A 5-year-old 2.9-kg (6.39-lb) sexually intact female Pomeranian (dog 1) was referred for evaluation of nonambulatory tetraparesis. Two weeks previously, the dog had suddenly developed paraparesis after swimming, and MRI (1.5-T magneta) performed at that time revealed a dorsal compressive AA band (ie, a thick, dorsal band of fibrous tissue involving the ligamentum favum1), cervical syringohydromyelia, Chiari-like malformation, mild hydrocephalus, and multifocal cervical intervertebral disk disease. The dog was treated with prednisone (2 mg/kg [0.9 mg/lb], PO, q 12 h; tapered to 0.5 mg/kg [0.23 mg/lb], PO, q 12 h) prior to referral. There was no perceived improvement, and the neurologic deficits progressed to nonambulatory tetraparesis.
The dog was referred to the Konkuk Veterinary Medical Teaching Hospital for further evaluation and possible surgical treatment. Results of a physical examination were unremarkable; neurologic examination revealed nonambulatory tetraparesis with an absence of postural responses in all 4 limbs. Cranial and spinal nerve refexes and sensation were intact.
A CBC revealed leukocytosis (23,570 WBCs/μl; reference range, 5,050 to 16,760 WBCs/μl) and neutrophilia without toxic changes (18,460 neutrophils/μl; reference range, 2,950 to 11,640 neutrophils/μl). Serum biochemical analyses revealed mildly high alanine aminotransferase (140 U/L; reference range, 10 to 100 U/L) and alkaline phosphatase (214 U/L; reference range, 23 to 212 U/L) activities and hyperlactatemia (3.92 mg/dL; reference range, 0.5 to 2.5 mg/dL). All other laboratory values were within reference ranges.
Sagittal T2-weighted images obtained during the previous MRI procedure were evaluated, and severity of the dorsal compressive AA band was graded as 3 on a scale from 0 to 3 (0 = no compression; 1 = reduction, but not elimination, of the underlying subarachnoid space; 2 = elimination of the underlying subarachnoid space and questionable spinal cord compression; and 3 = compression or deformation of the underlying spinal cord). In addition, the dorsal compression index (ie, the percentage of dorsal compression of the spinal cord), calculated as described,2 was 28.6% (Figure 1). No other abnormalities severe enough to cause tetraparesis were identified, and the dog had not improved with medical treatment. Therefore, the owner elected to proceed with decompressive surgery.
Preoperative T2-weighted sagittal MRI images of the craniocervical junction and cranial cervical region in a 5-year-old 2.9-kg (6.39-lb) sexually intact female Pomeranian (dog 1) with nonambulatory tetraparesis. A—The dorsal subarachnoid space is not evident in the region of C1-C2, and the spinal cord is focally compressed by a dorsal compressive AA band (yellow arrow). Chiari-like malformation (white arrow) and cervical spinal cord syringohydromyelia (red arrows) are also evident. B—Dorsal compression index, calculated as the ratio of the compressed length (CL) to the entire length of the adjacent unaffected spinal cord (EL), was 28.6%.
Citation: Journal of the American Veterinary Medical Association 255, 6; 10.2460/javma.255.6.700
Preoperative T2-weighted sagittal MRI images of the craniocervical junction and cranial cervical region in a 5-year-old 2.9-kg (6.39-lb) sexually intact female Pomeranian (dog 1) with nonambulatory tetraparesis. A—The dorsal subarachnoid space is not evident in the region of C1-C2, and the spinal cord is focally compressed by a dorsal compressive AA band (yellow arrow). Chiari-like malformation (white arrow) and cervical spinal cord syringohydromyelia (red arrows) are also evident. B—Dorsal compression index, calculated as the ratio of the compressed length (CL) to the entire length of the adjacent unaffected spinal cord (EL), was 28.6%.
