The 6-minute walk test and other clinical endpoints in duchenne muscular dystrophy: Reliability, concurrent validity, and minimal clinically important differences from a multicenter study

Muscle and Nerve

Volumn 48, Issue 3, 2013, Pages 357-368

  Mcdonald, Craig M ^a   Henricson, Erik K ^a   Abresch, R Ted ^a   Florence, Julaine ^b   Eagle, Michelle ^c   Gappmaier, Eduard ^d   Glanzman, Allan M ^e   Spiegel, Robert ^f   Barth, Jay ^f   Elfring, Gary ^f   Reha, Allen ^f   Peltz, Stuart W ^f  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

^d UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^e CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^f PTC THERAPEUTICS   (United States)

Author keywords

6 minute walk test; Ambulation; Duchenne muscular dystrophy; Energy expenditure index; Muscular dystrophy; Myometry; Natural history; PedsQL; Timed function test

Indexed keywords

6 MINUTE WALK DISTANCE; ADOLESCENT; ADULT; ARTICLE; CHILD; CLINICAL EVALUATION; CONCURRENT VALIDITY; DUCHENNE MUSCULAR DYSTROPHY; ENERGY EXPENDITURE; FOLLOW UP; FUNCTION TEST; FUNCTIONAL STATUS; HEART RATE; HUMAN; MALE; MULTICENTER STUDY; OUTCOME ASSESSMENT; PRIORITY JOURNAL; RANGE OF MOTION; SCHOOL CHILD; SCREENING; TEST RETEST RELIABILITY;

6-MINUTE WALK TEST; AMBULATION; DUCHENNE MUSCULAR DYSTROPHY; ENERGY EXPENDITURE INDEX; MUSCULAR DYSTROPHY; MYOMETRY; NATURAL HISTORY; PEDSQL; TIMED FUNCTION TEST;

DISEASE PROGRESSION; EXERCISE TEST; HEART RATE; HUMANS; MALE; MUSCULAR DYSTROPHY, DUCHENNE; OUTCOME ASSESSMENT (HEALTH CARE); OXADIAZOLES; REPRODUCIBILITY OF RESULTS; TIME FACTORS; WALKING;

EID: 84883050768     PISSN: 0148639X     EISSN: 10974598     Source Type: Journal    
DOI: 10.1002/mus.23905     Document Type: Article

References (78)

