Intervertebral disk disease (IVDD) is the most common spinal disease that results in neurological dysfunction in dogs.1,2 Hansen Type 1 IVDD, common in chondrodystrophic dog breeds, is characterized by chondroid metaplasia of the nucleus pulposus (NP). Extrusion of NP into the vertebral canal causes compression and/or contusion of the spinal cord and subsequent neurological dysfunction.3,4 Fenestration is a surgical technique that involves the complete mechanical removal of NP by making a window in the annulus fibrosus and is described as a prophylactic procedure to reduce reoccurrence of IVD extrusion (IVDE).3,5
Multiple veterinary studies strongly support the prophylactic effect of fenestration in dogs with previous episodes of symptomatic IVDE.3,6,7 Published information suggests reoccurrence rates of 0% to 24.4% with prophylactic disk fenestration8–13 and 2.67% to 41.7% without fenestration.10,12,14–17 With around 90% of IVDEs predictably occurring between T13 and L3,18 prophylactic fenestration can be targeted to those disks most likely to cause problems in the future.19 Despite the reported benefits of fenestration, the effectiveness of the procedure is determined by the amount of NP removed,19 which can be variable and is dependent on the surgical approach, technique used, and surgeon experience.3,20,21 Further, it has been shown that the effectiveness of disk fenestration is governed by the amount of nucleus pulposus removed.22 Finally, it has been reported that reoccurrences of extrusion at a previously fenestrated disk space may be related to incomplete removal of disk material from the disk space at the time of fenestration.12 Therefore, the development of a method to reliably estimate the in situ volume of NP in clinical patients using advanced imaging such as MRI would be useful for veterinary surgeons to assess the effectiveness of fenestration in terms of the amount of NP removed and also to calculate the amount of extruded material within the spinal canal.
The rabbit lumbar spine was chosen as a preclinical model and proof of concept in this study for NP volume measurement in the in vivo clinical setting for canine patients. The objective of this study was to compare NP volume measurement from rabbit lumbar IVDs using 3 different methods: (1) MRI scans, (2) gross dimensions of the NP space, and (3) water volumetry of the dissected NP. We hypothesized that there would be no significant difference in NP volume measurements between the 3 methods.
Methods
Sample collection
Lumbar spines were harvested from 9-month-old, skeletally mature female entire New Zealand White Rabbits (n = 12), weighing 3.5 to 4.5 kg, that were euthanized as part of other ethically approved studies conducted by a single institution. Skeletal maturity was confirmed before animal recruitment by a radiographic screening of physes; commonplace at our institution. Lumbar spines were dissected en bloc from the thoracolumbar junction to the sacrum, ensuring the L1/L2 through to L5/L6 (inclusive) were included in each dissected specimen. Only L1/L2 through to L5/L6 were used for analysis given New Zealand White rabbits have variable numbers of lumbar vertebrae.23 Lumbar IVDs were chosen for this model given they are a common site for IVDE in dogs clinically and our familiarity with rabbit lumbar spine anatomy at our institution.
MRI volume measurement region of interest (ROI) calculation
Immediately after humane euthanasia, lumbar spines were harvested and scanned by a 3T MRI scanner (Philips Ingenia CX, Philips Healthcare) using a 16-channel transmit-receive (T-R) knee coil. T2-weighted modified Dixon turbo spin echo (TSE) sequences were acquired in the sagittal plane with an anterior-posterior phase direction and right-to-left slice direction. Slices were acquired at 0.6 X 0.6 X 1.5 mm voxels, reconstructed to 0.2 to 0.25 mm. Scan time was 5 minutes 37 seconds, TR 2852 ms, TE 95 ms. Images were reviewed in third-party viewing software (Horos, Nimble Co LLC d/b/a Purview) by a single experienced observer to allow estimation of the NP volume for disk spaces L1/2 through to L5/6 inclusive. The volume of each NP was calculated using the closed polygon region of interest (ROI) tool, where all slices in the sagittal plane were measured, followed by the calculation of volume (Figure 1).
Representative T2 sagittal MRI sequences of L1/2, L2/3, L3/4, L4/5, and L5/6 intervertebral disk spaces in a rabbit. The nucleus pulposus for each disk space has been outlined using the region of interest (ROI) tool to calculate volume.
