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Abstract

PURPOSE:

The aim of the study was to investigate the inter- and intra-rater reliability of the Modified Modified Ashworth Scale (MMAS) in the assessment of lower extremity spasticity in children with spastic cerebral palsy (CP).

METHODS:

Fifteen children (10 boys) with a mean age of 8.7±3.4 years participated. Two physiotherapists rated the spasticity of the hip adductors, knee extensors, and ankle plantar flexors for inter-rater reliability. Each child was examined again by one of the physiotherapists (same physiotherapist for all of the children) for intra-rater reliability (mean interval = 7 days). A random sequence of raters and muscles tested was applied.

RESULTS:

The reliability of the intraclass correlation coefficients (ICC) for individual muscle groups ranged between good to excellent (ICC_agreement of 0.60–0.83). The ICC values for overall inter-rater (ICC_agreement = 0.82) and intra-rater reliability (ICC_agreement = 0.85) were excellent.

CONCLUSION:

The MMAS showed excellent reliability for the assessment of lower extremity muscle spasticity in children with cerebral palsy. However, an interpretation should be made with caution due to the small sample size and wide range of confidence interval values.

Keywords

Cerebral palsy muscle spasticity lower extremity modified modified ashworth scale inter-rater reliability intra-rater reliability

1 Background

Cerebral palsy (CP) is the most common cause of severe physical disabilities in childhood, characterized by a persistent disorder of posture, movement, or both, resulting from a non-progressive disturbance of the infant brain [1]. The aetiology of CP is complex and incompletely understood [2]. CP is a component of the upper motor neuron (UMN) syndrome with spasticity as one of the major symptoms. Spasticity as a motor disorder is estimated in 72–92% of children with CP [3]. Spastic CP is the most common type, and severe spasticity is one of the most disabling motor problems in children with CP [4]. The accepted definition of spasticity characterizes it as a velocity-dependent increase in the muscle tone felt as a resistance during passive stretch of the muscle [5]. Spasticity must be controlled, otherwise it can cause disability interfering with mobility, activities of daily living, and social functioning.

The assessment of spasticity is important in order to identify the presence and degree of it, make decisions about the type of intervention, and evaluate the effect of treatment. Clinically, it is assessed by evaluating the resistance to passive stretch when the limb is moved through the full range of motion. However, there are neurological and mechanical contributions to hyper-resistance felt during passive movement and various clinical scales to assess spasticity. The examiner using these tests applies passive stretch at one or more velocities. Slow passive elongation is used to assess the mechanical component, and high stretch velocities are used to detect resistance due to the neural component. However, it is difficult to determine the neural or mechanical origin of hyper-resistance [6]. The Ashworth scale (AS) and the Bohannon-Smith Modified Ashworth Scale (MAS) are the tools used most commonly for assessing muscle spasticity. The AS uses high velocity to stretch the muscle through a range of movement and grade the hyper-resistance with a single value. To use the AS, there should be no significant muscle contracture so that the muscle may be passively stretched through the range of movement. A study found that the degree of soft tissue contracture determines the magnitude of the mechanical component to joint hyper-resistance, and if patients without significant contracture are tested, the mechanical resistance does not contribute significantly to spasticity [7].

The Ashworth Scale (AS) was presented in 1964 as a clinical scale to evaluate the effects of the anti-spastic drug carisoprodol in patients with multiple sclerosis. The AS is an ordinal level measure with five grades, ranging from “0” (no increase in tone) to “4” (affected part rigid in flexion or extension). Later in 1987, with the aim to increase the scale sensitivity at the lower grades, Bohannon and Smith modified it by adding an additional grade of “1+” between “1” (Slight increase in muscle tone) and “2” (More marked increase in muscle tone) termed as the modified AS (MAS). By adding grade “1+”, Bohannon and Smith reduced the measurement level of MAS as a nominal scale of spasticity. Both the scales assume that the resistance to passive movement felt by the examiner during passive stretch is due to spasticity. However, these two scales may not be reliable and valid for use as clinical outcome measures [8 –10]. A study to compare the reliability of the AS and MAS in assessing elbow flexors of patients with hemiplegia after stroke found a similar poor reliability for both scales [8]. Authors reported that the error was between grades “1 and “2” for the AS, and between “1” and “1+” as well as “1+” and “2” for the MAS. A further study to investigate the validity and inter-rater reliability of the original AS for the spasticity assessment of upper and lower limbs found insufficient validity and reliability and concluded that it should no longer be used to assess muscle spasticity [10]. Subsequently, an updated version of the Ashworth scale was developed known as the Modified Modified Ashworth Scale (MMAS) [8].

