Cervical End-Range Joint Motion Does Not Indicate Maximum Cervical Joint Motion In Healthy Adults. An Observational Study


 BackgroundIn clinical diagnosis, the largest motion associated with cervical range of motion is thought to be found at end-range and it is this perception that forms the basis for the interpretation of flexion/extension studies. There have however, been representative cases of joints producing their maximum motion before end-range, but this phenomenon is yet to be quantified. PurposeTo provide a quantitative assessment of the difference between maximum motion and end-range in healthy subjects. Secondarily to classify joints into type based on their motion and to assess the proportions of these joint types. Study designThis is an observational study. Subject sampleThirty three healthy subjects participated in the study. Outcome measuresMaximum motion, end-range motion and surplus motion in degrees were extracted from each cervical joint. MethodsThirty-three subjects performed one flexion and one extension motion excursion under video fluoroscopy. The motion excursions were divided into 10 percent epochs between the initial upright position and the end-range position, from which maximum motion, end-range and surplus motion were extracted. Surplus motion was then assessed in quartiles and joints were classified into type according to end-range. ResultsFor flexion 48.9% and for extension 47.2% of joints produced maximum motion before end-range (type Surplus). For flexion 45.9% and for extension 46.8% of joints produced maximum motion at end-range (type Classic) and 5.2% of joints in flexion and 6.1% of joints in extension concluded their motion anti-directionally (type Anti-directional). Mann-Whitney U tests produced significant results for C2/C3, C3/C4 and C4/C5 in flexion and C1/C2, C3/C4 and C6/C7 in extension when comparing end- range motion for type Classic and type Surplus. The average contributions to cervical range-of-motion (ROM) (C0 to C7) for flexion and extension were 60.23֯ and 67.86֯ for type Classic and 42.22֯ and 49.05֯ for type Surplus respectively. Thus, the average contribution to cervical ROM was larger for type Classic than for type Surplus. The average pro-directional surplus motion was 2.41֯ ± 2.12֯ with a range of range (0.07֯ -14.23֯) for flexion and 2.02֯ ± 1.70֯ with a range of 0.04°-6.97° for extension.ConclusionThis is the first study to categorise joints by type of motion. Type Surplus constituted approximately half of the joints analysed in this study. Therefore, end-range motion cannot be assumed to be a demonstration of a joint´s maximum motion.


Abstract Background
In clinical diagnosis, the largest motion associated with cervical range of motion is thought to be found at end-range and it is this perception that forms the basis for the interpretation of exion/extension studies.
There have however, been representative cases of joints producing their maximum motion before endrange, but this phenomenon is yet to be quanti ed.

Purpose
To provide a quantitative assessment of the difference between maximum motion and end-range in healthy subjects. Secondarily to classify joints into type based on their motion and to assess the proportions of these joint types.

Study design
This is an observational study.

Subject sample
Thirty three healthy subjects participated in the study.

Outcome measures
Maximum motion, end-range motion and surplus motion in degrees were extracted from each cervical joint.

Methods
Thirty-three subjects performed one exion and one extension motion excursion under video uoroscopy.
The motion excursions were divided into 10 percent epochs between the initial upright position and the end-range position, from which maximum motion, end-range and surplus motion were extracted. Surplus motion was then assessed in quartiles and joints were classi ed into type according to end-range.

Results
For exion 48.9% and for extension 47.2% of joints produced maximum motion before end-range (type Surplus). For exion 45.9% and for extension 46.8% of joints produced maximum motion at end-range (type Classic) and 5.2% of joints in exion and 6.1% of joints in extension concluded their motion antidirectionally (type Anti-directional).

