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Journal of Biomechanics 48 (2015) 36503655

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Journal of Biomechanics
journal homepage: www.elsevier.com/locate/jbiomech
www.JBiomech.com

The envelope of motion of the cervical spine and its inuence


on the maximum torque generating capability of the neck muscles
Sorin Siegler a, Paolo Caravaggi b,n, James Tangorra a, Mary Milone a, Ramya Namani a,
Paul A. Marchetto c
a
Department of Mechanical Engineering, Drexel University, Philadelphia, PA, USA
b
Movement Analysis Laboratory, Istituto Ortopedico Rizzoli, Bologna, Italy
c
The Rothman Institute, Thomas Jefferson University Hospital, Philadelphia, PA, USA

art ic l e i nf o a b s t r a c t

Article history: The posture of the head and neck is critical for predicting and assessing the risk of injury during high
Accepted 13 August 2015 accelerations, such as those arising during motor accidents or in collision sports. Current knowledge
suggests that the head's range-of-motion (ROM) and the torque-generating capability of neck muscles
Keywords: are both dependent and affected by head posture. A deeper understanding of the relationship between
Neck head posture, ROM and maximum torque-generating capability of neck muscles may help assess the risk
Head of injury and develop means to reduce such risks. The aim of this study was to use a previously-validated
Range of motion device, known as Neck Flexibility Tester, to quantify the effects of head's posture on the available ROM
Torque and torque-generating capability of neck muscles.
Risk of injury
Ten young asymptomatic volunteers were enrolled in the study. The tri-axial orientation of the
Isometric Maximum Voluntary Contraction
subjects' head was controlled via the Neck Flexibility Tester device. The head ROM was measured for
each exed, extended, axially rotated, and laterally bent head's orientation and compared to that in
unconstrained neutral posture. Similarly, the torque applied about the three anatomical axes during
Isometric Maximum Voluntary Contraction (IMVC) of the neck muscles was measured in six head's
postures and compared to that in fully-constrained neutral posture.
The further from neutral the neck posture was the larger the decrease in ROM and IMVC. Head
extension and combined two-plane rotations postures, such as extension with lateral bending, produced
the largest decreases in ROM and IMVC, thus suggesting that these postures pose the highest potential
risk for injury.
& 2015 Elsevier Ltd. All rights reserved.

1. Introduction Manoogian et al., 2006; Yoganandan et al., 2001; Yoganandan et al.,


2000) or from impact forces applied to a football player's helmet
Trauma of the cervical spine is common in motor vehicle acci- during collisions (Brolinson et al., 2006; Viano and Pellman, 2005;
dents (Nahum and Melvin, 2002; Siegmund et al., 2005; White and Viano et al., 2007). The cervical spine can be injured by forces that
Panjabi, 1978; Whiting and Zernicke, 1998) and in contact sports cause excessive motion about any of its major axes (lateral bending
such as American football (Banerjee et al., 2004; Mueller, 1998; (), exionextension (), and axial rotation (), Fig. 1) (White and
Mueller and Cantu, 2008; Proctor and Cantu, 2000; Torg et al., Panjabi, 1978; Whiting and Zernicke, 1998) but may be most sus-
2002). Most of the injuries occur when forces acting on the neck ceptible to injury when forces are applied in multiple directions. For
exceed the combined resistance of muscle, soft tissue, and bones example, exion combined with axial compression can lead to
and deform the neck beyond its physiologic Range of Motion compression fractures of the vertebrae (Torg et al., 1977; Torg, 1985,
(ROM). The excessive loads may be caused by inertial forces that 1997; Torg et al., 2002; Torg et al., 1979a, 1979b) while extension
develop during vehicular accidents (King, 2000; Maher, 2000; combined with either axial rotation or lateral bending can result in
cervical cord neurapraxia, also known as stinger or burner
n
(Castro, 2003; Kuhlman and McKeag, 1999).
Correspondence to: Movement Analysis Laboratory, Istituto Ortopedico Rizzoli
A combination of passive and active mechanisms act to protect
Via di Barbiano 1/10 Bologna 40136, Italy.
Tel.: 39 051 636 6500; fax: 39 051 636 6561. the cervical spine against injury. Passive protection is provided by
E-mail address: paolo.caravaggi@ior.it (P. Caravaggi). the tissues that surround the cervical spine, including ligaments,

http://dx.doi.org/10.1016/j.jbiomech.2015.08.014
0021-9290/& 2015 Elsevier Ltd. All rights reserved.
S. Siegler et al. / Journal of Biomechanics 48 (2015) 36503655 3651