1. Hoffman EP, Brown RH Jr, Kunkel LM. Dystrophin: the protein product of the Duchennemuscular dystrophy locus. Cell 1987;51:919-928.
2. Mendell JR, Shilling C, Leslie ND, Flanigan KM, al-Dahhak R, Gastier-Foster J, et al. Evidence-based path to newborn screening for Duchenne muscular dystrophy. Ann Neurol 2012;71:304-313.
3. Prevalence of Duchenne/Becker muscular dystrophy among males aged 5-24 years-four states, 2007. MMWR Morb Mortal Wkly Rep 2009;58:1119-1122.
4. Bushby K, Finkel R, Birnkrant DJ, Case LE, Clemens PR, Cripe L, et al. Diagnosis and management of Duchenne muscular dystrophy, part 1: diagnosis, and pharmacological and psychosocial management. Lancet Neurol 2010;9:77-93.
5. Bushby K, Finkel R, Birnkrant DJ, Case LE, Clemens PR, Cripe L, et al. Diagnosis and management of Duchenne muscular dystrophy, part 2: implementation of multidisciplinary care. Lancet Neurol 2010;9:177-189.
6. Dent KM, Dunn DM, von Niederhausern AC, Aoyagi AT, Kerr L, Bromberg MB, et al. Improved molecular diagnosis of dystrophinopathies in an unselected clinical cohort. Am J Med Genet A 2005;134:295-298.
7. Hirawat S, Elfring GL, Leonard EM, Miller LL Request for FDA orphan drug designation for ataluren as treatment of Duchenne muscular dystrophy. PTC Therapeutics Orphan Drug Designation Application; 2004.
8. Hirawat S, Elfring GL, Leonard EM, Miller LL Request for EMEA orphan product designation for ataluren as treatment of Duchenne muscular dystrophy. PTC Therapeutics Orphan Product Designation Application; 2004.
9. Chamberlain JS, Rando TA. Duchenne muscular dystrophy: advances in therapeutics. New York: Taylor & Francis, 2006.
10. Welch EM, Barton ER, Zhuo J, Tomizawa Y, Friesen WJ, Trifillis P, et al. PTC124 targets genetic disorders caused by nonsense mutations. Nature 2007;447:87-91.
11. Goemans NM, Tulinius M, van den Akker JT, Burm BE, Ekhart PF, Heuvelmans N, et al. Systemic administration of PRO051 in Duchenne's muscular dystrophy. N Engl J Med 2011;364:1513-1522.
12. Kinali M, Arechavala-Gomeza V, Feng L, Cirak S, Hunt D, Adkin C, et al. Local restoration of dystrophin expression with the morpholino oligomer AVI-4658 in Duchenne muscular dystrophy: a single-blind, placebo-controlled, dose-escalation, proof-of-concept study. Lancet Neurol 2009;8:918-928.
13. Crespo CJ, Keteyian SJ, Heath GW, Sempos CT. Leisure-time physical activity among US adults. Results from the Third National Health and Nutrition Examination Survey. Arch Intern Med 1996;156:93-98.
14. Brooke MH, Fenichel GM, Griggs RC, Mendell JR, Moxley R, Florence J, et al. Duchenne muscular dystrophy: patterns of clinical progression and effects of supportive therapy. Neurology 1989;39:475-481.
15. McDonald CM, Fowler WM Jr. The role of the neuromuscular medicine and physiatry specialists in the multidisciplinary management of neuromuscular disease. Phys Med Rehabil Clin N Am 2012;23:475-493.
16. McDonald CM, Abresch RT, Carter GT, Fowler WM Jr, Johnson ER, Kilmer DD, et al. Profiles of neuromuscular diseases. Duchenne muscular dystrophy. Am J Phys Med Rehabil 1995;74(suppl):S70-92.
17. ATS statement: Guidelines for the six-minute walk test. Am J Respir Crit Care Med 2002;166:111-117.
18. Takeuchi Y, Katsuno M, Banno H, Suzuki K, Kawashima M, Atsuta N, et al. Walking capacity evaluated by the 6-minute walk test in spinal and bulbar muscular atrophy. Muscle Nerve 2008;38:964-971.
19. Rubin LJ, Badesch DB, Barst RJ, Galie N, Black CM, Keogh A, et al. Bosentan therapy for pulmonary arterial hypertension. N Engl J Med 2002;346:896-903.
20. Dumas HM, Fragala MA, Haley SM, Skrinar AM, Wraith JE, Cox GF. Physical performance testing in mucopolysaccharidosis I: a pilot study. Pediatr Rehabil 2004;7:125-131.
21. Muenzer J, Wraith JE, Beck M, Giugliani R, Harmatz P, Eng CM, et al. A phase II/III clinical study of enzyme replacement therapy with idursulfase in mucopolysaccharidosis II (Hunter syndrome). Genet Med 2006;8:465-473.