The MMAS removed the grade “1+” and redefined the grade “2” which resulted in the MMAS being more reliable and valid than the original and modified version. The MMAS has been evaluated in various neurological conditions [11 –21]. Considering the improvements on the new MMAS, a recent review suggested the MMAS as a more appropriate scale to be used in future investigations [22]. The previous investigations on the reliability and validity of the MMAS have been performed in adult populations. No study has evaluated the reliability of the MMAS in a paediatric population with spasticity.

1.1 Aim

Therefore, the aim of the present study was to investigate the inter- and intra-rater reliability of MMAS in the assessment of lower extremity spasticity in children with spastic cerebral palsy.

2 Materials and methods

2.1 Study design

This study used a cross-sectional design with repeated assessments. The study protocol was approved by the Research Council, School of Rehabilitation, Tehran University of Medical Sciences (TUMS). The ethical approval was obtained from the Ethics Committee of TUMS. Written informed consent to participate in the study was obtained from the children or their parents/carergivers.

2.2 Participants

Fifteen children with CP were recruited consecutively for the study between June 2017 and September 2017 from outpatient physiotherapy and occupational therapy clinics of the “Chain of Hope, International Charity Institute”, and “Tavanayab Charity”, Tehran, Iran. Inclusion criteria were: (1) Diagnosed with spastic CP; (2) Aged 5 to 18 years; (3) No history of surgery and botulinum toxin injections in the limbs within the last 6 months; (4) Not taking medications for spasticity; and (5) Ability to understand and follow study instructions. Exclusion criteria were: (1) Contraindication to passive movement; (2) Presence of fixed muscle contracture; or (3) Unwillingness to participate in the study.

2.3 Raters

The raters were two female physiotherapists with a mean age of 29.6 years who had 5 and 2 years of clinical experience in the paediatric field, especially in the treatment of children with CP. A one-hour practice session was held before initiating the study to review the test procedures and methodology on healthy subjects and children with CP under the supervision of the third author who is an experienced physiotherapist and University Professor.

2.4 Spasticity assessment

The Persian version of the MMAS [23] was used to assess spasticity (Table 1). Three spastic muscle groups in the lower extremity (i.e., hip adductors, knee extensors, and ankle plantar flexors) were assessed following the standardized positions and procedure which has been described and used in previous studies [16, 24]. Briefly, patients were placed in supine position for hip adductors and ankle plantar flexors with the knee in extension, and side lying for knee extensors. For hip adductors, the rater was positioned on the side being tested. They placed one hand underneath the limb close to the knee while the other hand grasped the limb close to the ankle and moved the leg from adduction into full abduction. During the assessments of hip adductor muscle spasticity, the opposite limb was stabilized. For ankle plantar flexors, the rater grasped the ball of the foot with one hand while the other hand stabilized the limb just proximal to the ankle. Then, they moved the ankle from maximum plantar flexion into maximum dorsiflexion. For knee extensors, the rater was positioned behind the child, then placed one hand on the lateral surface of thigh just proximal to the knee to stabilize the femur while the other hand grasped the leg just proximal to ankle. The rater moved the knee from maximum extension to maximum flexion. For rating spasticity, only one passive movement was allowed, which was applied over 1 second by counting one thousand one [8].