In light of the above discussion, it is expected that both the


ROM and the IMVC at a given neck posture decrease as the dis-
tance from this neck's posture to the neutral neck posture
increases. This further suggests that the risk for a cervical spine
injury resulting from large external forces depends on the posture
of the neck at the time of loading. For example, a football player
who is hit on the head frontally while the head is turned, or a
driver whose head is turned to the side while being hit from
behind by another vehicle are both critical situations where the
cervical spine is at higher risk of injury due to the out-of-neutral
posture at the time of impact. Subsequently, the goal of this study
is to quantitatively describe the dependence of the cervical spine's
ROM and IMVC on neck posture. This has the potential to provide
valuable information for establishing safety guidelines and for the
design of improved neck protective devices and safety equipment
for athletic activities and for motor vehicles.

2. Methods
Fig. 1. Anatomical coordinate system for describing rotations, ROM, and IMVC of
the cervical spine. Here: and M are respectively the rotation and torque around 2.1. Subjects
the lateral bending axis e1 (xed to base of the cervical spine, oriented anteriorly
and aligned with C7-T1 junction); and M are the rotation and torque around the Ten young asymptomatic volunteers consisting of six males and four females
exion/extension oating axis e2 (perpendicular to e1 and to e3); and M are the (age 257 4.9 years) with no history of neck or shoulder pathology participated in
rotation and torque around the axial rotation axis e3 (xed to the head and oriented the study. The testing protocol was approved by Drexel University's Institutional
perpendicular to the Frankfurt horizontal plane). Review Board. All subjects provided written informed consent after the testing
procedure was explained. General anthropometric data, consisting of age, height,
bones, discs, and connective tissues. These tissues provide the weight, Body Mass Index (BMI), head circumference, neck circumference, and neck
length, were recorded from each subject (Table 1). Preliminary tests showed that
spine with its stiffness characteristics (McClure et al., 1998; McGill the chosen population size was sufcient to achieve a statistical power of at least
et al., 1994) and dictate the spine's ROM (Castro et al., 2000; Fer- 0.8 at 0.05 level of signicance.
rario et al., 2002; Fielding, 1956; Lind et al., 1989; Lynch-Caris
et al., 2006; Roozmon et al., 1993). The neck's stiffness and ROM in 2.2. Instrumentation
the major anatomical planes have been found to vary with age,
gender (Castro et al., 2000; Dvorak et al., 1992; Lansade et al., The main characteristics evaluated in this study, passive ROM and IMVC, were
2009; McClure et al., 1998; Sforza et al., 2002; Trott et al., 1996), dened and measured relative to an anatomical coordinate system (Grood and
Suntay, 1983) recommended by the International Society of Biomechanics (Wu
posture (McClure et al., 1998; Panjabi et al., 1993) and the presence et al., 2002) and adapted to the cervical spine (McClure et al., 1998) (Fig. 1). These
of pathological conditions (Antonaci et al., 2002; Heikkila and were measured using a six-degree-of-freedom validated instrumented linkage,
Wenngren, 1998; Hilibrand et al., 2006; Hino et al., 1999; Puglisi referred to as the Neck Flexibility Tester (NFT, Fig. 2). Details of this device have
et al., 2004). However, no quantitative data are available to been provided previously (McClure et al., 1998). The NFT measured the subject's
ROM via rotational sensors and IMVC via torque sensors at any neck posture
describe the relationship between lateral bending ROM and neck's (McClure et al., 1998). Each rotational axis could be moved and locked in position so
orientation in exion, extension, or axial rotation. It is expected that a subjects' head could be positioned, oriented and xed anywhere within the
