above question should be of particular importance for determining the optimal time in the onset of treatment in patients with knee OA. However, recent studies on muscle weakness and OA were just comparing OA patients and healthy controls without regard to differences in the severity of OA [13,20,36]. Moreover, in the studies investigating the influence of physiotherapeutical exercises of quadriceps motor function obviously only patients with relatively early stages of knee OA were included [19]. Therefore, in the present study we investigated quadriceps motor function at two distinctly different stages of osteoarthritic knee joint destruction.
Methods Putients
At our department, measurements of quadriceps strength and activation were performed in a total of 367 patients designated for knee surgery for primary OA of the knee. In the present study, we investigated 223 of these patients. The patients were selected retrospectively using the following inclusion criteria: clinical and radioiogicai signs of O A of the knee according to the ACR criteria [2]; intraoperatively visible cartilage damage: either grade I1 damage of the medial femoral and tibial condyle according to Outerbridge [301 but without damage of the lateral compartment or grade IV damage of both the medial and the lateral femoral and tibial condyle according to Outerbridge [30]; operative procedures: either arthroscopy and high tibial osteotomy or knee arthroplasty. According to the intraoperatively visible cartilage damage, patients were retrospectively divided into two groups. Group I included 68 patients with grade I1 damage of the medial femoral and tibial condyle according to Outerbridge [30]but without damage of' the lateral compartment. These patients of group I were designated to be treated by high tibial osteotomy for medial coinpartment knee OA. Prior to the high tibial osteotomy, all of these patients had undergone knee arthroscopy for assessment of the extent of the cartilage damage. Group I1 consisted of 154 patients who showed varus deformity of the same extent as those in group I but had grade I V damage of both the medial and the lateral femoral and tibial condyle according to Outerbridge [30]. Patients of group 11 were designated for bicondylar knee arthroplasty.
Rewrirch 22 (2004) Y6-1113
97
As controls. we used a group of 85 age related subjects who were staff members of our department or their relatives. According t o the criteria of the ACR [2], none of the controls had clinical signs of knee OA. Also, there was no evidence for any other knee damage in either knee in these subjects. and none of them had a history of significant knee trauma. Subjects with lower-extremity-joint replacements, with neuromuscular disorders, or with any other intercurrent illness were excluded from this study. None of the tested subjects showed significant atrophy of the quadriceps muscle of either leg with differences in thigh circumference of more than 1 cm as compared to the contralateral side. This, however. does not necessarily exclude bilateral quadriceps atrophy. At clinical examination, none of the patients had palpabk knee effusions and there were no signs of knee instability. As the contralateral knees of the OA patients of both groups showed osteoarthritic changes ranging between stage I and 111 according to Kellgren and Lawrence [22], they were excluded from the assessments. Demographic data of the OA patients and the controls included in this study are given in Table I . For pain assessment, we used the pain score of an evaluated German version of the WOMAC with a possible range of 0-10 for each of the five questions [38]. In addition, patients were asked to give the duration of knee symptoms in months. According to the duration of symptoms. OA patients were divided into three groups: patients with short-term duration (< 12 months), patients with medium-term duration (12 60 months), patients with long-term duration (>60 months) (Table 2). All experimental procedures were approved by the local ethics committee. and all subjects gave informed consent to the testing procedure. Assessnirnt of srrengtli, V A ~ i n dtrue niusculur cupucifj ( T M C ) qf' the quudricrps niiiscle
Quadriceps strength was assessed during an isometric MVC o n a purpose built chair [4,23,24,43]. The quantification of the maximal voluntary muscle activation (VA) is based on the principle that if the muscle fibres of a muscle can not be fully recruited during a maximal VA, additional force is generated by superimposed electrical muscle stimulation (twitch) [4, I 1.231. Providing over 25% of the MVC, the additional force generated by superimposing electrical stimulation is known t o have a linear relationship to the voluntarily elicited initial force [4,11.29]. The linearity is used to extrapolate the twitch amplitude at 0% MVC ('resting' muscle). Then the VA of the muscle is calculated as:
