Change in mobility function and its causes in adults with cerebral palsy by Gross Motor Function Classification System level: A cross-sectional questionnaire study

Abstract

BACKGROUND:

The prognosis for mobility function by Gross Motor Function Classification System (GMFCS) level is vital as a guide to rehabilitation for people with cerebral palsy.

OBJECTIVE:

This study sought to investigate change in mobility function and its causes in adults with cerebral palsy by GMFCS level.

METHODS:

We conducted a cross-sectional questionnaire study.

RESULTS:

A total of 386 participants (26 y 8 m, SD 5 y 10 m) with cerebral palsy were analyzed. Participant numbers by GMFCS level were: I (53), II (139), III (74) and IV (120). The median age of participants with peak mobility function in GMFCS level III was younger than that in the other levels. 48% had experienced a decline in mobility. A Kaplan-Meier plot showed the risk of mobility decline increased in GMFCS level III; the hazard ratio was 1.97 (95% CI, 1.20–3.23) compared with level I. The frequently reported causes of mobility decline were changes in environment, and illness and injury in GMFCS level III, stiffness and deformity in level IV, and reduced physical activity in level II and III.

CONCLUSIONS:

Peak mobility function and mobility decline occurred at a younger age in GMFCS level III, with the cause of mobility decline differing by GMFCS level.

Keywords

Cerebral palsy mobility gross motor function

1 Introduction

Most people with cerebral palsy (CP) experience a decline in their functional mobility after reaching adulthood (Morgan & McGinley, 2014; Novak, Hines, Goldsmith, & Barclay, 2012), despite the brain lesion being considered to be nonprogressive (Rosenbaum et al., 2007). Decline in walking and overall functional mobility during adolescence and early adulthood is described in several studies (Andersson & Mattsson, 2001; Bottos, Feliciangeli, Sciuto, Gericke, & Vianello, 2001; Jahnsen, Villien, Egeland, Stanghelle, & Holm, 2004; Murphy, Molnar, & Lankasky, 1995; Opheim, Jahnsen, Olsson, & Stanghelle, 2009). Several studies have also documented the causes of the decline in mobility function including pain (Jahnsen, Villien, Aamodt, Stanghelle, & Holm, 2004; Jahnsen, Villien, Egeland, et al., 2004; Jensen, Engel, Hoffman, & Schwartz, 2004; Opheim et al., 2009), fatigue (Jahnsen, Villien, Egeland, et al., 2004; Opheim et al., 2009), lack of physical activity (Jahnsen, Villien, Egeland, et al., 2004), reduced balance (Opheim et al., 2009), and decreased lower extremity strength (Davids, Oeffinger, Bagley, Sison-Williamson, & Gorton, 2015). The prevention of decline and maintenance of functional mobility is, therefore, an important goal in intervention for individuals with CP, as well as for their parents and healthcare professionals.

Recent intervention paradigms for people with CP have been enhanced by consideration of their Gross Motor Function classification System (GMFCS) (Palisano et al., 1997; Palisano, Rosenbaum, Bartlett, & Livingston, 2008) and age. Hanna et al. reported the improvement and decline curves for gross motor function in children and youths (aged 2 to 21) with CP and showed changes over time by GMFCS level (Hanna et al., 2009). Therefore, it is quite possible that the improvement and decline in mobility function differ by GMFCS level. Although the prognosis for mobility function by GMFCS level is vital as a guide to intervention, change in mobility function and its causes have not yet been examined by GMFCS level. The purpose of this study was, therefore, to investigate the time of peak mobility function and subsequent mobility decline, as well as self-reported thoughts about the causes of decline in persons with CP by GMFCS level.

2 Methods

2.1 Design

This study was a secondary analysis conducted using the Health Survey of Adult Patients with Cerebral Palsy, which is a nationwide, cross-sectional questionnaire survey conducted by the Japan Society of Surgery for Cerebral Palsy from July to September in 2015. The aims of this survey were to understand the health conditions of adults with CP (aged 19 to 39), and it covered areas such as subject mobility function, manual function, and communication function, identification of medical examinations and rehabilitation, as well as lifestyle, education and work, and sports.

2.2 Participants

Participants consisted of adults aged 19 to 39 years with CP. Participants included patients from twenty-seven medical centers and facilities of different sizes and located in different areas across Japan. The medical centers and facilities covered both rural and urban areas. Survey packets were sent to these centers and facilities, and the questionnaires, together with a letter containing information about the study, were distributed by physicians, nurses, physical therapists or medical social workers to people with cerebral palsy or their parents by hand or mail. The questionnaires were returned to each center or facility by hand or mail. The study protocol was approved by the ethics committee of each medical center and facility, and informed consent was obtained from all participants.