Citation: American Journal of Veterinary Research 85, 1; 10.2460/ajvr.23.07.0165
Gross measurement of volume
After MRI scanning, L1/2 through to L5/6 disk spaces were dissected from the lumbar spine specimens. Each disk space was transected transversely to expose the cranial (Figure 2) and caudal endplates (Figure 2). The gross volume of the NP was calculated by multiplying the length, width, and height of the space occupied by the NP. All measurements were made using digital calipers and measured in millimeters (mm). Due to the ovoid shape of the cavity, 3 measurements for height were taken across the space and averaged (Figure 2). The craniocaudal length of the NP space was measured at the most lateral aspect of the IVD as the distance between the 2 adjacent vertebral bodies. Volume (mm3) was then calculated for each NP cavity by multiplying length, width, and height.
Cranial (a) and caudal (b) endplates of L1/2 sectioned transversely through the disk space. The red line represents the width of the NP space. The height was averaged across 3 measurements (blue line). AF = annulus fibrosus; NP = nucleus pulposus.
Citation: American Journal of Veterinary Research 85, 1; 10.2460/ajvr.23.07.0165
Water volumetry measurement
After each NP space was exposed and gross measurements taken, each NP was completely dissected out of the cavity with fine dissecting equipment. The suspension technique was then used to determine the volume of each specimen. This was done by Archimedes principle and a variation of the hydrostatic weighing technique, whereby measuring the weight of an object in 2 mediums of known density, the density, and hence the volume of the object can be determined. All measurements were made using a Mettler Toledo precision electronic microbalance (Figure 3).
Setup for suspension method of water volumetric analysis using Mettler Toledo microbalance. Sample pictured is a dissected nucleus pulposus suspended in distilled water on hydrostatic weighing scale apparatus. The weight of the nucleus pulposus is displayed in grams.
Citation: American Journal of Veterinary Research 85, 1; 10.2460/ajvr.23.07.0165
The density (ρ) of an object can be calculated using the mass of the object in air (ma) and distilled water (mw) as well as the known density of the distilled water ρw (0.99997g/cm3), and air ρa (0.0012g/cm3), using the following equation.
The volume V of an object can then be calculated using its mass and density by the following equation.
Statistical analysis
Descriptive data is presented as mean ± SD unless otherwise stated. Statistical differences between mean volumes of each of the 3 measurement methods for each IVD were evaluated by a repeated measured 1-way ANOVA and Tukey post hoc test. Statistical analysis was performed using SPSS for Windows (SPSS). For all analyses, statistical significance was set at P < .05.
Results
The calculated NP volumes are presented for each IVD for the 3 measurement methods (Table 1). For all 3 measurement methods, NP volume increased for disk spaces moving from cranial to caudal. NP volume using gross measurements of the NP space and the ROI tool from MRI scans were significantly higher than the water volumetry technique for all disk spaces in all samples (L1/2 through to L5/6). Gross measurement estimates provided the highest values at each site. Volume estimates made by MRI were significantly higher than those made using water volumetry at all sites; L1/L2 (P = .044) L2/L3 (P = .012), L3/L4 (P = .015), L4/L5 (P < .001), and L5/L6 (P < .001). Gross measurements significantly overestimated volume when compared to water volumetry at all sites; L1/L2 (P = .021), L2/L3 (P = .025), L3/L4 (P = .001), L4/L5 (P < .001), and L5/L6 (P < .001). MRI and gross volume estimates were significantly different at L4/L5 (P = .035) and L5/L6 (P = .030). NP volume using gross measurements of the NP space were significantly higher than MRI measurements for the L4/5 and L5/6 disk spaces. There was no significant difference in volume measured by MRI and gross measurements for the L1/2, L2/3, and L3/4 disk space.
Nucleus pulposus (NP) volume measurements for intervertebral disk (IVD) spaces of rabbit lumbar spines using gross measurement, MRI, and water volumetry techniques. Volumes are presented as mean ± SD in mm3.
