Share this article on:

Six-Minute Walk Test in Children With Spastic Cerebral Palsy and Children Developing Typically

Fitzgerald, Diarmaid PT, PhD; Hickey, Claire PT, BSc; Delahunt, Eamonn PT, PhD; Walsh, Michael PT, MMedSc; O'Brien, Timothy MCh, FRCSI

doi: 10.1097/PEP.0000000000000224
Research Reports

Purpose: To quantify the 6-minute walk test (6MWT) in children with spastic cerebral palsy (CP) functioning at Gross Motor Function Classification System (GMFCS) levels I to III and to compare with a sample of children with typical development (TD).

Methods: A total of 145 children with CP and 137 children with TD completed the 6MWT.

Results: Mean 6MWT scores were 439.57 ± 49.81 m for children functioning at GMFCS level I (n = 74), 386.74 ± 66.47 m for GMFCS level II (n = 53), 305.28 ± 66.95 m for GMFCS level III (n = 18), and 528.42 ± 67.77 m for children with TD (n = 137). Results of a pair-wise comparison showed significant differences (P < .001) between 6MWT scores of children with CP across GMFCS levels I to III and children with TD.

Conclusion: A range of 6-minute walk distance reference values for children with spastic CP and children with TD were established.

Quantification of the 6-minute walk test (6MWT) in children with spastic cerebral palsy (CP) functioning at Gross Motor Function Classification System levels I to III.

Gait Laboratory (Dr Fitzgerald, Mr Walsh, and Mr O'Brien), Central Remedial Clinic, Dublin, Ireland; School of Public Health, Physiotherapy and Sports Science (Ms Hickey and Dr Delahunt), University College Dublin, Dublin, Ireland.

Correspondence: Diarmaid Fitzgerald, PT, PhD, Gait Laboratory, Central Remedial Clinic, Vernon Ave, Dublin 3, Ireland (diarmaidfitzgerald@campus.ie).

The authors declare no conflicts of interest.

Back to Top | Article Outline

INTRODUCTION

The 6-minute walk test (6MWT) is a standardized, self-paced walking test commonly used to assess functional ability in children with cerebral palsy (CP).1 The test has been reported to reflect functional capacity in terms of activities of daily living.2 In a recent Delphi study3 surveying the views of 15 physical therapy and exercise physiology experts, the 6MWT has been recommended as a submaximal exercise test for children with CP of Gross Motor Function Classification System4 (GMFCS) levels I to III. The 6MWT is used in children with CP to monitor changes in functional ability throughout childhood through multiple repeated assessments and also to aid assessment of functional outcomes of surgical or nonsurgical interventions.5 The test is inexpensive and easy to administer in the clinical setting,2 but differing assessment protocols can limit the comparability among research studies reported in the scientific literature.

The body of evidence reporting acceptable levels of validity and reliability for the 6MWT is growing in both children with CP and in children that are healthy and typically developing (TD). Nsenga Leunkeu and colleagues6 reported good reproducibility (r = 0.87; P = .007; intraclass correlation coefficient [ICC] = 0.80) and validity (r = 0.948; P < .001) of this measure in children with CP functioning at GMFCS levels I and II in the age range 10 to 16 years. Thompson et al7 and Maher et al1 showed excellent test-retest reliability in children with CP classified in GMFCS levels I to III aged 4 to 18 years (ICC = 0.98) and 11 to 17 years (ICC = 0.98), respectively. Results reported by Maher et al also suggested that a practice walk was not required before the test walk as the distance walked varied by less than 1% between the 2 6MWT trials in their study. In children that are healthy and TD, the research from Li et al8 showed high reliability (ICC = 0.94) in a group 12 to 16 years old. All studies outline the importance of a standardized systematic approach to testing methods.1,6,7,8 The American Thoracic Society (ATS) 6MWT statement is the commonly used consensus outlining the testing guideline.8 The guidelines recommendations include indoor testing, on a straight hard surface of 30 m, a starting line of bright tape on the floor to mark start and end of each 60-m lap, an orange cone for the turnaround point, and specific standardized instructions given before and during the test.9