Citation: Journal of the American Veterinary Medical Association 255, 6; 10.2460/javma.255.6.700
Preoperative T2-weighted sagittal MRI images of the craniocervical junction and cranial cervical region in a 5-year-old 2.9-kg (6.39-lb) sexually intact female Pomeranian (dog 1) with nonambulatory tetraparesis. A—The dorsal subarachnoid space is not evident in the region of C1-C2, and the spinal cord is focally compressed by a dorsal compressive AA band (yellow arrow). Chiari-like malformation (white arrow) and cervical spinal cord syringohydromyelia (red arrows) are also evident. B—Dorsal compression index, calculated as the ratio of the compressed length (CL) to the entire length of the adjacent unaffected spinal cord (EL), was 28.6%.
Citation: Journal of the American Veterinary Medical Association 255, 6; 10.2460/javma.255.6.700
General anesthesia was induced, and the dog was positioned in sternal recumbency with a towel placed between the surgical table and the neck to slightly elevate the cranial cervical vertebrae. After aseptic preparation, a dorsal cervical skin incision was made from the external occipital protuberance to the spinous process of the third cervical vertebra, and the epaxial muscles were elevated to expose the dorsal aspects of C1 and C2. To approach the AA band located between the dorsal laminas of C1 and C2, the dorsal AA ligament and cranial third of the C2 spinous process were removed with a bone cutter, rongeur, and scalpel. An AA band was identified between the C1 and C2 laminas and was carefully excised with a No. 11 scalpel blade and tenotomy scissors (Figure 2). The AA band was adhered to the underlying dura mater and was carefully dissected free. After removal of the AA band, a pool of CSF was found under the dura mater at the level of the C1–2 intervertebral space. A durotomy was performed, and approximately 3 mL of CSF spontaneously drained out of the opening. The underlying spinal cord appeared compressed, but the parenchyma was otherwise grossly normal.
Intraoperative photographs obtained during excision of the dorsal compressive AA band via a dorsal craniocervical approach in the dog in Figure 1. A—After removal of the dorsal AA ligament and cranial third of the spinous process of C2 (black arrow), hypertrophied fibrous tissue (AA band) was observed between the dorsal laminas of C1 and C2 (white arrows). B—After excision of the AA band, stagnant CSF was identified. C—A durotomy was performed, resulting in spontaneous drainage of a large amount of CSF. An iris tissue forceps is being used to hold the incised dura mater in this image. D—The spinal cord appeared to be compressed and split, but the parenchyma was otherwise grossly normal (black arrow).
Citation: Journal of the American Veterinary Medical Association 255, 6; 10.2460/javma.255.6.700
Intraoperative photographs obtained during excision of the dorsal compressive AA band via a dorsal craniocervical approach in the dog in Figure 1. A—After removal of the dorsal AA ligament and cranial third of the spinous process of C2 (black arrow), hypertrophied fibrous tissue (AA band) was observed between the dorsal laminas of C1 and C2 (white arrows). B—After excision of the AA band, stagnant CSF was identified. C—A durotomy was performed, resulting in spontaneous drainage of a large amount of CSF. An iris tissue forceps is being used to hold the incised dura mater in this image. D—The spinal cord appeared to be compressed and split, but the parenchyma was otherwise grossly normal (black arrow).
Citation: Journal of the American Veterinary Medical Association 255, 6; 10.2460/javma.255.6.700
Intraoperative photographs obtained during excision of the dorsal compressive AA band via a dorsal craniocervical approach in the dog in Figure 1. A—After removal of the dorsal AA ligament and cranial third of the spinous process of C2 (black arrow), hypertrophied fibrous tissue (AA band) was observed between the dorsal laminas of C1 and C2 (white arrows). B—After excision of the AA band, stagnant CSF was identified. C—A durotomy was performed, resulting in spontaneous drainage of a large amount of CSF. An iris tissue forceps is being used to hold the incised dura mater in this image. D—The spinal cord appeared to be compressed and split, but the parenchyma was otherwise grossly normal (black arrow).
Citation: Journal of the American Veterinary Medical Association 255, 6; 10.2460/javma.255.6.700
An autogenous fat graft was placed over the exposed spinal cord, and the epaxial muscles and fascia were reapposed. To ameliorate the instability resulting from removal of the dorsal AA ligament, a dorsal AA stabilization procedure was performed with a double strand of 2-0 polydioxanoneb as described.3 The suture was placed between the dorsal muscles of the atlantooccipital area (obliquus capitis cranialis muscle) and the contralateral dorsal muscles of C2 (obliquus capitis caudalis muscle) bilaterally (Figure 3).
