Widespread impairment of tactile spatial acuity and sensory-motor control in patients with chronic nonspecific neck pain with neuropathic features

Musculoskeletal Science and Practice 47 (2020) 102138

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Original article

Widespread impairment of tactile spatial acuity and sensory-motor control in patients with chronic nonspecific neck pain with neuropathic features �pez-de-Uralde-Villanueva a, *, Irene Tostado-Haro b, Beatriz Noval-Granda b, Ibai Lo ~ a b, c, d, Tamara Del Corral b, c Raúl Ferrer-Pen a

Department of Radiology, Rehabilitation and Physiotherapy, Faculty of Nursing, Physiotherapy and Podiatry, Complutense University of Madrid, Madrid, Spain Departamento de Fisioterapia, Facultad de Ciencias de la Salud. Centro Superior de Estudios Universitarios La Salle, Universidad Aut� onoma de Madrid, Spain Motion in Brains Research Group, Instituto de Neurociencias y Ciencias del Movimiento (INCIMOV), Centro Superior de Estudios Universitarios La Salle, Universidad Aut� onoma de Madrid, Spain d Centro de Salud Entrevías, Gerencia de Atenci� on Primaria, Fundaci� on para la Investigaci� on e Innovaci� on Biom�edica en Atenci� on Primaria de la Comunidad de Madrid (FIIBAP), Servicio Madrile~ no de Salud, Madrid, Spain b c

A R T I C L E I N F O

A B S T R A C T

Keywords: Position sense Tactile sense Proprioception Neck pain/diagnosis Somatosensory discrimination disorder

Objective: To assess differences in tactile spatial acuity and in sensory-motor control between patients with chronic nonspecific neck pain (CNSNP) with and without neuropathic features (NF), as well as asymptomatic. Methods: 183 participants were included, 135 had CNSNP classified by the Self-report version of Leeds Assess­ ment of Neuropathic Symptoms and Signs scale in order to identify pain with NF: (1) CNSNP with NF (n ¼ 67), (2) CNSNP with No-NF (n ¼ 68), and (3) asymptomatic subjects (n ¼ 48). The following tests in the following order were assessed after determining the participants’ clinical character­ istics: 1) two-point discrimination, 2) joint position error, and 3) craniocervical flexion test. Results: Both neck pain groups showed a significant reduction in their ability to discriminate two points in the trapezium and masseter, as well as a significant deficit of a moderate to large magnitude in craniocervical motor control compared with the asymptomatic group. However, only the CNSNP with NF group showed a significant impairment of the two-point discrimination in the tibia (d ¼ 0.57) and a significant impairment of the kinesthetic sense (neck rotation, d ¼ 0.73; neck lateroflexion, d ¼ 0.69), compared with the asymptomatic group. Significant differences in pain intensity, disability and psychological factors between the CNSNP groups were also found, observing the poorest results in the NF group. Conclusions: Patients with CNSNP with NF have a greater sensory, motor and psychological impairment than those without NF, more pain intensity, disability and negative psychological factors, as well as more impaired tactile spatial acuity in areas remote to the pain and impaired cervical kinesthetic sense.

1. Introduction Neck pain is one of the musculoskeletal conditions that creates the most disability worldwide (Vos et al., 2016; Hoy et al., 2014) and tends to become chronic (Vos et al., 2008; Carroll et al., 2009). Most cases of chronic neck pain are labeled as nonspecific, due to the difficulty in identifying the causes of the pain (Sluka, 2016; Blanpied et al., 2017). This difficulty, coupled with the lack of relationship between tissue damage/disease (Hogg-Johnson et al., 2009; Nakashima et al., 2015) and pain, could suggest the presence of maladaptive central pain

mechanisms responsible for maintaining the pain over time and the low rate of success with treatment (Bier et al., 2018; Nijs et al., 2016a; Sterling, 2010). New classification models for neck pain have therefore been developed in recent decades, based on clinical characteristics rather than merely anatomical and biomechanical aspects (Blanpied et al., 2017; Dewitte et al., 2016; Fritz and Brennan, 2007). Identifying the different patterns of somatosensory impairment within neck pain could therefore facilitate the application of more specific treatments with higher success rates (Blanpied et al., 2017; Dewitte et al., 2016; Fritz and Brennan, 2007).

* Corresponding author. Department of Radiology, Rehabilitation and Physiotherapy, Faculty of Nursing, Physiotherapy and Podiatry, Complutense University of Madrid, Plaza Ram� on y Cajal nº 3, Ciudad Universitaria, 28040, Madrid, Spain. E-mail addresses: [email protected] (I. L� opez-de-Uralde-Villanueva), [email protected] (I. Tostado-Haro), [email protected] (B. NovalGranda), [email protected] (R. Ferrer-Pe~ na), [email protected] (T. Del Corral). https://doi.org/10.1016/j.msksp.2020.102138 Received 1 November 2019; Received in revised form 4 February 2020; Accepted 24 February 2020 Available online 25 February 2020 2468-7812/© 2020 Elsevier Ltd. All rights reserved.

