The effect of chiropractic spinal manipulation on the H-reflex and muscle strength in children with cerebral palsy: A feasibility study

2.1 Study design and recruitment

This study was conducted as a feasibility study utilizing a single-blinded, parallel group, randomized, controlled design. Participants were recruited through the New Zealand Cerebral Palsy Registry (NZCPR). Participants were identified in the NZCPR database that consented to being contacted for research studies. Those identified were further assessed for eligibility for this study. Potential participants were then posted a letter of invitation to participate and a flyer with information about the study. Parents were asked to contact the lead researcher with any questions and/or if they wished to participate in the study. Prior to participation in the study, written informed consent was obtained from the parents of the participants and the participants provided written informed assent. Consent was not obtained from the participants themselves as they were under the age of 16 years, which is the legal age of consent in New Zealand. Written informed assent was obtained from participants instead, as required by the Health and Disability Ethics Committee in New Zealand.

The chiropractor, who was not involved in data collection or analysis, randomized the participants into one of two groups, SM intervention or passive movement control intervention, through a coin toss in a separate room. A more rigorous randomization procedure, such as computer-generated randomization, was not used because of the small sample size, but would be used in a larger scale study to reduce group differences and potential bias.

Following pre-intervention recordings, the chiropractor then took the participant and caregiver to a separate room to perform the spinal examination and provide the SM or control intervention. Participants or caregivers were not informed of the group they were in. Following the intervention, the chiropractor brought the participant and caregiver back to the data collection room for post recordings and then left. Documentation regarding the intervention was maintained by the chiropractor until the data analysis was complete. At no time before this, the researchers involved in data collection and analysis were made aware of the group allocation.

2.2 Participants

Inclusion criteria for this study were children diagnosed with spastic diplegic CP, aged 8-13 years and classified as Level I-II on the Gross Motor Function Classification System (GMFCS). Participants were required to be proficient in English and have been able and willing to sign written informed assent. Exclusion criteria were any known contraindications to chiropractic SM (previous reaction to spinal manipulation, fracture, cancer, recent trauma, ligamentous instability, and known inflammatory or infectious arthritis). Participants who had undergone surgery, inhibiting casts, or botulinum toxin treatment in the last 6 months were also excluded from this study.

2.3 Intervention and control

After the pre-recording session was completed, participants and caregivers were collected by the chiropractor and placed in a separate room. If allocated to the intervention group, participants received chiropractic SM by a registered chiropractor. A full spine check was conducted, and SM was performed on specific segments exhibiting evidence of joint dysfunction, such as restricted intersegmental range of motion, tenderness on palpation, and intervertebral muscle tension. These are all indicators commonly used in chiropractic practice and have been shown to be reliable indicators of spinal dysfunction.^35–38 Chiropractors have specific training in pediatric care, and participants were thoroughly assessed and technique adapted to lower force applications when necessary. All SM’s performed, and on which vertebral segments, were recorded by the chiropractor.

If allocated to the control group, the participants received a control intervention that involved non-specific movements of their head, spine, and body, but did not include the thrust that was given with SM. This was done to control for proprioceptive input that could have neurological consequences that occur during the procedure of checking for spinal dysfunction and placing a person into positions for SM. Following the intervention, the participants were returned to the data collection room, and post-recordings were conducted in the same manner as the pre-recordings.

2.3 Procedure

Participants and their caregivers attended one data collection session at the Health and Rehabilitation Research Institute of the Auckland University of Technology (AUT). Prior to the recording of outcome measures, the primary researcher discussed the procedures for the study, answered any questions, and obtained informed consent from the participant and caregiver. Following this, a structured interview was conducted to gather information on patients’ age, sex, ethnicity, and health history. Muscle strength, H-reflex, and V-wave recordings were conducted by the primary researcher and a biomedical engineer. To assess compliance and tolerance to the data collection protocol, notes were taken on any observations or comments the participant made about tolerance of the procedures, such as discomfort, boredom, and wanting to stop. At the end of the data collection session, the participants and their families were also asked if they were okay and how they felt about it.

