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Abstract

Objectives

The aim of this study was to evaluate the presence of the cutaneous trunci reflex (CTR) in a population of neurologically abnormal cats in regard to age, body condition score (BCS), sex, breed, evidence of traumatic injury, pain, known metabolic disease, mentation, neurolocalization and diagnostic classification.

Methods

A retrospective medical record review was performed to identify cats with a history of neurologic disease undergoing a complete neurologic assessment between 24 September 2012 and 20 March 2019. CTR outcome (present, absent), signalment, evidence of traumatic injury, pain, known metabolic disease, mentation, neurolocalization and diagnostic classification were recorded.

Results

A total of 182 cats were identified. The CTR was present in 118 cats (64.8%) and absent in 64 cats (35.2%). Statistical analysis revealed no association between CTR outcome and age, BCS, sex, breed, evidence of traumatic injury, non-spinal pain, known metabolic disease, mentation, neurolocalization or diagnostic classification. A significant association was found between spinal pain and CTR outcome (P = 0.037).

Conclusions and relevance

These findings suggest that elicitation of the CTR in the cat can be unreliable. Further prospective controlled studies are warranted to determine whether continued inclusion of the CTR in feline neurologic examinations is justified. Consideration of the reliability of the CTR is indicated, particularly in the context of fractious or anxious patients for which only a limited window for examination may be present.

Keywords

Cutaneous trunci myelopathy neuromuscular panniculus reflex

Introduction

Evaluation of the cutaneous trunci reflex (CTR) is a standard component of the veterinary neurologic examination in both dogs and cats.^1,2 While it has been reported that the CTR may be absent in neurologically normal dogs, several more recent studies conclude otherwise.^3,4 In dogs, the sensory field of the CTR has been mapped and the repeatability of the CTR has been evaluated.⁴ The presence, absence or sequential change in the CTR has likewise been assessed in the dog both as a mechanism of localizing thoracolumbar spinal cord injuries and as a predictor of recovery following disc extrusions.^3,5

It has been reported that visually healthy and neurologically normal cats may not demonstrate a menace response with the same reliability as dogs.⁶ Similarly, eliciting the CTR can be difficult and provide inconsistent results, especially when the cats are stressed. In the authors’ experience, the absence of a consistently elicitable CTR in a cat may not indicate neurologic impairment. Nevertheless, to the best of the authors’ knowledge, no published clinical study has evaluated the CTR in neurologically abnormal cats. The purpose of this retrospective study was to evaluate whether the presence, or absence, of the CTR in a population of neurologically abnormal cats may be affected by age, body condition score (BCS), sex, breed, evidence of traumatic injury, pain, metabolic disease, mentation, neurolocalization or diagnostic classification.

Materials and methods

A retrospective search of medical records was conducted to identify all cats evaluated by the Neurology & Neurosurgery Service at the University of Illinois Veterinary Teaching Hospital (VTH) between 24 September 2012 and 20 March 2019. As this was a retrospective study, informed consent for patients to be examined by clinicians within the Neurology & Neurosurgery Service was obtained at the time of the patient’s presentation to the VTH. Additionally, informed consent for the utilization of data collected during the provision of care and treatment for research and publication purposes is also obtained for all animals presenting to the VTH as part of the Hospital Admission Consent Form.

Medical records were reviewed and clinical data were collected relating to: signalment; date of examination; age (months); weight (kg); BCS (graded on a nine-point scale, where a BCS of 1/9 indicated a severely underweight animal, a BCS of 5/9 indicated an appropriately conditioned animal and a BCS of 9/9 indicated a grossly overweight animal);^7,8 mentation (alert, inappropriate, dull, obtunded, stuporous, comatose); temperament (when reflected in the medical record); CTR outcome (absent, fully intact, unilateral/partially intact, inconsistent, not evaluated); neurolocalization (forebrain, non-thalamus brainstem, cerebellum, peripheral vestibular, central vestibular, undetermined vestibular, C1–C5 myelopathy, C6–T2 myelopathy, T3–L3 myelopathy, L4–S3 myelopathy, multifocal myelopathy, neuromuscular, multifocal non-myelopathy); traumatic injury; pain; metabolic dysfunction (diagnosed diabetes mellitus [DM] or hyperthyroidism); and diagnosis (definitive, suspected or open). Data regarding imaging studies, biopsy results and necropsy findings were also collected.