22. Muenzer J, Gucsavas-Calikoglu M, McCandless SE, Schuetz TJ, Kimura A. A phase I/II clinical trial of enzyme replacement therapy in mucopolysaccharidosis II (Hunter syndrome). Mol Genet Metab 2007;90:329-337.
23. Harmatz P, Giugliani R, Schwartz IV, Guffon N, Teles EL, Miranda MC, et al. Long-term follow-up of endurance and safety outcomes during enzyme replacement therapy for mucopolysaccharidosis VI: Final results of three clinical studies of recombinant human N-acetylgalactosamine 4-sulfatase. Mol Genet Metab 2008;94:469-475.
24. Wraith JE, Clarke LA, Beck M, Kolodny EH, Pastores GM, Muenzer J, et al. Enzyme replacement therapy for mucopolysaccharidosis I: a randomized, double-blinded, placebo-controlled, multinational study of recombinant human alpha-L-iduronidase (laronidase). J Pediatr 2004;144:581-588.
25. van der Ploeg AT, Clemens PR, Corzo D, Escolar DM, Florence J, Groeneveld GJ, et al. A randomized study of alglucosidase alfa in late-onset Pompe's disease. N Engl J Med 2010;362:1396-1406.
26. McDonald CM, Henricson EK, Han JJ, Abresch RT, Nicorici A, Elfring GL, et al. The 6-minute walk test as a new outcome measure in Duchenne muscular dystrophy. Muscle Nerve 2010;41:500-510.
27. McDonald CM, Henricson EK, Han JJ, Abresch RT, Nicorici A, Atkinson L, et al. The 6-minute walk test in Duchenne/Becker muscular dystrophy: longitudinal observations. Muscle Nerve 2010;42:966-974.
28. Mazzone E, Martinelli D, Berardinelli A, Messina S, D'Amico A, Vasco G, et al. North Star Ambulatory Assessment, 6-minute walk test and timed items in ambulant boys with Duchenne muscular dystrophy. Neuromuscul Disord 2010;20:712-716.
29. Mazzone E, Vasco G, Sormani MP, Torrente Y, Berardinelli A, Messina S, et al. Functional changes in Duchenne muscular dystrophy: a 12-month longitudinal cohort study. Neurology 2011;77:250-256.
30. Jaeschke R, Singer J, Guyatt GH. Measurement of health status. Ascertaining the minimal clinically important difference. Control Clin Trials 1989;10:407-415.
31. Beaton DE, Bombardier C, Katz JN, Wright JG, Wells G, Boers M, et al. Looking for important change/differences in studies of responsiveness. OMERACT MCID Working Group. Outcome measures in rheumatology. Minimal clinically important difference. J Rheumatol 2001;28:400-405.
32. de Vet HC, Terwee CB, Ostelo RW, Beckerman H, Knol DL, Bouter LM. Minimal changes in health status questionnaires: distinction between minimally detectable change and minimally important change. Health Qual Life Outcomes 2006;4:54.
33. Hays RD, Woolley JM. The concept of clinically meaningful difference in health-related quality-of-life research. How meaningful is it? Pharmacoeconomics 2000;18:419-423.
34. Wells G, Anderson J, Beaton D, Bellamy N, Boers M, Bombardier C, et al. Minimal clinically important difference module: summary, recommendations, and research agenda. J Rheumatol 2001;28:452-454.
35. Jacobson N, Follette WC, Revenstorf D. Toward a standard definition of clinically significant change. Behav Ther 1986;17:308-311.
36. Crosby RD, Kolotkin RL, Williams GR. Defining clinically meaningful change in health-related quality of life. J Clin Epidemiol 2003;56:395-407.
37. Crosby RD, Kolotkin RL, Williams GR. An integrated method to determine meaningful changes in health-related quality of life. J Clin Epidemiol 2004;57:1153-1160.
38. Jacobson NS, Truax P. Clinical significance: a statistical approach to defining meaningful change in psychotherapy research. J Consult Clin Psychol 1991;59:12-19.
39. Deyo RA, Diehr P, Patrick DL. Reproducibility and responsiveness of health status measures. Statistics and strategies for evaluation. Control Clin Trials 1991;12(suppl):142S-158S.
40. Deyo RA, Centor RM. Assessing the responsiveness of functional scales to clinical change: an analogy to diagnostic test performance. J Chronic Dis 1986;39:897-906.
41. Wyrwich KW, Nienaber NA, Tierney WM, Wolinsky FD. Linking clinical relevance and statistical significance in evaluating intra-individual changes in health-related quality of life. Med Care 1999;37:469-478.
