Man Ther. 2015 (Dec); 20 (6): 736–744 ~ FULL TEXT
J. de Vries, B.K. Ischebeck, L.P. Voogt, J.N. van der Geest, M. Janssen, M.A. Frens, G.J. Kleinrensink
Department of Neuroscience,
Erasmus MC, P.O. Box 2040,
3000 CA Rotterdam,
Department of Physical Therapy,
Rotterdam University of Applied Sciences,
Rochussenstraat 198, 3015 EK Rotterdam,
BACKGROUND: Several studies in recent decades have examined the relationship between proprioceptive deficits and neck pain. However, there is no uniform conclusion on the relationship between the two. Clinically, proprioception is evaluated using the Joint Position Sense Error (JPSE), which reflects a person's ability to accurately return his head to a predefined target after a cervical movement.
OBJECTIVES: We focused to differentiate between JPSE in people with neck pain compared to healthy controls.
STUDY DESIGN: Systematic review according to the PRISMA guidelines.
METHOD: Our data sources were Embase, Medline OvidSP, Web of Science, Cochrane Central, CINAHL and Pubmed Publisher. To be included, studies had to compare JPSE of the neck (O) in people with neck pain (P) with JPSE of the neck in healthy controls (C).
RESULTS/FINDINGS: Fourteen studies were included. Four studies reported that participants with traumatic neck pain had a significantly higher JPSE than healthy controls. Of the eight studies involving people with non-traumatic neck pain, four reported significant differences between the groups. The JPSE did not vary between neck-pain groups.
CONCLUSIONS: Current literature shows the JPSE to be a relevant measure when it is used correctly. All studies which calculated the JPSE over at least six trials showed a significantly increased JPSE in the neck pain group. This strongly suggests that 'number of repetitions' is a major element in correctly performing the JPSE test.
KEYWORDS: Joint position error; Joint position sense; Neck pain; Proprioception
From the FULL TEXT Article
The primary measure to clinically operationalize cervical proprioception
is the Joint Position Sense Error (JPSE) (Armstrong et al.,
2008; Strimpakos, 2011). Joint position sense, an individual's ability
to reproduce and perceive previous predetermined positions or
ranges of motion of a joint, is amajor component of proprioception.
The error people make whilst reproducing the predefined position
is defined as the JPSE. Recently, several studies on the relation between
neck pain and JPSE have been published (Woodhouse and
Vasseljen, 2008; Cheng et al., 2010; Chen and Treleaven, 2013).
Cervical proprioception is the sense of position of the head or
neck in space, describing the complex interaction between afferent
and efferent receptors to monitor the position and movement
(Newcomer et al., 2000). In the cervical spine, this sense has its
neurological basis in muscle spindles (Proske and Gandevia, 2012)
and, to a lesser extent, in tendon organs (Golgi receptors)
(Hogervorst and Brand, 1998), cutaneous receptors, and joint receptors
(McCloskey, 1978; Grigg, 1994; Lephart et al., 1997; Proske
et al., 2000). The cervical muscles provide information to (Bolton
et al., 1998) and receive information from the central nervous
system (Kalaska, 1994; Hellstrom et al., 2005). Afferent information
from the cervical muscles converges in the vestibular nuclei, where
the head movement-related information from the visual and
vestibular system also converges (Corneil et al., 2002). Malmstrom
et al. (2009) showed that accurate head-on-trunk orientation can
be achieved without vestibular information. This suggests that
proprioceptive information of the cervical spine is important for
head-on-trunk orientation. The cervical JPSE is assessed by testing
the ability of a blindfolded participant to accurately relocate their
head to the trunk relative to a predefined target (often the neutral
position of the head) after a cervical movement. Other examples of
joint regions in which JPSE has been used for testing proprioception
are the shoulder (Anderson and Wee, 2011), the knee (van der Esch
et al., 2013), and the ankle (Nakasa et al., 2008).