Table 1
Modified Modified Ashworth Scale for grading muscle spasticity

Grade Description

0 No increase in muscle tone

1 Slight increase in muscle tone, manifested by a catch and release or by minimal resistance at the end of the range of motion when the affected part(s) is moved in flexion or extension

2 Marked increase in muscle tone, manifested by a catch in the middle range and resistance throughout the remainder of the range of motion, but affected part(s) easily moved

3 Considerable increase in muscle tone, passive movement difficult

4 Affected part(s) rigid in flexion or extension

Grade	Description
0	No increase in muscle tone
1	Slight increase in muscle tone, manifested by a catch and release or by minimal resistance at the end of the range of motion when the affected part(s) is moved in flexion or extension
2	Marked increase in muscle tone, manifested by a catch in the middle range and resistance throughout the remainder of the range of motion, but affected part(s) easily moved
3	Considerable increase in muscle tone, passive movement difficult
4	Affected part(s) rigid in flexion or extension

All assessments were carried out at the Physiotherapy Clinic of Chain of Hope Institute in the morning between 9–12 AM. The testing area was quiet. Before assessing the muscles, the children were asked to rest on the bed for five minutes. Two raters assessed each patient during a single session with a 5-minute interval for inter-rater reliability. For intra-rater reliability, the first rater reassessed the patients after three to eleven days (average = seven days). The order of raters’ assessments and the sequence of muscles tested were randomized. Each rater recorded the spasticity scores according to the MMAS on a separate sheet. A third therapist collected the sheets, thus having the raters blinded to each other’s assessment. Raters were not allowed to discuss their assessments and assigned scores. If the children had hemiplegia, only the affected limb was assessed. For the children with diplegia or quadriplegia, both lower extremities were assessed in a random order.

2.5 Statistical analyses

The ICC and 95% confidence intervals (CI) were calculated to analyse the inter-rater and intra-rater reliability. The ICC that is the equivalent of the Weighted Kappa for ordinal measures determines the absolute agreement taking into consideration of repeated measures analysis of variance to compare the repeated measurements. It is a better measure as it accounts for both relative and absolute reliability. The level of reliability was analysed by Intra-class Correlation Coefficient (two-way random effects model, absolute agreement, and average measure). This type of ICC model is appropriate for clinical rater based assessments and indicates that each patient was assessed for muscle spasticity by each rater. An average of two raters’ scores was taken for analysis because both were involved in the study. In the ICC model of two-way random effects, the raters are assumed to be random representatives of the larger population of raters. The reliability results can be generalized to any raters with the same characteristics as those who participated in the study. Absolute agreement indicates the extent to which the assigned scores are the same. The ICC was calculated for each individual muscle group as well as for overall agreement on total assigned scores across all three muscle groups. ICC values were interpreted as: Excellent (ICC≥0.75); Good (ICC between 0.60 and 0.75); and Fair (ICC between 0.40 and 0.59) [25]. The SPSS version 18.0 (SPSS Inc; Chicago, Illinois) was used for all statistical analyses.

3 Results

3.1 Participants

Fifteen children (10 boys, 5 girls) with a mean age of 8.7±3.4 years (range: 5.3–14.3) participated in this study. Nine had diplegia, three hemiplegia, and three quadriplegia. Overall, 26 limbs were assessed; one of the lower extremities of a child with quadriplegia had a previous surgery and was excluded from the assessment. The levels of Gross Motor Function Classification System (GMFCS) were documented as follows: level I, n = 3; level II, n = 5; level III, n = 2; level IV, n = 3; and level V, n = 2. Two children with diplegia (GMFCS = IV) and hemiplegia (GMFCS = II) participated only in the inter-rater session of measurements. Therefore, 13 children participated for intra-rater measurements. The mean interval between measurements for intra-rater reliability was 7.0 days (range 3.0–11.0).

3.2 Inter-rater reliability

The ICC values for inter-rater reliability were excellent for hip adductors and good for both knee extensors and ankle plantar flexors. The overall inter-rater value for all muscle spasticity assessments was excellent (Table 2). Raters scored all MMAS grades from 0 to 4, and the children were mostly scored the grades of 1 and 3 across all muscle groups. The term “most” indicated above relates to the same score most frequently assigned by raters across three lower extremity muscle groups (Table 3).