| IVD space | Measurement technique | NP volume (mm3) |
|---|---|---|
| L1/L2 | Gross | 21.18 ± 6.01a |
| MRI | 19.7 ± 4.48a | |
| Water volumetry | 16.26 ± 3.32 | |
| L2/L3 | Gross | 22.92 ± 6.01a |
| MRI | 21.4 ± 2.84a | |
| Water volumetry | 18.42 ± 2.46 | |
| L3/L4 | Gross | 29.28 ± 5.19a |
| MRI | 25.73 ± 3.67a | |
| Water volumetry | 21.02 ± 4.95 | |
| L4/L5 | Gross | 37.96 ± 9.83ab |
| MRI | 30.77 ± 5.71a | |
| Water volumetry | 22.32 ± 4.32 | |
| L5/L6 | Gross | 41.64 ± 11.02ab |
| MRI | 33.5 ± 5.01a | |
| Water volumetry | 22.73 ± 6.09 |
Discussion
This study compared NP volume measurement from rabbit lumbar IVDs using 3 different methods as a preclinical model for the in vivo canine setting. We hypothesized that NP volume measurements by MRI, gross dimensions of the NP space, and water volumetry of the dissected NP, would not be significantly different. In this model, MRI and gross dimensions estimates were greater than the water volumetry method for all disk spaces between L1/2 and L5/6 inclusive. Therefore, we rejected the null hypothesis and accepted the alternate hypothesis. The results of this study are useful as a proof-of-concept study and are relevant to the in vivo clinical setting where MRI might be used to estimate in situ NP volume in dogs and, therefore, to assess the efficacy of surgical removal of NP via fenestration and potentially the volume of extruded material into the spinal canal.
Multiple studies advocate for prophylactic fenestration in at-risk breeds to prevent future occurrence of IVDE; however, it is not clear how much NP needs to be removed to prevent extrusion.21,24 Shores et al (1985) reported that the effectiveness of disk fenestration is determined by the amount of nucleus pulposus removed. Knapp et al (1990) speculated that IVDE at previously fenestrated disk spaces is likely related to the incomplete evacuation of NP at the time of fenestration. Therefore, there is a clinical need for a repeatable method of NP volume estimation before and after prophylactic fenestration to determine efficacy and guide the likelihood of future extrusion at that disk space. Advanced diagnostic imaging modalities such as MRI would seem the most likely means to achieve this in the in vivo setting, hence the need for evaluation in this preclinical study.
MRI is considered the gold standard imaging modality for the spine in human and veterinary medicine. MRI allows for differentiation between the NP and annulus fibrosus soft tissue structures of the disk.2,3,25 On T2-weighted MRI images of the spine, the native IVD exhibits high signal intensity in the inner water- and proteoglycan-rich NP, with low signal intensity in the fibrocartilaginous annulus fibrosus. In this study, rabbit lumbar NP volume was consistently over-estimated on MRI compared to the water volumetry method. Despite this, MRI estimation for NP volume is obviously the only possible method in the in vivo setting and was more accurate than the gross measurements technique in this study. As long as the method for volume estimation using MRI and associated software tools is repeatable, then a comparison of volume assessment pre- and postfenestration would be valuable to the clinician, with the knowledge that the actual number may be an overestimation of the true volume.
The findings of this study suggest that gross measurements provide the least accurate estimate of NP volume, and MRI, as the most theoretically accurate imaging tool of soft tissue volume calculation, is indeed an estimate in the rabbit. This is likely applicable to the dog’s lumbar spine. MRI scans can distinguish between soft tissue structures based on scanning protocol. In extruded degenerative disks the NP is distinguishable as it has lower water content and altered proteoglycan composition resulting in a lower signal intensity on T2-weighted scans.2,26 In healthy nondegenerative disks, however, studies have shown both the NP and inner part of the annulus fibrosus to be hyperintense, due to their higher water component.27 This could support the finding in this study which used healthy spine samples, demonstrating it may be difficult to obtain completely accurate volume estimates when differentiating between tissue borders on MRI reconstructions. Similarly, in acutely herniated nondegenerative disks due to trauma, differentiating between NP and annulus fibrosus may be difficult.
While this study used MRI as the diagnostic imaging modality of choice, computed tomography (CT) has also been used to estimate NP volume and volume of extruded material in clinically affected dogs. CT scans are commonly used to diagnose IVD extrusion, most useful for mineralized extruded disk material within the spinal canal. CT is unable to differentiate between the soft tissue structures of the IVD. Despite this, some studies have used CT to report on the amount of extruded material into the canal in dogs presenting with thoracolumbar T3-L3 myelopathies. A recent study by Sakaguchi et al (2023) reported that the volume of extruded materials is correlated with neurologic severity in dogs with type I IVDE. In that study, the authors used the ROI tool to estimate the volume of extruded material in the canal relative to the nonextruded adjacent disk space and reported the affected disk had a greater volume than the native disk. This method is unreliable as the IVD and extruded material were counted twice and considered “one disk” and then compared to the immediate adjacent disks, as CT could not differentiate the NP from the annulus for volume measurement. Further, when extrusion occurs it is seldom the annulus fibrosus that extrudes but rather the degenerate, calcified NP. Improved accessibility to MRI in modern-day veterinary medicine means that this imaging modality would be useful and more widely available to clinicians for the estimation of NP volume, although the time taken to complete postoperative scanning is a logistical challenge that should be considered.
