# Reliability of a novel neck external loading dynamometer

Marc Julia, Loic Damm, Simon Pla, Jean-Paul Micallef, Arnaud Dupeyron, S. Perrey

► To cite this version:

Marc Julia, Loic Damm, Simon Pla, Jean-Paul Micallef, Arnaud Dupeyron, et al.. Reliability of a novel neck external loading dynamometer. Journal of Biomechanics, 2024, 177, pp.112400. 10.1016/j.jbiomech.2024.112400. hal-04795445

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Short communication

# Reliability of a novel neck external loading dynamometer

Marc Julia<sup>a,b,*</sup>, Loic Damm<sup>a</sup>, Simon Pla<sup>a</sup>, Jean-Paul Micallef<sup>a</sup>, Arnaud Dupeyron<sup>a,c,1</sup>,
Stéphane Perrey<sup>a,1</sup>

<figure><img src="image_2.png" /></figure>

ARTICLE INFO

Keywords:

Rugby

Head and neck injury

Muscle

Cervical reflex

Concussion

A B S T R A C T

Cervistab is an electro-pneumatic device that produces flexion push-loading events in an ecological rugby position (i.e. similar to on-pitch position) to assess neck extensors muscle response to a flexion perturbation. This response is important for preventing head/neck injuries in Rugby, however there is a clear lack of validated devices in the literature.

This study tested the reliability of this new device designed to investigate the extensor neck muscle response to flexion head push-loading event. Twelve healthy volunteers were tested with Cervistab in a test/retest protocol. Participants experienced push-loading events with preloading on extensors muscles at 50 % and 20 % of their maximum voluntary isometric extension strength. Muscle mechanical latency, non-reflex and reflex rates of force development were measured twice, 7 days apart. Reliability was assessed by intraclass correlation coefficient (ICC), coefficient of variation (CV), and the Bland and Altman graphical approach.

For both preloading conditions, muscle mechanical latency showed good ICC values from 0.81 to 0.88 and good CV (3.5%). Non-reflex and reflex rates of force development showed good reliability with ICC ranging from 0.78 to 0.89, and moderate CV values ranging from 8.5% to 14.5%, depending on the preloading condition (20% and 50% of maximal isometric extension contraction respectively). Bland and Altman plots showed no significant fixed or proportional bias.

Overall, the reliability of measurements obtained with Cervistab is good. Cervistab can be used in practice to improve our understanding of the neuromechanical factors that influence neck stability, to help prevent head/ neck injuries and to guide the decision to return to play after a head or neck injury.

1. Introduction

Head and neck injuries are a critical issue in many sports where high speed and head contact are frequent (Chan et al., 2016; Van Pelt et al., 2021). To protect against these injuries, the role of the neck muscles has been highlighted as important in clinical studies (Collins et al., 2014; Hrysomallis, 2016), although a recent systematic review by Daly et al. (2021) found a lack of evidence that strengthening the neck reduces the risk of neck/head injuries. For concussion specifically, biomechanical laboratory studies did not really show a positive effect of higher cervical muscle strength to mitigate short term kinematics: Eckersley et al. (2019) found no effect while Mortensen et al. (2020) noted a limited statistically significant effect. However the lack of evaluation of muscle reaction time and time to peak force was cited as a major limitation.

Coupling laboratory and clinical data, Schmidt et al. (2014) found that generation of greater neck stiffness, thanks to cervical muscle activation, could reduce odds of sustaining higher magnitude head impacts after perturbation.

In a recent systematic review of clinical studies, Garrett et al. (2023) found that the association between greater neck strength and risk of sport concussion-related was very small and non-significant. However, they pointed out that analysing the role of muscles using isometric strength is insufficient and that the focus should be on the timing and quality of muscle activation (rate of force development, RFD).