['"'
1 - twitch amplitude at MVC [N m] x IOO'X~ estimated twitch amplitude at resting muscle [Nnil
Extrapolation of the resting muscle twitch amplitude instead of direct measurement was done as twitches below 25% of MVC have been shown to have an odd relationship to the initial torque [11.29]. Knowing the MVC and the VA, the extension torque was calculated corresponding to 100'%1muscle activation. representing the T M C of the quadriceps muscle: TMC [Nm]=
maximal voluntary contraction [Nm] x voluntary activation ['XI]
loo'%,
Table 1 Demographic data and grouping of the subjects investigated OA patients chondropathy stage 11 Number of subjects Mean age ( f S D ) Gender (malelfemale) Mean height (kSD) Mean weight (+SD) Mean duration of knee symptoms (+SD) Mean WOMAC Pain score ( f S D )
OA patients chondropathy stage IV
Controls
68
154
56.7 years (k9.5) 40'1/;,/600/;1 164 cm ( i 8 . 7 ) 74 kg (f9.4) 34 months (215) 5.2 (f1.6)
65.6 years (f6.0)
85 58.1 years (f8.7)
41'%1/590/;1
36'%J64'%1
166 cm (f7.2) 76 kg (f11.9) 51 months ( f 1 3 ) 5.5 (k1.7)
173 cm (1-6.8) 75 kg (k9.7) 0
G Pap et ul I Journul of Orthopuedic R e x u r t h 22 (2004) 96-103
98
Table 2 MVC and VA according to the symptom duration
MVC (mean f SD) VA (mean k SD)
Symptom duration < I 2 month ( n = 31)
Symptom duration 12-60 months ( n = 89)
Symptom duration 260 months (n = 102)
80.7 k 40.7 N m 80.9 f 10.3'%1
72.8 k 33.5 N m 74.7 f 13.4%
76.9 38.3 N m 77.7 k 13.6%
Experimental procedure Assessment of MVC and VA was done as described previously [8,23.24,43]. For measurements of MVC and VA, all subjects were seated in an upright position on a purpose-built chair with their hips and knees flexed to 90". The lower legs were fixed to the lever arm of a force-measuring device based on an analogue strain gauge using a noiiextensible leather strap. For electrical muscle stimulation, aluminium plate electrodes of 5 x 10 cm. covered with thin, saline-soaked sponges for better skin contact, were strapped to the middle of the quadriceps muscle (cathode) and to the distal quadriceps muscle 10 cm above the patella (anode). Electrical stimulation of the quadriceps muscle was done using a constant current stimulator (Dantec Counterpoint MK 11) applying single, square-wave stimuli with 100 mA amplitude and 500 11s duration. Self-written software was used for data acquisition and for highly sensitive. automated twitch detection as described by Hales and Gandevia [15]. The sensitivity and reliability of this method had been investigated before [1,1 I]. First, subjects were instructed under intense encouragement to fully extend their knee ( 5 s ) for determination of the MVC and for maximum potentiation of the twitch response [41]. Immediately after twitch potentiation. the subjects performed isometric contractions with 90'%1. 75'%),50'%).25% and 100% of their MVC by matching the visualised torque level to the liiie on the monitor of the desired torque level. When the torque was kept stable three single stimuli were applied to the muscle generating additional force (twitch). During the testing procedure, none of the subjects reported on pain or pain dependent limitation in performing the tests in either knee. On the day of testing. none of the subjects had taken analgesics, muscle relaxants o r psychotropic agents. Tests were performed between 11 am and 3 pm in all patients. In both groups of OA patients, the experimental procedure included testing of the most affected knees that were designated for knee
Y
2I /I
operation one day before the very procedure. In the controls both knees were tested. All subjects were tested by one single, experienced technician, who has done this kind of testing procedure within different studies [4,8,23,24,42,43]. Sfufi.sticu1rmulysis The results are demonstrated as cumulative distribution function. To construct this function, the data points were sorted in ascending order and the function jumps vertically by the reciprocal of the number of data points when scanning the ordered points from left to right. This function allows to visualise the data points without the necessity for the arbitrary choice of a smoothening parameter that is necessary to construct a histogram [ 3 ] . In calculating the cumulative distribution functions, there was no adjustment for age, gender o r BMI of the subjects. In addition, results are given as means and standard deviations. Non-parametric Kolmogorow-Smirnow test was performed to compare MVCs, VAs and TMCs of osteoarthritic and control knees. The level of statistical significance was set to a p-value of p < 0.05.