After recording these data for each patient visit, the following exclusion criteria were applied: patient visits without (1) record of a neurologic examination; (2) recorded body weight; (3) an attempt to elicit CTR; and (4) observed neurologic deficits, except for history of seizure activity. Neurologic examination data for any subsequent patient visits were also excluded. All neurologic examinations were performed by clinicians within the VTH Neurology & Neurosurgery Service, including board-certified veterinary neurologists, residency trained veterinary neurologists and neurology house officers (neurology specialty intern and/or neurology resident) under the supervision of a board-certified veterinary neurologist.

All variables analyzed were evaluated visually for normality and satisfied normal distributions. Single-factor ANOVA was utilized to separately evaluate mean BCS and mean age relative to CTR outcome. χ² analysis was utilized to separately evaluate sex, breed, mentation, traumatic injury, pain, metabolic disease, neurolocalization and diagnostic classification relative to CTR outcome. For all metrics, a P value <0.05 indicated statistical significance. If statistical significance had been achieved for any χ² analysis involving <5 data points, a Fisher’s exact test would have been run. Statistical analysis was performed using standard software (Microsoft Excel, version 16.0.11425.20228).

Results

A total of 182 cats meeting the inclusion criteria were identified. An observed CTR was present in 118 cats (64.8%) and absent in 64 cats (35.2%). All single-factor ANOVA analyses are summarized in Table 1, and all χ² analyses are summarized in Table 2.

Table 1

Single-factor ANOVA analysis for mean age (months) and mean body condition score (BCS) relative to cutaneous trunci reflex (CTR) outcome

Metric	F statistic	F critical value	P value
Age and CTR outcome (n = 182)	0.147	3.894	0.702
BCS and CTR outcome (n = 180)	0.126	3.894	0.723

Table 2

χ² analysis for sex, breed, evidence of traumatic injury, pain on examination, spinal pain on examination, metabolic disease (diabetes mellitus or hyperthyroidism), diabetes mellitus, neurolocalization, mentation and diagnostic classification relative to cutaneous trunci reflex (CTR) outcome in 182 cats

Metric	χ²	df	Critical value	P value
Sex and CTR outcome	0.696	1	3.841	0.404
Breed and CTR outcome	2.883	1	3.841	0.090
Mentation and CTR outcome	0.015	1	3.841	0.904
Traumatic injury and CTR outcome	1.929	1	3.841	0.165
Pain and CTR outcome	3.297	1	3.841	0.069
Spinal pain and CTR outcome	4.348	1	3.841	0.037
Metabolic disease and CTR outcome	0.000	1	3.841	0.987
Diabetes mellitus and CTR outcome	0.014	1	3.841	0.906
Neurolocalization and CTR outcome	3.963	6	12.591	0.682
Myelopathy vs non-myelopathy neurolocalization and CTR outcome	1.893	1	3.841	0.169
Diagnostic classification and CTR outcome	5.560	7	14.067	0.566

Influence of age, breed and BCS

Patient age ranged from 2 to 264 months (mean ± SD 106 ± 71 months). Mean ages were calculated for each CTR outcome (absent: 108.3 months; present: 104.1 months). No significant association was found between age and CTR outcome (P = 0.702). The study population consisted of 70 females (13 intact, 57 spayed) and 112 males (12 intact, 100 castrated). No significant association was observed between sex, without regard to neuter status and CTR outcome (P = 0.404). While most patients were of mixed breed (n = 159), the following recognized breeds were represented: Abyssinian (n = 2), Bengal (n = 3), Birman (n = 1), Egyptian Mau (n = 1), Exotic Shorthair (n = 1), Maine Coon (n = 3), Norwegian Forest Cat (n = 1), Persian (n = 2), Ragdoll (n = 2), Siamese (n = 6) and Snowshoe (n = 1). No significant association was found between breed and CTR outcome (P = 0.090).

BCS was recorded for 180 patients and ranged from 1.5/9 to 9/9 (mean ± SD 5.0 ± 1.6). Two patients lacked a recorded BCS and were therefore excluded from BCS-related statistical analyses. No significant association was found between BCS and CTR outcome (P = 0.723).

