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LITERATURE REVIEWS

COUPLING BEHAVIOR OF THE CERVICAL SPINE:


A SYSTEMATIC REVIEW OF THE LITERATURE
Chad Cook, PhD, PT, MBA,a Eric Hegedus, PT, DPT,b Christopher Showalter, PT,c and Phillip S. Sizer Jr, PhD, PTd

ABSTRACT
Objective: The purpose of this study was to investigate evidence of consistency of reported directional coupling patterns
among selected studies and to determine its use in manual medical treatment.
Methods: The study was a systematic literature review of English-only journals using PubMed and CINAHL. The
keywords included bcervical vertebrae,Q bbiomechanics,Q bcoupling,Q and bthree-dimensional movementQ and required
coupling directional assessment of individual spine segments.
Results: Four 2-dimensional and 8 3-dimensional studies met inclusion criteria. This study found 100% agreement in
coupling direction (side flexion and rotation to the same side) in lower cervical vertebral segments (C2-3 and lower) and
variation in coupling patterns in the upper cervical segments of occiput-C1 (during side flexion initiation) and C1-2.
Dissimilarities may be explained by differences in measurement devices, movement initiation, in vivo vs in vitro
specimens, and anatomical variations.
Conclusions: These findings suggest that use of 3-dimensional analyzed cervical coupling patterns for the lower
cervical vertebral during apposition and treatment application may show clinical use for manual clinicians. The use of
directional coupling based on 2-dimensional cervical coupling patterns or upper cervical spine coupling that addresses
C1-2 should be questioned. (J Manipulative Physiol Ther 2006;29:570Q575)
Key Indexing Terms: Cervical Vertebrae; Spine; Biomechanics; Manual Therapy

oupled spinal motion is the rotation or translation


of a vertebral body about or along one axis that is
consistently associated with the main rotation or
translation about another axis.1 During movement, translation occurs when all elements within that segment move in

Assistant Professor, Division of Physical Therapy, Department


of Community and Family Medicine, Duke University, Durham,
NC.
b
Assistant Clinical Professor, Duke University, DUMC 3907,
Durham, NC.
c
Clinical Director, Maitland Australian Physiotherapy Seminars,
P.O. Box 1244, Cutchogue, NY.
d
Professor and Program Director, ScD Program in Physical
Therapy, Department of Rehabilitation Sciences, Texas Tech
University Health Sciences Center, Lubbock, Tex.
Submit requests for reprints to: Chad Cook, PhD, PT, MBA,
Assistant Professor, Division of Physical Therapy, Department of
Community and Family Medicine, Duke University, Durham, NC
27710 (e-mail: chad.cook@duke.edu).
Paper submitted December 27, 2005; in revised form April 22,
2006; accepted April 26, 2006.
0161-4754/$32.00
Copyright D 2006 by National University of Health Sciences.
doi:10.1016/j.jmpt.2006.06.020

570

the same direction with the same velocity.1 With movement,


rotation occurs as a spinning or angular displacement of the
vertebral body around some axis.
Biomechanical coupling is 3-dimensional (3D), takes
place within 6 df, and is often described using the Cartesian
coordinate system.2 The 6 df can translate along and rotate
about each orthogonal axis.1 The 3D motions in humans
correspond to flexion/extension, rotation, and side-bending
forces; one specific movement initiation (such as sidebending) theoretically activates movement in the other
5 component motions. The behavior of the coupled pattern
is dependent on the first motion of initiation (eg, sidebending), the posture of the spine, and the pathology of
the segment.3
Coupling of the cervical spine is of importance to manual
clinicians during assessment of pathology and treatment
application. In theory, measurements of coupling motion are
useful to diagnose pathologic disorders such as clinical
instability due to degeneration, disease, or trauma.4,5
Variations in coupling behavior reportedly identify potential
risk factors for treatment such as spontaneous atlas
dislocation.6,7 Hypothetically, both the quantity and quality
of coupling motion are important clues in the detection of
selected elements of spine pathology.

