Opheim, Arve,P.T., M.S.C., Jahnsen, Reidun,P.T., P.H.D., Olsson, Elisabeth,P.T., P.H.D., & Stanghelle, Johan K,M.D., P.H.D. (2009). Walking function, pain, and fatigue in adults with cerebral palsy: A 7-year follow-up study. Developmental Medicine and Child Neurology, 51(5), 381-8. -
A multidimensional questionnaire was mailed to 226 people with unilateral (hemiplegic) or bilateral (diplegic) spastic CP who had participated in a 1999 survey. People with additional diagnoses were excluded. Special emphasis was placed on participants with deterioration in walking. The questionnaire was the same as in 1999. One hundred and forty-nine participants (76 males, 73 females with a diagnosis of unilateral or bilateral) spastic CP responded. Fifty-two per cent of all participants reported deterioration in walking function since debut of walking, compared with 39% 7 years previously. In participants with bilateral CP, 71% reported deteriorated walking; compared with 37% of participants with unilateral CP. Participants with deteriorated walking function had greater pain frequency, pain intensity, impact of pain on daily activities, and physical fatigue and reduced balance. The number of people reporting overall mobility problems was almost double compared with 7 years previously.
The main finding was an increased prevalence of deteriorated walking, significantly associated with bilateral spastic CP, pain, fatigue, and reduced balance. Comprehensive rehabilitation programs addressing these areas are needed.
Article:
Walking function, pain, and fatigue in adults with cerebral palsy: a 7-year follow-up studyAuthor: Opheim, Arve, PT, MSC; Jahnsen, Reidun, PT, PHD; Olsson, Elisabeth, PT, PHD; Stanghelle, Johan K, MD, PHDAbstract:To compare walking function, pain, and fatigue in adults with cerebral palsy (CP) 7 years after an initial survey.A multidimensional questionnaire was mailed to 226 people with unilateral (hemiplegic) or bilateral (diplegic) spastic CP who had participated in a 1999 survey. People with additional diagnoses were excluded. Special emphasis was placed on participants with deterioration in walking. The questionnaire was the same as in 1999.One hundred and forty-nine participants (76 males, 73 females; mean age 40y 5mo, SD 10y 7mo, range 24-76y) with a diagnosis of unilateral (n=81) or bilateral (n=68) spastic CP responded. Fifty-two per cent of all participants reported deterioration in walking function since debut of walking, compared with 39% 7 years previously. In participants with bilateral CP, 71% reported deteriorated walking, compared with 37% of participants with unilateral CP. Participants with deteriorated walking function had greater pain frequency, pain intensity, impact of pain on daily activities, and physical fatigue and reduced balance. The number of people reporting overall mobility problems was almost double compared with 7 years previously.The main finding was an increased prevalence of deteriorated walking, significantly associated with bilateral spastic CP, pain, fatigue, and reduced balance. Rehabilitation programmes addressing these areas are needed.Full text:A new definition of cerebral palsy (CP) has recently been adopted, which is: 'a group of permanent disorders of the development of movement and posture, causing activity limitation, that are attributed to non-progressive disturbances that occurred in the developing fetal or infant brain. The motor disorders of cerebral palsy are often accompanied by disturbances of sensation, perception, cognition, communication, and behaviour, by epilepsy, and by secondary musculoskeletal problems'.1 The disturbances of motor control are often accompanied by problems in body structure and function, such as abnormal muscle tone and coordination, contractures, and deformities. Activity limitations, such as locomotion problems,2 and participation restrictions, such as reduced employment, are also seen.HeadnoteAIM To compare walking function, pain, and fatigue in adults with cerebral palsy (CP) 7 years after an initial survey.
METHOD A multidimensional questionnaire was mailed to 226 people with unilateral (hémiplégie) or bilateral (diplegie) spastic CP who had participated in a 1999 survey. People with additional diagnoses were excluded. Special emphasis was placed on participants with deterioration in walking. The questionnaire was the same as in 1999.
RESULTS One hundred and forty-nine participants (76 males, 73 females; mean age 4Oy 5mo, SD 10y 7mo, range 24-76y) with a diagnosis of unilateral (n=81) or bilateral (n=68) spastic CP responded. Fifty-two per cent of all participants reported deterioration in walking function since debut of walking, compared with 39% 7 years previously. In participants with bilateral CP, 71% reported deteriorated walking, compared with 37% of participants with unilateral CP. Participants with deteriorated walking function had greater pain frequency, pain intensity, impact of pain on daily activities, and physical fatigue and reduced balance. The number of people reporting overall mobility problems was almost double compared with 7 years previously.
