Revised Hammersmith Scale for spinal muscular atrophy: A SMA specific clinical outcome assessment tool

PLoS ONE

Volumn 12, Issue 2, 2017, Pages

  Ramsey, Danielle ^a   Scoto, Mariacristina ^a   Mayhew, Anna ^b   Main, Marion ^a   Mazzone, Elena S ^c   Montes, Jacqueline ^d   De Sanctis, Roberto ^c   Young, Sally Dunaway ^d   Salazar, Rachel ^d   Glanzman, Allan M ^e   Pasternak, Amy ^f   Quigley, Janet ^f   Mirek, Elizabeth ^f   Duong, Tina ^g   Gee, Richard ^g   Civitello, Matthew ^h   Tennekoon, Gihan ⁱ   Pane, Marika ^c   Pera, Maria Carmela ^c   Bushby, Kate ^b   Day, John ^g   Darras, Basil T ^f   De Vivo, Darryl ^d   Finkel, Richard ^h   Mercuri, Eugenio ^a,c   Muntoni, Francesco ^a   more..

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c CATHOLIC UNIVERSITY   (Italy)

^d Department of Medicine   (United States)

^e CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^f BOSTON CHILDREN S HOSPITAL   (United States)

^g STANFORD UNIVERSITY   (United States)

^h UNIVERSITY OF CENTRAL FLORIDA COLLEGE OF MEDICINE   (United States)

ⁱ UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADOLESCENT; ADULT; ARTICLE; CHILD; CONCURRENT VALIDITY; CONSTRUCT VALIDITY; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DISEASE CLASSIFICATION; FEMALE; HUMAN; MAJOR CLINICAL STUDY; MALE; MOBILIZATION; OBSERVATIONAL STUDY; OUTCOME ASSESSMENT; PHYSICAL CAPACITY; PILOT STUDY; PSYCHOMETRY; RASCH ANALYSIS; RATING SCALE; RELIABILITY; REVISED HAMMERSMITH SCALE; SPINAL MUSCULAR ATROPHY; SPINE SURGERY; CLINICAL TRIAL; DISEASE COURSE; HEREDITARY SPINAL MUSCULAR ATROPHY; INFANT; MIDDLE AGED; MOTOR ACTIVITY; MULTICENTER STUDY; PRESCHOOL CHILD; PROCEDURES; SEVERITY OF ILLNESS INDEX; WALKING DIFFICULTY; YOUNG ADULT;

ADOLESCENT; ADULT; CHILD; CHILD, PRESCHOOL; DISEASE PROGRESSION; FEMALE; HUMANS; INFANT; MALE; MIDDLE AGED; MOBILITY LIMITATION; MOTOR ACTIVITY; OUTCOME ASSESSMENT (HEALTH CARE); PILOT PROJECTS; PSYCHOMETRICS; SEVERITY OF ILLNESS INDEX; SPINAL MUSCULAR ATROPHIES OF CHILDHOOD; YOUNG ADULT;

EID: 85013487380     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0172346     Document Type: Article

References (46)