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More so than with diagnosis, manual clinicians use


coupling of the cervical spine during administration of
treatment techniques. Many manual medicine disciplines
base specific mobilization, manipulation, and muscle energy
techniques on selected theories of coupling direction.8-11
Common to these manual medicine treatment techniques is a
concept called apposition. Apposition is a close packed
combined movement and is, in essence, the biomechanical
opposite of a coupled movement. This close packed movement is often preselected, based on the theoretical preexisting direction of coupled motion. Apposition movements
are frequently used during manipulative procedures and are
termed in osteopathic literature as a locked position.12
Ironically, treatment methods that are based on coupling
theories are often inconsistently reported and are generally
defined through bexpert-basedQ learning models.13,14 The
feasibility exists that, if practicing clinicians do not share
consistent directional coupling pattern expectations, the
results of their assessment and treatment may be dissimilar.
The purpose of this study was to investigate evidence of
consistency among reported directional coupling pattern
among selected studies and to determine its use in manual
medicine treatment. Within clinical practice, the side-bend
and axial rotation initiation of movement are used more
frequently than flexion/extension initiation. Because of
clinical relevance and the lack of representation in the
literature of flexion/extension initiation, only coupling
studies associated with initiation of side-bend and/or axial
rotation motion were investigated within this study.

METHODS
Criteria
Only manuscripts written in English were considered.
Studies that investigated in vivo (live subjects) or in vitro
(cadaveric specimens) cervical spine coupled motion during
2-dimensional (2D) or 3D experimental analyses were
selected. For inclusion, each study required an experimental
analysis for detection of quantity and direction of coupling
movement. The analysis was required for a specific level;
not combined multiple levels. In addition, this study
focused on the report of coupling during side-bending and
rotation movements with either movement as the initiation.
Notably absent from selection are textbook references to
cervical spine coupling because the likelihood that the
coupling patterns reported were determined by empirical
means is questionable.

Search Strategy for Selection of Studies


Study selection was initiated with the aide of the
computer-based search engines of PubMed, which included
MEDLINE (February 1966 to April 2006), Old Medline
(1950-1965), in-process citations, and CINAHL (February

Cook et al
Cervical Spine Coupling

Table 1. Search strategy to identify cervical spine coupling


manuscripts (April 21, 2006)
No.

Search history

Results

1
2
3
4
5
6

exp Cervical Vertebrae/


exp BIOMECHANICS/
1 and 2
coupling.mp.
Three-dimensional movement.mp.
3 and (4 or 5)

19 279
477 285
1083
48 183
77
13

1982 to April 2005). The search strategy is outlined in


Table 1. Each search included the search terms of bcervical
vertebrae,Q bbiomechanics,Q bcoupling,Q and bthree-dimensional movement.Q Furthermore, a comprehensive hand
search of all articles references from those studies collected
in the computer-based search and those known to the
authors were performed.

Methods of Review
Studies were selected by the lead author (CC) and
reviewed for inclusion. When coupling values were reported
per segment, the results were included in the 2D or 3D
analysis. When an article was deemed questionable, a
second author (EH) was consulted to review the study.

RESULTS
The PubMed search identified 13 articles using the
combined keywords of bcervical vertebrae,Q bbiomechanics,Q
bcoupling,Q and bthree-dimensional movement.Q The
CINAHL search netted 7 studies, 2 of which were not
represented in the PubMed search. A hand search identified
28 additional articles that were obtained for review. The
43 articles were obtained for review. Of the 43, 5 were
written in German or Swedish and were excluded. Twentytwo others did not define a directional coupling pattern and
did not qualify (confirmed by EH). Three others did not
report a specific segmental coupling pattern (global coupling
was measured), and 1 reported only values from the thoracic
spine. Upon completion of the review, 12 articles were
identified as plausible investigatory analyses of coupling
motion of the cervical spine. Four of the articles used 2D,
whereas 8 used 3D methods of investigation.
Four studies qualified as 2D analyses of side-bend
initiation of coupling motion. Table 2 outlines the findings.
None of the 2D articles reported the sex, age, ethnicity, or
disease process within the studies. One study used clinical
observation of passive and active movements,15 whereas
another used clinical palpation of passive movement during
assessment of directional coupling movement.16 Lovett15
used cadaveric specimens placed on a wooden slab and
passively moved to reproduce coupling behavior. In addition,
Lovett used live subjects who actively moved in all move-

571

572

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Cervical Spine Coupling

Journal of Manipulative and Physiological Therapeutics


September 2006

Table 2. Coupled cervical motion with side-bend initiation (neutral spine) 2D analyses
Author

C0-1

C1-2

C2-3

C3-4

C4-5

C5-6

C6-7

C7-T1

Capobianco et al16 (in vivo)


Fielding17 (in vivo)
Lovett 190515a (both)
Lysell18 (in vitro)

NT
NT
S
NT

NT
NT
S
NT

NT
S
S
S

V
S
S
S

NT
S
S
S

NT
S
S
S

NT
S
S
S

NT
S
S
S

Side (lateral)bend initiation of movement.


