INTRODUCTION
Muscle contractures contribute to loss of joint range of motion and decreased functional movement for children with a diagnosis of cerebral palsy (CP).1,2 Stretching programs are an important component of physical therapy intervention with this group of children. The use of muscle stretching is based on the assumptions that stretching will increase muscle extensibility, preserve joint range of motion for functional movement, and prevent or delay the need for orthopedic surgical interventions.3,4 Physical therapists use various strategies for muscle stretching including: (1) passive stretching (the stretch is performed by another person and the child does not actively participate); (2) active stretching (the child initiates and/or maintains the stretch); or (3) prolonged positioning (positioning is used to achieve a longer duration stretch of a particular muscle or muscle group). All three techniques are often used in conjunction with other interventions such as splints and orthoses, serial casting, surgery, or spasticity reducing medications. Despite the widespread use of stretching as a physical therapy management strategy for children with CP, knowledge about the effectiveness of stretching techniques is limited for two reasons. First, the mechanisms and etiology of muscle contractures in children with CP are not well understood, making it difficult to determine if the theory underlying muscle stretching is correct. Second, clinical research evaluating the effectiveness of stretching techniques with children with CP is inconclusive and cannot guide therapists’ clinical decision making.
In this article, we review current knowledge of both the underlying mechanisms of muscle contracture and the effectiveness of stretching strategies with children with CP. We also present the results of a survey of stretching practices conducted with pediatric physical therapists in Canada. We conclude with a discussion of considerations for community-based approaches to flexibility and fitness and some suggestions for directions of future research.
Mechanisms of Muscle Contracture with Children with CP
Increased muscle tone and poor selective motor control affect many children with CP and both of these impairments may contribute to decreased frequency and variety of voluntary movement.5 It is assumed that reduced movement contributes to a decrease in muscle belly length due to an adaptive response of the muscle involving a reduction in the number of in-series sarcomeres.6 However, little is actually known about the structural and mechanical changes that occur within the muscles of children with spasticity. Knowledge about the physiological mechanisms involved in contracture development has the potential to inform intervention strategies used in pediatric physical therapy.
Traditional theories of muscle contracture development were based on classic animal model studies performed in the 1970s by a group of researchers in France.7–12 These researchers evaluated differential responses of cat and rodent muscles to immobilization in different positions. When the soleus muscles in these animal models were immobilized in a shortened position, the muscles adapted by a shortening of the muscle fibers because of a significant reduction (up to 40%) in the number of in-series sarcomeres.7 When the soleus muscles were immobilized in elongated positions, the muscles adapted by increasing the number of in-series sarcomeres. These studies provided evidence that the soleus muscles of these animals responded to joint immobilization by modifying the number of in-series sarcomeres. The results of these animal model studies have been extrapolated to explain human muscle response to immobilization, but there has not been rigorous evaluation of the assumption that human muscles respond similarly to the animal models.6 In a well-known study with children with CP, Tardieu et al13 observed increased muscle hypoextensibility (resistance to passive stretch) in the triceps surae muscles compared with muscles of typically developing children and concluded that decreased muscle extensibility was the result of the adaptive response (ie, reduction of the number of in-series sarcomeres) observed in the animal models. They did not, however, directly measure either muscle fiber length or the number of sarcomeres to confirm this theory of muscle contracture.