Neurologic examination findings, metabolic disease and diagnostic classification

Based upon history and neurologic examination, each patient was assigned one of the following neurolocalizations: forebrain (n = 34), non-vestibular brainstem (n = 4), cerebellum (n = 3), peripheral vestibular (n = 13), central vestibular (n = 22), undetermined vestibular (n = 7), C1–C5 myelopathy (n = 4), C6–T2 myelopathy (n = 3), T3–L3 myelopathy (n = 13), L4–S3 myelopathy (n = 15), multifocal myelopathy (n = 10), neuromuscular (n = 24) or multifocal non-myelopathy (n = 30). For analytical purposes, all vestibular neurolocalizations were grouped together (n = 42) and all myelopathy neurolocalizations were grouped together (n = 45). There was no significant association between (1) neurolocalization and CTR outcome (P = 0.682), or (2) myelopathy and non-myelopathy neurolocalization relative to CTR outcome (P = 0.169). The distribution of neurolocalizations for patients in which the CTR was elicited and those in which the CTR was not elicited is presented in Table 3.

Table 3

Lesion neurolocalization in 118 cats in which the cutaneous trunci reflex (CTR) was elicited and 64 cats in which the CTR was not elicited

CTR status	FB	nTBS	CB	V	MY	NM	MF
Absent (n = 64)	12	1	1	15	12	12	11
Present (n = 118)	22	3	2	27	33	12	19

FB = forebrain; nTBS = non-thalamus brainstem; CB = cerebellum; V = vestibular; MY = myelopathy; NM = neuromuscular; MF = multifocal

Based on a review of patient history and examination findings, 11 patients were found to have sustained traumatic injury resulting in their neurologic abnormalities. Of these injuries, three involved head trauma, seven involved spinal trauma and one involved a suspected brachial plexus avulsion. There was no significant association between traumatic injury and CTR outcome (P = 0.165).

Patients were evaluated for signs of pain during examination. Pain was localized to the cranium/calvarium (n = 5), C1–T2 spine (n = 3), T3–L3 spine (n = 13), L4–S3 spine (n = 6), sacrococcygeal spine (n = 1), multifocal (n = 5) or other (cranial abdomen [n = 1], hips [n = 1], pelvic limbs [n = 1]). There was no significant association between the presence of pain and CTR outcome (P = 0.069). A significant association was found between patients exhibiting spinal pain (n = 28), including multifocal spinal pain, and CTR outcome (P = 0.037).

Twenty patients with known metabolic diseases (DM or hyperthyroidism) were enrolled in the study. There was no significant association between (1) metabolic disease and CTR outcome (P = 0.987), or (2) DM and CTR outcome (P = 0.906).

Patient mentation was graded as appropriate (n = 147), inappropriate (n = 4), dull (n = 27), obtunded (n = 2), stuporous (n = 1) or comatose (n = 1). There was no significant association between mentation (appropriate, other) and CTR outcome (P = 0.904).

Suspected or definitive diagnoses were achieved in 108 cases – often with the assistance of advanced diagnostics, such as CT imaging, MRI, cerebrospinal fluid analysis, biopsy and/or necropsy – with the diagnoses in the remaining 74 cases remaining open. These 108 diagnoses were subdivided into the following categories: congenital/anomalous (n = 3), degenerative (n = 7), idiopathic (n = 6), inflammatory/infectious (n = 24), metabolic (n = 7), neoplastic (n = 26), traumatic (n = 11) and vascular (n = 24). There was no significant association between diagnostic classification and CTR outcome (P = 0.566).