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Musculoskeletal Science and Practice 47 (2020) 102138

A systematic review published in 2015 established that typical signs associated with central sensitization are not typically present in chronic nonspecific neck pain (CNSNP), although its presence should not be ruled out in some cases given it is a highly heterogeneous condition (Malfliet et al., 2015). Recent publications have suggested that only CNSNP with neuropathic features (NF) could be associated with signs of �pez-de-Uralde-Villanueva et al., 2016a; central sensitization (Lo �pez-de-Uralde-Villanueva et al., 2016b). Some of the specific sensory Lo impairments that have led to the suggestion of a major central compo­ nent are widespread mechanical/thermal hypersensitivity, especially cold hyperalgesia, as well as increased neural mechanosensitivity in the upper limb (Ng et al., 2014; Sterling, 2008; Sterling and Kenardy, 2008). Loss of somatosensory function (e.g. hypoaesthesia) has been observed in patients with cervical pain with signs of central sensitization (Chien et al., 2009). However, none of the mentioned studies assessed tactile spatial acuity, whose assessment through two-point discrimination (TPD) could be useful in identifying a reduction in somatosensory function. In fact, it has been suggested that changes in tactile spatial acuity are related to the presence of maladaptive changes in the primary somatosensory cortex (Catley et al., 2013, 2014a; Adamczyk et al., 2018a). The presence of maladaptive cortical reorganization is relevant because it is an additional finding/sign for determining with greater certainty the presence of central sensitization in CNSNP with NF (Pel­ €fner, 2009; Nijs et al., 2016b). Ev­ letier et al., 2015; Seifert and Maiho idence on an impairment in tactile spatial acuity in patients with chronic neck pain is scarce and controversial, relying on small samples composed at times of neck pain of various origins (traumatic and nonspecific) and assessing this variable exclusively in the painful region or in related dermatomes (Moreira et al., 2017; Cheever et al., 2017; Elsig et al., 2014), except for one study that also assessed it at a remote site (Harvie et al., 2018). Based on the fact that pain with NF is associ­ ated with signs of central sensitization, the authors consider that the presence of NF in CNSNP could be a determining factor in terms of shedding more light on these inconclusive results. There is a need for further studies with larger sample sizes that evaluate tactile acuity in areas distant from the location of the pain. The objective of a rehabilitation program is to eradicate the symp­ toms and recover motor function, given that the latter is not automati­ cally re-established after the pain has ceased (Hodges and Moseley, 2003; Sterling et al., 2003a). The loss of proprioception is one of the contributing factors to impaired of motor function (Botnmark et al., 2016; Hillier et al., 2015; Riemann and Lephart, 2002), which can facilitate re-injury and pain chronification (Hall et al., 1995; Kristjans­ son and Treleaven, 2009). Identifying potential proprioceptive disorders through sensory-motor control tests is therefore relevant (Kristjansson and Treleaven, 2009). The joint position error (JPE) test and cranio-cervical flexion test (CCFT) are the most widely used of these tests, the results of which have suggested that patients with CNSNP exhibit poor neuromotor control compared with asymptomatic subjects (de Zoete et al., 2017; Stanton et al., 2016a; Jull et al., 2008). Impaired tactile acuity can potentially result in impairment of craniocervical motor control and JPE because the neck position sense is obtained through afferent stimuli from sensory receptors in the skin, joints and muscles (Bolton, 1998; McLain, 1994; de Vries et al., 2015). In addition, the impairment of tactile acuity may reflect the disruption of intra­ cortical inhibition mechanisms, so the loss of somatosensory acuity may also be responsible for the perpetuation of pain (Harvie et al., 2016). Considering that patients with neuropathy clearly present impaired tactile spatial acuity (Saeidian et al., 2011; Eryilmaz et al., 2013; Chiu et al., 2014), the authors consider that the presence of NF could be essential when observing a marked clinical difference between patients with CNSNP and asymptomatic subjects. The main objective of the present study is therefore to assess dif­ ferences in tactile spatial acuity and in sensory-motor control between patients with CNSNP with and without NF, as well as those of asymp­ tomatic subjects. Also, to assess the differences in the clinical

characteristics between these populations. 2. Materials and methods 2.1. Study design A research study with a cross-sectional, observational, descriptive and nonprobabilistic design was implemented. The assignment of pa­ tients with CNSNP to the NF and non-NF groups was conducted ac­ cording to the Spanish version of the Self-report version of the Leeds Assessment of Neuropathic Symptoms and Signs scale (S-LANSS) �pez-de-Uralde-Villanueva et al., 2016c), in the same manner as (Lo �pez-de-Uralde-Villanueva employed in previous research studies (Lo �pez-de-Uralde-Villanueva et al., 2016b). The Ethics et al., 2016a; Lo Committee of La Salle University Center for Advanced Studies (Madrid, Spain) ensured that the study met the principles established in the Declaration of Helsinki and approved its implementation. The sample size was calculated using the statistical software G*Power© (University of Dusseldorf, Germany). An independent t-student test, with 80% power and 0.05 α error, was performed to assess differences in tactile spatial acuity between patients with CNSNP with and without NF. A moderate effect-size (d ¼ 0.5) was selected because this magnitude could be considered clinically relevant (Angst et al., 2017), the minimal effect-size was chosen in order to obtain the greatest number of partic­ ipants and thus not to decrease study power. Thus, a total sample size of at least 128 patients with CNSNP (64 with NF and 64 without NF) was established. The study also included a control group consisting of a large sample (n > 30) of asymptomatic subjects. 2.2. Participants The participants selection was conducted between November 2015 and May 2017. The study sample consisted of patients with CNSNP recruited from the Miraflores Health Centre (Alcobendas, Madrid, Spain) and from the Entrevías Health Centre (Madrid, Spain) using convenience sampling. All participants were required to read and sign the informed consent document. The inclusion criteria established for the symptomatic groups were an age between 18 and 65 years, neck pain of unknown etiology, pain for at least six months and the ability to read and speak Spanish. The exclusion criteria were as follows: rheumatic disease, cancer, fibromyalgia, osteoporosis, cervical radiculopathy, myelopathy, a history of surgery/trauma in the cervical spine, neuro­ logical diseases, pregnancy and having undergone therapy targeted to their pain (including physical therapy and drugs) within the last month. The asymptomatic group consisted of subjects between the ages of 18 and 65 years. In addition to meeting the exclusion criteria established for the symptomatic groups, the asymptomatic group needed to be pain free for at least the last three months. The requirement for this last criterion was increased to 12 months in the case of pain circumscribed to the neck, orofacial, arms and upper chest regions. 2.3. Variables All assessments were performed by two examiners, who were blin­ ded to the group to which the participants belonged. Both evaluators were instructed on performing the measurement protocol in a stan­ dardized manner to reduce, as much as possible, measurement errors inherent in any assessment. The assessment protocol began in a separate room with the completion of the questionnaires aimed at determining the participants’ clinical characteristics. The examiners then assessed the following tests in the following order: 1) TPD, 2) JPE and 3) CCFT. This order was established because the TPD and JPE tests can be affected by fatigue and muscle contraction (Owens et al., 2006; Han et al., 2015).