1. Piepers S, van den Berg LH, Brugman F, Scheffer H, Ruiterkamp-Versteeg M, van Engelen BG, et al. A natural history study of late onset spinal muscular atrophy types 3b and 4. J Neurol. 2008; 255(9):1400-4. Epub 2008/06/26. doi: 10.1007/s00415-008-0929-0 PMID: 18575920
2. Feldkötter M, Schwarzer V, Wirth R, Wienker TF, Wirth B. Quantitative analyses of SMN1 and SMN2 based on real-time lightCycler PCR: fast and highly reliable carrier testing and prediction of severity of spinal muscular atrophy. Am J Hum Genet. 2002; 70(2):358-68. doi: 10.1086/338627 PMID: 11791208
3. Farrar MA, Vucic S, Johnston HM, du Sart D, Kiernan MC. Pathophysiological insights derived by natural history and motor function of spinal muscular atrophy. The Journal of pediatrics. 2013; 162(1):155-9. Epub 2012/07/20. doi: 10.1016/j.jpeds.2012.05.067 PMID: 22809660
4. Arnold WD, Kassar D, Kissel JT. Spinal muscular atrophy: Diagnosis and management in a new therapeutic era. Muscle & nerve. 2015; 51(2):157-67.
5. Darras BT, Markowitz JA, Monani UR, De Vivo DC. Chapter 8-Spinal Muscular Atrophies. Neuromuscular Disorders of Infancy, Childhood, and Adolescence ( Second Edition). San Diego: Academic Press; 2015. p. 117-45.
6. Wang CH, Finkel RS, Bertini ES, Schroth M, Simonds A, Wong B, et al. Consensus Statement for Standard of Care in Spinal Muscular Atrophy. Journal of child neurology. 2007; 22(8):1027-49. doi: 10.1177/0883073807305788 PMID: 17761659
7. Mercuri E, Bertini E, Iannaccone ST. Childhood spinal muscular atrophy: controversies and challenges. Lancet Neurol. 2012; 11(5):443-52. doi: 10.1016/S1474-4422(12)70061-3 PMID: 22516079
8. Castro D, Iannaccone ST. Spinal muscular atrophy: therapeutic strategies. Curr Treat Options Neurol. 2014; 16(11):316. doi: 10.1007/s11940-014-0316-3 PMID: 25245431
9. Finkel R, Bertini E, Muntoni F, Mercuri E. 209th ENMC International Workshop: Outcome Measures and Clinical Trial Readiness in Spinal Muscular Atrophy 7-9 November 2014, Heemskerk, The Netherlands. Neuromuscular disorders: NMD. 2015; 25(7):593-602. Epub 2015/06/06. doi: 10.1016/j.nmd. 2015.04.009 PMID: 26045156
10. Main M, Kairon H, Mercuri E, Muntoni F. The Hammersmith Functional Motor Scale for Children with Spinal Muscular Atrophy: a Scale to Test Ability and Monitor Progress in Children with Limited Ambulation. European Journal of Paediatric Neurology. 2003; 7(4):155-9. PMID: 12865054
11. Krosschell KJ, Maczulski JA, Crawford TO, Scott C, Swoboda KJ. A modified Hammersmith functional motor scale for use in multi-center research on spinal muscular atrophy. Neuromuscular Disorders. 2006; 16(7):417-26. http://dx.doi.org/10.1016/j.nmd.2006.03.015. PMID: 16750368
12. Krosschell KJ, Scott CB, Maczulski JA, Lewelt AJ, Reyna SP, Swoboda KJ. Reliability of the Modified Hammersmith Functional Motor Scale in young children with spinal muscular atrophy. Muscle & nerve. 2011; 44(2):246-51. Epub 2011/06/24.
13. O'Hagen JM, Glanzman AM, McDermott MP, Ryan PA, Flickinger J, Quigley J, et al. An expanded version of the Hammersmith Functional Motor Scale for SMA II and III patients. Neuromuscular disorders: NMD. 2007; 17(9-10):693-7. Epub 2007/07/31. doi: 10.1016/j.nmd.2007.05.009 PMID: 17658255
14. Krosschell K, Maczulski J. Modified Hammersmith Functional Motor Scale for Children with Spinal Muscular Atrophy-Research Trial Protocol Administration and Scoring Manual Online: Project Cure SMA; 2004 [cited 2015 14.08.2015]. www.smaoutcomes.org/hammersmith-manual/manual-1.html.
15. Mazzone E, De Sanctis R, Fanelli L, Bianco F, Main M, van den Hauwe M, et al. Hammersmith Functional Motor Scale and Motor Function Measure-20 in non ambulant SMA patients. Neuromuscular disorders: NMD. 2014; 24(4):347-52. Epub 2014/02/05. doi: 10.1016/j.nmd.2014.01.003 PMID: 24491485
