Cervical vertebral malformations in 9 dogs: radiological findings, treatment options and outcomes

Atlantoaxial pseudoarthrosis

In humans, pseudoarthrosis between the posterior arch of the atlas and the lamina of the axis was first reported by in 1951 [5]. Viallet [5] speculated that the contact of the atlas and axis was similar to Baastrup disease of degenerative lumbar spine, in which spinous processes contact each other closely. However, the exact mechanism of its occurrence is unclear, and reports about the relationship between such findings and clinical symptoms are scarce [6–9]. Therefore, there have been few reports showing whether the pseudoarthrosis caused any clinical symptoms such as cervical myelopathy [6–9]. Assuming that the interpretation of osteophyte formation is pseudoarthrosis, there have been only two human patients with diffuse idiopathic skeletal hyperostosis (DISH) [6, 7] and one with KFS in which osteophytes were formed at the pseudoarthrosis site of C1-C2 caused cervical myelopathy [8]. Myiakoshi and colleagues also reported atlantoaxial pseudoarthrosis associated with a chondroma in a 58-years old man [9].

The occurrence of pseudoarthrosis between the dorsal (posterior) arch of the atlas and the lamina of the axis has been recognized as one of the radiologic features occurring at the upper cervical spine [5–9] (Fig. 1a). In our canine cases, osteophytes were formed at the pseudoarthrosis between the dorsal arch of the atlas and the lamina of the axis, causing myelopathy at this level. Our cases did not reveal malformations of the dorsal arch of the atlas. Therefore, we suggest that instability may be the main trigger for the development of pseudoarthrosis, which in association with the close contact of the dorsal arch of the atlas and the lamina of the axis may well be contributory to the subsequent massive osteophyte formation. Interestingly, these abnormalities were detected in young dogs while the human case reports were described in elderly humans. In humans, pseudoarthrosis was diagnosed in combination with osteochondromas, Klippel-Feil syndrome and DISH. These underlying aetiologies were not detected in our population. Therefore, we speculate that clinically relevant atlantoaxial pseudoarthrosis in young dogs has a different (congenital or developmental) aetiology.

In the human literature, decompressive surgical interventions resulted in good outcomes [6–9]. This was another difference noticed with our canine population. In case 2, decompressive spinal cord surgery led to a relapse of the clinical signs and consequently to a ventral stabilisation. In case 1, ventral stabilization was performed in the first instance which resulted in resolution of the clinical signs (Fig. 1e). This difference suggests that instability has a more significant role in the development of the clinical signs than compression. This finding potentially suggests a different aetiology for the development of pseudoarthrosis in humans and dogs. However, definitive conclusions are impossible to reach given the small number of cases.

(Congenital) atlantoaxial rotatory displacement (CARD)

The term atlantoaxial rotatory displacement have been used to describe a spectrum of rotational abnormalities of the atlantoaxial joint observed in the absence of major trauma [10]. The degree of rotation of the atlas depends on the integrity of the ligamentous structures [10]. Although the transverse ligament is the primary stabiliser to prevent dorsal displacement of the atlas, the alar ligaments are also vital to prevent excessive rotation of the atlas [11]. Atlantoaxial rotatory subluxation has been noted to occur in paediatric human patients with developmental disorders including juvenile rheumatoid arthritis, Down syndrome, and Morquio Syndrome [12, 13]. The underdevelopment of the cervical musculature, incomplete ossification of the odontoid process and overall ongoing immature bone ossification, a larger head to body mass ratio, and ligamentous laxity contributes to segmental hypermobility that may predispose the immature atlantoaxial region to injury [10, 12, 13]. In addition, the fulcrum of motion in the immature cervical spine is at the level of C2–C3, rather than the caudal cervical spine in adults [12, 13]. Therefore, in the paediatric patient, the atlantoaxial region is predisposed to several anatomic and biomechanical factors that increase its susceptibility to injury [12].

CARD is a radiographic diagnosis and asymmetry in size of the articular facets of C2 raises the suspicion for this diagnosis [14]. Pathologic findings identified in chronic cases include contracture of the periarticular soft tissues, interposition of fibrous tissue, osseous cross union, and adaptive changes in facet morphology [14]. Subsequently, a CT scan can help in aiding the diagnosis, especially in mild cases, and a dynamic CT study can help in distinguishing fixed from flexible deformities [14]. In humans, the normal cervical rotation is approximately 70°-80° to each side and the maximum divergence between C1 and C2 during normal rotation to either side ranges from 29° to 45° [13]. Important concerns include how C1 and C2 move relative to one another throughout the arc of rotation (C1-C2 angle or angle of separation) and whether C1 crosses over C2 [14]. This is a limitation in veterinary medicine and imaging protocols should be performed in order to establish the physiological degree of rotation in the paediatric and adult dog as recognising an early diagnosis improves outcomes.

