The relationship between cervical flexor endurance, cervical extensor endurance, VAS, and disability in subjects with neck pain

Background Several tests have been suggested to assess the isometric endurance of the cervical flexor (NFME) and extensors (NEE) muscles. This study proposes to determine whether neck flexors endurance is related to extensor endurance, and whether cervical muscle endurance is related to disability, pain amount and pain stage in subjects with neck pain. Methods Thirty subjects (18 women, 12 men, mean ± SD age: 43 ± 12 years) complaining of neck pain filled out the Visual Analogue Scale (VAS) and the Neck Pain and Disability Scale-Italian version (NPDS-I). They also completed the timed endurance tests for the cervical muscles. Results The mean endurance was 246.7 ± 150 seconds for the NEE test, and 44.9 ± 25.3 seconds for the NMFE test. A significant correlation was found between the results of these two tests (r = 0.52, p = 0.003). A positive relationship was also found between VAS and NPDS-I (r = 0.549, p = 0.002). The endurance rates were similar for acute/subacute and chronic subjects, whereas males demonstrated significantly higher values compared to females in NFME test. Conclusions These findings suggest that neck flexors and extensors endurance are correlated and that the cervical endurance is not significantly altered by the duration of symptoms in subjects with neck pain.


Introduction
Neck pain (NP) is a condition that is becoming more and more widespread and its associated economic and social costs are ever-increasing [1]. Some possible factors are sedentary work, the increase in activities such as the use of personal computers and Internet, the use of motor vehicles, and changes of work type [2]. Some psychosocial factors are considered as the strongest prognostic factors for NP and contributing factors for slower or less complete recovery [3] and persistent pain [4]. Moreover, these factors influence the perception of pain and disability and decrease the self-efficacy perception [5].
According to various studies, in many cervical conditions such as whiplash associated disorders (WAD) or cervicogenic headache, a dysfunction of deep cervical flexors (DCF) such as longus colli and longus capitis can be found [6,7]. Other studies also describe the deep cervical extensors as being dysfunctional: especially semispinalis, sub-occipital and multifidus muscles [8][9][10].
From the literature, it seems that muscular dysfunction in the cervical spine refers to changes in structure [8][9][10][11][12] and function [13][14][15]. Moreover, the following deficiencies have been observed in people affected by NP: reductions in maximal strength, in accuracy of head position during dynamic movements and repositioning, in efficiency of contraction, and in muscle endurance [16].
Recent tests for cervical muscles have been suggested, such as the Cranial Cervical Flexion test [6], which assesses the endurance of the DCF, and the Neck Flexor Muscle test (NFME) [17,18], which evaluates the endurance of both the superficial and the deep cervical flexor muscles. In addition, other tests have recently been proposed to appraise the deep and superficial cervical extensors. The Neck Extensor Endurance test (NEE) [7,19] is probably the most common one, because it can be used in the clinical setting without any complicated tools.
Several studies have shown a relationship between pain and the strength and endurance of flexor muscles [6,[19][20][21][22], and some research has been done to investigate the relationship between pain and extensor muscles strength [7,19,21]. The relationship between endurance and the time from which the pain was present has been insufficiently studied, showing a lack of correlation between fatigability of some flexor muscles (sternocleidomastoid and anterior scalene) and duration of symptoms in chronic neck pain patients [23]. The purpose of this study was to investigate the isometric endurance of the neck extensor and neck flexor muscles in subjects complaining of acute, subacute or chronic NP, to determine whether there was any relationship between neck flexor muscle endurance, neck extensor muscle endurance, amount of pain and disability, and between endurance and duration of pain.

Subjects
We conducted an observational study. Informed consent was obtained from all subjects and the study was conducted following the ethical rules of the Orthopaedic Manual Physiotherapy Masters Research Committee at the University of Zaragoza (Spain). All procedures were carried out in accordance with the Declaration of Helsinki. Prior to participation in the study, all subjects signed an informed consent form.
Thirty-four subjects, 60% female (mean ± SD age: 43 ± 12 years), with a primary complaint of NP were assessed at the Fisioplus Private Practice (Savignano sul Panaro, Modena, Italy). The recruitment of eligible subjects was carried out by means of notices on the Internet and on information boards located in some general practitioners consulting rooms in the area of the clinic.
To be included in the study, the subjects had to be between 18-80 years of age and have a diagnosis of NP, including a thorough anamnesis and physical examination. The exclusion criteria were: the presence of positive neurological signs (abnormalities on myotomes, dermatomes and reflexes), systemic, muscular, or connective tissue disorders, cognitive disorders, and a history of trauma in the last six months.

Procedure of the tests and questionnaires
The subjects included in the study completed the Visual Analogue Scale (VAS) and the Neck Pain and Disability Scale -Italian version (NPDS-I) [24]. The score of NPDS-I can range between 0 and 100 [25], where 0-30 it is considered to be low disability; 30-70 is fairly high disability; and 70-100 is considered high disability.
Subjects were asked not only to state their pain intensity, but also to define the location of their pain on a body chart as well as the duration and frequency of their symptoms. The investigator showed pictures to the subjects (taken from studies by Harris et al. [26] and Lee et al. [7]), in order to familiarize them with the tests and explained in detail how the tests would be carried out [27]. A fluid inclinometer (G314S Plasty, Milano, Italy) was used to check the degrees of head displacement on the sagittal plane.

