L E T T E R S

To the Editor: Chiu and Ada’s review article1 is welcome as they point out that various methods for using electrical stimulation (ES) are available; however, they only focus on 2 methods. These authors were interested in doing a high-quality system meta-analysis to see whether using functional electrical stimulation (FES) during an activity was better than working on activity training alone. It was somewhat surprising that so few studies in this area were found that they could not do as they had wished. Only a few articles on ES with children were found, but limiting a search to articles that use the acronym FES may further limit the search. ES has many acronyms. And as a result understanding the various ES methods becomes confusing. Initially ES was applied to strengthen muscles, improve range of motion, decrease spasticity, and was called neuromuscular electrical stimulation (NMES). Neuromuscular electrical stimulation was usually used during physical therapy, which also includes goals to increase function and alignment. Later when NMES was used to replace an ankle brace or an arm sling, it was called FES and considered a subtype of NMES. There are no rules that say that FES and NMES have specific or different application parameters, or muscles to which they might be applied, or the timing of the muscle contraction (ie, within a functional context), which could then distinguish one form of ES from the other. Sometimes the acronym FES was not used in publications even when stimulation was given functionally or task specifically as FES was considered to be a brace substitute.2,3 For example, van der Linden’s later study used the term ES; they did not use FES or NMES.4 In this letter, the acronym ES is used to include all uses of electrical stimulation. Electrical stimulation has various names and methods, which makes evaluation to determine which is most beneficial for improving function difficult. Four basic variables need to be considered when ES is used to promote muscle contraction to improve function and alignment. These are: (1) the muscle(s) being stimulated, (2) ES parameters (including pulse duration, waveform, frequency, and amplitude), (3) whether the timing of stimulation is given in the context of the specific task or not, and (4) whether the ankle and foot joints are blocked when ES is used to improve gait. These 4 variables need to be studied Pediatric Physical Therapy

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and compared across different studies. Not considering all 4 of these variables in a meta-analysis may obscure the effects of ES and confuse the outcomes. Muscle choice is critical but is surrounded by controversy. For example, for those with an equinus or drop foot, the controversy lies between choosing to stimulate the antagonist to the spastic muscle or the spastic muscle itself. Those ascribing to each viewpoint say that they are stimulating the weaker muscle. In the past, spastic muscles were thought to be stronger than their antagonists and to prevent their antagonists from functioning. However, in the past 20 or more years, studies have shown that spastic muscles are weaker than their antagonists,5,6 and so it is not logical to assume that the weaker muscle prevents the stronger muscle’s function. Chiu and Ada found only 3 systematic reviews related to this issue and preferred Cauraugh and colleague’s systematic study.7 Cauraugh and colleagues mentioned that there were those who stimulated the tibialis anterior and those that stimulated the calf. Consistent and potentially profound walking effects from calf stimuation were shown, as well as benefits on long-term function and structure3,8 ; however, these results were overshadowed by larger studies of FES to the peroneal nerve, which failed to find benefits. The review did not compare or study the effect of the differences in muscles being studied. It could be very enlightening to compare one group of children receiving ES to the tibialis anterior and another group receiving ES to the medial gastrocnemius muscle according to the typical gait timing without blocking the ankle or metatarsal joints. Because parameter settings can effect muscle contraction, they need to be evaluated when studying effects of ES. In addition, pulse duration is inversely proportional so that when pulse duration is shortened, amplitude must be increased to get the same contraction response. Increasing the amplitude leads to discomfort. Initially when ES was used in clinics, the pulse durations of NMES units could not be changed. They were fixed at 280 to 300 mμs. Later lowering the pulse duration was incorrectly thought to lead to more comfort as sensation and contraction levels are further apart in the strength duration curves. This increase of discomfort when pulse duration is shortened and amplitude is raised seems to have occurred in the van der Linden study where pulse duration was shortened.4 The Letters to the Editor

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gluteus maximus muscle’s strength and hip extension did not improve statistically or clinically. Perhaps this was because children experiencing a lower pulse duration could not tolerate an amplitude high enough to obtain adequate muscle contraction. In my clinic, children using ES with the pulse duration at 300 to 400 mμs applied to the gluteus maximus do achieve visible muscle contraction on a regular basis. In the Hazlewood article when ES with a pulse duration of 280 to 300 mμs was applied to the tibialis anterior, passive and active dorsiflexion was improved, but not gait.9 Neither study used ES appropriately timed within the context of the task. Chiu and Ada had expected the intensity of ES to be high enough to move a body part. Raising the amplitude to have approximately 68% of maximal voluntary contraction (MVC) to cause body part movement would likely be much above patient tolerance levels, which is a standard limiting factor for NMES. This requirement may make the stimulation so uncomfortable that the child might withdraw from therapy or a study. However, more importantly in adults it has been shown that a high MVC is not helpful and better results are found with 15% of MVC.10 Case studies may be an easier place to first study high-amplitude stimulation that results in limb movement as an individual child’s reactions can be observed and addressed. Other reasons for not using high-intensity stimulation are that muscles are of different types and sizes and function differently. High-intensity NMES can cause joint or body movement when given to calf muscles during gait and might increase plantar flexion and prevent increased dorsiflexion such that the child would probably not walk with a plantar grade foot as would occur when the intensity is not so high.2 The timing of the stimulation should be appropriate to the task. Parameter settings may also affect the timing. Some studies have used constant stimulation; some stimulated at set times within the task and some used a handheld remote switch to more appropriately time stimulation according to the task. If the timing of stimulation is set to be on and off for a set pattern, likely the timing will not match the child’s activities, as no one walks with an exact set time pattern. Thus, stimulation would occur while the child is active but not at an appropriate time within the context of the task. Furthermore, if the stimulation intensity is ramped up, the peak of the stimulation may not arrive at the muscle at the appropriate time. Providing NMES to the muscle while the child is active but without regard to the specifics of the task would not seem to result in appropriate motor learning. The last variable that must be considered is whether the ankle joint or metatarsal joints are prevented from movement during gait. It has been shown that orthoses may not be better than shoes,11 and that they can also prevent more typical movement and the child may then compensate with unwanted movement. This unwanted movement might be misconstrued to be a result of the upper motor lesion and not a result of the orthoses.12 488

