AAEP 360° Pain in the Neck / 2016

Functional Anatomy and Clinical Biomechanics of the Equine Cervical Spine Kevin K. Haussler, DVM, DC, PhD, DACVSMR  Author’s address — Gail Holmes Equine Orthopaedic Research Center, Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO 80523; e-mail: [email protected]. Take Home Message - There has been a greater awareness of the role of neck pain and dysfunction in athletic performance across equine disciplines. To better understand how to manage these issues and to differentiate clinical signs of forelimb lameness originating from the lower cervical spine versus the forelimb itself, a working knowledge of structural and functional relationships of the cervical region and cervicothoracic junction is needed.

I. INTRODUCTION The neck forms an important component of the axial skeleton, especially for ridden exercise, as it forms the connection between the rider’s hands and the horse’s head and the rider’s seat and leg contact with the horse’s trunk. A basic understanding of the functional anatomy and biomechanics of the neck and cervicothoracic junction is needed for practitioners to diagnose, treat and provide training recommendations for horses with neck injuries or to optimize sport horse performance. The structural and functional contributions of individual vertebral anatomical features to segmental mobility or stability need to be fully recognized and understood to direct diagnostic and therapeutic approaches in affected horses. The effects of induced head and neck positions on local tissues, upper airway dynamics, regional spinal biomechanics, and overall locomotion patterns is an area of active research.1-3 The short-term effects of different head and neck positions on measures of performance and equine welfare has been recently evaluated; however, the long-term effects of extreme head and neck positions in flexion (rollkur) or prolonged elevation in extended head and neck positions are not currently known. The following material presents the structural and functional relationships in local anatomical features of the cervical vertebrae, regional influences of the cervical musculature and nuchal ligament, and systemic effects of induced head and neck positions related to the etiology, diagnosis and management of clinical issues.

II. STRUCTURE-FUNCTION OF THE CERVICAL VERTEBRAL COLUMN The cervical spine consists of a long bony column that is cantilevered from the trunk of the body with a complex support system of passive and active structural and functional elements that provide a stable foundation for head positioning and its associated physiologic processes.4 The neck is formed by a series of flexible linkages consisting of seven cervical vertebrae that are highly modified structures in upper cervical region to support fine motor movements of the head (Fig. 1). Head positioning is critical to a large range of behaviors that include: visual and auditory orientation, balance, feeding, grooming, defense, locomotion, and lameness adaptations.5 Large ranges of joint motion occur within the cervical region, which are a result of specific anatomic features. These include the ball and socket shape of the vertebral body extremities, wide intervertebral disks, the size, shape and orientation of the articular facets, rudimentary spinous processes, large bifid transverse processes for enhanced muscle attachment, and the presence of a highly elastic nuchal ligament to support large ranges of head and neck movements instead of the fibrous supraspinous or interspinous ligaments that restrict segmental mobility within other spinal regions (Fig. 2).6 A working knowledge of the specific anatomical features and their function within the cervical region greatly enhances diagnostic capabilities and provides the opportunity to create focused treatment and rehabilitation plans within individual horses.

III. VERTEBRAL CANAL AND INTERVERTEBRAL FORAMEN The cervical vertebrae contain a central vertebral canal for passage of the spinal cord and intervertebral foramina laterally for transmission of spinal nerves to the peripheral tissues (Fig. 2). Neck position affects the cervical spinal cord and spinal nerves. Short-term changes of neural and muscular function have been identified with maximum flexion of the head and cranial neck.7 Laterolateral radiographs of the cervical vertebrae are reported to be inaccurate in determining the site of spinal cord lesions.8 This is most likely due to predominant dorsolateral narrowing of the vertebral canal during induced flexion-extension (and much less direct dorsoventral narrow-

AAEP 360° Pain in the Neck / 2016 combined neck pain and forelimb lameness.10 However, recent evidence suggests that this is an oversimplified explanation and other biomechanical features (e.g., induced head and neck positions) and neuromuscular influences related to neck pain and proprioception are likely more relevant issues.3,11

IV. INTERVERTEBRAL ARTICULATIONS

Fig. 1. Lateral view of the cervical and cranial thoracic vertebrae (C1-T3).

