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RESEARCH ARTICLE Psychophysiological responses to a multimodal physiotherapy program in fighter pilots with flight-related neck pain: A pilot trial Carlos Ferna ´ndez-MoralesID 1 , Luis Espejo-Antu ´nezID 1 , Marı ´a de los A ´ngeles Cardero- Dura ´nID 1 *, Deborah FallaID 2 , Juan Manuel Moreno-Va ´zquez 3 , Manuel Albornoz-CabelloID 4 1Department of Medical-Surgical Therapy, Faculty of Medicine and Health Sciences, University of Extremadura, Badajoz, Spain, 2Centre of Precision Rehabilitation for Spinal Pain (CPR Spine), College of Life and Environmental Sciences, School of Sport, Exercise and Rehabilitation Sciences, University of Birmingham, Birmingham, United Kingdom, 3Department of Physiotherapy, University of Seville, Seville, Spain, 4Department of Physiology, Faculty of Medicine and Health Sciences, University of Extremadura, Badajoz, Spain *[email protected] Abstract Background The physical and cognitive demands of combat flying may influence the development and persistence of flight-related neck pain (FRNP). The aim of this pilot study was to analyse the effect of a multimodal physiotherapy program which combined supervised exercise with laser-guided feedback and interferential current therapy on psychophysiological variables in fighter pilots with FRNP. Methods Thirty-one fighter pilots were randomly assigned to two groups (Intervention Group: n = 14; Control Group: n = 17). The intervention consisted of 8 treatment sessions (twice per week) delivered over 4 weeks. The following primary outcomes were assessed: perceived pain intensity (Numeric Pain Rating Scale–NPRS) and Heart Rate Variability (HRV; time-domain, frequency-domain and non-linear variables). A number of secondary outcomes were also assessed: myoelectric activity of the upper trapezius and sternocleidomastoid, pain catastrophizing (Pain Catastrophizing Scale–PCS) and kinesiophobia (TSK-11). Results Statistically significant differences (p�0.05) within and between groups were observed for all outcomes except for frequency domain and non-linear HRV variables. A significant time*group effect (one-way ANOVA) in favour of the intervention group was found for all variables (p<0.001). Effect sizes were large (d�0.6). PLOS ONE PLOS ONE | https://doi.org/10.1371/journal.pone.0306708 July 5, 2024 1 / 17 a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Ferna ´ndez-Morales C, Espejo-Antu ´nez L, Cardero-Dura ´n MdlA ´, Falla D, Moreno-Va ´zquez JM, Albornoz-Cabello M (2024) Psychophysiological responses to a multimodal physiotherapy program in fighter pilots with flight-related neck pain: A pilot trial. PLoS ONE 19(7): e0306708. https://doi.org/ 10.1371/journal.pone.0306708 Editor: Andre ´Pontes-Silva, UFSCar: Universidade Federal de Sao Carlos, BRAZIL Received: March 1, 2024 Accepted: June 20, 2024 Published: July 5, 2024 Copyright: ©2024 Ferna ´ndez-Morales et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the manuscript and its Supporting Information files. Powered by. Funding: The author(s) received no specific funding for this work. Competing interests: The authors have declared that no competing interests exist.