16. Mazzone E, Montes J, Main M, Mayhew A, Ramsey D, Glanzman AM, et al. Old measures and new scores in spinal muscular atrophy patients. Muscle & nerve. 2015. Epub 2015/06/27.
17. Chiriboga CA, Swoboda KJ, Darras BT, Iannaccone ST, Montes J, De Vivo DC, et al. Results from a phase 1 study of nusinersen (ISIS-SMN(Rx)) in children with spinal muscular atrophy. Neurology. 2016; 86(10):890-7. doi: 10.1212/WNL.0000000000002445 PMID: 26865511
18. Mercuri E, Finkel R, Montes J, Mazzone ES, Sormani MP, Main M, et al. Patterns of disease progression in type 2 and 3 SMA: Implications for clinical trials. Neuromuscular disorders: NMD. 2016; 26 (2):126-31. Epub 2016/01/19. doi: 10.1016/j.nmd.2015.10.006 PMID: 26776503
19. Glanzman AM, O'Hagen JM, McDermott MP, Martens WB, Flickinger J, Riley S, et al. Validation of the Expanded Hammersmith Functional Motor Scale in spinal muscular atrophy type II and III. Journal of child neurology. 2011; 26(12):1499-507. Epub 2011/09/24. doi: 10.1177/0883073811420294 PMID: 21940700
20. Kaufmann P, McDermott MP, Darras BT, Finkel RS, Sproule DM, Kang PB, et al. Prospective cohort study of spinal muscular atrophy types 2 and 3. Neurology. 2012; 79(18):1889-97. Epub 2012/10/19. doi: 10.1212/WNL.0b013e318271f7e4 PMID: 23077013
21. Cano SJ, Mayhew A, Glanzman AM, Krosschell KJ, Swoboda KJ, Main M, et al. Rasch analysis of clinical outcome measures in spinal muscular atrophy. Muscle & nerve. 2014; 49(3):422-30. Epub 2013/07/ 10.
22. Mensch SM, Rameckers EAA, Echteld MA, Evenhuis HM. Instruments for the evaluation of motor abilities for children with severe multiple disabilities: A systematic review of the literature. Research in Developmental Disabilities. 2015; 47:185-98. doi: 10.1016/j.ridd.2015.09.002 PMID: 26436614
23. U.S. Department of Health and Human Services Food and Drug Administration, Centre for Drug Evaluation and Research, Centre for Biologics Evaluation and Research, Centre for Devices and Radiological Health. Guidance for Industry. Patient-Reported Outcome Measures: Use in Medical Product Development to Support Labeling Claims. In: Research CfDEa, Research CfBEa, Health CfDaR, editors. 2009.
24. Mokkink LB, Terwee CB, Patrick DL, Alonso J, Stratford PW, Knol DL, et al. The COSMIN checklist for assessing the methodological quality of studies on measurement properties of health status measurement instruments: an international Delphi study. Quality of Life Research. 2010; 19(4):539-49. doi: 10. 1007/s11136-010-9606-8 PMID: 20169472
25. Walton MK, Powers JH III, Hobart J, Patrick D, Marquis P, Vamvakas S, et al. Clinical Outcome Assessments: Conceptual Foundation: Report of the ISPOR Clinical Outcomes Assessment-Emerging Good Practices for Outcomes Research Task Force. Value in Health. 2015; 18(6):741-52. doi: 10.1016/j.jval. 2015.08.006 PMID: 26409600
26. Pane M, Staccioli S, Messina S, D'Amico A, Pelliccioni M, Mazzone ES, et al. Daily salbutamol in young patients with SMA type II. Neuromuscular disorders: NMD. 2008; 18(7):536-40. Epub 2008/06/27. doi: 10.1016/j.nmd.2008.05.004 PMID: 18579379
27. World Health Organisation. ICF: international classification of functioning, disability and health / World Health Organization. Geneva: W.H.O.; 2001.
28. Scott E, Eagle M, Mayhew A, Freeman J, Main M, Sheehan J, et al. Development of a functional assessment scale for ambulatory boys with Duchenne muscular dystrophy. Physiother Res Int. 2012; 17(2):101-9. doi: 10.1002/pri.520 PMID: 21954141
29. Glanzman AM, Mazzone E, Main M, Pelliccioni M, Wood J, Swoboda KJ, et al. The Children's Hospital of Philadelphia Infant Test of Neuromuscular Disorders (CHOP INTEND): test development and reliability. Neuromuscular disorders: NMD. 2010; 20(3):155-61. Epub 2010/01/16. doi: 10.1016/j.nmd.2009. 11.014 PMID: 20074952