Discussion

The cutaneous trunci muscle (CTM) comprises a thin muscular sheath beneath the skin of the thorax and abdomen. In the cat, its boundaries are the latissimus dorsi muscle cranioventrally and the linea alba ventrally, with insertion primarily into the thoracic and lumbosacral spinal regions, and the ventrolateral tail.⁹ Unlike most skeletal muscle, the CTM lacks muscle spindles.^9,10 Afferent innervation is provided by the skin.^9,10 The lateral thoracic nerve, arising from the C8–T1 spinal cord segments via the brachial plexus, supplies efferent innervation.^9,11 While evocation of the CTR in mice and rats requires a noxious stimulus, light touch is sufficient to elicit the CTR in various other species, including cats.¹² Stimulation of the skin overlying the thoracolumbar CTM – such as through pinching with hemostatic forceps – transmits a signal through ascending propriospinal pathways to the CTM motor nucleus in the ventrolateral aspect of the ventral horn of C8–T1.⁹ Cutaneous afferents in the thoracolumbar region enter the spinal cord at their respective spinal cord segment and terminate in the gray matter, with interneurons projecting to the CTM motor nucleus.⁹ The CTM motor nucleus, via the lateral thoracic nerve, stimulates the CTM and causes a twitch.⁹ Ipsilateral stimulation results in a bilateral motor response.^9,10 Only a portion of the CTM is involved in the CTR.¹³ In addition to the shiver-like response seen in the CTR, the CTM may play a minor role in respiration through abdominal straining.^9,13

The CTR has been reasonably well characterized clinically in the dog, where it can be consistently elicited in nearly 100% of neurologically normal patents.^3,4 Measurement of the CTR is utilized to assist with patient neurolocalization, and its change over time can potentially provide prognostic information.^3,5 In the horse, evaluation of the CTR has been proposed as a measure of dose-related analgesia and as an adjunctive method to differentiate equine degenerative myeloencephalopathy and cervical stenotic myelopathy.^14,15 In laboratory animals, the CTR has been utilized for many purposes, including assessment of nociception and recovery from spinal cord injury.^12,16–18 A major unifying factor in these studies is the ability to consistently and repeatably elicit the CTR.

The present study revealed that the CTR in the cat may be less reliably invoked than in the abovementioned species. In the present study population of neurologically abnormal cats, the CTR was elicited in only 64.8% of patients. While approximately one-quarter of these patients had lesions that might be expected to influence the CTR due to the neurophysiology of the reflex pathway – particularly thoracolumbar myelopathies – no significant association was found between neurolocalization and CTR.⁵ For unknown reasons, the CTR was elicited in a greater percentage of patients with a myelopathy neurolocalization (73.3%; n = 45) than patients with a non-myelopathy neurolocalization (60.1%; n = 137). While this finding was not statistically significant, a statistically significant relationship was identified between the presence of spinal pain and ability to elicit the CTR. One possible explanation for both findings is that the examining clinicians were more thorough in their evaluation of the CTR in patients with myelopathies and/or spinal pain.

In the rat, CTR hyperreflexia resulted within 6 weeks following unilateral surgical spinal cord hemisection at T10.¹⁹ CTR response was measured through nociceptive dorsal cutaneous nerve stimulation and was found to be significantly increased relative to baseline ipsilaterally and contralaterally, and cranial and caudal, to the locus of hemisection.¹⁹ While the CTR pathways differ in these species, and severe spinal cord injury would necessarily result in other measurable neurologic deficits, further study may be warranted to evaluate whether CTR hyperreflexia may occur in the cat following spinal cord injury. This finding could conceivably explain a perceived improvement in the ability to elicit the CTR in cats recovering from spinal cord injury. Additionally, this retrospective study investigated CTR outcome only in neurologically abnormal cats. Further conclusions regarding CTR assessment and reliability in the cat will require controlled study of healthy cats lacking evidence of neurologic disease.

The absence of statistically significant relationships between CTR outcome and age, sex, breed, BCS and mentation were anticipated based upon the neurophysiology of the reflex. The high percentage of cats in which the CTR could not be elicited, despite the lack of a statistically discernible cause such as disruption of the reflex pathway resulting from spinal cord injury, raises concerns about the ability to consistently elicit this reflex in the feline patient and warrants further study. Attempts to elicit the reflex may also contribute to patient stress and irritation, potentially rendering further examination more challenging. Future studies are indicated to determine whether the CTR can be reliably elicited in neurologically normal cats and to compare the CTR between neurologically normal and abnormal populations.

