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Paper
Paper Dorsal vertebral column abnormalities in dogs with disseminated idiopathic skeletal hyperostosis (DISH) S. De Decker, H. A. Volk Although disseminated idiopathic skeletal hyperostosis (DISH) most often affects the ventral aspect of the vertebral column, this study evaluated the occurrence, nature and clinical relevance of dorsal vertebral column abnormalities in 10 dogs with DISH for which CT or MRI and a complete neurological examination were available. Dorsal vertebral column abnormalities were present in eight dogs and included articular process hypertrophy (n=7 dogs), periarticular new bone formation (n=1), pseudoarthrosis between spinous processes (n=4) and thickening of the dorsal lamina (n=4). These dorsal vertebral abnormalities caused clinically relevant vertebral canal stenosis in six dogs and were the only cause of clinical signs in four of these dogs. Although the lumbosacral joint was not affected by DISH, these six dogs demonstrated lumbosacral vertebral canal stenosis and clinical signs of cauda equina compression, which included paraparesis (n=5 dogs), lumbosacral pain (n=4), urinary incontinence (n=4), faecal incontinence (n=1) and urinary and faecal incontinence (n=1). There is a possible association between DISH and hypertrophy of dorsal vertebral structures, potentially resulting in vertebral canal stenosis. Although these changes occurred at segments fused by DISH, they predominantly affected adjacent non-affected segments.
Introduction
Diffuse idiopathic skeletal hyperostosis (DISH) is a systemic disease characterised by calcification and ossification within soft tissues of both the axial and the appendicular skeleton (Resnick and Niwayama 1976, Kranenburg and others 2011). Although DISH is relative commonly encountered in humans (Holton and others 2011), only a few reports have discussed its presence in dogs (Kranenburg and others 2011, Ortega and others 2012). A recent radiographic study has estimated the prevalence of DISH to be 3.8 per cent in clinically normal dogs with a significantly higher prevalence in older animals, males and the Boxer breed (Kranenburg and others 2010). Although DISH can affect multiple anatomical structures, it affects most typically the ventral longitudinal ligament, resulting in the formation of contiguous bone ventral to the vertebral column with complete bony fusion of consecutive vertebral segments (Kranenburg and others 2011). There is debate considering the diagnostic criteria for DISH in dogs (Greatting and others 2011, Ciepluch and others 2013). To improve comparisons with human medicine, three criteria have been suggested to confirm a diagnosis of DISH in dogs: (1) flowing calcification and ossification along the ventrolateral aspect of at least four contiguous vertebral bodies; (2) preservation of the intervertebral disc width and the absence of overt radiographic changes indicative of degenerative Veterinary Record (2014) S. De Decker, DVM, PhD, MvetMed. DipECVN, H. A. Volk, DVM, PhD, DipECVN, Department of Veterinary Clinical Science and Services, The Royal Veterinary College, University of London, Hawkshead Lane, North Mymms, Hertfordshire AL97TA, UK;
doi: 10.1136/vr.102492 E-mail for correspondence: [email protected] Provenance: not commissioned; externally peer reviewed Accepted April 9, 2014
intervertebral disc disease; and (3) the absence of articular process ankylosis, sacroiliac joint erosion, sclerosis or intra-articular osseous fusion (Resnick and Niwayama 1976, Greatting and others 2011). However, several case reports have reported dogs in which prominent abnormalities were associated with dorsal vertebral structures, including the articular and spinous processes (Woodard and others 1985, Morgan and Stavenborn 1991, Ciepluch and others 2013, Kornmayer and others 2013). Therefore, additional diagnostic criteria have been proposed in dogs that include dorsal vertebral column abnormalities (Morgan and Stavenborn 1991). The clinical relevance of DISH in dogs has not been fully determined (Kranenburg and others 2011). DISH is usually an incidental radiological finding not associated with clinical signs. Reported clinical signs of DISH in dogs include stiffness, and axial and appendicular skeletal pain (Woodard and others 1985, Morgan and Stavenborn 1991, Kranenburg and others 2011). Several human and veterinary studies have suggested that spinal stiffness associated with DISH could biomechanically predispose to adjacent segment disease, vertebral canal stenosis, vertebral subluxations and spinal fractures after minor trauma (Pascal-Mousselard and others 2006, Chi and others 2008, Kawabori and others 2009, Westerveld and others 2009, Koizumi and others 2010, Holton and others 2011, Ortega and others 2012, Kornmayer and others 2013). It has been postulated that DISH in dogs may result in biomechanical changes comparable to spinal fusion (Ortega and others 2012). In vitro biomechanical and experimental animal studies have demonstrated progressive degenerative changes of the articular and spinous processes after spinal fixation (Cramer and others 2004, Little and others 2004, Cramer and others 2010, Homb and Henderson 2012). However, little is known about the occurrence of such changes in dogs with DISH. Therefore, the primary goal of this study was to evaluate the occurrence of dorsal vertebral column abnormalities in dogs with DISH. The secondary aims were to report the clinical relevance and associated clinical signs of these changes. June 21, 2014 | Veterinary Record
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Paper Materials and methods
The digital database of the Small Animal Referral Hospital, Royal Veterinary College, University of London, was searched between 2007 and 2013 for dogs diagnosed with DISH. Used search terms included DISH. Patients were included if they had (1) complete medical records available, if (2) a complete neurological examination was performed, and if (3) MR or CT imaging of the vertebral column demonstrated complete osseous fusion of at least four adjacent vertebral segments (Resnick and Niwayama 1976). Dogs were excluded if the clinical records or diagnostic imaging studies were incomplete or were unavailable for review. Because of difficulties in assessment of articular process abnormalities on survey radiographs (De Decker and others 2011), dogs with only spinal radiographs available were not included in this study. Information retrieved from the medical records included signalment, duration and type of clinical signs before presentation, general physical and neurological examination findings, results of ancillary diagnostic tests, details of CT and MR imaging studies, final diagnosis, treatment and follow-up data. MR and CT imaging examinations were performed under general anaesthesia. Although anaesthesia protocols could vary between individual cases, a commonly used protocol included premedication with a combination of acepromazine (0.01 mg/kg intravenously) and methadone (0.1–0.2 mg/kg intravenously), followed by induction with propofol (4–6 mg/kg intravenously) and maintenance of general anaesthesia with isoflurane in oxygen. MRI was performed with a 1.5T magnet (Intera, Philips Medical Systems, Eindhoven, the Netherlands) and included a minimum of T2 and T1-weighted sagittal and transverse sequences. The images of the transverse plane were aligned perpendicular to the respective intervertebral disc spaces. CT imaging
was performed by a 16-slice helical CT scanner (PQ 500, Universal Systems, Solon, Ohio, USA). After completion of the transversal CT study, sagittal, dorsal and three-dimensional reconstructions were made. All imaging studies were reviewed by the first author (SDD) using Osirix Dicom viewer (Osirix Foundation, V.5.5.2 Geneva, Switzerland). Emphasis was placed on assessment of dorsal vertebral abnormalities, such as periarticular new bone formation, articular process hypertrophy, pseudoarthrosis between adjacent spinous processes and laminar thickening. Short-term follow-up information was retrieved from r e-examination visits at our institution. Long-term follow-up information was obtained by a telephone interview with the referring v eterinary surgeon. All follow-up information was retrieved by the first author (SDD).