Six-minute walk distance (6MWD) may potentially be affected by many factors such as age, anthropometric, clinical, cognitive, and emotional factors. Previous studies have reported 6MWD in children with CP and children that are TD (Tables 1 and 2).1,6–8,10–20 Average group scores in these studies vary from 334 to 455 m in children with CP and from 471 to 677 m in children that are TD.1,6–8,10–20 Assessment of respiratory function was the original application of the 6MWT in 1982 when Butland and colleagues21 adapted the previously used 12-minute walk test to assess exercise tolerance in patients with chronic respiratory disability. In children with CP, the 6MWT reflects a compromise of multiple body systems along with the possibility of respiratory compromise.1 Reduced functional walking ability in some children with CP may be largely due to pathological inefficiencies of the musculoskeletal system during gait. The cerebral lesion can result in varied musculoskeletal impairments such as alterations in tone, poor selective motor control, and muscle weakness.22 In the growing child, these factors cause altered joint forces resulting in structural abnormalities that develop in both the bony skeleton and surrounding soft tissue structures.23 Abnormal bony torsion and soft tissue contractures cause lever arm dysfunction across the joints, increasing the energy expenditure during movements such as walking.24 Additional factors that contribute to reduced functional walking ability in children with CP include reduced cardiopulmonary endurance, poor balance and altered muscle structure and metabolism resulting in increased fatigability of muscles.25–27

A number of studies reported typical 6MWD in children with CP; however, testing protocols vary greatly across studies.1,6,7,10 The same test protocol needs to be evaluated in children with CP who are ambulatory and children that are TD to enable comparative analysis. The primary aim of this study was, therefore, to quantify average 6MWD in a sample of children with CP and their age-matched peers that are TD using a standardized test protocol. A secondary aim was to assess the relationship between the 6MWT score and age, height, and body mass in children with and without CP.

Back to Top | Article Outline

METHODS

Participants

A total of 145 children with spastic CP, aged 4 to 17 years, who were referred to a gait analysis laboratory for comprehensive gait assessments were evaluated prospectively as outlined in Table 3. Children diagnosed with athetoid, ataxic, or dyskinetic types of CP were not included. Any children with CP who had undergone surgery during the previous 18 months were not included.

These 145 children that were TD, aged 4 to 17 years, were recruited via advertising within the rehabilitation center and in local schools in the area. Participants were screened for exclusion criteria via the Physical Activity Readiness Questionnaire28 modified for children, and the questionnaire was completed by a parent/guardian of the child. Participants that were TD were excluded from the study if they had any cardiac-related conditions, previously reported chest pain during physical activity, issues relating to dizziness, poor balance or loss of consciousness, musculoskeletal problems that could affect their ability to participate in walking, uncontrolled asthma, or any other pathology that might prevent the child from participating in physical activity.

Parents/guardians for both study groups gave consent for the use of data for clinical research at the time of testing. The project was approved by both the University and Clinic Research Committees.

Back to Top | Article Outline

Experimental Protocol

Participants' body mass and height were measured using an electronic scale and an assembled wall stadiometer. Both groups completed a modified 6MWT protocol as described in the ATS statement.9 The modifications were (1) to increase the length of the course in this study, which was 70 m straight from the starting point to the end point (30 m in the ATS protocol), (2) to modify the turnaround points, which were indicated by signs on the wall (traffic cones used in the ATS protocol), and (3) to give no demonstration lap (although suggested in the ATS protocol). All other aspects of the ATS protocol were followed.

All testing was performed by the first and second authors, and all evaluations took place indoors, in the same straight corridor, with a flat hard surface, free of obstacles. No additional verbal comment or encouragement was given other than those recommended by the ATS guidelines, which allows 1 standardized comment every minute such as “you are doing well, you have only 1 minute to go.” Before commencement, participants were told that “the objective of the test is to walk as far as possible in 6 minutes.” The tester walked behind the participant during the test so as not to influence the child's walking speed, and no practice walk or warm-up was permitted. To minimize bias or distractions, participants were tested 1 at a time. The number of lengths completed and the distance covered in the final uncompleted length were recorded on a scoring sheet to the nearest meter.

