INTRODUCTION AND PURPOSE
With 15-year survival rates in pediatric oncology reaching 82%,1 the population of pediatric cancer survivors is rising. Accordingly, the recognition of long-term consequences is growing, and prevention, as well as therapy strategies, is becoming increasingly important. In this context, a major concern in pediatric cancer survivors is physical inactivity. Pediatric cancer survivors are often inactive,2 participate less in physical education at school,3 and show impairments in participating in sporting activities.4 This inactive behavior might influence survivors' social reintegration after anticancer therapy, and might impact their quality of life5 and lead to an increased risk for chronic illness.6 In contrast, adequate physical activity (PA) during childhood and adolescence promotes overall healthy development7 and, as PA is an integral part of juvenile life,8 improves children's quality of life.
In the pediatric cancer population, the level of PA can additionally be influenced by functional impairments of the lower limbs, as these impairments interfere with mobility, gait, and consequently PA. Several recent studies supported that impairments of the lower limbs including poor muscle strength,9 impaired joint range of motion (ROM),10 and reduced balance control9 are side effects of a cancer diagnosis, anticancer therapy, and associated immobility. Improving such impairments could sustainably promote an active lifestyle among pediatric cancer survivors. Adequate functional skills are fundamental for successful participation in active leisure time and sports activities. Consequently, focus has been set on the development of supportive care strategies.
A common supportive care strategy in pediatric oncology is exercise programs. The increased implementation of exercise programs is driven by promising results, showing positive effects of exercise on lower limb impairments. Positive effects include improvements in strength,11–15 ankle dorsiflexion ROM,12 , 16 and functional mobility.14 , 15 , 17 However, not all studies confirm these positive results.12 , 18 , 19
Research on specific exercises to counteract functional impairments that interfere with PA is lacking. A potential exercise strategy that might contribute toward filling this gap is whole-body vibration (WBV). WBV training is a novel therapeutic approach that has gained increased use in the rehabilitation of children with disabilities, showing the potential to improve health-related physical fitness including lower limb function.20 Thus, WBV may be a beneficial adjunct to therapeutic exercise programs in pediatric oncology, as has been seen in with adults with cancer.21
There is one intervention study in pediatric cancer survivors assessing the effects of a home-based, low-magnitude, high-frequency stimulation training on bone mineral density.22 There is no research on WBV as an exercise modality to improve functional impairments of the lower limbs. A pilot study in children and adolescents after inpatient anticancer therapy was conducted to provide an initial assessment of WBV in this context, determining feasibility, adherence, program acceptance, and areas of effectiveness.
This pilot study was performed in accordance with the latest Declaration of Helsinki. It was reviewed and approved by the ethics committee of the German Sport University Cologne and registered in the German Clinical Trials Register. This single-group trial was conducted over a 12-week period at a the Children's Hospital Amsterdamer Straße, Cologne.
Participants were eligible if they were between 4 and 20 years of age, had been treated for an oncological disease, had completed inpatient cancer care within the last 5 years, provided written informed consent from the legal guardian as well as a child-specific informed assent from the participant prior to study participation, and received medical clearance of the treating physician prior to study participation. Participants were excluded if they had exclusion criteria according to the suggestions of the device manufacturer, including pregnancy; acute thrombosis; implants in activated regions of the body; acute inflammation of the locomotor system, active arthrosis, or arthropathy; acute tendinopathy in activated regions of the body; acute hernia; acute discopathy; fresh fractures in activated regions of the body; gallstones or stones in the urinary tract collection system; postsurgery wounds and fresh wounds in activated regions of the body or incomplete wound healing; rheumatoid arthritis; and epilepsy. Participants were also excluded if they had specific physiological or psychosocial impairments that would prevent participation in the WBV intervention (in accordance with the physician's advice, including, ie, severe orthopedic disorders and depression). The recruitment was performed by the therapeutic exercise program for childhood cancer outpatients established in the outpatient clinic for pediatric hematology/oncology of the Children's Hospital Amsterdamer Straße, Cologne.