INTERPRETATION The main finding was an increased prevalence of deteriorated walking, significantly associated with bilateral spastic CP, pain, fatigue, and reduced balance. Rehabilitation programmes addressing these areas are needed.
ABBREVIATION
SF-36 General Health Survey Short Form 36
Extensive research has been conducted in the paediatric CP population. In the adult population, however, there are relatively few studies and most of these are cross-sectional and not follow-up studies.2-7 Many are hospital- rather than population-based. Murphy et al.3 included a large proportion of people with dyskinesia and quadriplegia, but only 20% with hemiplegia and diplegia, and Turk et al.4 studied only women. The studies by Bottos et al.,6 Andersson and Mattsson,2 and Jahnsen5 are rehabilitation-based, meaning that the recruited participants had been in contact with habilitation and rehabilitation services; these studies have proportionally higher numbers of people with diplegia and hemiplegia, which reflects the known distribution of the subtypes Ln the population with CP.8
Deterioration in walking and overall functional mobility in adulthood is described in several studies.2^1'6'9 In the study by Jahnsen et al.,9 45% of the respondents reported deteriorated walking function and, of these, 70% reported that this had happened before the age of 35 years. Selfreported causes of deterioration in walking function included musculoskeletal pain, fatigue, and lack of physical activity. Andersson and Mattsson2 found that 35% of the respondents reported deterioration in walking, which had happened before the age of 35 years in 63 % of these.
Several authors have hypothesized about the causes of the deterioration in walking. Proposed causes include abnormal biomechanical forces in muscles and joints, leading to excessive stress, strain, and overuse syndromes,3 and an imbalance between physiological resources and demands. Adults with CP have reported increasing pain,11'12 fatigue,13 reduced overall functioning in everyday activities, and reduced social integration and participation in work and sports activities.7
The course of and changes in walking function, pain, and fatigue with increasing age in adults with CP has not been sufficiently investigated. In a continuing effort to learn more about the consequences of living with this lifelong disability, there is a need for longitudinal and intervention studies.
The aim of the present study was to compare the results from a survey by Jahnsen5 with data from the same participants 7 years later. Special emphasis was placed on walking function, pain, and fatigue in participants with unilateral (hémiplégie) or bilateral (diplegie) spastic CP. The prevalence of pain and fatigue in those who reported deterioration in walking was also studied.
METHOD
Participants
In the autumn of 2006 we followed up a subgroup of participants from a survey of the health status of adults with CP in Norway conducted in 1999.5 We used the diagnostic classification system from the Surveillance of Cerebral Palsy in Europe,14 in which CP is classified as spastic, dyskinetic, or ataxic, and spastic CP is further classified as unilateral or bilateral.
Inclusion criteria in the present study were unilateral (hémiplégie) or bilateral (diplegie) spastic CP at Gross Motor Function Classification System (GMFCS) levels I to IV,15 and currently or previously able to walk indoors with or without support. Exclusion criteria were dyskinetic, ataxic, or bilateral CP at GMFCS levels IV or V and inability to walk indoors with support, and documented intellectual disabilities.
The same questionnaire was used as in 1999.5 It was sent by mail, and a written reminder was sent after approximately 3 weeks. The answers were coded and entered into the Statistical Package for Social Sciences, version 14.0 (SPSS Inc., Chicago, IL, USA). The questionnaire contained reliable and validated scales on walking function, pain, and fatigue. Additional questions on fatigue were asked.
Walking function
GMFCS levels in 2006 were obtained through self-reporting, which has excellent agreement with professional ratings.16 In 1999, the GMFCS levels were scored professionally post hoc, on the basis of the available information on walking function. Perceived changes in walking function since walking debut were graded as better, unchanged, or deteriorated. Participants also reported the age at which the change in walking function occurred. This was given in 5-year intervals (e.g. 20-2 4y, 25-29y). Characteristics of the changes in walking were expressed as alternatives, such as improved or deteriorated balance, increased or reduced muscle strength, increased or reduced cardiorespiratory fitness, and faster or slower walking speed. Overall mobility in work and leisure time was expressed as no movement problems, difficulties in moving, or not able to move at all when required.