Back to Top | Article Outline

Statistical Analysis

Statistical analysis was carried out using IBM SPSS Statistics 20 (IBM Ireland Ltd, Dublin, Ireland). Descriptive statistics of demographic details and outcome measures were presented as means and standard deviations (SDs). For statistical analysis, participants with CP were categorized into subgroups on the basis of their GMFCS level. A 1-way between-groups analysis of covariance was conducted to compare 6MWD across groups. The independent variable was group—(1) GMFCS I, (2) GMFCS II, (3) GMFCS III, and (4) TD—and the dependent variable was 6MWD. Participants' age, height, and body mass were used as covariates in the analysis. To determine differences between groups, a Bonferroni adjusted pair-wise comparison was undertaken. Standard multiple regression was used to assess the ability of age, height, and body mass to predict 6MWD in each of the groups.

Back to Top | Article Outline

RESULTS

Six-Minute Walk Distance

Preliminary checks were conducted to ensure no violation of the assumptions of normality, linearity, homogeneity of variances, homogeneity of regression slopes, and reliable measurement of the covariates were made. After adjusting for age, height, and body mass, a significant difference was found among all groups (F(3, 282) = 88.57; P < .001; partial η2 = 0.49; observed power = 1.00) as outlined in Table 4 and Figure 1.

Back to Top | Article Outline

Regression Analysis

Age, height, and body mass variables were analyzed individually for their ability to predict 6MWD.

GMFCS I. The total variance in 6MWD explained by age, height, and body mass was 26.2% [R2 = 0.26; F(3, 73) = 8.27; P < .001]. Height was the only independent variable (β value = 0.62) that contributed significantly (P < .05) to explaining 6MWD. The part correlation coefficients indicated that height uniquely explained 6% of the variance in 6MWD.

GMFCS II. The total variance in 6MWD explained by age, height, and body mass was 35% [R2 = 0.35; F(3, 52) = 9.00; P < .001]. Age was the only independent variable (β value = −1.13) that contributed significantly (P = .001) to explaining 6MWD. The part correlation coefficients indicated that age uniquely explained 15.9% of the variance in 6MWD.

GMFCS III. The total variance in 6MWD explained by age, height, and body mass was 43% [R2 = 0.43; F(3, 17) = 3.53; P < .05]. Age (β value = −0.23), height (β value = 0.98), or body mass (β value = −0.11) did not independently contribute significantly (P > .05) to explaining 6MWD.

TD. The total variance in 6MWD explained by age, height, and body mass was 37.1% [R2 = 0.37; F(3, 136) = 26.16; P < .01]. Age was the only independent variable (β value = 0.54) that contributed significantly (P < .01) to explaining 6MWD. The part correlation coefficients indicated that age uniquely explained 3% of the variance in 6MWD.

Back to Top | Article Outline

DISCUSSION

The focus of this research was to quantify the ambulatory capabilities of children with CP on a flat surface compared with their peers that were TD using the 6MWT. The results showed that the 6MWT can differentiate between walking ability across the 4 different test groups of children classified in GMFCS levels I, II, and III and TD. These reference datasets will be useful in clinical and research practice to allow comparison of both, individuals and groups of children with CP. They may also be used to track changes over time in response to growth and potential clinical interventions.

Children with spastic CP functioning at GMFCS level III walked an average distance of 305.28 m (SD = 66.95 m) in 6 minutes, approximately 223 m less than the average distance walked by their peer group that was TD, who covered a mean distance of 528.42 m (SD = 67.77 m) in 6 minutes. On average, children functioning at GMFCS level II varied from their peers that were TD by 142 m, walking a mean distance of 386.74 m (SD = 66.47 m). Of interest, children with spastic CP functioning at GMFCS level I still walked an average of 89 m less than their peers that were TD, covering a mean distance of 439.57 m (SD = 49.81 m). This indicates that CP as a pathology still affects the functional walking ability of the highest functioning child with CP when compared with a peer group that is TD.