People with neck pain originating from trauma and people
whose neck pain has developed more gradually both seem to have a
higher JPSE than people without neck pain (Feipel et al., 2006;
Cheng et al., 2010). This implies that an increase in JPSE may not
be caused solely by soft tissue damage or neurological impairments
following trauma (Revel et al., 1991; Sterling et al., 2003).
Narrative reviews of the literature on cervical JPSE have been
published (Armstrong et al., 2008, Strimpakos, 2011). Both reviews
give conflicting conclusions concerning the presence of a higher
JPSE in people with neck pain. The present study is a comprehensive,
systematic overview according the PRISMA guidelines of the
literature. It presents the data of the JPSE of the cervical spine
caused by neck pain of traumatic and non-traumatic origin in
comparison of the JPSE in healthy controls.
The PRISMA guidelines (Preferred Reporting Items for Systematic
Reviews and Meta-Analyses) (Moher et al., 2009) were used in
this systematic literature review to report the method of literature
search, appraisal, and presentation of evidence.
To be included in this systematic review, studies had to report
on joint position sense error of the neck (O); and, include participants
with neck pain (P), compared to healthy controls (C). It is
important to compare the JPSE of people with neck pain with the
JPSE of healthy controls because it is assumed that a higher JPSE test
reflects aberrant afferent input from the neck (Revel et al., 1991;
Heikkila and Wenngren, 1998; Treleaven et al., 2003; Malmstrom
et al., 2009). Therefor a reference score form healthy controls is a
Information sources and search parameters
In order to be as comprehensive as possible, the following databases
were searched on December 17th 2014:Embase, Medline
OvidSP, Web of Science, Cochrane Central, CINAHL and Pubmed
Publisher. Keywords were derived from the research question and
transformed to associated “Emtree” terms and free-text words. For
Embase, the following Emtree terms were used: sensorimotor
integration, sensorimotor function, somatosensory system, somatosensory
cortex, balance impairment, motor control,
proprioception, body equilibrium, eye movement, proprioceptive
feedback, cornea reflex, neck pain, and whiplash injury.
The free-text words were as follows: deep sensitivity, kinesthe*,
propriorecep*, propriocep*, kinesio NEXT/1 percept*, cornea*, eye*
OR ocular OR cervicoocul* NEAR/3 reflex*, movement*,body, musculoskelet*,
postural, NEAR/3 balanc*, equilibr*, sway, control, joint
position, head position, neck position, NEAR/3 error*, sense*,
reproduc*, abilit*, inaccura*, accura*, replicat*, head NEAR/3
steadiness, balance NEAR/3 impair*, difficult*, neck, cervic* NEAR/6
pain*, hyperextension*, ache, neckache*, Cervicalgia*, Cervicodynia*,
whiplash. In addition, Medline, OvidSP, Web of Science,
Cochrane Central, CINAHL and Pubmed Publisher were similarly
searched with their own thesaurus used for indexing studies and
free entries, in order to be as comprehensive as possible.
In order to be included, studies had to meet the following
(1) Participants in the study had to be over 18 years old;
(2) Participants had to suffer from neck pain;
(3) The outcome measures in the study had to be the JPSE;
(4) Control subjects had to be healthy individuals; and
(5) The study had to be written in English.
Initially, the search results were screened based on title and abstract.
The studies that fulfilled all inclusion criteria were evaluated
in full-text, and included in the systematic review.
Data items and collection
Information was extracted from the included studies and presented
in three evidence tables (Tables 1–3). This information is
presented in the evidence table regarding
(2) sample size,
(3) characteristics of the participants,
(4) JPSE testing instrument,
(5) JPSE testing protocol, and
Data extraction was executed by author JV and checked by author LV.
