Are spasticity, weakness, selectivity, and passive range of motion related to gait deviations in children with spastic cerebral palsy? A statistical parametric mapping study

Autoři: Eirini Papageorgiou aff001;  Cristina Simon-Martinez aff001;  Guy Molenaers aff003;  Els Ortibus aff003;  Anja Van Campenhout aff003;  Kaat Desloovere aff001
Působiště autorů: KU Leuven Department of Rehabilitation Sciences, Leuven, Belgium aff001;  Clinical Motion Analysis Laboratory, University Hospitals Leuven, Leuven, Belgium aff002;  KU Leuven Department of Development and Regeneration, Leuven, Belgium aff003;  Department of Orthopedics, University Hospitals Leuven, Leuven, Belgium aff004
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article


This study aimed to identify the relationships between clinical impairments and gait deviations in children with cerebral palsy (CP). A retrospective convenience sample of 367 children with CP was selected (3–18 years old) and divided in two groups based on clinical symptomatology [unilateral (uCP) / bilateral CP (bCP), (n = 167/200)]. All children underwent a three-dimensional gait analysis and a standardized clinical examination. Gait was inspected on a vector level (all sagittal motions combined), and an individual joint level (pelvis, hip, knee and ankle joint motions). Statistical non-parametric mapping was applied to identify specific parts of the gait cycle displaying relationships between the gait deviations of both groups and the impairment scores of spasticity, weakness, selectivity, and passive range of motion. Impairment scores were summarized in two ways: a) composite impairment scores (e.g. combined spasticity of all assessed muscles acting around the hip, knee and ankle joints) and b) joint specific impairment scores (e.g. spasticity of the muscles acting around the knee joint). Results showed that the vector and most of the individual motions were related to the composite scores. Direct and carry-over relationships were found between certain individual motions and joint impairment scores (around the same or neighboring joints, respectively). All correlations were more prominent for children with bCP compared to uCP, especially regarding the relationships of gait deviations with weakness and reduced selectivity. In conclusion, this study enabled the mapping of relationships between clinical impairments and gait deviations in children with CP, by identifying specific parts of the gait cycle that are related to each of these impairments. These results provide a comprehensive description of these relationships, while simultaneously highlighting the differences between the two CP groups. Integration of these findings could lead to a better understanding of the pathophysiology of gait deviations and, eventually, support individualized treatment planning.

Klíčová slova:

Ankle joints – Ankles – Gait analysis – Hip – Knee joints – Knees – Skeletal joints – Visual impairments


1. Gage JR, Schwartz M, Koop SE H., Novacheck TF. The Treatment of Gait Problems in Cerebral Palsy. Clinics in Developmental Medicine No. 164–165. Gage JR, editor. London, United Kingdom: Mac Keith Press; 2004. 448 p.

2. Nieuwenhuys A, Papageorgiou E, Schless S-H, De Laet T, Molenaers G, Desloovere K. Prevalence of joint gait patterns defined by a Delphi consensus study is related to gross motor function, topographical classification, weakness, and spasticity, in children with cerebral palsy. Front Hum Neurosci [Internet]. 2017 Apr;11(185). Available from:

3. Desloovere K, Molenaers G, Feys H, Huenaerts C, Callewaert B, Walle P Van de. Do dynamic and static clinical measurements correlate with gait analysis parameters in children with cerebral palsy? Gait Posture. 2006;24(3):302–13. doi: 10.1016/j.gaitpost.2005.10.008 16303305

4. Zhou JY, Lowe E, Cahill-Rowley K, Mahtani GB, Young JL, Rose J. Influence of impaired selective motor control on gait in children with cerebral palsy. J Child Orthop. 2019;13.

5. Van Campenhout A, Bar-On L, Aertbelien E, Huenaerts C, Molenaers G, Desloovere K. Can we unmask features of spasticity during gait in children with cerebral palsy by increasing their walking velocity? GAIT {&} POSTURE. 2014;39(3):953–7.

