Acute idiopathic polyneuritis with spontaneous remission in an Abyssinian cat

Abstract

An Abyssinian kitten was presented after a sudden onset of neurological disorders consistent with a polyneuropathy. Electrophysiological and histological investigations revealed an inflammatory polyneuropathy. No infectious agents were detected. Spontaneous recovery occurred rapidly without relapse (2 years follow-up). This is the first description of a histologically confirmed self-limiting feline polyneuritis.

Introduction

Polyneuropathies are rare in cats and particularly in kittens. Their origin can be inherited or acquired (1–5). Acquired polyneuropathies in cats are immune-mediated (6–12), paraneo-plastic (7,13), toxic (2,3,7,9,10,14), metabolic (2,3,15), or of unknown origin (6,8,16). Reported self-limiting remission from polyneuropathies in cats is rare and includes demyelinating/remyelinating polyneuropathies in Bengal cats (9,17), axonal neuropathy in Snowshoe cats (1,7), motor polyneuropathies (6,8,10), and undetermined polyneuropathies (6–9,11,18). Histologically confirmed idiopathic inflammatory polyneuropathy (polyneuritis) has been rarely documented in feline medicine (7,9,10), and all reported cats were euthanized due to a worsening neurological status. Here we describe an acute histologically confirmed case of polyneuritis with spontaneous remission without medical treatment and without relapse after 2 y.

Case description

A 6-month-old intact female Abyssinian cat was presented 4 d after the sudden appearance of abnormal gait. Six days before presentation, the kitten had vomited once. Since then, the owners reported reluctance to walk and jump that slowly evolved to pelvic limb weakness. The cat had been vaccinated 3 mo earlier and the last external parasite treatment had been given 2 wk earlier. The kitten had no access to the outdoors, drugs, or plants, and was fed a high quality commercial food. No contact with any other animal was reported.

At the time of presentation, the neurological examination revealed a normal mental status and behavior. The cat sat for most of the time. Pelvic limbs weakness, plantigrade stance, associated with short-strided gait involving just pelvic limbs, and absent flexion of the tarsal joints were clearly apparent (see video file: https://youtu.be/xSAwCJtPySA). No involuntary movement was observed. Examination of the cranial nerves revealed no abnormalities. A proprioceptive positioning response was absent in the pelvic limbs, normal in the thoracic limbs. Hopping was decreased in the pelvic limbs, slightly decreased in the thoracic limbs. Spinal appendicular reflexes were decreased (patellar reflex, thoracic limb flexion) to absent (distal pelvic limb flexion). Mild distal appendicular muscle atrophy was detected. Evaluation of sensory system was unremarkable.

An acute and diffuse neuromuscular disease was suspected from the physical examination. An electrophysiological examination (Nicolet Viasys Viking Select EMG machine; Viasys, Geispolsheim-Gare, France) and neuromuscular biopsies were carried out under general anesthesia and analgesia. Electromyography was performed on the head, paraspinal, and appendicular muscles of the left side of the kitten. Diffuse abnormal spontaneous activity (fibrillation and positive sharp waves) was observed in the appendicular muscles. The intensity of this activity was higher in the most distal muscles (plantar and palmar interossei m., tibialis cranialis m., gastrocnemius m., flexor carpi radialis m., and extensor carpi radialis m.). A tibial, fibular, and ulnar nerve conduction study was performed. The amplitudes of the proximal and distal compound motor action potentials were significantly decreased. Sensory and motor nerve conduction velocities were low compared with the published reference intervals for kittens (15) (Table 1). F-waves latency of the tibial nerve was increased and the F-wave ratio was normal compared with published reference intervals for the adult cat (6,16). Repetitive nerve stimulation was not performed. Muscle biopsies (right tibialis cranialis and right triceps brachii muscles) revealed scattered angular atrophied fibers adjacent to normal fibers, which suggested denervation. These fibers were predominantly type 2 but atrophic type 1 fibers were also found. The intramuscular nerve branches showed myelinated fiber loss (Figure 1). These abnormalities were more consistent in the tibialis cranialis muscle. Immunostaining for CD3 was performed and no CD3 positive cells were noted. A hematoxylin-eosin-safran stained histological appearance of the right peroneal nerve biopsy was unremarkable, but examination after teased fiber preparation revealed fiber-invasive mononuclear cell infiltrates in non-degenerative fibers entering intact myelin tube at the Schmidt-Lanterman clefts, consistent with an immune-mediated neuropathy (Figure 2). Nerve immunostraining was not possible due to a lack of tissue. A diagnosis of polyneuritis was established. Lumbar cerebrospinal fluid (CSF) cytological examination (red blood cells 920/mm³, white blood cell 1/mm³, 0 after centrifugation) and CSF total protein (0.23 g/L) were unremarkable. Serum biochemistry and urine analysis were normal, and serum creatine kinase was normal (375 UI/L, reference range: 641 to 700 UI/L). Serum protein electrophoresis revealed an alpha-2 globulin increase. Tests for serum feline immunodeficiency virus antibody and feline leukemia virus antigen were negative. A Toxoplasma IgM titer was negative and IgG titer was slightly positive suggesting past exposure (1:64, normal < 1:32). Thoracic radiographs and abdominal ultrasound images were unremarkable. An idiopathic polyneuritis was diagnosed from these results.