The severity of spinal cord injury is multifactorial, with the rate of extrusion, degree of contusive injury suffered, and the duration of spinal cord compression 3 of the major contributors to neurological dysfunction.28 Multiple studies have reported that the maximal transverse spinal cord compression ratio is not correlated with neurologic severity for dogs with type I thoracolumbar IVDE.29–31 The most recent of these studies by Sakaguchi et al (2023) investigated if the volume of compression might affect neurological severity. The authors concluded that the volume of extruded material is at least partly responsible for the presenting neurologic severity in dogs with type I thoracolumbar IVDE. Residual disk material is also not uncommonly found postoperatively in the spinal canal after decompressive surgery.19 Aside from evaluating the effectiveness of fenestration, this proof-of-concept study may also be useful for estimation of the amount of extruded material within the vertebral canal causing spinal cord compression in dogs with thoracolumbar IVDE. This would be of benefit to veterinary clinicians for the estimation of compression at the affected site of extrusion which may assist with case management.
Water volumetry based on Archimedes’ principle was considered the gold standard reference for NP volume measurement in this study and likely reflects the “true volume” of the NP. Archimedes’ principle states that the volume of any object submerged in a fluid is equal to the volume of the fluid it displaces.32 Any submerged object experiences an upward-acting buoyancy force equal to the weight of the fluid displaced causing the phenomenon.32,33 Water volumetry is commonly used to calculate the true volume of irregularly shaped objects and validate the accuracy and reliability of advanced imaging modalities.32,34–37 In human medicine, water displacement is often used when determining subtle, early volumetric changes to oedematous peripheral limbs.38,39 Many studies have also used water volumetry to validate the accuracy and reliability of 3D imaging modalities in volumetric assessment of various tissue types including thyroid glands,40 liver,37 bones,36 and dissected soft tissue.34 Water displacement becomes challenging when the volume of the object measured is so small,41 such as the rabbit NP. True volume measurements in this study were taken using the suspension technique, a variation of the hydrostatic weighing technique that incorporates Archimedes’ principle of water displacement and buoyancy forces to provide a more accurate and precise volume measurement.41 The technique states that the difference in weights of an object measured in 2 mediums of known density allows the observer to calculate the density of the object and the volume.41 Our model shows even current gold-standard imaging techniques may not provide us with the actual volume of the NP. However, water volumetry has little clinical practicality as even if NP material is removed and measured, there is no reference point preoperatively for comparison. In the clinical setting, MRI will still remain the most practical option when comparing pre- and postoperative volume measurements. Although MRI gives an estimate, provided the measurement method is the same, and subject to the same limitations, the comparison is relative and still useful for the assessment of the effectiveness of NP removal.
The volume of NP for all rabbit lumbar IVDs sequentially increased from the cranial L1/2 IVD to L5/6 as measured by all methods. Without further studies repeating this method for other species, no direct comparisons can be made. However, we suspect that moving caudally along the lumbar spine, surgeons could expect to remove a greater volume of NP from nonextruded in situ NP when performing prophylactic fenestration. As stated previously, postoperative MRI would be required to evaluate the effectiveness of fenestration by volume measurement compared to preoperative imaging.
We acknowledge some limitations in this study. Rabbit and canine lumbar spines have some anatomical differences. Rabbit lumbar spines were selected as a preclinical model for the dog due to greater sample accessibility. Further, age and sex-matched rabbits from a closed breeding colony were used to minimize variation between samples to provide a more accurate means for comparison between measurement methods. Additionally, this study did not assess cervical, and caudal thoracic disks where IVDE is also common in dogs. Despite anatomical differences in size and shape of the vertebrae, intervertebral disks, and spinal cord, the principles behind the imaging modalities and volume estimate techniques used to identify these structures remain the same for dogs and other species.42 Future studies could use our model of volume estimation to more accurately evaluate the effectiveness of fenestration in cadavers with pre- and postoperative MRI evaluation. The results of that study may then be extrapolated to the in vivo preclinical setting and finally to our canine patients, first in native, nondegenerate disks before considering assessment of pathological disk spaces. This method would allow for an objective measurement of the effectiveness of fenestration that is determined by how much NP has been removed, as reported by Shores et al (1985).