Conclusions The use of a multimodal physiotherapy program consisting of supervised exercise with laser-guided feedback and interferential current appears to show clinical benefit in fighter pilots with FRNP. Trial registration ClinicalTrials.gov: NCT05541848. Introduction Combat flying exposes fighter pilots to highly stressful situations, which can affect their physical and cognitive performance [1,2]. Exposure to high gravitational accelerations (G-forces) and the operation of heavy technological equipment may influence the development of flightrelated neck pain (FRNP) [3,4]. FRNP impacts a pilot’s ability to perform critical tasks and is associated with a physiological stress response [4–7]. As a result, NATO recommends monitoring physiological parameters such as Heart Rate Variability (HRV) to assess symptoms and clinical signs in fighter pilots with FRNP [4]. Nevertheless, to date, these measures have only been used to assess flight performance [1,2]. In the workplace, it has been observed that workers with musculoskeletal pain may show a decrease in HRV [8], with a marked reduction in parasympathetic activity [9]. An autonomic dysregulation has also been related to alterations in the electrical activity of muscles [10]. The role of psychological responses as modulators of the autonomic nervous system of people with chronic neck pain has also been investigated [11]. Parr et al. [12] indicated that pain catastrophism and fear of movement (i.e., kinesiophobia) influence the persistence of pain in this population, with HRV being an indicator that relates to certain psychological phenomena associated with the experience of pain [8]. Combined therapeutic interventions such as exercise [6], manual therapy [13] or interferential current therapy (ICT) [14–16] have been shown to be most effective in musculoskeletal back disorders [17]. A novel procedure within this approach is electrostimulation therapy known as electromassage, which applies ICT together with manual therapy simultaneously [18]. This modality has shown clinical benefits due to its ability to penetrate deeper into tissues and its greater tolerance to low-frequency currents [17]. In addition, ICT has been shown to induce psychophysiological effects such as changes in HRV when these techniques are combined within a multimodal physiotherapy program [14]. With respect to exercise, a recent systematic review found that cervical motor control exercises are more effective in reducing pain in fighter pilots with FRNP than exercise protocols which only involve strength or endurance [19]. Moreover, the combination of these exercises guided with an external locus (e.g., a laser pointer) further improves the outcome [20,21]. Recent studies analyzing work-related musculoskeletal disorders have stated that the lack of studies in this context is due to the difficulty in accessing the population, which makes sampling difficult [22]. Despite this, and to the best of the authors’ knowledge, there are no studies analysing the psychophysiological responses derived from a multimodal physiotherapy in fighter pilots with FRNP. The hypothesis is that a multimodal physical therapy program will produce significant improvements in psychophysiological parameters compared to a control PLOS ONE Psychophysiological responses to a multimodal physiotherapy in fighter pilots with flight-related neck pain PLOS ONE | https://doi.org/10.1371/journal.pone.0306708 July 5, 2024 2 / 17
group receiving no intervention. Therefore, the aim of this pilot study was to investigate the effects of a multimodal physiotherapy intervention on psychophysiological parameters in fighter pilots with FRNP. Materials and methods Study design A randomized controlled single-blind pilot trial was conducted with concealed allocation, intention-to-treat analysis and with a blinded assessor and statistician. The study was carried out in compliance with recommendations of CONSORT [23]. The present study was conducted following the Declaration of Helsinki and was approved by the Ethical Research Committee of the University of Extremadura (approval number 54/2020). It was also registered prospectively at ClinicalTrials.gov (NCT05541848). All participants provided written informed consent. Participants Via convenience sampling, recruitment took place from September 2022 to December 2022 at Talavera´s Air Base in Southern Spain. An initial, potentially eligible sample of 37 F-5 fighter pilots were recruited. The inclusion criteria were: (i) fighter pilots (male and female) who, at the time of the assessment, were an instructor or