Regression analysis of the data assessing the ability of age, height, or body mass to predict 6MWT scores indicated that height contributed significantly to predicting the 6MWT score in children functioning at GMFCS I and that age predicted 6MWT scores in children functioning at both GMFSC II and TD. However, part correlation coefficients in this regression analysis ranged from 0% to 16%, limiting the predictability and therefore clinical usefulness of these findings.

Back to Top | Article Outline

Previous Research in Children With CP

Only 1 previous study, by Thompson and colleagues,7 outlined the 6MWT scores in children with CP classified across the GMFCS levels I to III as shown in Table 1. In their study, they examined the test-retest reliability of 31 children with spastic CP, and therefore, 2 6MWT trials were performed with a retest interval of 1 to 2 weeks.7 Comparison of results shows the current study (Table 4) has lower scores for children functioning at GMFCS level I, but higher scores for those classified in GMFCS levels II and III. There are methodological differences limiting the comparability of results, and 1 factor that might have contributed to the variance in 6MWD may have been the differing course shape and length. We used a 70-m straight corridor compared with a 20-m × 45-m rectangular course used by Thompson et al.7 Therefore, a lower frequency of turning events was used in the current study, whereas the test protocol of Thompson et al7 did not require a full 180° turn. The rectangular course may have helped the higher functioning GMFCS level I group maintain momentum at the 90° corners, but this repeated change of direction was perhaps more difficult for children classified in GMFCS levels II and III.

In the study by Chong et al,10 an oval-shaped course was used. This type of course may reduce the difficulties that participants may have when making 180° turns, as is necessary when performing the 6MWT on a straight course. An oval-shaped course may make the test easier to perform, particularly for participants who use assistive devices such as walkers. This is reflected by a larger mean 6MWD of 455.4 m in the study by Chong et al10 (GMFCS levels I-IV and age range 94.4-776.2) compared with the mean values found in our study.

Results of the current study also showed a significant relationship between participant height and 6MWT scores in children with CP classified in GMFCS level I, and in children classified in GMFCS level II a significant relationship between age and 6MWT scores was found. For children classified in GMFCS level III, no significant predictor of 6MWT scores was found. Perhaps at higher levels of disability, age or height is not as important in determining differences in walking distance. None of the previous 4 studies assessing 6MWT scores examined the relationship of score with age, height, or body mass.1,6,7,10 However, in the current study, these relationships showed low predictability levels limiting their clinical usefulness, and further research is warranted to assess the implications of these varying anthropometric and demographic associations.

Back to Top | Article Outline

Previous Research in Children That Were TD

When results of the group that was TD are compared with previous studies, our mean score of 530 m falls below all studies outlined in Table 2, except for the study by Lammers et al14 in the United Kingdom who reported mean scores of 471 m. A comparison of height profiles shows that all other studies were conducted on a cohort with a higher mean height with the exception of the Brazilian study by D'Silva et al12 who, along with Lammers et al,14 reported on children with a lower mean height. Li et al15 have previously shown a strong correlation between height and 6MWT scores.

Additional factors that may affect 6MWT scores reported in the literature include motivation levels and differences in the interpretation of instructions by participants. Studies by Geiger et al13 and Tonklang et al19 used modified protocols, which included measuring wheels as an incentive or rubber bands as “collecting tokens” given to each participant on completion of a lap (Table 2). These modified protocols create an incentive for participants to walk as far as possible. In the current study, 1 observation was that motivation and interpretation of how the test should be performed varied among participants. Participants were told that “the object of the test is to walk as far as possible in 6 minutes.” Some participants interpreted this by walking quickly, whereas others seemed to walk at a slower, more natural pace. It was also noted that many younger children seemed to lose interest in the object of the test. These factors were not formally evaluated in this study.