The muscle strength was recorded by measuring the isometric force of the plantar flexors using a custom-made force transducer. The foot of the affected leg was placed in the force transducer and strapped using Velcro fasteners. The distal thigh was also fixed in place using Velcro fasteners to reduce leg movements during plantar flexion. Once the leg was fixed, the knee angle was measured again post intervention/control to maintain the same conditions. The participant was instructed to push down with their foot as hard as possible for 5 s, which was repeated a total of three times. The participants were verbally encouraged during each MVC to aid in the highest possible contraction. The force was recorded with a CED Power 1401 MK 2 Data Acquisition Board at a sample rate of 1 kHz and an isometric strain gauge (Model MLP100 transducer Techniques Tennecula, California, USA). The corresponding computation was performed using Spike software (https://ced.co.uk/products/spkovin). The strongest MVC of the three measurements was used to compute the 10% amount required as a background plantar flexion contraction during the H- and V-wave recordings.

Surface electromyography (sEMG) measures the electrical activity of a muscle by placing electrodes on the skin over the belly of the muscle.³⁹ The sEMG was used to record the motor response of the soleus muscle for the H, M, and V wave recordings during this experiment. The soleus muscle was identified by asking the patient to stand on the tip of their toes to produce plantar flexion and then palpate the location just lateral to the gastrocnemius muscle. To produce a clear signal and reduce skin impedance, the skin was first prepared by shaving the area, gently abrading the skin with sandpaper, wiping the skin with Nuprep gel, and cleaning the area with alcohol wipes. Subsequently, two bipolar surface electrodes were placed two cm apart along the belly of the soleus muscle, perpendicular to the muscle fibers, to record the innervation zone.⁴⁰ A ground electrode was placed on the bony prominence of the medial malleolus. The electrodes were then connected via cables to a custom-built amplifier with a built-in stimulus artifact suppressor and a high-pass filter (20 Hz), and the signals were recorded using the SIGNAL software (https://ced.co.uk/products/sigovin).

The H reflex and Mmax and V waves of the soleus muscle were elicited via electrical stimulation of the tibial nerve. After explaining the procedure to the participant and caregiver, a stimulating electrode (cathode) was placed in the popliteal fossa and the anode electrode was placed just proximal to the patella. This positioning ensures that the H-reflex can be elicited at the lowest possible threshold as the current passes transversely through the tibial nerve. The knee was then bandaged to apply pressure on the cathode for ease of stimulation. Electrical stimulation was delivered by using a Digitimer-isolated stimulator (Digitimer DS7AH, Digitimer Ltd, Hertfordshire, UK). The position of the electrodes was altered accordingly to provide the lowest stimulation intensity while ensuring the activation of the entire soleus muscle.

2.4 Data recording

The M wave recording was elicited by electrical stimulation of the tibial nerve starting at 5mA and was progressively increased in 5mA increments until the M wave appeared in the sEMG. M-max, which represents the recruitment of all motor axons, is reached when the motor response does not increase with further increases in electrical stimulation, and the H reflex response has disappeared. This value was then recorded as M-max, 10% of which was calculated and used in the H-reflex recording.

For the H-reflex recording, the participant was asked to push down their foot gently to maintain a contraction at 10% of M-max (as determined above in section 3.2.4.1). This was displayed on a computer screen directly in front of the patient, as a line for visual feedback. The purpose of this low-level constant contraction is to allow for some stable background electrical activity throughout the stimulation protocol so that any changes in the H-reflex can be determined to be due to other test conditions.⁴⁰ The H-reflex is then elicited via electrical stimulation of the tibial nerve. The participants received 48 stimulations at different intensities, and each stimulation was given at 0.5 ms intervals. Equally dividing the M-max into 16 determined the intensity levels, and then three stimulations per level were applied. The levels were randomly stimulated to reduce the predictability of the participants’ responses.

The V-wave was then recorded using sEMG and force measurements. Participants were asked to perform three separate MVC’s by pushing down their feet as hard as possible while being verbally encouraged by the researcher. During each of these MVC’s they were given three electrical stimulations at a supra-maximal intensity (110%) of M-max.