The cranial vertebral body is convex in shape and the caudal vertebral body is concave (Fig. 3). Therefore, most equine intervertebral joints resemble shallow ball-and-socket configurations, which provide joint stability without restricting vertebral mobility. Ligamentous tissues that connect adjacent vertebrae include the combination of fibrocartilaginous intervertebral disks, fibrous joint capsules and elastic ligamentum flava. The ligamentum flavum consist of elastin and interconnects the lamina of adjacent vertebrae. In horses with dynamic cervical instability, the ligamentum flavum is reported to be hypertrophied and contribute to spinal cord compression during extension of the cervical spine.12 The occiput-C1-C2 joint complex is specialized and has the typical intervertebral disks replaced by a single contiguous synovial articulation. The cervical intervertebral disks in horses consist of strong, annular fibers, but lack a well-developed nucleus pulposus. This configuration produces relatively thinner but stronger intervertebral disks, compared to other species. Horses have a much lower prevalence of spinal cord injury due to herniated disk material, compared to dogs or humans. The stiffness of the equine cervical spine is dependent on the direction of the loading and is 2-7 times less stiff than the thoracolumbar vertebral column.13 Within the cervical spine, mean dorsoventral stiffness is 297 ± 135 N/m in flexion, 1347 ± 2083 N/m in extension, and 421 ± 164 N/m in lateral bending, which has implications in applying joint mobilization techniques and in assessing neck pain and stiffness in horses.

Fig. 2. Craniocaudal view of a transverse cross-section of the cervical spine at the level of the C3-C4 intervertebral articulation.

ing); thereby, partially explaining the under-representation of vertebral canal and subsequent spinal cord compression visualized on laterolateral radiographs or myelograms. Spinal nerve root compression and inflammation results from the interplay of the intervertebral foraminal dimensions, nerve root size, and the location of the nerve root within the individual intervertebral foramen. Extension of the equine cervical spine causes a significant decrease in intervertebral foramina dimensions through C4–T1, compared to the neutral position.9 Conversely, neck flexion causes a significant increase in intervertebral foramina dimensions at segments C4–T1, with the largest dimensional changes at C6-C7. These effects may be more profound in patients with reduced intervertebral foramina space, for example in the presence of cervical facet osteoarthritis.9 Direct compression or inflammation of the lower cervical nerves that contribute to the brachial plexus are often thought to be the primary etiology of horses with

Fig. 3. Lateromedial view of a sagittal section of the cervical spine at the level of the C3-C4-C5 intervertebral articulations. Cranial is toward the left.

AAEP 360° Pain in the Neck / 2016

V. SYNOVIAL ARTICULATIONS The articular processes support both vertebral stability and mobility due to deeply-interlocking articular surfaces. The size, shape, and orientation of the cervical articular facets and the functional status of these articulations determine the amplitude and direction of segmental vertebral motion. Regional spinal motion is due to the cumulative effects of small amounts of individual segmental vertebral motion. In the cervical vertebral region, the articular surfaces lie at approximately 45 to horizontal and allow large ranges of flexion-extension and lateral bending (Fig. 4).14 A fibrous joint capsule surrounds the synovial articulations located on the articular processes. The cervical vertebral joint capsules contain craniocaudal and dorsoventral outpouches, which have diagnostic and clinical relevance. The cranial and caudal outpouches are the largest (11.3 ± 1.9 mm and 7.8 ± 2.1 mm, respectively), which provide the best sites for synoviocentesis and direct visualization of the joint capsule.15 The dorsolateral outpouch is smaller (3.7 ± 0.7 mm) and has overlying multifidi muscle attachments.15,16 The average volume of the cervical joint capsule is 3 ml and protrudes ventromedially into the spinal canal about 2.7 ± 0.6 mm, but does not come into contact with the dura mater in normal horses, even during induced cervical flexion.15 In the absence of any other soft tissue or bony changes, any cervical joint effusion is unlikely to cause spinal cord compression. Folds of synovial membrane (i.e., synovial folds) have been identified in the cranial and caudal aspects of the cervical synovial articulations.17 The width of the synovial folds is 25.4 mm (range 4.0 to 41.1 mm) and the height is 5.6 mm (range 1.0 to 17.8 mm). Awareness of the presence, location and size of the synovial folds is important with the development of advanced diagnostic imaging modalities (e.g., CT and MRI). The size of the synovial folds indicates that the structures could be damaged by injection, acute injury or chronic disease.18 Histologically, 38% of the synovial folds are of adipose type and localized more to the cranial joint capsule; 41% of fibrous type localized to the caudal joint capsule; and 21% of mixed fibroadipose tissues.17 The synovial folds contain nociceptive nerve fibers, which make them clinically relevant as a potential source of noxious stimuli with entrapment or inflammation.19

