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Abstract

Objectives

The primary objective of this study was to investigate the prevalence of epileptic seizures and of presumed idiopathic epilepsy (PIE, describing epilepsy of unknown origin) in a cohort of British Shorthair (BSH) cats in Sweden. The secondary objective was to describe epileptic seizure characteristics and outcome for cats with PIE.

Methods

Owners of BSH cats born between 2006 and 2016 and registered with SVERAK (the Swedish Cat Clubs’ National Association) were invited to reply to a questionnaire about their cat’s general health. Owners who indicated that their cat had experienced epileptic seizures were invited to participate in an in-depth telephone interview about the epileptic seizures. The clinical characteristics of epileptic seizures in BSH cats were determined from the results of the interview.

Results

In this population comprising 1645 BSH cats (representing 28% of registered BSHs), the prevalence of epileptic seizures was 0.9% and for PIE it was 0.7%. BSH cats with PIE presented with infrequent but consistent epileptic seizures. Twenty-seven percent of BSH cats with epileptic seizures had cluster seizures but none presented with status epilepticus. None of the BSH cats was treated with antiepileptic drugs, and none of the owners reported epileptic seizure remission in their cat.

Conclusions and relevance

The prevalence of PIE in this population of BSH cats was 0.7%. The prevalence of epileptic seizures was 0.9%. In general, PIE in the BSH cat displayed a relatively benign phenotype where progression of epileptic seizures was uncommon.

Keywords

Behaviour epidemiology epileptic seizure intracranial seizures semiology

Introduction

Epileptic seizures are clinical manifestations of abnormal synchronous neuronal activity in the forebrain.^1,2 Epilepsy is a chronic condition characterised by recurrent epileptic seizures.^1–3 The reported prevalence of epileptic seizures presented to veterinary referral institutions in cats is 2.1–3.5%.^4,5 Historically, the majority of cats with epilepsy have been reported to have structural brain disease or reactive seizures with a metabolic or toxic aetiology.^6–10 During the past decade, several studies have shown that cats may present with epilepsy without an underlying disease, suggesting the presence of idiopathic epilepsy (IE) in cats similar to what has been reported in dogs and people.^4,5,11–13 IE has since been reported in 22–64% of cats with epileptic seizures.^{4,5,7,14–17} However, in cats, there are no published agreed clinical criteria to differentiate cats with IE from those with structural brain disease and therefore the term ‘presumed idiopathic epilepsy’ (PIE) will be used throughout this study to describe epilepsy of unknown origin in cats.

In the general dog population, the estimated prevalence of IE is 0.6–0.75%.^17,18 For individual dog breeds, the reported prevalence is higher (3–17%), suggesting a genetic aetiology.^19–24 Kuwabara et al described a familial spontaneous epileptic strain in laboratory-bred cats,¹¹ but a genetic origin of IE in a specific cat breed has not been confirmed. Currently, epidemiological data on epileptic seizures and PIE in cats are limited to data from primary and referral veterinary practices.^4,5,25 Reports of the prevalence of PIE in the general cat population or in any particular cat breed are lacking. The results of a recent study indicated that some cat breeds, including the British Shorthair (BSH), might have an increased risk of epilepsy, compared with domestic cats.²⁵ The aim of this study was to further investigate the prevalence of epileptic seizures and PIE in a cohort of BSH cats. In addition, we aimed to describe the clinical characteristics of BSH cats with PIE.

Materials and methods

Data collection

Owners of BSH cats born between 2006 and 2016 were identified using the Swedish Cat Clubs’ National Association (SVERAK) register. In phase 1, the owners of BSH cats were invited to participate in an online general health questionnaire. The responses were analysed, and cats reported to show seizure-like activity were identified. In phase 2, these owners were contacted for a follow-up interview.

Phase 1: questionnaire

All owners of BSH cats born between 2006 and 2016 and registered in SVERAK with a valid email address on file were sent an electronic invitation to participate in an online survey named ‘Health in the British Shorthair cat’ in September 2017. A link to an online questionnaire was provided. The Swedish BSH cat breeding club published information about the survey on their website and Facebook page.

Owners of multiple BSH cats received a separate invitation for each cat. It was only possible to answer the questionnaire once for every cat. A reminder was emailed to owners that had not completed the survey within 14 days.