Introduction
Neck range of motion (ROM) is a traditional method employed for the assessment of neck motion (1)(2)(3)(4)(5) in both clinical (6,7) and scienti c environments. Neck range-of-motion (ROM) is frequently assessed as a change of head position from the forward facing upright head position to a new position after movement of the neck. The neck ROM is assessed between the head and a lower anatomical point, commonly the chin and sternal notch (8). The neck ROM can further be divided into the motions of joints between two cervical vertebrae. Although there are multiple intervertebral joints between two cervical vertebrae, the multi-joint complex will henceforward be referred to as a joint.
The largest cervical joint motion associated with neck ROM in clinical diagnosis is perceived to be found at the end of the neck movement (9,10). This perception is used in the interpretation of exion and extension X-rays to measure the maximum joint motion. However, neck ROM contains little information about motion between the measuring points, as the measurements are taken from static positions. Studies have demonstrated representative cases where the maximum joint motion is greater than the motion found at end-range (11)(12)(13)(14)(15). Thus, in these cases the joint position at end-range could not represent the maximum joint motion. Similar concepts of maximum motion have been documented as repeatable. Breen et al demonstrated substantial to excellent reliability of repeated measurements of intervertebral range of angular joint motion in low back joint motion analysis, measured under video uoroscopy (16). Consequently, it can be theorised that repeated measurements of intervertebral range of motion in the cervical spine are similarly reliable.
New studies document multiple sources of joint motion variability, demonstrating that cervical joint motion cannot be perceived to be curvilinear or uniform (11)(12)(13)17). Cervical joints in the upright posture do not return to a precise upright joint position after neck motion. With two repeated joint motion excursions of the cervical spine, joints return to the upright intervertebral joint positon with an average joint reposition error of 2 degrees (18). Additionally, the direction of joint motion alternates between prodirectional joint motion (movement in the direction of neck motion) and anti-directional joint motion (movement in the opposite direction to that of neck motion) during neck motion (12). The time periods and motion contributions in degrees of anti-directional motion can be small or large. Anti-directional joint motion is frequent during neck exion and extension. For C0-C7 ROM anti-directional motion is approximately 40% of the pro-directional motion and approximately 70% of the resultant motion (12). The study suggested that the smaller intermittent anti-directional motions were for motor control purposes, while the larger anti-directional motions were a natural part of a healthy joint motion pattern (12). These results suggest that healthy cervical joints can move further than the motion found at end-range, and that this additional surplus motion is common during joint motion and may be necessary for normal healthy cervical joint motion.
Studies of pain effects on joint motion have documented that experimental neck pain and recurrent neck pain alter the amount of anti-directional motion between the upright neck position and end-range position (19)(20)(21). Thus, pain may increase anti-directional motion in one of two ways, either by increasing the amount of anti-directional motion per joint or by increasing the number of joints with anti-directional motion. Additionally, the pattern of joint motion may also be altered.
Studies of cervical joint motion have previously demonstrated cervical joints with greater joint motion before end-range than at end-range (5,11). The surplus joint motion has been classi ed as compensatory, paradoxical or para-physiologic motion (14,(22)(23)(24). Intuitively, a joint's ability to perform surplus motion would be necessary for simultaneous motion in multiple planes, as multiplane motion would be di cult if joint structures were fully stretched by motion in just one plane.
Assessment of maximal cervical joint motion in previous studies appears to be based on the assumption that cervical joints cannot move further than end-range and that joint motions are linear and continuous (9,10). This assumption is not supported by recent studies (11-13, 15, 25). The aims of this study were rstly, to describe the maximum pro-directional and anti-directional joint motion in 10% epochs between the initial upright position and the end-range position, exploring the relationship between maximum motion and end-range motion. Secondly, to analyse the maximum surplus joint motion in quartiles, and to suggest possible subdivisions of joint motion and joint classi cation based on type of motion. This study proposes a joint classi cation of single cervical joint motion types based on end range (terminal position) and the maximum joint motion.