Results
Fig. 1 shows the cumulative distribution function of the maximum MVCs in the two groups of OA patients and in the controls. It can be seen that in the control knees, MVC values are significantly higher (1 26.8 k 47.3, range 44.1-279 N m ) as compared to both the patients
I
-
c
I
0
. _ -
I
0
50
*
I
I00
I 50 MVC J N m l
, 200
,
250
I
300
Fig. I . Cumulative distribution function of the MVC of the quadriceps femoris muscle. Continuous-line: Group I , OA patients with grade IV chondropathy; dashed-line: Group 11, OA patients with grade 11 chondropathy; dashed-dot-line: controls, without knee joint damage.
G. Pup
0
(If
10
nl. I Journtrl of Ortliopuetlic Resrrircli 22 (2004) 96 103
20
30
40 50 60 voluntarq activation [%]
70
RO
90
99
100
Fig. 2. Cumulative distribution function of the VA of the quadriceps femoris muscle. Continuous-line: Group I, OA patients with grade IV chondropathy; dashed-line: Group 11, OA patients with grade 11 chondropathy; dashed-dot-line: controls, without knee joint damage.
with stage I1 chondropathy (75.9 k41.7, range 15.7216.1 N m ) and to the patients with stage IV chondropathy (70.3 36.9, range 13.0-290.9 N m ) (p < 0.001 for both OA groups). In contrast, cumulative distribution functions of the MVCs in patients with stage I1 and stage IV chondropathy were comparable, with no significant differences between these two groups of OA patients (p = 0.635). Evaluation of the cumulative distribution functions of quadriceps muscle VA revealed different results (Fig. 2). In the control knees, the VA values were significantly higher VA (89.3k8.0, range 55.4-98'1/0) than in both groups of OA patients 0, < 0.001). Surprisingly, in knees with chondropathy stage IV, however, VA values were significantly higher (77.2 13.2, range 37.5-97.5'56) than in knees with stage I1 chondropathy (70.8k 16.0, range 4.5-97.3'%1) (p = 0.004). Fig. 3 shows the cumulative distribution function of the total muscular capacities (TMCs) in OA patients and in the controls. Again, TMC values of the control knees were significantly higher (141.8 k 50.6, range 56.9-293.4 N m) than in both groups of OA patients (p < 0.001). In contrast to the above findings with MVC and VA, measurements yielded significantly lower TMCs in stage IV chondropathy (90.6k43.7, range 19.8-331.1 N m ) than in the knees with chondropathy stage I1 (109.6 51.O, range 37.2-352.1 N m) (p = 0.026). Analysis of symptom duration revealed significantly shorter knee symptoms in patients with chondropathy stage I1 (mean k SD: 50.8 k 43.4 months) than in patients with chondropathy stage IV (mean ? SD: 97.5 85.3 months) (p = 0.001). In contrast, there was no
*
*
* *
difference in both the MVC and the VA between patients with short-term, medium-term and long-term symptom duration, although in patients with short-term symptom duration both parameters were slightly higher as compared to patients with middle and long-term duration of symptoms (Table 2).
Discussion In the present study, we determined quadriceps muscle function at different severities of osteoarthritic cartilage damage. The assessment of osteoarthritic knee damage was performed on the basis of visualisation of the joint surface which has been estimated the golden standard for the classification of cartilage destruction in knee OA by different authors [5,9] especially because it is considered to be more sensitive than other methods of evaluating joint surface integrity as e.g. plain radiographs, computerised tomography and magnetic resonance imaging [6,9,12]. Thus, in the present investigation, evaluation of the extent of osteoarthritic joint damage and subsequent grouping of the patients according to the visible severity of cartilage destruction is probably more exact than in previous studies in which radiographs were used to asses the severity of joint damage [14,36,40]. However, it has to be considered that the patients with Outerbridge grade 11 or Outerbridge grade IV changes represent a specific subset of OA patients and are not necessarily representative of those with mild or severe OA as a whole. Therefore, our observations concerning MVC and VA changes refer only to
100
G. Pop et al. I Journcrl
of
Orrlicipaedic Rrsearcll 22 (2004) 96-103
Fig. 3. Cumulative distribution function of the TMC of the quadriceps femoris muscle. Continuous-line: Group I. OA patients with grade 1V chondropathy; dashed-line: Group 11, OA patients with grade 11 chondropathy: dashed-dot-line: controls, without knee joint damage.