S, Axial rotation coupling to the same side as side-bend; O, axial rotation coupling to the opposite side of side-bend; NT, not tested; V, variable coupling
pattern among specimens.
a
Lovett did not maintain neutral position, thus determined the movement was to the same side

Table 3. Coupled cervical motion with side-bend initiation (neutral spine) 3D analyses
Author

C0-1

C1-2

C2-3

C3-4

C4-5

C5-6

C6-7

C7-1

Panjabi et al24 (in vitro)


Panjabi et al5 (in vitro)
Panjabi et al25 (in vitro)
Penning et al23 (in vivo)
Ischii et al21 (in vivo)

NT
S
S
S
0

NT
O
S
S
0

S
NT
S
S
S

S
NT
S
S
S

S
NT
S
S
S

S
NT
S
S
S

S
NT
S
S
S

S
NT
S
S
S

Side (lateral)bend initiation of movement.

ment planes. Two studies17,18 used radiographic assessments


(cineroentgenography) in determining coupling motion, but
neither study reported the type of subjects or specimens,
whether control was used to ensure nondegenerative spinal
units, and how the movement pattern was introduced. All
studies found that during side-bend initiation, axial rotation
occurs simultaneously to the same side at the levels tested.
Five studies qualified for 3D analyses of coupling motion
with side-bend initiation, whereas 6 studies qualified for 3D
analyses of coupling motion with rotation initiation. Mimura
et al,19 Ischii et al,20,21 and Iai et al22 performed in vivo
analyses. Mimura et al included 25 normal male subjects 25
to 31 years of age who performed planar active range of
motion movements of rotation. Iai et al used a similar
protocol including 20 normal men 27 to 40 years of age who
performed the active range of motion of rotation. Ischii et al
used an in vivo 3D magnetic resonance imaging system to
measure the active range of motions of side flexion21 and
rotation.20 In the study detecting side flexion initiation,
Ischii et al used 12 healthy volunteers (6 men and 6 women).
In the study detecting rotation initiation. Ischii et al20
included 10 healthy volunteers (5 men and 5 women).
Penning23 failed to report the subject characteristics within
his in vivo trial. The 3 distinct in vitro studies by Panjabi
et al5,24,25 used up to 16 fresh cadaveric single-segment
specimens or multiple segment specimens with normal
degenerative changes to produce 3 different distinctive data
sets. The in vitro specimens were cleaned, prepared, and
attached to a mechanical device and passively moved during
the measurement processes. None of the in vitro studies5,24,25 reported the sex or age of the cadaveric donors.
Five studies qualified as 3D analyses of coupling motion
with side-bend initiation. Table 3 outlines those findings.

Every study identified the simultaneous occurrence of the


coupled movements of flexion and rotation at all levels
tested. Generally, there was remarkable agreement among
all studies at most segmental levels. All studies that tested
C2-3, C3-4, C4-5, C5-6, C6-7, and C7-1 found consistent
side-bend and axial rotation to the same side. Three studies
reported that side-bend and axial rotation occurred in
opposition at C1-2 and 2 others found coupling movement
to the same side. Only Ischii et al21 found side flexion and
rotation coupling in the opposite direction compared with
3 others who reported the same side.
Table 4 outlines the coupled movements of the cervical
spine during axial rotation initiation. Five studies measured
rotation, 2 of which measured all levels. Similar to sidebend initiation, axial rotation initiation showed strong
agreement among researchers. All studies that tested C0-1,
C1-2, C3-4, C4-5, C5-6, C6-7, and C7-1 showed absolute
agreement. Levels C0-1 and C1-2 exhibited side-bend to the
opposite direction as the initiated movement of axial
rotation. The spinal levels C2-3, C3-4, C4-5, C5-6, C6-7,
and C7-1 exhibit side-bend to the same direction as the
initiated movement of axial rotation. Only 2 studies reported
the movement values of C2-3 and C3-4 and found rotation
and side flexion occurred to the same side.
Most 3D studies provided accuracy measures associated
with experimental procedure. Table 5 outlines the error values
for translation, side flexion, and rotation for each study. Of
the 8 3D studies included, Panjabi et al24 used an in vitro
study and reported the lowest degree of error during the
analysis. Two in vivo studies19,22 showed a high degree of
inaccuracy during lateral side flexion. Both Ischii et al20,21
studies that used a 3D magnetic resonance imaging found
error values that were less than the Iai et al22 and Mimura