42. Kazis LE, Anderson JJ, Meenan RF. Effect sizes for interpreting changes in health status. Med Care 1989;27(suppl):S178-189.
43. Yost KJ, Eton DT. Combining distribution- and anchor-based approaches to determine minimally important differences: the FACIT experience. Eval Health Prof 2005;28:172-191.
44. Beaton DE, Boers M, Wells GA. Many faces of the minimal clinically important difference (MCID): a literature review and directions for future research. Curr Opin Rheumatol 2002;14:109-114.
45. Brooke MH, Griggs RC, Mendell JR, Fenichel GM, Shumate JB, Pellegrino RJ. Clinical trial in Duchenne dystrophy. I. The design of the protocol. Muscle Nerve 1981;4:186-197.
46. Brooke MH, Fenichel GM, Griggs RC, Mendell JR, Moxley R, Miller JP, et al. Clinical investigation in Duchenne dystrophy: 2. Determination of the "power" of therapeutic trials based on the natural history. Muscle Nerve 1983;6:91-103.
47. Mendell JR, Moxley RT, Griggs RC, Brooke MH, Fenichel GM, Miller JP, et al. Randomized, double-blind six-month trial of prednisone in Duchenne's muscular dystrophy. N Engl J Med 1989;320:1592-1597.
48. Griggs RC, Moxley RT III, Mendell JR, Fenichel GM, Brooke MH, Pestronk A, et al. Prednisone in Duchenne dystrophy. A randomized, controlled trial defining the time course and dose response. Clinical Investigation of Duchenne Dystrophy Group. Arch Neurol 1991;48:383-388.
49. Fowler WM Jr, Abresch RT, Aitkens S, Carter GT, Johnson ER, Kilmer DD, et al. Profiles of neuromuscular diseases. Design of the protocol. Am J Phys Med Rehabil 1995;74:S62-69.
50. Beenakker EA, Fock JM, van Tol MJ, Maurits NM, Koopman HM, Brouwer OF, et al. Intermittent prednisone therapy in Duchenne muscular dystrophy: a randomized controlled trial. Arch Neurol 2005;62:128-132.
51. Pradhan S, Ghosh D, Srivastava NK, Kumar A, Mittal B, Pandey CM, et al. Prednisolone in Duchenne muscular dystrophy with imminent loss of ambulation. J Neurol 2006;253:1309-1316.
52. McDonald CM, Henricson EK, Abresch RT, Han JJ, Escolar DM, Florence JM, et al. The CINRG Duchenne Natural History Study-a longitudinal natural history study in the era of glucocorticoid therapy: design of the protocol and methods. Muscle Nerve 2013;48:32-54.
53. Beenakker EA, van der Hoeven JH, Fock JM, Maurits NM. Reference values of maximum isometric muscle force obtained in 270 children aged 4-16 years by hand-held dynamometry. Neuromuscul Disord 2001;11:441-446.
54. Hyde SA, Steffensen BF, Floytrup I, et al. Longitudinal data analysis: an application to construction of a natural history profile of Duchenne muscular dystrophy. Neuromuscul Disord 2001;11:165-170.
55. Stuberg WA, Metcalf WK. Reliability of quantitative muscle testing in healthy children and in children with Duchenne muscular dystrophy using a hand-held dynamometer. Phys Ther 1988;68:977-982.
56. Brussock CM, Haley SM, Munsat TL, Bernhardt DB. Measurement of isometric force in children with and without Duchenne's muscular dystrophy. Phys Ther 1992;72:105-114.
57. Varni JW, Seid M, Kurtin PS. PedsQL™ 4.0: reliability and validity of the Pediatric Quality of Life Inventory™ Version 4.0 Generic Core Scales in healthy and patient populations. Med Care 2001;39:800-812.
58. Varni JW Seid M, Knight TS, Uzark K, Szer IS. The PedsQL 4.0 Generic Core Scales: sensitivity, responsiveness, and impact on clinical decision-making. J Behav Med 2002;25:175-193.
59. Varni JW BT, Seid M, Skarr D. The PedsQL 4.0 as a pediatric population health measure: feasibility, reliability, and validity. Ambul Pediatr 2003;3:329-341.
60. Varni JW LC, Burwinkle TM. How young can children reliably and validly self-report their health-related quality of life?: an analysis of 8, 591 children across age subgroups with the PedsQLTM 4.0 Generic Core Scales. Health Qual Life Outcomes 2007;3:1.
61. McDonald CM, McDonald DA, Bagley A, Sienko Thomas S, Buckon CE, Henricson E, et al. Relationship between clinical outcome measures and parent proxy reports of health-related quality of life in ambulatory children with Duchenne muscular dystrophy. J Child Neurol 2010;25:1130-1144.