The only definitive method of determining muscle fiber length is to dissect fibers from whole muscles. For obvious reasons, this invasive technique is not used with humans.6 Alternate methods have been developed to measure muscle fiber length in spastic muscles of children with CP. Lieber et al14 used an intraoperative laser diffraction technique to compare the sarcomere length of the flexor carpi ulnaris muscles of individuals with wrist flexion contractures (ie, 5 children with CP and 1 adult with spasticity) and 12 participants without disabilities. Their data suggested that sarcomere length of the individuals with spasticity was increased whereas serial sarcomere number and muscle fiber length were not different from the control group. Ultrasound has also been used to measure muscle fiber length of children with CP.15,16 Shortland et al16 measured the muscle thickness and deep fascicle angle (angles at which fascicles arise from the deep aponeurosis) of the medial gastrocnemii muscles of 5 adults without disabilities (24 to 36 years), 7 children with spastic diplegic CP (6 to 13 years), and 5 children without disabilities (7 to 11 years). Deep fascicle angles of the children with spastic diplegia were reduced significantly compared with the control group, but the actual muscle fiber length did not differ between the two groups. Both of these studies14,16 suggest that the underlying mechanism of muscle contracture is not a reduction of in-series sarcomeres. Shortland et al16 hypothesized that the gastrocnemii muscle bellies are shortened in individuals with CP because of muscle fiber atrophy rather than decreased sarcomere length or decreased number of in-series sarcomeres. Because the gastrocnemius is a pinnate muscle composed of fibers that run at an angle to the force generated, a decrease in muscle fiber diameter could conceivably contribute to muscle belly shortening. Mohagheghi et al.15 used the same ultrasound technique and found that gastrocnemii muscle thickness was reduced in the involved legs compared with the uninvolved legs of 8 children with spastic hemiplegia. However, in contrast to Shortland et al, Mohagheghi et al reported that muscle fascicle lengths were reduced in the involved legs. The authors concluded that their data may support a reduction of both in-series and in parallel sarcomeres in the involved gastrocnemii of children with spastic hemiplegia.
Our understanding regarding the mechanism of contracture in spastic muscles is limited. The studies reviewed here suggest different underlying mechanisms of muscle shortening: reduction of the number of in-series sarcomeres, reduction of in-parallel sarcomeres, and muscle fiber atrophy. The traditional theory that decreased movement causes muscle shortening by reduction of the number of in-series sarcomeres supports classic stretching of the muscles, whereas the explanation of muscle fiber atrophy would indicate the use of muscle strengthening techniques to prevent or reduce contractures. If muscle fiber atrophy is associated with muscle contracture, resistance training and electrical stimulation will need to be explored as strategies for contracture treatment. More information is needed about the mechanisms of muscle contracture to guide selection of the most appropriate intervention choices.
Clinical Research on Muscle Stretching
Pin et al17 recently conducted a systematic review to summarize the evidence regarding efficacy of passive stretching with children with CP. We conducted a similar search of the literature, but expanded the search to include studies that evaluated the effects of active stretching. The search was limited to published studies, available in English and included the following electronic databases: Cinahl (1937 to June 2007), EMBASE (1988 to June 2007), MEDLINE (1950 to June 2007), PsycINFO (1985 to June 2007), and Scopus (1960 to June 2007). Search terms used were “cerebral palsy” combined with “range of motion,” “stretching,” “contracture,” and “positioning.” One hundred eleven articles were identified and 104 studies were excluded because they were not intervention studies, participants were not children, the studies evaluated serial casting or the effects of splints and orthoses, or stretching was used in conjunction with pharmacological or surgical interventions.
The literature on passive stretching, active stretching, and therapeutic positioning is summarized in Tables 1 and 2. Each study was rated by its level of evidence (Table 1), which categorizes the strength of the study by its research design, and studies with greater internal validity (levels of evidence I–III) also received a conduct rating evaluating potential threats to internal validity (Table 2). The levels of evidence and conduct rating criteria were developed by the American Academy for Cerebral Palsy and Developmental Medicine.18 The paucity of studies and the lack of methodologically rigorous evaluation of existing studies are evident. Adequately powered, randomized controlled trials have not been conducted, and the single subject design studies have not been replicated. In addition, of the group studies included in Table 1, only 3 studies19,20,21 demonstrated any statistically significant treatment effects. The stretching techniques evaluated differed on the stretching time and number of repetitions, suggesting no standardization of stretching techniques. Despite the current clinical focus on functional (activity and participation level) outcomes, most of the research to date has focused on impairment level outcomes such as joint range of motion and spasticity. Only one study22 evaluated active stretching for children with CP; treatment effects were not demonstrated.