Methods And Materials
De nitions of concepts: Anti-directional surplus motion refers to surplus motion in opposition to the primary motion direction. This motion occurs beyond the upright position.
End-range refers in this study to the end or terminal position of a motion.
Epoch: An epoch is de ned as a time period representative of 10% of the total time required to complete a exion or extension motion.
Maximum motion refers to the maximum motion in degrees measured during a video uoroscopy motion excursion. Maximum motion can also refer to the maximum motion capacity of an individual joint.
Motion excursion: A motion task performed from point A-to point B. In the case of this study, from upright to end range exion or end-range extension.
Motion type refers to a classi cation of a single joint's motion during neck motion. We have de ned 3 types of motion, and all are de ned according to their end-range.
1) Classic, where the maximum motion < terminal position.
2) Surplus, this type is classi ed using pro-directional surplus motion, where maximum motion is > terminal position.
3) Anti-directional where the terminal position < the start position. In this study, the start position is upright and the terminal position is end-range. All types of joint motion include anti-directional motion, this motion is found within the joint motion used for classi cation.
When referring to a type of motion by name, a capital letter is used, as in type Surplus. However, the occurrence of surplus motion, is written in the lower case.
Pro-directional surplus motion refers to surplus motion found beyond end-range.
Range of motion refers to the angular motion in degrees between the start position of the motion to the end position of the motion (end-range) -range of motion can be of an individual joint or of the neck and can be measured from static or video images.
Surplus motion refers to motion, that occurs outside the boundaries of upright (start position) and endrange. Surplus motion is the difference, in degrees, between the upright start position or the end-range position and the maximum motion for a single joint. Surplus motion can be pro-directional or antidirectional and a single joint can produce surplus motion in both directions.
Upright refers in this study to the upright start position of neck motions.

Subjects
There were thirty-three participants in the study, of which twelve were female. Due to the increased risk of cancer posed to healthy subjects by exposure to ionizing radiation, data was extracted and re-analysed from a previous study investigating the repeatability of cervical joint motion (26). The demographics for the subjects can be found in Table 1. Subjects were aged between 20 and 37 and were recruited from campus and via social media, and in accordance with the following exclusion criteria: possible pregnancy, in ammatory or neurological disorders, cervical trauma, or neck pain in the last three months. Subjects were paid 22 $ an hour.
Two motion directions were analysed ( exion and extension) for 7 cervical joints in 33 subjects. The motion was analysed in 10% time epochs of total cervical motion. All participants signed informed consent forms prior to participating in the study. The study was conducted in accordance with the Helsinki declaration and ethical approval was given by the regional ethics committee (N20140004).

Motion analysis
Total joint motion and total neck range of motion were obtained by calculating the sum of the motion across the 10% epochs. Maximum motion, surplus motion and end-range were extracted for each joint. The average, standard deviation and range were subsequently calculated for individual joints and across joints.
Joints were subdivided into three types according to their end-range motion: Type classic (C) end-range motion = maximum motion; type Surplus (S) end-range motion < maximum motion and type Antidirectional (A) joints with anti-directional end-range motion. Two-hundred and thirty-one joints were included in the data set, each joint performed one exion motion and one extension motion. The initial analysis was of all joints. The secondary stage excluded joints with anti-directional end-range in order to focus on pro-directional surplus motion. Tertiary stage analysis assessed surplus motion in quartiles of the associated end-range joint motions, with the smallest endranges in the rst quartile and the largest in the fourth. The surplus motion (marked with green in Fig. 2) was expressed in degrees and percentages of end-range motion (marked with red in Fig. 2). The motion and percentages of pro-directional surplus motion were rst averaged across quartiles and then averaged across joints. The quartile data was further divided into upper cervical joints (C0 and C3) and lower cervical joints (C3 and C7), because preliminary data analysis indicated that the different anatomy of the upper and lower cervical joints would in uence the results.
Statistical tests were applied to compare the end-ranges of type Classic and type Surplus. Type Classic are illustrated in purple in Fig. 2.
The nal stage re-introduced type Anti-directional (marked with blue in Fig. 2) and looked at the frequency and contribution to motion for each of the three joint types.

Experimental procedures
Both the reproducibility of image analysis and the experimental procedures have been previously published (27). Prior to the uoroscopic procedure subjects were instructed to practice the exion and extension motion excursions. One complete excursion was to be performed with a smooth and even tempo and to be completed at 16 seconds, with 2 seconds at the upright and 2 seconds at end-range positions. The subjects were instructed to follow with their eyes a line marked on the oor, wall and ceiling in order to reduce out of plane motion. Custom glasses were worn, the attached external markers provided better visual tracking of occiput. The motion excursions were performed while sitting with knees, hips, ankles and elbows at 90° (12,18).