Musculoskeletal pain
The number of pain sites was reported with checkboxes for eight body parts, and pain frequency was reported as never, seldom, monthly, weekly, or daily. Daily pain for more than 1 year was considered chronic, and the prevalence was compared with that of the general population in Norway.17 The generic health-related quality of life instrument, Short Form 36 (SF-36) domain 'bodily pain' was used to measure the combination of pain intensity and the impact of pain on work and activities of daily life. The SF-36 uses a 0-100 scale, where 0 represents the greatest and 100 the least impact of pain on daily Ufe and health.18 The results were compared with normative data from the Norwegian general population,19 which has an age distribution containing more elderly people than the present study. Pain intensity during the last month was assessed with a 100mm visual analogue scale, with the anchor points 'no pain' and 'worst possible pain'.20 This type of scale is frequently used in pain studies, but to our knowledge it has not been validated in people with CP.
Fatigue
The experience of feeling exhausted, tired, weak, or lacking energy21 was measured using two scales, the Fatigue Questionnaire22 and the Fatigue Severity Scale.23 The former was used in the original study and has a population-based norm, thus allowing comparisons.24 The age distribution in the reference material for the Fatigue Questionnaire is the same as for the SF-36. Chronic fatigue was considered according to Loge et al.24 The Fatigue Severity Scale was added because it does not require the respondents to compare fatigue status retrospectively and it explores the agreement with different expressions related to the impact of fatigue. The Fatigue Severity Scale has been translated and validated in the Norwegian population and has population-based norms.25
Statistics
Descriptive data were given as means and SDs for normally distributed continuous data and as medians and 25th to 75th centiles for ordinal or skewed data. Prevalence estimates are presented as percentages and 95% confidence intervals (CI). Parametric methods (f-tests) were used for continuous data with a normal distribution, and non-parametric methods were used for ordinal variables and variables with a skewed distribution. The non-parametric methods included the Mann-Whitney U test for comparison of independent groups and the Wilcoxon signed rank test for paired data. Pearson's χ^sup 2^ test was used for comparison of independent groups of categorical data, and die McNemar test for paired categorical data. Kaplan-Meier statistics with corresponding log-rank tests for comparison of different CP diagnoses were used to explore the age at which a deterioration in walking function was reported. GraphPad calculators (GraphPad Software Inc., La Jolla, CA, USA) were used for norm-based comparisons with the SF-36, Fatigue Questionnaire, and Fatigue Severity Scale.
Approval for the study was obtained from the regional ethics committee in soudi-eastern Norway and from the Commissioner for the Protection of Privacy in Research. All participants gave written informed consent.
RESULTS
Of the 288 people with unilateral or bilateral CP who participated in the original study,9 62 could not be reached, had died, or had said no to further studies, resulting in 226 people eligible for the follow-up study. Of these, 73 were non-responders, and four were excluded because of selfreported additional diagnoses like multiple sclerosis (w=3) and psoriatic arthritis (w=l). Thus, 149 people (66% of the eligible and 52% of the original participants) were included in the present study. A non-responder analysis was conducted, including all of the participants with uni- or bilateral spastic CP in the 1999 survey, except those who were dead, had never walked, or were excluded. There was no difference between respondents and non-respondents in age, sex, or diagnosis. A larger proportion of people at GMFCS level ? and a lower proportion of those at level TJI were found in the respondents (χ^sup 2^=7.6, df=3, p=0.055). Participants' demographic and diagnostic characteristics are presented in Table I. Compared with the original study, the present study included a slightly larger proportion of people with bilateral CP at GMFCS levels I and ?, and of people with a higher education level.
Walking function
In the whole group of 149 participants, 16% reported improved, 31% unchanged, and 52% deteriorated walking since dieir walking debut The prevalence of deterioration increased from 39% in 1999. In people with bilateral CP, 71% reported deteriorated walking compared with 37% in unilateral CP. Of me 89 people who reported unchanged or improved walking in 1999, walking had deteriorated in 29 (33%) in 2006, whereas 1 1 (19%) of those with a deteriorated walking in 1999 (»=58) reported improved or unchanged walking in 2006 (p<0.001).
The GMFCS levels of unilateral and bilateral CP of respondents in 1999 and 2006 are presented in Table ?. There were frequent shifts between levels I and ? and vice versa. Forty-three per cent of those at level ? in 1999 had shifted to level I in 2006, and 26% had shifted in the opposite direction. In addition to the shifts between levels I and ?, three people, all with unilateral CP, shifted across two levels, and 15 people shifted across one level towards a reduced function. Nine of the 10 people who shifted from level HI to level IV had bilateral CP. Two people shifted from level HI to level ?: one was using crutches after an accident in 1999, and the other was walking without aids but also using a wheelchair. The change from level IV to level ? in one person is probably due to an error from 1999 (Table ?).
