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Keywords:

  • horse;
  • cervical spine;
  • intervertebral foramina;
  • flexion and extension;
  • computed tomography

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Conflicts of interest
  9. Manufacturers' addresses
  10. References

Reasons for performing study: In dressage, the head and neck position has become an issue of concern as certain extreme positions may imply a welfare risk for the horse. In man, extension and flexion of the cervical spine cause a decrease and increase in intervertebral foramina dimensions, respectively. However, in horses, the influence of flexion and extension on foramina dimensions and its possible interference with peripheral nerve functioning remains unknown.

Objectives: To determine the effect of ex vivo flexion and extension on intervertebral foramina dimensions in the equine cervical spine.

Methods: Computed tomography was performed on 6 cadaver cervical spines from adult Warmblood horses subjected to euthanasia for reasons unrelated to cervical spine abnormalities, in a neutral position, in 20 and 40° extension, and in 20 and 40° flexion. Multiplanar reconstructions were made to obtain transverse images perpendicular to the long axis of each pair of intervertebral foramina from C2–T1. Intervertebral foramina dimensions were measured in the 5 positions.

Results: Compared to the neutral position, 40° extension caused a decrease in foramina dimensions at segments C4–C5, C5–C6, C6–C7 (P<0.001) and C7–T1 (P<0.002); 20° extension caused a decrease in foramina dimensions at segments C5–C6 (P<0.02), C6–C7 (P<0.001) and C7–T1 (P<0.01); 20° flexion caused an increase in foramen length at segment C6–C7 (P<0.01).

Conclusions:Ex vivo extension of the cervical spine causes a decrease in intervertebral foramina dimensions at segments C4–T1, similar to that found in man.

Potential relevance:In vivo extension of the cervical spine could possibly interfere with peripheral nerve functioning at segments C4–T1. This effect may be even more profound in patients with a reduced intervertebral foramina space, for example in the presence of facet joint arthrosis.


Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Conflicts of interest
  9. Manufacturers' addresses
  10. References

Enlargement of the articular processes of the cervical vertebrae in horses has been described as a cause of reduction in intervertebral foramina space (Down and Henson 2009). Clinical signs of peripheral neuropathy including localised sweating, pain, stiffness, reluctance to bend the neck and eventually forelimb lameness (Moore et al. 1992; Ricardi and Dyson 1993; Marks 1999) have been suggested to be related to this phenomenon. Electromyographic studies confirmed the existence in the horse of peripheral neuropathy caused by cervical facet joint arthrosis (Wijnberg et al. 2004, 2009). In man, a corresponding condition, also known as cervical radiculopathy, is commonly found in patients with complaints of pain in the neck and shoulder region (Abbed and Coumans 2007).

In man, many ex vivo as well as in vivo studies have been conducted to evaluate the influence of normal range of neck flexion and extension on cervical intervertebral foramina dimensions (Yoo et al. 1992; Humphreys et al. 1998; Lu et al. 2000; Muhle et al. 2001; Nuckley et al. 2002; Kitagawa et al. 2004; Ebraheim et al. 2006), local pressure on nerve roots (Schnebel et al. 1989; Farmer and Wisneski 1994; Hubbard and Winkelstein 2008) and corresponding electrophysiological findings (Sabbahi and Abdulwahab 1999; Morishita et al. 2006). The studies on intervertebral foramina dimensions documented a decrease in foramina dimensions caused by extension and ipsilateral bending and an increase caused by flexion and contralateral bending. This information proved to be helpful in the development of diagnostic as well as therapeutical interventions for cervical radiculopathy (Tanaka et al. 2006). A similar observation has been made in the horse, albeit in general terms without specific quantitative information per intervertebral junction (Denoix and Pailloux 2001).