6. Chang CH, Chen YY, Yeh KK, Chen CL. Gross motor function change after multilevel soft tissue release in children with cerebral palsy. Biomed J [Internet]. 2017;40(3):163–8. Available from: doi: 10.1016/ 28651738

7. Bonnefoy-Mazure A, Sagawa Y, Pomero V, Lascombes P, De Coulon G, Armand S. Are clinical parameters sufficient to model gait patterns in patients with cerebral palsy using a multilinear approach? Comput Methods Biomech Biomed Engin [Internet]. 2016;19(7):800–6. Available from: doi: 10.1080/10255842.2015.1064112 26237712

8. Van Der Krogt MM, Doorenbosch CAM, Becher JG, Harlaar J. Dynamic spasticity of plantar flexor muscles in cerebral palsy gait. J Rehabil Med. 2010;42(7):656–63. doi: 10.2340/16501977-0579 20603696

9. Balzer J, Marsico P, Mitteregger E, van der Linden ML, Mercer TH, van Hedel HJA. Influence of trunk control and lower extremity impairments on gait capacity in children with cerebral palsy. Disabil Rehabil [Internet]. 2017;0(0):1–7. Available from:

10. Meyns P, Van Gestel L, Leunissen I, De Cock P, Sunaert S, Feys H, et al. Macrostructural and Microstructural Brain Lesions Relate to Gait Pathology in Children With Cerebral Palsy. Neurorehabil Neural Repair [Internet]. 2016; Available from:

11. Holmes SJ, Mudge AJ, Wojciechowski EA, Axt MW, Burns J. Impact of multilevel joint contractures of the hips, knees and ankles on the Gait Profile score in children with cerebral palsy. Clin Biomech [Internet]. 2018;59(November 2017):8–14. Available from:

12. Rozumalski A, Schwartz MH. Crouch gait patterns defined using k-means cluster analysis are related to underlying clinical pathology. Gait Posture [Internet]. 2009 Aug [cited 2014 May 20];30(2):155–60. Available from: doi: 10.1016/j.gaitpost.2009.05.010 19535249

13. Chruscikowski E, Fry NRD, Noble JJ, Gough M, Shortland AP. Selective motor control correlates with gait abnormality in children with cerebral palsy. Gait Posture [Internet]. 2017 Feb;52:107–9. Available from: doi: 10.1016/j.gaitpost.2016.11.031 27889619

14. Krautwurst BK, Wolf SI, Heitzmann DWW, Gantz S, Braatz F, Dreher T. The influence of hip abductor weakness on frontal plane motion of the trunk and pelvis in patients with cerebral palsy. Res Dev Disabil [Internet]. 2013 Apr;34(4):1198–203. Available from: doi: 10.1016/j.ridd.2012.12.018 23396196

15. Baker R, Esquenazi A, Benedetti MG, Desloovere K. Gait analysis: clinical facts. Eur J Phys Rehabil Med. 2016;52(August):560–74.

16. Rose J. Neuromuscular correlates of motor function in cerebral palsy: towards targeted treatment. Dev Med Child Neurol [Internet]. 2018;1–2. Available from:

17. Armand S, Decoulon G, Bonnefoy-Mazure A. Gait analysis in children with cerebral palsy. EFORT Open Rev [Internet]. 2016;1(12):448–60. Available from: 28698802

18. Zhou J, Butler EE, Rose J. Neurologic Correlates of Gait Abnormalities in Cerebral Palsy: Implications for Treatment. Front Hum Neurosci [Internet]. 2017;11(March):1–20. Available from:

19. Nieuwenhuys A, Papageorgiou E, Pataky T, De Laet T, Molenaers G, Desloovere K, et al. Literature review and comparison of two statistical methods to evaluate the effect of botulinum toxin treatment on gait in children with cerebral palsy. PLoS One [Internet]. 2016;11(3):e0152697. Available from: doi: 10.1371/journal.pone.0152697 27030973

20. Crosbie J, Alhusaini AAA, Dean CM, Shepherd RB. Plantarflexor muscle and spatiotemporal gait characteristics of children with hemiplegic cerebral palsy: An observational study. Dev Neurorehabil. 2012;15(2):114–8. doi: 10.3109/17518423.2011.643927 22494083

21. Hoffman RM, Corr BB, Stuberg WA, Arpin DJ, Kurz MJ. Changes in lower extremity strength may be related to the walking speed improvements in children with cerebral palsy after gait training. Res Dev Disabil. 2018;73(November 2017):14–20. doi: 10.1016/j.ridd.2017.12.005 29245044