The age when changes in walking function had occurred was reported by 105 people, of whom 75 reported a deterioration. A Kaplan-Meier plot of the time to walking deterioration in the unilateral and bilateral groups is shown in Figure 1. The plot displays a marked group difference around the age of 35 years. The Kaplan-Meier estimate of the median age of walking deterioration was 52 years in unilateral CP (95% CI 34-70) and 37 years in bilateral CP (95% CI 34-39; log rank χ^sup 2^=7.8, df=l,/>=0.005).
In the youngest age group in 1999 (S25y), diree out of 31 people experienced deterioration in walking between 1999 and 2006.
Of those who reported improved or unchanged walking in 2006 (w=71), 26 participants (37%) regarded the improvement as a result of improved balance, 20 participants (28%) a result of increased muscle strength, and 14 participants (20%) a result of improved cardiorespiratory fitness. Of those who reported deteriorated walking in 2006 (n=78), 51 (65%) regarded the deterioration as a result of impaired balance, 26 (33%) a result of reduced muscle strengm, and 22 (28%) a result of bodi reduced cardiorespiratory fitness and reduced walking speed. Spasms, stiffness, 'wear and tear', pain, and reduced training were reported by 19 participants (24%). The number of people with problems of overall mobility increased from 20 (13%) in 1999 to 37 (25%) in 2006 (mean difference 12%, 95% CI 5-19%,p=0.001).
Subgroup analysis showed that the group with improved or unchanged walking in 2006 had a higher proportion of participants at GMFCS level I, whereas the group reporting deteriorated walking were at higher GMFCS levels (χ^sup 2^=36.8, df=4,p<0.001; Table IH).
Pain
Musculoskeletal pain scores showed that the prevalence of daily pain increased from 23% in 1999 to 3 1% in the present survey (mean difference 8%, 95% CI 1-14%, /»=0.027). The proportion of people reporting 'seldom' or 'no' pain was reduced from 52 to 41% (mean difference 11%, 95% CI 4-19%, p=0.004). The number of people reporting pain from one or more sites increased non-significandy from 1 17 (79%) to 123 (83%, 95% CI 76-88%), and the median number of pain sites was unchanged at 3 (25di to 75th ceñidles 2-5). The most common pain sites were back, neck, and feet; of those reporting pain, 67, 51, and 50% respectively, reported it at these sites. Median pain frequency increased between 1999 and 2006 from 'seldom' to 'monthly' (z=- 3.1, p=0.002), whereas mean pain intensity on the visual analogue scale and die prevalence of chronic pain were unchanged, from 20 to 24% (95% CI 17-31%, P=OAS). The median score in the SF-36 domain 'bodily pain' changed significandy in a negative direction from 62 (25th to 75th centiles 41-100) to 61 (41-84; z^3.47, p=0.001).
As in the study by Jahnsen et al.,11 scores in the SF-36 domain 'bodily pain' were significantly lower dian in die Norwegian general population, except for the men in 1999 (p<0.001).19 The prevalence of chronic pain was higher in the CP population than in the general population at 24 and 15% respectively (mean difference 9%, 95% CI 2-16%, i=2.6, df=148,p=0.01).
Subgroup analysis of the participants in 2006 showed that those who reported deterioration in walking function also reported significandy increased pain frequency, more pain sites, higher pain intensity, and more impact of pain on daily life and activities (Table IH).
Fatigue
Fatigue scores showed no change in the physical or mental fatigue subscales between 1999 and 2006. As in 1999,13 on the Fatigue Questionnaire, the mean score for the physical domain (9.2 [SD 3.3]) and total score (13.5 [4.5]) were significandy higher than in the general population (7.9 [3.1] and 12.2 [4.0] respectively, t=4.9 and 3.8, df=2432, p<0.001); there was no difference in the Fatigue Questionnaire mental subscale. The proportion of participants with chronic fatigue was significandy higher in the population with CP than in the general population (22%, 95% CI 15-29%, vs 11%, t=3.3, df=148, p=0.001).24 The Fatigue Severity Scale scores were also significandy higher dian in the general population (4.4 [1.4] vs 4.0 [1.3], mean difference 0.4, 95% CI 0.18-0.62, t=3.5, df=2002, p<0.001).25
Subgroup analysis of the participants in 2006 showed that the Fatigue Questionnaire physical subscale and the Fatigue Severity Scale scores were significandy higher in the group with deteriorated walking, whereas the improved or unchanged group had similar fatigue scores to those of the general population. There was no group difference in the mental fatigue score (Table III).
