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PHYS THER
Vol. 86, No. 9, September 2006, pp. 1231-1239
DOI: 10.2522/ptj.20050189
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Research Reports

Measurement of Muscle Thickness as Quantitative Muscle Evaluation for Adults With Severe Cerebral Palsy

Koji Ohata, Tadao Tsuboyama, Noriaki Ichihashi and Satosi Minami

K Ohata, PT, MS, is Instructor, Department of Physical Therapy, School of Health Sciences, Faculty of Medicine, Kyoto University, Kyoto, Japan
T Tsuboyama, MD, PhD, is Professor, Department of Physical Therapy, School of Health Sciences, Faculty of Medicine, Kyoto University
N Ichihashi, MD, PhD, is Professor, Department of Physical Therapy, School of Health Sciences, Faculty of Medicine, Kyoto University
S Minami, PT, is Research Assistant, Course of Physical Therapy, Department of Medical Rehabilitation, Faculty of Rehabilitation, Kobegakuin University, Kobe, Japan

Address all correspondence to Mr Ohata at: oohata{at}hs.med.kyoto-u.ac.jp


Submitted June 13, 2005; Accepted April 27, 2006


   Abstract
 
Background and Purpose. The muscle strength of people with severe cerebral palsy (CP) is difficult to quantify because of cognitive and selective motor control problems. However, if muscle strength is related to muscle atrophy caused by activity limitation, quantitative morphological analysis such as analysis of muscle thickness (MTH), measured by ultrasound imaging, may be used to examine the muscle condition in daily use. The primary purpose of this investigation was to clarify the difference in MTH of several muscles by the motor functions used in daily activity in adults with CP with different levels of severity of involvement. The secondary purpose was to examine whether MTH is associated with age, body characteristics, and muscle spasticity. Subjects. Data were collected from a convenience sample of 25 adults with severe CP. Methods. The MTH of the biceps brachii (BB), quadriceps femoris (QF), triceps surae (TS), and longissimus (LO) muscles was measured with an ultrasound imaging device. The severity of the condition was classified with the Gross Motor Function Classification System (GMFCS), and functional status in sitting and standing was evaluated with a questionnaire administered to the staff assisting in the care of the subjects. Muscle spasticity was assessed with the Modified Ashworth Scale (MAS). Results. The MTH of the QF, LO, and TS showed significant differences according to the GMFCS level, and the MTH of the QF and LO differed significantly depending on functional status during activities of daily living. Age and body mass index showed no significant correlation with the MTH of any muscle. Body weight was correlated with the MTH of the BB and LO. The girth of the extremity was correlated only with the MTH of the BB. There was no relationship between MTH and MAS scores. Discussion and Conclusion. These results suggest that the MTH of the QF and LO differed significantly depending on the subjects' motor function during daily activity. The measurement of MTH may be an alternative method of quantitative muscle evaluation for people with severe CP for whom direct measurement of muscle strength is difficult.

Key Words: Cerebral palsy • Muscle thickness • Quantitative evaluation • Ultrasound sonography


   Introduction
Top
 Abstract
 Introduction
Method
 Results
 Discussion
 Conclusion
 References
 
Cerebral palsy (CP) is an umbrella term that covers a group of nonprogressive, but often changing, motor impairment syndromes secondary to lesions or anomalies of the brain arising in the early stage of development.1 Motor impairment in CP is not fixed in early development, but continues to be modified until reaching adulthood. Although the types and severity of the disorder vary, most problems related to physical abilities continue for life. Bottos and colleagues2 investigated the development of individuals with CP from childhood to adulthood. Their results showed that contact with health care providers and rehabilitation professionals had been reduced by the time the subjects reached adulthood and that many subjects underwent functional deterioration such as loss of mobility when they became adolescents. Problems of lower-extremity pain, back pain, and physical fatigue also have been reported in adults with CP.3–5 It is possible that pain and fatigue play a role in causing further deterioration of function and physical inactivity. Sandstrom and colleagues6 reported that one third of adults with CP deteriorated in function during adolescence. They concluded that decreased functional ability and secondary musculoskeletal problems are common in adults with CP and that general health also can be impaired in association with these problems.