Fluoroscopic recordings
The source-to-subject difference was 76 cm, and was measured prior to exposure. The uoroscope produces 45 KV, 208 mA, 6.0 ms X-ray pulses at 25 frames per second (Philips BV Libra, 2006, Netherland). The estimated average radiation exposure from the two uoroscopic videos was 0.24 mSv (PCXMC software, STUK, Helsinki, Finland).

Image analysis
Manual image analysis was performed using a MATLAB-based program (27). Twenty-two osseous points were marked in accordance with a previously validated and published procedure (10,12,18,27). The MATLAB program calculated joint rotation in degrees using the vertebral midplane with respect to the horizontal plane, calculating the joint midline position from two neighboring mid-planes (10,12,13,18,27). Positive degrees indicate joint motion in extension and negative degrees indicate joint motion in exion; either motion direction could be anti-directional with respect to the pro-directional neck motion.

Statistical analysis
Data was normality tested with Shapiro-Wilk and Kolmogorov-Smirnov test in SPSS (IBM Statistics 26).
Comparisons of joint motion were performed with independent sample t-tests and Mann Whitney U tests. Signi cance was accepted at p<0.05. Minimum sample size for statistical tests was set at n = 7. Data was presented as mean ± SD and in percentages.

Results
Approximately 6% of all joints produced anti-directional end range motion, terminating their motion in opposition to the direction of head motion.
The average contributions to cervical ROM (C0 to C7) for exion and extension were 60.23 and 67.86 for type Classic and 42.22 and 49.05 for type Surplus respectively. Thus, the average contribution to cervical ROM was larger for type Classic than for type Surplus.
Mann-Whitney U tests were performed in order to compare the pro-directional end-range motion of type Classic and type Surplus. Statistical analysis was performed on eleven joints after the exclusion of joint sample sizes of less than seven. Three joints were excluded due to a low sample size (for exion C1/C2 and C6/C7 and for extension C0C1).
For type Surplus the average pro-directional surplus joint motion was 2.41 ± 2. Quartiles of surplus exion motion.
The pro-directional surplus exion motion was divided into quartiles of the associated end-range motion.
Flexion motion surplus to end-range was demonstrated by 113 joints.
The quartile with the smallest end-ranges had an average pro-directional surplus motion of 2.79 and 152.0% of the associated end-range motion. The quartile with the largest end-ranges had an average prodirectional surplus motion of 1.94 and 24.3% of the averaged associated end-range motion. Table 4 shows pro-directional surplus joint motion for exion and extension divided into upper and lower cervical joints. Percentages of average pro-directional surplus motion ranged from 21.2% to 359.4% in the upper cervical quartiles and from 0.8% to 94.0% in the lower cervical quartiles. In exion, the upper cervical quartiles ranged from 1.18 to 4.36 and from 0.12 to 5.46 in the lower cervical quartiles. Average surplus motion as a percentage of end-range motion decreased with an increase in end-range motion. However, there was no clear pattern of data distribution for surplus motion in degrees.
Of the 231 joints included in the study for extension motion, 108 joints (46.8%) were type Classic, 109 joints (47.2%) were type Surplus and 14 joints (6.1%) were type Anti-directional. The average prodirectional surplus extension motion was 2.02 ± 1.7 0 with a range of 0.04 -6.9 7.
As with exion the pro-directional surplus motion in the upper cervical region 2.84 ± 1.9 1 range (0.0 5-6.9 7) was numerically larger than the pro-directional surplus motion in the lower cervical region 1.4 2 ± 1.2 7 range (0.04 -4.7 5). The pro-directional surplus extension motion is presented in table 3.