Risk of bias in individual studies
The validity and risk of bias of the remaining studies was
checked by using the “Methodology Checklist 4: Case-control
studies” version 2.0, provided by the Scottish Intercollegiate
Guidelines Network (SIGN) (www.sign.ac.uk). The SIGN-group develops
evidence-based clinical practice guidelines in order to
translate new knowledge into clinical action. One aspect of the
work of this group is the development of critical appraisal checklists.
Studies were scored on a clearly focused research question, on
the description of the internal validity: i.e. the selection of subjects;
exclusion of selection bias; clear definition of outcomes; blinding of
assessors; reliable assessment of exposure; identification of potential
confounders; and provision of confidence intervals. For the
studies, the grading score has been set from “Low quality” (0), to
“Acceptable” (+), to “High quality” (++). In the present review, only
studies graded as “Acceptable” (+) or “High quality” (++) were
included. This criterion was set a priori.
Methodological quality of the included studies was assessed
blindly and independently by authors JV and LV. After both researchers
had appraised the selected studies, results were
compared and any differences discussed after screening the studies
a second time. In the event of disagreement a third opinion was
provided by author GK.
The principal outcome measure of this review was the JPSE,
which was the main issue to be researched in the included studies.
In 9 of the 14 included studies, JPSE was defined as “the ability to
reposition the head to the starting position after a maximal active
movement of the head in a vertical or horizontal plane with
occluded vision” (Revel et al., 1991; Treleaven et al., 2003; Sterling
et al., 2003; Armstrong et al., 2005; Feipel et al., 2006; Sjolander
et al., 2008; Woodhouse and Vasseljen, 2008; Cheng et al., 2010;
Uthaikhup et al., 2012; Chen and Treleaven, 2013). The outcome
measure was given in degrees or centimeters.
A total of 1163 studies were identified. As shown in Figure 1, 14
studies remained after two screening phases.
The characteristics of the data that were extracted from the
included studies (study, sample size, characteristics of the participants,
JPSE testing instrument, JPSE testing protocol, and results)
are presented in Tables 1–3. In nine out of 14 included studies JPSE
was assessed in participants with traumatic neck pain (Heikkila and
Wenngren, 1998; Kristjansson et al., 2003; Sterling et al., 2003;
Treleaven et al., 2003; Armstrong et al., 2005; Feipel et al., 2006;
Grip et al., 2007; Sjolander et al., 2008; Woodhouse and
Vasseljen, 2008). Seven of those nine studies used the classification
of the Quebec Task Force on Whiplash-Associated Disorders
(WAD) (Spitzer et al., 1995; Rydevik et al., 2008). In this classification
system, WAD grade 1 corresponds to complaints of neck pain,
stiffness or tenderness only without physical signs that are noted
by an examining physician; WAD grade 2 corresponds to complaints
of neck pain and musculoskeletal signs, such as a decreased
range of motion and point tenderness in the neck; and WAD grade 3
includes additional signs (decreased or absent deep tendon reflexes,
weakness, and sensory deficits). Of these nine studies, four
also included a group of people with non-traumatic neck pain
(Kristjansson et al., 2003; Grip et al., 2007; Sjolander et al., 2008;
Woodhouse and Vasseljen, 2008). The studies that reported both
on participants with traumatic and with non-traumatic neck pain
are presented in Tables 1 and 2 Another study, described in Table 3,
had a combined group consisting of both participants with traumatic
and idiopathic neck pain (Chen and Treleaven, 2013).
Risk of bias
Thirty-six of the included studies remained after the first
screening. These 36 studies fulfilled all of the inclusion criteria,
based on title and abstract. After the first full-text reading, two
researchers agreed on twelve studies. On two studies, the researchers
disagreed regarding the validity of the measurement
protocol. Another studywas subject of discussion with regard to the
outcome measure. After a second reading and comparison of the
differences, the researchers reached consensus for the three
studies. Both conflicting studies regarding the validity of the
measurement protocol were included. The study thatwas subject of
discussion with regard to the outcome measure was excluded,
resulting in 14 included studies.