Results
Ten dogs were included in this study (Table 1). Dogs underwent MR imaging as the only diagnostic technique (n=6 dogs), CT as the only diagnostic technique (n=1) or a combination of CT and MRI (n=3). Survey radiographs from the referring veterinary surgeon were available for three dogs. The complete spine was imaged in two dogs, the thoracic, thoracolumbar, lumbar and lumbosacral spine in five dogs and the thoracolumbar, lumbar and lumbosacral spine in three dogs. In two dogs, no changes affecting dorsal vertebral structures were noted. One of these dogs (case 1) was neurologically normal and DISH was considered an incidental finding, while the other dog (case 2) demonstrated a stiff pelvic limb gait and lumbar and lumbosacral hyperaesthesia on palpation. Although not considered clinically relevant, these two dogs demonstrated additional spondylosis deformans at the lumbosacral junction without intervertebral disc degeneration.
Table 1. Clinical presentation, imaging findings, treatment and outcome of 10 dogs with DISH Case
Signalment
Clinical presentation
DISH
Dorsal vertebral changes
Cause of clinical signs
Treatment
Follow-up
1
Boxer, 7y9m, Fn
T10-L3
None
Syncope
None
2
Golden Retriever, 3y, Fn Boxer, 7y8m, Mn
Two collapse episodes. Neurological examination unremarkable Stiff PL gait and spinal hyperaesthesia of 7d duration Progressive ataxia and proprioceptive deficits PLs of 5m duration LS hyperaesthesia and proprioceptive deficits right PL of 14d duration
L3-L7
None
DISH
T6-L2
Hypertrophy left articular processes T13-L1 and L1-L2 Periarticular new bone formation L4-L5 and L5-L6. Pseudoarthrosis L¬2-L3 Hypertrophy articular processes L7-S1, thickened lamina L7, pseudoarthrosis T5-L5
Presumed degenerative myelopathy Discospondylitis L7-S1
Meloxicam and gabapentin Physiotherapy
Euthanasia 5y3m after diagnosis unrelated to study Static condition 5m after diagnosis Euthanasia 5.5m after diagnosis
3
T12-L6
Analgesia, antibiotics
Euthanasia 14d after diagnosis
Restricted exercise, prednisolone
Euthanasia 15m after diagnosis unrelated to study. Remained urinary incontinent
Meloxicam, gabapentin, physiotherapy Restricted exercise and meloxicam
Euthanasia 3.5m after diagnosis. Remained urinary incontinent Euthanasia 3w after diagnosis. Remained urinary incontinent
LSS
Lumbosacral dorsal laminectomy
Improved, but still u rinary incontinent 3y4m after surgery
Hypertrophy articular processesL7-S1, thickened lamina L7
LSS
Lumbosacral dorsal laminectomy
Hypertrophy articular processes L7-S1, pseudoarthrosis L1-L2
LSS
None
Full recovery Recovered faecal continence. Fibrotic myopathy 2m after surgery. Receives hydro -and physiotherapy 9m after surgery Euthanasia at moment of diagnosis
4
Great Dane, 4y7m, M
5
Giant Schnauzer, 11y6m, Fn
Lethargy, ataxia and paresis PLs, proprioceptive deficits all limbs, cervical and LS h yperaesthesia, urinary incontinence of 7d duration
L2-L7
6
Boxer, 10y2m, Mn
T7-L7
Hypertrophy articular processes L7-S1
7
Boxer, 10y11m, Mn
T7-L7
Hypertrophy articular processes L7-S1, thickened lamina L7
8
Cross breed, 10y7m, Fn
T2-L7
Hypertrophy articular processes L7-S1, thickened lamina L7, pseudoarthrosis T12-L2
9
German Shepherd, 6y10m, Fn
Ataxia and paresis PLs, LS hyperaesthesia, urinary incontinence of 1m duration Paraparesis, proprioceptive deficits and decreased spinal reflexes PLs, decreased perianal sensation, and urinary incontinence of 2m duration Paraparesis, p roprioceptive deficits and decreased withdrawal reflexes PLs, LS, absent perianal reflex, flaccid tail and urinary incontinence of 2m duration Lumbosacral hyperaesthesia, absent perianal reflex, flaccid tail of 8m duration. Faecal incontinence of 2w duration
T13-L7
10
Beagle, 9y3m, Fn
T11-L7
Flaccid tail, absent perianal reflex, urinary and faecal incontinence of 3d duration
LSS, multiple cervical intervertebral disk protrusions, immune mediated haemolytic anemia LSS, Presumed degenerative myelopathy LSS
d, days; Fn, female neutered; LS, lumbosacral; LSS, lumbosacral stenosis; M, male; m, months; Mn, Male neutered; PL, pelvic limb; w, weeks; y, years.