TABLE 1: Summary of Studies—Interventions, Participants, and Results
TABLE 2: Conduct of Study (for Levels I, II, and III Group Designs Only)
No strong conclusions about the effects of passive stretching, active stretching, or therapeutic positioning on joint range of motion in individuals with CP can be reached from this body of research. As Pin et al17 reported, the research in this area is weak because of methodological issues, small sample sizes, and the existence of only a small number of studies. In addition, there has been little attention in the research literature to the evaluation of active stretching with children with CP as demonstrated by the one study in our review that evaluated active stretching.22
Current Stretching Practices—A Survey of Canadian Pediatric Rehabilitation Centers
We invited 46 Canadian rehabilitation centers to respond to a survey to identify stretching practices with children with CP; 26 sites responded (response rate 56.5%). The survey included questions about the prevalence of passive, active, and therapeutic positioning strategies used by therapists at each centre, the stretching parameters typically used (duration and frequency of stretches), specific muscle groups targeted, and the therapists’ goals for stretching. The therapists at each site completed the survey collaboratively, resulting in one completed survey from each participating centre.
Sites reported that therapists spend approximately 10% (median) of their time (range 5%–33%) performing stretching techniques and 15% (median) of their time (range 1%–25%) teaching children, parents, and caregivers how to stretch. Therapists select specific stretching techniques (passive, active, or positioning) by considering a variety of factors including age of the child, severity of spasticity and contracture, perceived compliance of child and/or caregiver, tolerance and/or motivation for stretching, cognitive level of the child, functional abilities of the child as rated by the Gross Motor Function Classification System,26 and the child’s environment.
Therapeutic positioning and active stretching are frequently used for the hip flexors, hip adductors, knee flexors, and ankle plantarflexors. Passive stretching was reported as a prevalent management strategy for all muscle groups, particularly the hip flexors, hip adductors, knee flexors, and ankle plantar flexors. Choice of stretching approach did not vary with age of the child. The parameters for stretching intervention varied considerably across the reporting sites. The number of repetitions for passive stretching ranged from 1 to 10 (median = 4), the length of time to hold the stretch varied from 15 to 90 seconds (median = 30). Parameters for active stretching ranged from 1 to 10 repetitions (median = 4) and 15 to 90 seconds duration (median = 21). The reasons for using stretching techniques were to (1) maintain current range of motion (all sites); (2) increase range of motion for functional tasks (all sites); (3) defer or avoid surgery (12 of 26 sites); and (4) attain full range of motion (11 of 26 sites). This small survey suggests a lack of standardization of stretching techniques. The common assumption across all sites is that stretching will maintain range of motion and may positively affect functional abilities. Many of the sites also assumed that stretching may delay or avoid surgical intervention for muscle contractures. Research studies have not confirmed these assumptions and therefore it is evident that a significant gap exists between clinical rationale for stretching and research evidence.
DISCUSSION
Our understanding of the mechanisms of contractures in spastic muscles is rudimentary. Ideally our clinical decisions should be guided by good scientific inquiry.27 There is a need for laboratory research into the mechanisms of muscle contracture to provide additional information about the theoretical assumptions that guide physical therapy interventions for children with CP.