Table 1.

Electrophysiological values in the kitten compared with previously published reference intervals (mean ± standard deviation) in young^a and adult^b cats

	Proximal CMAP amplitude (mV)	Distal CMAP amplitude (mV)	Proximal CMAP duration (ms)	Distal CMAP duration (ms)
Peroneal nerve	2.6 (24.5 ± 10.5)	4.1 (32.8 ± 6.2)	3.3 (3.7 ± 1.2)	1.8 (3.5 ± 0.7)
Tibial nerve	8.8 (17.8 ± 4.9)	9.0 (26 ± 1.8)	4.8 (8.1 ± 2.5)	2.6 (8.0 ± 2.1)
Radial nerve	3.8 (26.8 ± 10.1)	6.9 (24.7 ± 5.8)	4.0 (4.9 ± 1.6)	4.0 (3.7 ± 0.8)
	MNCV (m/s)	SNCV (m/s)	F-wave latency (ms)	F-ratio
Peroneal nerve	67 (101 ± 20.4)	65 (84.7 ± 11.1)	12.8 (NR)	NM
Tibial nerve	59 (95.5 ± 9.7)	NM	13.5 (9.5 ± 1.0)	1.72 (1.75 ± 0.2)
Radial nerve	80 (83.9 ± 8.0)	62 (75.6 ± 3.6)	10.3 (NR)	1.05 (NR)

^aData from references 6, 8, 15.

^bData from references 6, 16, 17.

CMAP — compound muscle action potential; MNCV — motor nerve conduction velocity; SNCV — sensory nerve conduction velocity; NM — not measured; NR — not reported.

Figure 1.

Tibialis cranialis muscle histology. A — Grouped multiple small angulated fibers (Hematoxylin and eosin stain, bar = 100 μm); B — Intramuscular nerve branch in a normal 8-month-old cat (Gomori’s trichrome stain, bar = 10 μm); C — Intramuscular nerve branch of the kitten (Gomori’s trichrome stain, bar = 10 μm).

Figure 2.

Teased peroneal nerve after osmium tetroxide with/without hematoxylin counterstaining. Note the mononuclear round cells attached to (red arrows) or invading (blue arrows) the large myelinated fibers (bar = 20 μm).

A slight improvement of the gait was observed the following day, without treatment. After a week the patient still showed pelvic limb weakness but was not reluctant to walk anymore. Postural reactions were normal for the thoracic limbs but still diminished for the pelvic limbs. Spinal reflexes were still diminished for the pelvic limbs, normal for the thoracic limbs. Two weeks later, the gait was normal according to the owner. Six months later, a clinical follow-up confirmed the normal neurological examination. Toxoplasma IgG titer was negative. Two years after the onset, no relapse was reported by the owner.