Veterinary Record | June 21, 2014
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Paper The remaining eight dogs (cases 3–10) were neurologically abnormal and demonstrated a variable degree of changes affecting the dorsal vertebral column. Although not considered to be the cause of clinical signs, seven of these eight dogs also demonstrated lumbosacral spondylosis deformans and lumbosacral intervertebral disc degeneration with mild-to-moderate protrusion. The presence of lumbosacral discospondylitis precluded evaluation of intervertebral disc degeneration and protrusion in one dog (case 4). In two of these dogs (cases 3 and 4), neither DISH nor the dorsal vertebral column changes were considered to be the cause of neurological deficits (Table 1). One dog of these two dogs (case 3) demonstrated thoracolumbar articular process hypertrophy without spinal cord compression, while the other dog (case 4) demonstrated pseudoarthrosis between the base of several lumbar spinous processes and a variable degree of lumbar periarticular new bone formation (Table 1). Clinical signs in these two dogs were attributed to presumed canine degenerative myelopathy (homozygous SOD-1 mutation) (case 3) and lumbosacral discospondylitis (case 4). The remaining six dogs (cases 5–10) demonstrated clinical signs that could, at least in part, be explained by dorsal vertebral column changes. These dogs demonstrated extensive DISH formation including L7, but not the lumbosacral joint. They also demonstrated prominent dorsal vertebral column changes resulting in lumbosacral vertebral canal stenosis. More specifically, these abnormalities included severe hypertrophy of the lumbosacral articular processes (n=6 dogs) and a thickened dorsal lamina of L7 (n=4 dogs) (Figs 1–3). Pseudoarthrosis of the thoracolumbar and lumbar spinous processes was seen in three of these dogs (Table 1) (Fig 4). These six dogs demonstrated clinical signs consistent with cauda equina compression, including paraparesis (n=5 dogs), lumbosacral hyperaesthesia on palpation (n=4), flaccid tail (n=3), urinary incontinence (n=4), faecal incontinence (n=1) or a combination of urinary and faecal incontinence (n=1) (Table 1). Although not considered to be the main cause of clinical signs, these dogs also demonstrated lumbosacral spondylosis deformans and intervertebral disc degeneration with mild-to-moderate disc protrusion. Concurrent neurological disorders were present in two of these six dogs; one dog (case 5) was also diagnosed with multiple cervical intervertebral disc protrusions between C3 and C7, while the other dog (case 6)
was presumptively diagnosed with canine degenerative myelopathy (homozygous SOD-1 mutation). Both dogs were managed medically. Although they remained urinary incontinent, they were ultimately euthanised for reasons other than lumbosacral disease (Table 1). In the four remaining dogs (cases 7–10), stenosis of the lumbosacral vertebral canal, associated with severe hypertrophy of the articular processes and laminar thickening, was considered to be the only cause of clinical signs. One of these dogs was treated medically with a combination of restricted exercise and meloxicam (case 7), two were treated surgically by a dorsal laminectomy (cases 8 and 9) and the remaining dog was euthanised at the time of diagnosis (case 10). The medically treated dog (case 7) did not improve and was euthanised three weeks after diagnosis. One of the surgically treated dogs (case 8) improved remarkably after surgery, but remained urinary incontinent. The other surgically treated dog (case 9) regained a neurologically normal status, but developed bilateral fibrotic myopathy of the gracilis muscle two months after surgery. This dog still visits our institution for weekly hydro- and physiotherapy sessions nine months after surgery.
Discussion
This study assessed the occurrence and nature of dorsal vertebral column abnormalities in dogs with DISH. Dorsal vertebral column changes occurred both at segments fused by DISH and adjacent nonaffected vertebral segments (Table 1 and Fig 5). Several dogs of this study demonstrated hypertrophy of dorsal vertebral structures, leading to lumbosacral vertebral canal stenosis (Figs 1–3). Radiological or clinical evidence of lumbosacral intervertebral disc disease has been reported in dogs with DISH (Kranenburg and others 2011, Ortega and others 2012). Although these previous studies did not specifically focus on abnormalities of the lumbosacral vertebral canal, they favour the hypothesis that lumbosacral vertebral canal stenosis in dogs with DISH might be more common than previously considered. Although all clinically affected dogs in this study demonstrated mildto-moderate lumbosacral intervertebral disc protrusion, cauda equina compression was predominantly dorsal in direction and caused by severe articular process hypertrophy (Figs 1 and 2). Other observed dorsal vertebral column abnormalities were periarticular new bone
FIG 1: Sagittal T1-weighted (a) and a transverse CT image at the lumbosacral junction (b) of an almost seven-year-old female German shepherd dog with disseminated idiopathic skeletal hyperostosis and lumbosacral vertebral canal stenosis (case 9). Transverse CT image at the level of the lumbosacral junction of a neurologically normal seven-year-old female German shepherd dog (c). (a) Although there is mild lumbosacral intervertebral disc protrusion, cauda equina compression is mainly dorsal in direction (arrow). When compared with (c), it is obvious that lumbosacral vertebral canal stenosis (b) is predominantly caused by articular process hypertrophy (arrows).
June 21, 2014 | Veterinary Record
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Paper
FIG 2: Transverse CT image at the level of the lumbosacral joint (a) and a three-dimensional reconstructed CT image (b) of a 10-year -7-month-old female Beagle (case 10) with disseminated idiopathic skeletal hyperostosis and lumbosacral stenosis. Severe hypertrophy of the articular processes and periarticular new bone formation distort the normal vertebral anatomy and are the main cause of severe lumbosacral vertebral canal stenosis (arrows). Transverse CT image (c) at the level of the lumbosacral joint and a three-dimensional reconstructed CT image of a neurologically normal four-year-old female cross breed dog (d) for comparison.
formation, pseudoarthrosis between the base of adjacent spinous processes and thickening of the dorsal lamina (Figs 3 and 4). The nature of these dorsal vertebral changes is uncertain. Prominent dorsal vertebral column abnormalities have been reported in dogs with DISH, and although controversial, such changes have even been considered to represent a diagnostic criterion for dogs with DISH (Woodard and others 1985, Morgan and Stavenborn 1991, Ciepluch and others 2013).
Therefore, it is possible that the dorsal vertebral column changes observed in this study represent a variation of lesion distribution in dogs with DISH. It can however not be excluded that these abnormalities represent a biomechanical consequence of DISH. The contiguous new bone formation has been suggested to cause decreased flexibility with increased stiffness of the affected vertebral segments. This can result in altered biomechanics on adjacent mobile segments
FIG 3: Transverse CT images at the level of L7 (a) and sagittal reconstructions (b) of and an almost seven-year-old female German shepherd dog with disseminated idiopathic skeletal hyperostosis (DISH) (case 9) and lumbosacral stenosis and a neurologically normal seven-yearold female German shepherd dog (c and d) The German shepherd dog with DISH demonstrates thickening of the dorsal lamina of L7 and less obviously of L4, L5 and L6. This is best appreciated on the transverse images (a). The thickness of the dorsal lamina in (a) is similar to the height of the vertebral body, while the dorsal lamina in (c) is much thinner than the height of the vertebral body. Hypertrophy of the lumbosacral articular processes was the main cause of cauda equina compression (arrow in b).