Children participated in the supervised WBV intervention for 12 weeks. All WBV sessions were performed on a side-alternating vibration platform (Galileo, Novotec Medical GmbH, Pforzheim, Germany). Participants stood on the platform or performed dynamic exercises (Supplemental Digital Content 1, available at: http://links.lww.com/PPT/A220) that were supervised by an exercise physiologist to ensure correct performance. Feet were placed at equal distance from the center of the vibration platform (Figure 1). During exercising, participants transferred their weight to the forefoot and stood with knees and hip slightly bent (Figure 1). They wore tight socks (eg, nonslip socks) or gymnastic shoes to avoid skidding and to prevent dampening of vibration stimulus through footgear. For safety reasons, the supervising exercise physiologist could stabilize the participants if needed.
The applied vibration protocol was developed following effective protocols for improving functional impairments and mobility in children with disabilities.23–25 The protocol consisted of one 9- to 13-minute WBV session per week, with 5 to 9 minutes' overall vibration time. Vibration segments of 60 to 120 seconds and 60 seconds' rest were used throughout the intervention period; vibration frequencies ranged from 18 to 27 Hz, with a steady 2-mm peak-to-peak displacement and peak accelerations with a range of 1.3 to 2.9 g26 (Figure 2). To allow for gradual increase of the vibration load, training progression in terms of 1 adjustment of either vibration frequency or segment duration was possible each session using the following protocol: for every frequency (21, 24, and 27 Hz), the duration was increased in 3 stages (60, 90, and 120 seconds). Reaching 120 seconds, frequency was increased and duration was reset to the shortest duration and, subsequently, increased again. Progression was dependent on the child's ability to tolerate the vibration and was controlled by qualified and experienced exercise physiologists.
Feasibility. The program's primary outcome was feasibility, defined as the ability to participate in WBV training without WBV-related adverse events leading to health deterioration (eg, bone fractures, bleeding, and severe pain) and, according to the physician's advice, to training cancelation and study dropout. To ensure proper training, an exercise physiologist supervised each training session recording problems. All exercise physiologists underwent a competency training prior to the study, which was performed by a qualified and experienced “gold standard setter” assuring that training supervision would be provided as standardized as possible. Exercise physiologists were educated about WBV and its potential side effects. They performed training sessions on the vibration platform themselves. They received a single supervised WBV training with an individual to gain practical experience.
WBV-related side effects such as increased muscle weakness or soreness, increased bone soreness, or increased fatigue were recorded. To identify immediate side effects associated with WBV training, participants were questioned after each training session regarding side effects or discomfort. To identify delayed side effects, parents were instructed to provide supervision of their children for 24 hours following WBV and to consult the principal investigator or the treating physician in case of suspected adverse reactions.
To allow for precise analysis of the applied vibration protocol, training progression was recorded. The program's aim was for the children to reach the maximum vibration frequency (27 Hz), as muscle activity during WBV increases with rising frequency.27 All data were documented in a logbook and discussed with the treating physician as required.
To ensure safe WBV, relative contraindications (specific situations in which training was suspended) were established prior to the study. These relative contraindications were defined following published contraindications to exercise in the pediatric cancer population.28 However, adaptions were made in terms of thrombocytes. Since thrombopenia is a frequently reported issue in pediatric oncology29 and experience with, as well as reference values for WBV, is lacking in this population, the platelet count threshold was increased to 30 000/μl after consultation with the treating physician. As such, training was suspended when children were experiencing acute thrombosis, nausea, vomiting, dizziness, fever (<38°C), or severe infections; had muscle/tendon/ligament/bone/joint injuries that would prevent participation temporarily; had thrombocytes less than 30 000/μl; and for up to 7 days after minor and for at least 14 days after major surgical procedures.
Adherence. The number of offered and completed training sessions was documented to assess program adherence. Reasons for nonparticipation were recorded.