2.3 Questionnaire

The questionnaire is a self and/or proxy report measure developed for the Health Survey of Adult Patients with Cerebral Palsy. In this study, seven items covered patient background: age, sex, education, GMFCS level, respondent, possession or not of a nursing notebook, and surgical history.

The GMFCS provides clinicians with an alternate method of classifying motor function in people with CP (Palisano et al., 1997; Palisano et al., 2008). The five levels of the classification represent meaningful distinctions in motor function and are based on self-initiated movement. Our study included adults with CP classified from level I to IV who were able to move in their daily environment. Exclusion criteria were adults with GMFCS level V who were unable to demonstrate any functional mobility. In the current study, we used the Japanese translation of the GMFCS, which has been found to have good test-retest reliability and evidence of content validity (Kondo et al., 2003; Kondo, Teranishi, Iwata, Sonoda, & Saitoh, 2009). In this study, the highest GMFCS level attained in each participant’s life was employed.

In Japan, a nursing notebook is issued to those with intellectual disabilities as certification to make it easier for them to access various welfare services. Having this certificate demonstrates that the individual has an intellectual disability.

Participants provided the age at which they had peak mobility function in response to the item; “Please tell me the age that you had highest mobility function. If you have highest mobility function now, please write your present age.”

The age at mobility decline was obtained in response to the item; “Have you experienced mobility decline? If you have, when did you experience it? If you have not experienced mobility decline, please choose the appropriate options”; “Early teens (before graduating junior high school)”, “Late teens (after graduating junior high school)”, “Twenties”, “Thirties”, “Has remained the same” and “Has improved”.

The participants were asked to describe any causes they thought contributed to a decline in mobility. The descriptions obtained were coded under categories such as change in physique (weight gain and increased height), work, change in environment (transition, graduation, change in lifestyle, divorce and moving), reduced rehabilitation, stress and psychological problems, illness and injury, stiffness and deformity, pain, reduced muscle strength and cardiorespiratory function, reduced physical activity, aging, change in mobility tools and falls.

2.4 Statistical analyses

The differences in age at peak mobility function among GMFCS levels were analyzed by the Kruskal-Wallis test. For a post-hoc test, the Mann-Whitney U test with Bonferroni correction was used. Kaplan-Meier method with corresponding log-rank tests for comparison of different GMFCS levels were used to explore the age at which a decline in mobility was reported. Cox proportional hazards models were used to compare the risk of mobility decline among GMFCS levels. Models were adjusted for age, sex, respondent, possession or not of a nursing notebook, and surgical history. Hazard ratios (HRs) and 95% confidence intervals (CIs) were provided. Differences in the causes of mobility decline among GMFCS levels were analyzed using Pearson chi-square or Fisher exact tests. Data were analyzed using IBM SPSS Statistics ver. 24. The significance level was set at p < 0.05.

No outside funding was obtained for the performance of this study.

3 Results

Of the eight hundred and sixty responses obtained from 673 (78.3%) adults with CP, those with GMFCS level V (n = 197) or with no response for GMFCS level (n = 90) were excluded. 386 adults with CP, consisting of 213 males and 172 females (sex was unknown for 1 respondent) were analyzed. Table 1 shows the distribution of participants by GMFCS level: level I (n = 53), level II (n = 139), level III (n = 74), and level IV (n = 120). The mean age of participants was 26 years 8 months (SD 5 years 10 months; range 19–39 years). Fifty-five percent of the respondents completed the questionnaire themselves, 39% of the participants had a Nursing notebook, and 54% of the participants had a history of surgery.

Table 1
Characteristics, age at peak mobility function and change in mobility function in adults with cerebral palsy by Gross Motor Function Classification System level

GMFCS

Total (n = 386) Level I (n = 53) Level II (n = 139) Level III (n = 74) Level IV (n = 120)

Age, mean (SD) 26y8 m (5y10 m) 27y4 m (5y9 m) 26y3 m (6y1 m) 26y2 m (5y6 m) 27y1 m (5y10 m)

Sex

Male 213 34 72 45 62

Female 172 19 67 29 57

No answer 1 0 0 0 1

Respondent

Oneself 214 36 87 36 55

Family 150 14 45 32 59

Care-giver 14 3 3 4 4

Other 8 0 4 2 2

No answer 1 0 1 0 0

Education

Primary (9y) 2 1 0 0 1

Secondary (12y) 299 31 98 64 106

Tertiary (>12y) 76 20 38 8 10

No answer 9 1 3 2 3

Nursing notebook

Yes 150 20 48 30 52

No 219 31 85 42 61

No answer 17 2 6 2 7

Surgery

Yes 210 24 84 41 61

No 158 27 51 27 53

No answer 18 2 4 6 6

Age at peak mobility function, 17.00 19.00 17.00 12.50 18.00

median (interquartile range) (12.00 to 20.00) (16.00 to 24.75) (13.00 to 20.00) (10.00 to 17.00) (12.00 to 20.25)