Clinical evaluation of the effects of stretching techniques is also needed because existing research evidence is not adequate to support or refute the effectiveness of stretching as a management strategy. Pediatric physical therapists have an essential role to play in this area of evaluation. The primary outcome evaluated in studies examining the effects of passive stretching in individuals with CP has been joint range of motion. Goniometric measurements are appropriate because the primary outcome expected with stretching is a change in muscle length and joint range of motion. Therapists use stretching interventions for children with CP with the assumption that the stretching program will not only assist with maintenance of joint range of motion, but positively impact the functional abilities of the child. Many therapists also use stretching to avoid or delay the development of secondary complications. The current body of research on stretching does not include any investigation of the relationship between changes of joint range of motion and changes in functional abilities or need for surgery. The International Classification of Functioning, Disability and Health (ICF)28 explicitly cautions against assuming a direct relationship between factors at the component of body function and structure (eg, range of motion, spasticity) and changes at the component of activity (eg, dressing or riding a bike) and participation (e.g. integration in classroom activities). For example, maintaining a child’s hamstring length may not make it any easier for him to get on and off the school bus (activity) or to participate in gym class at school (participation). A recent study evaluated the interrelationships among muscle tone, passive range of motion, selective motor control, and gross motor function in a group of children with CP and reported only a modest relationship between motor impairments and participation in everyday activities.29 It is essential that future research includes the evaluation of the relationships among outcomes representing body functions and structures, activity and participation to determine both the physiological and functional outcomes of stretching programs, particularly because enhancing functional abilities is one of the reasons why therapists use stretching as a clinical intervention.
Another reason to consider alternative outcomes is the documented measurement error of goniometry with children with a diagnosis of CP. McDowell et al30 reported significant variability with measurements errors as high as 14° for 3 of the 6 range of motion measurements with 12 children with spastic diplegia. Other researchers have also reported significant measurement error using goniometry to measure joint range of motion with children with CP.31–33 Researchers need to consider more precise ways of measuring joint range of motion and the use of different outcome measures to document changes in children’s functioning.
Passive stretching is, by its very nature, a “passive” technique that is done without the child’s participation. Isolated active stretching and positioning practices such as prone lying and stretching hamstrings in long sitting are also not particularly fun for the child or family. Parents may be hesitant to use traditional stretching techniques as they may be uncomfortable for their children34 and they may already be overwhelmed by a number of other interventions their children require. Contemporary approaches to rehabilitation for children with CP are changing to include community participation, fitness, and functional goals35–37 and therapists are challenged to explore innovative management approaches that reflect these values. Perhaps the focus on maintaining joint range of motion needs to change to an emphasis on maintaining flexibility and encouraging the exploration and maintenance of a variety of movement options. All children, including children with physical disabilities, need to have opportunities to engage in physical activities that will enhance their levels of physical fitness. They also need opportunities to participate in fun activities with other children. From this perspective, the emphasis on joint range of motion changes to a focus on encouraging movement opportunities that enable children with CP to experience a repertoire of movement experiences and participate in enjoyable activities while enhancing their physical fitness. Therapists may want to consider activities such as yoga, Tai Chi, horseback riding, ballet, and swimming programs that allow children to stretch and move within a functional, participatory context. Through such programs, children with CP could become active participants in fitness programs that encourage flexibility instead of passive recipients of therapeutic stretching routines. Therapists can use their expertise to identify innovative flexibility options that are enjoyable for everyone and will lead to life long fitness opportunities for the child.38
Physical therapists possess the knowledge of development, movement, and CP to assist children and adolescents with CP to participate in community fitness programs. Therapists can play an important role in the development of transitional programs in rehabilitation centers, in which typical fitness programs are adapted to meet individual movement abilities. Therapists can also help families to identify community programs and provide support for the transition to these programs. Therapists can work with families and community fitness facilities to encourage children and adolescents with CP to integrate flexibility exercises into their regular fitness routines and to modify program content so that children and youth with motor disabilities can participate effectively and safely. Our experience with a community-based fitness program for children and adolescents with CP21 convinced us that community fitness programs are a viable alternative to medically oriented therapy programs. It is an exciting time in pediatric rehabilitation and an ideal time for therapists to use their creativity, knowledge, and skills to develop innovative and fun strategies to integrate therapy with fun physical activities and to contribute to the rigorous evaluation of stretching strategies used in pediatric rehabilitation.