The concern in the international dressage world about the head and neck position of the horse mainly relates to methods in which the horse is trained with an extremely flexed head and neck position. This position has historically been named ‘rollkur’ (Meyer 1992), ‘low, deep and round’ (Janssen 2003), or ‘hyperflexion’ (Jeffcott et al. 2006). Recently, a redefinition of terminology was agreed upon with the terms ‘Rollkur’ or ‘hyperflexion’ reserved for the extremely flexed position obtained in an aggressive way or with undue force and ‘low, deep and round’ indicating the same position obtained without forceful intervention (Anon 2010). Recent studies demonstrated that a change in head and neck position influences back kinematics and loading pattern of the locomotor apparatus in the unridden as well as the ridden high-level dressage horse. A flexed head and neck position induced an increase in range of motion of the thoracic and the lumbar back in the unridden horse, which implies an activated use of the hindlimbs, a better step under the horse's body and a more equally divided weight load between fore- and hindlimbs (Gómez Álvarez et al. 2006). However, the effect in the lumbar back could not be reproduced while ridden, whereas the thoracic area could not be investigated due to the saddle (Rhodin et al. 2009). An extremely elevated neck, however, caused an increase in extension of the thoracic and lumbar back in the unridden as well as in the ridden horse (Gómez Álvarez et al. 2006; Rhodin et al. 2009). An extremely elevated neck also affected the functionality of the locomotor apparatus much more than an extremely low neck, as evidenced by an increase in peak vertical forces in the forelimbs, which is a potential risk factor for injury (Weishaupt et al. 2006; Waldern et al. 2009).

To our knowledge, no in vivo or ex vivo data are available regarding the influence of flexion and extension, related to various head and neck positions used in earlier studies (Gómez Álvarez et al. 2006; Weishaupt et al. 2006; Rhodin et al. 2009; Sleutjens et al. 2009; Waldern et al. 2009), on cervical intervertebral foramina dimensions in the horse. This information could contribute to a greater understanding of the effect of training techniques regarding the head and neck position in healthy horses as well as in horses suffering from pathological conditions in the neck.

The aim of the present study was to investigate quantitatively the effect of ex vivo flexion and extension on intervertebral foramina dimensions in the healthy equine cervical spine.

Materials and methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Conflicts of interest
  9. Manufacturers' addresses
  10. References

Cervical spines

Six freshly harvested equine cadaver spines (C2–T2) were obtained from adult horses (mean ± s.d. age 15 ± 3 years; 5 Dutch Warmbloods, one Westfaler; 5 geldings, one mare) subjected to euthanasia for reasons not related to pathology of the cervical region. All the musculature, except for the Musculus multifidus cervicis and Musculus longies colli, was dissected from the specimens within 24 h after death. Care was taken not to damage the joint capsules and ligaments. The specimens were then stored at -20°C until studied.

One equine cadaver spine (C1–T13), dissected as described, was used to make 5 wooden frames to fixate the spines and simulate the desired positions. This spine was firmly anchored to a table, so that there was no movement from T6–T13. A horizontal line from the top of the spinous process of T6 until the wing of the atlas was defined as the neutral position. Then the cervical spine was flexed (20 and 40°) and extended (20 and 40°) by manual force in, respectively, a ventral-caudal and dorsal-caudal direction. The positions were defined by the previously mentioned angle in order to compare these ex vivo angles to in vivo measured head and neck positions (Sleutjens et al. 2009). In each position, the ventral line of the dissected neck was used to construct 5 wooden frames (Fig 1).

image

Figure 1. Typical example of a neck fixated in a neutral position in a wooden frame, for CT measurements in the median and transverse plane (C2–T1).

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Computed tomography

After thawing, each specimen (C2–T2) was firmly anchored to each frame. In each position, computer tomography of the cervical spine was performed with a single slice helical CT scanner (Philips Secura)1, using 120 kV, 220 mA, 1 s scanning time and 2 mm thick contiguous slices.

Measurements

Reconstructions of the original images in a median plane were used to measure the angles between adjacent cervical vertebrae in the different positions. The angle of each vertebra was defined as the measured angle between the line parallel to the bottom of the vertebral canal and the vertical running through its caudal extremity (Fig 2). The angle between adjacent vertebrae was calculated by subtracting adjacent angles, for example the angle of C3 minus the angle of C2.

image

Figure 2. Typical example of a median CT image of the cervical spine (C2–T2) in the neutral position. Vertical line at C4; the angle between the line parallel to the bottom of the vertebral canal and the vertical running through the caudal extremity is measured for C4. Oblique line at segment C5–C6, defines the transverse plane; from the caudal extremity of the vertebral arch of the cranial vertebra to the vertebral head of the caudal vertebra for C5–C6.

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Multiplanar reconstructions were made to obtain images of each vertebral transition in a transverse plane, running from the caudal extremity of the vertebral arch of the cranial vertebra to the vertebral head of the caudal vertebra (Fig 2). From these transverse images the smallest height of each intervertebral foramen was measured between the articular process of the cranial vertebra and the vertebral body of the caudal vertebra, using commercially available software (ImageJ)2 (Fig 3). The length of each intervertebral foramen was calculated from the number of images on which the foramen was visible multiplied by the thickness of the slices (2 mm).

image

Figure 3. Typical example of how intervertebral height was measured between the articular process of the cranial vertebra and the vertebral body of the caudal vertebra in the transverse plane, created as illustrated in Figure 2.