2.5 Data processing

Variations can be seen in the H reflex due to changes in subject position during recording, alterations in electrode positioning or contact, and/or alterations in the muscle itself, which can affect study results if adequate H-reflex curve analysis is not performed.^40,41 Furthermore, thresholds to elicit the H reflex and M wave can differ not only between subjects but also within subjects, even if tested on the same day.⁴¹ In order to account for these changes, to obtain results that reflect genuine H reflex changes from the intervention and to determine the H reflex and V wave at different intensities along the recruitment curve, it is necessary to perform curve fitting and normalization on the raw H reflex data.⁴¹ This was performed using the procedure described by Brinkworth⁴¹ and used in previous H-reflex studies with chiropractic SM as the intervention.^22,28

First, the peak-to-peak amplitudes of the H, M, and V waves were obtained from the EMG signals. Normalization was then performed to compare the results between subjects, with M-Max recorded in the pre-assessment used as a normalization factor in that particular session. For each participant in both the pre- and post-sessions, M-max was used for the corresponding H-reflex, M-wave, and V-waves to provide H/Mmax and V/Mmax ratios for each participant. Having this normalized to the specific H-reflex or V-wave stimuli, for each subject and each session allows for a more accurate assessment of the changes in the H-reflex and V-wave represent.^22,41 Once normalization was performed, these values were modeled for curve fit analysis with a hyperbolic function for the M wave and a Gaussian equation for the H and V waves.⁴¹

After curve fitting and normalization were performed, the H-reflex was analyzed for threshold levels by identifying the intensity when the H-reflex curve started to rise. MATLAB code was used as an automatized procedure; however, the time windows for each data set were also manually inspected to ensure the accuracy of this level. The results of each session were then superimposed and post intervention/control results were compared with the intervention/control results. Parameters extracted from the curve-fitted H reflex data were the H reflex threshold, s50, and slope.

After curve fitting and normalization, the V wave was analyzed using peak-to-peak amplitudes, which were then superimposed and averaged to produce a mean value difference between the pre- and post sessions.

To determine the difference in force measurements of maximum voluntary contractions, the EMG signal was manually inspected and analyzed using peak-to-peak amplitude calculations. This was done by placing one cursor at the baseline immediately before the contraction started and placing a second cursor at the end of the contraction immediately before the return to baseline, and then calculating the difference. These values were then compared pre- and post-intervention/control.

3.1 Feasibility

3.1.1 Recruitment

The participants in this study were recruited through NZCPR. At the time of this study, NZCPR was newly established, and this was the first study to use it for recruitment. Consequently, it took considerable time to set up the process to recruit through them, from the first contact in May 2016 until the first flyers were sent out in July 2017. In addition, because they were a new organization, they were still in the process of approving the registrations that they had on their system, which meant that only the approved registrations could be contacted for this study.

In total, 50 families that were registered in the Auckland region with a GMFCS of I-II and aged between 8-13 years old were sent the study information over a six-week recruitment period. From this 50, five parents (10%) made contact via email inquiring about participating in the study. Of these, three met the inclusion criteria and were included in the study. The two participants that were not included were excluded because one had athetoid dyskinetic CP and the other was only going to turn eight years old in December, after the study period had finished. This resulted in a recruitment rate of only 6%.

There was a 100% retention rate for every participant who completed the session. The characteristics of the sample are listed in Table 1. Due to the small and unequal sample sizes, the intervention and control groups were inevitably not equally distributed. Interestingly, although this was not an inclusion criterion, all the participants had previous experience with chiropractic SM.

The recruitment period was set at 6 weeks, both for timely purposes of completing the study and to have a set limit in place in order to assess the recruitment rate. With three people successfully recruited into the study over a 6-week period, this gives an average of one participant every two weeks.

For a large scale RCT, an estimated sample size of 128 participants is predicted based on a calculation with a given effect size (d) of 0.5, type 1 error probability (α) of 0.05 and a power of 0.8 (minimally acceptable). Based on this recruitment strategy and a rate of one participant every two weeks, it would take 256 weeks or almost five years to recruit enough people. With a recruitment rate of 6 %, more than 2000 families/potential participants would need to be contacted.

3.1.2 Data collection procedure

All data collection took place at the Health Research and Rehabilitation Institute of the AUT. This was well received by all participants and had ease of access to disability carparks; families were also familiar with the location due to the gait analysis clinic for children being in the same area. All consent and child assent forms were received and reported to the researcher to be understood by the parent and child. Participants were advised that the sessions would take approximately two hours for the pre- and post-combined. This was fairly accurate for sessions between 90 minutes and two hours.

