Surgical stabilization of craniocervical junction abnormalities in two cats

Abstract

Two cats were evaluated because of clinical signs consistent with tetraplegia or ataxia of four limbs and cerebellar signs. The cats were diagnosed with craniocervical junction abnormalities (CJAs) by radiographs, computed tomography and magnetic resonance imaging. Both cats underwent surgical stabilization using a patient-specific titanium atlantoaxial (AA) fixation plate and drill guide templates. In case 2, in addition to AA fixation, the separated dens and the occipital bone compressing the cerebellum were removed. Repositioning and fixation of the AA joint using a custom drill guide template and titanium plate system improved the gait of both cats, but the cerebellar signs persisted. Although CJAs are uncommon in cats, the present cases indicate that surgical stabilization with a custom fixation system may represent a feasible treatment option.

Craniocervical junction abnormalities (CJAs) include Chiari-like malformation, atlantooccipital overlapping, atlantoaxial (AA) instability, occipitoatlantoaxial malformation, AA dural bands, and dens abnormality [7]. They typically affect miniature breed dogs and rarely affect cats [4, 10, 12, 15]. CJAs may be congenital or secondary to trauma [10]. They typically present with neck pain and varying degrees of ataxia in all four limbs. The treatment of CJAs involves surgical stabilization of the craniocervical or AA junction and decompression of the cerebellum and brainstem [7, 10].

AA instability is rare in cats and is treated by ventral fixation [4, 12, 15]. For ventral fixation, the atlas and axis are anchored by screws or Kirschner wires; however, accurate placement of implants is particularly challenging in small animals. We previously reported a custom-made titanium plate and drill guide template system for AA fixation in toy breed dogs, which achieved safe and accurate fixation of AA instability [5]. Here we describe two cases of CJAs in cats, including the clinical signs, magnetic resonance imaging (MRI) and computed tomography (CT) findings, and the fixation technique for AA instability using a custom-made titanium plate.

An 8-month-old spayed female, mixed breed cat (case 1) weighing 2.75 kg was referred to the Japan Animal Referral Medical Center Nagoya with a 7-day history of tetraplegia after falling from a window frame (day 1). The cat was alert and had head and neck tremors. Postural reactions were absent in all four limbs, whereas the spinal reflexes of all limbs and cranial nerve functions were unremarkable. The lesion was clinically localized to the cerebellum and/or C1–C5 spinal cord segments. Radiographs revealed the absence of dens and mildly increased distance between the dorsal arch of C1 and spinous process of C2 on flexed lateral views (Fig. 1A, 1B). CT (ECLOS; Hitachi Medical Corp., Tokyo, Japan) revealed incomplete ossification of the dorsal arch of atlas and synostosis of the occipital bone and atlas (Fig. 1C). 0.3-Tesla MRI (AIRIS VentoLT; Hitachi Medical Corp.) revealed an intramedullary hyperintense lesion on a T2-weighted image (T2WI) (Fig. 1D) and isointense on a T1WI (Fig. 1E) at the level of the AA joint. The lesion showed enhancement after the administration of gadolinium-based contrast (Omniscan intravenous injection; GE Healthcare, Chicago, IL, USA) (Fig. 1F). These MRI findings were consistent with a common finding in spinal cord injuries associated with atlantoaxial instability, known as dens contusions [6]. Based on the radiological and MRI findings, the cat was diagnosed with CJA, occipitalization of the atlas, and AA instability.

Fig. 1.

Diagnostic imaging, intraoperative photograph and postoperative radiograph of the craniocervical junction of case 1. Lateral neutral (A) and flexed (B) radiographs showing slightly widened laminae of C1 and C2 on the flexed view (*). Radiographs (A, B) and sagittal multiplanar reconstruction CT (C) showing lack of the dens and synostosis of occipital bone and atlas (black arrow). Sagittal MRI showing the intramedullary T2-weighted hyperintense (D), T1-weighted isointense (E) and contrast enhanced (F) lesion of the spinal cord at the level of the atlantoaxial (AA) junction (white arrow). Surgical stabilization of the AA junction was performed using a patient-specific titanium AA plate (G). Postoperative radiograph (H) showing realignment of the AA junction and accurate placement of the titanium plate.