2

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2.4. Clinical characteristics

each variable is detailed below:

Various psychological variables were assessed in all study partici­ pants with the help of various Spanish-validated scales with acceptable psychometric properties. The fear of movement, pain catastrophizing, anxiety and depression were evaluated by the short version of the Tampa Scale of Kinesiophobia (scores range from 11 to 44) �mez-P� (Go erez et al., 2011), the Pain Catastrophizing Scale (scores range from 0 to 52) (García Campayo et al., 2008) and the Hospital Anxiety and Depression Scale —divided into two subscales for anxiety and depression and the range of scores as 0–42— (Quintana et al., 2003), respectively. For all of these scales, a higher score indicated greater involvement of the psychological construct assessed by the scales. Only the patients with CNSNP completed the following scales directed at cataloguing the pain characteristics in greater depth. The SLANSS was used to identify pain with NF (scores range from 0 to 24), a score � 12 indicates pain with NF (sensibility ¼ 88.7%; specificity ¼ �pez-de-Uralde-Villanueva et al., 2016c). The pain intensity 76.6%) (Lo was measured by the Visual Analogue Scale (Jensen et al., 1999). The patients were asked to indicate their pain intensity at the time by marking it at the 100-mm horizontal line (0 ¼ “no pain” and 100 ¼ “the worst pain imaginable”) (Bijur et al., 2001). Finally, the Neck Disability Index (NDI) was used to evaluate perceived neck disability level (scores range from 0 to 50) (Andrade Ortega et al., 2010), a higher score indi­ cated greater disability.

- Cervical kinesthetic sense: The cervical JPE test (Revel et al., 1991a), which mainly assesses afferent disorders in the neck joints and particularly in the muscle receptors (de Vries et al., 2015), was applied to assess the kinesthetic sense. The test was performed with the participants seated on a fixed chair with a backrest placed 90 cm from a target attached to the wall. A laser device was then attached to the participant’s head, who was instructed to identify, feel and memorize their neutral position. To measure the degree of position error, the participant’s eyes were covered, and they were asked to perform the physiological movements of the neck region in a sub­ maximal manner (without reaching the end of the range of motion), returning in each occasion to the starting position as accurately as possible. The movements were performed slowly (to minimize vestibular afferents) in the following order: (1) flexion, (2) extension, (3) right rotation, (4) left rotation, (5) right lateroflexion and (6) left lateroflexion. Before each movement, the participants could reposi­ tion their head in the neutral position with visual help. The distance between the final location of the laser and the center of the target was used to calculate the magnitude of the position error expressed in degrees (Chen and Treleaven, 2013). Each movement was performed on three occasions, using the mean of the values for the statistical analysis. Measuring JPE with a laser device is useful and reliable in the clinical setting (Juul et al., 2013). - Craniocervical motor control: The assessment of craniocervical motor control was performed using the CCFT (Jull et al., 2008). For this test, the participants were positioned in supine decubitus with the head and neck in a neutral position. Once the participant was in this position, a pressure sensor (Stabilizer, Chattanooga Stabilizer Group Inc., Hixson, TN, USA) was placed on the back of the neck and inflated to a stable pressure of 20 mmHg. The participant was then asked to perform craniocervical flexion (moving the chin down to the chest —double chin—), increasing the stabilizer pressure as much as possible without exceeding 30 mmHg. For the statistical analysis, the highest pressure level that the patient could maintain for 10 s without performing compensations (activation score) was recorded. In the event of compensatory movements, these were adjusted only once, concluding the test if they reoccurred (Elsig et al., 2014). The CCFT has been shown to be reliable when applied to patients with neck pain (Jørgensen et al., 2014).