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Statistical analysis

Statistical analysis was performed with software analysis packet R version 2.8.1. Data were considered as continuously dependent data with horse as the experimental unit. Changes resulting from the different positions were assessed by pair wise comparisons. Models were tested by comparing the maximum of likelihoods. Differences were tested in a full 2-way factorial mixed linear model with random intercept and segment as random slope. Normality was tested by plotting the residuals in a P-P plot. Regression analysis was performed with a general linear model. Significance level was set at *P<0.05 or **P<0.001 after post hoc Bonferroni correction. Means are expressed as ± s.d.

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Conflicts of interest
  9. Manufacturers' addresses
  10. References

Angles between adjacent cervical vertebrae

Compared to the neutral position, extension of 40° caused a more positive angle between adjacent vertebrae C4–C5, C5–C6, C6–C7 and C7–T1 (P<0.001). Extension of 20° caused a more positive angle between adjacent vertebrae C5–C6, C6–C7 and C7–T1 (P<0.001). Flexion of 20° caused a more negative angle between adjacent vertebrae C2–C3 (P<0.044), flexion of 40° did not cause significant differences (Table 1).

Table 1. Mean ± s.d. of ex vivo angles between adjacent cervical vertebrae measured in the median plane, as illustrated in Figure 2 (n = 6)
 C2–C3C3–C4C4–C5C5–C6C6–C7C7–T1
  • *

    Statistical significance P<0.05,

  • **

    P<0.001, including Bonferroni post hoc correction.

Extension 40°−11.0 ± 5.9−12.3 ± 3.4−0.8 ± 4.5**6.2 ± 3.4**13.0 ± 4.6**25.3 ± 5.2**
Extension 20°−8.8 ± 8.7−15.8 ± 3.4−15.3 ± 1.5−2.7 ± 5.6**7.7 ± 8.2**23.5 ± 5.4**
Neutral−15.0 ± 5.5−17.7 ± 3.4−18.3 ± 2.1−13.2 ± 3.1−6.5 ± 6.18.0 ± 6.8
Flexion 20°−7.8 ± 9.1*−14.8 ± 5.0−21.0 ± 3.6−14.7 ± 2.6−11.0 ± 3.52.3 ± 4.0
Flexion 40°−9.8 ± 8.8−18.5 ± 3.6−17.0 ± 1.8−14.7 ± 2.3−11.2 ± 4.33.8 ± 4.1

Compared to 40° extension, flexion of both 20 and 40° caused a more negative angle between adjacent vertebrae C4–C5, C5–C6, C6–C7 and C7–T1 (P<0.001). Compared to 20° extension, flexion of both 20° and 40° caused a more negative angle between adjacent vertebrae C5–C6, C6–C7 and C7–T1 (P<0.001). Extension of 40° caused a more positive angle between adjacent vertebrae C4–C5 (P<0.001) and C5–C6 (P<0.0072) than 20° of extension (Table 1).

Intervertebral foramina height

In the neutral position foramina height was greatest at C6–C7 and decreased both cranially and caudally. Compared to the neutral position, extension of 40° caused a decrease in foramina height at segments C4–C5, C5–C6, C6–C7 and C7–T1 (P<0.001). Extension of 20° caused a decrease in foramina height at segments C5–C6 (P<0.016), C6–C7 and C7–T1 (P<0.001). The most profound effect on height was seen at segment C6–C7 (Table 2). Compared to the neutral position, flexion caused no statistical significant effect on foramina height.

Table 2. Mean ± s.d. of ex vivo intervertebral foramina height (mm), measured in the transverse plane as illustrated in Figure 3 (n = 6)
 C2–C3C3–C4C4–C5C5–C6C6–C7C7–T1
  • *

    Statistical significance P<0.05,

  • **

    P<0.001, including Bonferroni post hoc correction.