VI. NUCHAL LIGAMENT The nuchal ligament is a specialized structure in horses that aids in supporting the heavy head and upper cervical vertebrae in both stance and locomotor activities.5 The nuchal ligament consist of a funicular (thick cord) portion dorsally and a laminar (thinner sheet) portion that extends ventrally to attach to the C2C4 dorsal spinous processes within the cervical region. Early depictions and most of the existing equine anatomic textbooks incorrectly illustrate the laminar portion with attachments on the C5-C6-C7 spinous processes.20 During locomotion, the neck stores elastic energy within the passive tissues such as ligaments, joint capsules and fasciae. The nuchal ligament has a high elastin content that contributes to 55% of the work of moving the head and neck at the walk, 33% at the trot, and 31% at the canter.5 Induced head and neck positions appear to either

unload certain portions of the nuchal ligament or overload the attachments at the caudal occiput and C2 dorsal spinous process, which may have implications in enthesis formation and head tossing behaviors.21

Fig. 4. Caudal view of the sixth cervical vertebra (C6). Note the rudimentary dorsal spinous process (white arrow), angulation of the articular surfaces (black lines) and the large bifid transverse processes.

VII. CERVICAL MUSCULATURE The cervical vertebrae are surrounded by a large mass of muscles, which makes direct bony palpation and physical examination challenging (Fig. 2). The intrinsic muscles of the cervical region and cervicothoracic junction include superficial muscles with long, parallel fibers that contribute to general neck movements and a series of deep paraspinal muscles with short, pennate fibers that stabilize individual intervertebral joints and provide postural control.16 The epaxial cervical musculature has multiple functional capabilities such as head positioning, static and dynamic postural support, and damping locomotor oscillations associated with the impact of the ground reaction forces.5 Extrinsic muscles of the cervical region are characterized as having attachments spanning from the neck to adjacent body regions, which include muscles for mandibular and head movements, forelimb attachment and motion, cervicothoracic stability, and sternal and rib attachments. The better understanding of the musculature interactions that occur with forelimb lameness and neck pain is needed to improve diagnostic and treatment approaches in this region.

VIII. SPINAL KINEMATICS The three-dimensional kinematics of the cervical vertebrae include primary flexion-extension joint movements, with

AAEP 360° Pain in the Neck / 2016 lateral bending and axial rotation as secondary movements.14,22 The atlantooccipital (Occ-C1) articulation supports vertical motion within the sagittal plane (i.e., nodding the head in a ‘yes’ motion). Combined ranges of flexion and extension are 86º, which accounts for 32% of the total cervical range of motion in flexion-extension.14 Combined ranges of left and right lateral bending at the atlantooccipital articulation are 88º, which are limited by the impingement of the paracondylar processes of the occipital bone and the lateral arch of the atlas. The amount of lateral bending is greater when the atlantooccipital joint is extended, compared to when flexed.14 The atlantoaxial joint forms a unique articulation; characterized by a pivot joint that supports a large amount of axial rotation (i.e., shaking the head in a ‘no’ motion) within the transverse plane. The combined ranges of left and right axial rotation are 108º, which accounts for 73% of axial rotation within the cervical region.14 The large ranges of joint motion within the upper cervical region support the gyroscopic-like motion of the head and orientation of the visual and vestibular systems. The primary joint motions of C2T2 include flexion-extension and lateral bending. The articular facets are placed wider and oriented progressively more vertical within the C2 to C7 vertebrae, which support a gradual increase in combined flexion and extension from 21º to 32º and increase in lateral bending from 25º to 45º.14 In foals, the total amount of flexion-extension is 22%; lateral bending is 19% and the axial rotation is 17% higher than the overall cervical range of motion measured in adult horses.22 Knowledge of segmental joint ranges of motion is required to assess restricted joint motion and to preform joint mobilization techniques.