Table 2
ICC values for inter-rater reliability of the MMAS^*

Muscle groups ICC_agreement^** 95% Confidence Interval ICC interpretation Fleiss scale [23] ICC interpretation Portney-Watkins scale [25]

Hip adductors 0.78 0.52–0.90 Fleiss scale: Fair-Excellent Excellent Good

Portney-Watkins scale: Moderate-Excellent

Knee extensors 0.73 0.41–0.88 Fleiss scale: Fair-Excellent Good Moderate

Portney-Watkins scale: Poor-Good

Ankle plantar flexors 0.60 0.09–0.82 Fleiss scale: Poor-Excellent Good Moderate

Portney-Watkins scale: Poor-Good

Overall 0.82 0.70–0.89 Fleiss scale: Good-Excellent Excellent Good

Portney-Watkins scale: Moderate-Good

^*Modified Modified Ashworth Scale; ^**Intraclass Correlation Coefficient (two-way random effects model using an absolute agreement definition).

Muscle groups	ICC_agreement^**	95% Confidence Interval	ICC interpretation Fleiss scale [23]	ICC interpretation Portney-Watkins scale [25]
Hip adductors	0.78	0.52–0.90 Fleiss scale: Fair-Excellent	Excellent	Good
		Portney-Watkins scale: Moderate-Excellent
Knee extensors	0.73	0.41–0.88 Fleiss scale: Fair-Excellent	Good	Moderate
		Portney-Watkins scale: Poor-Good
Ankle plantar flexors	0.60	0.09–0.82 Fleiss scale: Poor-Excellent	Good	Moderate
		Portney-Watkins scale: Poor-Good
Overall	0.82	0.70–0.89 Fleiss scale: Good-Excellent	Excellent	Good
		Portney-Watkins scale: Moderate-Good

Table 3

Total assigned scores by two raters across three lower extremity muscle groups using Modified Modified Ashworth Scale (MMAS) in children with spastic cerebral palsy

	MMAS Scores: Rater 2
MMAS Scores: Rater 1	0	1	2	3	4	Total
0	2	6	0	0	0	8
1	2	13	1	0	0	16
2	1	6	9	2	0	18
3	0	3	9	16	1	29
4	0	0	2	5	0	7
Total	5	28	21	23	1	78

^*Note: ICC_agreement for the entire lower extremity = 0.82 (95% Confidence Interval: 0.70–0.89), p < 0.001.

3.3 Intra-rater reliability

The ICC values for intra-rater reliability were good for both hip adductors and knee extensors and excellent for ankle plantar flexors. The overall intra-rater value for all muscle spasticity assessments was excellent (Table 4). The rater scored all MMAS grades from 0 to 4, and the children were mostly scored grades of 1 and 3 across all muscle groups. Again the term “most” relates to the same score most frequently assigned by the rater across the three lower extremity muscle groups (Table 5).

Table 4
ICC values for intra-rater reliability of the MMAS^*

Muscle groups ICC_agreement^** 95% Confidence Interval ICC Fleiss scale [23] ICC interpretation Portney-Watkins scale [25]

Hip adductors 0.70 0.29–0.87 Fleiss scale: Poor-Excellent Good Moderate

Portney-Watkins scale: Poor-Good

Knee extensors 0.70 0.30–0.87 Fleiss scale: Poor-Excellent Good Moderate

Portney-Watkins scale: Poor-Good

Ankle plantar flexors 0.83 0.61–0.93 Fleiss scale: Good-Excellent Excellent Good

Portney-Watkins scale: Moderate-Excellent

Overall 0.85 0.76–0.91 Fleiss scale: Excellent-Excellent Excellent Good

Portney-Watkins scale: Good-Excellent

^*Modified Modified Ashworth Scale; ^**Intraclass Correlation Coefficient (two-way random effects model using an absolute agreement definition).