differences in cartilage damage and not necessarily to differences in OA stages in general. Measurements of quadriceps activation by twitch superimposition technique, as used in this study, have been established by several groups for the evaluation of muscle function in different joints [4,20,35,43]. In particular, assessment of MVC and VA of the quadriceps muscle has been shown to be highly reliable and reproducible both in our hands [4,8,23,24,42,43] and in those of other groups (1). This good reproducibility has also been shown for subjects with OA by our group (8) [23,24]. The present study demonstrates that in comparison to healthy controls, patients with osteoarthritic cartilage damage are widely suffering from a significant loss of strength and VA of the quadriceps muscle. This is consistent with previous studies, reporting on quadriceps muscle weakness in knee OA [lo], although correlations between radiographic severity of OA and quadriceps strength have not been strong [20]. Previous studies describe quadriceps weakness in knee OA as characterised by both reduction of the MVC and the VA of the quadriceps muscle [20]. Hereby, the articular damage is supposed to stimulate articular mechanoreceptors-e.g. located in the joint capsule-evoking abnormal afferent information, which in turn decreases the excitability of 01motoneurons and thus leads to a reduced VA of the quadriceps [20]. Although there is much evidence for a complex inter-relationship between sensorimotor dysfunction of muscle, joint damage and disability [17], according to the theory of arthrogenous muscle inhibition in OA it seems to be rather likely that differences in the
extent of osteoarthritic cartilage damage should lead to differences in the abnormal afferent information and subsequently to differences in the extent of quadriceps muscle weakness and in the reduction of VA [37]. The results of the present study give strong support for this hypothesis showing that VA of the quadriceps muscle is significantly different not only between normal subjects and OA patients but also within the two groups of patients with different severities of osteoarthritic knee joint damage. However, the way VA differed between the two groups of OA patients was rather surprising. While in the control knees quadriceps VA was quite comparable to the values published for non-arthritic knees before [19,20], in the OA knees quadriceps VA did not decrease with increasing severity of osteoarthritic knee damage as one would have expected. Instead, quadriceps VA was significantly higher in knees with stage IV than in those with stage I1 cartilage damage and thus increasing with greater severity of knee OA. In addition, while-in concordance with literature-MVC in the control knees was significantly higher than in OA knees [20], comparison of quadriceps MVC between the two groups of OA patients revealed no differences. In other words, in the present study we did not find any signs of decreasing quadriceps strength with increasing severity of osteoarthritic cartilage damage. This is not necessarily in contrast to previous studies which found decreasing MVC being associated with greater disability in knee OA [20], since these studies did not assess the severity of osteoarthritic cartilage damage by evaluation of the joint surface itself but compared
G. Pup rf ul. I Journal of Orthopacdic Resc~tirch22 (2004) 96-103
different degrees of disability according to scoring systems [20] which do not necessarily correlate directly with the extent of joint damage [21,26]. In contrast to the findings with VA and MVC, the TMC showed a significant decline with increasing severity of osteoarthritic cartilage damage and was significantly inferior to that in the control knees. As the TMC:, as determined in the present study, is independent from the actual a-motoneuron activity, the decrease in TMC with greater cartilage damage reflects a loss in total strength of the entire quadriceps muscle with progression of this disease. Interestingly, despite this reduction of quadriceps TMC with progression of joint destruction, MVC was equal between the two different stages of cartilage damage. This is obviously due to the observed increase in VA of the quadriceps muscle in severe osteoarthritic joint destruction. As TMC is calculated as the ratio of MVC/VA, at lower TMC an increase in the VA is necessary to keep the MVC constant. In other words, the reduction of quadriceps TMC which takes place with progression of osteoarthritic joint damage might be compensated by an increase in the voluntarily achievable muscle activation, enabling patients with more severe forms of osteoarthritic joint damage to widely maintain quadriceps MVC as compared to patients with lesser extent of knee cartilage damage. The reasons for this phenomenon are not completely clear, yet. Since the mean age of the subjects both in the two OA groups and in the controls were slightly different, age dependent changes in quadriceps muscle function as described in previous studies [ 18,28,34] might contribute to our findings. However, as age dependent decline in quadriceps muscle strength has mostly been compared between young, middle-aged and elderly patients [ 18, 33,341, the extent to which ageing influences the changes of quadriceps muscle function in a subgroup of elderly patients