Methodological quality of all of the included studies was
“acceptable” (+) according to the SIGN criteria checklist. This implies
some weaknesses in the study, with an associated risk of bias.
Most of the studies lost points on “sample size” or “not blinding the
The included studies in this review used JPSE as an outcome
measure to reflect proprioception of the cervical spine. The JPSE
was described in angular units (degrees) or centimeters to measure
As shown in Table 1, four studies (Heikkila and Wenngren, 1998;
Kristjansson et al., 2003; Sterling et al., 2003; Treleaven et al., 2003)
reported that participants with traumatic neck pain had a significantly
higher JPSE than healthy controls. Of these four studies,
Sterling et al. (2003) reported a significant difference compared to
healthy controls on rotation to the right. Rotation to the left and
extension were not significantly different from the healthy controls.
In the studies of Kristjansson et al. (2003) (rotation), and Heikkila
and Wenngren (1998) (rotation and flexion-extension), all the
investigated directions of movement regarding the JPSE were
significantly higher in participants with traumatic neck pain. In the
study of Treleaven et al. (2003), JPSE in all the investigated directions
of movement (right rotation, left rotation, and extension) was
significantly higher compared to healthy controls, but only after
results from the two different neck pain groups were pooled. Five
studies that included participants with neck-pain of a traumatic
origin did not show a significantly altered JPSE compared to healthy
controls (Armstrong et al., 2005; Feipel et al., 2006; Grip et al., 2007;
Sjolander et al., 2008; Woodhouse and Vasseljen, 2008).
Non-traumatic neck pain
Eight studies were included, involving participants with nontraumatic
neck pain (Revel et al., 1991; Rix and Bagust, 2001;
Kristjansson et al., 2003; Grip et al., 2007; Sjolander et al., 2008;
Woodhouse and Vasseljen, 2008; Cheng et al., 2010; Uthaikhup
et al., 2012) as can be seen in Table 2. Of these eight studies, four
(Revel et al., 1991; Rix and Bagust, 2001; Kristjansson et al., 2003;
Cheng et al., 2010) reported a significantly higher JPSE in people
with non-traumatic neck pain than in controls. Joint position sense
error in the investigated directions of movement was significantly
higher in the studies of Kristjansson et al. (2003) (rotation), Revel
et al. (1991) (rotation and flexion-extension) and Cheng et al.
(2010) (flexion and extension). For the study of Rix and Bagust
(2001), this was not the case. In this study only, the flexion
movement was significantly higher than in healthy controls. With
respect to right rotation, left rotation and extension, JPSE in participants
with neck pain was not significantly different. The studies
of Woodhouse and Vasseljen (2008), Sjolander et al. (2008), Grip
et al. (2007), and Uthaikhup et al. (2012), did not report any significant
differences in JPSE between participants with nontraumatic
neck pain and healthy controls.
Combined group consisting of traumatic and non-traumatic neck pains
As shown in Table 3, Chen and Treleaven (2013) included participants
with chronic neck pain with either a traumatic or idiopathic
origin. This study used a laser pointer as well as the
“Fastrak™” instrument to measure the JPSE. The authors also used
two different measurement protocols for measuring the JPSE. In the
conventional protocol, participants were asked to actively rotate
their heads (left or right) as far as was comfortable, and then had to
return to the starting position as accurately as possible. In the
alternative protocol, participants had to actively rotate the trunk
(instead of the head) and return to the starting position. The chest
sensor and the chest laser were used to obtain data on trunk
rotation error. As can be seen in Table 3, for the conventional
measurement protocol only the pooled JPSE (left/right rotation)
significantly differed between participants with neck pain and
controls when measured with the laser pointer. The JPSE measured
with the “Fastrak™” did not show any significant differences when
measured with the conventional protocol.