62. Henricson E, Abresch R, Han JJ, Nicorici A, Goude Keller E, Elfring G, et al. Percent-predicted 6-minute walk distance in Duchenne muscular dystrophy to account for maturational influences. PLoS Curr 2012;4:RRN1297.
63. Geiger R, Strasak A, Treml B, Gasser K, Kleinsasser A, Fischer V, et al. Six-minute walk test in children and adolescents. J Pediatr 2007;150:395-399.
64. Rose J, Medeiros JM, Parker R. Energy cost index as an estimate of energy expenditure of cerebral-palsied children during assisted ambulation. Dev Med Child Neurol 1985;27:485-490.
65. Rose J, Gamble JG, Medeiros J, Burgos A, Haskell WL. Energy cost of walking in normal children and in those with cerebral palsy: comparison of heart rate and oxygen uptake. J Pediatr Orthop 1989;9:276-279.
66. Rose J, Gamble JG, Burgos A, Medeiros J, Haskell WL. Energy expenditure index of walking for normal children and for children with cerebral palsy. Dev Med Child Neurol 1990;32:333-340.
67. Rose J, Gamble JG, Lee J, Lee R, Haskell WL. The energy expenditure index: a method to quantitate and compare walking energy expenditure for children and adolescents. J Pediatr Orthop 1991;11:571-578.
68. Rose J, Haskell WL, Gamble JG, Hamilton RL, Brown DA, Rinsky L. Muscle pathology and clinical measures of disability in children with cerebral palsy. J Orthop Res 1994;12:758-768.
69. Beenakker EA, Maurits NM, Fock JM, Brouwer OF, van der Hoeven JH. Functional ability and muscle force in healthy children and ambulant Duchenne muscular dystrophy patients. Eur J Paediatr Neurol 2005;9:387-393.
70. Henricson EK, Abresch RT, Han JJ, Nicorici A, Goude E, de Bie E, McDonald CM. The 6-minute walk test and person-reported outcomes in boys with Duchenne muscular dystrophy and typically developing controls: Longitudinal comparisons and clinically-meaningful changes over one year. Presented at the Muscular Dystrophy Association National Scientific Meeting, April 21-24, 2013. Washington, D.C. Submitted for publication.
71. Ong EK MC, Walsh DD, Widman L, Walsh SA, Abresch RT, McDonald CM. Energy cost of locomotion in boys with Duchenne muscular dystrophy measured with a portable metabolic cart. Devel Med Child Neurol 1999;41:34.
72. Sienko Thomas S, Buckon CE, Nicorici A, Bagley A, McDonald CM, Sussman MD. Classification of the gait patterns of boys with Duchenne muscular dystrophy and their relationship to function. J Child Neurol 2010;25:1103-1109.
73. Jansen M, de Jong M, Coes HM, Eggermont F, van Alfen N, de Groot IJM. The assisted 6-minute cycling test to assess endurance in children with a neuromuscular disorder. Muscle Nerve 2012;46:520-530.
74. Du Bois RM, Weycker D, Albera C, Bradford WZ, Costabel U, Kartashov A, et al. Six-minute-walk test in idiopathic pulmonary fibrosis: test validation and minimal clinically important difference. Am J Respir Crit Care Med 2011;183:1231-1237.
75. Holland AE, Hill CJ, Conron M, Munro P, McDonald CF. Small changes in six-minute walk distance are important in diffuse parenchymal lung disease. Respir Med 2009;103:1430-1435.
76. Puhan MA, Mador MJ, Held U, Goldstein R, Guyatt GH, Schünemann HJ. Interpretation of treatment changes in 6-minute walk distance in patients with COPD. Eur Respir J 2008;32:637-643.
77. Gremeaux V, Troisgros O, Benaïm S, Hannequin A, Laurent Y, Casillas JM, et al. Determining the minimal clinically important difference for the six-minute walk test and the 200-meter fast-walk test during cardiac rehabilitation program in coronary artery disease patients after acute coronary syndrome. Arch Phys Med Rehabil 2011;92:611-619.
78. McDonald C, Henricson, EK, Abresch, RT, Florence JM, Eagle M, Gappmaier E, et al. The 6-minute walk test and other endpoints in nonsense-mutation-mediated dystrophinopathy: longitudinal natural history observations in a multicenter study. Muscle Nerve, in press.