NP volume measurements in rabbit lumbar IVDs made grossly and by MRI significantly overestimated the true volume as measured by water volumetry. NP volume increases with each IVD space caudally. Despite being an estimate, MRI will likely remain the most commonly used tool for NP volume estimates due to practicality. The findings of this preclinical model may be useful for veterinary surgeons when estimating the volume of in situ NP and during surgical planning for the removal of extruded material or performing prophylactic fenestration.
Acknowledgments
All authors contributed substantially to the study design, analysis, and interpretation of current literature. Jason Hawkins, James Crowley: study design, data collection, data analysis, and manuscript review. Matthew Pelletier: study design, manuscript review. William Walsh: study design, manuscript review. All authors have read and revised the manuscript and approved the final submitted version.
Disclosures
The authors have nothing to disclose. No AI-assisted technologies were used in the generation of this manuscript.
Funding
The authors have nothing to disclose
References
- 1.↑
Bergknut N, Egenvall A, Hagman R, et al. Incidence of intervertebral disk degeneration–related diseases and associated mortality rates in dogs. J Am Vet Med Assoc. 2012;240(11):1300–1309. doi:10.2460/javma.240.11.1300
- 2.↑
da Costa RC, De Decker S, Lewis MJ, et al. Diagnostic imaging in intervertebral disc disease. Front Vet Sci. 2020;7:782. doi:10.3389/fvets.2020.588338
- 3.↑
Brisson BA. Intervertebral disc disease in dogs. Vet Clin Small Anim Pract. 2010;40(5):829–858. doi:10.1016/j.cvsm.2010.06.001
- 4.↑
Fenn J, Olby NJ, Moore SA, et al. Classification of intervertebral disc disease. Front Vet Sci. 2020;7:707. doi:10.3389/fvets.2020.579025
- 5.↑
Olsson S-E. Observations concerning disc fenestration in dogs. Acta Orthop Scand. 1951;20(4):349–356. doi:10.3109/17453675108991182
- 6.↑
Brisson BA, Holmberg DL, Parent J, Sears WC, Wick SE. Comparison of the effect of single-site and multiple-site disk fenestration on the rate of recurrence of thoracolumbar intervertebral disk herniation in dogs. J Am Vet Med Assoc. 2011;238(12):1593–1600. doi:10.2460/javma.238.12.1593
- 7.↑
Aikawa T, Fujita H, Kanazono S, Shibata M, Yoshigae Y. Long-term neurologic outcome of hemilaminectomy and disk fenestration for treatment of dogs with thoracolumbar intervertebral disk herniation: 831 cases (2000–2007). J Am Vet Med Assoc. 2012;241(12):1617–1626. doi:10.2460/javma.241.12.1617
- 8.↑
Black A. Lateral spinal decompression in the dog: a review of 39 cases. J Small Anim Pract. 1988;29(9):581–588. doi:10.1111/j.1748-5827.1988.tb02177.x
- 9.
Butterworth S, Denny H. Follow-up study of 100 cases with thoracolumbar disc protrusions treated by lateral fenestration. J Small Anim Pract. 1991;32(9):443–447. doi:10.1111/j.1748-5827.1991.tb00983.x
- 10.↑
Davies J, Sharp N. A comparison of conservative treatment and fenestration for thoracolumbar intervertebral disc disease in the dog. J Small Anim Pract. 1983;24(12):721–729. doi:10.1111/j.1748-5827.1983.tb00360.x
- 11.
Funkquist B. Investigations of the therapeutic and prophylactic effects of disc evacuation in cases of thoraco-lumbar herniated discs in dogs. Acta Vet Scand. 1978;19(3):441–457. doi:10.1186/BF03547613
- 12.↑
Knapp D, Pope E, Hewett J, Bojrab M. A retrospective study of thoracolumbar disk fenestration in dogs using a ventral approach: 160 cases (1976 to 1986). J Am Anim Hospital Assoc. 1990;26(5):543–549.