In general, the data collection procedure was well tolerated. Owing to the nature of the measurement protocol using electrical stimulation, participants were advised at the beginning of the session that if they did not want to continue, they could ask us to stop at any time. One participant reported feeling bored, had difficulty concentrating, and sat in a chair for the required amount of time, and the parent had to give her a smartphone to play a game to distract her. This participant did not want to do the final part of the pre-session recording, which was the V-wave recording, so this was omitted from the post-session data collection. This was the only indication of poor compliance with the recording protocol. The other two participants had no issues, fully accepted the protocol, and did not complain.

3.1.3 Equipment

There were some issues with the custom-made force transducers. The one that was initially planned to be used was in use in another study at the time of the first data-collection session and could not be moved. Therefore, the older version that used the same measurement was used for the first participant. The participant reported this as being uncomfortable, which was the same participant who had difficulty accepting the full H, M, and V wave protocols, and it is possible that this was partly due to the discomfort from the force transducer. The second and third participants used the new version, originally planned for use in this study. There have been no reports of discomfort or problems associated with this condition.

All other equipment worked well and had no issues.

3.1.4 Intervention

The chiropractic SM and passive control interventions were well tolerated by all participants. No issues were reported by the chiropractor or participants, and all movements were well tolerated. No serious or minor adverse events were reported due to intervention or passive control. All participants had previously received chiropractic care more than one year prior to this study, which may have alleviated any potential concerns.

3.2 H-reflex, V wave and force

Due to the small sample size of the three participants and group variation, statistical analysis was not performed on the data obtained for the H reflex, V wave, and force. Therefore, no conclusions will be drawn regarding the efficacy of the intervention versus passive control. The following section will present the results and trends identified, with the aim of determining whether changes can be detected using this protocol and intervention in children with CP in future research studies.

3.2.1 H-reflex

Results from the H-reflex recording showed that both participants in the intervention group had a shift in the H-reflex threshold towards the left, or a lowered threshold, post intervention. This contrasts with the control participant, which had a shift in the H-reflex threshold towards the right, or a higher threshold, post-passive control intervention. Results of the s50 parameter showed that participants in the intervention group both had an increase in s50, suggesting a trend towards a greater number of motor neurons being recruited after chiropractic SM intervention at 50% stimulus compared to pre-intervention. Control participants showed a decrease in s50. Changes in slope showed similar trends with a slope gradient increase after chiropractic SM intervention, suggesting the ability to recruit motor neurons faster. This is in contrast to the passive control intervention, which resulted in a decreased slope gradient. The numerical data for these results are listed in Table 1.

3.2.2 V wave

As mentioned above, the first participant did not wish to continue with the protocol at that time; therefore, the V wave was only recorded in two participants, one control, and one intervention. The participant who received the passive control intervention showed a mean reduction in the V-wave amplitude post intervention of 0.39%, so there was no real change. The participants who received chiropractic SM intervention showed a mean reduction in V-wave amplitude post intervention of 62.6%. The results are presented in Table 2.

3.2.3 Force

Changes in MVC force were variable between participants.

The passive control participants had a 19.5% reduction in MVC force post intervention. In the chiropractic SM intervention group, one participant had a 14.3% increase in MVC force, and the other participant had a 48.9% decrease in MVC force. The results are presented in Table 3.

Limitations

This study was designed to answer specific feasibility questions, which it has done so adequately. The small sample size (n=3), change in equipment between participants, sampling bias, and uneven sample characteristics are factors that limit any further interpretation of results, efficacy of intervention, and generalizability.

There was also no formal assessment of tolerance of the data collection protocol or intervention, such as a post-study questionnaire assessing acceptability. This is a limitation of this feasibility study as it introduces bias from the researchers in their observations and questioning of the participants and from the chiropractor in assessing the tolerance of the intervention. The researcher also provided consent and asked if the participant and caregiver understood the consent and assent forms. This could have influenced the responses and introduced bias.

Another limitation of this study is that all participants had received chiropractic SM before, which means that there is a chance that they were able to guess which intervention they received, and conclusions cannot be made about the tolerance of chiropractic SM intervention in those who had not had SM before.