Program Acceptance. A self-developed questionnaire was used to determine WBV acceptance. The questionnaire comprised 3 dimensions: personal attitude toward WBV training, perceived physical discomfort through WBV training, and perceived effectiveness through WBV training. Questions were answered through a 5-point Likert scale. Questionnaires were offered to participants after the 12-week intervention. For those younger than 10 years, the questionnaire was completed via interview conducted by the exercise physiologist. In order to gain a better understanding of the perceived effectiveness through WBV training, participants' parents were additionally asked to answer the corresponding dimension.
Potential of WBV on Symptom Reduction. Physical changes during WBV intervention were analyzed through testing before and after the intervention. Selected functional parameters relevant for children with cancer (strength of ankle dorsiflexion and knee extension, ankle dorsiflexion ROM) were investigated. Strength measurements were done using a hand-held dynamometer (CITEC) by applying the break test30 in the positions described by van der Ploeg et al.31 During the break test, the examiner pushes the dynamometer against the participants' limb until the participant's capacity to hold is exceeded and the joint gives away.32 Active and passive ankle ROM were assessed as previously described by Beulertz et al,33 using a goniometer (Lafayette Instrument Company). ROM measurements were conducted with participants sitting with knees extended, and with participants lying in the supine position; their legs adequately padded and flexed. All functional measurements were done bilaterally and mean values of the 2 sides were calculated for analysis.
Walking efficiency and functional mobility were investigated. The time participants needed to walk 10 m at their preferred and maximum walking speed (short walking efficiency), and the longest distance that participants could cover within 2 minutes (long walking efficiency), was measured. These selected timed walking tests (10-m walking test, 2-minute walking test) have been used with children either with cancer or other chronic diseases.34 , 35 The Timed Up and Go Test was done, as previously described by Ness et al.34 Participants were asked to stand up from a chair, walk a distance of 3 m, turn, walk back, and sit down again. Two trials were performed and the fastest was included into the analysis. The participants' overall PA levels before and at the end of the intervention were measured using a visual analog scale (VAS) from “inactive” to “very active.”
A descriptive analysis was used to assess program feasibility and acceptance. WBV-related adverse events and WBV-related side effects were reported. Reasons for nonparticipation and changes of the vibration protocol were described. Adherence was calculated as the percentage of sessions attended, divided by the number of sessions offered. All questionnaires assessing program acceptance were analyzed and frequencies calculated. Participants' overall PA levels were calculated as the percentage of the VAS length up to the participants' mark divided by the total VAS length.
Due to the small sample size, the nonparametric Wilcoxon signed-rank test was applied to analyze physical changes during intervention. The level of significance was set to P < .05. Statistical analyses were performed with IBM SPSS Statistics 24.
Eleven children and adolescents after inpatient anticancer therapy were recruited. The data of 9 children and adolescents were evaluated in the final analysis. Baseline characteristics of the 9 participants are shown in Table 1. Diagnoses and disease treatment programs varied within the study sample; however, all participants received chemotherapeutic treatment during medical care.
Nine of 11 participants completed the 12-week intervention. During intervention, 2 participants withdrew for reasons unrelated to the study. One participant dropped out after 7 weeks due to an injury that occurred in physical education at school, making participation no longer possible. A second participant dropped out after 8 weeks, as he began to take part in a 4-week inpatient rehabilitation program for pediatric cancer participants, preventing further participation due to geographical distance. The remaining 9 participants completed the WBV intervention without WBV-related adverse events leading to health deterioration. Consequently, no WBV-related dropout occurred.