Quartiles of surplus extension motion.
The pro-directional surplus extension motion was divided into quartiles of the associated end-range motion. The quartile with the smallest end-ranges demonstrated an average pro-directional surplus motion of 2.21 , which was 87.5% of the associated end-range motion. The quartile with the largest endrange motion demonstrated an average pro-directional surplus motion of 1.43 , which was 10.3% of the associated end-range motion. The quartile percentage range across the upper cervical joints was 8.6% to 232.3% and across the lower cervical joints was 2.2% to 137.5% (Table 4).
Surplus extension motion for the upper cervical joints ranged between 0.96 and 4.53 , the range for the lower cervical joints was between 0.33 and 3.20 . Average surplus motion, both in degrees, and as a percentage of end range-motion decreased as end-ranges increased.
Anti-directional end-range motion.
Anti-directional end-range motion was demonstrated by 5.2% of cervical joints during exion motion and 6.1% of cervical joints during extension motion. Of those joints, 0.9% during exion and 2.2% during extension moved anti-directionally from the outset and never passed upright pro-directionally.
For exion, the average anti-directional motion was 2.33 ± 2.5 3 with a range of 0.03 to 18.50 . For extension, the average anti-directional motion was 2.24 ± 1.7 1 with a range of 0.09 to 8.73 . Antidirectional end-range motion was found predominantly in the upper cervical region, suggesting that the anatomical structure of the vertebrae may in uence the prevalence of this motion (Table 6).
Each subject performed one exion and one extension motion excursion; 14 joints were assessed in each subject, seven in exion and seven in extension. On average 1 out of every 18 joints produced antidirectional end-range. Average joint motion.
The average joint motion from upright to end-range for all 33 subjects before and after exclusion of type Anti-directional joints is presented in Fig. 3. No type Anti-directional joints were found at the C4/C5 and C5/C6 level. However, type Anti-directional motion excursions were found at the remaining cervical joint levels. This is re ected in the average joint motion presented in Fig. 3. The gure illustrates the difference between end-range and maximum motion of type Surplus across joints. Interestingly the average endrange joint motion of type Classic is larger than the average end-range joint motion of type Surplus for all joints.
A further point of interest was the small average exion motion of C0/C1 shown in Fig. 3. The upper cervical joint appeared to ex in the beginning of the exion motion excursion, but to move antidirectionally later in the motion, towards a lesser degree of exion. The small average motion of C0/C1 does not re ect the maximum motion capacity of C0/C1 during exion. This is illustrated by the maximum motion of type Surplus for C0/C1 (Fig. 3) and the large range for pro-directional surplus motion for C0/C1, shown in Table 3. The data suggests that the end-range motion does not re ect the maximum possible motion for an individual joint. The maximum demonstrated joint motion across subjects for each joint measured in this study is presented in Table 5.

Discussion
This study changes our understanding of cervical motion by demonstrating that a little under half of the cervical joints (48.1%) produced pro-directional surplus motion with an average of approximately 2°. Surplus motion should not be considered abnormal as 113 out of 219 joints in exion and 109 out of 217 joints for extension demonstrated motion surplus to end-range.
Approximately 1/5 of all joints demonstrated both pro-directional and anti-directional surplus motion, passing upright and end-range positions with similar frequency. Those joints that did not produce prodirectional surplus motion (Type classic) comprised 46.3% of the total joints. Surprisingly 5.7% of all joints produced anti-directional end-range (type Anti-directional) Type anti-directional joints were found predominantly in the upper cervical region, with only a few in the mid cervical region. The nding that joints can complete their motion in opposition to the direction of head motion is unexpected. Arguably previous documentation that large proportions of anti-directional cervical exion and extension motions were normal in healthy subjects, gave some indication of this possibility (12,(18)(19)(20)(21)26).
Cervical ROM is dependent on method, sex, age, joint degeneration and lifestyle factors (11). The average cervical ROM measured between upright and end-range in this study was similar to previous reports despite differences in the methodology. Cervical ROM in this study was measured between C0 and C7, and a control was applied for motion in the upper thoracic region (5,10,11,(23)(24)(25). Hole et al. reported that for healthy subjects between the ages of 20 and 69, cervical ROM ranged between 50.0° and 64.0°f or exion in males and between 51.6° and 63.3° for exion in females. Extension ranges were between 46.5° and 82.4° for males and 60.9° and 80.1° for females (28).
Cervical joint motion between upright and end-range positions has previously been assess by Wu et al using video uoroscopy. In this case motion was assessed in ranges of one third and the C0/C1 joint was omitted from the study. Wu et al. reported exion joint motion as C2/C3 5,5°, C3/C4 7.8°, C4/C5 10.0°, C5/C6 9.8°, C6/C7 9.2° and for extension joint motion for C2/C3 7,6°, C3/C4 9.8°, C4/C5 12.3°, C5/C6 9.4°, C6/C7 8.1° (5). The current study showed that end-range exion and end-range extension motion were signi cantly different for C0/C1, C5/C6 and C6/C7. By assessing range of motion in 10% epochs, this study aimed to give a more detailed picture of the motion pattern. The C0/C1 joint was also included as we know it to be important in its contribution to cervical spine motion.
The cervical exion motion of C0/C1 (2.3°) demonstrated the smallest average joint motion found in the study. No previous studies have reported the amount of motion found between upright and end-range exion for C0/C1. One study reported end-range exion to end-range extension motion for C0/C1, and the combined exion and extension motion of that study was comparable to the ndings of this study (10). Joint ROM from end-range exion to end-range extension, assessed from stationary exion and extension X-rays, for females and males has been reported to be as follows: 14.5° and 12.6° for C0/C1, 11.6° and 10.9° for C1/C2, 7.8° and 8.4° for C2/C3, 11.6° and 15.2° for C3/C4, 14.4° and 17.0° for C4/C5, 12.2° and 17.9° for C5/C6, 9.8° and 11.4° for C6/C7, respectively (10).