DISCUSSION
The major finding in the present study was that adults with CP experience a continuous deterioration in walking function. The prevalence of this problem increased among the respondents from 39% in 1999 to 52% in 2006 and was most common among participants with bilateral CP. This deterioration was associated with increased pain frequency and intensity, more pain sites, a higher impact of pain on daily life, and physical fatigue. There was an almost doubling of participants reporting problems of overall mobility between 1999 and 2006. Andersson and Mattsson2 found a somewhat lower prevalence of deteriorated walking ability (35%) in a population with CP that was 4 years younger than those in this study.
The present study indicates that people with bilateral CP at GMFCS level III have a higher risk of deterioration in walking dian those with bilateral CP and milder impairments or those with unilateral CP with mild or moderate impairments. A reason for this might be overuse, as the people at GMFCS level LTJ might be overusing their resources in order to have a walking function that meets social expectations (e.g. the ability to cross the road on the green light or to walk together with non-disabled peers). However, other important environmental factors, such as access to social services, home-based rehabilitation, and physical training, in addition to body functions such as pain, fatigue, and reduced balance, all contribute to the deterioration in walking. Some of the shifting in GMFCS levels can be a result of this deterioration, but it can also be a matter of choice, as some people might start using a wheelchair for energy conservation over longer distances.
In the youngest age group (<25y in 1999), 10% experienced deterioration since 1999. This is a serious problem, as they have a long life ahead of them.
The most frequendy reported characteristic of deteriorated walking was reduced balance. Balance is an important part of walking function, and impaired balance has been found in children with CP.26 The present study points to a relationship between deteriorated walking and reduced balance; further studies on postural control and balance in adults with CP are needed to investigate this relationship. This result also indicates that balance needs to be a specific focus in the follow-up of people with CP from an early age.
The near doubling of people reporting problems of overall mobility might have been caused by difficulties with public accessibility and transportation, and the availability of assistance. In the light of political efforts towards participation possibilities for all, these results are discouraging and show the need for increased efforts in this area.
There was no change in the experience of fatigue between 1999 and 2006. This is rather surprising but may be explained by the already high levels of physical fatigue13 compared with the general population.24 The facts that there was no difference in the Fatigue Questionnaire mental scale compared with the general population, and that those who reported deteriorated walking had significandy higher physical fatigue scores dian the general population, whereas the group without deteriorated walking reported the same fatigue level, indicate that the fatigue experienced in CP is mainly of physical origin. It is possibly caused by both overuse and reduced physical fitness. The reference material for both the Fatigue Questionnaire and the SF-36 has an older age distribution than the people in this study. As bodi 'bodily pain' and fatigue scores increase with age, this suggests even larger differences from the reference material if data had been age-corrected.
The number of pain sites and pain intensity on the visual analogue scale did not change from 1999 to 2006, but pain frequency and impact of pain on daily life increased. The relatively unchanged pain intensity and number of pain sites agree with a previous study.12 The more often pain is experienced, the more it may interfere with daily activities. This might be the reason for the increased impact of pain on daily activities that was found in the SF-36 bodily pain domain. Those who reported deteriorated walking had significandy higher pain scores on all scales dian those without deterioration. Pain management is therefore an important element to consider when aiming at preserving walking function in adults with CP.
Methodological considerations
The non-respondent analysis showed no major difference between the respondents and the non-respondents. Although the questionnaire was sent to all reachable participants from me 1999 survey who had bilateral or unilateral CP and were able to walk or had been walking, it seems that those with a relatively stable walking function and who were still walking were more likely to respond. The original study5 attempted to reach all people with CP in Norway, using all available registers in rehabilitation hospitals and from patient organizations, but it had relatively few representatives from older age groups. Two different mediods of obtaining GMFCS levels can to some extent explain the relatively large shifts between levels I and JJ and vice versa, probably because these levels are relatively close to each other, compared with the other levels.
CONCLUSION
The main finding in the present study was an increased prevalence of deteriorated walking function among adults with CP, associated with higher levels of pain, fatigue, and reduced balance. There was a near doubling of people reporting problems of overall mobility. Future studies should examine the relationship between walking and balance function, as well as the consequences on the level of participation that these results indicate. A more intense focus on pain and fatigue management as well as on balance training is needed in the follow-up of these people.
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