Veterinary Record | June 21, 2014
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Paper Homb and Henderson 2012). An in vitro human biomechanical study demonstrated increased stress and strains of articular processes at the mobile adjacent vertebral segments after lumbar spinal fixation (Little and others 2004). The results of this study contribute further to the controversy regarding appropriate diagnostic criteria for DISH in dogs. The generally accepted criteria of Resnick and Niwayama (1976) do not include changes affecting the dorsal vertebral column. It specifically excludes patients with articular process joint bony ankylosis, sacroiliac joint erosion, sclerosis or intra-articular osseous fusion. Although it is unclear whether articular process hypertrophy and periarticular new bone formation should be considered ‘articular process joint bony ankylosis’, the results of the study presented here do not favour following strictly the ‘Resnick’ criteria for DISH in dogs. In contrast, the diagnostic criteria proposed by Morgan and Stavenborn (1991) require dorsal vertebral column changes, specifically periarticular new bone formation or pseudoarthrosis between the bases of the spinous processes, to be present before a diagnosis of DISH can be made. Although most dogs of the present study demonstrated such dorsal vertebral abnormalities, this was not present in all cases. Therefore, the results of our study do not favour following these strict ‘Morgan’ criteria either. It is well known that both dogs and people with DISH can present with a variety in lesion distribution and localisation (Kranenburg and others 2013). This has led to a multitude of terms to refer to this disorder in people and highlights the difficulty of correctly defining and diagnosing DISH (Utsinger 1985). Although the results of this study suggest that DISH can be associated with dorsal vertebral column abnormalities and clinical signs, it is valuable to keep in mind that DISH is an incidental finding in the majority of affected animals (Kranenburg and others 2011). The results of the study presented here are unlikely to represent the overall prevalence of dorsal vertebral column abnormalities in dogs with DISH. Dogs had to have MR or CT imaging and a complete neurological examination performed before they could be included in this study. This likely caused a selection bias towards dogs with neurological or suspected neurological disorders. It is further unclear why some dogs with DISH develop dorsal vertebral column changes, while others do not. All dogs with lumbosacral vertebral canal stenosis had extensive DISH formation including L7. It is possible that the location and length of the affected vertebral segments play key roles in the development of these changes. However, the number of included animals in this study was too small to investigate this hypothesis. Further, several dogs of this study demonstrated concurrent spinal disorders, such as discospondylitis and presumptive degenerative myelopathy. Therefore, we cannot exclude that the occurrence of dorsal vertebral abnormalities was not influenced by the presence of these concurrent spinal disorders.
FIG 4: Sagittal reconstructed CT (a) and sagittal T1-weighted MR (b) image of an 11-year-6-month-old female Giant Schnauzer with disseminated idiopathic skeletal hyperostosis (case 5). Pseudoarthrosis is present between the bases of several adjacent lumbar spinous processes (white arrows).
(Kranenburg and others 2011). Adjacent segment disease has recently been reported in dogs with DISH and has been characterised by degenerative changes of the remaining mobile vertebral segment adjacent to fused, normally mobile, vertebral segments (Ortega and others 2012). In the present study, all dogs with lumbosacral vertebral canal stenosis had extensive DISH formation including L7, but not involving the lumbosacral joint. It is possible that the fused lumbar vertebral column caused increased biomechanical stresses on the lumbosacral junction where still some mobility persisted. Next to altered biomechanical forces at adjacent vertebral segments, it is also possible that fusion of ventral vertebral structures induces altered biomechanics on the dorsally unaffected anatomical structures. The hypothesis that these dorsal vertebral column changes could represent a biomechanical consequence of DISH is further supported by several experimental studies. Laboratory animal studies have demonstrated progressive degenerative changes of the articular processes and spinous process hypertrophy as a direct result of experimentally induced caudal lumbar spinal hypomobility. Although these degenerative changes occurred at both fused and non-fused segments, they were more severe at the fixed vertebral segments (Cramer and others 2004, Cramer and others 2010,
Prevalence of observed abnormalities
100
Dorsal Vertebral Changes
DISH
90 80 70 60 50 40 30 20 10
L7-s (n=10)
T1-L7 (n=10)
T1-L6 (n=10)
T1-L5 (n=10)
T1-L4 (n=10)
T1-L3 (n=10)
T1-L2 (n=10)
T1-L1 (n=10)
T1-T13 (n=9)
T1-T12 (n=9)
T1-T11 (n=8)
T1-T10 (n=8)
T1-T9 (n=7)
T1-T8 (n=7)
T1-T7 (n=7)
T1-T6 (n=7)
T1-T5 (n=7)
T1-T4 (n=7)
T1-T3 (n=7)
T1-T2 (n=6)
C7-T1 (n=6)
C6-C7 (n=6)
C5-C6 (n=5)
C4-C5 (n=3)
C3-C4 (n=2)
C2-C3 (n=2)
C1-C2 (n=2)
0
Distribution of observed abnormalities
FIG 5: Distribution and prevalence of dorsal vertebral column abnormalities in 10 dogs with disseminated idiopathic skeletal hyperostosis. The number in brackets indicates the number of dogs in which this specific segment was available for review.
June 21, 2014 | Veterinary Record
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Paper In summary, this study demonstrated a possible association between DISH formation and hypertrophy of dorsal vertebral structures, potentially resulting in vertebral canal stenosis. Although DISH is often encountered as an incidental radiological finding, attention should be paid to, possibly clinical important, abnormalities of the dorsal vertebral structures. In agreement with the study of Ortega and others (2012), we conclude that the diagnostic imaging evaluation of dogs with DISH should include the mobile vertebral segments immediately adjacent to the region of fusion.