student attached to the 23th Wing of Talavera Air Base, Spanish Air Force (SAF), Badajoz; (ii) fighter pilots diagnosed with FRNP, defined by NATO [4] as significant neck pain that occurs during or within 48 hours after the flight; it does not refer to pain that is attributed to other activities or causes; (iii) a minimum perceived pain of 3/10 on the Numeric Pain Rating Scale (NPRS) in an early-morning assessment within 48 hours of the last flight. The exclusion criteria were: (i) Personal Psychological Apprehension Scale (PPAS) score higher than 37.5 [24]; (ii) any contraindication for electrical stimulation; (iii) having received physiotherapy or any other routine medical care six weeks prior to data collection; (iv) any regular use of drugs within the prior two weeks before participating in this study that affect the autonomic nervous system or pain perception, including opioids, antidepressants, benzodiazepines, anti-inflammatory drugs, and beta-blockers; (v) being involved in ongoing medical–legal conflicts. The total sample consisted of 31 fighter pilots. Fig 1 provides a flow diagram of participant recruitment and flow through the study. Randomization An external website (http://www.randomization.com) (accessed on 27 August 2022) was used to complete the group allocation. Participants were randomly (using block randomization, 1:1) allocated into 1 of the 2 groups: the intervention group (IG) and the control group (CG). The randomization was performed by an external assistant who was not involved in recruitment. Blinding Two researchers carried out the study; a blinded researcher collected the measurements at baseline and immediately after the treatment whereas another researcher carried out the intervention. Both were physiotherapists with more than 15 years of experience. The allocation process was conducted in a protected area to ensure that both the examiner and the intervention provider remained blind. PLOS ONE Psychophysiological responses to a multimodal physiotherapy in fighter pilots with flight-related neck pain PLOS ONE | https://doi.org/10.1371/journal.pone.0306708 July 5, 2024 3 / 17
Intervention The participants in the IG (n = 14) followed a program of supervised neck-specific exercise with laser-guided feedback (ELGF) (S1 Appendix). Afterwards, they received an intervention based on manual therapy combined with current interferential therapy called electro-massage [25] (S2 Appendix). They completed a total of 8 sessions over 4 weeks (twice per week). The multimodal treatment program was carried out within 48 hours after their last flight and was carried out at Talavera´s Air Base (Spain) (Fig 2). The participants of the control group (n = 17) did not receive any intervention and continued with their normal combat and exercise flying activities. They were asked not to take medication or to seek alternative treatments. The interventions were led by 2 physical therapists. An adherence rate to the intervention of 75% (6 sessions) was established as a minimum for participants to be included in the final analysis. Neck-specific supervised exercises with laser-guided feedback (ELGF). ELGF is defined as a type of therapeutic exercise characterised by requiring the individual to pay attention to head/neck movement. This type of exercise (also called internal focus/locus of movement control exercise) play an important role in motor skill learning [20]. This has been attributed a to the facilitation of automatic control and retention of movement patterns in subjects with spinal pain [21,26]. The "Motion Guidance Clinician Kit" (Motion Guidance LLC, Denver, CO, USA.) was used, consisting of a panel and laser guide positioned on the forehead for precise execution of neck movements. The laser was positioned by means of an elastic band at the pilot’s forehead. Fig 1. Flow-chart diagram of the progress of patients through the study phases. https://doi.org/10.1371/journal.pone.0306708.g001 PLOS ONE Psychophysiological responses to a multimodal physiotherapy in fighter pilots with flight-related neck pain PLOS ONE | https://doi.org/10.1371/journal.pone.0306708 July 5, 2024 4 / 17