that posture of the cervical spine away from neutral will produce subject's physiological envelope of motion. In this study, neck motion and posture
deformations in soft tissues such as ligaments, intervertebral discs, are dened as the motion or posture of the head with respect to the base of the
cervical spine (rst thoracic vertebra). Data from the sensors (position and torque)
and tendons that will reduce the out-of-plane ROM and thus will
were collected through an A/D converter at a sampling rate of 20 Hz.
increase the risk of injury.
Active protection of the cervical spine is provided by sur- 2.3. Testing procedure
rounding musculature. The strength of these muscles has been
studied mainly through measurements of Isometric Maximum After explaining the testing protocol to the subject, he/she was seated in the
Voluntary Contraction (IMVC). Most studies quantied IMVC in NFT chair with his/her torso xed to the chair via Velcro straps. The NFT linkage
exion and extension only (Barton and Hayes, 1996; Garces et al., was attached to the subject's head via a lightweight helmet. The axes of the NFT
were aligned to the subject's head and base of the cervical spine, as described
2002; Jordan et al., 1999; Mayoux-Benhamou and Revel, 1993;
earlier, while maintaining a neutral posture (McClure et al., 1998). Neutral posture
Rezasoltani et al., 2005). Few studies quantied IMVC in other
directions, such as lateral bending and axial rotation (Chiu et al.,
Table 1
2002; Chiu and Sing, 2002; Seng et al., 2002; Van Wyk et al., 2010; Anthropometric data for the 10 tested subjects (mean 7SD). Head circumference
Vasavada et al., 2001; Vasavada et al., 2002), and the effect of was measured just above the ears level. Neck circumference was measured around
cervical spine posture on IMVC has only been studied in exion/ the laryngeal prominence. Neck length was measured by palpation from the
occipital condyle to the midpoint of the line between the C7 spinous process and
extension and lateral bending (Garces et al., 2002; Harms-Ring-
the T1 spinous process, referred to as the C7-T1 point.
dahl and Schldt, 1989; Jordan et al., 1999; Van Wyk et al., 2010).
The authors found no information on the effect of neck posture on Male Female All
IMVC in axial rotation. Furthermore, no information was found on
Age (years) 25.8 7 4.9 24.57 0.6 25.2 7 3.2
the effect of neck posture away from neutral on the IMVC in out-
Height (cm) 173.5 7 8.7 167.6 7 9.0 171.17 8.9
of-plane directions. For example, the effect of an axially rotated Weight (kg) 69.3 7 10.6 67.3 7 15.5 68.57 12.6
neck on the IMVC in exion is unknown. It is expected that pos- BMI (kg/m2) 22.9 7 2.7 23.6 7 2.8 23.2 7 2.7
ture of the cervical spine away from neutral will reduce the Head circumference (mm) 569.6 7 15.4 570.07 7.1 570.07 12.1
Neck circumference (mm) 365.8 7 16.2 342.0 7 37.7 356.07 24.8
maximal force generating capacity of neck musculature and thus
Neck length (mm) 150.8 7 25.3 127.7 7 14.9 141.6 7 21.1
will increase the risk of injury.
3652 S. Siegler et al. / Journal of Biomechanics 48 (2015) 36503655

position. Five measurements of neck ROM in each of the six directions were taken
for each subject.

2.5. Measurement of passive ROM at different neck postures

The subject's neck was moved and xed through the NFT into each of four 40
rotations from the neutral posture around the main axes (exion, extension, right
lateral bending and right axial rotation). Since the neutral posture data showed no
statistical difference (p 4 0.05) in ROM between left and right orientations in lateral
bending and in axial rotation (i.e. symmetric behavior of the vertebral bodies, see
also Youdas et al. (1992)), in order to minimize the acquisition time only the right-
side lateral bending and right-side axial rotation postures were assessed in this
test. With the head orientation xed with respect to the main axis, the ROMs about
the remaining two unconstrained axes were measured (Fig. 3). The order in which
the ROM measurements were performed was randomized between subjects.