However, there is little quantitative data on muscle strength (force-generating capacity) and functional status in adults with severe impairment. When people are evaluated by questionnaire or using tasks requiring effort, their comprehension is essential. For example, muscle strength is difficult to measure in people with severe CP because it is not easy for them to understand the task they need to perform. Therefore, an alternative method of quantitative muscle evaluation that can be performed without communication or effort would be beneficial.

In general, limited activity leads to muscle weakness and atrophy. Although people with severe CP usually show muscle atrophy caused by palsy and limited activity, it is still possible that muscle thickness (MTH) measured by ultrasound imaging reflects muscle strength, at least to some extent. It has been proposed that quantitative ultrasonography is a potentially useful tool for studying skeletal muscle.7–12 However, the difference in MTH for people with CP with different levels of motor function is not clear. Moreover, it is not understood whether MTH is influenced by age, body characteristics, and muscle spasticity in adults with CP. The primary purpose of this investigation was to clarify the difference in MTH of several muscles by motor function in daily activity in adults with severe CP. The secondary purpose was to examine whether MTH is associated with age, body characteristics, and muscle spasticity.


   Method
Top
 Abstract
 Introduction
 Method
Results
 Discussion
 Conclusion
 References
 
Subjects

The participants in this study were 25 people with CP (16 men and 9 women) who were aged 18 years and older. The subjects' mean age was 37.8 years (SD=10.6, range=19–60), their mean height was 149.5 cm (SD=11.9, range=122–176), and their mean weight was 43.0 kg (SD=10.0, range=24.0–61.4). The average BMI was 19.1 (SD=3.7, range=13.2–26.4) (Tab. 1). We recruited participants who had entered a rehabilitation center for people with severe handicap (Nikoniko House, Kobe, Japan) and whose motor function corresponded to Gross Motor Function Classification System (GMFCS) levels III to V,13 with communication disorder. Inclusion criteria were: (1) chronological age of 18 years or older, (2) without severe respiration and circulation disorder requiring respirator use, and (3) without severe epilepsy, possibly causing a seizure during the measurement. All subjects had clinically diagnosed spastic CP. Fifteen subjects had quadriplegia, and 10 subjects had diplegia. Most of the subjects were severely intellectually disabled. All subjects had an IQ of less than 35, and 19 subjects had an IQ of less than 20. In addition, 18 subjects had scoliosis. We explained the purpose of the study to the families of all subjects orally and in writing, and written consent was obtained.


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  		Table 1. Subject Characteristicsa

 
Measures

GMFCS
The severity of motor disability was assessed by attending physical therapists using the GMFCS.13 The GMFCS is a descriptive classification system that categorizes the motor function of children with CP into 5 levels, from level 1 (least impaired) to level 5 (most impaired). A Japanese version of the system also is available.14 To deal with the changing functional abilities of children with CP at different ages, the system describes gross motor function within specified age bands.13 The age band used in this study was "6 to 12 years," the oldest age band in the GMFCS, because all participants were 18 years of age or older. The reliability of data obtained with the system for children under 12 years of age has been verified.13,15 No specific training was provided to the therapists because a previous study13 indicated that the GMFCS can be used reliably by experienced developmental therapists without special instruction.

Functional state in activities of daily living (ADL)
Information on functional status in sitting and standing during ADL was obtained by a questionnaire given to the facility staff. They chose one category corresponding to the actual level of function in ADL of each participant. The state of sitting was classified for 2 groups according to the need for assistance to remain sitting. The first group, characterized as "sitting with assistance," needed assistance such as use of a seating system at least occasionally, and the second group, characterized as "sitting without assistance," needed no assistance for sitting in daily activity. For the functional state of standing, the participants were categorized as "not standing (NS)," "nonfunctional standing (NFS)," or "limited functional standing (LFS)." In this study, no one could stand independently, because the function of the participants was GMFCS level III, IV, or V. The NS category indicated that the subject could not stand at all, NFS indicated that the subject stood only during training and not during the actual ADL, and LFS indicated that the subject stood with assistance during the actual ADL. For instance, the subject's ability to support his or her own weight with assistance during transfer from a wheelchair corresponded to LFS.