Discussion

To our knowledge, this is the first histologically confirmed description of an acute self-limiting idiopathic polyneuritis in a kitten. In young animals, congenital or degenerative diseases can be suspected. In our case, a polyneuritis was identified histologically. Nerve pathology in inflammatory polyneuropathies has rarely been described in feline veterinary medicine (7,9,10,19). Two of the 4 described cases were based on postmortem examination of an acute form in an adult. In the first case (9), extensive destruction of myelin with macrophages and lymphocyte infiltrates was observed in the distal peripheral nerves, but the spinal nerve roots were not examined. In the second case (7), demyelination and accumulation of macrophages were observed in the ventral roots of the spinal cord and in all nerves. The third case concerned a chronic disease (10), with segmental demyelination, remyelination, and focal mononuclear cell infiltration of the dorsal and ventral spinal roots. Distal nerves showed less severe alterations. More recently, severe mononuclear nerve infiltration has been described in a cat with steroid responsive idiopathic polymyositis and polyneuritis (19). In our case, the semi-thin longitudinal sections were unremarkable, whereas the teased fiber preparation showed mononuclear cell adhesion and invasion but no concurrent features indicative of demyelination. Fiber-invasive cells entering the myelin tube is described in immune-mediated polyneuropathies in humans (20). Nerve fiber immunohistochemistry is necessary to confirm the nature of the infiltrates, but this was not possible due to the small amount of tissue. Despite minimal nerve fiber abnormalities, intramuscular nerves showed fiber loss. This finding could indicate a distal polyneuropathy. Ventral nerve root biopsies were considered, but not done due to the associated risks and the observation that the cat was already showing signs of improvement.

Histopathological diagnosis of polyneuritis is rare and often this disease is considered idiopathic in cats (7,9–12,19). Tests for Toxoplasma gondii, feline immunodeficiency virus, and feline leukemia virus did not detect any of these infectious agents in our kitten. Evolution of the disease in this cat was acute and self-limiting. Acute acquired polyneuropathies have been previously reported (6–9,11,18). In a case series of 9 cats with acute polyneuropathies (2–5,7), all the cats were middle-aged, except 1 which was 4 mo old. Two of the cats were euthanized due to worsening of the clinical signs; the other 7 cats were discharged without medication and made a full recovery within 4 to 6 wk, without any relapse during the following 2 y. The diagnosis of polyneuropathy was only clinical in 8/9 cats, and postmortem in 1 cat due to its worsening condition. Self-limiting evolution, or recurrent acute polyneuropathies have been identified in young Bengal and other breeds of cat (1,6,8,17). None of the histological examinations reported an inflammatory process. In another case report of acute polyneuropathy (7,9–12), improvement was observed after a few weeks of prednisolone therapy. Our case report confirmed that idiopathic acute polyneuritis could resolve spontaneously with no relapse over a 2-year period.

In our cat, the electrophysiological examination was consistent with an axonal polyneuropathy with a dominant motor component, suggestive of polyradiculopathy or distal motor polyneuropathy. These abnormalities have been previously described in motor polyneuropathies of undetermined origin (6,8,13). In our case, the proximo-distal repartition of the electromyographic abnormalities and the normal CSF could indicate a distal nerve disease. However, the tibial nerve F-ratio was within adult cat reference ranges, which should indicate an equal distribution of the neuropathy between the proximal and the distal parts of the nerve. To our knowledge, tibial nerve F-ratio reference ranges have not been established in young cats, and their accuracy in differentiating proximal, distal or equal distribution of neuropathy has not been assessed in cats. Albuminocytologic dissociation is commonly, but not always, observed in acute inflammatory polyneuropathy in humans (Guillain-Barré syndrome) (2,3,14,21), in acute idiopathic polyradiculoneuritis in dogs (2,3,22), and described once in a cat with idiopathic polyneuritis and polymyositis (19).

Idiopathic polyneuritis is a rarely diagnosed entity in cats, probably due to lack of advanced histopathological data. This case report focuses on the necessity for electrophysiology and advanced histopathology in feline neuromuscular disease investigation. Previous descriptions of documented inflammatory polyneuropathies have been associated with a poor prognosis or responding to long-term corticosteroid therapies. This is the first histopathological description of acute self-limiting idiopathic immune-mediated feline polyneuropathy.