- 13.↑
Levine S, Caywood D. Recurrence of neurological deficits in dogs treated for thoracolumbar disk disease. J Am Anim Hospital Assoc. 1984;20(6):889–894.
- 14.↑
Dhupa S, Glickman N, Waters DJ. Reoperative neurosurgery in dogs with thoracolumbar disc disease. Vet Surg. 1999;28(6):421–428. doi:10.1111/j.1532-950X.1999.00421.x
- 15.
Nečas A. Clinical aspects of surgical treatment of thoracolumbar disc disease in dogs. A retrospective study of 300 cases. Acta Vet Brno. 1999;68(2):121–130. doi:10.2754/avb199968020121
- 16.
Prata R. Neurosurgical treatment of thoracolumbar disks: the rationale and value of laminectomy with concomitant disk removal. J Am Anim Hospital Assoc. 1981;17:17–26.
- 17.↑
Scott H. Hemilaminectomy for the treatment of thoracolumbar disc disease in the dog: a follow-up study of 40 cases. J Small Anim Pract. 1997;38(11):488–494. doi:10.1111/j.1748-5827.1997.tb03303.x
- 18.↑
Aikawa T, Fujita H, Shibata M, Takahashi T. Recurrent thoracolumbar intervertebral disc extrusion after hemilaminectomy and concomitant prophylactic fenestration in 662 chondrodystrophic dogs. Vet Surg. 2012;41(3):381–390. doi:10.1111/j.1532-950X.2012.00970.x
- 19.↑
Jeffery ND, Freeman PM. The role of fenestration in management of type I thoracolumbar disk degeneration. Vet Clin Small Anim Pract. 2018;48(1):187–200.
- 20.↑
Holmberg D, Palmer N, VanPelt D, Willan A. A comparison of manual and power-assisted thoracolumbar disc fenestration in dogs. Vet Surg. 1990;19(5):323–327. doi:10.1111/j.1532-950X.1990.tb01199.x
- 21.↑
Morelius M, Bergadano A, Spreng D, Schawalder P, Doherr M, Forterre F. Influence of surgical approach on the efficacy of the intervertebral disk fenestration: a cadaveric study. J Small Anim Pract. 2007;48(2):87–92. doi:10.1111/j.1748-5827.2007.00269.x
- 22.↑
Shores A, Cechner P, Cantwell H, Wheaton L, Carlton W. Structural changes in thoracolumbar disks following lateral fenestration a study of the radiographic, histologic, and histochemical changes in the chondrodystrophoid dog. Vet Surg. 1985;14(2):117–123. doi:10.1111/j.1532-950X.1985.tb00838.x
- 23.↑
Crowley JD, Oliver RA, Dan MJ, et al. Single level posterolateral lumbar fusion in a New Zealand White rabbit (Oryctolagus cuniculus) model: surgical anatomy, operative technique, autograft fusion rates, and perioperative care. JOR Spine. 2021;4(1):e1135. doi:10.1002/jsp2.1135
- 24.↑
Brisson BA, Moffatt SL, Swayne SL, Parent JM. Recurrence of thoracolumbar intervertebral disk extrusion in chondrodystrophic dogs after surgical decompression with or without prophylactic enestration: 265 cases (1995–1999). J Am Vet Med Assoc. 2004;224(11):1808–1814. doi:10.2460/javma.2004.224.1808
- 25.↑
Naudé SH, Lambrechts NE, Wagner WM, Thompson PN. Association of preoperative magnetic resonance imaging findings with surgical features in Dachshunds with thoracolumbar intervertebral disk extrusion. J Am Vet Med Assoc. 2008;232(5):702–708. doi:10.2460/javma.232.5.702
- 26.↑
Benneker LM, Heini PF, Anderson SE, Alini M, Ito K. Correlation of radiographic and MRI parameters to morphological and biochemical assessment of intervertebral disc degeneration. Euro Spine J. 2005;14(1):27–35. doi:10.1007/s00586-004-0759-4
- 27.↑
Seiler G, Häni H, Scheidegger J, Busato A, Lang J. Staging of lumbar inter vertebral disc degeneration in nonchondrodystrophic dogs using low-field magnetic resonance imaging. Vet Radiol Ultrasound. 2003;44(2):179–184. doi:10.1111/j.1740-8261.2003.tb01268.x
- 28.↑
Griffin JF, Levine J, Kerwin S. Canine thoracolumbar invertebral disk disease: pathophysiology, neurologic examination, and emergency medical therapy. Compendium (Yardley, PA). 2009;31(3):E2–E2.