The cat was referred to The Animal Medical Center of Gifu University on day 7 after trauma for stabilization of the AA joint. We fabricated a patient-specific titanium AA plate and drill guide templates for the center screw hole of C1 and cranial two screw holes of C2, as described previously [5]. The trajectories of the screws in the atlas and axis were determined based on reconstructed bone images viewed from several optional planes. In the atlas, the screw trajectories were planned to penetrate the midline of the ventral arch at the midpoint in the rostro-caudal direction, with two additional lateral screws inserted into the ventral arch at a slight medial angle. In the axis, four screws were planned for insertion. The cranial screws were positioned at the thickest part of the vertebral body. The original technique was modified by the addition of a screw hole in the center of the cranial part of C2. The caudal screws were placed into the thick part of the caudal vertebral body. A luxated AA junction was reduced to its normal position using reconstructed 3D images in modeling software (Freeform; 3D Systems, Inc., Rock Hill, SC, USA). The surface area of the atlas and axis covered by the titanium plate was determined, and AA plates with a thickness of 1.5 mm were designed with screw holes that matched the predetermined locations and angles. Titanium plate printing was carried out on a 3D printer (Arcam A2X; Arcam AB, Mölndal, Sweden) using Grade 23 titanium Ti6Al4V powder. Drill guide templates for the central screw hole of C1 and the cranial two screw holes of C2 were designed. The platforms of the drill guide templates, which were made to fit the surfaces of each bone, were designed and cylindrical sleeves were attached to the platform to fit and lock the patient-specific 3D shape of the ventral surfaces of C1 and C2. The templates were fabricated from non-soluble acrylic using a 3D printing system (Connex500, Stratasys Ltd., Commerce Way, MN, USA). A neck brace (hold-collar mesh type; Animal Ortho Japan, Komaki, Japan) was applied and prednisolone (predonine tablets; Shionogi Pharma Co., Ltd., Osaka, Japan) 0.5 mg/kg/q48 hr was administered until surgery. On day 39, surgical stabilization using the patient-specific titanium AA plate was performed. The cat was able to stand and walk, though with ataxia. Persistent head and neck tremors was observed, and the postural reactions were decreased in all four limbs. The cat was anesthetized according to standard protocols and maintained with isoflurane in oxygen. The cat was placed in a dorsal recumbent position and autologous cancellous bone was harvested from the proximal humerus for bone grafting. The approach to the AA junction was described previously [9]. Because the cat was held in neck extension, the AA alignment was in a normal position. No dynamic assessment was performed, and no obvious intraoperative instability was identified. To expose the AA junction, capsulotomy was performed and articular cartilage was removed using a round burr and bone curette. The drill holes were made using 0.9-mm Kirschner wires and the patient-specific drill guide templates. After the autologous bone graft was placed in the AA joint space, the titanium plate was fixed with 1.2-mm-diameter titanium cortical screws (Universal CFM bone screw, cross-pin, self-tapping; Stryker, Kalamazoo, MI, USA) (Fig. 1E). The side screw holes of C1 and caudal two screw holes were made free-hand using the titanium plate. The titanium plate was fixed with 1.2-mm-diameter titanium cortical screws. The postoperative radiograph and CT confirmed alignment of the AA junction and appropriate placement of the titanium plate and screw (Fig. 1G). The cat was discharged 48 hr postoperatively and a neck brace was applied for 3 months.

On day 53, the cat was able to stand up and walk without support, with subjectively improved stability compared with the preoperative condition, although head and neck tremors persisted. One year after the surgery, the cat still showed ataxia of all four limbs and head and neck tremors; however, the cat was able to run and jump onto a table, suggesting a functional improvement in gait. Follow-up radiographs performed on days 60, 72, 107 135, and 226 (Fig. 1H), and CT performed on day 444, showed appropriate alignment of the AA junction without dislocation of the screws or titanium plate.

A 6-month-old male, mixed breed cat (case 2) weighing 2.60 kg was referred to The Animal Medical Center of Gifu University with a 2-week history of falls toward the left side and circling clockwise (day 1). The cat was alert and had dysmetria and ataxia in all four limbs. The postural reactions were decreased in the pelvic limbs, whereas the spinal reflexes were unremarkable. The lesion was clinically localized to the cerebellum. Radiographs revealed dysraphism of the dens and an increased distance between the dorsal arch of C1 and spinous process of C2 on the flexed lateral view (Fig. 2A, 2B). CT (Alexion; Canon Medical Systems Corp., Otawara, Japan) revealed an occipital bone deformity, with the edge of the foramen magnum bent inward and indenting on the cerebellum (Fig. 2C). 3-Tesla MRI (Achieva dStream; Philips, Amsterdam, Netherlands) revealed an enlarged lateral ventricle without periventricular hyperintensity on a T2WI (Fig. 2D) and FLAIR images. Since there were no findings of increased intracranial pressure, such as obscuration of the cerebral sulcus or brain herniation, it was determined that treatment was not indicated. The caudal cerebellum had a linear signal void on a sagittal T2WI and T1WI, suggesting occipital bone invagination (Fig. 2E). The spinal cord was mildly kyphotic at the level of the atlas, and there was dorsal compression by the AA band. Based on the radiological, CT and MRI findings, the cat was diagnosed with CJA, an occipital bone deformity, and AA instability.