Surplus motion
It may be possible to use the average pro-directional surplus motion as a percentage of end-range ROM as an indicator for the reliability of end-range motion to predict the maximum motion. Analysis of the quartiles of surplus motion demonstrated a clear pattern for both exion and extension. Surplus motion as a percentage of end-range motion decreased with an increase in end-range motion.
As small end-ranges are associated with large percentages of surplus motion, using end-range in these situations to predict a joint's maximum motion may be unreliable. Conversely, it could be argued that large end-ranges can be more readily utilised as a predictor for maximum motion due to their association with small percentages of surplus motion. This does however question the reliability of exion-extension X-rays as an accurate indicator for a joints maximum motion.
Maximum demonstrated joint motion.
The data suggests that the end-range motion does not re ect the maximum possible motion for an individual joint. This is especially clear for C0/C1 during exion, where the average ROM was 2.33° and the average pro-directional surplus motion was 2.36° with a range up to 14.23°. The maximum possible motion of healthy cervical joints is therefore unknown. It is not clear if the maximum measured motion found for all single joints in this study re ects the maximum possible motion capacity of healthy cervical joints.

Study limitations
Quanti cation and analysis of video-uoroscopy has some limitations. The largest confounder is the measurement error. The experimental procedures and reproducibility of image analysis have previously been published (27). High reliability of the vertebral marking procedures has been established and high ICCs have been documented in previous studies (12,17,27).
Neck pain is a recurrent disease and absence of neck pain does not ensure that the subject has a normal neck without any characteristics of neck pain.
The study group was primarily younger adult males and females. Other demographic or anatomical strati cation for sex, age, height, weight, posture, and type of neck: long, thin, short and amount of adipose tissue, may also in uence the cervical ROM and the study results.
Variations in the curvature of the neck, were not considered central to the investigation as all patients were deemed healthy and screened for previous trauma, disease processes or episodes of previous cervical pain. Additionally cervical range of motion in this study agrees with the results of previous studies. Future studies may look at the effect of variations in the cervical lordosis in healthy adults on the prevalence and distribution of surplus motion.
It is recognised in this study that surplus motion can be both pro-directional and anti-directional and that some joints produce surplus motions in both directions. For the purpose of clarity, and because the focus of this paper is maximum pro-directional joint motion, joint classi cation in this study is based on endrange. While type Classic joints in this study do not demonstrate pro-directional surplus motion, they may, in some cases, produce anti-direction surplus motion.
Likewise, type Surplus may also, in some cases, produce anti-directional surplus motion. It is also of note that the variability in joint motion will in uence how joints are grouped (Type, Classic, Surplus and Antidirectional) from motion to motion.
It could also be argued that the study is limited by the choice only to include exion and extension, as this does not allow us to investigate the full dynamic capability of the joints in multiple planes. However, there must be consideration given to the level of radiation exposure healthy subjects are subjected to.