Mobility function

Has decreased

Early teens 45 4 11 17 13

Late teens 61 6 21 19 15

Twenties 93 14 37 16 26

Thirties 24 1 8 4 11

Has remained same 117 23 46 13 35

Has improved 12 1 8 1 2

No answer 34 4 8 4 18

		GMFCS
Age, mean (SD)	26y8 m (5y10 m)	27y4 m (5y9 m)	26y3 m (6y1 m)	26y2 m (5y6 m)	27y1 m (5y10 m)
Sex
Male	213	34	72	45	62
Female	172	19	67	29	57
No answer	1	0	0	0	1
Respondent
Oneself	214	36	87	36	55
Family	150	14	45	32	59
Care-giver	14	3	3	4	4
Other	8	0	4	2	2
No answer	1	0	1	0	0
Education
Primary (9y)	2	1	0	0	1
Secondary (12y)	299	31	98	64	106
Tertiary (>12y)	76	20	38	8	10
No answer	9	1	3	2	3
Nursing notebook
Yes	150	20	48	30	52
No	219	31	85	42	61
No answer	17	2	6	2	7
Surgery
Yes	210	24	84	41	61
No	158	27	51	27	53
No answer	18	2	4	6	6
Age at peak mobility function,	17.00	19.00	17.00	12.50	18.00
median (interquartile range)	(12.00 to 20.00)	(16.00 to 24.75)	(13.00 to 20.00)	(10.00 to 17.00)	(12.00 to 20.25)
Mobility function
Has decreased
Early teens	45	4	11	17	13
Late teens	61	6	21	19	15
Twenties	93	14	37	16	26
Thirties	24	1	8	4	11
Has remained same	117	23	46	13	35
Has improved	12	1	8	1	2
No answer	34	4	8	4	18

GMFCS, Gross Motor Function Classification System.

The median age of peak mobility function was 19 years in GMFCS level I, 17 years in GMFCS level II, 12.5 years in GMFCS level III and 18 years in GMFCS level IV (Table 1 and Fig. 1). The peak mobility function for GMFCS level III participants was younger than that for GMFCS level I, II or IV (p < 0.001), while that for GMFCS level II participants was younger than that for GMFCS level I (p = 0.003). No significant differences were found among GMFCS level I and IV, and II and IV.

Fig.1

Comparison of age at peak mobility function by Gross Motor Function Classification System level. GMFCS, Gross Motor Function Classification System.

Fifty-eight percent of the participants reported a decline in mobility: 47.2% in GMFCS level I, 55.4% in level II, 75.7% in level III, and 54.2% in level IV, respectively (Table 1). A Kaplan-Meier plot of the time to mobility decline by GMFCS level is shown in Fig. 2. The risk of mobility decline was higher in GMFCS level III than in level I, II and IV (p < 0.001). No significant differences were found among GMFCS level I, II and IV. Cox proportional hazard analysis showed that the risk of mobility decline in GMFCS level III was 1.97 (95% CI, 1.20–3.23) compared with level I (Table 2). No significant differences were found among GMFCS level I and II, and I and IV.

Fig.2

Kaplan-Meier survival function for adults with cerebral palsy not experiencing a decline in mobility by Gross Motor Function Classification System level. GMFCS level I vs. level II: log-rank test, p = 0.420; GMFCS level I vs. level III: log-rank test, p < 0.001; GMFCS level I vs. level IV: log-rank test, p = 0.514; GMFCS level II vs. level III: log-rank test, p < 0.001; GMFCS level II vs. level IV: log-rank test, p = 0.859; GMFCS level III vs. level IV: log-rank test, p < 0.001; GMFCS, Gross Motor Function Classification System.

Table 2

Univariate and multivariate analysis of hazard ratios for mobility decline by Gross Motor Function Classification System level

	Univariate analysis			Multivariate analysis^a
	HR	95% CI	p	HR	95% CI	p
GMFCS
Level I	ref			ref
Level II	1.164	0.742–1.828	0.509	1.165	0.730–1.858	0.522
Level III	2.029	1.266–3.254	0.003	1.972	1.203–3.234	0.007
Level IV	1.146	0.730–1.825	0.566	1.105	0.678–1.800	0.690

^aMultivariate analyses were adjusted for age, sex, respondent, Nursing notebook and surgery. HR, hazard ratio; CI, confidence interval; GMFCS, Gross Motor Function Classification System.