Fig. 2.

Diagnostic imaging, postoperative and follow-up radiographs of the craniocervical junction of case 2. Lateral neutral (A) and flexed (B) radiographs showing slightly widened laminae of C1 and C2 on the flexed view (*) and subluxation of the atlantoaxial (AA) junction. Sagittal multiplanar reconstruction CT (C) showing dens dysraphism (black arrow). MRI of the brain revealed enlargement of the lateral ventricles without periventricular hyperintensity or obscuration of the sulci (D). CT and MRI showing an occipital bone deformity, with inward indentation of the edge of the foramen magnum and a linear signal void on the sagittal plane in the T2WI, suggesting invagination into the caudal cerebellum (E) (white arrow). Postoperative radiographs (F) showing realignment of the AA junction and accurate placement of the titanium plate. Follow-up radiograph performed 2 months after surgery showing loosening of the C1 left and center screws (G). At 1 year, the C1 right screw was completely displaced (H). However, CT revealed hyperostosis around the titanium plate (arrowhead) without alignment irregularity of the AA junction (I).

To stabilize the AA joint, we fabricated a patient-specific titanium AA plate and drill guide templates, similar to those fabricated for the first case. A neck brace (hold-collar mesh type; Animal Ortho Japan) was applied until surgery. On day 30, the cat underwent surgical stabilization of the AA joint. At that time, the cat exhibited dysmetria and ataxia in all four limbs, and reduced postural responses of the pelvic limbs as on day 1. The cat was anesthetized according to standard protocols and maintained with isoflurane in oxygen. First, the cat was placed in a dorsal recumbent position during surgical stabilization using the patient-specific titanium AA plate. After harvesting the autologous cancellous bone, the AA junction was exposed and the separated dens was removed by cutting the ligaments attached to the dens. Because the cat was held in neck extension, the AA alignment was in a normal position. No dynamic assessment was performed, so no obvious intraoperative instability was identified. After making screw holes using 1.0-mm-diameter Kirschner wires, the titanium plate was fixed using 1.3-mm-diameter titanium locking screws (TITAN LOCK screw; SUWA Inc., Yamanashi, Japan). The plate we developed does not feature a locking mechanism; therefore, a significant size difference between the screw shaft and the screw head is necessary to ensure a stronger fixation, allowing the plate to be securely pressed against the bone. C-arm radiography revealed reduced dorsal alignment of the AA junction by AA plate fixation. Then, the cat was placed in a ventral recumbent position for foramen magnum decompression. The occipital bone compressing the cerebellum was removed using an ultrasonic bone aspirator (SonoCure; Tokyo Iken Co., Ltd., Tokyo, Japan). Then, the dorsal dura mater lining the occipital bone was removed, releasing a large volume of cerebrospinal fluid, and the cerebellar pulsation was identified. The dural defect was covered using autologous temporal fascia and fibrin glue (Bolheal; KM Biologics Inc., Kumamoto, Japan). The postoperative radiograph and CT showed alignment of the AA junction and accurate placement of the titanium plate and screws (Fig. 2F). The cat was discharged 3 days postoperatively and a neck brace was applied for 3 months.

On day 45, the cat was able to stand up without support and walk with dysmetria. On day 60, the cat was capable of strenuous exercise, such as running and jumping up to the level of a table. Cervical radiography performed on day 60 showed loosening of the C1 left and center screws but appropriate alignment of the AA junction (Fig. 2G). On day 396, the cat remained slightly ataxic but had no limitation in activities of daily living, and slightly reduced postural responses of the pelvic limbs. Cervical radiography and CT revealed that the C1 right screw was completely pulled out and C1 left and center screws were loosened (Fig. 2H), but the titanium plate was completely adherent to the vertebrae. Furthermore, hyperostosis was observed around the titanium plate (Fig. 2I).

CJA, including AA instability, is a common disease. It typically affects toy breed dogs and only rarely affects cats [15]. Here we described two cases of AA instability and occipital bone deformity. In both cases, AA instability was diagnosed on flexed lateral radiographs and MRI findings. To the best of our knowledge, established diagnostic criteria for AA instability in cats have not been determined. The AA joint is considered a pivot joint that rotates around the dens of the axis [6]. Dorsally, the atlas is connected to the spinous process of the axis via the dorsal AA ligament, and therefore, mobility in the dorsoventral direction is considered absent [14]. In dogs with AA instability, it has been documented that the distance between the dorsal arch of the atlas and the spinous process of the axis increases on flexed lateral radiographs [11]. Accordingly, we hypothesized that in cats, a similar increase in the dorsal intervertebral distance of the AA joint during flexion would be indicative of instability. Occipital bone and atlas abnormalities, including incomplete ossification of the dorsal neural arch of the atlas, synostosis of the occipital bone and atlas, and inward indentation of the edge of the foramen magnum, were diagnosed on CT. Additionally, spinal cord contusion in case 1 and cerebellar indentation via the occipital bone in case 2 were identified on MRI. Multiple modalities were used to provide important information regarding the clinical condition and occipitoatlantal malformation.