For the trunk-to-head measurement protocol, left rotation and
the pooled left/right rotation significantly differed from the healthy
controls. This held for the laser pointer measurement instrument as
well as for the “Fastrak™” measurement instrument. Rotation to
the right was not significantly altered, regardless of measurement
instrument or protocol.
The main goal of this systematic review was to differentiate
between JPSE of the cervical spine in participants with neck pain of
a traumatic or a non-traumatic origin, compared to healthy controls.
The results of this review suggest that when the JPSE is
measured over 6 trials or more, the JPSE is generally higher in the
neck pain group than in the control group.
Various factors might influence the outcome of the JPSE measurement.
The first is the influence of the vestibular system. As the
peripheral and central vestibular systems provide and integrate
information essential for establishing the position of the head in
space, they indirectly influence the head-to-body position sense.
Deficits in any of the vestibular mediated pathways may thus affect
JPSE (Treleaven, 2008; Chen and Treleaven, 2013). However,
Pinsault et al. (2008) and Malmstrom et al. (2009) did not find an
increased JPSE in people with vestibular loss when compared to
healthy controls. Because the vestibulum is particularly sensitive to
fast, jerky head movements (Day and Fitzpatrick, 2005), the velocity
of head motion during measurement of the JPSE is important.
When participants move their heads faster than 2.1/s, cervical
input decreases and vestibular input increases (Kelders et al., 2003).
Thus, the faster the head moves, the more JPSE represents vestibular
afferention rather than cervical afferention. It is not clear
whether all the included studies tried to rule out as much afferention
from the vestibulum as possible, by having the subjects
move slowly. A study by Chen and Treleaven (2013) showed
interestingly that trunk-to-head rotation, excluding input of the
vestibulum, gave different results compared to the conventional
measurement protocol of head-to-trunk rotation. However, as the
differences were small, this measurement protocol should be
examined further to see whether possible vestibular input plays a
role in the conventional measurement protocol.
A second factor that may affect the conclusion is the anatomy of
the cervical spine. Large quantities of muscle spindles in the cervical
spine muscles provide (Bolton et al., 1998) and receive information
from the central nervous system (Kalaska, 1994; Hellstrom
et al., 2005). In the cervical spine, the information from muscles
(muscle afferention) is a dominant source of information
(Hogervorst and Brand, 1998; Proske and Gandevia, 2012). A study
using Magnetic Resonance Imaging has shown a widespread
presence of fatty infiltrates in the neck muscles of people with
persisting moderate to severe levels of pain following a whiplash
injury (Elliott et al., 2011). This implies that the intensity of the
perceived pain may influence proprioception. For the traumatic
group, the duration of complaints or severity of the WAD did not
seem to influence JPSE significantly. In the non-traumatic group,
therewas no correlation between the duration of the neck pain and
an altered JPSE. Likewise, the intensity of perceived pain, whichwas
described in all studies, did not seem to influence the JPSE. In some
of the included studies, relatively low perceived pain levels were
correlated with significantly altered JPSE, and vice versa.
A third factor is the variety of measurement devices used. Some
researchers used a laser pointer, where others used either the
electromagnetic tracking system 3 Space “Fastrak™” (Polhemus
Inc, USA), a ProReflex System (Qualisys Medical AB, Gothenburg,
Sweden), or different types of electrogoniometers. This made it
difficult to compare the various study results. The 3 Space “Fastrak
™” was the most commonly used instrument, employed in
eight out of fourteen studies (Kristjansson et al., 2003; Sterling
et al., 2003; Treleaven et al., 2003; Armstrong et al., 2005;
Sjolander et al., 2008; Woodhouse and Vasseljen, 2008;
Uthaikhup et al., 2012; Chen and Treleaven, 2013). The “Fastrak
™” system is an electromagnetic measuring instrument that
tracks the positions of sensors relative to a source in three dimensions.
Previously Jordan et al. (2000). demonstrated that it is a
reliable and valid measurement system with an accuracy of up to
±0.2. The nine studies using it produced contrasting results
regarding the JPSE in people with neck pain.