the articular facets undergo maximal overlap and form a closedpack position. The vertebral canal widens between the lamina of the leading vertebra and the cranial extremity of the trailing vertebra. The height of the intervertebral foramen decreases, which reduces the space for the intervertebral foramen contents (Fig. 5). The nuchal ligament and epaxial cervical muscles undergo shortening which induces extension of the cervical and thoracolumbar spine.6 The most common site for impingement of the thoracic dorsal spinous processes is the saddle region (i.e. T12 to T17). Altering a horse’s head and neck position affects the interspinous spaces between the thoracic dorsal spinous processes. A low head and neck position increases intervertebral distances between T8 to T15 dorsal spinous processes; whereas, a high head and neck position has the opposite effect.23 Interspinous space widths within the thoracic region decrease from cranial to caudal with intermediate head and neck positions.

A

IX. BIOMECHANICS OF CERVICAL FLEXION Flexion within the lower cervical region causes the caudal extremity of the leading vertebra to slide ventrally, relative to the cranial extremity of the trailing vertebra.6 A shear force is applied to the intervertebral disk and tension is produced within the joint capsules of the articular processes as the opposing surfaces of the articular facets are distracted. The vertebral canal is narrowed between the lamina of the leading vertebrae and the cranial extremity of the trailing vertebra. The height of the intervertebral foramen is increased (Fig. 5). The nuchal ligament and epaxial cervical muscles undergo lengthening. Lowering the neck places the nuchal ligament under increased tension and because of its attachment on the thoracic spinous processes, induces separation of dorsal spinous processes and elevation of the thoracic region.6 Knowledge of vertebral segment biomechanics is needed for development of focused rehabilitation programs in horses with neck pain and dynamic forms of spinal cord compression or instability.

X. BIOMECHANICS OF CERVICAL EXTENSION Extension of the lower cervical region causes the caudal extremity of the leading vertebra to slide dorsally, relative to the cranial extremity of the trailing vertebra. A reverse shear force is applied to the intervertebral disk. The joint capsules of the articular processes are relaxed as the opposing surfaces of

B Fig. 5. Lateral view of the C3-C4 vertebral segments during induced segmental flexion (A) and extension (B). Note the translation of the articular surfaces and changes in the intervertebral foramen dimensions (white arrow).

XI. STATIC HEAD AND NECK POSITIONS In horses, the cervical vertebral column forms a S-shaped structure with one inflection in the upper cervical region (C1C2-C3) and the other near the cervicothoracic junction (C6-C7T1-T2). Across vertebrates, the general orientation of the cervical vertebral column is vertical when animals are at rest, and not horizontal or oblique as suggested by the external appearance of the neck (Fig. 6).24 The vertical orientation of

AAEP 360° Pain in the Neck / 2016 the cervical vertebral column is interpreted to provide a stable and energy-saving balance of the head. At rest, quadrupeds hold the atlantooccipital joint in flexion and when the head is lowered or raised, the atlantooccipital and cervicothoracic junctions are predominantly involved, while the entire cervical column largely preserves its intrinsic sigmoid-shaped configuration.25

A

Fig. 6. Location of cervical transverse processes (C1-C6) during elevated (A), neutral (B), and lowered (C) head and neck positions.