Quantitative ultrasonography
Muscle thickness was measured with a B-mode ultrasound imaging device (Toshiba Medical System SSA320A*) on both left and right sides by a physical therapist (KO) who had trained in its use. The biceps brachii (BB), quadriceps femoris (QF), triceps surae (TS), and longissimus (LO) muscles were selected as the target muscles, because they can be identified and assessed most clearly. The locations of the ultrasound measurement were decided as areas where the target muscles could be most clearly identified. The thickness of the BB was measured at the midpoint between the acromion and cubital fossa with the elbows flexed at 90 degrees. The QF was measured at the midpoint between the anterior superior iliac spine and the proximal end of the patella with the knees flexed at 90 degrees. The thickness of the TS was measured on the line between the medial femoral condyle and the heel at one third of the distance from the medial femoral condyle with the ankle at maximal planter flexion. Measurement of the LO was carried out at 2 finger widths lateral from the spinous process of the eighth thoracic spine. Measurements of the BB, QF, and TS were carried out while the subjects were relaxed in the supine position, and that of LO was performed with the subjects lying on their side.

An ultrasound linear probe (Toshiba Medical System PLG-805S*) fitted with an 8-MHz transducer was placed on the skin perpendicular to the tissue interface. The scanning head was coated with water-soluble transmission gel to provide acoustic contact without depressing the dermal surface. The 2 interfaces, one between subcutaneous adipose tissue and muscle and the other between muscle and bone, were identified from the ultrasound image, and the greatest distance between these 2 interfaces was recorded as the MTH (Fig. 1). The MTH of each muscle was measured bilaterally, and the results were expressed as MTH on the "thick side" and the "thin side," depending on the side difference. The reason for examining "thick" and "thin" data sets separately was to determine whether the influence of GMFCS level was different between thick and thin sides. Ishida et al16 reported the reliability of B-mode ultrasound for measurement of MTH. They concluded that the contribution by investigators and trials to the variance was less than 1%. In our study, one investigator (KO), who did not know the other data, performed the ultrasound measurements.


Figure 1
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  		Figure 1. Ultrasonographic images showing the muscle thickness of the quadriceps femoris muscle in 3 adults with quadriplegia: (A) subject categorized as Gross Motor Function Classification System (GMFCS) level III, (B) subject categorized as GMFCS level IV, (C) subject categorized as GMFCS level V. All images are on the same scale, and the arrow shows the muscle thickness defined as the distance between 2 interfaces: the subcutaneous adipose tissue/muscle and muscle/bone.

 
We examined the intrarater reliability in adults who were healthy before measuring individuals with severe CP. The intraclass correlation coefficients (ICC[3,1]) were .92 for the BB, .98 for the QF, .96 for the TS, and .95 for the LO, which were similar to the previously reported ICC of .97.12

Clinical evaluation
The clinical evaluation was performed by a physical therapist who did not know the results of the ultrasound imaging done in this study. The body mass index (BMI) was calculated from each subject's weight and height. The heights of the subjects with scoliosis were measured as the sum of the head, trunk, and leg lengths. The head length was defined as the distance from the top of the head to the spinous process of C7, the trunk length was measured along the curve of the spine from the spinous process of C7 to the point between the spinous process of L4 and L5, and the leg length was measured from the point between the spinous process of L4 and L5 to the heel on the dorsal side of the leg. The girth of the extremities was measured at the maximum point in the middle of the upper arm, the calf, and 5 and 10 cm above the knee joint. Muscle spasticity was evaluated with the Modified Ashworth Scale (MAS) by passive extension and flexion at the elbows, knees, and ankle joints. The MAS is the most commonly used evaluation system for assessing spasticity, with classification by resistance throughout the course of passive movement.17,18 Each muscle group was rated 0, 1, 1+, 2, 3, or 4 according to the amount of resistance felt by an observer during passive stretching; 0 indicated no increase in muscle tone, and 4 indicated fixed muscle contracture.

Data Analysis

The primary interest in this study was to assess the MTH difference of each muscle according to the subjects' functional and ADL status. A 2-way, repeated-measures analysis of variance (ANOVA) was used to determine whether the MTH differed according to the GMFCS level and between the thick and thin sides. Post hoc testing (Scheffé F test) was used for multiple comparisons. The Student t test was used to determine the MTH difference according to the functional status of sitting, and a 1-way ANOVA was used to determine the MTH difference according to standing status. The average data of right and left (ie, thick and thin) sides were used to compare the difference according to the functional status of sitting and standing. In addition, the correlation between the MTH and age or body characteristics (weight, BMI, and girths of the extremities) was examined by Pearson correlation coefficient. The Spearman correlation coefficient by rank was used to examine the correlation between the MTH and MAS ratings. Significant levels for ANOVA, Scheffé F test, and Student t test were set at P<.0125 after adjustment by Bonferroni correction for multiple hypothesis testing (0.05 divided by the number of muscles tested). Significant levels for the other analyses were set at P<.05.