Illustration of the method used for dorsal stabilization of the AA joint in the dog in Figure 1. A double strand of 2-0 polydioxanone was placed between the dorsal muscles of the atlantooccipital area (obliquus capitis cranialis muscle [OCC]) and the contralateral dorsal muscles of C2 (obliquus capitis caudalis muscle [OCD]) bilaterally (black dotted lines).
Citation: Journal of the American Veterinary Medical Association 255, 6; 10.2460/javma.255.6.700
Illustration of the method used for dorsal stabilization of the AA joint in the dog in Figure 1. A double strand of 2-0 polydioxanone was placed between the dorsal muscles of the atlantooccipital area (obliquus capitis cranialis muscle [OCC]) and the contralateral dorsal muscles of C2 (obliquus capitis caudalis muscle [OCD]) bilaterally (black dotted lines).
Citation: Journal of the American Veterinary Medical Association 255, 6; 10.2460/javma.255.6.700
Illustration of the method used for dorsal stabilization of the AA joint in the dog in Figure 1. A double strand of 2-0 polydioxanone was placed between the dorsal muscles of the atlantooccipital area (obliquus capitis cranialis muscle [OCC]) and the contralateral dorsal muscles of C2 (obliquus capitis caudalis muscle [OCD]) bilaterally (black dotted lines).
Citation: Journal of the American Veterinary Medical Association 255, 6; 10.2460/javma.255.6.700
The subcutis and skin were closed in routine fashion. The dog recovered from anesthesia without any apparent immediate complications. Constant rate infusions of fentanyl (0.004 μg/kg/h [0.002 μg/lb/h]) and lidocaine (1.2 mg/kg/h [0.55 mg/lb/h]) were administered for 24 hours after surgery, followed by carprofen (2.2 mg/kg [1.0 mg/lb], PO, q 12 h) and tramadol (4 mg/kg [1.8 mg/lb], PO, q 12 h) for 7 days. A soft neck bandage was applied for 7 days, and cage rest was recommended for 2 weeks. Postoperative radiography revealed removal of the cranial part of the C2 spinous process with good alignment of C1 and C2 (Figure 4).
Lateral (A) and dorsoventral (B) postoperative radiographs of the dog in Figure 1. Partial removal of the spinous process of C2 and good alignment of C1 and C2 are evident.
Citation: Journal of the American Veterinary Medical Association 255, 6; 10.2460/javma.255.6.700
Lateral (A) and dorsoventral (B) postoperative radiographs of the dog in Figure 1. Partial removal of the spinous process of C2 and good alignment of C1 and C2 are evident.
Citation: Journal of the American Veterinary Medical Association 255, 6; 10.2460/javma.255.6.700
Lateral (A) and dorsoventral (B) postoperative radiographs of the dog in Figure 1. Partial removal of the spinous process of C2 and good alignment of C1 and C2 are evident.
Citation: Journal of the American Veterinary Medical Association 255, 6; 10.2460/javma.255.6.700
Postoperatively, the dog had consistent improvement in its neurologic status and was discharged 3 days after surgery, at which time it was able to walk with assistance. Normal ambulation was recovered 30 days after surgery. During a follow-up period of 17 months, the dog maintained normal ambulation with no signs of neck pain or neurologic deficits.
A 12-year-old 2.24-kg (4.94-lb) sexually intact female Pomeranian (dog 2) was examined because of an acute onset of nonambulatory tetraparesis. Before admission, the dog was apparently healthy, and there was no history of trauma. On physical examination, there were no abnormalities, except for bilateral grade 3 medial patellar luxation. Neurologic examination revealed an absence of postural reactions in all 4 limbs; there was no cervical hyperesthesia. No abnormalities were found on laboratory testing or radiographic examination.