2.5. Tactile spatial acuity Tactile spatial acuity was assessed using the TPD test because it is the most common test and has the greatest reliability for this purpose in the neck (Harvie et al., 2017). The TPD test was performed with the help of an esthesiometer (Two Point Discriminator, Baseline®) according to the protocol described by Luomajoki and Moseley (2011), although with some minor modifications. Throughout the assessment, the participant remained in supine decubitus with their eyes closed. The process con­ sisted of applying five series of stimuli to the skin in increasing order of distance between the two points, and five series in decreasing order (Catley et al., 2013). The amount of pressure exerted on each stimulus was sufficient to generate an indentation of approximately 2 mm in the skin and was not meant to generate any type of discomfort (Moberg, 1990). Upon the application of each stimulus, the participant indicated whether they perceived one point or two, answering with one if un­ certain. The series of stimuli in increasing order began with a distance of 0.3 cm between the two points and increased by steps of 0.3 cm until the participant was able to sense two points. The series of stimuli in decreasing order began with 7 cm of separation between the two points and decreased by steps of 0.3 cm until the participant sensed only one point. To prevent the participant from guessing based on the series pattern, “cheating” stimuli were included, consisting of distances outside the sequence or the application of a single point. The TPD threshold was established as the shortest distance in which the partici­ pant could perceive two points, considering that a shorter distance re­ flected better tactile spatial acuity. The test was performed in three regions (upper fibers of the trapezius, masseter and tibia), applied on the symptomatic side for the patients with unilateral pain and on the dominant side for patients with bilateral pain and for asymptomatic subjects. A horizontal direction was employed for the trapezium and a vertical direction for the masseter and tibia. The mean of the five increasing and decreasing series was used for the statistical analysis. This procedure has been used to assess tactile acuity in previous occa­ sions and has shown high reliability (Catley et al., 2013).

2.7. Statistical analysis The data analysis was performed with the software SPSS (Statistical Package for the Social Sciences 21, SPSS Inc., Chicago, IL USA). A value of p < 0.05 was considered statistically significant. A parametric sta­ tistical analysis was used because the three study samples were large (>30 participants per sample). Samples of this magnitude were considered large; therefore, based on the central limit theorem, the different evaluated variables showed a normal distribution (Nixon et al., 2010). The group factor was assessed using a one-way analysis of variance (ANOVA). The age was used in a covariate analysis, whereas this vari­ able may influence the TPD results. However, the results, when including age as a covariate, were identical when it was not included. The ANOVA effect size was calculated using the partial eta-squared (η2p), in which the magnitude of the effect was classified as small (0.01–0.059), medium (0.06–0.139) or large (>0.14). In the case of significant ANOVA findings, a multiple comparisons analysis with Bonferroni corrections was performed. Effect sizes were established between groups according to Cohen’s method (Cohen’s d): an effect size of 0.2–0.49 was considered as a small effect, 0.5–0.79 as a medium effect, and >0.8 as a large effect. In addition, because only patients had pain and disability, a student’s t-test was used to detect differences between disability and pain intensity between patients with

2.6. Sensory-motor control Sensory-motor control was assessed using the cervical kinesthetic sense and craniocervical motor control. The assessment procedure for 3

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CNSNP with and without NF.

Table 2 Descriptive data and between groups differences for tactile spatial acuity and sensory-motor control.

3. Results

Mean � SD

A total of 216 patients were invited to participate in the study, 48 of whom were asymptomatic subjects; the rest had neck pain. Of the total initial sample, 33 subjects were not included in the study for various reasons: 21 did not meet the inclusion criteria, and 12 decided not to participate in the research study. Ultimately, 183 participants met the inclusion criteria, agreed to enter the study and were distributed to the three groups as follows: CNSNP with NF group (n ¼ 67), CNSNP with No-NF group (n ¼ 68) and asymptomatic group (n ¼ 48). The groups had no significant differences in the anthropometric variables (P > 0.05), providing homogeneity to the groups, and were therefore of similar characteristics (Table 1).

NF (N ¼ 67)

No-NF (N ¼ 68)

AG (N ¼ 48)

TPD-Trapezius (mm)

50.18 � 11.03

47.96 � 10.89

42.55 � 9.61

TPD-Masseter (mm)

31.74 � 10.37

30.57 � 9.67

23 � 7.33

TPD-Tibial (mm)

41.52 � 9.75

37.7 � 9.76

35.4 � 11.78

JPE-Flexion (� )

5.01 � 2.64

4.1 � 2.32

3.97 � 1.5

JPE-Extension (� )

5.73 � 3.72

5.21 � 3.78

4.24 � 2.37

JPE-Rotation (� )

5.8 � 3.4

4.54 � 2.59

3.89 � 1.49

JPELateroflexion (� )

5.18 � 2.42

4.45 � 1.75

3.78 � 1.55

CCFT (mmHg)

25.52 � 2.85

25.91 � 2.82

27.71 � 2.02

3.1. Tactile spatial acuity The group factor analysis using one-way ANOVA revealed statisti­ cally significant differences for the TPD in all evaluated regions. [Trapezius (F ¼ 7.38; P ¼ 0.001; η2p ¼ 0.076); Masseter (F ¼ 12.69; P < 0.001; η2p ¼ 0.155); Tibia (F ¼ 5.23; P ¼ 0.006; η2p ¼ 0.055)]. In the multiple comparisons, there were no statistically significant differences between the CNSNP groups. Both neck pain groups showed a significant reduction in their ability to discriminate two points in the trapezium and masseter compared with the asymptomatic group. In the tibia evaluation, however, only the CNSNP with NF group showed sig­ nificant impairment in tactile spatial acuity compared with the asymp­ tomatic group. All effect sizes obtained in the significant differences observed between the CNSNP groups and the asymptomatic group were moderate to large, with the CNSNP with NF group presenting the highest magnitude. The means (�SD) values of the groups and the mean dif­ ference between the groups with their corresponding 95% CI are listed in Table 2. In addition, graphical representation of multiple comparisons between groups is shown in Fig. 1. 3.2. Sensory-motor control We obtained statistically significant differences in the group factor analysis for craniocervical motor control (F ¼ 10.36; P < 0.001; η2p ¼ 0.105) and kinesthetic sense for all physiological cervical movements except for extension [JPE-Flexion (F ¼ 3.76; P ¼ 0.025; η2p ¼ 0.041); JPE-Extension (F ¼ 2.60; P ¼ 0.078; η2p ¼ 0.029); JPE-Rotation (F ¼ 7.34; P ¼ 0.001; η2p ¼ 0.079); JPE-lateroflexion (F ¼ 6.76; P ¼ 0.002; η2p ¼ 0.075)]. The results obtained for the measurements of right side tilt merged with those of the left because the JPE of rotation and incli­ nation movements showed no statistically significant differences for side factor. This procedure has been used in previous studies (Stanton et al., 2016b).