Regarding immediate side effects associated with WBV training, 6 participants (#1, #2, #3, #6, #8, and #9) reported itching and skin redness in feet and calf areas while training on the WBV platform. Three participants did not feel itching (#4, #5, and #7). Because of itching symptoms, segment duration was shortened twice in 1 patient (from 120 to 90 seconds; #2). Four participants informed the exercise physiologist about symptoms of muscle weakness or soreness in the legs especially when doing squats (#1, #2, #4, and #6). Another 2 participants expressed discomfort, one in the forefoot (#8) and the other in the Achilles tendon (#9). Two participants had difficulties keeping the correct body posture required for WBV training (transferring the weight to the forefoot, standing with knees and hip slightly bent) in their first sessions (#6 and #8). These coordination problems occurred as a result of existing functional impairments, including restricted ankle mobility, and required an extension of the familiarization period from 1 to 2 sessions in 1 patient (#8). Regarding delayed side effects, transient muscle weakness or soreness that lasted for 1 or 2 days occurred in 7 participants.
Seven participants were able to reach the highest vibration frequency of 27 Hz, with segment durations of either 120, 90, or 60 seconds. Two participants did not reach the vibration frequency of 27 Hz but progressed to 24 Hz/90 seconds (#8) and 21 Hz/90 seconds (#2), respectively. No training session needed to be canceled due to relative contraindications.
Adherence rates ranged from 73% to 100%, corresponding to an overall adherence of 87.96% (median: 90.91%). Reasons stated for absences from WBV sessions were lack of time due to school/work tasks (4), illness (3), tiredness after a long and intense school trip (1), transportation issues (2), vacation (1), and lack of interest (1).
All 9 participants completed the questionnaire evaluating WBV acceptance. Five parents completed the questionnaire's dimension on perceived effectiveness (Table 2). Based on the participants' subjective reports, they did not generally feel pain during training and only 1 participant reported perceived discomfort (questions #3-5). Children generally liked the vibration stimulus and were not afraid to do something wrong (question #10-11, 13). Children agreed that training was physically demanding (question #12). Most participants and their parents reported subjective improvements in lower extremity functional performance and in mobility (see questions # 6-9 and parents report, respectively). No deterioration was reported.
Potential of WBV on Symptom Reduction
During the course of intervention, significant changes were found in the strength of knee extensors and in the active ankle dorsiflexion ROM measured with straight legs. Data from functional parameters are shown in Table 3. Participants' overall physical levels before and at the end of the intervention are in shown Table 1.
This pilot study demonstrates that WBV is a feasible, safe, and well-received exercise modality for children and adolescents after inpatient anticancer therapy. WBV does not affect participants' health and demonstrates the potential to improve functional impairments of the lower limbs. We did not observe withdrawals or health incidents directly related to WBV.
Some WBV-related side effects were reported, including itching and skin redness in the lower limbs or muscle weakness and soreness. These side effects, however, are well-known reactions to WBV.36 , 37 Younger participants(#2 and #8) or those close to the cessation of inpatient anticancer therapy (#6 and #9) experienced some difficulties including discomfort, coordination problems, or intense itching requiring changes to the load parameters. Younger participants had reduced tolerance to increased vibration load. This resulted in slower adjustments of vibration settings as well as lower maximum vibration frequencies. These instances of side effects might be due to excessive or overly fast increase in vibration load. This emphasizes that WBV training needs to be implemented carefully in 2 risk groups: younger children and those closest to the cessation of inpatient treatment. Exercise physiologists are recommended to start WBV training with low vibration load, which can be slowly increased. Although home-based training is possible,22 supervision is advised in these 2 risk groups to guarantee correct performance and to allow for training progression, feedback, and safety. Supervision should be provided optimally by qualified exercise physiologists. Supervision might also be conducted by other health care providers, if appropriately and sufficiently trained. In order to minimize or to avoid excessive vibration load, overall vibration time might also be divided into shorter vibration segments avoiding muscular fatigue, which is a limiting factor in WBV training.38
WBV intervention had high adherence (mean: 87.96%, range: 73%-100%) and general acceptance. The achieved adherence rates were greater than the 75% threshold set for feasibility in previous exercise intervention studies among childhood cancer survivors.39 The adherence rates were similar to rates reported in previous WBV programs with children with disabilities20 and in traditional exercise programs in pediatric oncology (67%-98%).40 Thus, the applied WBV training is appropriate for participants after inpatient anticancer therapy. The reasons children missed the sessions were unrelated to our program, except for 1 participant who reported motivation problems. Participants were accepting of the WBV training. This might ensure the translation into the nonresearch setting and support the idea of integrating WBV as an adjunctive modality into therapeutic exercise programs in pediatric oncology. Although a high volume of stimulation impulses is elicited during WBV in a short time,37 WBV is largely independent of training motivation, as the impulses are evoked involuntarily by reflexes.38 Moreover, as WBV does not evoke cardiovascular stress,38 , 41 the training stimulus might not be perceived as exhausting, which could facilitate the integration of WBV into therapeutic exercise programs. However, some children reported perceived minor side effects in the questionnaire and participants indicated that they felt slightly uncomfortable while standing on the vibration platform. Exercise physiologists should inform participants about possible symptoms associated with WBV (such as itching and reddening) prior to training to alleviate fears and concerns.