   Results
Top
 Abstract
 Introduction
 Method
 Results
Discussion
 Conclusion
 References
 
Influence of GMFCS on MTH

The subjects had moderate to severe impairment according to the GMFCS (level III for 5 subjects, level IV for 15 subjects, and level V for 5 subjects). Measurements of MTH of the BB in 2 subjects at level IV and of the QF in 1 subject at level III could not be obtained as will be discussed later. The average thickness of each muscle according to the GMFCS level is shown in Table 2. Most muscles of the subjects at level III were 1.5 to 2 times as thick as those of the subjects at level V. The lower limb and back muscles showed significant differences according to the GMFCS level without interaction with the thick and thin sides; however, no significant difference was observed in the BB. Multiple comparisons (Fig. 2) revealed that the MTH of the QF at level V decreased significantly compared with that at level III. The MTH of the TS at level V decreased significantly compared with that at level IV. The MTH of the LO at levels IV and V showed significant differences from that at level III.


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  		Table 2. Muscle Thickness According to the Gross Motor Function Classification System (GMFCS) Level and Sidea

 

Figure 2
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  		Figure 2. Box plots of muscle thickness by Gross Motor Function Classification System (GMFCS) level. The Scheffé F test with Bonferroni correction was used for multiple comparisons according to GMFCS level. BB=biceps brachii muscle, QF=quadriceps femoris muscle, TS=triceps surae muscle, LO=longissimus muscle. Asterisk indicates significant at P<.0125.

 
Influence of ADL Status on MTH

Eleven subjects could sit with assistance and 14 subjects could sit without assistance in daily activity. The former group consisted of 5 subjects at GMFCS level V and 6 subjects at GMFCS level IV. The latter group was composed of 9 subjects at GMFCS level IV and 5 subjects at GMFCS level III. A significant difference was observed between the groups for the MTH of the QF and LO, which was thicker in the subjects who could sit without assistance than in the subjects who could sits with assistance (Fig. 3); however, the MTH of the BB and TS showed no difference between the groups. According to the standing status, there were 14 subjects in group NS, 4 subjects in group NFS, and 7 subjects in group LFS. Group NS consisted of 5 subjects at GMFCS level V and 9 subjects at GMFCS level IV. The subjects in group NFS were at GMFCS level IV. Group LFS consisted of 2 subjects at GMFCS level IV and 5 subjects at GMFCS level III. The MTH of the QF and LO showed a significant difference according to the standing status (Fig. 4). There was a tendency toward less MTH of the BB and TS with increasing severity of standing disability, but the difference was not statistically significant. Multiple comparisons revealed that the QF and LO in group LFS were significantly thicker than those in group NS.


Figure 3
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  		Figure 3. Box plots of muscle thickness (MTH) by functional status of sitting. The Student t test with Bonferroni correction was used to compare the MTH of subjects who needed the assistance to sit ("with assistance") with the MTH of subjects who could sit independently ("without assistance"). BB=biceps brachii muscle, QF=quadriceps femoris muscle, TS=triceps surae muscle, LO=longissimus muscle. Asterisk indicates significant at P<.0125.

 

Figure 4
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  		Figure 4. Box plots of muscle thickness (MTH) by functional status of standing. One-way analysis of variance was used to examine the significance of the difference in MTH according to standing status, and the Scheffé F test with Bonferroni correction was used for multiple comparisons. NS=not standing, NFS=nonfunctional standing, LFS=limited functional standing, BB=biceps brachii muscle, QF=quadriceps femoris muscle, TS=triceps surae muscle, LO=longissimus muscle. Asterisk indicates significant at P<.0125.