To date, though Le Flao et al. (2018) pointed out the relevance of evaluating muscular response variables such as neck stiffness and muscle onset latency, few studies have explored these issues. Bussey et al. (2023) measured the electromyography (EMG) amplitude response of

<footnote><sup>a</sup> EuroMov Digital Health in Motion, Univ Montpellier, IMT Mines Ales, Montpellier, France</footnote>

<footnote><sup>b</sup> Department of Physical Medicine and Rehabilitation, CHU Montpellier, Univ Montpellier, France</footnote>

<footnote><sup>c</sup> Department of Physical Medicine and Rehabilitation, CHU Nîmes, Univ Montpellier, Nîmes, France</footnote>

<footnote>* Corresponding author at: EuroMov Digital Health in Motion, 700 avenue du Pic Saint Loup, 34090 Montpellier France.
E-mail address: m-julia@chu-montpellier.fr (M. Julia).</footnote>

<footnote n="1">¹ Shared co-last authorship.</footnote>
cervical muscles and head acceleration following a chest impact in up-
right position. They observed an altered motor control strategy (i.e.
delayed anticipatory and compensatory head adjustments) in the con-
cussed group of male rugby players exposed to external predictable and
unpredictable impact perturbations compared to controls.

A good understanding and characterization of cervical muscles
response appear crucial for the prevention of head and neck injuries in
collision sports such as rugby. In response to this gap in the literature, we
have developed a bespoke device, the Cervistab, which allows to study
the dynamic response of the neck extensor muscles (i.e., mechanical
muscle latency (ML) and RFD) under quasi-ecological (i.e. similar to on-
pitch position) conditions for rugby players. The reliability of such a
device is an important step, but is rarely realised in the literature (only
two studies reported in Le Flao et al. (2018)).

The aim of this study was to evaluate the between-session test-retest reliability of a novel neck dynamometer derived measures, such as the ML and RFD, following flexion head push-loading events.

**2. Materials and Methods**

2.1. Participants

As part of a larger clinical trial (NCT03712514), a sample of 12
healthy young male rugby players (mean ± SD, age: 20 ± 3 years, body
mass: 99 ± 17.2 kg, height: 177.5 ± 7.7 cm) volunteered to participate

in this study. They were recruited from the Rugby section of the Mont-
pellier Sports Faculty. All participants provided written informed con-
sent prior to inclusion and data collection. Research ethics approval was
obtained from the CPP Sud Méditerranée III (#20151102). Participants
were not included if they had a medical history of cervical injuries
requiring surgery, active cervical symptomatology, migraine or epi-
lepsy. Each participant was examined by a physician before each test
procedure, to check medical history, pain-free neck mobility and current
symptoms.

2.2. Device

The Cervistab is an innovative rugby scrummaging machine devel-
oped in-house. The aluminium frame of the BabyScrum® manufactured
by ADG company has been used as the base for the Cervistab (Fig. 1).

Both head pads are moved by an electro-pneumatic system to pro-
duce a flexion head push-loading event. Each pad is instrumented with a
load cell (Flintec PB-75 kg for head pads and Flintec PC60-750 KG-C3 for
shoulder pad) and the displacement of head pads is measured by linear
transducers (Gefran PC50). With Cervistab, each cylinder behind each
head pad delivers symmetrical push-loading events while the participant
is asked to counteract this induced hyperflexion movement, mimicking
the conditions encountered in the field. The pressure (P, kPa) within the
pressure vessel is regulated and adjusted in accordance with the surface
area of the ejection cylinder (A, m²) to exert a mechanical force (F, N)

<figure><img src="image_3.png" /><figcaption>**Fig. 1.** Overview of the Cervistab® scrummaging machine: A. Antero-lateral view; B. Postero-lateral view; C. Details of a cylinder and its force-applying pad; D. Picture of one participant in the testing position. Shoulder pad (1). Handgrips (2). Aluminum frame of the BabyScrum® (3). Head pad load cell (4). Shoulder pad load cell (5). Head pad linear transducers (6). Pad is made of polyether (density: 103—135 kg/m³ and compressive Stress/Strain response at 25 %: > 13 kPa).</figcaption></figure>
equivalent to 100 % of the maximal voluntary isometric contraction (MVIC) of the extensors, in accordance with the following equation: P = F/A. Therefore, the axial force applied to the pad in contact with the head is generated by the two ejection cylinders when delivered with pressurized air. The shoulder pad load cell is used to ensure that subject performs a combined movement of pushing forward (minimum of 50 % MVIC on shoulder pads) and pushing upward on the head pad (either 50 % or 20 % of MVIC). There is no movement of the shoulder pads. Time histories of the displacement, velocity, and acceleration of the pistons are presented in Fig. 2.