Atlantoaxial rotatory subluxation present for longer than 6 weeks may result in chronic ligamentous changes that can increase the risk of failure to respond to conservative treatment [15]. To prevent neurologic injury, reduce the CARD deformity, prevent dislocation recurrence, and maintain sagittal balance, posterior fixation with fusion from the occiput to C4 has been described in the human literature, especially in cases of CARD associated with Klippel-Feil syndrome [13]. In our case, ventral atlantoaxial stabilisation was followed by a dorsal laminectomy for decompression of the spinal cord. It is possible that this second procedure may have contributed to some degree of instability. In the human literature, decompression has not been reported for cases of CARD. Therefore we speculate that this may have been the cause of neurological deterioration after an initial clinical improvement. However, the chronic history of tetraparesis associated with chronic ligamentous changes may have contributed to the poor long-term outcome. The authors are unsure if more extensive stabilisation may have contributed to a better long-term outcome. However, no obvious evidence for atlanto-occipital or C2-C3 dorso-ventral instability were noticed on follow-up CT myelograms. The presence of stainless steel implants prevented follow-up MRI which might have provided evidence of increased motion at the occiput-C1 articulation. Another limitation in this case was the absence of dynamic CT scans before and after clinical resolution. Therefore we could not prove that normal dynamics was restored after the initial surgery.

Klippel-Feil syndrome

KFS is a complex, congenital condition that was initially reported in 1912 by Maurice Klippel and Andre Feil [16]. Studies have shown that 34 to 74% of KFS Human patients present with a low posterior hairline, short neck, and limited neck range of motion [16, 17]. However, the “hallmark” of this condition is the improper segmentation of cervical vertebral bodies with congenitally fused vertebrae [18]. KFS has been associated with other skeletal malformations such as rib anomalies and hemivertebrae; and scoliosis [18]. The incidence of KFS in the human population is believed to occur once in every 40,000 births [18] and up to 50% of paediatric KFS patients are symptomatic [16].

Mutations in the PAX gene family have been implicated in development of this syndrome [17]. Genetic testing has been performed in one case report of Klippel-Feil syndrome associated with Sprengel disease in a dog [19]. However, the underlying mutation responsible for the findings in that case could not be identified. In both cases presented in our study, genetic testing was not performed.

Samartzis and colleagues [16] proposed a radiographic classification scheme of congenitally fused cervical segments in patients with KFS. This classification scheme included three different criteria. Type I was defined as having a single congenitally fused cervical segment, Type II demonstrated multiple non-contiguous congenitally fused cervical segments and type III had multiple contiguous congenitally fused cervical segments. Human studies suggested a gender predilection with 60 to 70% of KFS cases occurring in females [16, 17]. However, in Gruber and colleagues retrospective study [18] this predilection could not be confirmed. Interestingly, it appeared to be a greater male predominance with increasing classification type, with the more innocuous Type I cervical fusion pattern occurring more in females, whereas Type III occurs mainly in males. The occurrence of Type II is similar in both males and females. The majority of patients were considered Type II (50%), with Type I (25%) and Type III (25%) demonstrating a similar prevalence. We present two male dogs that were classified as type III according to Samartzis scheme.

Xue and colleagues [17] concluded that in people with KFS and congenital scoliosis there was a mean of 3.29 fused segments from C2–T1. The most commonly fused segments were C2–C3, C3–C4 and C6–C7; each of which was noted in 60.7% of the patients [17]. Thirty two percent of the patients had 2 fused segments, 32.1% had 3 fused segments, 17.9% had 4 fused segments, 10.7% had 5 fused segments, and 7.1% had 6 fused segments. In our study, we observed vertebral fusion at the level of C3-C4 in case 4; and at the level of C2-C3, C3-C4 and C4-C5 in case 5, with failure of formation of the T3 vertebral body (hemivertebrae). With regard to the presence of vertebral malformations in human KFS [20], failure of segmentation was found in 3.6%, failure of formation in 17.9% and mixed deformities in 78.6%. Vertebral anomalies were also frequently seen in the thoracic region (71.4%), followed by lumbar region (17.9%) and thoracolumbar region (10.7%) [20]. Approximately 46 % of the patients with KFS exhibit rib anomalies (fused, bifid and missing ribs) [20]. Congenital scoliosis and rib anomalies were observed in both of our patients suggesting that this may be a common finding in the canine population with KFS. Also, failure of ossification of the sacral vertebrae were observed in case 3. Extra-skeletal anomalies associated with KFS included urological anomalies (35–64%), deafness (30%), congenital heart disease (14%), and Sprengel deformity (30–42%) [21]. In case 5, the urinary incontinence reported could not be clearly attributed to a myelopathy, however no urological disorder was detected and this dog was lost to follow-up after clinical improvement with phenylpropanolamine.