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Dorsal vertebral column abnormalities in dogs with disseminated idiopathic skeletal hyperostosis (DISH) S. De Decker and H. A. Volk Veterinary Record 2014 174: 632 originally published online May 14, 2014
doi: 10.1136/vr.102492 Updated information and services can be found at: http://veterinaryrecord.bmj.com/content/174/25/632
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Paper Dorsal vertebral column abnormalities in dogs with disseminated idiopathic skeletal hyperostosis (DISH) S. De Decker, H. A. Volk Although disseminated idiopathic skeletal hyperostosis (DISH) most often affects the ventral aspect of the vertebral column, this study evaluated the occurrence, nature and clinical relevance of dorsal vertebral column abnormalities in 10 dogs with DISH for which CT or MRI and a complete neurological examination were available. Dorsal vertebral column abnormalities were present in eight dogs and included articular process hypertrophy (n=7 dogs), periarticular new bone formation (n=1), pseudoarthrosis between spinous processes (n=4) and thickening of the dorsal lamina (n=4). These dorsal vertebral abnormalities caused clinically relevant vertebral canal stenosis in six dogs and were the only cause of clinical signs in four of these dogs. Although the lumbosacral joint was not affected by DISH, these six dogs demonstrated lumbosacral vertebral canal stenosis and clinical signs of cauda equina compression, which included paraparesis (n=5 dogs), lumbosacral pain (n=4), urinary incontinence (n=4), faecal incontinence (n=1) and urinary and faecal incontinence (n=1). There is a possible association between DISH and hypertrophy of dorsal vertebral structures, potentially resulting in vertebral canal stenosis. Although these changes occurred at segments fused by DISH, they predominantly affected adjacent non-affected segments.
Introduction
Diffuse idiopathic skeletal hyperostosis (DISH) is a systemic disease characterised by calcification and ossification within soft tissues of both the axial and the appendicular skeleton (Resnick and Niwayama 1976, Kranenburg and others 2011). Although DISH is relative commonly encountered in humans (Holton and others 2011), only a few reports have discussed its presence in dogs (Kranenburg and others 2011, Ortega and others 2012). A recent radiographic study has estimated the prevalence of DISH to be 3.8 per cent in clinically normal dogs with a significantly higher prevalence in older animals, males and the Boxer breed (Kranenburg and others 2010). Although DISH can affect multiple anatomical structures, it affects most typically the ventral longitudinal ligament, resulting in the formation of contiguous bone ventral to the vertebral column with complete bony fusion of consecutive vertebral segments (Kranenburg and others 2011). There is debate considering the diagnostic criteria for DISH in dogs (Greatting and others 2011, Ciepluch and others 2013). To improve comparisons with human medicine, three criteria have been suggested to confirm a diagnosis of DISH in dogs: (1) flowing calcification and ossification along the ventrolateral aspect of at least four contiguous vertebral bodies; (2) preservation of the intervertebral disc width and the absence of overt radiographic changes indicative of degenerative Veterinary Record (2014) S. De Decker, DVM, PhD, MvetMed. DipECVN, H. A. Volk, DVM, PhD, DipECVN, Department of Veterinary Clinical Science and Services, The Royal Veterinary College, University of London, Hawkshead Lane, North Mymms, Hertfordshire AL97TA, UK;
doi: 10.1136/vr.102492 E-mail for correspondence: [email protected] Provenance: not commissioned; externally peer reviewed Accepted April 9, 2014
intervertebral disc disease; and (3) the absence of articular process ankylosis, sacroiliac joint erosion, sclerosis or intra-articular osseous fusion (Resnick and Niwayama 1976, Greatting and others 2011). However, several case reports have reported dogs in which prominent abnormalities were associated with dorsal vertebral structures, including the articular and spinous processes (Woodard and others 1985, Morgan and Stavenborn 1991, Ciepluch and others 2013, Kornmayer and others 2013). Therefore, additional diagnostic criteria have been proposed in dogs that include dorsal vertebral column abnormalities (Morgan and Stavenborn 1991). The clinical relevance of DISH in dogs has not been fully determined (Kranenburg and others 2011). DISH is usually an incidental radiological finding not associated with clinical signs. Reported clinical signs of DISH in dogs include stiffness, and axial and appendicular skeletal pain (Woodard and others 1985, Morgan and Stavenborn 1991, Kranenburg and others 2011). Several human and veterinary studies have suggested that spinal stiffness associated with DISH could biomechanically predispose to adjacent segment disease, vertebral canal stenosis, vertebral subluxations and spinal fractures after minor trauma (Pascal-Mousselard and others 2006, Chi and others 2008, Kawabori and others 2009, Westerveld and others 2009, Koizumi and others 2010, Holton and others 2011, Ortega and others 2012, Kornmayer and others 2013). It has been postulated that DISH in dogs may result in biomechanical changes comparable to spinal fusion (Ortega and others 2012). In vitro biomechanical and experimental animal studies have demonstrated progressive degenerative changes of the articular and spinous processes after spinal fixation (Cramer and others 2004, Little and others 2004, Cramer and others 2010, Homb and Henderson 2012). However, little is known about the occurrence of such changes in dogs with DISH. Therefore, the primary goal of this study was to evaluate the occurrence of dorsal vertebral column abnormalities in dogs with DISH. The secondary aims were to report the clinical relevance and associated clinical signs of these changes. June 21, 2014 | Veterinary Record
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Paper Materials and methods
The digital database of the Small Animal Referral Hospital, Royal Veterinary College, University of London, was searched between 2007 and 2013 for dogs diagnosed with DISH. Used search terms included DISH. Patients were included if they had (1) complete medical records available, if (2) a complete neurological examination was performed, and if (3) MR or CT imaging of the vertebral column demonstrated complete osseous fusion of at least four adjacent vertebral segments (Resnick and Niwayama 1976). Dogs were excluded if the clinical records or diagnostic imaging studies were incomplete or were unavailable for review. Because of difficulties in assessment of articular process abnormalities on survey radiographs (De Decker and others 2011), dogs with only spinal radiographs available were not included in this study. Information retrieved from the medical records included signalment, duration and type of clinical signs before presentation, general physical and neurological examination findings, results of ancillary diagnostic tests, details of CT and MR imaging studies, final diagnosis, treatment and follow-up data. MR and CT imaging examinations were performed under general anaesthesia. Although anaesthesia protocols could vary between individual cases, a commonly used protocol included premedication with a combination of acepromazine (0.01 mg/kg intravenously) and methadone (0.1–0.2 mg/kg intravenously), followed by induction with propofol (4–6 mg/kg intravenously) and maintenance of general anaesthesia with isoflurane in oxygen. MRI was performed with a 1.5T magnet (Intera, Philips Medical Systems, Eindhoven, the Netherlands) and included a minimum of T2 and T1-weighted sagittal and transverse sequences. The images of the transverse plane were aligned perpendicular to the respective intervertebral disc spaces. CT imaging
was performed by a 16-slice helical CT scanner (PQ 500, Universal Systems, Solon, Ohio, USA). After completion of the transversal CT study, sagittal, dorsal and three-dimensional reconstructions were made. All imaging studies were reviewed by the first author (SDD) using Osirix Dicom viewer (Osirix Foundation, V.5.5.2 Geneva, Switzerland). Emphasis was placed on assessment of dorsal vertebral abnormalities, such as periarticular new bone formation, articular process hypertrophy, pseudoarthrosis between adjacent spinous processes and laminar thickening. Short-term follow-up information was retrieved from r e-examination visits at our institution. Long-term follow-up information was obtained by a telephone interview with the referring v eterinary surgeon. All follow-up information was retrieved by the first author (SDD).