## 2.3. Procedure and testing protocol

Participants completed a total of two sessions: the initial baseline assessment (V1) and a repeat assessment seven days later (V2). In each session, the neck extensor muscles were warmed up first with active mobilisation of the cervical spine, followed by a warm up in the Cervistab device: first in an isometric mode (10 sets of 3 sec isometric contractions with an increasing intensity), and then with flexion push-loading events of progressively increasing intensity.

The cervical flexion push-loading event was applied simultaneously on two points of participant's skull (on the postero-lateral left and right

<figure><img src="image_4.png" /><figcaption>B Force vs. piston velocity</figcaption></figure>

<figure><img src="image_5.png" /><figcaption>C Force vs. piston acceleration</figcaption></figure>

<figure><img src="image_6.png" /><figcaption>**Fig. 2.** Time histories of the displacement, velocity and acceleration of one piston. The force signal was smoothed using the 'loess' (Locally Estimated Scatterplot Smoothing) method. The maximum displacement possible of each cylinder piston (see Fig. 1) is 50 mm, with the beginning of the displacement occurring at around 10 ms after the onset of the push-loading event on the head. The maximum acceleration value is approximately 1 g.</figcaption></figure>
parts of the occipital bone, Supplementary materials1). The load magnitude was calibrated according to the individual extension MVIC testing completed by each volunteer at the beginning of each tasks block. The impact was manually triggered, once a predefined extension preload (PL) was achieved, as a percentage of the participant's MVIC (50 % or 20 % of MVIC).

The test protocol consisted of 3 blocks of 10 impacts each with 3 min rest breaks in-between. Each block began by a 4-s MVIC in the Cervistab. The first 5 impacts of each block were performed after the subject reached 50 % MVIC PL. The following 5 impacts were performed after a 20 % MVIC PL was reached (Fig. 3A).

## 2.4. Data processing and analysis

All acquisitions were recorded at 1 kHz using the PowerLab 16/30 data acquisition hardware and an octal bio-amplifier ML138 from ADInstruments Europe (Oxford, UK). Raw force data were imported into Matlab and analyzed using custom scripts. Each input produced an unfiltered signal sampled at 1 kHz. The force signal was smoothed using the 'loess' (Locally Estimated Scatterplot Smoothing) method due to its robustness and flexibility in handling non-linear data. LOESS is a non-parametric method that combines multiple regression models in a k-nearest-neighbor-based algorithm. We chose a smoothing factor of 0.05 based on the balance between smoothness and fidelity. This value was determined after careful examination to ensure that the smoothing did not overly distort the underlying signal. Empirical validation was necessary, so we conducted preliminary analyses to determine the optimal smoothing factor. Through these analyses, we observed that a smoothing factor of 0.05 provided the best performance in terms of noise reduction while retaining critical data characteristics. To support our choice, we provide visualizations comparing the original and smoothed data, demonstrating how the smoothing factor of 0.05 effectively reduces noise while preserving the variations of interest in the original

signal.

The onset of the head push-loading event was determined as the point where the first ascending slope of the force curve intersects with the regression line describing the baseline. The resultant vector, calculated from the addition of the left and right force vectors, was used for the calculation of the variables of interest described below for each push-loading. For each participant, values from all trials at 20 % and 50 % PLs were averaged for each preloading condition.