Aplasia of the atlas has been associated with KFS [22]. When segmentation failures of the second and third cervical vertebra occur in association with atlas abnormalities, atlantoaxial instability results due to the abnormal load placed on this motion segment [22]. Therefore, early identification of KFS is paramount to minimize the risk of neurologic injury during daily activities or operative management of such patients [22]. Interestingly, in a cohort of 32 patients with concomitant scoliosis and KFS, only 2 required surgical intervention [23]. The role of prophylactic surgical stabilization in people with isolated neck pain or without symptoms remains controversial [24]. However, persistent radicular symptoms or myelopathy may require surgical decompression and stabilization. Tetraparesis and cervical hyperesthesia were observed in case 4, where there was complete aplasia of the transverse process of the atlas on the left side. However, a gradual neurological improvement was observed. We theorised that the clinical improvement was due to the progressive cervical muscular hypertrophy characteristic of the breed, reduced head: neck ratio and presumed decreased laxity of the cranial cervical ligamentous structures. In our cases, no surgical intervention was required.

Congenital C2-C3 canal stenosis and deficiencies of the dorsal arch

Isolated anomalies of the dorsal (posterior) elements of the axis are rare, with reported prevalence of 0.15% in the human population [25]. Posterior element anomalies may be caused by impairment of fusion between the primary ossification centres lying at the base of the articular process [25]. In humans, headache, neck pain and paresis have been reported symptoms [26]. In most cases, anomalies are found incidentally in asymptomatic patients, when the patient undergoes a radiologic assessment for neck pain, radiculopathy, neck mass or following trauma [26]. Common anomalies of the axis include total or partial absence of the odontoid process, non-fusion of the odontoid process, segmentation failure of the second and third cervical vertebrae [27]. The two cases reported here, were presented with a chronic progressive history of tetraparesis associated with cervical pain. Imaging studies revealed absence of the dorsal laminae of the axis and a cleft at the level of the dorsal neural arch of atlas. These malformations have been suggested to be a result of dysregulated genes expression, incorrect tissue interactions, cellular migration and proliferation [25]. Interestingly, both dogs were Shih Tzus and a genetic breed predisposition could be speculated. However, the small numbers do not allow us to reach a definitive conclusion.

The range of clinical and radiological manifestation in humans makes the proposition of a standard treatment protocol challenging [27, 28]. As a generally accepted rule a conservative approach in asymptomatic patients consisting of rest, administration of analgesics or muscle relaxants, cervical collars and physical therapy is advisable. However, surgery is the ideal treatment for patients with atlantoaxial subluxation [27, 28]. We postulate that the deficiencies in the dorsal laminae of C1 and C2 contributed to moderate instability and increased mechanical loading to the cervical spine, particularly at the level of C2-C3. The presence of mild intervertebral disc degeneration and mild protrusion of the C2-C3 level was indicative of this. The relatively mild protrusion may have exacerbated an already compromised spinal cord from instability, causing a more acute recent deterioration. Give the current evidence in the human literature [25, 26, 28] and the two cases reported, surgery should be the treatment of choice in patients with radiological evidence of instability, intractable long-standing neck pain and neurologic deficits. The surgical management of these cases through ventral stabilisation resulted in a successful long-term clinical outcome for both patients, despite the initial complications associated with implant failure in case 7.

Congenital cervical fusion

A fused vertebra (‘block vertebrae’) is the result of failure of segmentation, attributed to abnormalities of the intersegmental arteries in the developing embryo [29, 30]. The malformation may occur at any point along the vertebral column and may involve part or all of a vertebrae [31, 32]. Often the fused vertebra is shorter in length than the equivalent number of normal segments, and abnormal angulation or stenosis of the vertebral canal may be present [29, 31]. A fused or ‘block’ vertebra is usually an incidental radiographic finding [31]. However, Nouri and colleagues [32] reported a relatively high prevalence (3.9%) of congenital cervical fusion (CCF) in a cohort study of human patients surgically treated with degenerative cervical myelopathy (DCM), suggesting that individuals with congenitally fused cervical vertebrae are at an increased risk of degenerative changes leading to myelopathy. The majority of these cases (78%) consisted of C2-C3 fusion of the posterior elements with complete preservation of the C2–3 intervertebral disc leading to myelopathy C3-C4 [32]. A similar anatomical localisation was observed in case 9. This was most likely related to the fact that C3-C4 was adjacent to a fused level and adjacent levels are known to experience increased biomechanical stress and accelerated degeneration [33]. The trend toward increased degeneration at levels adjacent to fused segments is consistent with observations in post-operative patients that have undergone cervical fusions [32]. Similar findings have been observed in veterinary studies [34, 35].