Results
Ten dogs were included in this study (Table 1). Dogs underwent MR imaging as the only diagnostic technique (n=6 dogs), CT as the only diagnostic technique (n=1) or a combination of CT and MRI (n=3). Survey radiographs from the referring veterinary surgeon were available for three dogs. The complete spine was imaged in two dogs, the thoracic, thoracolumbar, lumbar and lumbosacral spine in five dogs and the thoracolumbar, lumbar and lumbosacral spine in three dogs. In two dogs, no changes affecting dorsal vertebral structures were noted. One of these dogs (case 1) was neurologically normal and DISH was considered an incidental finding, while the other dog (case 2) demonstrated a stiff pelvic limb gait and lumbar and lumbosacral hyperaesthesia on palpation. Although not considered clinically relevant, these two dogs demonstrated additional spondylosis deformans at the lumbosacral junction without intervertebral disc degeneration.
Table 1. Clinical presentation, imaging findings, treatment and outcome of 10 dogs with DISH Case
Signalment
Clinical presentation
DISH
Dorsal vertebral changes
Cause of clinical signs
Treatment
Follow-up
1
Boxer, 7y9m, Fn
T10-L3
None
Syncope
None
2
Golden Retriever, 3y, Fn Boxer, 7y8m, Mn
Two collapse episodes. Neurological examination unremarkable Stiff PL gait and spinal hyperaesthesia of 7d duration Progressive ataxia and proprioceptive deficits PLs of 5m duration LS hyperaesthesia and proprioceptive deficits right PL of 14d duration
L3-L7
None
DISH
T6-L2
Hypertrophy left articular processes T13-L1 and L1-L2 Periarticular new bone formation L4-L5 and L5-L6. Pseudoarthrosis L¬2-L3 Hypertrophy articular processes L7-S1, thickened lamina L7, pseudoarthrosis T5-L5
Presumed degenerative myelopathy Discospondylitis L7-S1
Meloxicam and gabapentin Physiotherapy
Euthanasia 5y3m after diagnosis unrelated to study Static condition 5m after diagnosis Euthanasia 5.5m after diagnosis
3
T12-L6
Analgesia, antibiotics
Euthanasia 14d after diagnosis
Restricted exercise, prednisolone
Euthanasia 15m after diagnosis unrelated to study. Remained urinary incontinent
Meloxicam, gabapentin, physiotherapy Restricted exercise and meloxicam
Euthanasia 3.5m after diagnosis. Remained urinary incontinent Euthanasia 3w after diagnosis. Remained urinary incontinent
LSS
Lumbosacral dorsal laminectomy
Improved, but still u rinary incontinent 3y4m after surgery
Hypertrophy articular processesL7-S1, thickened lamina L7
LSS
Lumbosacral dorsal laminectomy
Hypertrophy articular processes L7-S1, pseudoarthrosis L1-L2
LSS
None
Full recovery Recovered faecal continence. Fibrotic myopathy 2m after surgery. Receives hydro -and physiotherapy 9m after surgery Euthanasia at moment of diagnosis
4
Great Dane, 4y7m, M
5
Giant Schnauzer, 11y6m, Fn
Lethargy, ataxia and paresis PLs, proprioceptive deficits all limbs, cervical and LS h yperaesthesia, urinary incontinence of 7d duration
L2-L7
6
Boxer, 10y2m, Mn
T7-L7
Hypertrophy articular processes L7-S1
7
Boxer, 10y11m, Mn
T7-L7
Hypertrophy articular processes L7-S1, thickened lamina L7
8
Cross breed, 10y7m, Fn
T2-L7
Hypertrophy articular processes L7-S1, thickened lamina L7, pseudoarthrosis T12-L2
9
German Shepherd, 6y10m, Fn
Ataxia and paresis PLs, LS hyperaesthesia, urinary incontinence of 1m duration Paraparesis, proprioceptive deficits and decreased spinal reflexes PLs, decreased perianal sensation, and urinary incontinence of 2m duration Paraparesis, p roprioceptive deficits and decreased withdrawal reflexes PLs, LS, absent perianal reflex, flaccid tail and urinary incontinence of 2m duration Lumbosacral hyperaesthesia, absent perianal reflex, flaccid tail of 8m duration. Faecal incontinence of 2w duration
T13-L7
10
Beagle, 9y3m, Fn
T11-L7
Flaccid tail, absent perianal reflex, urinary and faecal incontinence of 3d duration
LSS, multiple cervical intervertebral disk protrusions, immune mediated haemolytic anemia LSS, Presumed degenerative myelopathy LSS
d, days; Fn, female neutered; LS, lumbosacral; LSS, lumbosacral stenosis; M, male; m, months; Mn, Male neutered; PL, pelvic limb; w, weeks; y, years.