22. Øtensjø S, Carlberg EB, Vøllestad NK. Motor impairments in young children with cerebral palsy: Relationship to gross motor function and everyday activities. Dev Med Child Neurol [Internet]. 2004;46(9):580–9. Available from: doi: 10.1017/s0012162204000994 15344517

23. Pataky TC, Vanrenterghem J, Robinson MA. The probability of false positives in zero-dimensional analyses of one-dimensional kinematic, force and EMG trajectories. J Biomech [Internet]. 2016;49(9):1468–76. Available from: doi: 10.1016/j.jbiomech.2016.03.032 27067363

24. Pataky TC, Robinson MA, Vanrenterghem J. Vector field statistical analysis of kinematic and force trajectories. J Biomech [Internet]. 2013;46(14):2394–401. Available from: doi: 10.1016/j.jbiomech.2013.07.031 23948374

25. Goudriaan M, Van den Hauwe M, Simon-Martinez C, Huenaerts C, Molenaers G, Marleen H, et al. Gait deviations in Duchenne muscular dystrophy—Part 2. Statistical non-parametric mapping to analyze gait deviations in children with Duchenne muscular dystrophy. Gait Posture [Internet]. 2018;63(April):159–64. Available from:

26. Simon-Martinez C, Jaspers E, Mailleux L, Desloovere K, Vanrenterghem J, Ortibus E, et al. Negative influence of motor impairments on upper limb movement patterns in children with unilateral cerebral palsy. A statistical parametric mapping study. Front Hum Neurosci. 2017;11(October).

27. Dobson F, Morris ME, Baker R, Graham HK. Gait classification in children with cerebral palsy: a systematic review. Gait Posture [Internet]. 2007 Jan [cited 2014 May 8];25(1):140–52. Available from: doi: 10.1016/j.gaitpost.2006.01.003 16490354

28. Papageorgiou E, Nieuwenhuys A, Vandekerckhove I, Van Campenhout A, Ortibus E, Desloovere K. Systematic review on gait classification in children with cerebral palsy: an update. Gait posture [under Revis. 2018;

29. Gómez-Pérez C, Font-Llagunes JM, Martori JC, Vidal Samsó J. Gait parameters in children with bilateral spastic cerebral palsy: a systematic review of randomized controlled trials. Dev Med Child Neurol [Internet]. 2018;1–13. Available from:

30. McGinley JL, Baker R, Wolfe R, Morris ME. The reliability of three-dimensional kinematic gait measurements: A systematic review. Gait Posture. 2009 Apr;29(3):360–9. doi: 10.1016/j.gaitpost.2008.09.003 19013070

31. Kainz H, Graham D, Edwards J, Walsh HPJ, Maine S, Boyd RN, et al. Reliability of four models for clinical gait analysis. Gait Posture [Internet]. 2017;54(March):325–31. Available from:

32. Ferrari A, Benedetti MG, Pavan E, Frigo C, Bettinelli D, Rabuffetti M, et al. Quantitative comparison of five current protocols in gait analysis. Gait Posture. 2008;28(2):207–16. doi: 10.1016/j.gaitpost.2007.11.009 18206374

33. Davis RB, Ounpuu S, Tyburski D, Gage JR. A gait analysis data collection and reduction technique. Hum Mov Sci. 1991;10(5):575–87.

34. Schwartz MH, Trost JP, Wervey R a. Measurement and management of errors in quantitative gait data. Gait Posture. 2004;20(2):196–203. doi: 10.1016/j.gaitpost.2003.09.011 15336291

35. Bohannon RW, Smith MB. Interrater Reliability of a Modifies Ashworth Scale of Muscle Spasticity. Phys Ther. 1987;67(1):206–7.

36. Hislop H, Montgomery J. Daniels and Worthingham’s Muscle Testing: Techniques of Manual Examination. 8th ed. Saunders; 2007. 496 p.

37. Gage JR, Schwartz M. Pathological gait and lever-arm dysfunction. In: Gage JR, editor The treatment of gait problems in cerebral palsy Clinics in Developmental Medicine No 164–165. London, United Kingdom: Mac Keith Press; 2004. p. 180–204.