Interestingly, Nouri and colleagues [32] also reported that CCF patients present with symptoms of myelopathy at an older age than KFS patients (average age of 67.0 years compared with 58.8 years in the KFS group), which may be explained by the fact that a large proportion had fusions at C2–3. Anatomically, the canal at C3–4 in humans is relatively larger compared with C5-C6, making the development of myelopathy likely to require a greater degree of degeneration and thus clinical signs may take longer to manifest [32].

CCF human patients tend to be older, with a greater number of operated levels, and more frequent ossification of the posterior longitudinal ligament [32]. It makes intuitive sense that congenital fusion at C3–4 is more likely to show adjacent segment cord compression at C4–5 than C2–3 because the spinal canal is narrower at this level [33]. Furthermore, this interesting fact was also noticed in our study. Case 9, was presented with a CCF at the level of C2-C3 and DCM at the level of C3-C4. This patient was represented with DCM at the level of C4-C5 after decompressive surgery on the cranial segment. This patient was considerably older (3782 days versus 2010 days) relative to the patient number 8 that was presented with CCF at the level of C4-C5 and DCM at the level of C5-C6, suggesting that the same principle can be applied in humans and dogs. Both dogs diagnosed with fused vertebrae were considerably older than the dogs diagnosed with KFS in our study, favouring the findings observed in this human study (average of 2896 days versus 262.5 days). Despite the rarity of congenital cervical fusion, evidence suggests that CCF predisposes patients to DCM associated with adjacent segment disease.

Surgical discussion

Veterinary studies concerning the surgical management of CVM are reserved to atlantoaxial instability [36–40]. A direct comparison of surgical techniques cannot be made due to different follow-up periods and outcome measures [36]. Other uncontrolled factors influence outcome such as the surgeon’s experience, initial neurological status, age of the dog and chronicity of neurological signs [36].

In the human literature controversy persists regarding the best surgical approach for management of cervical malformations. Anterior decompression by a transoral approach or mandibular split is indicated if spinal cord compression occurs from an anterior position. This approach is optimal for decompression of the cervicomedullary junction [27]. However, compared to the posterior approach, the anterior approach has disadvantages, including a more complicated technique, higher invasiveness, difficulty in primary fixation, higher incidence of postoperative infection, and increased incidence of respiratory tract disorders [27]. Jones and colleagues [41] reported that 7 of 44 patients that underwent an anterior approach, had complications such as dysphagia, nasal regurgitation and infection. In contrast, posterior approaches are increasingly more popular because osseous compression can be resolved by the reduction of abnormally positioned bone without the above-mentioned complications. However, spinal cord decompression could be insufficient if the reduction is not successful [41].

Grosso and colleagues [42] reported that 25% of the human patients suffered with at least one perioperative complication. The most common perioperative complications were thrombosis (10.5%), deep wound infection (7.9%), pneumonia (5.2%), pulmonary embolism (3.9%), postoperative hematoma (3.9%) and dysphagia (2.6%). The overall mortality rate was 4%. Perioperative complication rates with combined ventral and dorsal procedures were higher (40%) compared to ventral-alone (30%), and dorsal-alone (27%) procedures. Implant malposition was present in 5.3% of patients. Sixteen percent of patients underwent revision surgery, which includes 5.2% of patients who underwent revision because of infection. Implant malposition occurred in 10% of patients who underwent the dorsal approach, 10% who underwent the ventral, and 2.5% of patients who underwent the combined approach. Revision surgery was needed in 15, 10, and 18% of cases for the dorsal, ventral, and combined approaches, respectively. In our cases series, no immediately post-operative complications were reported. In case 7, implant failure led to revision surgery which was considered successful. The relapse of the clinical signs 323 days after the initial presentation was attributed to the chondrodystrophic nature of the breed and predisposition to intervertebral disc disease, rather than adjacent segment disease. Grosso found that the ventral approach had similar degrees of reduction, lower complication rates, and possibly greater neurological improvement when compared to the combined approach [42]. These results suggest that a ventral approach alone is an effective method for surgical correction of cervical malformations, and may be safer than the combined approach. This fact could be observed in our population diagnosed with atlantoaxial pseudoarthrosis, where case 2 required a ventral stabilisation after a dorsal decompression (Fig. 1d) while in case 1 a ventral stabilisation alone resulted in resolution of the clinical signs (Fig. 1e). Given the heterogeneity and the limited number of cases in this study, it is difficult to compare ventral and combined approaches. Further studies would be required to determine statistical relevance regarding the relative success of surgical approaches.

The major limitations of this study are its retrospective nature and the limited number of cases. The lack of standardisation of radiological investigations and follow-ups are also limitations as different follow-ups performed at different timings may have resulted in different outcomes. Dynamic studies were not performed in all cases. Some patients were followed-up with radiographs only while others underwent MR or CT scanning which, again may have contribute to a different outcome. The heterogeneity of the population studied also have contributed for the different clinical approaches of the veterinary surgeons responsible for each case.