ML (ms), non-reflex and reflex rates of force development (NR-RFD and R-RFD) (kN.s⁻¹) of the neck extensor muscles in response to flexion head push-loading event were measured as described by Ogiso et al. (2002): "an imposed stretch on a muscle evokes an immediate increase in the torque, a transient drop in the torque and a subsequent re-increase in the torque". NR-RFD was defined as the first ascending slope and R-RFD as the second ascending slope on the force/time graph (see Fig. 3C). ML was defined as the delay between the onset of head push-loading event and the onset of the reflex torque (local minimum after the initial peak on the force/time graph). The second slope (R-RFD) was calculated over the interval from 5 to 25 ms after the onset of the reflex torque.

## 2.5. Statistics

The mean values of NR-RFD, R-RFD and ML measures for each condition (50 % and 20 % PLs) and each participant from V1 and V2 were compared. The intraclass correlation coefficient (ICC) for two-way mixed effects, absolute agreement and multiple measurements (ICC 3, k; Shrout and Fleiss, 1979), was used for test-retest assessment. The coefficient of variation (CV) and the graphical approach (bias and 95 % limits of agreement) of Bland and Altman (Berchtold, 2016) were used to examine the agreement between measurements. Based on the 95 % confidence intervals (CI) of the ICC estimate, ICC was considered as excellent over 0.9, good over 0.75, moderate over 0.5 and poor below

<figure><img src="image_7.png" /><figcaption>**Fig. 3.** Push-loading protocol on the Cervistab® computer interface. A. The illustration depicts the relationship between force and time on a single head pad. The initial ascending slope represents the voluntary force generated by the participant (the predefined preload, PL) to reach the designated force target, which is either 20 or 50 % of the maximal voluntary extension isometric contraction (MVIC). Once the target has been reached, the examiner randomly triggers the flexion push-loading event (with a magnitude load of 100 % MVIC) within an interval of 5 s. In this example, five loading events were observed. B. Please note that this is an enlargement focusing on one representative trial of the push-loading event. Note: an artefact occurs at the release of the muscular contraction (Time: 11.67 10⁴ ms). C. NR-RFD is the first ascending slope and R-RFD is the second ascending slope on the force/time graph. ML is the delay between the onset of head push-loading and the onset of the reflex torque (local minimum after the initial peak on the force/time graph).</figcaption></figure>
(Koo and Li, 2016). The CV was calculated as the standard error of measurement (SEM)/grand mean * 100, where the SEM was calculated as (SD Δ/√2)).

Two-way repeated measures ANOVAs were performed to determine the effects of preload (50 % vs. 20 %) and test time (V1 vs. V2) on NR-RFD, R-RFD and ML. Significance was set at *p* < 0.05.

## 3. Results

The twelve subjects completed the two sessions, one week apart, and there were no adverse events during or in the days after the tests.

R-RFD and ML were normally distributed (p > 0.05) as assessed by Shapiro-Wilk's test of normality on the studentized residuals. NR-RFD was normally distributed (p > 0.05) except for 50 % PL in V1 (p = 0.029). The main effect of preload showed a statistically significant difference. The NR-RFD was significantly higher when the preload was higher (50 % vs 20 %, F(1, 11) = 14.13, p = 0.003, η²p = 0.56), while the R-RFD was significantly lower with the higher preload (F(1, 11) = 128.15, p = 0.002, η²p = 0.92). For the ML, a significant effect with lower ML was found when the preload was higher (F(1, 11) = 24.16, p < 0.001, η²p = 0.69) (Table 1). No effect of test time was found for NR-RFD (F(1, 11) = 0.89, p = 0.37, η2p = 0.07), R-RFD (F(1, 11) = 0.4, p = 0.54, η2p = 0.03) or ML (F(1, 11) = 2.87, p = 0.12, η2p = 0.21).

For the NR-RFD, R-RFD and ML measurements (Table 1), all ICC values were good, whatever the PL (ranging from 0.78 to 0.89). All CVs were below < 10 %, except for R-RFD (CV < 15 %).