Letters to the Editor

This letter is a plea for anyone planning to examine ES to compare groups using the same 4 variables with groups using different variables in a systematic manner. Judy Carmick, MA, PT Private Practitioner, 3060 Miranda Ave, Alamo, California

REFERENCES 1. Chiu H-I, Ada L. Effect of functional electrical stimulation on activity in children with cerebral palsy: a systematic review Phys Ther. 2014;26:283-288. 2. Carmick J. Clinical use of neuromuscular electrical stimulation for children with cerebral palsy, part 1: lower extremity. Phys Ther. 1993;73:505-513. 3. Comeaux P, Patterson N, Rubin M, Meiner R. Effect of neuromuscular electrical stimulation during gait in children with cerebral palsy. Pediatr Phys Ther. 1997;9:103-109. 4. van der Linden ML, Hazlewood ME, Aitchison AM, Hillman SJ, Robb JE. Electrical stimulation of gluteus maximus in children with cerebral palsy: effects on gait characteristics and muscle strength. Dev Med Child Neurol. 2003;45:385-390. 5. Brown JK, Rodda J, Walsh EG, Wright GW. Neurophysiology of lower-limb function in hemiplegic children. Med Child Neurol. 1991;33:1037-1047. 6. Ross SA, Engsberg JF. Relation between spasticity and strength in individuals with spastic diplegic cerebral palsy. Dev Med Child Neurol. 2002;44:148-157. 7. Cauraugh JH, Naik SK, Hsu WH, Coombes SA, Holt KG. Children with cerebral palsy: a systematic review and meta-analysis on gait and electrical stimulation. Clin Rehabil. 2010;24:963-978. 8. Carmick J. Clinical use of neuromuscular electrical stimulation for children with cerebral palsy, part 2: upper extremity. Phys Ther. 1993;73:514-527. 9. Hazlewood ME, Brown JK, Rowe PJ, Salter PM. The use of therapeutic electrical stimulation in the treatment of hemiplegic cerebral palsy. Dev Med Child Neurol. 1994;36:661-673. 10. Kawashima N, Popovic MR, Zivanovic V. Effect of intensive functional electrical stimulation therapy on upper-limb motor recovery after stroke: case study of a patient with chronic stroke. Physiother Can. 2013;65(1):20-28. 11. Churchill AJ, Halligan PW, Wade DT. Relative contribution of footwear to the efficacy of ankle-foot orthosis. Clin Rehabil. 2003;17:553-557. 12. Carmick J. Managing equinus in children with cerebral palsy: merits of hinged ankle-foot orthoses. Dev Med Child Neurol. 1995;37:10061010.

The author declares no conflicts of interest. DOI: 10.1097/PEP.0000000000000088

To the Editor: I read the newly published article “Adapting to Higher Demands Using Innovative Methods to Treat Infants Presenting With Torticollis and Plagiocephaly.”1 The authors said no reference values for infants’ neck range of motion were available and no standardized way to measure infants’ neck range of motion had been reported. Yet, in our article “Reference Values for Range of Motion and Muscle Function in the Neck—in Infants,”2 we provided reference values, and the infants were measured in a standardized way, a method used in a prior study3 and 3-5 by other authors4-7 as well (see Cheng et al ). Pediatric Physical Therapy

Copyright © 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins and the Section on Pediatrics of the American Physical Therapy Association. Unauthorized reproduction of this article is prohibited.

¨ Anna Ohman, PT, PhD The Queen Silvia Children’s Hospital, Sahlgrenska University Hospital Goteborg, Sweden ¨ REFERENCES 1. Suprenant D, Milne S, Moreau K, Robert N. Adapting to higher demands using innovative methods to treat infants presenting with torticollis and plagiocephaly. Pediatr Phys Ther. 2014;25:339-345. ¨ 2. Ohman A, Beckung E. Reference values for range of motion and muscle function in the neck—in infants. Pediatr Phys Ther. 2008;20:53-58. ¨ 3. Ohman AM, Perbeck Klackenberg EB, Beckung ERE, Haglund˚ Akerlind Y. Functional and cosmetic status after surgery in congenital muscular torticollis. Adv Physiother. 2006;8(4):182-187.

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4. Cheng JCY, Tang SP, Chen TMK, Wong MWN, Wong EMC. The clinical presentation and outcome of treatment of congenital muscular torticollis in infants—a study of 1086 cases. J Pediatr Surg. 2000;35(7):1091-1099. 5. Cheng JC-Y, Tang SP, Chen TMK. Sternocleidomastoid pseudotumor and congenital muscular torticollis in infants: a prospective study of 510 cases. Pediatrics. 1999;134(6):712-716. 6. Cheng J, Metrewell C, Chen T, Tang SP. Correlation of ultrasonographic imaging of congenital muscular torticollis with clinical assessment in infants. Ultasound Med Biol. 2000;26(8):1237-1241. 7. Perbeck Klackenberg E, Elfving B, Haglund Y, Brogren Carlberg E. Intra-rater reliability in measuring range of motion in infants with congenital muscular torticollis. Adv Physiother. 2005;7(2):84-91.

The author declares no conflicts of interest. DOI: 10.1097/PEP.0000000000000093

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