Age (years) Gender (female: male) Height (cm) Weight (kg)

CNSNP with NoNF (N ¼ 68)

Asymptomatic Group (N ¼ 48)

Pvalues

41.82 � 13.26 48:19

39.91 � 14.36 49:19

36.6 � 14.14 30:18

0.142a 0.482b

165.68 � 9.96 68.7 � 16.22

168 � 10.25 70.45 � 14.53

169.48 � 8.58 69.19 � 12.62

0.116a 0.789a

a) 2.22 ( 2.2 to 6.64); d ¼ 0.2 b) 7.62 (2.77–12.48); d ¼ 0.74 y c) 5.4 (0.57–10.24); d ¼ 0.53 * a) 1.16 ( 3.47 to 5.8); d ¼ 0.12 b) 8.73 (4.2–13.26); d ¼ 0.97 y c) 7.57 (2.91–12.23); d ¼ 0.88 y a) 3.82 ( 0.48 to 8.11); d ¼ 0.39 b) 6.11 (1.4–10.83); d ¼ 0.57 y c) 2.3 ( 2.41 to 7); d ¼ 0.21 a) 0.91 ( 0.05 to 1.87); d ¼ 0.37 b) 1.04 ( 0.006 to 2.08); d ¼ 0.48 c) 0.13 ( 0.91 to 1.17); d ¼ 0.07 a) 0.52 ( 0.94 to 1.97); d ¼ 0.14 b) 1.49 ( 0.1 to 3.07); d ¼ 0.48 c) 0.97 ( 0.61 to 2.54); d ¼ 0.31 a) 1.26 (0.09–2.42); d ¼ 0.42 * b) 1.91 (0.66–3.16); d ¼ 0.73 y c) 0.65 ( 0.59 to 1.9); d ¼ 0.31 a) 0.73 ( 0.13 to 1.59); d ¼ 0.35 b) 1.4 (0.47–2.33); d ¼ 0.69 y c) 0.67 ( 0.26 to 1.6); d ¼ 0.41 a) 0.4 ( 1.51 to 0.72); d ¼ 0.14 b) 2.19 ( 3.41 to 0.98); d ¼ 0.89 y c) 1.8 ( 3 to 0.59); d ¼ 0.73 y

Abbreviations: AG, Asymptomatic Group; CCFT, Craneocervical Flexion Test; CI, Confidence Interval; JPE, Joint Position Error; NF, Neuropathic Features; TPD, Two-Point Discrimination; *P < 0.05. yP < 0.01.

Table 1 Anthropometric characteristics of participants. Values are presented as mean � SD and absolute frequency (number). CNSNP with NF (N ¼ 67)

Mean difference (95% CI); effect size (d) a) NF vs No-NF b) NF vs AG c) No-NF vs AG

Table 2 shows the multiple comparison analysis, and its graphical representation can be observed in Fig. 1. Both neck pain groups showed a significant deficit of a moderate to large magnitude in craniocervical motor control compared with the asymptomatic group. In terms of the kinesthetic sense, there were significant differences between the two symptomatic groups, with a greater JPE in the CNSNP with NF group for the rotation movement. Only the CNSNP with NF group showed sig­ nificant impairment of the kinesthetic sense compared with the asymptomatic group, specifically for neck rotation and lateroflexion movements, showing effect sizes of 0.73 and 0.69, respectively. How­ ever, there were no differences in the kinesthetic sense between the CNSNP with No-NF group and the asymptomatic group.

Abbreviations: CNSNP, Chronic Nonspecific Neck Pain; NF, Neuropathic Features. a One-way Analysis of Variance (ANOVA). b Chi-squared test. 4

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Fig. 1. Graphical representation of multiple comparisons for tactile spatial acuity and sensory-motor control. AG, Asymptomatic Group; NF, Neuropathic Features. Error bars represent the standard deviations. *P < 0.05.

3.3. Clinical characteristics

psychological factors than the asymptomatic group, finding significant differences of considerable magnitude (d ¼ 0.60–1.81), especially when compared with the NF group. The means (�SD) values of the groups and the mean difference between the groups with their corresponding 95% CI are listed in Table 3.