The online questionnaire was constructed so that the next question was not revealed until the current question had been answered. The questionnaire was initiated with general questions regarding age, reproduction status, if the cat was deceased or alive, and in the event the cat was deceased, the reason for euthanasia/death (see supplementary material 1). The main question (MQ), ‘Have you recognised potential seizures in your cat?’, followed the general questions. The MQ was accompanied by a short description of common epileptic seizure characteristics in cats.

Phase 2: telephone interview

All owners who responded that they had recognised potential epileptic seizures in their cat and agreed to be contacted further were approached for an in-depth telephone interview. All interviews were conducted by the same person (MT). Questions included open questions related to the characteristics of the epileptic seizure (possible preictal, ictal and postictal signs, potential autonomous signs), age at epileptic seizure onset, frequency of epileptic seizures at seizure onset and progress of epileptic seizure frequency over time, time of the day/year when the epileptic seizures occurred, if the cat was interictally normal or not, history of a potential cause of the epileptic seizures (eg, head trauma or concurrent metabolic disease), the use of antiepileptic or other drugs, response to treatment, concurrent diseases and outcome (see supplementary material 2). Rhetorical questions were asked to ensure that the interviewer had understood the owner’s description of the epileptic seizures correctly.

Phase 3: data analysis

Information gained from the telephone interviews was reviewed by two board-certified neurology specialists (CR, SVM). Cats were only included in the epileptic seizure group when both reviewers agreed that the episode recognised by the owner was likely to have been an epileptic seizure. Epileptic seizures were defined as generalised or focal. Generalised epileptic seizures were characterised by transient episodes with the acute onset of lateral recumbency and tonic–clonic limb movements with loss of responsiveness. Focal epileptic seizures were defined as transient episodes with the acute onset of lateralised and/or regional signs of abnormal movements of one part of the body, such as contractions of one limb or facial muscle group.³ To be categorised as an epileptic seizure, transient episodes of rapid running had to be accompanied by at least one autonomous sign. Autonomic signs included mydriasis, salivation, involuntary urination, involuntary defaecation or vocalisation.

Cluster seizures (CSs) were defined as more than one epileptic seizure within 24 h with full recovery of consciousness between epileptic seizures. Status epilepticus was defined as continuous seizure activity lasting >5 mins or more than two epileptic seizures without full recovery of consciousness between the epileptic seizures.³

To be included in the study population the owners had to have answered the MQ: ‘Have you recognised potential seizures in your cat?’. Cases in which the owner stated that the cat had suffered from potential epileptic seizures, but the owner subsequently declined to take part in phase 2 of the study, were excluded from the study population.

All cats considered to have experienced at least one epileptic seizure were included in the epileptic seizure group.

To be included in the PIE group the cat had to have shown a minimum of two epileptic seizures >24 h apart and the time period between the first and the last noted epileptic seizure had to be >6 months. Epileptic seizure onset had to be before 8 years of age. In addition, the cat had to be interictally normal for ⩾1 year after the onset of epileptic seizures. Seizure remission was defined as no epileptic seizures for >1 year.

Statistical analysis

Descriptive statistics were used for characteristics such as sex and reproductive status, epileptic seizure type, postictal signs, autonomous signs, mortality and changes in epileptic seizure frequency and duration with time.

Data are reported as median (interquartile range [IQR]) for continuous variables.

Results

In total, 5809 BSH cats born between 1 January 2006 and 31 May 2016 were registered with SVERAK (Figure 1). An invitation to participate in the study was sent to all owners with a valid email address in the SVERAK register; this group consisted of 4383 BSH cat owners (Figure 1).

Figure 1

Flowchart of the epidemiological investigation of epilepsy carried out in purebred British Shorthair cats from 2006 to 2016. Note 1: three owners with cats with suspected seizures did not want to participate in a telephone interview; their cats were excluded from the study. Note 2: four owners had changed their mind and were sure their cats never had experienced any seizure-like episode. These cats were included in the group without seizures

A response to the MQ was provided by 1652 owners. Twenty-six owners (1.6%) answered ‘Yes’ to the MQ and were invited to participate in the telephone interview (phase 2). Seven (7/26) owners responding ‘yes’ to the MQ in the questionnaire declined to participate in phase 2; these cats were excluded from the study population. The final study population included 1645 responders corresponding to 38% of BSH cats whose owners were invited to participate in the study, and 28% of all nationally registered BSH cats during this period (Figure 1).