2.6. Measurement of IMVC at different neck postures

Fig. 2. The NFT device used to measure the neck's ROM and IMVC. The NFT's axes The IMVC test (see Fig. 4) was performed with the subject's neck xed through
are aligned with e1, e2 and e3 axes of the subject's neck (see Fig. 1). the NFT into one of seven preset postures: neutral; 40 exion; 40 extension; 30
right lateral bending; 20 right axial rotation; 40 extension with 20 right lateral
bending, and 40 extension with 20 right axial rotation. The latter coupled pos-
of the neck was dened as the posture in which, when the torso is erect, the
tures, extension with lateral bending and extension with axial rotation (Fig. 4),
Frankfurt Horizontal plane (the plane containing the left and right auditory
were selected according to the observation that many neck injuries, such as
meatus and the infra-orbital notch) is horizontal with zero tilt in either the sagittal
stingers in football occur when the head/neck is in these particular postures
or frontal planes and the head has zero axial rotation (McClure et al., 1998).
(Castro, 2003; Kuhlman and McKeag, 1999; Torg et al., 1990). All the above values
A testretest was performed on six subjects from the same population to assess
were chosen according to previous trial and error tests aimed at identifying neck
the reliability of the NFT in measuring ROM and IMVC between sessions. The NFT
postures that could be tolerated by the subjects without pain or discomfort while
reliability was assessed via ICC model 2,k (Weir, 2005) since subjects were mea-
applying IMVC. During the IMVC measurements, the neck was completely xed
sured by the same examiner in two sessions and each sample was the average of
through the NFT to approximate isometric conditions. In each posture, the subject
three repetitions (k 3). For the testretest of ROM parameters, these were mea-
was instructed to generate an IMVC in one of six directions: exion; extension;
sured with the neck in neutral posture in the three anatomical planes, and with
right lateral bending; left lateral bending; right axial rotation; and left axial rota-
neck at 40 exion in lateral bending and axial rotation. For IMVC parameters, these
tion. A 30 s rest period was provided following each contraction to minimize
were measured with the neck in neutral posture, at 40 extension, and at combined
fatigue. The order of testing was randomized between subjects.
40 extension and 20 lateral bending. ROM and IMVC were calculated for both left
A full testing session comprised the ROM and the IMVC tests and was repeated
and right rotations in each neck posture.
on each subject on two different days. The maximum ROM and IMVC values from
the two sessions were used in the data analysis.
2.4. Measurement of passive neutral ROM
2.7. Data analysis
An examiner measured the passive ROM of each subject's neck in the six main
anatomical directions: exion; extension; left lateral bending; right lateral bend- Repeated measure analysis of variance (ANOVA) was conducted to compare the
ing; left axial rotation; and right axial rotation. These measurements were per- effect of ve different postures on the ROM in six different directions. Repeated
formed with the neck in neutral posture and no motion restrictions imposed measure ANOVA was also conducted to compare the effect of seven cervical spine
through the NFT. The examiner applied torque slowly to the subject's head to postures on the IMVC in six different directions. Once signicant differences were
produce rotation in the desired direction until the subject gave a verbal indication found, the StudentNeumanKeuls tests were performed at p o 0.05 signicance
of their limit. Subjects were encouraged to tolerate a stretching sensation, but were level to identify specic signicant differences.
not encouraged to withstand pain. A complete cycle consisted of moving the head
in one direction, back to neutral, in the opposite direction, and back to the starting

3. Results

AR ICC data showed good repeatability of the NFT in measuring


both ROM and IMVC in different neck postures. ICC ranged

EA

ROM-LR
ROM-LL IMVC-AL

IMVC-LL
IMVC-LR

IMVC-E

IMVC- F
ROM-E
ROM-F

Fig. 3. Neck passive ROM measuring setup. The subject is relaxed and the operator
(not-represented in the gure) induces motion in a specic direction through a Fig. 4. IMVC measuring setup. With all NFT axes locked and the subject's neck
torque applicator until the ROM in that specic direction is reached. In the gure, orientation xed (), the subject produces IMVC in six directions: E extension;
rotation around e3 is locked with the head axially rotated (AR) by 40. The operator F exion; LL left lateral bending; LR right lateral bending; AL left axial
induces motion around e1 and e2 to measure the range of motion in four directions: rotation, and AR right axial rotation. In the gure, IMVC is measured with the
E extension; F exiom; LL left lateral bending, and LR right lateral bending. neck extended by 40 and axially rotated by 20 (EA).
S. Siegler et al. / Journal of Biomechanics 48 (2015) 36503655 3653