Magnetic resonance imaginga performed on the first day of admission revealed a dorsal compressive AA band that was associated with syringohydromyelia, Chiari-like malformation, and mild compression of the cervical spinal cord resulting from multifocal cervical intervertebral disk disease. The AA band severity was grade 3, and the dorsal compression index was 31%. A degenerative nodule was found incidentally in the caudate nucleus.
Prednisone (1.0 mg/kg [0.45 mg/lb], PO, q 12 h; tapered to 0.5 mg/kg, PO, q 24 h) was administered to the dog for 2 weeks; however, there was no improvement in the neurologic deficits. Therefore, after a discussion of possible outcomes and complications, the owner elected to proceed with surgical treatment. The dog underwent a similar procedure as described for dog 1. Intraoperative observations in dog 2 were similar to those in dog 1, except there was no adhesion between the AA band and the dura mater. The AA band was removed without requiring a C1-C2 dorsal laminectomy, and stagnant CSF was identified under the dura mater at the site of the lesion. A durotomy was performed, resulting in spontaneous drainage of a considerable amount of CSF. The underlying spinal cord appeared compressed, but the parenchyma was otherwise grossly normal. No major complications occurred, and the dog recovered from anesthesia uneventfully. Postoperative treatment, including analgesic treatment and neck bandaging, was the same as reported for dog 1. Postoperative radiography revealed removal of the cranial portion of the spinous process of C2 and good alignment of C1 and C2.
The dog was hospitalized for 3 days. There were no apparent improvements in the neurologic deficits until 7 days after surgery. On postoperative day 12, the dog attempted to stand, showed increased movement, and recovered proprioception in the right forelimb. On postoperative day 19, the dog could stand and walk with minimal assistance, and proprioception was normal in all limbs except the left forelimb. The dog's gait consistently improved, and the dog regained normal ambulation with normal postural reactions on postoperative day 25. During the recovery period, rehabilitation, including muscle massage, manipulation, and assisted walking, was performed consistently by the owner. The dog had not developed any long-term complications or any recurrence of neurologic deficits in the 19 months after surgery.
A 13-year-old 4.3-kg (9.5-lb) castrated male Yorkshire Terrier (dog 3) with a 2-month history of progressive tetraparesis was referred for evaluation. Initially, the dog had had an acute onset of ambulatory paraparesis. The referring veterinarian did not identify an underlying cause and prescribed treatment with firocoxib (5 mg/kg [2.3 mg/lb], PO, q 24 h) and tramadol (3 mg/kg [1.4 mg/lb], PO, q 12 h). However, the neurologic deficits worsened and progressed to nonambulatory tetraparesis.
Evaluation at the time of the referral revealed an obese dog with a body condition score of 5/5. The dog was laterally recumbent but appeared to have a normal mental status. No other abnormalities were found on physical examination. The dog had a history of hyper-adrenocorticism and had been undergoing treatment for this disorder. On neurologic examination, the dog showed spastic paresis with absent postural reactions in all 4 limbs. There was no cervical hyperesthesia. The remaining findings of the neurologic examination were unremarkable. Results of a CBC were within reference limits; serum biochemical abnormalities included high alanine aminotransferase (222 U/L; reference range, 10 to 100 U/L) and aspartate aminotransferase (52 U/L; reference range, 0 to 50 U/L) activities and hyperlactatemia (4.9 mg/dL; reference range, 0.5 to 2.5 mg/dL). No remarkable findings were observed on survey radiographs.
Magnetic resonance imaginga revealed a dorsal compressive AA band, Chiari-like malformation, and mild spinal cord compression associated with multifocal cervical and thoracolumbar intervertebral disk disease. Syringohydromyelia was not detected. On the basis of sagittal T2-weighted images, the AA band severity was grade 3 with a dorsal compression index of 28.8%. Mild contrast enhancement of the pituitary gland was incidentally found on sagittal T1-weighted images.
Considering the lack of response to medical treatment and the progression of the neurologic deficits, the owner elected to proceed with surgical treatment. Decompressive surgery was performed as described for dogs 1 and 2. Intraoperative findings, including a thick AA band adhering to the dura mater, pooling of CSF, and dorsally compressed but otherwise grossly normal spinal parenchyma, were similar to those for dogs 1 and 2. The excised AA band was examined histologically and was found to be composed entirely of dense collagenous connective tissue with reactive fibroblasts. There was no evidence of neoplasia or inflammation in the sections examined. There were no surgical complications. and no abnormalities were found on postoperative radiographs, other than removal of the cranial portion of the spinous process of C2.