- 29.↑
Levine J, Fosgate G, Chen A, et al. Magnetic resonance imaging in dogs with neurologic impairment due to acute thoracic and lumbar intervertebral disk herniation. J Vet Internal Med. 2009;23(6):1220–1226. doi:10.1111/j.1939-1676.2009.0393.x
- 30.
Penning V, Platt S, Dennis R, Cappello R, Adams V. Association of spinal cord compression seen on magnetic resonance imaging with clinical outcome in 67 dogs with thoracolumbar intervertebral disc extrusion. J Small Anim Pract. 2006;47(11):644–650. doi:10.1111/j.1748-5827.2006.00252.x
- 31.↑
Sakaguchi Y, Nishida H, Tanaka H, Kitamura M, Akiyoshi H, Nakayama M. The volume of extruded materials is correlated with neurologic severity in small-breed dogs with type I thoracolumbar intervertebral disk herniation. J Am Vet Med Assoc. 2023;1(aop):1–5. doi:10.2460/javma.22.07.0326
- 32.↑
Mohazzab P. Archimedes’ principle revisited. J Appl Math Physics. 2017;5(04):836. doi:10.4236/jamp.2017.54073
- 33.↑
Mohazzabi P, James MC. A simple apparatus for demonstrating fluid forces and Newton’s Third Law. Phys Teach. 2012;50(9):537–539. doi:10.1119/1.4767486
- 34.↑
Hyer JN, Murta F, Juniat VA, Ezra DG. Validating three-dimensional imaging for volumetric assessment of periorbital soft tissue. Orbit. 2021;40(1):9–17. doi:10.1080/01676830.2020.1711780
- 35.
Lee SJ, Chong S, Kang KH, et al. Semiautomated thyroid volumetry using 3D CT: prospective comparison with measurements obtained using 2D ultrasound, 2D CT, and water displacement method of specimen. Am J Roentgenol. 2014;203(5):W525–W532. doi:10.2214/AJR.13.12206
- 36.↑
Luo J, Annesley-Williams DJ, Adams MA, Dolan P. How are adjacent spinal levels affected by vertebral fracture and by vertebroplasty? A biomechanical study on cadaveric spines. Spine J. 2017;17(6):863–874. doi:10.1016/j.spinee.2017.01.013
- 37.↑
Niehues SM, Unger J, Malinowski M, Neymeyer J, Hamm B, Stockmann M. Liver volume measurement: reason of the difference between in vivo CT-volumetry and intraoperative ex vivo determination and how to cope it. Euro J Med Res. 2010;15(8):345–350. doi:10.1186/2047-783X-15-8-345
- 38.↑
Kremer RL, Wolfe ME, Brueckner NJ, Viola MC, Fisher MI. Validity and reliability of three-dimensional imaging to measure limb volume: a systematic review. Phys Ther Rev. 2020;25(1):21–28. doi:10.1080/10833196.2019.1698160
- 39.↑
Montalibet A, Rastel D, Chaigneau C, Grenier E, McAdams E. Swollen Lower Limbs in Patients with Negative Pitting Test Leg Oedema: Prediction of Water Displacement Changes by Anthropometry and Bioimpedance Spectroscopy. Paper presented at: 2020 42nd Annual International Conference of the IEEE Engineering in Medicine & Biology Society (EMBC); 2020.
- 40.↑
Vurdem ÜE, Acer N, Ertekin T, Savranlar A, Topuz Ö, Keceli M. Comparison of three volumetric techniques for estimating thyroid gland volume. Turk J Med Sci. 2012;42(Sup. 1):1299–1306. doi:10.3906/sag-1112-6
- 41.↑
Hughes SW. Archimedes revisited: a faster, better, cheaper method of accurately measuring the volume of small objects. Phys Ed. 2005;40(5):468. doi:10.1088/0031-9120/40/5/008
- 42.↑
Toossi A, Bergin B, Marefatallah M, et al. Comparative neuroanatomy of the lumbosacral spinal cord of the rat, cat, pig, monkey, and human. Sci Rep. 2021;11(1):1–15. doi:10.1038/s41598-021-81371-9