Neck Flexor Muscle Endurance Test (NFME test)
The test was performed in the supine and crook lying positions [26,28,29]. With the chin maximally tucked and maintained isometrically, the subject lifted the head and neck until the head was approximately 2.5 cm off the plinth while maintaining the chin retracted to the chest ( Figure 1). During the test verbal commands such as "tuck your chin in" or "hold your head up" were given whenever there was a loss of chin tuck. The test was stopped if the subject's head touched the investigator's hand for more than one second, if the skin folds began to separate due to a loss of chin tuck for the same amount of time, or if the subject wanted to stop because of fatigue or pain. The test was also stopped if the subject lost more than 5°for over two seconds (degrees measured with the inclinometer).
Holding time was recorded in seconds with a stopwatch and the reason for stopping the test was noted. Then the subject was asked to sit up and the Velcro strap was turned 180°so that the fluid inclinometer (G314S Plasty, Milano, Italy) could be fixed above the occipital bone. At least 5-minute resting period was allowed between measurements.

Neck Extensor Endurance Test (NEE test)
The subject was put in a prone position with the head protruding from the plinth [7,19,30,31], and supported on a stool, arms at side and a physiotherapy belt was fastened and tightened across the T6 level in order to support the upper thoracic spine. A plumb line was fixed underneath the Velcro strap attached around the subject's head and a small weight suspended from it (105 grams altogether), which hung to just short of the floor. Then the subject was asked to retract the chin and hold the head steady in a horizontal position while the stool was removed (Figure 2). At this point the stopwatch was started and the endurance time was measured in seconds.
The test was stopped if the subject could not maintain the head in a horizontal position (the suspended weight touched the floor), or if the subject lost more than 5°of chin tuck for over three seconds (measured with the inclinometer). The test was also discontinued if the subject wanted to stop because of fatigue or pain. After the NEE test the subject was asked to stay prone with his/her head supported for 1 minute and then to sit up.

Statistical analysis
Data were analyzed by SPSS version 15.0 (IBM Corp., Armonk, NY, USA). The Kolgomorov-Smirnov test was used to analyze the normal distribution of the variables (p > 0.05). To compare the two groups (acute/subacute or chronic NP), an unpaired t test, a Mann-Whitney U test, or a chi-square test was performed, depending on the nature and distribution of the data. An initial analysis of variance was used to compare the groups in terms of their age and gender.
Pearson's correlation coefficient was used to assess the bivariate associations of the variables intensity of pain (VAS), NP and disability (NPDS-I), endurance of the flexor neck muscles (NFME test) and endurance of the extensor neck muscles (NEE test). We considered this statistic, in keeping with the recommendations of Atkinson and Nevill [32], as follows: fair correlation when inferior to 0.30, moderate when ranging from 0.30 to 0.60 and good when superior to 0.60. The statistical analysis was conducted at a 95% confidence level, and p < 0.05 was considered statistically significant.

Results
Thirty-three subjects agreed to participate in this study. Following a thorough anamnesis, history-taking, and filling out a body chart, three of these subjects were excluded from the study: two of them had shoulder pain without cervical involvement, and one subject suffered from a genetic disease affecting the face and shoulder girdle musculature (FSH Dystrophy). Thirty subjects were included, of which 18 (60%) were female and 12 (40%) were male. The mean age was 43 ± 12 years. Sixteen subjects (53.3%) were referred from physical therapists, eight subjects (26,7%) by means of notices on the Internet boards, six subjects (20%) came with a referral from physicians.
In the 30 subjects, the performance of the NEE test was on average 246.7 ± 150 seconds (range = 48-661), whereas the performance of the NFME test was on average 44.9 ± 25.3 seconds (range = 11-112). Seven subjects in NEE test and six subjects in NFME had less than 50% of the mean score and only two subjects had more than 100% of the mean score in both tests. More than the 50% of subjects demonstrated endurance rates near the mean values in both tests. The subjects reported a mean pain VAS score of 36.67 ± 23.71 and a mean NPDS-I score of 42.95 ± 17.61.
A significant correlation was found between the results of the two endurance muscle tests (r = 0.52, p = 0.003) and a positive relationship was also found between VAS and NPDS-I (r = 0.55, p = 0.002) in the entire sample. No relevant correlation was found between the endurance tests and pain or disability (all, r < 0.26, p > 0. 21) Two included people (6.66%) complained of acute pain, 11 (36.66%) of subacute pain, and 17 (56.66%) of chronic pain. Due to the very small number of acute cases, we decided to merge acute and subacute subjects: as a consequence, our further analyses considered two different groups, which we named acute/subacute and chronic. There was no significant difference between these two groups with regard to age, sex, localization or frequency of the symptoms, referred symptoms along their arms or referred symptoms such as headache, migraine, and dizziness (Table 1). Moreover, compared with acute/subacute group, chronic NP group had no statistically significant difference in intensity of NP, although the score of NPDS-I was significantly higher in chronic group ( Table 2). Endurance of the neck extensor and neck flexor muscles appeared similar in these two groups. There were no significant differences between the groups in terms of reason to stop the isometric endurance muscle tests (pain, other symptoms, tension, fear, muscular or psychological fatigue). A significant effect of gender on NFME test was revealed [F [1,26] = 9.2, p < 0.001], but no effects of age on endurance test were demonstrated.
In chronic NP group, VAS score and NPDS-I were significantly correlated (r = 0.696, p = 0.001). In acute/ subacute NP group, intensity of pain and NPDS-I were also significantly correlated (r = 0.705, p = 0.007), and there was another significant correlation between the endurance of the flexor and extensor neck muscles (r = 0.810, p = 0.001).
Similar duration (p = 0.42) and intensity of pain (p = 0.75) and level of disability (p = 0.44) were demonstrated in males and females subgroups, in our sample. The male group lasted more time the isometric contraction in NFME test (59.33 ± 29.36 seconds) compared to female group (35.33 ± 16.98 seconds). The Mann-Whitney test showed this difference statistically significant (p = 0.035), however no other significant differences were found between these groups. In female group a positive relationship was found between VAS and NPDS-I (r = 0.55, p = 0.016), in male group the relationship was between endurance muscle tests (r = 0.781, p = 0.003).