The dog received the same postoperative care as did dogs 1 and 2. Of the 3 dogs, dog 3 had the quickest recovery from neurologic deficits and could stand and walk a few steps without assistance on the day of surgery despite having mild rigidity of the limbs. On postoperative day 2, the dog could walk for a longer time and had improved proprioception in the forelimbs. The dog was discharged 5 days after surgery, at which time it could walk on its own although proprioception in the hind limbs had not returned to normal. Normal ambulation was evident on postoperative day 18. At a 4-month recheck visit, the dog had normal ambulation and reportedly had had no signs of recurrence.
Discussion
A dorsal compressive AA band is a dorsal constrictive lesion resulting from thickened soft tissue located between the dorsal laminas of C1 and C2.1,4–6 Depending on the thickness of the AA band, various degrees of dorsal compression of the subarachnoid space and spinal cord can occur, which can cause secondary lesions such as syringohydromyelia and associated clinical signs.1,2,5,7 A dorsal compressive AA band is one of the more frequently diagnosed craniocervical junction anomalies in toy-breed dogs, especially Cavalier King Charles Spaniels.1,2,5,6,8,9 Despite the high prevalence of dorsal compressive AA bands in dogs, data regarding treatment options are lacking. In particular, there are, to our knowledge, no published reports of outcome following surgical treatment in dogs with severe neurologic deficits secondary to an AA band.
All 3 dogs in the present report were examined because of nonambulatory tetraparesis. However, neurologic deficits this severe are not common in dogs with dorsal compressive AA bands, and most dogs with AA bands are examined because of cervical hyperesthesia characterized by scratching of the neck or head.1,5 In a recent study1 of Cavalier King Charles Spaniels with dorsal compressive AA bands, all dogs were examined because of neck pain, and none of the dogs had gait problems such as ataxia or paresis. The relationship between AA bands and the severity of clinical signs is still debated in veterinary medicine, even though dorsal compressive AA bands have been strongly associated with the presence of clinical signs in both veterinary and human medicine.1,4,10 On the other hand, several studies1,5,11,12 have failed to find a significant association between the degree of spinal cord compression caused by an AA band and the severity of clinical signs in dogs. In the present report, all 3 dogs had grade 3 AA bands. Therefore, we initially thought that severe compression of the spinal cord might have been the main cause of the nonambulatory tetraparesis. However, in a previous retrospective study,1 grade 3 AA band severity was detected in 5 of 36 (13.9%) dogs with only neck pain. In addition, dorsal compression indexes for dogs in that study, which only had neck pain, ranged from 20% to 30%, which was similar to the indexes for dogs in the present report (28.6%, 28.8%, and 31%).
Concomitant diseases such as Chiari-like malformation and intervertebral disk disease were also considered as potential causes of the severe clinical signs in the dogs described in the present report. However, the concomitant diseases identified in these dogs were relatively mild and, therefore, considered unlikely to have been contributing factors. The presence of syringohydromyelia may affect clinical signs and prognosis; however, clinical signs and treatment outcomes were not different between the 2 dogs with syringohydromyelia (dogs 1 and 2) and the dog without (dog 3). Despite these complicating factors, the outcomes for these 3 dogs strongly suggested that dorsal compressive AA bands can be associated with severe neurologic deficits. Nevertheless, further studies are needed to better understand the relationship between dorsal compressive AA bands and the severity of clinical signs in affected dogs.