Bland and Altman plots (Fig. 4) showed no systematic bias nor proportional bias for the NR-RFD, R-RFD and ML even if we observe a slight trend to proportional bias for R-RFD at 20 % preload.

## 4. Discussion

Cervistab is an experimental device for the assessment of cervical neck muscle response to head push-loading event in rugby players. The current results showed good day-to-day reliability values in terms of ICC, CV and Bland and Altman plot, for the measures of neck extensor loading rates (NR-RFD and R-RFD) and ML after a sudden head push-loading event in the two PL conditions investigated.

According to Koo and Li. (2016), all ICC values ranging from 0.75 to

<table><caption>**Table 1**

**Absolute values and reliability** of Non-Reflex rates of force development (NR-RFD), Reflex rates of force development (R-RFD) and muscle Mechanical Latency (ML) for the two sessions (V1 and V2), according to the preload condition. For all 3 variables (NR-RFD, R-RFD and ML), the main effect of pre-load was noticed * at *p* < 0.01.</caption><thead><tr><th rowspan="2"></th><th rowspan="2">Condition<br>Preload</th><th colspan="2">Absolute Values</th><th colspan="2">Reliability</th></tr><tr><th>V1</th><th>V2</th><th>ICC<br>[95 % CI<br>]</th><th>CV<br>(%)</th></tr></thead><tbody><tr><td rowspan="2">Non-Reflex rate of<br>force development<br>(NR-RFD)<br>N/s (SD)</td><td>50 %</td><td>8225<br>(2022)*</td><td>7876<br>(1668)*</td><td>0.89<br>[0.64<br>0.97]</td><td>9.9</td></tr><tr><td>20 %</td><td>7674<br>(1557)</td><td>7463<br>(1274)</td><td>0.88<br>[0.61<br>0.97]</td><td>8.5</td></tr><tr><td rowspan="2">Reflex rate of force<br>development (R-RFD)<br>N/s (SD)</td><td>50 %</td><td>1666<br>(362)*</td><td>1576<br>(309)*</td><td>0.81<br>[0.37<br>0.94]</td><td>11.3</td></tr><tr><td>20 %</td><td>2970<br>(621)</td><td>2907<br>(773)</td><td>0.78<br>[0.20<br>0.94]</td><td>14.5</td></tr><tr><td rowspan="2">Mechanical Latency<br>(ML) ms (SD)</td><td>50 %</td><td>75.4<br>(6.2)*</td><td>78.4<br>(5.2)*</td><td>0.88<br>[0.62<br>0.97]</td><td>3.5</td></tr><tr><td>20 %</td><td>81.2<br>(5.1)</td><td>81.7<br>(4.9)</td><td>0.81<br>[0.33<br>0.94]</td><td>3.5</td></tr></tbody></table>

0.89 are good, regardless of the PL conditions. Regarding the CV, all parameters showed good values (CV < 10 %), except for the two parameters related to the R-RFD, but with values still below 15 %. In these cases, however, the ICC values remained good for 50 % PL (ICC = 0.81) and 20 % PL (ICC = 0.78). These results seem good, considering the physiological variability of the reflex response. In their study, Santos et al. (2011) measured low to moderate ICC values (range 0–0.62) for the reliability of back muscle EMG reflex response to a sudden load applied to the trunk. They recommended increasing the number of trials above 8 to increase the reliability. The present study shows that measurements of ML and NR-RFD based on the force/time curves can be used with confidence in practice.

Preload affects the characteristics of the post push-loading neck muscle reflex response in terms of latency and RFD. When the preload is higher (50 % MVIC), the absolute value of the R-RFD is lower (Table 1). The higher neck muscle stiffness induced by the higher preload could explain this association, creating more spinal stability. Thus, subjects may require less reflex muscular response to stabilize the neck after the impact (weaker R-RFD). These results are consistent with those of Granata et al. (2004) on the paraspinal lumbar muscles: the gain of the impulse response function tended to decrease with preload, although their results did not reach statistical significance. Our results are also consistent with published measurements suggesting that the paraspinal reflex response was partially inhibited as trunk preload increased (Stokes et al., 2000). Shahvarpour et al. (2015) reported similar findings for the lumbar muscle in terms of force production: when the preload was higher, the peak of muscle active forces after impact was lower. It appears that the cervical part of the spine has the same response pattern to push-loading event.