The panel was placed 1.5 metres away from the wall. The program consisted of 4 exercises, which progressed in difficulty according to the tolerance achieved over the course of the sessions: a) Maintaining the head position (cervical stabilisation); b) Cervical flexion-extension; c) Right-left rotations; d) Right-left lateral-flexions. Each exercise consisted of 4 series of 8 repetitions, except the first one. The head position is maintained by pointing the laser at the centre of the panel for 30 seconds (4 series) (S1 Appendix). Between each series there was 10 seconds of rest. The subjects began seated on a stool and then moved to standing from the 3 rd session onwards. From the 5 th session onwards, the distance between the signals to be reached with the laser was increased, with the aim of increasing the range of cervical movement in the 3 planes of space. The interventions were carried out in compliance with the recommendations of the CERT [27] and TIDieR [28] statements. Interferential current electro-massage. Electro-massage is a novel procedure that simultaneously combines interferential current with manual therapy [25], involving a 15-minute treatment performed in the cervical region. We used a current bipolar mode, using a carrier frequency of 4000 Hz at constant voltage and an amplitude-modulated frequency of 100 Hz (Sonopuls 6921; Enraf-Nonius BV, Rotterdam, The Netherlands). The therapist applies manual soft tissue therapy while administering ICT through moistened sponges, focusing on the neck, shoulder, and scapular regions. The protocol includes various techniques such as superficial strokes, deep sliding movements, kneading of the upper trapezius, and gentle stretching of cervical muscles [25]. During the manual therapy, the sliding of the electrodes was accompanied by the necessary pressure according to each phase of the electro-massage sequence (S2 Appendix). Outcome measures Participants were evaluated in separate rooms within their workplace, with the rooms at the same temperature, in order to maintain the environmental conditions consistent between Fig 2. Illustration of ELGF and ICE interventions. https://doi.org/10.1371/journal.pone.0306708.g002 PLOS ONE Psychophysiological responses to a multimodal physiotherapy in fighter pilots with flight-related neck pain PLOS ONE | https://doi.org/10.1371/journal.pone.0306708 July 5, 2024 5 / 17
participants. All measures were conducted within 48 hours after the flight, in both the baseline and final assessment, in the same order and under the same conditions for all participants. HRV was recorded in both groups with participants in a prone position and this was conducted in the early morning after fasting overnight [29]. The recording was performed weekly: the first day of the intervention week for the IG after the end of the treatment; and the first day of the week for the CG at the same time and in the same position, to serve as a control for this group. Finally, the mean of all measurements taken in both groups was calculated. The rater, who was blinded to group allocation, collected the baseline clinical data. Demographic, anthropometric, and clinical data were collected using a self-assessment questionnaire created for this study. Primary outcomes Neck pain intensity—Numeric Pain Rating Scale. The Numeric Pain Rating Scale (NPRS) is a 11-point numeric rating scale, where 0 denotes “no pain” and 10 denotes “the maximum pain imaginable”. The minimum clinically important difference (MCID) for this tool has been established at 1.5 points and the minimum detectable change (MDC) at 2.6 points, in individuals with neck pain. The NPRS is a valid scale with moderate test-retest reliability in this population (Intraclass Coefficient Correlation (ICC): 0.76, 95% CI 0.58 to 0.93) [30,31]. Heart rate variability. HRV is a non-invasive marker which reflects changes in the autonomic response associated with stress [15]. Interbeat time interval (R-R) variation was used to determine the autonomic modulation using Firstbeat Bodyguard equipment (Firstbeat Technologies, Jyva¨skyla¨, Finland). This device was used to record HRV data for 15 min (at rest and after the intervention). Recordings were exported from the devices to the computer via Firstbeat Uploader Software (Firstbeat Technologies) and analysed using Kubios Software (University of Eastern Finland, Kuopio, Finland). To calculate the autonomous balance, the HRV method based on the Poincare ´plot was used [29,32]. This software has proven to be valid and capable of recording non-linear trends that are frequently present on R-R intervals of record [15]. Recommendations of the Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology [33], as well as instructions derived from previous studies that used the heart rate monitor Firstbeat Bodyguard1, were followed [29]. Mean heart rate and time domain parameters were measured: percentage of consecutive RR intervals that differ by more than 50 ms from each other (pNN50) and root mean square of successive differences (rMSSD); frequency-domain parameters: low-frequency power (LF), hight-frequency power (HF) and low/high-frequency ratio (LF/HF); diameters of Poincare ´ plot, the short-term variability’s sensitivity of HRV non-linear specter (SD1); and the longterm variability of HRV non-linear specter (SD2). rMSSD and SD1 are considered indicators of parasympathetic activity [14,15]. The physiological meaning of SD2 is not entirely clear, but it is thought to reflect the long-term changes in RRIs, and it is considered an inverse indicator of sympathetic activity [14,15]. Naranjo-Orellana et al. [32] described two new indexes to simplify the physiological interpretation of Poincare ´plot: the stress score (SS) and sympathetic-parasympathetic ratio (S/PS). The SS is expressed as the inverse of SD2 diameter multiplied by 1000, and it is directly proportional to sympathetic activity at the sinus node. The S/ PS ratio is expressed as the quotient of SS and SD1, and it is considered to reflect autonomic balance, that is, the relationship between sympathetic and parasympathetic activity. Secondary outcomes Myoelectric activity. Myoelectric activity was measured using surface electromyography (sEMG) following NATO expert panel recommendations [4]. The sEMG recordings were PLOS ONE Psychophysiological responses to a multimodal physiotherapy in fighter pilots with flight-related neck pain PLOS ONE | https://doi.org/10.1371/journal.pone.0306708 July 5, 2024 6 / 17
acquired using a portable EMG system (mDurance1system, mDurance Solutions SL, Granada, Spain), which has been validated for measuring muscle activity during dynamic contractions [34]. Disposable electrodes (35x42 mm, Ag/AgCl, Blue Sensor N-00-S, Medicotest A/S, Olstykke, Denmark) were placed pairwise on the upper trapezius and sternocleidomastoid muscles according to established guidelines [35,36] following skin preparation. A reference electrode was placed over the acromion (Fig 3). The raw data were processed and filtered using a fourth-order Butterworth bandpass filter with a 20–450 Hz cut-off frequency. The maximum voluntary contraction (MVC) value was calculated using the average of the three maximum peaks of the root mean square (RMS) during MVC contractions [34]. The pilots sat in the cockpit of the flight simulator, reproducing the position and motion during combat flight. Familiarization tests consisted of the participant performing shoulder elevation and cervical retraction, pushing against the resistance offered by the seat. Participants were then placed in a neutral cranio-cervical position, and were instructed to perform the same contractions and push with increasing force up to a MVC force and hold for this 5 s. Three trials were done with 1 min rest in between each repetition [37]. The variable recorded for muscle activity was the mean RMS measured during MVC (μV). Catastrophizing. The Spanish version of the Pain Catastrophizing Scale (PCS) is a selfadministered scale (Likert scale) of 13 items and one of the most used and reliable to assess pain catastrophizing in military personnel [38]. Participants were asked to refer to their past painful experiences and indicate the degree to which they experienced each of the 13 thoughts or feelings; the score ranges from 0 (never) to 4 (always). Kinesiophobia. The Spanish version of the Tampa Kinesiophobia Scale (TSK-11) was used [39]. This questionnaire contains 11 items to assess the patient’s fear of moving and reinjury. Each item is associated with a 4-point Likert scale (1 = “strongly disagree”, 4 = “strongly agree”). Scores range from 11 to 44 points; higher scores correspond with a greater fear of pain, movement and injury. The Spanish version of the TSK-11 has shown good reliability and validity (Cronbach alpha: 0.79) [39]. Sample size Sample size calculation for detecting changes in the primary outcome (NPRS scale) was performed using G*power 3.1 software. The calculations were based on the minimal clinically important difference (MCID) of 2.5 points in the NPRS scale (estimated for a variance of 10 points in patients with neck pain) [31], assuming a standard deviation (SD) of 2.5 points. Considering an effect size (F-test) of 0.27 for ANOVA: repeated measures, within-between interaction groups differences, an alpha level of .05, and a power of 80%, a total sample size of 30 participants was estimated. To account for potential dropouts, the sample was inflated by 10%, resulting in a final target sample size of 34. This calculation indicated that a sample size of 17 participants per group was required to achieve a 95% confidence