This study calls into question the potential utility of the CTR as a diagnostic and prognostic aid for cats with suspected spinal cord injury. Ascending–descending myelomalacia (ADM) develops in approximately 10% of dogs with nociceptive negative paraplegia resulting from thoracolumbar myelopathy.⁵ This progressive disorder, in which spinal cord vascular thrombosis causes cranial and caudal expansion to the underlying spinal cord injury, is irreversible and uniformly fatal.^5,20 Cranial movement of the caudal border of the CTR in dogs is strongly associated with development of ADM and confers a grave prognosis.⁵ ADM has been documented in the cat and, in at least one case study, the CTR was absent bilaterally.^21,22 Owing to the high percentage of cats without demonstrable CTR, and the lack of significant association between CTR and neurolocalization, CTR measurement may not provide significant prognostic value in feline patients in which the CTR is unable to be elicited.

Several limitations were present in this retrospective study. Data were collected from, and limited to, pre-written medical records; follow-up queries and direct patient examination were not possible. Lesion localization was limited in many cases to the history provided by the client or veterinarian and was the result of a single neurologic examination performed by one of several clinicians with varying levels of training and experience. In a prior canine study, measurement of the caudal border of the CTR demonstrated moderate but imperfect inter-observer agreement.⁴ While all participating veterinarians in this study were trained to measure the CTR in the same manner, inter-observer reliability has not been evaluated in the cat. Additionally, patient anxiety was generally not recorded, except to the extent the patient posed a danger to handlers, as indicated by notation within the medical record as being fractious or a bite risk. Examination-related stress and anxiety may affect various physiologic processes in the cat, such as blood pressure, heart rate, temperature, respiratory rate and menace response.^6,23–25 Patient stress may likewise impact the ability to elicit (or perceive) the CTR, such as through increased baseline CTM tone.

Lastly, the presence of dermatologic disease and certain endocrine diseases could affect the CTR. The majority of the medical records did not identify skin disease, with most references to dermatologic disease comprising flea dirt and scale. Therefore, the data available from the sample population are insufficient to draw any conclusions regarding the effect of skin disease on the CTR. Subsequent larger-scale studies on the CTR in cats with dermatologic disease are recommended. Additionally, 20/182 cats had concurrent metabolic disease, such as DM and hyperthyroidism. DM has been associated with loss of skin innervation in humans,^11,26 and diabetic degenerative neuropathy in the cat is functionally identical to the equivalent human condition.^27,28 Further study is warranted to evaluate whether this condition – and other systemic endocrine or metabolic derangements, such as hyperthyroidism – may affect the ability to elicit the CTR.

Conclusions

This study has revealed that the CTR cannot be reliably elicited in the neurologically abnormal cat. Eliciting the CTR appears to be independent of age, BCS, sex, breed, evidence of traumatic injury, non-spinal pain, metabolic disease, mentation, neurolocalization and diagnostic classification. A significant association was found between spinal pain and the ability to elicit the CTR. Further studies are warranted in neurologically normal cats, as well as cats with spinal pain as the lone identifiable neurologic deficit, to determine whether these findings are generalizable or if a specific technique may result in a more reliable CTR response. If the CTR cannot be consistently and reliably elicited, re-evaluation of its value as a component of the feline neurologic examination may be indicated, particularly given the possible patient stress and discomfort resulting from its continued measurement.

Footnotes

Accepted: 17 March 2020

Author note

Parts of this study were presented at the 32nd ECVN/ESVN Annual Symposia, Wroclaw, Poland, September 2019.

Conflict of interest

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

Ethical approval

This work involved the use of non-experimental animal(s) only (owned or unowned), and followed established internationally recognized high standards (‘best practice’) of individual veterinary clinical patient care. Ethical approval from a committee was therefore not necessarily required.

Informed consent

Informed consent (either verbal or written) was obtained from the owner or legal custodian of all animal(s) described in this work for the procedure(s) undertaken. No animals or humans are identifiable within this publication, and therefore additional informed consent for publication was not required.

ORCID iD

Aaron M Paushter

Kari D Foss

William E Sander

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Assessment of the cutaneous trunci muscle reflex in neurologically abnormal cats

Abstract

Objectives

Methods

Results

Conclusions and relevance

Keywords

Introduction

Materials and methods

Results

Influence of age, breed and BCS

Neurologic examination findings, metabolic disease and diagnostic classification

Discussion

Conclusions

Footnotes

Author note

Conflict of interest

Funding

Ethical approval

Informed consent

ORCID iD

References