between 0.78 and 0.98 for ROM measurements (0.90 7 0.07) and exion and extension signicantly reduce the ROM in axial rota-
between 0.79 and 0.98 for IMVC measurements (0.92 70.06). tion, whereas Dvorak et al. (1992) found that extension did not
The ROM of the cervical spine in exion, extension, lateral signicantly affect the axial rotation ROM (Table 4). Most of the
bending, and axial rotation was the largest when the neck is in studies reporting the effect of neck posture on IMVC focused only
neutral posture (Table 2). Lateral bending and axial rotation on the effect of a sagittal-plane posture on the IMVC in exion/
reduced the passive ROM in exion by approximately 20% com- extension (Garces et al., 2002; Harms-Ringdahl and Schldt, 1989;
pared to the ROM in neutral (Table 2 and Fig. 5). ROM in extension Jordan et al., 1999; Van Wyk et al., 2010). These studies, including
resulted signicantly reduced by lateral bending posture, but not the present investigation, found that exed posture of the neck
signicantly affected by axial rotation posture. The cervical spine's increased slightly the IMVC in extension and decreased the IMVC
ROM in lateral bending was not signicantly inuenced by exion in exion as compared to neutral. Extension decreased IMVC in all
posture, but was signicantly inuenced by extension. Lateral directions. The few studies that considered the effect of lateral
bending was affected by axial rotation only in the ipsi-lateral bending on the IMVC in the same direction (Chiu et al., 2002; Seng
direction (i.e., lateral bending to the right is only inuenced by et al., 2002) reported minimal effects, in contrast to the present
axial rotation to the right). Axial rotation ROM was reduced by study were large decreases in IMVC were recorded. No published
posture away from neutral, with exion producing the largest data could be found on either the effect of variations in the
reduction in the ROM. transverse plane posture (axial rotation) or on the effect of varia-
When in neutral posture, the IMVC in exion and extension tions in the out-of-plane posture on the in-plane IMVC, such as the
was signicantly larger than in lateral bending or axial rotation effect of positioning the neck in extension while measuring the
(Table 3). When the neck posture was away from neutral the neck IMVC in axial rotation or lateral bending. Also, no studies were
was still strongest in exion and extension and IMVC decreased, or found that investigated the effect of complex neck postures
remained the same, in all directions, with two exceptions: IMVC in involving more than a single plane rotation on IMVC.
extension and in axial rotation increased slightly when the neck's In this study, both the ROM and IMVC of the cervical spine were
posture was maintained in exion. The two combined-rotations found to be strongly dependent on neck posture. It was further
postures (extension with lateral bending and extension with axial
rotation) produced large and signicant decreases in IMVC, with e3
the exception of the small and insignicant effect of extension
AR
combined with lateral bending on axial rotation. AL
LL e3
e3 64%
e1 e1
71%
70% LR
4. Discussion 71% 64%
69%
96%
This study is part of a long-term effort to develop effective 87%
guidelines and external protective devices to protect the neck e1
against injury producing loads in high-risk activities such as col-
lision sports. In particular, this study aimed at quantifying the N
effect of neck posture on the passive and active natural protection
mechanisms of the neck in order to identify those postures in E
F
which the neck is least naturally protected and thus may be at
e3
higher risk for injury from applied loads.
The effect of neck posture on ROM and IMVC was, albeit only AR
partially, investigated in previous studies. Both Dvorak et al. (1992) e3 AL
e2 E
78%
and Walmsley et al. (1996) reported the effect of exion and 81% 69% e2
extension on the passive ROM in axial rotation (Table 4). Similarly 81%
F
to Walmsley et al. (1996), the present study found that both