ACKNOWLEDGMENTS
The authors express their appreciation to Monica Gorassini, PhD, and the two anonymous reviewers for their valuable suggestions that improved this manuscript.
REFERENCES
1. Pirpiris M, Graham HK. Management of spasticity in children. In: Barnes MP, Johnson GR, eds.
Upper Motor Neurone Syndrome and Spasticity: Clinical Management and Neurophysiology. Cambridge: Cambridge University Press; 2001:266–305.
2. Wilson JM. Cerebral palsy. In: Campbell SK, ed.
Clinics in Physical Therapy: Pediatric Neurologic Physical Therapy. 2nd ed. New York: Churchill Livingstone; 1991:301–360.
3. Holt S, Baagoe S, Lillelund F, et al. Passive resistance of the hamstring muscles in children with severe multiple disabilities?
Dev Med Child Neurol. 2000;42:541–544.
4. Olney SJ, Wright MJ. Cerebral palsy. In: Campbell SK, Vander Linden DW, Palisano RJ, eds.
Physical Therapy for Children. 2nd ed. Philadelphia: WB Saunders Co.; 2000.
5. Wilson-Howle JM. Cerebral palsy. In: Campbell SK, ed.
Decision Making in Pediatric Neurologic Physical Therapy. New York: Churchill Livingstone; 1999:23–83.
6. Lieber RL, Steinman S, Barash IA, et al. Structural and functional changes in spastic skeletal muscle.
Muscle Nerve. 2004;29:615–627.
7. Tabary JC, Tabary C, Tardieu C, et al. Physiological and structural changes in the cat’s soleus muscle due to immobilization at different lengths by plaster casts.
J Physiol (Lond). 1972;224:231–244.
8. Huet de la Tour E, Tardieu C, Tabary JC, et al. Decrease of muscle extensibility and reduction of sarcomere number in soleus muscle following a local injection of tetanus toxin.
J Neurol Sci. 1979;40:123–131.
9. Huet de la Tour E, Tabary JC, Tabary C, et al. The respective roles of muscle length and muscle tension in sarcomere number adaptation of guinea-pig soleus muscle.
J Physiol (Paris). 1979;75:589.
10. Hayat A, Tardieu C, Tabary C. Left cortical lesion and soleus muscle sarcomere number.
Brain Res. 1979;167:408.
11. Tardieu G, Tabary JC, Tardieu C, et al. Proceedings: influence of plaster-caste immobilization on the length of peroneus profundus muscle fibers in the cat. Comparative study on the soleus.
J Physiol (Paris). 1973;67:359A.
12. Tabary JC, Tabary C, Tardieu C, et al. Physiological and structural changes in the cat’s soleus muscle due to immobilization at different lengths by plaster casts.
J Physiol (Lond). 1972;224:231.
13. Tardieu C, Huet de la Tour E, Bret M, et al. Muscle hypoextensibility in children with cerebral palsy: I. Clinical and experimental observations.
Arch Phys Med Rehabil. 1982;63:97–102.
14. Lieber RL, Friden J. Spasticity causes a fundamental rearrangement of muscle-joint interaction.
Muscle Nerve. 2002;25:265–270.
15. Mohagheghi AA, Khan T, Meadows TH, et al. Differences in gastrocnemius muscle architecture between the paretic and non-paretic legs in children with hemiplegic cerebral palsy.
Clin Biomech. 2007;22:718–724.
16. Shortland AP, Harris CA, Gough M, et al. Architecture of the medial gastrocnemius in children with spastic diplegia.
Dev Med Child Neurol. 2002;44:158–163.
17. Pin T, Dyke P, Chan M. The effectiveness of passive stretching in children with cerebral palsy.
Dev Med Child Neurol. 2006;48:855.
18. Treatment Outcomes Committee of the American Academy for Cerebral Palsy and Developmental Medicine.
AACPDM Methodology to Develop Systematic Reviews for Treatment Interventions (Revision 1.1). 2004. Available at:
http://www.aacpdm.org/resources/systematicReviewsMethodology.pdf. Accessed October 31, 2007.