The sensor placement is another possible source of measurement
bias. Not all studies used the same placement, or described
the placement of the sensors precisely. This inconsistency could
have consequences for the validity of the measurements and the
ability to compare the different study results.
The laser method, which is also commonly used to assess the
JPSE (four out of fourteen studies), has a good test-retest reliability
and a strong correlation with an ultrasound technique for
measuring JPSE (Roren et al., 2009). It is remarkable that all four
studies (Revel et al., 1991; Heikkila and Wenngren, 1998; Rix and
Bagust, 2001; Chen and Treleaven, 2013) using a laser pointer
showed significantly higher cervical joint reposition errors in
people with neck pain than in controls. However, in none of these
four studies were the examiners blinded for “controls” or “participants
with neck-pain”. The results in these studies may, therefore,
have been influenced by expectation bias. Revel et al. (1991)
compared the inter-observer reliability of the laser pointer instrument
in 11 controls. This test showed no significant difference
between the examiners.
The application of various testing protocols and data-analysis
software is a fourth possible factor influencing the conclusion.
Swait et al. (2007) reported that at least six trials were needed to
optimize the stability and reliability of the cervical JPSE measurement.
Nonetheless, in only four of the fourteen studies did
the researchers use six or more trials to calculate the mean JPSE.
All four studies (Revel et al., 1991; Heikkila and Wenngren, 1998;
Rix and Bagust, 2001; Chen and Treleaven, 2013), in which the
mean JPSE was calculated over six or more trials, showed
significantly higher joint position errors in people with neck pain
than in controls. These studies used a laser pointer as a JPSE
testing device. An explanation for this could lie in the applied
statistics. It might be that the vulnerability to outliers is less
when the mean JPSE is calculated over more trials hereby
reducing the standard error of the mean. This stresses the
importance of calculating the joint position error over at least six
trials. Further research needs to be performed on the effect on
learning curves in the presence of pain and/or after (traumatic)
damage to the joints of the cervical spine.
The studies with an electronic testing device used custom-made
analysis software (Kristjansson et al., 2003; Sterling et al., 2003;
Treleaven et al., 2003; Armstrong et al., 2005; Feipel et al., 2006;
Sjolander et al., 2008; Woodhouse and Vasseljen, 2008;
Uthaikhup et al., 2012; Chen and Treleaven, 2013). As only a general
description of the algorithms of this software was given, the
reproducibility of these experiments are low. Absence of the presentation
of raw data in most studies is in line with the previous
point. Only when both the data-analysis protocol and the (raw)
data are presented, readers can interpret results and conclusions of
the studies. Another threat to the validity and reliability of the
included studies is the small number of participants that some of
them included (Rix and Bagust, 2001; Sjolander et al., 2008; Cheng
et al., 2010). However, studies which have included a relative high
number of participants do not show other or more robust results
than the studies with a smaller amount of participants.
In general, data cannot be compared without harmonization of
testing protocols and data analysis systems. Therefore, it was not
possible to conduct a meta-analysis of the included studies. This
pooling of data would help to resolve the problem of the small
number of participants included in some of the studies. Besides
improving the current study designs, it is also important to correlate
JPSE with other specific variables (i.e. age, gender, location of
perceived pain, anxiety levels, perceived disability, and cervical
range of motion).
In general, the results of the included studies give an equivocal
answer to the question of whether the JPSE is higher in people with
cervical spine lesions caused by trauma and/or non-traumatic neck
complaints than in controls. The JPSE is overall higher in the neck
pain group when measured over at least 6 trials.
The authors wish to thank Wichor Bramer, biomedical information
specialist at Erasmus MC, for the support with the literature
search and David Alexander for the language editing.We are
grateful for the financial support of TC2N (EU Interreg; MF & JG),
and Stichting Coolsingel (MF). The authors have no conflict of interest
relevant to the content of this systematic review.
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