with knee OA remains elusive. Moreover, as in the present study MVC remains unchanged and VA even increases with greater severity of osteoarthritic cartilage damage (and thus also with increasing age of the patients), ageing alone cannot be made responsible for the changes in quadriceps motor function observed here. This seems to be even more likely as in different studies no age dependent change of the quadriceps VA was found [18,31,33]. As in the present study only two distinct stages of chondropathy were compared, for final prove of a decline of TMC with increasing severity of OA cartilage damage (i.e. a proportional relationship) further studies including patients with different degrees of OA cartilage damage will be needed. As articular cartilage itself is aneural, arthrogenous decline in muscle activation cannot originate in cartilage but should be due to consequent changes of receptor-rich intra-articular structures such as the knee joint capsule. Characterisation of such capsular changes, e.g. by means of histological and ini-
101
munohistochemical examinations should be included in further studies to gain further insights into the contribution of this factor to the phenomenon of AMI. In addition, as cross-sectional studies like the present one have certain limitations, in these further studies longitudinal analyses will be necessary to confirm this hypothesis. Hereby, consideration of factors such as pain, duration of pain, BMI, activity limitation, joint alignment and the influence of pharmacologic agents etc. should be included to elucidate how the extent of visible cartilage damage relates to other signs and symptoms of OA and thus to disease severity as a whole. In particular, duration of symptoms seems to be a very important factor. It is well known that even terrible locking X-rays of knees can have very little symptoms. Therefore, a hyposthesis that is just as reasonable as articular damage being the source of inhibition would be the duration of symptoms. In the present study, patients with short-term duration of knee symptoms seemed to have a greater MVC and a higher VA than patients with middle and long-term symptom duration. This difference, however, was statistically not significant. This might be related to the fact that the present study did not primarily focus on this relationship. Thus, the parameter symptom duration was assessed only retrospectively on the basis of the patients reports at preoperative examination. In order to comprehensively investigate this interesting aspect, further studies will have to be conducted including standardized self assessment questionnaires capable of recording the parameter symptom duration more precisely. Moreover, there are some other possible confounding factors which might have influenced the results of this study. First, this concerns the contralateral knees of the OA patients in which radiographic signs of OA ranging between stage I and I11 according to Kellgren and Lawrence [22] were found. Although adjustment for this factor would have been rather useful, assessment of cartilage damage should be done with the same accuracy as for the involved knees. As visualisation of the cartilage of the contralateral knees was not possible, adjustment for the cartilage damage of these knee was not done in the present study, but should possibly be included in further studies. Second, although day to day variability and diurnal variation have been found to be rather low in normal subjects [8,23,24,42,43] it has to be considered that in patients with knee OA pain and functional impairment often increase as the day progresses. In order to minimise that possible variable, all patients were tested between 11 am and 3 pm, however, this parameter should be seen as a possible confounding factor. Third, it has to be considered that because all the testing was performed at 90" of knee flexion, results at other, functionally important, angles of knee flexion are unknown and could be very different from those presented here [7,39]. Also, in the present study the criterion
I02
G. Pup rt ul. I Journul of Orthopedic Rrsrurch 22 (2004) 96-103
for quadriceps atrophy was only a difference of more than 1 cm in the circumference of the two thighs. Therefore, more sophisticated methods for the measurement of muscle atrophy should be included in further studies to see in how far more distinct degrees of quadriceps atrophy affect the leg strength of OA patients. This is also important as differences in preoperative physical therapy and training to strengthen the quadriceps could certainly cause differences quadriceps MVC. Although rather difficult to exactly determine, in the present study there was no evidence that patients with advanced OA had more P.T. and training to strengthen the quadriceps than patients with mildmoderate OA. In conclusion, however, from the present study it seems that not MVC but TMC is the parameter of muscle function that decreases with greater severity of osteoarthritic knee joint destruction. Although speculative, we assume that a decrease of TMC might occur with increasing severity of osteoarthritic cartilage damage and, in consequence, VA increases to maintain quadriceps MVC. Further studies will have to prove this hypothesis and should study the role of other possible confounders such as symptom duration.