Nineteen (1.2%) BSH cat owners participated in phase 2 (Figure 1). Each telephone interview lasted between 40 mins and 1 h.

Prevalence of epileptic seizures and PIE

Based on the review of the owner’s description of their cat’s episodes, 14 BSH cats (0.9%) were categorised as having had at least one epileptic seizure. No cat was excluded owing to lack of agreement between reviewers. The five cats that were not included in the epileptic seizure group after the review presented with the following signs: rapid running without autonomous signs (n = 2) and paroxysmal events not suggesting epileptic seizures (n = 3). Ten of 14 owners with cats with epileptic seizures (71%) had consulted a veterinarian because of the epileptic seizures, eight had consulted a primary care veterinarian and two owners both a primary care and referral practice veterinarian.

Three of the cats reported to have shown seizure-like activity did not meet the inclusion criteria for PIE; two cats presented with only one epileptic seizure and one cat presented with CSs during parturition. Finally, 11 cats (0.7%) met the inclusion criteria for PIE.

A traumatic event or known toxic exposure was not reported by any of the owners.

Clinical phenotype of BSH cats with PIE

The PIE group (n = 11) included five neutered male cats, five neutered females and one intact female. The median age at first epileptic seizure was 18 months (IQR 8–48) and the median length of follow-up after epileptic seizure onset was 2 years (IQR 1.5–4). Epileptic seizure frequency (SF) at seizure onset, SF progress over time and the occurrence of CSs in cats with PIE are described in Table 1.

Table 1

Epileptic seizure frequency (SF) at seizure onset, SF progress over time, the occurrence of cluster seizures (CSs) and CS progress over time for British Shorthair cats with presumed idiopathic epilepsy

Variable	SF estimate per month at seizure onset	Variation of SF over time	Occurrence of CSs	Variation of CSs over time
All cats	Median 0.5 (IQR 0.25–1)	82% (n = 9) not changed, 9% (n = 1) decreased frequency, 9% (n = 1) increased frequency	73% (n = 8) no CSs, 27% (n = 3) CSs	33% (n = 1) decreased, 33% (n = 1) increased
Cat 1	0.75	No	No	–
Cat 2	6	Gradual decrease, at the time of writing having about one seizure every week instead of CSs every day at the beginning	Yes	CSs at seizure onset, gradual decrease, at the time of writing no CSs for several years
Cat 3	0.5	No	No	–
Cat 4	2	No	No	–
Cat 5	0.25	No	No	–
Cat 6	0.2	No	No	–
Cat 7	0.5	No	No	–
Cat 8	0.3	No	Yes	Only once, two seizures during 24 h
Cat 9	1	Yes, frequency gradually increased in number over 1 year	Yes	CSs every day before euthanasia
Cat 10	0.25	No	No	–
Cat 11	0.1	No	No	–

IQR = interquartile range

Preictal signs or an environmental trigger were not recognised by any of the BSH cat owners. Ictal clinical signs were all reported to have had a sudden onset. The duration of the ictal phase, variation of ictal phase over time, autonomous clinical signs, postictal clinical signs and duration of postictal clinical signs in the PIE group are presented in Table 2.

Table 2

Duration of the ictal phase, variation of ictal phase over time, autonomous clinical signs, postictal clinical signs and duration of postictal clinical signs in British Shorthair cats with presumed idiopathic epilepsy

Variable	Ictal signs	Progress of ictal signs over time	Duration of ictal signs (mins)	Autonomous signs	Postictal signs
All cats	55% (n = 6) focal seizure only 36% (n = 4) generalised seizures only 9% (n = 1) both focal and generalised	91% (n = 10) no change 9% (n = 1) less severe than before	Median 1.5 (IQR 0.75–5)	82% (n = 9) salivation36% (n = 4) mydriasis9% (n = 1) urination9% (n = 1) vocalisation18% (n = 2) no autonomous signs	82% (n = 9) postictal signs18% (n = 2) no postictal signs
Cat 1	Focal seizures; stares at the wall	No	5	Excessive salivation, mydriasis	None
Cat 2	Focal seizures; twitching over one eye, chewing	The twitching in the face decreased with time	5	Excessive salivation, vocalisation	Fatigue
Cat 3	Focal seizures; ambulatory but rapid running	No	5	Excessive salivation, mydriasis	Stressed, hyperventilating at first, fatigue
Cat 4	Generalised tonic–clonic epileptic seizures	No	1	None	Fatigue
Cat 5	Generalised tonic–clonic epileptic seizures	No	0.5	Excessive salivation	Fatigue, disoriented, does not seem to know its owner
Cat 6	Focal seizures; stares at the wall	No	5	Excessive salivation, mydriasis	Hungry, fatigue
Cat 7	Generalised tonic–clonic epileptic seizures	No	0.75	Excessive salivation, urination, mydriasis	Ataxic, fatigue
Cat 8	Two types of seizures: sometimes generalised tonic–clonic epileptic seizures; sometimes rapid running	No	1.5	Salivation	Disoriented, hungry, less social than normal
Cat 9	Generalised tonic–clonic epileptic seizures	No	0.5	None	Fatigue
Cat 10	Focal seizure; tonicity in one body half, which makes it lean to one side	No	1.5	Salivation	Ataxic
Cat 11	Focal seizure; stares at the wall, hides	No	10	Excessive salivation	None