Surgical treatment of fibrous bands causing compression of the spinal cord has rarely been reported in dogs, with only 2 reports providing detailed information on surgical procedures involving fibrous band excision in dogs.13,14 Skytte et al13 described fibrous band excision with C1-C2 dorsal laminectomy for surgical treatment of an AA band in 2 dogs. Both of these dogs were examined because of signs of neck pain without gait dysfunction, and surgical treatment resulted in good outcomes in both cases. Cerda-Gonzalez et al14 reported a toy-breed dog with a fibrous band compressing the underlying spinal cord caudal to the foramen magnum. That dog also had signs of neck pain, which resolved after surgical excision of the fibrous band. In both of these reports, surgery was performed to decompress the spinal cord and improve CSF flow by removing the compressive fibrous band. Additionally, Skytte et al13 reported that the C1-C2 dorsal laminectomy was successful in removing the compressive band and the adhesion. To remove the AA bands in the dogs described in the present report, we used a surgical procedure similar to that described by Skytte et al,13 except that we did not perform a dorsal laminectomy because the fibrous tissue forming the AA bands did not invade under the dorsal lamina of C1 or C2 in these dogs. We suggest that dorsal laminectomy can be optional depending on the extent of the AA band. However, leaving the dorsal lamina intact can help reduce postlaminectomy adhesions between the exposed spinal cord and surrounding tissues.
For the dogs described in the present report, we performed a durotomy to improve CSF flow following excision of the AA band. This procedure can ultimately have the effect of alleviating syringohydromyelia through the so-called slosh phenomenon of CSF flow theory, which refers to the tendency of CSF to flow into a syringohydromyelia cavity rather than a compressed subarachnoid space.
The dorsal AA ligament is a thick ligament extending from the C1 dorsal lamina to the C2 spinous process that contributes to stabilization of the AA joint,15 and removal of the dorsal AA ligament may cause considerable AA joint instability. Dorsal AA stabilization techniques are intended to mimic the function of the dorsal AA ligament so as to ameliorate AA joint instability. Among the various dorsal stabilization techniques that have been described, the cross-suture technique developed by Sánchez-Masian et al3 was chosen owing to its safety and simplicity. Originally, this technique was developed for dorsal stabilization of AA joint subluxation in toy-breed dogs, and it has been reported to be safe, effective, and simple.3 The sutures play a role similar to that of the dorsal AA ligament, counteracting the main forces, such as distraction and tension, between C1 and C2 created by ventral flexion of the head. The technique works by fixing the dorsal cervical muscles extending from the atlanto-occipital joint to the axis.3 In addition, this technique is relatively minimally invasive and less complicated than other dorsal stabilization techniques because it relies on muscular stabilization, whereas other dorsal techniques require bone stabilization. Therefore, the cross-suture technique is not associated with surgical complications reported for other dorsal stabilization techniques, such as perioperative spinal cord injury and implant failure.3 We used a synthetic suture with a long absorption time for the cross-sutures because long-term stability after this procedure is probably due to fibrosis across the dorsal aspects of C1 and C2, not due to the suture itself.3
Long-term outcomes following surgical treatment of dorsal compressive AA bands in dogs have not been reported previously. In dogs with Chiari-like malformation, which is treated with foramen magnum decompression, fibrous tissue removal, and durotomy, a recurrence of clinical signs can be expected in 25% to 53% by 3 years after surgery, despite the initial postoperative improvement that is observed in most dogs.7,16–19 The reasons for this high recurrence rate are not yet certain; however, it has been suggested that postlaminectomy adhesions between the exposed neural tissue and adjacent fibrous or scar tissue might disturb CSF flow and aggravate syringohydromyelia.17 Postlaminectomy adhesions are a common postoperative complication causing chronic pain in humans.20 In addition, growth of fibrous or scar tissue might compress the subarachnoid space or spinal cord directly.17 To decrease the possibility of postlaminectomy adhesions, we reduced the extent of spinal cord exposure by preserving the C1 and C2 dorsal laminas and applied an autogenous fat graft over the exposed spinal cord. There was no recurrence of neurologic deficits during follow-up periods of 4 to 19 months; however, dogs should be monitored long term for late complications.
ABBREVIATIONS
| AA | Atlantoaxial |
| C1 | First cervical vertebra (atlas) |
| C2 | Second cervical vertebra (axis) |
Footnotes
Magnetom Essenza 1.5-T magnet, Siemens, Erlangen, Germany.
PDS II (polydioxanone) suture, Ethicon Inc, Somerville, NJ.
References
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