ML values of 80 ms are very consistent with those reported in the literature. In fact, (Siegmund et al. (2002) reported a reflex time of 73 ± 15 ms, with an additional electromechanical delay of 13 ± 1 ms. Thus, the sum of the reflex time and the electromechanical delay (i.e. 86 ms) as described by Siegmund et al. (2002), is very close to our measurement (75–82 ms). When the preload is higher, the ML is significantly shorter. According to Siegmund et al. (2002), the shortening of the ML could be the result of either a shorter reflex time or a shorter electromechanical delay. For Shahvarpour et al. (2015), muscle force latencies decreased significantly at higher preload, with no effect of preload on onset of EMG. This suggests that the effect of preload may be primarily a shortened electromechanical delay. This may have implications for training to minimize the risk of cervical spine injury.

## 5. Conclusion

Overall, the Cervistab device shows good reliability in assessing the neck extensor muscles response after a sudden head push-loading event under near-ecological conditions. This device could be used in primary or secondary prevention to guide players toward a safe return to play after a head/neck injury (Leider et al., 2021).

### CRediT authorship contribution statement

**Marc Julia:** Writing – original draft, Visualization, Validation, Supervision, Software, Resources, Project administration, Methodology, Investigation, Funding acquisition, Formal analysis, Data curation, Conceptualization. **Loic Damm:** Writing – review & editing, Visualization, Software, Methodology, Formal analysis, Data curation, Conceptualization. **Simon Pla:** Writing – review & editing, Validation, Methodology, Formal analysis, Data curation. **Jean-Paul Micallef:** Writing – review & editing, Validation, Methodology, Conceptualization. **Arnaud Dupeyron:** Writing – review & editing, Validation, Supervision, Methodology, Conceptualization. **Stéphane Perrey:** Writing – review & editing, Validation, Supervision, Resources, Project administration, Methodology, Funding acquisition, Conceptualization.
Non-reflex rate of force development, 50% MVC

<figure><img src="image_8.png" /></figure>

Reflex rate of force development, 50% MVC

<figure><img src="image_9.png" /></figure>

Muscular latency, 50% MVC

<figure><img src="image_10.png" /></figure>

Non-reflex rate of force development, 20% MVC

<figure><img src="image_11.png" /></figure>

Reflex rate of force development, 20% MVC

<figure><img src="image_12.png" /></figure>

Muscular latency, 20% MVC

<figure><img src="image_13.png" /></figure>

**Fig. 4.** Bland Altman plots with 95 % limits of agreement (LOA) for each dependent measure between each test session. The dashed black lines represent the 95 % LOA, the solid black line represents the bias, and the square represents the average of all trials from each participant (n = 12). For NR-RFD in 50 % PL results, V2 was on average 35 N.s⁻¹ lower than V1 (Fig. 4, top left panel). For the 20 % PL results, V2 was on average 21 N.s⁻¹ lower than V1 (Fig. 4, top right panel). The R-RFD measured at 50 % PL was on average 9 N.s⁻¹ lower at V2 than at V1 (Fig. 3, middle left panel). At 20 % PL, the result was on average 6.3 N.s⁻¹ lower in V2 than in V1 (Fig. 4, middle right panel). ML measured at 50 % PL was on average 3 ms longer in V2 than in V1 (Fig. 4, bottom left panel). 20 % PL was on average 0.3 ms longer in V2 than in V1, (Fig. 4, bottom right panel). None of the small differences observed above were statistically significant.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

This research was funded in part by grants from the Institut National du Sport, de l'Expertise et de la Performance (#12-R-26) and grants from the University of Montpellier and the Fédération Française de Rugby (#3034).
# Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.jbiomech.2024.112400.

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