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Cook et al
Cervical Spine Coupling

Table 4. Coupled cervical motion with rotation initiation (neutral spine) 3D analyses
Author

C0-1

C1-2

C2-3

C3-4

C4-5

C5-6

C6-7

C7-1

Ishii et al20 (in vivo)


Mimura et al19a (in vivo)
Panjabi et al5 (in vitro)
Panjabi et al25 (in vitro)
Penning et al23 (in vivo)
Iai et al22 (in vivo)

O
NT
O
O
O
S

O
NT
O
O
O
O

NT
NR
NT
S
S
S

NT
NR
NT
S
S
S

NT
S
NT
S
S
S

NT
S
NT
S
S
S

NT
S
NT
S
S
S

NT
S
NT
S
S
S

Axial rotation initiation of motion. NR, not reported.


a
Mimura et al reported the movements of occiput-C2, not C0-1 and C1-2 individually.

Table 5. Accuracy reports for experimental procedure in 3D


investigations
Author

Translation
(mm)

Rotation

Lateral
bending

Iai et al22 (in vivo)


Ishii et al20 (in vivo)
Mimura et al19 (in vivo)
Panjabi et al24 (in vitro)
Panjabi et al5 (in vitro)
Panjabi et al25 (in vitro)
Ischii et al21 (in vivo)
Penning et al23 (in vivo)

1.0
0.41
1.0
0.11
0.22
0.22
.41-52
NR

1.58
0.438
1.58
0.028
0.178
0.178
0.438
NR

4.58
0.318
NR
NR
NR
0.338
0.318
NR

Error measurements in millimeters or degrees.

et al19 data but higher than the in vitro studies. Penning23


failed to report the accuracy measure of his mathematical
analysis of motion.

instrumentation,26,31 which allows the measurement of finite


movements in multiple planes.
We elected to include studies that used 2D imagery
because many clinicians still report the use of 2D
theories,32 the most notable are those of the so-called
Laws of Physiologic Spinal Motion suggested by Fryette.33
In 1954, Fryettes findings were published and were
largely based upon the findings of Lovett.15 Fryettes
perception of coupling of the cervical region was that, b. . .
side bending is accompanied by rotation of the bodies of
the vertebrae to the concavity of the lateral curve, as in
the lumbar (spine).Q The findings of Fryette were not
included because they did not include a systematic,
investigatory method of evaluation. At best, Fryette
included 2D technology to visualize coupling patterns
and, most likely, inaccurately documented the coupling
movements of the upper cervical spine. Despite the lack of
a systematic investigatory method, Fryettes laws have
been the basis of manual medicine application in many
manipulative textbooks.8-11

DISCUSSION
In 2003, Cook13 detailed that numerous studies reported
variable coupling methods for the lumbar spine. The author
suggested that evidence to support a bnormalQ directional
coupling pattern of the spine was poor. Unlike the lumbar
spine, our study advocates that a directional pattern to
coupling of the lower cervical spine does display predictability and across-study agreement. Similar to the lumbar
spine findings, the upper cervical spine exhibits variation in
coupling, and coupling appears that cross-study comparisons are influenced by the type analysis and the movement
used to initiate the coupling.

Two-Dimensional Analysis
It has been identified that 2D analysis of coupling
motions fails to report accurate axial rotation and may be
ineffective at measuring coupling direction and quantity.26,27 Two-dimensional imagery has been criticized
because it may lead to magnification errors, projection of
translations as rotations, and misleading results.28-30 To
represent the true accurate motion behavior of the spine,
intervertebral coupling motion is best measured with 3D

Three-Dimensional Analysis
According to our assessment of 3D analyses, all
investigators reported that side flexion and rotation occur
to the same side during side flexion or rotation initiation at
the cervical segments of C2-3 and caudal. In addition,
consistency was observed in the upper cervical segments
(C0-1, C1-2) during rotation initiation, where the segments
exhibit side flexion motion to the opposite side. However,
C0-1 and C1-2 shows less consistency across studies during
side flexion initiation. There may be several reasons for this
coupling variability.
Anatomical variation, structure, and mechanical influences may explain the minor variations at C1-2 during side
flexion initiation. Earlier studies described the C1-2 motion
as a convex on convex behavior, a finding based on
radiographic assessment.34 Moreover, the occipitoatlantoaxial complex exhibits intricate interactions between
bony and soft tissue structures (especially with regard to
the interactions of the alar ligament complex, which can
show anatomical variation in themselves) that regulate the
stability and mobility of this region.35 The multifactorial