In dogs, CJA rarely causes cerebellar symptoms. In humans, symptoms of occipitalization of the atlas vary from cosmetic deformity to pain and varying degrees of neurological dysfunction [16, 17]. A recent study showed that 40% of clinically normal cats exhibited foramen magnum herniation due to Chiari-like malformation, similar to brachycephalic dogs [3]. Therefore, the shapes of the cerebellum and occipital bone in cats exhibit several normal morphological variations [2, 3]. In case 1, the cat had head and neck tremors, whereas MRI did not reveal anatomical abnormalities of the cerebellum. In case 2, compression of the caudal cerebellum due to the abnormal occipital bone resulted in cerebellar symptoms, which were improved by removing the invaginated occipital bone. Our cases suggest that CJA of the cat is associated with structural or functional dysplasia of the cerebellum. Symptomatic cerebellar compression requires removal of the abnormal occipital bone. In both cases, walking improved after stabilization of the AA junction, suggesting that spinal cord compression due to the unstable AA junction was the major cause of the clinical signs. In case series of cats with traumatic AA instability, short-term improvement with medical treatment was observed in most cases [6], and in our cases, observed improvements in clinical signs may not be solely attributable to surgical intervention. However, in dogs with AA instability, additional mechanical forces may lead to dislocation of the unstable AA joint and sudden death from respiratory arrest; thus, surgical treatment is often performed to achieve long-term reduction of subluxation of the AA joint. Therefore, when AA instability is suspected, as in our cases, surgery may also be considered an option in cats.

Surgical treatment for AA instability has rarely been reported in cats. Most previous veterinary studies have suggested that the atlas and axis be anchored by screws, threaded pins, or Kirschner wires, and supported by polymethylmethacrylate or plates [1, 9, 11]. We expected difficulty with safe insertion of screws into the atlas and axis because both cats were in the growth period. Previously, we used 3D printing technology for planning the implant trajectory and designing implants for the surgical management of AA instability in small breed dogs [5]. The custom-made drill guide template provided accurate and safe guidance for screw placement. The custom-made titanium plate achieved repositioning and fixation of the AA joint by fixing the plate on the ventral side of the C1 and C2 vertebrae. In case 2, screw loosening was found postoperatively in the C1 left and center screws. Bone mineral density and cortical thickness affect the screw pull-out strength [13, 14]. It may be difficult to achieve bicortical screw fixation of the C1 vertebra in cats that are small or in the growth period. In addition, screw holes manufactured with a 3D printer have limited dimensional accuracy compared with those of commercially available plates. This limitation made it difficult to incorporate a reliable locking system into the custom-made plate used in this study, and therefore it was necessary to ensure firm contact between the plate and the bone. In case 2, screws with a larger difference between the shaft diameter and head diameter were selected—not to increase pull-out strength, but to ensure sufficient compression of the plate against the bone, compensating for the limited precision of the screw holes. Cortical bone screws, such as those used in case 1, are generally expected to increase pull-out strength, although loosening has been observed even with cortical screws in dogs [5], indicating that there remains room for further improvement in achieving optimal stability. AA instability causes dorsal displacement of the axis into the vertebral canal [10]; therefore, we considered it essential to securely fix the custom-made plate to the C2 vertebral body, and the selected screw was used in this study. All C1 screws were pulled out or loosened by 1 year after surgery, no abnormal vertebral displacement was noted. Titanium is commonly used for implants during spinal surgery because of its ability to facilitate bone growth in and around the implant [8]. Hyperostosis was observed around the titanium plate, likely reflecting the early stages of osseointegration in response to the implant, although localized inflammation due to screw back-out cannot be excluded. As osseointegration progresses, the titanium plate may contribute to stronger fixation by fusing with the vertebrae. The custom-made titanium plate and drill guide templates were successfully applied during the treatment of AA instability in cats, which may have contributed to improvement in limb motor function.

In this report, we described CJA in two cats. AA instability in cats may be associated with occipital bone abnormalities. The postoperative improvement of cerebellar signs in case 2 suggests that removal of the abnormal occipital bone compressing the cerebellum may be effective. In both cases, improvement in limb motor function was noted after repositioning and fixation of the AA junction using a custom-made drill guide template and titanium plate system, suggesting that this technique can be applied for AA stabilization in such cases. However, further studies are needed to clarify the role of AA stabilization in cats.

CONFLICT OF INTEREST

The authors declare no conflicts of interest.