38. Trost J. Physical assessment and observational gait analysis. In: Gage JR, editor The treatment of gait problems in cerebral palsy Clinics in Developmental Medicine No 164–165. London, United Kingdom: Mac Keith Press; 2004. p. 71–89.

39. Hobbs SJ, Robinson MA, Clayton HM. A simple method of equine limb force vector analysis and its potential applications. PeerJ [Internet]. 2018;6:e4399. Available from: doi: 10.7717/peerj.4399 29492341

40. Pataky TC. One-dimensional statistical parametric mapping in Python. Comput Methods Biomech Biomed Engin [Internet]. 2012;15(3):295–301. Available from: 21756121

41. Nieuwenhuys A, Õunpuu S, Van Campenhout A, Theologis T, De Cat J, Stout J, et al. Identification of joint patterns during gait in children with cerebral palsy: A Delphi consensus study. Dev Med Child Neurol [Internet]. 2016 Mar;58(3):306–13. Available from: doi: 10.1111/dmcn.12892 26330338

42. Wolf SI, Mikut R, Kranzl A, Dreher T. Which functional impairments are the main contributors to pelvic anterior tilt during gait in individuals with cerebral palsy? Gait Posture [Internet]. 2014 Jan [cited 2014 May 7];39(1):359–64. Available from: doi: 10.1016/j.gaitpost.2013.08.014 24054350

43. Õunpuu S. Patterns of gait pathology. In: Gage JR, editor The treatment of gait problems in cerebral palsy Clinics in Developmental Medicine No 164–165. London, United Kingdom: Mac Keith Press; 2004. p. 217–37.

44. Crenna P. Spasticity and “spastic” gait in children with cerebral palsy. Neurosci Biobehav Rev. 1998;22(4):571–8. 9595571

45. van den Noort JC, Bar-On L, Aertbeliën E, Bonikowski M, Braendvik SM, Broström EW, et al. European consensus on the concepts and measurement of the pathophysiological neuromuscular responses to passive muscle stretch. Eur J Neurol. 2017;24(7):981–e38. doi: 10.1111/ene.13322 28557247

46. Goudriaan M, Nieuwenhuys A, Schless SH, Goemans N, Molenaers G, Desloovere K. A new strength assessment to evaluate the association between muscle weakness and gait pathology in children with cerebral palsy. PLoS One. 2018;13(1):1–22.

47. Fowler EG, Staudt LA, Greenberg MB, Oppenheim WL. Selective Control Assessment of the Lower Extremity (SCALE): development, validation, and interrater reliability of a clinical tool for patients with cerebral palsy. Dev Med Child Neurol. 2009 Aug;51(8):607–14. doi: 10.1111/j.1469-8749.2008.03186.x 19220390

48. Cuthbert SC, Goodheart GJ Jr. On the reliability and validity of manual muscle testing: a literature review. Chiropr Osteopat. 2007;15(4):9–15.

49. Mutlu A, Livanelioglu A, Gunel MK. Reliability of Ashworth and Modified Ashworth scales in children with spastic cerebral palsy. BMC Musculoskelet Disord. 2008;9:44. doi: 10.1186/1471-2474-9-44 18402701

50. Sangeux M, Wolfe R, Graham HK. One side or two? Dev Med Child Neurol. 2013;55(9):786–7. doi: 10.1111/dmcn.12230 23924082

51. Rethlefsen SA, Kay RM. Transverse plane gait problems in children with cerebral palsy. J Pediatr Orthop [Internet]. 2013;33(4):422–30. Available from: doi: 10.1097/BPO.0b013e3182784e16 23653033

52. Rethlefsen SA, Blumstein G, Kay RM, Dorey F, Wren TAL. Prevalence of specific gait abnormalities in children with cerebral palsy revisited: influence of age, prior surgery, and Gross Motor Function Classification System level. Dev Med Child Neurol [Internet]. 2017;59(1):79–88. Available from: doi: 10.1111/dmcn.13205 27421715

53. Chung CY, Lee KM, Park MS, Lee SH, Choi IH, Cho TJ. Validity and reliability of measuring femoral anteversion and neck-shaft angle in patients with cerebral palsy. J Bone Jt Surg—Ser A. 2010;92(5):1195–205.

Článek vyšel v časopise


2019 Číslo 10
Nejčtenější tento týden