Veterinary Record | June 21, 2014
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Paper The remaining eight dogs (cases 3–10) were neurologically abnormal and demonstrated a variable degree of changes affecting the dorsal vertebral column. Although not considered to be the cause of clinical signs, seven of these eight dogs also demonstrated lumbosacral spondylosis deformans and lumbosacral intervertebral disc degeneration with mild-to-moderate protrusion. The presence of lumbosacral discospondylitis precluded evaluation of intervertebral disc degeneration and protrusion in one dog (case 4). In two of these dogs (cases 3 and 4), neither DISH nor the dorsal vertebral column changes were considered to be the cause of neurological deficits (Table 1). One dog of these two dogs (case 3) demonstrated thoracolumbar articular process hypertrophy without spinal cord compression, while the other dog (case 4) demonstrated pseudoarthrosis between the base of several lumbar spinous processes and a variable degree of lumbar periarticular new bone formation (Table 1). Clinical signs in these two dogs were attributed to presumed canine degenerative myelopathy (homozygous SOD-1 mutation) (case 3) and lumbosacral discospondylitis (case 4). The remaining six dogs (cases 5–10) demonstrated clinical signs that could, at least in part, be explained by dorsal vertebral column changes. These dogs demonstrated extensive DISH formation including L7, but not the lumbosacral joint. They also demonstrated prominent dorsal vertebral column changes resulting in lumbosacral vertebral canal stenosis. More specifically, these abnormalities included severe hypertrophy of the lumbosacral articular processes (n=6 dogs) and a thickened dorsal lamina of L7 (n=4 dogs) (Figs 1–3). Pseudoarthrosis of the thoracolumbar and lumbar spinous processes was seen in three of these dogs (Table 1) (Fig 4). These six dogs demonstrated clinical signs consistent with cauda equina compression, including paraparesis (n=5 dogs), lumbosacral hyperaesthesia on palpation (n=4), flaccid tail (n=3), urinary incontinence (n=4), faecal incontinence (n=1) or a combination of urinary and faecal incontinence (n=1) (Table 1). Although not considered to be the main cause of clinical signs, these dogs also demonstrated lumbosacral spondylosis deformans and intervertebral disc degeneration with mild-to-moderate disc protrusion. Concurrent neurological disorders were present in two of these six dogs; one dog (case 5) was also diagnosed with multiple cervical intervertebral disc protrusions between C3 and C7, while the other dog (case 6)
was presumptively diagnosed with canine degenerative myelopathy (homozygous SOD-1 mutation). Both dogs were managed medically. Although they remained urinary incontinent, they were ultimately euthanised for reasons other than lumbosacral disease (Table 1). In the four remaining dogs (cases 7–10), stenosis of the lumbosacral vertebral canal, associated with severe hypertrophy of the articular processes and laminar thickening, was considered to be the only cause of clinical signs. One of these dogs was treated medically with a combination of restricted exercise and meloxicam (case 7), two were treated surgically by a dorsal laminectomy (cases 8 and 9) and the remaining dog was euthanised at the time of diagnosis (case 10). The medically treated dog (case 7) did not improve and was euthanised three weeks after diagnosis. One of the surgically treated dogs (case 8) improved remarkably after surgery, but remained urinary incontinent. The other surgically treated dog (case 9) regained a neurologically normal status, but developed bilateral fibrotic myopathy of the gracilis muscle two months after surgery. This dog still visits our institution for weekly hydro- and physiotherapy sessions nine months after surgery.
Discussion
This study assessed the occurrence and nature of dorsal vertebral column abnormalities in dogs with DISH. Dorsal vertebral column changes occurred both at segments fused by DISH and adjacent nonaffected vertebral segments (Table 1 and Fig 5). Several dogs of this study demonstrated hypertrophy of dorsal vertebral structures, leading to lumbosacral vertebral canal stenosis (Figs 1–3). Radiological or clinical evidence of lumbosacral intervertebral disc disease has been reported in dogs with DISH (Kranenburg and others 2011, Ortega and others 2012). Although these previous studies did not specifically focus on abnormalities of the lumbosacral vertebral canal, they favour the hypothesis that lumbosacral vertebral canal stenosis in dogs with DISH might be more common than previously considered. Although all clinically affected dogs in this study demonstrated mildto-moderate lumbosacral intervertebral disc protrusion, cauda equina compression was predominantly dorsal in direction and caused by severe articular process hypertrophy (Figs 1 and 2). Other observed dorsal vertebral column abnormalities were periarticular new bone
FIG 1: Sagittal T1-weighted (a) and a transverse CT image at the lumbosacral junction (b) of an almost seven-year-old female German shepherd dog with disseminated idiopathic skeletal hyperostosis and lumbosacral vertebral canal stenosis (case 9). Transverse CT image at the level of the lumbosacral junction of a neurologically normal seven-year-old female German shepherd dog (c). (a) Although there is mild lumbosacral intervertebral disc protrusion, cauda equina compression is mainly dorsal in direction (arrow). When compared with (c), it is obvious that lumbosacral vertebral canal stenosis (b) is predominantly caused by articular process hypertrophy (arrows).
June 21, 2014 | Veterinary Record
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Paper
FIG 2: Transverse CT image at the level of the lumbosacral joint (a) and a three-dimensional reconstructed CT image (b) of a 10-year -7-month-old female Beagle (case 10) with disseminated idiopathic skeletal hyperostosis and lumbosacral stenosis. Severe hypertrophy of the articular processes and periarticular new bone formation distort the normal vertebral anatomy and are the main cause of severe lumbosacral vertebral canal stenosis (arrows). Transverse CT image (c) at the level of the lumbosacral joint and a three-dimensional reconstructed CT image of a neurologically normal four-year-old female cross breed dog (d) for comparison.
formation, pseudoarthrosis between the base of adjacent spinous processes and thickening of the dorsal lamina (Figs 3 and 4). The nature of these dorsal vertebral changes is uncertain. Prominent dorsal vertebral column abnormalities have been reported in dogs with DISH, and although controversial, such changes have even been considered to represent a diagnostic criterion for dogs with DISH (Woodard and others 1985, Morgan and Stavenborn 1991, Ciepluch and others 2013).
Therefore, it is possible that the dorsal vertebral column changes observed in this study represent a variation of lesion distribution in dogs with DISH. It can however not be excluded that these abnormalities represent a biomechanical consequence of DISH. The contiguous new bone formation has been suggested to cause decreased flexibility with increased stiffness of the affected vertebral segments. This can result in altered biomechanics on adjacent mobile segments
FIG 3: Transverse CT images at the level of L7 (a) and sagittal reconstructions (b) of and an almost seven-year-old female German shepherd dog with disseminated idiopathic skeletal hyperostosis (DISH) (case 9) and lumbosacral stenosis and a neurologically normal seven-yearold female German shepherd dog (c and d) The German shepherd dog with DISH demonstrates thickening of the dorsal lamina of L7 and less obviously of L4, L5 and L6. This is best appreciated on the transverse images (a). The thickness of the dorsal lamina in (a) is similar to the height of the vertebral body, while the dorsal lamina in (c) is much thinner than the height of the vertebral body. Hypertrophy of the lumbosacral articular processes was the main cause of cauda equina compression (arrow in b).