Table 2
ROM of the cervical spine (deg, mean 7 SD) at different neck postures. Columns
represent different neck postures and rows represent different directions of ROM
measurements. In each direction, statistically different (p o 0.05) ROM between N
neck postures are shown with corresponding letters in parentheses. LR
e1
Neck postures
LL
N F E LR AR e1
LR 92%
F
Flexion 737 12 59 715 607 15 e2 79%
(LR, AR) (N) (N) E
Extension 68 710 53 714 627 16 82%
(LR) (N, AR) (LR) 91%
Left lateral bending 527 7 507 5 377 15 48 7 15 e2
(E) (E) (N, F)
Right lateral bending 527 8 457 9 367 13 417 11
(E, AR) (E) (N, F) (N)
Left axial rotation 777 7 49 7 9 547 16 53 712 N AR
(F, E, LR) (N) (N) (N)
Right axial rotation 727 8 467 11 51 7 10 58 79 Fig. 5. From top to bottom, a schematic representation of the neck postures used in
(F, E, LR) (N, LR) (N) (N, F) the study to determine the passive neck ROM. Here: N is the neutral posture; E is
the 40 extension; F is the 40 exion; LR is the 40 right lateral bending, and AR is
N neutral; F 40 exion; E 40 extension; LR 40 right lateral bending; AR the 40 right axial rotation. The percentages represent the average ROM measured
right axial rotation. along each direction with respect to that measured in neutral posture.
3654 S. Siegler et al. / Journal of Biomechanics 48 (2015) 36503655

Table 3
IMVC (Nm) of the cervical spine at different neck postures. Columns represent different neck postures and rows represent different directions of IMVC measurements. The
percentage of reduction (negative) or increase (positive) in IMVC in a given direction, compared to the IMVC in neutral posture, is shown in parentheses. In each direction,
statistically different (p o0.05) IMVC between neck postures is shown with corresponding letters in parentheses.

Neck postures

N F E LR AR EA EL

Flexion 207 11 15 76(-25%) 15 77(  25%) 17 78(  15%) 16 79(  20%) 137 8(  35%) 147 7(  30%)
(E, AR, EA, EL) (N) (N) (N) (N)
Extension 217 11 237 11( 9%) 14 78 (  33%) 17 710(  24%) 19 710 (  9.5%) 127 8 (  43%) 137 6(  38%)
(E, EA, EL) (E, LR, AR, EA, EL) (N, F, LR, AR) (F, E, EA, EL) (F, E, EA, EL) (N, F, LR, AR) (N, F, LR, AR)
Left lateral bending 127 4 10 75(  17%) 87 3(  33%) 8 75(  33%) 10 75(  17%) 87 4(  33%) 8 74(  33%)
(F, E, LR, AR, EA, EL) (N) (N, AR) (N, AR) (N, F, E, LR, EA, EL) (N, AR) (N, AR)
Right lateral bending 117 6 87 4(  27%) 77 3(  36%) 5 72(  55%) 10 74(  9%) 77 3(  36%) 5 72(  55%)
(E, LR, EA, EL) (LR, EL) (N) (N, F, AR) (LR, EA, EL) (N, AR) (N, F, LR)
Left axial 97 6 87 4(  11%) 77 4(  22%) 7 74(  22%) 97 5(0%) 77 4(  22%) 7 74(  22%)
rotation (E, EA) (N, AR) (E, EA, EL) (N, AR) (AR)
Right axial rotation 87 5 97 5( 12.5%) 77 4(  12.5%) 8 75(0%) 87 4(0%) 67 3(  25%) 7 74(  12.5%)
(E, EA) (E, EA, EL) (N, F, LR) (E, EA, EL) (N, F, LR) (F, LR)

N neutral; F exion (40); E extension (40); LR right lateral bending (30); AR right axial rotation (20); EA extension (40) combined with right axial rotation
(20); EL extension (40) combined with right lateral bending (20).

Table 4 ways including properly designed protective mechanisms such as


Review of the current literature on the effect of exion/extension neck posture on neck braces for contact sports or headrests for vehicle seats.
the axial rotation ROM (deg). In parentheses, the percentage of decrease in ROM
compared to that measured in neutral posture.

Neutral Flexion Extension Conict of interest statement

Dvorak et al. (1992) 183 71 (61%) 162 (11%)


No conict of interests has been reported by the authors.
Walmsley et al. (1996) 149 100 (33%) 78 (48%)
Present study (average) 149 95 (36%) 105 (29%)

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