30. Mercuri E, Mayhew A, Muntoni F, Messina S, Straub V, Van Ommen GJ, et al. Towards harmonisation of outcome measures for DMD and SMA within TREAT-NMD; report of three expert workshops: TREAT-NMD/ENMC workshop on outcome measures, 12th-13th May 2007, Naarden, The Netherlands; TREAT-NMD workshop on outcome measures in experimental trials for DMD, 30th June-1st July 2007, Naarden, The Netherlands; conjoint Institute of Myology TREAT-NMD meeting on physical activity monitoring in neuromuscular disorders, 11th July 2007, Paris, France. Neuromuscular disorders: NMD. 2008; 18(11):894-903. Epub 2008/09/27. doi: 10.1016/j.nmd.2008.07.003 PMID: 18818076
31. Mazzone ES, Messina S, Vasco G, Main M, Eagle M, D'Amico A, et al. Reliability of the North Star Ambulatory Assessment in a multicentric setting. Neuromuscular disorders: NMD. 2009; 19(7):458-61.Epub 2009/06/26. doi: 10.1016/j.nmd.2009.06.368 PMID: 19553120
32. Hays RD, Morales LS, Reise SP. Item Response Theory and Health Outcomes Measurement in the21st Century. Medical care. 2000; 38(9 Suppl):II28-II42. PMID: 10982088
33. Chang CH, Reeve BB. Item response theory and its applications to patient-reported outcomes measurement. Evaluation & the health professions. 2005; 28(3):264-82. Epub 2005/08/27.
34. Reeve BB, Burke LB, Chiang YP, Clauser SB, Colpe LJ, Elias JW, et al. Enhancing measurement in health outcomes research supported by Agencies within the US Department of Health and Human Services. Quality of life research: an international journal of quality of life aspects of treatment, care and rehabilitation. 2007; 16 Suppl 1:175-86. Epub 2007/05/29.
35. Hobart JC, Cano SJ, Zajicek JP, Thompson AJ. Rating scales as outcome measures for clinical trials in neurology: problems, solutions, and recommendations. Lancet Neurol. 2007; 6(12):1094-105. Epub 2007/11/23. doi: 10.1016/S1474-4422(07)70290-9 PMID: 18031706
36. de Vet HC, Terwee CB, Mokkink LB, Knol DL. Measurement in medicine: a practical guide. Cambridge: Cambridge University Press; 2011.
37. Andrich D. Sufficiency and Conditional Estimation of Person Parameters in the Polytomous Rasch Model. Psychometrika. 2010; 75(2):292-308.
38. RUMM 2030 [computer program]. Perth, WA: RUMM Laboratory Pty Ltd; 1997-2012.
39. Wijnhoven TM, de Onis M, Onyango AW, Wang T, Bjoerneboe GE, Bhandari N, et al. Assessment of gross motor development in the WHO Multicentre Growth Reference Study. Food and nutrition bulletin. 2004; 25(1 Suppl):S37-45. Epub 2004/04/09. PMID: 15069918
40. IBM SPSS Statistics version 22 [computer program]. IBM Corporation; Release 22.0.0.0, 32 Bit edition 1989-2013.
41. Dubowitz V. Chaos in the classification of SMA: a possible resolution. Neuromuscular disorders: NMD. 1995; 5(1):3-5. Epub 1995/01/01. PMID: 7719138
42. Dubowitz V. Very severe spinal muscular atrophy (SMA type 0): an expanding clinical phenotype. European Journal of Paediatric Neurology. 1999; 3(2):49-51. PMID: 10700538
43. Munsat TL. International SMA Collaboration. Neuromuscular Disorders. 1991; 1(2):81.
44. Munsat TL, Davies KE. International SMA Consortium Meeting (26-28 June 1992, Bonn, Germany). Neuromuscular Disorders. 1992; 2(5):423-8.
45. McDonald CM, Henricson EK, Abresch RT, Florence JM, Eagle M, Gappmaier E, et al. The 6-minute walk test and other endpoints in Duchenne muscular dystrophy: longitudinal natural history observations over 48 weeks from a multicenter study. Muscle & nerve. 2013; 48(3):343-56. Epub 2013/05/18.
46. Goemans NM, Tulinius M, van den Hauwe M, Kroksmark AK, Buyse G, Wilson RJ, et al. Long-Term Efficacy, Safety, and Pharmacokinetics of Drisapersen in Duchenne Muscular Dystrophy: Results from an Open-Label Extension Study. PloS one. 2016; 11(9):e0161955. Epub 2016/09/03. doi: 10.1371/ journal.pone.0161955 PMID: 27588424