Discussion
Our study showed significantly higher endurance of neck extensor muscles compared to flexor ones and significant relationships between pain and disability and between NFME and NEE tests. No significant relationship between each of the endurance tests, pain and disability in subjects with neck pain were found.
Results did not significantly differ between acute/subacute, and chronic subjects, nonetheless chronic subjects appeared more disabled. Falla et al. [23] had demonstrated the lack of relationship between fatigability and duration of symptoms in chronic subjects, however a relevant less endurance in chronic subjects compared to acute/subacute ones was expected. Similar characteristics for amount and location of pain in these subgroups might explain these results, despite the higher disability of chronic subjects in the sample. Another reason may be that the chronic subjects did not have fear of movement or catastrophization [33,34].
Regarding the age of subjects, no significant relationship between age and muscle endurance was found. The analyses of gender in our sample showed a significantly higher endurance on NFME test for male subjects. This finding is coherent with the study of Grimmer & Trott [18], Peolsson et al. [35,36], and Kumar at al [37]. Hormonal differences between sex might have indirect effect on muscle strength production [38,39].
NEE test results differ significantly from those of Edmondston et al. [19,21] and Lee et al. [7] (Table 3). In the latter study, an extendable tape measure (approximately 20 gr) was used. Edmondston et al. [19,21] modified NEE test proposed by Lee et al. [7] added a 2 kg weight to the bottom part of the chain, in order to reduce the duration of the test.
The NFME test was always performed first and in more than 50% of the sample it was stopped for pain or pain associated with fatigue or fear. The NFME test results are in line with the study by Edmondston et al. [19], where head and neck positioning with verbal and tactile feedback were continuously assisted. Results of this study differ from the findings obtained by  Piper et al. [20], Harris et al. [26], Placzek et al. [40], and Blizzard et al. [41] (Table 4). This could be due to the differences related to the characteristics of the groups, the examiner's methodology, or simply to physiological differences in normal populations.
According to the findings of this study, the NFME test could be considered a useful tool in the clinical setting as an examiner could use it to quickly assess the endurance of the cervical flexors without needing any complicated or expensive equipment.

Limitations of the study
We recognize that the sample size was small, although sufficient to determine significance and the lack of a control group. However, since this pathology is often accompanied with depression and neurodegenerative disorders, we had an important number of subjects with NP that were excluded of the study. The assessment of the subjects was carried out by a sole examiner, and gender differences were identified. The inclusion criteria considered a diagnosis of non-specific NP, regardless of the presence of cognitive or behavioral dysfunctions, especially in chronic subjects. Finally, we did not perform any intra-examiner reliability tests, so we cannot comment on the reliability of the clinical tests performed in the study.

Conclusion
A significant correlation was found between the results of these two tests, and a positive relationship was also found between VAS and NPDS-I in subjects with neck pain. We did not find any significant differences in results between acute/subacute and chronic subjects, whereas the comparison between males and females showed high endurance for male group in NFME test. Comparison between this study and other similar ones demonstrated some variability of endurance during the NMFE or NEE tests between different samples. On the other hand, the NEE test might be less useful in a clinical situation because it is time-consuming.

Competing interests
The authors declare that they have no competing interests.
Authors' contribution SP, JMT and CV provided idea for the research and created the hypothesis; EE, SP and CV planned the methods to generate the results; CV, CO'R and SP were responsible for organization and implementation; SP, CV, CO'R, and JHV wrote the manuscript; EE and SP were responsible for experiments, patient management, organization and reporting data; EE and SP were responsible for statistical analysis, evaluation, and presentation of the results; SP performed the literature search; SP, CV and CO'R were responsible for writing a substantive part of the manuscript; JMT, JHV and CV revised manuscript. All authors read and approved the final manuscript.   Group of symptomatic subjects who required treatment