Regression analysis of our group that was TD showed that age was the only significant predictor of 6MWT scores, but again, the predictability level was low. When previous research reports of similar studies were evaluated, no consistent trend was seen. Our findings agreed with the results of the study by Ulrich et al20 conducted in Switzerland with 496 children aged 4 to 16 years, reporting that age was the best predictor of 6MWT scores. Lammers et al14 in the UK showed that height, weight, and age all correlated with the test scores in 328 children of 4 to 11 years. Li et al15 in Hong Kong, who assessed 1445 children that were TD from ages 7 to 16 years, showed height to have the greatest correlation with 6MWT scores in children that are TD. Although difficult to infer the implications of these varying results, they might suggest that race or country of origin could be a factor.

Back to Top | Article Outline

Study Limitations and Future Research

Limitations of this research include the fact that no assessment of intellectual ability was conducted during testing. Some participants with CP with cognitive involvement might have reduced understanding of instructions and ability to follow directions during testing, which could have potentially negatively affected their test scores. Sex differences were not assessed in the data analysis, which may have shown additional differences. The cohort of children with CP was a sample of convenience from a gait laboratory database. A population-based study, generated from a registry of children with CP, may be more representative of this patient population. In addition, there may be a limitation in terms of sample size, particularly in the group that was TD, when compared with Li and colleagues15 who reported on 1445 children.

Future research in the area may be directed at including additional physiological monitoring, such as the assessment of heart rate, to evaluate energy expenditure. It may also be useful to use activity monitoring sensors over a series of days to assess whether higher 6MWD correlates with higher activity levels in the daily activities in children with CP. Finally, an unmeasured observation of the study during testing was that some children may have benefited from more instruction. It may be useful to test a modified protocol for children, with instructions given every 30 seconds rather than every minute and assess the results for possible score changes.

Back to Top | Article Outline

CONCLUSION

This study outlines a reference range of 6MWD across children with spastic CP who are ambulatory and functioning at GMFCS levels I to III and their peers that were TD and shows significant differences among all groups. Our findings also show that height may be a predictor of 6MWD in children with spastic CP classified in GMFCS level I and that age may be a predictor in children classified in GMFCS level II; however, further research is warranted to explore the significance of these findings.