XII. DYNAMIC HEAD AND NECK MOVEMENTS DURING LOCOMOTION The head and neck appears to be an essential element of equine gait mechanisms due to different characteristic oscillations at the walk, trot, and gallop that are closely linked to the movement patterns of the trunk and limbs.5 At the walk, canter, and gallop, the horse moves its head and neck to a greater extent than at trot, where the head and neck position is more constant.2 During body movements at stance and locomotion, the head and neck provide a major craniocaudal and lateral balancing mechanism employing input from the visual, vestibular, and proprioceptive systems.26 Stability and position of the head support the vestibular apparatus and help to hold the visual field in a horizontal plane. The cervical joint capsules and muscles contain mechanoreceptors that are important in maintaining stable head and neck positions for overall balance, coordination, and motor control during locomotion.27 With added weight associated with ridden exercise, the natural biomechanical response is head and neck elevation, trunk extension, forelimb protraction, and hind limb retraction postures.28

XIII. INDUCED HEAD AND NECK POSITIONS DURING RIDDEN EXERCISE

B

C

Human preferences for head and neck postures in horses are often based on esthetics and ease of training and often include accentuated head and neck flexion.29 Different head and neck conformations have been selected for across horse breeds and disciplines presumably due to advantages for certain types of work or inducing specific gait characteristics. Collection is associated with increased stride duration and fore- and hind limb stance duration while speed and stride length are usually reduced. The idea behind raising the neck and head is to create a greater degree of elevation by redirecting the horizontal movement towards a more vertical direction.3 It is proposed that elevation of the head and neck allows a more effective transfer of propulsive forces from the hindquarters to the trunk.3 However, among riders it is often claimed that back activity is improved by lowering the head and neck. The opposing orientation of the head and neck to that of the traditional approach implies a different balance between forehand and hindquarters. An increased prevalence of extreme neck flexion acquired through rein tension has been reported in both dressage and Western pleasure training methods. Dressage horses are commonly ridden during warm-up for competitions with their nasal plane behind the vertical.30 It is hypothesized that overflexion of the head and neck maximize control of the horse’s movement, induces trunk elevation, and may aid in training new movements. The short-term effects of induced head and neck positions have been recently evaluated by several researchers (Table 1), compared to an unrestrained head and neck position. In general, it seems that the height of the neck positioning influences movement within other body regions more than the present or absence of poll flexion. Extreme

AAEP 360° Pain in the Neck / 2016 positions induce more changes than the less extreme positions.31 It is unknown what the long-term consequences of these exaggerated head and neck positions are related to joint physiology, vestibular mechanisms, motor control, and general equine welfare.

XIV. CONCLUSION

function. Increased knowledge of these structural and functional relationships will help the equine practitioner to better manage horses with neck pain and dysfunction. Any induced head and neck position has measurable effects on trunk and limb function. Awareness of these influences will help to guide rehabilitation and training recommendations across athletic disciplines.

Specific anatomic features of the cervical vertebrae have direct biomechanical and clinical influences on neck mobility and

Table 1. The Effects of Elevated and Flexed Head and Neck Positions During Unridden and Ridden Exercise at Different Gaits on Other Body Regions or Systems

Induced Head and Neck Positions Parameter

Elevated

Neutral

Flexed

At stance, thoracic interspinous spaces23

Significant narrowing of interspinous spaces

Reference

Significant widening of interspinous spaces

Unridden, at walk, thoracolumbar kinematics31

Increased trunk extension; increased lumbosacral flexion

Increased thoracic flexion

Increased trunk flexion; increased lumbosacral extension

Unridden, at trot, thoracolumbar kinematics31

Increased trunk extension; decreased lateral bending and axial rotation; decreased intervertebral symmetry

Reference

Increased thoracic and lumbosacral extension

Unridden, at walk, hind limb kinematics31

Decreased hind limb protraction (increased hind limb retraction)

Reference

Increased hind limb protraction

Unridden, at walk, horse comfort31

Most uncomfortable position

Reference

Unridden, walk, on a treadmill, limb kinetics32

Largest effect on limb timing and load distribution; weight shift to the hind limbs; decreased forelimb vertical impulse, decreased stride length

Decreased forelimbs peak vertical force

Weight shift to the hind limbs

Unridden, trot, on a treadmill, limb kinetics32

Decreased forelimb stance duration; increased forelimb peak vertical force; decreased forelimb vertical impulse