Muscle groups	ICC_agreement^**	95% Confidence Interval	ICC Fleiss scale [23]	ICC interpretation Portney-Watkins scale [25]
Hip adductors	0.70	0.29–0.87 Fleiss scale: Poor-Excellent	Good	Moderate
		Portney-Watkins scale: Poor-Good
Knee extensors	0.70	0.30–0.87 Fleiss scale: Poor-Excellent	Good	Moderate
		Portney-Watkins scale: Poor-Good
Ankle plantar flexors	0.83	0.61–0.93 Fleiss scale: Good-Excellent	Excellent	Good
		Portney-Watkins scale: Moderate-Excellent
Overall	0.85	0.76–0.91 Fleiss scale: Excellent-Excellent	Excellent	Good
		Portney-Watkins scale: Good-Excellent

Table 5

Total assigned scores by first rater across three lower extremity muscle groups using Modified Modified Ashworth Scale (MMAS) in children with spastic cerebral palsy

	MMAS Scores: 2^nd Trial (approximately 1 week later)
MMAS Scores: 1^st Trial	0	1	2	3	4	Total
0	1	2	0	1	0	4
1	3	19	3	0	0	25
2	0	4	11	3	0	18
3	0	1	4	16	0	21
4	0	0	0	1	0	1
Total	4	26	18	21	0	69

^*Note: ICC_agreement for the entire lower extremity = 0.85 (95% Confidence Interval: 0.76–0.91), p < 0.001.

4 Discussion

The aim of this study was to determine the inter-and intra-rater reliability of the MMAS in children with CP. As far as we know, this is the first study assessing the reliability for spastic muscle groups of lower extremity in children with CP. The results indicated excellent overall reliability of the MMAS to measure lower extremity muscle spasticity which is in line with previous investigations assessing adult subjects with spasticity [11 , 18].

Experience of the raters performing the assessments and amount of formal training received by the two raters are important factors that could impact the reliability results [15]. However, participation of experienced and trained raters in a reliability study of a scale may not be relevant to clinical practice [14]. In the clinics, therapists with any experience and without formal training on a clinical scale are required to assess muscle spasticity.

The raters in this study were not using the MMAS in the clinic prior to this study. Only one of the raters was familiar with the MMAS. They did not undergo extensive training for using the MMAS. They commented that the one-hour practice session was sufficient for training, as the MMAS was easy to understand and apply.

Despite the limted experience of raters, differences in years of experience between the two raters, and the short one-hour training session, excellent reliability was obtained. This implies that the revisions to the original assessment tools (i.e., AS and MAS) resulting in the present MMAS improves reliability [22], and that the new MMAS is easy to implement and score regardless of the raters’ experience and training.

Between raters, the lowest reliability was found for plantar flexors. Reasons for this finding could be that greater spasticity (i.e., scores of 3 and 4) is observed for plantar flexors and there is less ankle range of motion. Raters reported that the above-mentioned factors (i.e., greater spasticity and decreased range of motion) were challenging for them to grade the level of spasticity. Raters had no experience in the use of the MMAS. Despite good inter-rater reliability found for plantar flexors, increased experience using the MMAS could possibly increase the reliability even more. Generally, formal training along with experience may increase reliability. The intra-rater reliability found for the ankle plantar flexors was excellent. This may imply that with experience obtained during the study by the rater (who was familiar with the scale previously) and participation in the intra-rater reliability stage of the study, a higher reliability was obtained.

Although the agreements between raters and within rater for all muscle groups were excellent or good in this study, the 95% CI boundaries need to be considered when interpreting the ICCs as they may provide a plausible estimate of reliability in this sample of patients with CP from which the data are collected. For the individual muscle groups, while the lower bounds of 95% CI ranged from poor to good between raters and within rater, the upper bounds were excellent. The findings on the low ICC values in the lower bound of 95% CI may be interpreted as non-significant reliability. Regardless, the data in the upper bound indicate an excellent reliability. Low ICC values found for the low bound of 95% CI might be due to the small sample of patients, small number of raters, and lack of variability among the CP patients included in this study. To draw a definitive conclusion on the strength of reliability of MMAS in patients with CP, further studies with more patients and more examiners are warranted to clarify the strength of reliability. The authors suggest at least 30 heterogeneous patients involving at least 3 raters for a reliability study [26].