Veterinary Record | June 21, 2014
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Paper Homb and Henderson 2012). An in vitro human biomechanical study demonstrated increased stress and strains of articular processes at the mobile adjacent vertebral segments after lumbar spinal fixation (Little and others 2004). The results of this study contribute further to the controversy regarding appropriate diagnostic criteria for DISH in dogs. The generally accepted criteria of Resnick and Niwayama (1976) do not include changes affecting the dorsal vertebral column. It specifically excludes patients with articular process joint bony ankylosis, sacroiliac joint erosion, sclerosis or intra-articular osseous fusion. Although it is unclear whether articular process hypertrophy and periarticular new bone formation should be considered ‘articular process joint bony ankylosis’, the results of the study presented here do not favour following strictly the ‘Resnick’ criteria for DISH in dogs. In contrast, the diagnostic criteria proposed by Morgan and Stavenborn (1991) require dorsal vertebral column changes, specifically periarticular new bone formation or pseudoarthrosis between the bases of the spinous processes, to be present before a diagnosis of DISH can be made. Although most dogs of the present study demonstrated such dorsal vertebral abnormalities, this was not present in all cases. Therefore, the results of our study do not favour following these strict ‘Morgan’ criteria either. It is well known that both dogs and people with DISH can present with a variety in lesion distribution and localisation (Kranenburg and others 2013). This has led to a multitude of terms to refer to this disorder in people and highlights the difficulty of correctly defining and diagnosing DISH (Utsinger 1985). Although the results of this study suggest that DISH can be associated with dorsal vertebral column abnormalities and clinical signs, it is valuable to keep in mind that DISH is an incidental finding in the majority of affected animals (Kranenburg and others 2011). The results of the study presented here are unlikely to represent the overall prevalence of dorsal vertebral column abnormalities in dogs with DISH. Dogs had to have MR or CT imaging and a complete neurological examination performed before they could be included in this study. This likely caused a selection bias towards dogs with neurological or suspected neurological disorders. It is further unclear why some dogs with DISH develop dorsal vertebral column changes, while others do not. All dogs with lumbosacral vertebral canal stenosis had extensive DISH formation including L7. It is possible that the location and length of the affected vertebral segments play key roles in the development of these changes. However, the number of included animals in this study was too small to investigate this hypothesis. Further, several dogs of this study demonstrated concurrent spinal disorders, such as discospondylitis and presumptive degenerative myelopathy. Therefore, we cannot exclude that the occurrence of dorsal vertebral abnormalities was not influenced by the presence of these concurrent spinal disorders.
FIG 4: Sagittal reconstructed CT (a) and sagittal T1-weighted MR (b) image of an 11-year-6-month-old female Giant Schnauzer with disseminated idiopathic skeletal hyperostosis (case 5). Pseudoarthrosis is present between the bases of several adjacent lumbar spinous processes (white arrows).
(Kranenburg and others 2011). Adjacent segment disease has recently been reported in dogs with DISH and has been characterised by degenerative changes of the remaining mobile vertebral segment adjacent to fused, normally mobile, vertebral segments (Ortega and others 2012). In the present study, all dogs with lumbosacral vertebral canal stenosis had extensive DISH formation including L7, but not involving the lumbosacral joint. It is possible that the fused lumbar vertebral column caused increased biomechanical stresses on the lumbosacral junction where still some mobility persisted. Next to altered biomechanical forces at adjacent vertebral segments, it is also possible that fusion of ventral vertebral structures induces altered biomechanics on the dorsally unaffected anatomical structures. The hypothesis that these dorsal vertebral column changes could represent a biomechanical consequence of DISH is further supported by several experimental studies. Laboratory animal studies have demonstrated progressive degenerative changes of the articular processes and spinous process hypertrophy as a direct result of experimentally induced caudal lumbar spinal hypomobility. Although these degenerative changes occurred at both fused and non-fused segments, they were more severe at the fixed vertebral segments (Cramer and others 2004, Cramer and others 2010,
Prevalence of observed abnormalities
100
Dorsal Vertebral Changes
DISH
90 80 70 60 50 40 30 20 10
L7-s (n=10)
T1-L7 (n=10)
T1-L6 (n=10)
T1-L5 (n=10)
T1-L4 (n=10)
T1-L3 (n=10)
T1-L2 (n=10)
T1-L1 (n=10)
T1-T13 (n=9)
T1-T12 (n=9)
T1-T11 (n=8)
T1-T10 (n=8)
T1-T9 (n=7)
T1-T8 (n=7)
T1-T7 (n=7)
T1-T6 (n=7)
T1-T5 (n=7)
T1-T4 (n=7)
T1-T3 (n=7)
T1-T2 (n=6)
C7-T1 (n=6)
C6-C7 (n=6)
C5-C6 (n=5)
C4-C5 (n=3)
C3-C4 (n=2)
C2-C3 (n=2)
C1-C2 (n=2)
0
Distribution of observed abnormalities
FIG 5: Distribution and prevalence of dorsal vertebral column abnormalities in 10 dogs with disseminated idiopathic skeletal hyperostosis. The number in brackets indicates the number of dogs in which this specific segment was available for review.
June 21, 2014 | Veterinary Record
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Paper In summary, this study demonstrated a possible association between DISH formation and hypertrophy of dorsal vertebral structures, potentially resulting in vertebral canal stenosis. Although DISH is often encountered as an incidental radiological finding, attention should be paid to, possibly clinical important, abnormalities of the dorsal vertebral structures. In agreement with the study of Ortega and others (2012), we conclude that the diagnostic imaging evaluation of dogs with DISH should include the mobile vertebral segments immediately adjacent to the region of fusion.
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Dorsal vertebral column abnormalities in dogs with disseminated idiopathic skeletal hyperostosis (DISH) S. De Decker and H. A. Volk Veterinary Record 2014 174: 632 originally published online May 14, 2014
doi: 10.1136/vr.102492 Updated information and services can be found at: http://veterinaryrecord.bmj.com/content/174/25/632
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