The physical changes noted through functional testing before and after the WBV intervention suggest that WBV has the potential to positively impact functional impairments of the lower limbs, especially strength of knee extensors and active ankle dorsiflexion ROM. Since walking efficiency and functional mobility remained nearly unchanged, results of this pilot study could not indicate that it is possible for participants to automatically convert functional improvements into a more complex movement pattern such as walking. Considering the general increase of PA observed during the 12-week intervention, other activities, which children may have performed in addition to the WBV training, could have influenced the functional improvements. There is also the possibility that WBV may have triggered the observed increase in PA. Future studies should screen for PA when investigating the efficiency of WBV training on functional abilities.
In agreement with previous intervention studies among children with chronic diseases,20 WBV demonstrates potential to improve lower limb function. WBV might be integrated into therapeutic programs as a specific exercise to counteract functional impairments interfering with mobility, gait, and PA. Improving these functional impairments might provide an opportunity to promote an active lifestyle among children with cancer, including participation in active leisure time and sport activities.
The present study has limitations, which include study design, sample group, and WBV intervention. The trial is single-armed without a control group and with only a small number of participants. This design was sufficient to demonstrate feasibility, adherence, and acceptance of WBV aiming to improve functional impairments. The participant characteristics are heterogeneous with a wide range of age, both sexes, and mixed cancer diagnoses. This heterogeneity was desired. It emphasizes that WBV is an appropriate exercise modality for children after anticancer therapy, which can be applied independent of children's age, sex, or cancer diagnosis. In addition, training was only offered once a week and the training session had to be canceled for some participants due to public holidays, meaning that participants had the chance to receive either 11 (n = 7) or 12 (n = 2) WBV sessions. However, this approach guaranteed that all sessions could be supervised by qualified and experienced exercise physiologists. Moreover, no target total amount of vibration time over the 12-week intervention was defined prior to the study. This, however, ensured adequate individualization of training in this novel therapy program. Despite these limitations, our results contribute to a gain in knowledge, as this study provides relevant information about implementing WBV into the pediatric cancer setting. We aim to enhance the recognition of WBV as a potential therapy method in this population and to encourage further intervention studies.
WBV appears to be a feasible, safe, and well-received exercise modality for children and adolescents after inpatient anticancer therapy. Research should focus on confirming our results regarding effectiveness through larger, well-designed randomized controlled trials. Future research should assess feasibility and effectiveness of WBV training in pediatric cancer participants while on treatment. WBV should be considered for inclusion in therapy programs in pediatric oncology.
The authors thank all participants and their families for taking part in this study. A special thank goes to Jonas Boehme, Felicitas Harscheidt, and Nadja Gressler without whose support the project would not have been possible as they supported us in conducting the WBV training. Moreover, the authors would also like to say thank you to Alexander Schenk and Michelle Holthaus for their support during the study period as well as to all physicians and physiotherapists of the Childrens Hospital Amsterdamer Straße for the successful cooperation. Finally, the authors want to acknowledge Meaghan Hagerty and Jan-Philipp Burde for proofreading and editing the manuscript.
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