The one-way ANOVA showed statistically significant differences in the group factor in the psychological variables [TSK-11 (F ¼ 19.70; P < 0.001; η2p ¼ 0.184); PCS (F ¼ 37.18; P < 0.001; η2p ¼ 0.296); HADS-A (F ¼ 32.20; P < 0.001; η2p ¼ 0.268); HADS-D (F ¼ 19.21; P < 0.001; η2p ¼ 0.179)]. The post-hoc analysis obtained statistically significant differences in pain intensity, disability and psychological factors between the CNSNP groups, observing poorer results for these variables in the NF group. Practically all the effect sizes were moderate, except for neck disability, which showed a difference of considerable magnitude (d ¼ 1). Addi­ tionally, both neck pain groups reported higher levels of negative

4. Discussion As far as the authors know, this is the first study on patients with CNSNP that assessed whether the presence of pain with NF results in greater sensory-motor impairment (deficit in craniocervical motor control and cervical kinesthetic sense). It is also the first time that tactile spatial acuity has been assessed in areas neuro-anatomically unrelated 5

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found no significant differences between these patients and asymp­ tomatic subjects (Moreira et al., 2017; Elsig et al., 2014). The discrep­ ancy could lie in the fact that the patients included in these studies presented a less intense and disabling pain, given that neck TPD has been positively related to pain intensity (Harvie et al., 2018). Never­ theless, these studies’ sample sizes were dramatically smaller than ours, and the assessment protocols sometimes only included an ascending and descending series; our findings might therefore be stronger. A systematic review conducted on chronic lower back pain established that patients required approximately 10 mm more than asymptomatic subjects to correctly discriminate two points (Adamczyk et al., 2018b), a distance that resembles that observed in our NF group. Moreover, reliability studies conducted on the spinous process at the C7 level found a stan­ dard error of measurement and a minimum detectable change of 3.7 mm (Harvie et al., 2017) and 24 mm (Catley et al., 2013), respectively. Therefore, the difference observed in our study only exceeded the standard error of measurement. All of this, along with the considerable intragroup and intergroup variability (as can be seen by the large standard deviation), means that our findings should be interpreted with caution, as should their comparison with those of other studies. Never­ theless, the magnitude of the effect size (a measure that considers the variability) between the patients and asymptomatic subjects was mod­ erate, which, according to certain authors, could be considered clinically relevant (Angst et al., 2017). Although the authors could not firmly conclude that there are differences in the neck region between the pa­ tients with CNSNP and the asymptomatic subjects, our results suggest that having CNSNP increases the degree of tactile spatial acuity dysfunction, especially when the pain presents NF. Based on our results, tactile spatial acuity impairment is not exclu­ sively circumscribed to the area of pain. In fact, both pain groups pre­ sented impaired TPD in a neuro-anatomically related area (masseter muscle, due to the converge of stimuli from the trigeminal and neck area in the caudal trigeminal-cervical nucleus) (Bartsch and Goadsby, 2003; Sessle, 1999), but only the NF group present impaired TPD in a remote area. Recent studies support these results, showing how patients with chronic neck pain were less able to discriminate two points in the C5 dermatome (Cheever et al., 2017) and at the lumbar level (Harvie et al., 2018); however, there are studies on patients with lower back pain that reported no impairment in tactile discrimination in areas without pain (Peters and Schmidt, 1991; Moseley, 2008). TPD requires peripheral and central mechanisms. A number of authors have suggested that the cen­ tral mechanisms have greater relevance in back pain because the sensory thresholds are not altered (Luomajoki and Moseley, 2011). In central sensitization processes, skin stimuli could trigger nociceptive mecha­ nisms (Woolf et al., 2006). This situation, coupled with a reduction in pain thresholds, could generate supraspinal noise due to a loss of inhi­ bition, resulting in impaired tactile spatial acuity (Luomajoki and Moseley, 2011). This hypothesis is reinforced by evidence suggesting that TPD depends to a greater extent on the magnitude of the stimulus than on its spatial dimension (Tong et al., 2013; Craig and Johnson, 2000). All of this could explain our results because patients with CNSNP seem to exclusively have peripheral/segmental hyperalgesia (Malfliet et al., 2015), unlike patients with CNSNP with NF who appear to have generalized hyperalgesia (L� opez-de-Uralde-Villanueva et al., 2016a; �pez-de-Uralde-Villanueva et al., 2016b). Surprisingly, the difference Lo in tactile acuity on the masseter between the asymptomatic group and both pain groups was also greater than in the neck area. Most people spend long hours seated (Clemes et al., 2014; Rezende et al., 2016), easily adopting postures with the head positioned forward, which pro­ motes sustained contractions of the posterior neck muscles (Patwardhan et al., 2018; Edmondston et al., 2011) and increases the activity of the masticatory muscles (Ohmure et al., 2008). The sustained contraction of all these muscles can worsen the TPD on these areas, even in asymp­ tomatic subjects (Han et al., 2015). Our results help increase the evidence supporting an impairment of the motor pattern in patients with chronic neck pain (Elsig et al., 2014;

Table 3 Descriptive data and between groups differences for clinical features. Mean � SD NF (N ¼ 67)

No-NF (N ¼ 68)

AG (N ¼ 48)

Pain intensity [VAS(mm)]

61.69 � 19.99

53.27 � 20.23

–

Neck disability (NDI)

24.07 � 10.49

14.7 � 8.14

–

Kinesiophobia (TSK-11)

28.45 � 6.63

24.56 � 5.83

20.67 � 7.03

Pain Catastrophizing (PCS)

21.92 � 12.57

15.66 � 11.42

4.46 � 5.39

Anxiety (HADS-A)

9.92 � 3.92

7.19 � 3.50

4.63 � 2.68

Depression (HADSD)