The 147 participants (65.9%) reporting a decline in mobility gave a total of 201 causes (Table 3): 30 (20.4%) regarded the mobility decline to be the result of reduced physical activity, 28 (19.0%) the result of a change in physique, 24 (16.3%) the result of a change in environment and stiffness and deformity, 21 (14.3%) the result of illness and injury, 17 (11.6%) the result of reduced rehabilitation, while pain and reduced muscle strength and cardiorespiratory function were reported by 12 participants (8.2%), and work was reported by 11 participants (7.5%). Change in environment (p = 0.030), and illness and injury (p = 0.001) were more frequently reported among GMFCS level III participants than among those in other levels. Stiffness and deformity was more frequently reported in GMFCS level IV (p = 0.023), reduced physical activity in level II and III (p = 0.004), and falls in level II (p = 0.029).

4 Discussion

This study shows the change in mobility function and its causes in people with CP by GMFCS level. This information is important for planning future intervention for person with CP in consideration of their GMFCS level and age.

In this study, fifty-eight percent of participants had experienced a decline in mobility. Andersson et al. found that 35% of participants reported that their walking ability had decreased (Andersson & Mattsson, 2001), Bottos et al. reported a similar loss in walking ability during adulthood (Bottos et al., 2001), Jahnsen et al. documented that 44% reported deterioration in locomotio n (Jahnsen, Villien, Egeland, et al., 2004), and Opheim found that 42% of participants reported deterioration in walking function (Opheim et al., 2009). Many participants in these previous studies may have had higher gross motor function than those in our study. In Andersson’s study (Andersson & Mattsson, 2001), 49% of participants were able to walk without walking aids. In Bottos’s study (Bottos et al., 2001), 41.4% of participants moved by independent walking. In Jahnsen’s study (Jahnsen, Villien, Egeland, et al., 2004), 53% of participants were able to walk without support and, in Opheim’s study (Opheim et al., 2009), 46% of participants were GMFCS level I. In our study, only 13.7% participants were GMFCS level I who could move without restriction and had limitations only in advanced skills. Furthermore, in the previous studies, the questionnaire on mobility decline concerned ‘walking ability’, while our study asked about ‘mobility function’. Mobility function may include higher-level functions (e.g., climbing stairs, running or jumping) and high-level mobility function deteriorates more easily. These various differences may have contributed to our results.

Table 3

Self-reported cause of mobility decline

	GMFCS
	Total* (n = 201)	Level I (n = 13)	Level II (n = 75)	Level III (n = 55)	Level IV (n = 58)	p
Change in Physique	28	0	8	8	12	0.062
Work	11	2	5	2	2	0.788
Change in environment	24	2	5	10	7	0.030
Reduced rehabilitation	17	2	6	4	5	0.970
Stress and psychological problems	5	0	4	0	1	0.204
Illness and injury	21	0	5	11	5	0.001
Stiffness and deformity	24	1	5	4	14	0.023
Pain	12	1	8	1	2	0.166
Reduced muscle strength and cardiorespiratory function	12	3	3	3	3	0.587
Reduced physical activity	30	1	16	10	3	0.004
Aging	4	1	2	1	0	0.589
Change in mobility tools	8	0	3	1	4	0.521
Falls	5	0	5	0	0	0.029

*Total contains repetitions (147 participants described total 201 causes of mobility decline). GMFCS, Gross Motor Function Classification System.

No significant differences were found in the Kaplan-Meier plot of the time to mobility decline among GMFCS level I, II and IV. For those in GMFCS level I and II, differences in age at mobility decline may be seen at over forty years, as shown in a previous study (Opheim et al., 2009). Further long-term study concerning GMFCS level I and II is necessary. For people in GMFCS level IV, mobility function probably includes rolling and crawling. Such mobility functions can be maintained and do not deteriorate as easily as high-level functions. Rolling and crawling are indoor mobility functions. Palisano et al. shows that age and environmental setting influence the method of mobility of individuals with CP (R. J. Palisano, Hanna, Rosenbaum, & Tieman, 2010). Therefore, this is a limitation of our study. Further study taking into consideration the environment setting is needed.