Acknowledgements This work was supported by Deutsche Forschungsgemeinschaft AW 512-2, AW 512-4 and NE 50514-2. The authors thank Brigitte von Specht for her technical assistance in performing the measurements. References [I] Allen GM, Gandevia SC, McKenzie DK. Reliability of measurements of muscle strength and voluntary activation using twitch interpolation. Muscle Nerve 1995;18:593400. [2] Altman R, Asch E, Bloch D, Bole G, Borenstein D, Brandt K, et al. Development of criteria for the classification and reporting of osteoarthritis. Classification of osteoarthritis of the knee. Diagnostic and Therapeutic Criteria Committee of the American Rheumatism Association. Arthritis Rheum 1986;29:103949. 131 Awiszus F. Spike train analysis. J Neurosci Meth 1997;74:155-66. [4] Awiszus F, Wahl B, Meinecke I. Influence of stimulus cross talk on results of the twitch-interpolation technique at the biceps brachii muscle. Muscle Nerve 1997;20:1187-90. [5] Ayral X . Diagnostic and quantitative arthroscopy: quantitative arthroscopy. Baillieres Clin Rheumatol 1996;10:477-94. [6] Ayral X, Gueguen A, Ike RW, Bonvarlet JP, Frizzier0 L, Kalunian K. et al. Inter-observer reliability of the arthroscopic quantification of chondropathy of the knee. Osteoarthr Cartilage 1998;6:160-6. [7] Becker R, Awiszus F. Physiological alterations of maximal voluntary quadriceps activation by changes of knee joint angle. Muscle Nerve 2001;24:667-72. [8] Berth A, Urbach D, Awiszus F. Improvement of voluntary quadriceps muscle activation after total knee replacement. Arch Phys Med Rehab 2002:10:1432.
[9] Blackburn-WD J, Bernreuter WK, Rominger M, Loose LL. Arthroscopic evaluation of knee articular cartilage: a comparison with plain radiographs and magnetic resonance imaging. J Rheumatol 1994;21:675-9. [lo] Brandt KD. Putting some muscle into osteoarthritis. Ann Intern Med 1997;127:154-6. [I 11 Bulow PM, Norregaard J, Mehlsen J, Danneskiold-Samsoe B. The twitch interpolation technique for study of fatigue of human quadriceps muscle. J Neurosci Meth 1995;62:103-9. [12] Fife RS, Brandt KD, Braunstein EM, Katz BP, Shelbourne KD, Kalasinski LA, et al. Relationship between arthroscopic evidence of cartilage damage and radiographic evidence of Joint space narrowing in early osteoarthritis of the knee. Arthritis Rheum 1991;34:377-82. [13] Fisher NM, Pendergast DR. Reduced muscle function in patients with osteoarthritis. Scand J Rehabil Med 1997;29:213-21. [I41 Fisher NM, White SC, Yack HJ, Smolinski RJ, Pendergast DR. Muscle function and gait in patients with knee osteoarthritis before and after muscle rehabilitation. Disabil Rehabil 1997; 19:47-5 5. [15] Hales JP, Gandevia SC. Assessment of maximal voluntary contraction with twitch interpolation: an instrument to measure twitch responses. J Neurosci Meth 1988;25:97-102. [I61 Hurley MV. Quadriceps weakness in osteoarthritis. Curr Opin Rheumatol 1998;10:246-50. [17] Hurley MV. The role of muscle weakness in the pathogenesis of osteoarthritis. Rheum Dis Clin North Am 1999;25:283-98. [IS] Hurley MV, Rees J, Newham DJ. Quadriceps function, proprioceptive acuity and functional performance in healthy young, middle-aged and elderly subjects. Age Ageing 1998;27:55-62. [I91 Hurley MV, Scott DL. Improvements in quadriceps sensorimotor function and disability of patients with knee osteoarthritis following a clinically practicable exercise regime. Br J Rheumatol 1998;37:1181-7. [20] Hurley MV, Scott DL, Rees J, Newham DJ. Sensorimotor changes and functional performance in patients with knee osteoarthritis. Ann Rheum Dis 1997;56:641-8. [21] Jewel1 FM, Watt I, Doherty M. Plain radiographic features of osteoarthritis. In: Brandt KD, Lohmander LS, Doherty M, editors. Osteoarthritis. Oxford, New