 
Relationship Between MTH and Age, Body Characteristics, or MAS

We abandoned the measurement of the BB in 2 subjects and of the QF in another subject because of their reluctance to participate during the session. Although ultrasound images can be recorded if a person remains still for only 10 seconds, these 3 subjects kept moving during the measurement. The correlation coefficients between the MTH and body characteristics are shown in Table 3. Body weight showed a significant correlation with BB and LO. In contrast, age and BMI showed no significant correlation with the MTH of any muscle. The mean (±SD) girths of the extremities were 24.7±3.9 cm for the upper arm, 25.7±4.1 cm for the calf, 32.5±5.2 cm at 5 cm above the knee, and 35.3±6.7 cm at 10 cm above the knee. The correlation of the MTH with the corresponding girth was significant only between the MTH of the BB and the girth of the upper arm. The MTH showed no significant correlation with the MAS rating of each corresponding muscle (Tab. 4).


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  		Table 3. Correlation Coefficients Between Muscle Thickness (MTH) and Body Characteristicsa

 

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  		Table 4. Correlation Coefficients Between Measurements of Muscle Thickness (MTH) and Modified Ashworth Scale (MAS) Scoresa

 

   Discussion
Top
 Abstract
 Introduction
 Method
 Results
 Discussion
Conclusion
 References
 
Our main hypothesis was that MTH, as measured from ultrasound images, differs depending on the severity of motor impairment and functional disability because inactivity causes muscle atrophy in people with higher severity and lower motor function. The present study showed that the MTH differed for both GMFCS level and functional status. Significant differences were found in the MTH of the QF, TS, and LO according to the GMFCS level; however, there was no difference in the MTH of the BB. Moreover, the MTH of the QF and LO significantly differed by the functional status of sitting and standing. There was a significant correlation between body weight and the MTH of the BB and LO; however, there was no correlation between body weight and the MTH of the lower-extremity muscles. There was no relationship between the MTH and the MAS score.

Several researchers19–21 have reported that muscle strengthening resulted in improvements in physical health and functional status in children with CP. Andersson and colleagues22 reported on the effects of strength training for adults with spastic diplegia. All individuals who participated in their study were ambulatory but had various levels of motor ability, ranging from functional walkers to individuals who required walking aids and regularly used a wheelchair. Although the cognitive status of the participants was not clearly described, they probably had no severe cognitive disorder, because they could understand and perform several strength training exercises. Significant improvements were found in muscle strength, motor function, and gait speed. From these previous studies, we can speculate that even adults with CP can improve their function, maintain their ADL status, and prevent deterioration by strength training. Rimmer23 indicated that most muscular strength and endurance training studies involving people with CP have been targeted at children, and he emphasized that it is necessary to study muscle strength training in adults with CP. There has been little research on muscle training in adults with severe CP. It is difficult to examine muscle strength in people with severe to moderate CP, especially because of cognitive disorders that complicate CP. Thus, an alternative evaluation method of muscles should be established.

Ultrasound imaging is useful for evaluating the morphological characteristics of muscles in adults with severe CP because it does not require an understanding of the measurement task. Quantitative analyses of ultrasound imaging have been performed on adults with several neuromuscular diseases24 and children with neuromuscular diseases.25–27 However, in these studies, ultrasound imaging was not used for an evaluative purpose as was the focus in the present study, but for a diagnostic purpose. There have been no reports on measurement of MTH as quantitative evaluation of muscle in adults with CP.

In general, muscle strength is determined by anatomical and neurological factors and by activity level. Muscle thickness and cross-sectional areas are anatomical indicators and factors in determining muscle strength. The relationship between the size and strength of a muscle has been investigated in previous studies. Young et al7 showed a correlation between QF size and isometric strength in elderly men. More recently, Gur and Cakin28 reported that the cross-sectional area of the QF was moderately correlated with concentric and eccentric torques of the QF in people with osteoarthritis; however, they stated that anatomical factor analysis alone (eg, MTH, cross-sectional area) cannot be considered as a single predictor of muscle strength28 because quantitative muscular changes such as muscle atrophy are not sufficient to explain the strength loss related to knee osteoarthritis. This finding suggested that muscle strength is not determined only by anatomical factors; nevertheless, it is the one of the most important factors related to muscle strength. The current study did not provide direct evidence for a relationship between MTH and muscle strength in adults with severe CP. The results of the current study demonstrated that the MTH of the QF and LO, which play an important role in activities involving sitting and standing, showed significant differences according to ADL status. Conversely, the MTH of the upper-limb muscle showed no difference according to functional status in sitting and standing, probably because it is not directly used for sitting and standing. These results are indirect supporting evidence of the relationship between MTH and muscle strength in daily activity. The difference in MTH according to GMFCS level also is interesting because GMFCS level is related to the general health status of people with CP.29

