First, demographic data, such as sex, age, weight, and height of each participant were collected. After completing the NDI questionnaire, participants were asked to sit with a straight back on a workout bench. Two of the three measurement locations [the spinous processes of C2 (high-cervical) and C7 (low-cervical)] were manually identified by two experienced manual therapists, with the spinous process of C2 being the most cranial one that can clearly be palpated and using the flexion-extension test to locate C7 (Povoa et al., 2018). C2 and C7 were marked with ink to label the location for spinal stiffness assessment and the marking was verified by both therapists to increase accuracy. For the third mid-cervical (MC) assessment location, half of the distance between the spinous process of C2 and C7 was taken.

A computer-assisted device (PulStarFRAS, Sense Technology Inc., Pittsburgh, PA) was used to measure posterior-to-anterior spinal stiffness (Leach et al., 2003). This device possesses good test–retest reliability, with intraclass correlation coefficient (ICC) values greater than 0.83 (Hausler et al., 2020). Spinal stiffness is defined as the impulse response to the deformation of the spine system; a linear, time-invariant response to a very short (<1 ms) impulse. This time invariance allows the impulse response to be measure in Newton, rather than Newton seconds (as in classical measurements) (Girod et al., 2003). A preload of 18 N was applied to trigger the assessment and overcome possible confounders caused by soft tissue components. After reaching the preload of 18 Newton, the device automatically applied an impulse with a single contact probe—a force of 27 N in a 90° angle relative to the surface of the back.

Baseline characteristics of study participants were summarized using descriptive statistics. Mean cervical spinal stiffness and 95% confidence intervals (CI) of each measurement location in all testing situations were plotted graphically.

Forty-nine male participants were recruited [mean age: 19.9 ± (SD) 1.1 years; mean height: 179.8 ± 11.4 cm; mean weight: 74.4 ± 11.4 kg]. None were excluded and none reported pain during the assessments. Figures 3–5 represents mean spinal stiffness with 95% CI for all three measurement locations, in both head positions and loading conditions.

Spinal stiffness measurements showed good reliability in both head position and measurement locations with ICCs > 0.799 and Cronbach’s alpha 0.808—0.948. All reliability values of both head position, two loading conditions, and measurement locations are shown in Table 1. All cervical stiffness values split in measurement locations are shown in Figures 3–5.

Levene’s test showed that the assumption of homogeneity of variance was satisfied. A three-way ANOVA was performed to examine the interaction effects of head position, loading, and measurement location regarding cervical spinal stiffness. There was a significant three-way interaction [F(2, 576) = 9.305, p < 0.001]. Significant two-way interactions were found between loading x measurement location [F(2, 576) = 15.688, p < 0.001] and head position × measurement location [F(2, 576) = 9.263, p < 0.001]. There was no significant interaction between loading × head position [F(1, 576) = 0.692, p = 0.406]. Post hoc analysis showed reduction of stiffness in all three measurement locations in flexion position. There was a decrease in stiffness in C2 with loading, increase in stiffness in C7 and no change in MC. The post hoc results are shown in Table 2 and Supplementary Figures 1–3 show the respective interactions.

The decrease in spinal stiffness in the flexion head position could be due to the flexion relaxation phenomenon (FRP) of the cervical spine, which describes a myoelectric “silence” of the neck extensor muscles during cervical flexion (Simon et al., 2006). This can be explained by a transfer of the extension moment from the active to the passive structures of the spine with further flexion (Pialasse et al., 2009). The FRP has been observed only for the cervical erector spinae muscle, whereas the upper trapezius muscle showed no FRP response (Colloca and Hinrichs, 2005; Maroufi et al., 2013). Furthermore, cervical flexor muscles, as antagonists, are likely to be less activated in the flexion position (Maroufi et al., 2013). At the low-cervical spine, a smaller decrease in stiffness was found in the 45-degree flexion position compared to the neutral head position. More likely, the low-cervical spine is at the end of motion given that the cervicothoracic junction experiences less flexion than other segments of the cervical spine (Nightingale et al., 2007). Therefore, this could have caused a smaller decrease in spinal stiffness. Overall, it can be hypothesized that less support by a less active muscular subsystem led to decreased cervical stiffness in the flexion head position.

Another explanation for the decrease in cervical spinal stiffness could be the pressure on the cervical intervertebral discs during flexion. During the movement of the neck in the different directions, the loads on the cervical intervertebral discs increases resulting in an increase in cervical intervertebral disc pressure (Bayoglu et al., 2019). Another study reported a twofold increase in pressure in the cervical discs with flexion and a fourfold increase of the shear forces (Barrett et al., 2020). This additional load, generated by flexion, leads to capsular ligament laxity of the facet joints (Steilen et al., 2014), the so-called buckling effect (Nightingale et al., 1996). By reducing the passive stability, the buckling effect might have decreased the spinal stiffness in the present study.

The interaction effect between loading and measurement location showed that loading had some effect. A decrease in stiffness in the high cervical region and an increase in the low-cervical spine was observed. The change in stiffness in the high cervical spine due to the additional load might be explained by capsular ligament laxity due to the buckling effect (Nightingale et al., 1996). Thus, the reduced tension on the passive structures might have led to a play between the structures that resulted in a reduction in spinal stiffness. The unchanged spinal stiffness in the mid-cervical vertebrae might be the results of opposite effects that cancel each other out, namely muscle activity and buckling. In contrast to the high-cervical spine, more low cervical muscle activity is needed to stabilize not only the head and the additional load, but also the high-cervical spine (Bergmark, 1989; Swanenburg et al., 2020; Glaus et al., 2021). This increased muscle activation would be expected to lead to an increase in spinal stiffness (Swanenburg et al., 2020). Thus, the unchanged stiffness of the mid-cervical spine might be the net effect of buckling effects and increased muscle activity. The stiffness at the low-cervical spine increased with additional load. This increase in spinal stiffness can be explained by an increase in muscle activity to stabilize not only the head and extra load, but also the decreased stiffness of the high-cervical spine. Moreover, mobility is maximal at the low-cervical spine (Penning, 1978). Compression of the cervical spine due to the additional load and the consequent relaxation of the stabilizing ligaments appears to be less dominant in the low-cervical spine. More muscle activity is needed to stabilize the cervical spine because of the lesser passive stability (Izzo et al., 2013). Additionally, the low-cervical spine is closer to structures that provide additional stability, such as the ribs and the sternum. It could be argued that the more mobile low-cervical spine needs more muscle activation to stabilize the cervical spine with the additional load, which led to increased stiffness at the low-cervical spine.

There is relationship between a flexion neck posture and neck pain symptoms (Barrett et al., 2020), especially if this flexed posture is sustained for a long period of time, as in the case of excessive use of mobile devices (Ariens et al., 2001; Bayoglu et al., 2019). Avoiding prolonged static postures and a flexed head position greater than 30 degrees might help to prevent neck pain.

The generalizability of the present study’s results is unknown because only asymptomatic young male subjects were included. Additionally, other factors that might influence cervical spinal stiffness were not measured. For example, muscle activity was not directly assessed by electromyography (EMG). The activity of the deep neck flexors, such as the longus capitis and longus colli, cannot be measured with superficial EMG; this would require the use of a nasopharyngeal catheter, the application of which would have been invasive and impractical in the study environment (Robinson et al., 2009). Individual differences in muscle dimensions that stabilize the cervical spine were not considered. The individuals’ cervical range of motion in flexion direction was not assessed. Nevertheless, all participants were able to assume the 45-degree flexion position without any difficulty.