6.06 � 3.98

4.16 � 3.06

2.27 � 2.05

Mean difference (95% CI); effect size (d) a) NF vs No-NF b) NF vs AG c) No-NF vs AG a) 8.42 (1.58–15.27); d ¼ 0.42 * b) – c) – a) 9.37 (6.03–12.71); d¼1y b) – c) – a) 3.89 (1.18–6.61); d ¼ 0.62 y b) 7.78 (4.77–10.79); d ¼ 1.14 y c) 3.89 (0.91–6.86); d ¼ 0.60 y a) 6.26 (1.78–10.74); d ¼ 0.52 y b) 17.46 (12.55–22.38); d ¼ 1.81 y c) 11.2 (6.35–16.05); d ¼ 1.25 y a) 2.73 (1.27–4.19); d ¼ 0.74 y b) 5.3 (3.69–6.9); d ¼ 1.58 y c) 2.57 (0.99–4.14); d ¼ 0.82 y a) 1.9 (0.55–3.26); d ¼ 0.54 y b) 3.79 (2.31–5.28); d ¼ 1.2 y c) 1.89 (0.43–3.35); d ¼ 0.73 y

Abbreviations: AG, Asymptomatic Group; CI, Confidence Interval; HADS-A, Hospital Anxiety and Depression Scale-Anxiety; HADS-D, Hospital Anxiety and Depression Scale-Depression; NDI, Neck Disability Index; NF, Neuropathic Features; PCS, Pain Catastrophizing Scale; TSK-11, Tampa Scale of Kinesiophobia-11; VAS, Visual Analogue Scale. *P < 0.05. yP < 0.01.

to the neck region. Although CNSNP has a high prevalence (Hogg-­ Johnson et al., 2009; Haldeman et al., 2010), little is known about the sensory deficit that underlies this condition. Identifying sensory deficits is relevant because their presence can result in impaired movement and in disruption of intracortical inhibition mechanisms (Elsig et al., 2014; Botnmark et al., 2016; Hillier et al., 2015; Riemann and Lephart, 2002; Harvie et al., 2016; Luomajoki and Moseley, 2011), which in turn can be responsible for greater recurrence and chronification of pain (Hall et al., 1995; Kristjansson and Treleaven, 2009; Harvie et al., 2016). Extensive evidence has shown TPD impairment in patients who experience neuropathy (Saeidian et al., 2011; Eryilmaz et al., 2013; Chiu et al., 2014; Nurmikko and Bowsher, 1990), leading to the hypothesis that tactile spatial acuity dysfunction is a product of a lesion in the pe­ ripheral nervous system (Dellon et al., 1974). In contrast, various studies have reported TPD impairment in conditions of chronic pain such as lower back pain (Ehrenbrusthoff et al., 2018; Adamczyk et al., 2018b; Catley et al., 2014b), suggesting that the main factor responsible for this dysfunction is the pain itself, regardless of its origin (Adamczyk et al., 2018c; Frahm et al., 2017). Our findings agree with the latter hypoth­ esis, because both CNSNP groups presented less TPD in the neck region. In accordance with our results, Harvie et al. (2018) reported differences between patients with chronic neck pain (75% of traumatic origin and 25% of nontraumatic origin) and asymptomatic subjects. In contrast, the scarce studies conducted with patients with CNSNP on the neck region 6

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Musculoskeletal Science and Practice 47 (2020) 102138

Falla, 2004; Falla et al., 2004; Wing Chiu et al., 2005), as can be deduced from the results of the craniocervical motor control test. Motor function impairment has been related to psychological/subjective factors (e.g., pain, fear of movement) (Amiri Arimi et al., 2018; Meisingset et al., 2015; De Pauw et al., 2018; Oddsdottir and Kristjansson, 2012). Our results are therefore not surprising, given that both symptomatic groups showed a higher degree of maladaptive psychological factors. However, in terms of the kinesthetic sense, only the patients with NF shown a greater JPE than the asymptomatic subjects, exceeding the critical threshold of 4.5� (Revel et al., 1991b) in all movements, which might be relevant at the clinical level (Angst et al., 2017). Nevertheless, it is worth noting that the JPE of the CNSNP with No-NF group approached 4.5� in all movements and even exceeded it in extension. These findings invite us to consider the hypothesis that there are shared mechanisms between JPE and tactile spatial acuity. At present, the authors cannot determine with certainty the presence of a dysfunction in the kinesthetic sense in patients with CNSNP. It is possible that the presence of pain with NF helps explain this uncertainty because pain with these characteristics is more intense and disabling, as can be observed in our results and in those of previous studies (L� opez-de-Uralde-Villanueva et al., 2016a; L� opez-de-Uralde-Villanueva et al., 2016b; Bouhassira et al., 2008; Sterling and Pedler, 2009). Ac­ cording to the literature, the level of disability could be the most determinant factor for the presence of an impairment in the kinesthetic sense in patients with chronic neck pain (Elsig et al., 2014; Treleaven et al., 2003a; Armstrong et al., 2008; Sterling et al., 2003b). Supporting this theory, Teng et al. (2007) observed no differences in the JPE be­ tween patients with CNSNP with a neck disability index less than 15 points and asymptomatic subjects, which reinforces our results because the CNSNP with No-NF group showed a mean neck disability index below this limit. Additionally, patients with moderate/severe disability due to pain after experiencing whiplash (considered a condition with NF) (Chien et al., 2008, 2009) have presented cervical extensor musculature atrophy (Elliott et al., 2011). This fact could explain the impairment in kinesthetic sense because the muscle spindles of the intrinsic neck muscles seem to be one of the most determinant stimuli for appropriate proprioception (Bolton, 1998; McLain, 1994; Kulkarni et al., 2001). Therefore, patients with NF have greater JPE perhaps due to atrophy of the intrinsic muscles, given that they report moderate-severe disability (Vernon, 2008). Nevertheless, that is just one hypothesis and should be evaluated using imaging tests in future studies. This study has a number of limitations. Firstly, given that this was a cross-sectional study, the results are descriptive and do not have a pre­ dictive character, nor can they be used to establish causal relationships. Secondly, the JPE assessment was performed using three measurements rather than six as recommended by a number of authors (Swait et al., 2007). Nevertheless, there are previous studies that have evaluated JPE with three measurements (Uthaikhup et al., 2012; Treleaven et al., 2003b; Sterling et al., 2003c). The authors therefore opted for this op­ tion so as to not excessively extend the assessment. It might have been interesting to monitor the sensor-motor control test using surface elec­ tromyography to accurately quantify the motor recruitment pattern, as well as evaluate the intrinsic neck muscles using ultrasonography. Lastly, the authors did not record postural variables because a sustained contraction of the posterior neck muscles due to a forward head position could affect the results of the tactile spatial acuity (Han et al., 2015) and sensory-motor control (Owens et al., 2006). Future studies are needed to rectify these limitations and to confirm the presence of cortical reorga­ nization in patients with CNSNP using neuroimaging techniques such as MRI.