Back to Top | Article Outline

REFERENCES

1. Maher CA, Williams MT, Olds TS. The six-minute walk test for children with cerebral palsy. Int J Rehabil Res. 2008;31:185–188.
2. Solway S, Brooks D, Lacasse Y, Thomas S. A qualitative systematic overview of the measurement properties of functional walk tests used in the cardiorespiratory domain. Chest. 2001;119:256–270.
3. Verschuren O, Ketelaar M, Keefer D, et al. Identification of a core set of exercise tests for children and adolescents with cerebral palsy: a Delphi survey of researchers and clinicians. Dev Med Child Neurol. 2011;53:449–456.
4. Palisano RJ, Rosenbaum PL, Walter SD, Russell DJ, Wood EP, Galuppi BE. Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol. 1997;39:214–223.
5. Beard L, Harro C, Bothner K. The effect of body weight support treadmill training on gait function in cerebral palsy: two case studies. Pediatr Phys Ther. 2005;17:72.
6. Nsenga Leunkeu A, Shephard RJ, Ahmaidi S. Six-minute walk test in children with cerebral palsy gross motor function classification system levels I and II: reproducibility, validity, and training effects. Arch Phys Med Rehabil. 2012;93:2333–2339.
7. Thompson P, Beath T, Bell J, et al. Test-retest reliability of the 10-metre fast walk test and 6-minute walk test in ambulatory school-aged children with cerebral palsy. Dev Med Child Neurol. 2008;50:370–376.
8. Li AM, Yin J, Yu CC, et al. The six-minute walk test in healthy children: reliability and validity. Eur Respir J. 2005;25:1057–1060.
9. American Thoracic Society Statement. Guidelines for the Six-Minute Walk Test. Am J Respir Crit Care Med. 2002;166:111–117.
10. Chong J, Mackey AH, Broadbent E, Stott NS. Relationship between Walk Tests and Parental Reports of Walking Abilities in Children with Cerebral Palsy. Arch Phys Med Rehabil. 2011; 92:265–270.
11. Basso RP, Jamami M, Pessoa BV, Labadessa IG, Regueiro EM, Di Lorenzo VA. Assessment of exercise capacity among asthmatic and healthy adolescents. Rev Bras Fisioter. 2010;14:252–258.
12. D'silva C, Vaishali K, Venkatesan P. Six-minute walk test-normal values of school children aged 7-12 y in India: a cross-sectional study. Indian J Pediatr. 2012;79:597–601.
13. Geiger R, Strasak A, Treml B, et al. Six-minute walk test in children and adolescents. J Pediatr. 2007;150:395–399.
14. Lammershttp AE, Hislop AA, Flynn Y, Haworth SG. The 6-minute walk test: normal values for children of 4-11 years of age. Arch Dis Child. 2008;93:464–468.
15. Li AM, Yin J, Au JT, et al. Standard reference for the six-minute-walk test in healthy children aged 7 to 16 years. Am J Respir Crit Care Med. 2007;176:174–180.
16. Limsuwan A, Wongwandee R, Khowsathit P. Correlation between 6-min walk test and exercise stress test in healthy children. Acta Paediatr. 2010;99:438–441.
17. Morinder G, Mattsson E, Sollander C, Marcus C, Larsson UE. Six-minute walk test in obese children and adolescents: reproducibility and validity. Physiother Res Int. 2009;14:91–104.
18. Priesnitz CV, Horak Rodrigues G, Da Silva Stumpf C, et al. Reference values for the 6-min walk test in healthy children aged 6-12 years. Pediatr Pulmonol. 2009;44:1174–1179.
19. Tonklang N, Roymanee S, Sopontammarak S. Developing standard reference data for Thai children from a six-minute walk test. J Med Assoc Thai. 2011;94:470–475.
20. Ulrich S, Hildenbrand FF, Treder U, et al. Reference values for the 6-minute walk test in healthy children and adolescents in Switzerland. BMC Pul Med. 2013;13:49.
21. Butland RJ, Pang J, Gross ER, Woodcock AA, Geddes DM. Two-, six-, and 12-minute walking tests in respiratory disease. Br Med J (Clin Res Ed). 1982;284:1607–1608.
22. Rosenbaum PL, Walter SD, Hanna SE, et al. Prognosis for gross motor function in cerebral palsy: creation of motor development curves. JAMA. 2002;288:1357–1363.
23. Carter DR, Tse B. The pathogenesis of osteoarthritis in cerebral palsy. Dev Med Child Neurol. 2009;51(Suppl 4):79–83.
24. Gage JR. Gait analysis: an essential tool in the treatment of cerebral palsy. Clin Orthop Relat Res. 1993;288:126–134.
25. van den Berg-Emons HJ, Saris WH, de Barbanson DC, Westerterp KR, Huson A, van Baak MA. Daily physical activity of schoolchildren with spastic diplegia and of healthy control subjects. J Pediatr. 1995;127:578–584.
26. Opheim A, Jahnsen R, Olsson E, Stanghelle JK. Balance in relation to walking deterioration in adults with spastic bilateral cerebral palsy. Phys Ther. 2012;92:279–288.
27. Barrett RS, Lichtwark GA. Gross muscle morphology and structure in spastic cerebral palsy: a systematic review. Dev Neurorehabil. 2010;52:794–804.
28. Canadian Society for Exercise Physiology. Physical Activity Readiness Questionnaire. 2002. http://www.csep.ca/cmfiles/publications/parq/par-q.pdf. Accessed on December 11, 2014.

activities of daily living; cerebral palsy; child; exercise test; female; male; physical endurance; reference values

Copyright © 2016 Wolters Kluwer Health, Inc. and Section on Pediatrics of the American Physical Therapy Association. All rights reserved.