Clinical implications
The results indicate that the end-range motion seen on exion-extension X-rays may not be reliable for the diagnosis of reduced joint motion, as joints with small end-range motion were associated with large surplus motion percentages. In contrast, cervical joints with large end-range motion were associated with small percentages of surplus motion, consequently offering a more reliable prediction of the maximum motion of a joint. It is reasonable to consider that the entirety of a cervical joint's motion capacity is not expended at end-range, as multiplane motion would be di cult if joint structures were fully stretched by motion in just one plane.
However, it is clear that in most clinical interpretations of neck motion the concept of surplus motion is not applied, and yet clinical experience indicates the presence of surplus motion.
Orthopedic surgeons use the terminology compensation for additional joint motion found in joints adjacent to a surgical fusion. The compensation is perceived as a new ability for further cervical single joint motion; however, the compensation may be pre-existing surplus motion of the adjacent joints. This clinical implication may raise the question; is the success of surgical fusion dependent upon pre-surgical surplus motion in the adjacent joints?
Chiropractors have previously used the term para-physiological space to explain the motion which allows an adjustment to occur when a cervical joint is brought to tension.
However, it is possible that the para-physiological space may simply be the surplus motion of the cervical joints. It would seem that we cannot fully understand cervical motion during a physical examination, the xation or the manipulation without rst having a better understanding of surplus motion. The complexity of joint motion has been demonstrated in recent research (12,(18)(19)(20)(21)26).

Conclusion
This is the rst study to categorise joints by type of motion. Type surplus constituted approximately half of the joints analysed in this study. Therefore, end-range motion cannot be assumed to be a demonstration of a joint´s maximum motion. This also throws into question the reliability of exion/extension X-rays as a measure of the total motion capacity of the cervical spine. The traditional view of joint motion seems to describe the motion pattern of a type Classic joint. Only half the joints represented in this study produced a type Classic motion pattern, suggesting that the traditional view of joint motion represents an incomplete picture.
Until now the presence of surplus motion has been acknowledged, but never quanti ed, yet it is undeniably a persistent nding. Quantifying surplus motion provides reference values against which Page 14/19 symptomatic patient data can be compared.

Declarations
Ethics approval and consent to participate.
All participants signed informed consent forms prior to participating in the study. The study was conducted in accordance with the Helsinki declaration and ethical approval was given by the regional ethics committee (N20140004).

Consent for publication.
All participants gave consent to publication and signed the appropriate forms prior to participating in the study.

Availability of data and materials
The datasets generated and/or analysed during the current study are not publicly available due to data protection of participants but are available from the corresponding author on reasonable request. Demographic characteristics of the 33 subjects included in this study. Age, height, weight and body mass index (BMI). The Mann-Whitney U comparisons of pro-directional end-range motion between type classic and type surplus. Motion direction and joints for comparison are shown in rows one and two, rows three and four

Tables
show the joint motion as a mean ± SD of Type Classic and Type Surplus. Table 3 Pro-directional surplus joint motion Pro-directional surplus motion, SD and range in degrees for exion and extension joint motion (C0/C1 to C6/C7). No signi cant differences were found between exion and extension surplus motion. Table 4 Joint motion surplus to end-range in quartiles The quartiles of pro-directional surplus exion and extension motion for joints C0/C1 to C6/C7. The motions were divided into quartiles of end-range motion, with the smallest end-range motion in The calculations for exion of C5/C6 and C6/C7 included only 8 and 5 joints respectively.
The smallest number of joint observations in the extension table was eight, seen at C0/C1. The maximum demonstrated exion and extension motion in degrees. Table 6. Anti-directional joint motion. Table 6 shows anti-directional end-range motion and anti-directional surplus motion for exion and extension.
Due to technical limitations, table 3, 4 and 6 is only available as a download in the Supplemental Files section.