There are different methods for interpreting levels of associations and clinical significance [25, 27]. The cut-off points suggested for interpretations of relationships are inconsistent [Table 2, Table 4]. While researchers would agree that a lower end value indicates a low reliability (ICC < 0.5) [27] and upper end values as high one (ICC > 0.75) [25], values in middle ranges are disputable and are interpreted differently. For example, an ICC value of 0.60 could either be interpreted as a “good” [25] or “moderate” reliability [27], depending on the applied method. The Fleiss scale [25] used in this study and that of Portney-Watkins scale [27] are widely used and accepted ones for interpretation of relationship strengths. The ICC values estimated in this study are≥0.60 and considering any method will not significantly change the interpretations. However, interpreting the confidence interval bounds, not the ICC statistics, indicates that caution is required regarding the level of reliability of the MMAS in this sample of patients with CP.

In subjects with spasticity following UMN lesions such as CP, several muscles are affected in the lower or upper extremity. In this study, reliability for individual muscle groups of the lower extremity was established. In the meantime, the reliability across all muscle groups of the affected limb was also evaluated to give an overall agreement in the limb. In this study, excellent inter-and intra-rater reliability assessment of spasticity for the lower extremity was achieved. This finding is in line with a previous study in adults with various neurological conditions that showed an overall high degree of intra-rater reliability for lower-extremity muscle spasticity [16].

4.1 Limitation

In this study, lower extremity spastic muscle groups were evaluated. The upper extremity is also affected in children with CP. Hence, the reliability of the MMAS should be examined for spastic muscle groups of the upper extremity. The sample size of children with CP included in the present study was small. The COSMIN (COnsensus-based Standards for the selection of health status Measurement INstruments) guideline for evaluating measurement properties suggests sample sizes of at least 30 subjects [28]. Therefore, future studies must recruit larger samples of children to verify the results of the present study. Another limitation is that the raters in our study were physiotherapists that may limit the generalizability of the findings to examiners from other health professions. The testing environment was standardized and controlled for potential external factors that could affect the children’s participation, their spasticity and assessment results (i.e., assessments limited to the mornings, maintaining a quiet testing area, and allowing children to rest for 5 minutes before assessing them). However, it is uncertain whether the wide range of days (3–11 days) for the intra-rater assessments could significantly impact the results. It is possible that with so few participants and a mean of 7.0 days between assessments by the same assessor, the physiotherapist could have recalled their prior ratings. Nevertheless, a study to compare the time intervals of 2 days and 2 weeks found no significant differences in the test-retest reliability [29].

5 Conclusions

In conclusion, this study examined the inter-and intra-rater reliability of the MMAS in assessing the lower extremity muscle spasticity of children with spastic CP. The MMAS offers a reliable tool for professionals working with children with spastic CP to determine the presence and degree of spasticity and to evaluate the effect of treatment. However, due to the small sample size and wide range of confidence interval values, an interpretation of results should be made with caution. The findings indicate that more investigations are needed to estimate the MMAS reliability of measurements in children with CP.

Footnotes

Acknowledgments

We would like to thank the Research Deputy, Tehran University of Medical Sciences for supporting this study. We also would like to thank the subjects for their participation in the study.

Conflict of interest

The authors have no conflict of interest to report.

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Inter- and intra-rater reliability of the modified modified ashworth scale in the assessment of muscle spasticity in cerebral palsy: A preliminary study

Abstract

PURPOSE:

METHODS:

RESULTS:

CONCLUSION:

Keywords

1 Background

1.1 Aim

2 Materials and methods

2.1 Study design

2.2 Participants

2.3 Raters

2.4 Spasticity assessment

3 Results

3.1 Participants

3.2 Inter-rater reliability

4.1 Limitation

5 Conclusions

Footnotes

Acknowledgments

Conflict of interest

References