Extension 40°11.1 ± 3.611.6 ± 1.88.6 ± 1.3**7.2 ± 2.6**7.5 ± 2.1**10.2 ± 3.3**
Extension 20°11.4 ± 3.713.7 ± 3.114.9 ± 2.211.9 ± 3.3*8.6 ± 3.9**11.2 ± 2.8**
Neutral10.3 ± 3.413.6 ± 4.215.3 ± 2.915.7 ± 1.919.9 ± 5.817.5 ± 3.8
Flexion 20°10.9 ± 4.514.0 ± 3.816.2 ± 3.017.6 ± 3.018.4 ± 4.519.7 ± 4.4
Flexion 40°11.1 ± 4.014.6 ± 2.915.4 ± 2.617.9 ± 3.123.1 ± 8.320.4 ± 4.0

Compared to 40° of extension, flexion of both 20 and 40° caused an increase in foramina height at segments C4–C5, C5–C6, C6–C7 and C7–T1 (P<0.001). Compared to 20° of extension, flexion of both 20 and 40° caused an increase in foramina height at segments C5–C6, C6–C7 and C7–T1 (P<0.001). Extension of 40° caused a greater decrease in foramina height at segments C4–C5 (P<0.001) and C5–C6 (P<0.002) than 20° of extension. Flexion of 40° caused a greater increase in foramina height at segment C6–C7 (P<0.002) than 20° of flexion (Table 2).

Intervertebral foramina length

In the neutral position foramina length was greatest at C7–T1 and decreased cranially.

Compared to the neutral position, extension of 40° caused a decrease in foramina length at segments C4–C5, C5–C6, C6–C7 (P<0.001) and C7–T1 (P<0.002). Extension of 20° caused a decrease in foramina length at segments C5–C6 (P<0.011), C6–C7 (P<0.001) and C7–T1 (P<0.01). Flexion of 20° caused an increase in foramina length at segment C6–C7 (P<0.01). The most profound effect on length was seen at segment C6–C7 (Table 3).

Table 3. Mean ± s.d. of ex vivo intervertebral foramina length (mm), measured in the transverse plane (n = 6)
 C2–C3C3–C4C4–C5C5–C6C6–C7C7–T1
  • *

    Statistical significance P<0.05,

  • **

    P<0.001, including Bonferroni post hoc correction.

Extension 40°36.6 ± 5.637.0 ± 5.435.8 ± 1.6**35.0 ± 2.3**34.0 ± 3.9**40.5 ± 3.6*
Extension 20°38.5 ± 4.838.3 ± 4.440.0 ± 2.837.5 ± 2.4*34.6 ± 3.0**40.0 ± 5.2*
Neutral36.8 ± 5.438.7 ± 4.940.3 ± 2.840.6 ± 2.740.2 ± 4.344.1 ± 3.7
Flexion 20°36.1 ± 6.839.5 ± 4.941.3 ± 3.041.0 ± 2.943.2 ± 5.0*45.2 ± 4.2
Flexion 40°37.8 ± 5.838.7 ± 5.540.5 ± 3.040.8 ± 3.141.7 ± 5.245.3 ± 3.8

Compared to 40° of extension, flexion of both 20° and 40° caused an increase in foramina length at segment C4–C5, C5–C6, C6–C7 and C7–T1 (P<0.001). Compared to 20° of extension, flexion of both 20° and 40° caused an increase in foramina length at segment C5–C6 (P<0.003, P<0.005, respectively), C6–C7 (P<0.001) and C7–T1 (P<0.002, P<0.001, respectively). Extension of 40° caused a greater decrease in foramina length at segment C4–C5 (P<0.001) than 20° of extension. There was no significant difference in foramina length between 20° and 40° of flexion (Table 3).

Regression analysis demonstrated a significant correlation between intervertebral foramina height and length at segment C4–C5 of r2= 0.38 (P<0.001), C5–C6 of r2= 0.34 (P<0.001) and C6–C7 of r2= 0.41 (P<0.001) (Fig 4).

image

Figure 4. Regression analysis between intervertebral foramina length and height for segments C4–T1.

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Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Conflicts of interest
  9. Manufacturers' addresses
  10. References

The present study demonstrates that compared to the neutral position, extension of the equine cervical spine causes a significant decrease in intervertebral foramina dimensions at segments C4–T1. Furthermore, compared to the extended positions, flexion of the spine causes a significant increase in intervertebral foramina dimensions at segments C4–T1. These results are in concurrence with human studies (Yoo et al. 1992; Humphreys et al. 1998; Lu et al. 2000; Muhle et al. 2001; Nuckley et al. 2002; Kitagawa et al. 2004; Ebraheim et al. 2006).