19. Tremblay F, Malouin F, Richards CL, et al. Effects of prolonged muscle stretch on reflex and voluntary muscle activations in children with spastic cerebral palsy.
Scand J Rehabil Med. 1990;22:171–180.
20. Richards CL, Malouin F, Dumas F. Effects of a single session of prolonged plantarflexor stretch on muscle activations during gait in spastic cerebral palsy.
Scand J Rehabil Med. 1991;23:103–111.
21. O’Dwyer N, Neilson P, Nash J. Reduction of spasticity in cerebral palsy using feedback of the tonic stretch reflex: a controlled study.
Dev Med Child Neurol. 1994;36:770–786.
22. Darrah J, Wessel J, Nearingburg P, et al. Evaluation of a community fitness program for adolescents with cerebral palsy.
Pediatr Phys Ther. 1999;11:18–23.
23. Fragala MA, Goodgold S, Dumas HM. Effects of lower extremity passive stretching: pilot study of children and youth with severe limitations in self-mobility.
Pediatr Phys Ther. 2003;15:167–175.
24. McPherson JJ, Arends TG, Michaels MJ, et al. The range of motion of long term knee contractures of four spastic cerebral palsied children: a pilot study.
Phys Occup Ther Pediatr. 1984;4:17–34.
25. Miedaner JA, Renander J. The effectiveness of classroom passive stretching programs for increasing or maintaining passive range of motion in non-ambulatory children: an evaluation of frequency.
Phys Occup Ther Pediatr. 1987;7:35–43.
26. Palisano RJ, Rosenbaum P, Walter SD, et al. Development and reliability of a system to classify gross motor function in children with cerebral palsy.
Dev Med Child Neurol. 1997;39:214–223.
27. Whyte J, Hart T. It’s more than a black box; it’s a Russian doll: defining rehabilitation treatments.
Am J Phys Med Rehabil. 2003;82:639–652.
28. World Health Organization. International Classification of Functioning, Disability and Health (ICF). Geneva: WHO; 2001.
29. Ostensjo S, Carlberg EB, Vollestad NK. Motor impairments in young children with cerebral palsy: relationship to gross motor function and everyday activities.
Dev Med Child Neurol. 2004;46:580–589.
30. McDowell BC, Hewitt V, Nurse A, et al. The variability of goniometric measurements in ambulatory children with spastic cerebral palsy.
Gait Posture. 2000;12:114.
31. Watkins B, Darrah J, Pain K. Reliability of passive ankle dorsiflexion measurements in children: comparison of universal and biplane goniometers.
Pediatr Phys Ther. 1995;7:3–8.
32. Ashton BB, Pickles B, Roll JW. Reliability of goniometric measurements of hip motion in spastic cerebral palsy.
Dev Med Child Neurol. 1978;20:87–94.
33. Stuberg WA, Fuchs RH, Miedaner JA. Reliability of goniometric measurements of children with cerebral palsy.
Dev Med Child Neurol. 1988;30:657–666.
34. Hadden KL, von Baeyer CL. Pain in children with cerebral palsy: Common triggers and expressive behaviours.
Pain. 2002;99:23–83.
35. Helders PJM, Engelbert RHH, Custers JWH, et al. Creating and being created: the changing panorama of paediatric rehabilitation.
Pediatr Rehabil. 2003;6:5–12.
36. Palisano RJ, Snider LM, Orlin MN. Recent advances in physical and occupational therapy for children with cerebral palsy.
Semin Pediatr Neurol. 2004;11:66–77.
37. Darrah J, Law M, Pollock N. Family-centered functional therapy—a choice for children with motor dysfunction.
Infants Young Child. 2001;13:79–87.
38. Campbell SK. Therapy programs for children that last a lifetime.
Phys Occup Ther Pediatr. 1997;17:1–15.