Although GMFCS level I, II and IV participants experienced their peak mobility function in their late teens, they also experienced a decline in mobility in their twenties to thirties. On the other hand, many GMFCS level III participants had their peak mobility function in their early teens and experienced a decline in mobility in their late teens. Furthermore, GMFCS level III participants have a two times higher risk of mobility decline than level I participants. To our knowledge, this is the first report on the risk of mobility decline by GMFCS level. People classified as GMFCS level III demonstrated variations in mobility method in all environmental settings (Graham, Harvey, Rodda, Nattrass, & Pirpiris, 2004; Palisano et al., 2010). People in GMFCS level III may experience mobility acquisition, and maintain or experience a decline in mobility in a different manner to GMFCS level I, II and IV participants, and they may not able to maintain their peak mobility function for a long period of time. This information is important for intervention planning based on different approaches by GMFCS level.

The most common self-reported causes of mobility decline were reduced physical activity and change in environment. In their free descriptions, participants reported that reduced physical activity and having rehabilitation accompanied change in environment, especially when they transitioned out of the school system. Within the Japanese health care system, the opportunity for exercise and rehabilitation is reduced after leaving high school. Youths typically change from structured high school environments to more complex college or work environments, and work toward establishing independence from their parents. It is important to support individuals undertaking a change in environment carefully for the prevention of mobility decline, especially in GMFCS level II and III individuals. Change in physique, stiffness and deformity, and illness and injury were also frequently reported causes. Weight gain and increased height, which are typical in adolescence, may cause mobility decline. For GMFCS level III individuals, illness and injury were significantly more frequently reported as the causes of the decline in mobility function. These results suggest that hospitalization and rest may be the cause of mobility decline in those with limited mobility function. However, in this study, there was a lack of responses regarding the cause of mobility decline, especially among GMFCS level I participants. Further clinical studies are, therefore, needed to investigate potential causal pathways of the early mobility decline in persons with CP.

There are several limitations to this study. Firstly, experiences are dependent on memory and may be biased. Events that happened a long time ago, such as the age at which a decline in mobility occurred, may be forgotten or misremembered. Minor losses of function may have been neglected or become an unconscious habit. Although we asked the cause of mobility decline in the questionnaire, the cross-sectional design of our study limited our ability to describe strict causal relationships and clarify the decline in mobility function was it happened all of the sudden or over a long time. Also there was quite a large amount of missing data; therefore, we were not able to account for this in the analyses, and results should be interpreted with caution. Future longitudinal prospective study is necessary to clarify the causal relationship concerning changes in mobility function.

The major finding from this study was that fifty-eight percent of adults with CP reported a decline in mobility. GMFCS level III participants showed a peak mobility function and experienced a decline in mobility at a younger age than did GMFCS level I, II and IV participants, and they have two times higher risk of mobility decline than those level I participants. Participants reported that the causes of mobility decline were reduced physical activity, change in physique, change in environment, stiffness and deformity, illness and injury, and reduced rehabilitation. These causes of mobility decline differed by GMFCS level. However, this questionnaire study may have potential recall bias and it is important that the longitudinal measurement of mobility function is performed prospectively.

Conflict of interest

The authors declare no potential conflicts of interest with respect to the authorship and/or publication of this article.

Funding

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Footnotes

Acknowledgments

We extend our special thanks to all participants who gave us their time to answer the questionnaire and provide us with much useful information.

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		GMFCS
	Total (n = 386)	Level I (n = 53)	Level II (n = 139)	Level III (n = 74)	Level IV (n = 120)
Age, mean (SD)	26y8 m (5y10 m)	27y4 m (5y9 m)	26y3 m (6y1 m)	26y2 m (5y6 m)	27y1 m (5y10 m)
Sex
Male	213	34	72	45	62
Female	172	19	67	29	57
No answer	1	0	0	0	1
Respondent
Oneself	214	36	87	36	55
Family	150	14	45	32	59
Care-giver	14	3	3	4	4
Other	8	0	4	2	2
No answer	1	0	1	0	0
Education
Primary (9y)	2	1	0	0	1
Secondary (12y)	299	31	98	64	106
Tertiary (>12y)	76	20	38	8	10
No answer	9	1	3	2	3
Nursing notebook
Yes	150	20	48	30	52
No	219	31	85	42	61
No answer	17	2	6	2	7
Surgery
Yes	210	24	84	41	61
No	158	27	51	27	53
No answer	18	2	4	6	6
Age at peak mobility function,	17.00	19.00	17.00	12.50	18.00
median (interquartile range)	(12.00 to 20.00)	(16.00 to 24.75)	(13.00 to 20.00)	(10.00 to 17.00)	(12.00 to 20.25)
Mobility function
Has decreased
Early teens	45	4	11	17	13
Late teens	61	6	21	19	15
Twenties	93	14	37	16	26
Thirties	24	1	8	4	11
Has remained same	117	23	46	13	35
Has improved	12	1	8	1	2
No answer	34	4	8	4	18