The lower cervical segments C4–T1 were shown to be mainly responsible for the total amount of flexion and extension in the equine cervical spine, which is consistent with findings by others (Clayton and Townsend 1989). A possible explanation for this phenomenon is that the caudal facet joints have a progressively more medial orientation, which is associated with an increase in the range of movement (Clayton and Townsend 1989). In this study, the extended positions had a greater effect on the angle between adjacent vertebrae and on intervertebral foramina dimensions than the flexed positions. This could be caused by the definition of the neutral position in which the cervical spine was already somewhat extended. It would have been more accurate to define the neutral position as a horizontal line between the transverse process of T1 and the wing of the atlas. However, the aim to relate these ex vivo positions to in vivo measured angles made it necessary to use the angle between the spinous process of T6 and the wing of the atlas and to use a maximum of 40° of flexion and extension. Additionally, we compared the flexed to the extended positions to demonstrate that flexion did indeed cause an increase in intervertebral foramina dimensions.

To place the specimens accurately in the frames, it was necessary to remove most of the surrounding muscles. This, together with the fact that we simulated flexion and extension by manual force, must be kept in mind when relating the results to the in vivo situation. However, human studies performed on intervertebral foramina dimensions, showed comparable results between ex and in vivo studies (Yoo et al. 1992; Humphreys et al. 1998; Lu et al. 2000; Muhle et al. 2001; Nuckley et al. 2002; Kitagawa et al. 2004; Ebraheim et al. 2006). Other soft tissue structures, such as the intervertebral discs, were not taken into account. These were deemed to be of no particular importance for the present study because, although they can admittedly influence the intervertebral angles, they will have no direct effect on foramen size.

The results of this ex vivo study suggest that an increase in extension of the healthy equine cervical spine could have an effect on the functionality of the cervical nerve roots at segment C4–T1. In patients with a reduced intervertebral foramina space, for example in the presence of facet joint arthrosis, or in case of a cervical intervertebral disk prolapse (Jansson 2001) this effect could be even more profound. Flexion on the other hand may, through the opening of the intervertebral foramina, help in relieving pain from possible constrictions or irritations in the area, as observed earlier by Denoix and Pailloux (2001).

In horses, symptoms similar to human patients suffering from cervical radiculopathy, e.g. forelimb lameness unrelated to primary forelimb pain in combination with neck pain and scapular muscle atrophy, have been documented in association with radiographic abnormalities of the cervical vertebrae (Ricardi and Dyson 1993; Marks 1999). Additionally, Moore et al. (1992) documented intervertebral foramina impingement on nerve roots, using post mortem contrast-enhanced computed tomography. More recent studies using electromyography (EMG) demonstrated the association between peripheral neuropathy and cervical facet joints arthrosis seen on radiography (Wijnberg et al. 2004, 2009).

Human cervical radiculopathy is a commonly found condition that usually results from compression and inflammation of the cervical nerve root or roots at or near the intervertebral foramen (Abbed and Coumans 2007). The cause of pain due to cervical radiculopathy is usually multifactorial. It is generally thought that, in addition to mechanical compression, ischaemic change within or around the neural tissue, leading to local axonal inflammation and degeneration, is important in the development of pain (Kitagawa et al. 2004).

Nerve root compression results from the interplay between the foramina dimensions, nerve root size and location of the nerve root within the intervertebral foramen. The dorsal root ganglions are the largest neural structures in the cervical spine other than the spinal cord. In man, it is known that the position of the dorsal root ganglions can vary among spinal levels and individuals. This implies that intervertebral foramina stenosis cannot be diagnosed using only intervertebral foramina dimensions and that the critical dimensions of the intervertebral foramen may vary among levels and individuals (Kitagawa et al. 2004).

In conclusion, our study demonstrated that extension and flexion of the neck cause a decrease and increase in foramina dimensions in the lower C4–T1 equine cervical spine, respectively, as measured in transverse slices, with the most extreme effect seen at segment C6–C7. In our opinion, these results offer new possibilities for further, in depth neuromuscular research, which will add to our understanding of the effect of head and neck position in healthy horses as well as in patients with cervical facet joint arthrosis.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Conflicts of interest
  9. Manufacturers' addresses
  10. References

The authors acknowledge the technical assistance of Arend Schot and of the clinical assistants of the Department of Equine Sciences and of the Division of Imaging, Department of Companion Animal Sciences.

Manufacturers' addresses

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Conflicts of interest
  9. Manufacturers' addresses
  10. References

1 Philips Secura, Philips N.V., Eindhoven, The Netherlands.

2 National Institute of Health, Bethesda, Maryland, USA.

References

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Conflicts of interest
  9. Manufacturers' addresses
  10. References
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