York, Tokyo: Oxford University Press; 1998. p. 217-37. [22] Kellgren JH, Lawrence JS. Radiological assessment of osteoarhrosis. Ann Rheum Dis 1957;16:494-501. [23] Machner A, Pap G, Awiszus F. Evaluation of quadriceps strength and voluntary activation after unicompartmental arthroplasty for medial osteoarthritis of the knee. J Orthop Res 2002;20: 10811. [24] Machner A, Pap G, Krohn A, Rohkohl K, Awiszus F. Quadriceps muscle function after high tibia1 osteotomy for osteoarthritis of the knee. Clin Orthop 2002;399: 177-83. [25] McAlindon TE, Cooper C, Kirwan JR, Dieppe PA. Determinants of disability in osteoarthritis of the knee. Ann Rheum Dis 1993;52:258-62. [26] McAlindon TE, Wilson PW, Aliabadi P, Weissrnan B, Felson DT. Level of physical activity and the risk of radiographic and symptomatic knee osteoarthritis in the elderly: the Framingham study. Am J Med 1999;106:151-7. [27] Minor MA. Exercise in the treatment of osteoarthritis. Rheum Dis Clin North Am 1999;25:397415. [28] Murray MP, Duthie EH, Gambert SR, Sepic SB, Mollinger LA. Age related difference in knee muscle strength in normal women. J Gerontol 1985;40:280. [29] Norregaard J, Lykkegaard JJ, Bulow PM, Danneskiold-Samsoe B. The twitch interpolation technique for the estimation of true quadriceps muscle strength. Clin Physiol 1997;17:523-32. [30] Outerbridge RE. The ethiology of chondromalacia patellae. J Bone Joint Surg [Br] 1961;43-B:752-7.
G. Pup et ul. I Journal
of
Orthopuedic Reseurch 22 (2004) 96-103
[31] Phillips SK, Bruce SA, Newton D, Woledge RC. The weakness of old age is not due to failure of muscle activation. J Gerontol 1992;47:M45-9. [32] Pritzker KPH. Pathology of osteoarthritis. In: Brandt KD, Doherty M, Lohmander LS, editors. Osteoarthritis. Oxford, New York, Tokyo: Oxford University Press; 1998. p. 5&61. [33] Roos MR, Rice CL, Connelly D M , Vandervoort AA. Quadriceps muscle strength, contractile properties, and motor unit firing rates in young and old men. Muscle Nerve 1999;22:1094103. [34] Rutherford OM, Jones D. The relationship between muscle and bone loss and activity levels with age in women. Age Ageing 1992;21:286-93. [35] Rutherford OM, Jones DA, Newham DJ. Clinical and experimental application of the percutaneous twitch superimposition technique for the study of human muscle activation. J Neurol Neuro Surg Psychiat 1986;49:1288-91. [36] Slemenda C, Brandt KD, Heilman DK, Mazzuca S, Braunstein EM, Katz BP, et al. Quadriceps weakness and osteoarthritis of the knee. Ann Intern Med 1997;127:97-104. [37] Stokes M, Young A. The contribution of reflex inhibition to arthrogenous muscle weakness. Clin Sci 1984;67:7-14.
103
[38] Stucki G , Meier D, Stucki S, Michel BA, Tyndall AG, Dick W, et al. Evaluation of a German version of WOMAC (Western Ontario and McMaster Universities) Arthrosis Index. Z Rheuniato1 1996;55:40-9. [39] Suter E, Herzog W. Extent of muscle inhibition as a function of knee angle. J Electromyogr Kinesiol 1997;7: 123-30. [40] Tan J, Balci N, Sepici V, Gener FA. Isokinetic and isometric strength in osteoarthrosis of the knee. A comparative study with healthy women. Am J Phys Med Rehabil 1995:74:364 9. [41] Thomas CK, Johansson RS, Westling G , Bigland-Ritchie B. Twitch properties of human thenar motor units measured in response to intraneural motor-axon stimulation. J Neurophysiol 1990;64:133946. [42] Urbach D, Awiszus F. Effects of transcranial magnetic stimulation on results of the twitch interpolation technique. Muscle Nerve 2000;23:1125-8. [43] Urbach D, Nebelung W, Weiler H-T, Awiszus F. Bilateral deficit of voluntary quadriceps muscle activation after unilateral isolated rupture of the anterior cruciate ligament. Med Sci Sport Exer 1999;3 I :1691-6.