In a study of Japanese people who were healthy by Abe and Fukunaga,30 the standard MTH of the QF was 5.3 and 3.8 cm in men aged 20 to 29 and 70 to 79 years, respectively. Compared with these data, the MTH of the QF in people with severe CP in the present study, even at GMFCS level III, was less than that of people of advanced age who are healthy. However, the standard MTH of the BB is 3.0 and 2.8 cm in young and aged men who are healthy, respectively.30 Therefore, no remarkable difference in MTH between subjects who were healthy and subjects with CP was observed in the BB. This discrepancy is probably due to the fact that the antigravity muscles, such as the QF, are strongly influenced by the severity of the condition expressed by GMFCS level. Regarding muscle hypertrophy, Abe et al12 reported on time-related changes in strength and MTH following resistance training of the upper and lower extremities. Subjects without motor disability trained 3 days a week for 12 weeks. The mean relative increases for knee extension strength were 19% in both male and female subjects, and the relative increases in the lower-extremity MTH were 7% to 9% in the male subjects and 7% to 8% in the female subjects. Changes in MTH following muscle atrophy also were reported by Kawakami and colleagues,31,32 who found decreased MTH of the leg muscles after a program of head-down bed rest for 20 days. In our study, there were significant differences in MTH of the QF and LO between the NS and LFS groups for functional standing status. The daily activity of the subjects in the NS group was comparable to long-term bed rest. It should be emphasized that MTH can be maintained to some extent even with slight activity. This suggests the importance of increasing the ADL of adults with CP even when they have severe disability.

In this investigation, an age-related MTH change was not observed. Because the participants showed a wide variety of functional levels, the influence of functional status on MTH was probably much greater than that of aging. There was a significant correlation between weight and MTH of the BB and LO. However, the MTH of the lower limbs showed no relationship with weight. This finding may suggest that the MTH of the QF and TS was influenced by the severity of the condition rather than by body size in adults with CP. The subjects' height and BMI scores, however, showed no significant correlation with measurements of MTH of any muscles. The reliability of the height measurement for people with severe scoliosis might be a problem. The girths of the lower extremities were not correlated with the MTHs of the QF and TS, probably due to the influence of subcutaneous adipose tissue in the thigh and calf. In addition, the relationship between measurements of MTH and MAS scores, that is the level of spasticity, was small. This finding is consistent with the results of a previous study22 that showed no relationship between muscle strengthening training and spasticity.


   Conclusion
Top
 Abstract
 Introduction
 Method
 Results
 Discussion
 Conclusion
References
 
We found that MTH of the knee extensors and trunk extensors differed according to the sitting and standing status in daily activity in adults with moderate to severe CP. Measurement of MTH may be an alternative method of quantitative muscle evaluation for people with severe CP for whom direct measurement of muscle strength is difficult. This quantitative evaluation may be a useful tool for clarifying the training outcome of adults with severe CP in the future. However, further validation is necessary because the evidence from the present study is limited and indirect. An observation in a larger cohort, a longitudinal study with or without training intervention, and a confirmation of the relationship between MTH and muscle strength among people with less severe CP would be informative in assessing the validity of data obtained with the method.


   Footnotes
 
Mr Ohata provided concept/idea/research design and data collection and analysis. Mr Ohata and Dr Tsuboyama provided writing. Mr Ohata and Mr Minami provided facilities/equipment. Mr Minami provided subjects, institutional liaisons, and clerical support. Dr Tsuboyama and Dr Ichihashi provided project management and consultation (including review of manuscript before submission).

The project, the information communicated to participants' families, and the consent forms were approved by Kyoto University Graduate School and Faculty of Medicine Ethics Committee.

This research was presented as an abstract at the 40th Annual Congress of the Japan Physical Therapy Association; May 26–28, 2005; Osaka, Japan.

* Toshiba Medical Systems Corp, 26-5, Hongo 3-Chome, Bunkyo-ku, Tokyo 113-8456, Japan. Back


   References
Top
 Abstract
 Introduction
 Method
 Results
 Discussion
 Conclusion
 References
 

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