interval with 80% power. Statistical analysis An intention-to-treat analysis was conducted. Descriptive analysis was conducted for each variable. Normality of the variables was assessed using the Shapiro-Wilk test, which indicated a normal distribution for all variables, allowing for the use of parametric tests. Mean ±SD was used to report the data. To compare the demographic and clinical variables between groups at baseline, the chi-square test was employed for categorical data, while the independent-samples t-test was used for quantitative data. Differences in measurements were detected by analysis of variance of repeated measures (ANOVA) 2x2, mixed analysis of variance (ANOVA) to PLOS ONE Psychophysiological responses to a multimodal physiotherapy in fighter pilots with flight-related neck pain PLOS ONE | https://doi.org/10.1371/journal.pone.0306708 July 5, 2024 7 / 17
Fig 3. Detail of the placement of the EMG electrodes. https://doi.org/10.1371/journal.pone.0306708.g003 PLOS ONE Psychophysiological responses to a multimodal physiotherapy in fighter pilots with flight-related neck pain PLOS ONE | https://doi.org/10.1371/journal.pone.0306708 July 5, 2024 8 / 17
evaluate group x time interactions*, including the effect of time (baseline, four weeks after treatment) as intra-subjects’ factor and group effects (Intervention Group vs Control Group) as inter-subjects’ factors. Eta square (η 2 ) was used to calculate the effect size (small when 0.01� η 2 �0.06; medium when 0.06�η 2 >0.14; large when η 2 >0.14). Statistical significance was determined at p<0.05. Additionally, Cohen’s d coefficient was calculated to determine the effect size, with values above 0.8 considered high, 0.5 considered moderate, and less than 0.2 considered low [40]. Statistical significance was set at p <0.05. Data analysis was carried out using SPSS version 26.0 (SPSS Inc., Chicago, IL, USA). Results Table 1 lists the baseline clinical and demographic features of the participants. There were no significant differences between groups at baseline for any of the variables (all, p >0.05). Three participants dropped out of the IG due to work-related demands. No adverse events were recorded. Table 2 shows the baseline and post-intervention scores and the mean differences between and within groups for all the variables. Compared to baseline values, the IG showed significant changes (p<0.001) and moderate effect sizes (d�0.6) for PCS, RMS, pNN50 and rMSSD, and large effect sizes (d�0.8) for NPRS, TSK-11, RMS measured during MVC and SD1. Table 1. Baseline characteristics of participants (mean ±standard deviation). Total sample (n = 31) Intervention Group (n = 14) Control Group (n = 17) Age (years) 25 ±6.4 24 ±5.5 26 ±7.1 Height (cm) 178 ±6.5 179 ±5.8 178 ±7.1 Weight (kg) 76.2 ±8.4 77.7 ±6.8 75.0 ±9.6 BMI (kg/m 2 )23.8 ±1.9 24.0 ±1.4 23.6 ±2.2 Number of flight hours / week 4.4 ±1.5 3.8 ±1.2 4.8 ±1.6 Number of hours of physical activity / week 3.6 ±1.7 3.9 ±1.4 3.3 ±1.9 NPRS (0–10) 5.5 ±1.7 6.1 ±1.8 5.1 ±1.5 PCS (0–62) 17 ±6.1 18 ±6.5 17 ±6.0 TSK-11 (1–68) 36 ±2.6 36 ±2.8 35 ±2.5 RMS UT Right (μV) 152.1 ±49.5 152.4 ±21.4 146.3 ±29.2 RMS UT Left (μV) 164.9 ±48.1 160.9 ±56.2 168.2 ±41.9 RMS SCM Right (μV) 19.5 ±11.6 18.6 ±8.7 20.3 ±13.8 RMS SCM Left (μV) 21.3 ±13.4 20.2 ±10.6 22.3 ±15.5 Mean HR (bpm) 74.8 ±13.7 74.3 ±15.3 75.1 ±12.7 pNN50 (%) 13.5 ±16.5 11.8 ±12.4 14.9 ±19.6 rMSSD (ms) 30.1 ±10.6 29.5 ±12.9 30.6 ±8.5 LF (ms 2 )1484.3 ±789.3 1519.4 ±757.7 1455.4 ±836.4 HF (ms 2 )294.1 ±139.2 259.5 ±106.5 322.6 ±158.7 LF/HF ratio 5.4 ±3.1 6.4 ±3.9 4.6 ±1.9 SD1 (ms) 21.4 ±7.1 21.6 ±8.6 21.2 ±5.8 SD2 (ms) 61.9 ±27.9 63.5 ±37.1 60.6 ±18.4 SS (ms) 18.6 ±6.9 19.6 ±9.2 17.7 ±4.6 S/PS ratio 1.1 ±0.8 1.3 ±1.1 0.9 ±0.4 Data are reported as mean ±SD. BMI: Body Mass Index; NPRS: Numeric Pain Rating Scale; PCS: Pain Catastrophizing Scale; TSK-11: Tampa Scale of Kinesiophobia; RMS: Root mean square; UT: Upper trapezius; Mean HR = Average heart rate, beats per minute (bpm); SCM = Sternocleidomastoid; SD1 = transverse axis of Poincare ´ plot millisecond (ms); SD2 = longitudinal axis of Poincare ´plot, SS = stress score (inverse of diameter SD2 x 1000); S/PS ratio = quotient of SS and SD1; Min HR: Minimum heart rate variability; Max HR: Maximum heart rate variability, beats per minute (bpm). https://doi.org/10.1371/journal.pone.0306708.t001 PLOS ONE Psychophysiological responses to a multimodal physiotherapy in fighter pilots with flight-related neck pain PLOS ONE | https://doi.org/10.1371/journal.pone.0306708 July 5, 2024 9 / 17
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