the presence of NF, the patients with CNSNP showed reduced cranio­ cervical motor control and tactile spatial acuity in the painful region and in neuro-anatomically related areas. However, only the patients with NF had impaired tactile spatial acuity in areas remote to the pain and impaired cervical kinesthetic sense. Thus, our results could support a different pattern of somatosensory impairment within chronic neck pain, showing greater impairment in patients with NF compared to those without NF. Ethical statement The study protocol was approved by the local ethics committee of the Center for Advanced Studies University La Salle, Madrid, Spain, and the patient consent forms have been collected. Funding sources This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. Declaration of competing interest The authors certify that they have no affiliations with or financial involvement in any organization or entity with a direct financial interest in the subject matter or materials discussed in the article. Acknowledgments The authors thank the participants for volunteering their time and institutions that allowed them to use their dependences. They are also grateful for the strong support of Rosmy Villanueva-Rubio. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi. org/10.1016/j.msksp.2020.102138. References Adamczyk, W., Luedtke, K., Saulicz, E., 2018a. Lumbar tactile acuity in patients with low back pain and healthy controls: systematic review and meta-analysis. Clin. J. Pain 34, 82–94. https://doi.org/10.1097/AJP.0000000000000499. Adamczyk, W., Luedtke, K., Saulicz, E., 2018b. Lumbar tactile acuity in patients with low back pain and healthy controls: systematic review and meta-analysis. Clin. J. Pain 34, 82–94. https://doi.org/10.1097/AJP.0000000000000499. Adamczyk, W.M., Saulicz, O., Saulicz, E., Luedtke, K., 2018c. Tactile acuity (dys)function in acute nociceptive low back pain: a double-blind experiment. Pain 159, 427–436. https://doi.org/10.1097/j.pain.0000000000001110. Amiri Arimi, S., Ghamkhar, L., Kahlaee, A.H., 2018. The relevance of proprioception to chronic neck pain: a correlational analysis of flexor muscle size and endurance, clinical neck pain characteristics, and proprioception. Pain Med. 19, 2077–2088. https://doi.org/10.1093/pm/pnx331. Andrade Ortega, J.A., Delgado Martínez, A.D., Alm�ecija Ruiz, R., 2010. Validation of the Spanish version of the neck disability index. Spine 35, E114–E118. https://doi.org/ 10.1097/BRS.0b013e3181afea5d. Phila Pa 1976. Angst, F., Aeschlimann, A., Angst, J., 2017. The minimal clinically important difference raised the significance of outcome effects above the statistical level, with methodological implications for future studies. J. Clin. Epidemiol. 82, 128–136. https://doi.org/10.1016/j.jclinepi.2016.11.016. Armstrong, B., McNair, P., Taylor, D., 2008. Head and neck position sense. Sports Med. 38, 101–117. Bartsch, T., Goadsby, P.J., 2003. Increased responses in trigeminocervical nociceptive neurons to cervical input after stimulation of the dura mater. Brain 126, 1801–1813. https://doi.org/10.1093/brain/awg190. Bier, J.D., Scholten-Peeters, W.G., Staal, J.B., Pool, J., van Tulder, M.W., Beekman, E., Knoop, J., Meerhoff, G., Verhagen, A.P., 2018. Clinical practice guideline for physical therapy assessment and treatment in patients with nonspecific neck pain. Phys. Ther. 98, 162–171. https://doi.org/10.1093/ptj/pzx118. Bijur, P.E., Silver, W., Gallagher, E.J., 2001. Reliability of the visual analog scale for measurement of acute pain. Acad. Emerg. Med. 8, 1153–1157. Blanpied, P.R., Gross, A.R., Elliott, J.M., Devaney, L.L., Clewley, D., Walton, D.M., Sparks, C., Robertson, E.K., 2017. Neck pain: revision 2017. Clinical practice guidelines linked to the international classification of functioning, disability and health from the orthopaedic section of the American physical therapy association.

5. Conclusion The results of this study show that the patients with CNSNP with NF experience more intense/disabling pain and have a higher degree of maladaptive psychological factors than those without NF. Regardless of 7

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