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Cook et al
Cervical Spine Coupling

interplay among structures may consequentially alter the


coupling pattern and may explain the variation of results
seen during side flexion vs rotation initiation. The
occipitoatlantoaxial complex exhibits the highest degree
of variance in total range of motion when compared with
other cervical segments23 and is the region in which range
of motion is most altered by head position.36
Second, the instrument used during the measurement
process may lead to variable results. Ischii et al21 reported
0.28 of coupled rotation at C0-1, which is a value less than
the accuracy of the instrument. Two studies19,22 showed
high degrees of error in side flexion; error values that
occasionally exceeded the actual movement of side flexion
at C1-2. Nonetheless, the variation found at C1-2 may not
be explained completely because of this because Panjabi et
al5 found similar coupling patterns using instrumentation
with significantly lower error measurements.
Another variation may include the differences associated
with in vitro and in vivo specimens, an explanation
acknowledged by Panjabi et al.25 Cadaveric specimens do
not have the same postural influence associated with studies
that use subjects that maintain an intact chin and skull.
These postural differences associated with the chin and
skull may alter the movement of the upper cervical spine
into protraction and retraction movements and may affect
the coupling pattern of the upper cervical spine, specifically
at C1-2.1,25 Edmondston et al37 reported variations in global
coupling patterns during changes in upper cervical protraction and retraction and substantiated this finding.
Furthermore, the upper c-spine movement of rotation in
opposition of side flexion may be compensatory to allow
forward facing.21 This finding may be isolated to in vivo
findings secondary to muscle activity.21 Nonetheless,
variations in side flexion initiation were not wholly
associated with differences in in vivo and in vitro samples;
variation also occurred in 1 study that used cadaveric
specimens.5
The variations in C0-1 appear to be explained partially
by the movement initiated first. Cook13 reported similar
variations in coupling when side flexion was initiated during
coupling of the lumbar spine. He reported that rotation
initiation led to consistent coupling patterns among the
multiple studies investigated. Panjabi et al3,5 have recognized the influence on the initiated movement in previous
studies but have not identified a reason why this phenomenon occurs. Further investigation is needed to ascertain
why rotation initiation provides greater consistency across
studies than side flexion initiation.

Clinical Application
In most cases, apposition movements based on a
directional concept of coupling were used during manipulative procedures to lock out the segments above or below
the targeted joint. In the lower cervical spine, apposition

Journal of Manipulative and Physiological Therapeutics


September 2006

requires an isolated segmental movement in opposition to


coupled motion, subsequently, rotation and side flexion to
the opposite side. The theory behind apposition suggests
that the clinical application of a technique should be
focused toward the unopposed segment, thus allowing
targeted force toward the selected segment. In the lower
cervical spine, this concept appears consistent and may
show use for clinicians who have adopted this application
and the coupling pattern of ipsilateral side flexion and
rotation. In the upper cervical spine (C0-1 and C1-2), the
use of this concept may be applicable only for those
patients who follow the pattern advocated by the clinician
or when rotation initiation is used during application.
Moreover, a clinician should attend to the postural position
of the cervical spine when testing segmental motion and
treating limitations.

Limitations
Some studies have argued that the clinical utility of
coupling is limited for use during diagnosis because the
motions involved during coupling are very small and may be
beyond the capacity of the manual clinician to determine.13,21 Others have reported that when small amounts
of translatory motions are initiated, such as those commonly
used to btake up the slackQ during mobilization or manipulation, coupling patterns can vary from dictated norms.38
Furthermore, Panjabi et al5 reported that upper cervical spine
posture does affect coupling amount and direction, and
because the degree of postural change that does effect
coupling direction has not been verified, the ability to
standardize a position has not yet been verified. These
limitations may be outside a manual clinicians direct
influence during treatment application or diagnosis. Nonetheless, it does appear that when used judiciously within the
capabilities of a manual clinician, cervical spine coupling
directional theory may be a useful addition to clinical
examination and treatment.

CONCLUSIONS
This analysis showed that there is complete agreement
among investigations regarding the directional coupling
pattern of the lower cervical spine. The upper cervical spine
displays variations exhibiting coupling motions that are in
opposition during postural and movement initiation
changes. Future studies should investigate if manual
clinicians are able to discern selected coupling movements.
In addition, the effects of injury on coupling direction are a
worthwhile investigation. Lastly, determining whether the
use of preconceptual coupling assessment and treatment
methods positively changes the outcome of care when
compared against a patient response method would further
substantiate its use.

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