Reference

Decreased forelimb vertical impulse

Ridden, at walk, thoracolumbar kinematics2

Increased trunk extension; increased mid-thoracic lateral bending; decreased axial rotation

Reference

Increased trunk flexion; decreased mid-thoracic lateral bending

Ridden, at walk, stride parameters2

Decreased stride length; decreased hind limb protraction and retraction

Increased stride length

Intermediate stride length

Ridden, at walk, on treadmill, limb kinetics3

Largest effects; decreased stride duration; increased hind limb impulse

Reference

Fewer effects

Ridden, at trot, thoracolumbar kinematics2

Decreased mid-thoracic flexionextension

Reference

Ridden, at trot, stride parameters2

Stride length is independent of head position

Reference

Stride length is independent of head position

AAEP 360° Pain in the Neck / 2016 Ridden, at trot, on treadmill, limb kinetics3

Largest changes; increased hind limb forces; increased stride duration

Reference

Ridden, walk and trot, on treadmill, limb timing3

Largest changes; clear effect on the horse's movement patterns

Reference

Increased stride duration

Ridden, at extended trot, thoracolumbar kinematics33

Inconsistent effects; increased lumbar extension, increased vertical excursion of trunk

Reference

Inconsistent effects

Ridden, at extended trot, stride parameters.33

Inconsistent effects; increased hind limb flexion

Reference

Inconsistent effects

Nuchal ligament biomechanics21

Nuchal ligament is unloaded

Fully supports elastic properties

Induces excessive stretching of some portions of the nuchal ligament

Nuchal ligament modeling34

Decreased loading at C2 attachment

Loading is largest at C2 attachment

Largest loading at all attachment sites

Neck muscle activity (EMG)35

Splenius and trapezius muscles are activated

Highest activity of splenius and trapezius muscles

Increased brachiocephalicus muscle activation; reduced splenius and trapezius muscle activation

Neuromuscular transmission in neck muscles7

Increased motor unit action potential amplitudes, suggests recruitment of larger motor units and is indicative of increased workload

No significant changes after exercise

Pathological spontaneous activity in motor unit action potentials after exercise, suggesting delayed neuromuscular transmission

Muscle enzymes7

Increased lactate dehydrogenase (LDH) 4 hours post exercise; >2fold increase in creatine kinase (CK) activity

Reference

Largest and longest measurable increase in lactate dehydrogenase (LDH), 4 hours post exercise; >2fold increase in creatine kinase (CK) activity

Reference

Increased intrathoracic pressure during exercise

Intrathoracic pressure during exercise36 Pharyngeal diameter37

No consistent correlation found

Largest diameter

No consistent correlation found

Pharyngeal diameter1

Decreased pharyngeal diameter with poll flexion (head position)

Largest diameter

Increased pharyngeal diameter with poll extension (head position)

Pharyngeal diameter1

Neck position was less important

Reference

Neck position was less important

Welfare issues38

Increased conflict behavior; negative anticipation; increased saliva cortisol 5 and 30 min after exercise; increased heart rate variability

Reference

Negative anticipation, increased heart rate variability

REFERENCES

ACKNOWLEDGMENTS 1. Declaration of Ethics Authors have adhered to the Principles of Veterinary Medical Ethics of the AVMA.

2.

Conflict of Interest

3.

The Author declares no conflicts of interest.

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AAEP 360° Pain in the Neck / 2016 36. Sleutjens J, Smiet E, van Weeren R, et al. Effect of head and neck position on intrathoracic pressure and arterial blood gas values in Dutch Warmblood riding horses during moderate exercise. Amer J Vet Research 2012;73:522-528. 37. Go LM, Barton AK, Ohnesorge B. Pharyngeal diameter in various head and neck positions during exercise in sport horses. BMC Vet Res 2014;23:117. 38. Smiet E, Van Dierendonck MC, Sleutjens J, et al. Effect of different head and neck positions on behaviour, heart rate variability and cortisol levels in lunged Royal Dutch Sport horses. Vet J 2014;202:26-32.