When asked about interictal abnormalities, four owners (36%) spontaneously described their cats as more anxious in their interactions with other cats or people vs the behaviour of other cats in the household.

Outcome

None of the cats in the PIE group had gone into epileptic seizure remission and none of the cats was being treated with an antiepileptic drug (AED) at the time of the study.

Seven (64%) of the cats with PIE and 1470 (89%) of the cats in the study population were alive at the time of the study. Two (19%) of the cats with PIE were euthanased because of presumed poor quality of life due to the epileptic seizures (cat 4 had experienced two seizures every month since seizure onset and cat 9 developed CSs) between 1 and 1.5 years after the onset of epileptic seizures. Two additional cats (19%) with PIE were euthanased for reasons unrelated to PIE.

Discussion

To our knowledge, this is the first study to investigate the prevalence of epileptic seizures and epilepsy in a specific cat breed. Compared with previous reports, the prevalence of epileptic seizures in BSH cats (0.9%) was lower than in the general cat population.^1,2 Previous epidemiological evaluations of feline epileptic seizures and epilepsy have described cats registered at primary and/or referral veterinary practices, while our study included registered BSH cats (SVERAK), likely providing a more representative selection of the general population.^4,5,25 Prevalence rates have been shown to differ considerably for dogs, where hospital populations may present with a higher prevalence than the general canine population.³ The lower prevalence of epileptic seizures in BSH cats vs the general cat population may also be a consequence of our study including a younger population of cats (aged <10 years) vs cats included in previous studies.^4,5 In general, older cats are more at risk of developing epileptic seizures with a reactive or structural aetiology.^4,5,13,16,25

The prevalence of BSH cats with PIE in this study population was 0.7%, which is similar to the more well-established prevalence of IE (0.6–0.75%) in the general dog population.^17,18 Considerably higher prevalence rates of IE are reported for some dog breeds vs the prevalence estimated for the general dog population, suggesting a genetic predisposition.^{20–24,26,27} A 2020 study by O’Neill et al found that 0.15% of BSH cats and 0.16% of the total number of cats presenting to primary veterinary care over 1 year showed recurrent epileptic seizures and no convincing evidence for a high prevalence of recurrent epileptic seizures in any cat breed, but the small number of purebred cats with epilepsy might have influenced their results.²⁵ Although not an aim of this study, pedigree data available through SVERAK confirmed that two cats in the PIE group were closely related; both had generalised epileptic seizures. Further studies, including pedigree data with a larger number of affected cases, are needed to evaluate genetic epilepsy in cats.

By inviting BSH cat owners to respond to a questionnaire about ‘general health in British Shorthair cats’ instead of ‘prevalence of epilepsy in the British Shorthair cats’ we aimed to reduce the risk of responder bias. ‘Epilepsy’ is an emotionally charged word that might have affected the owners’ willingness to participate in the study. Indeed, seven of the owners who in the questionnaire reported potential epileptic seizures were excluded from the study population as they did not want to take part in a telephone interview or, upon contact, denied that their cat had ever had any seizures. A reason for this might be unwillingness to reveal the presence of epilepsy in the owner’s cat or breeding line.

The clinical characteristics of epileptic seizures in BSH cats corresponded well to previous studies on cats with PIE. All BSH cats with generalised epileptic seizures had tonic–clonic movements and focal ictal signs consisting mostly of paroxysmal events with cats staring at the wall and experiencing autonomous signs. The majority of cats in this study with PIE (82%) presented with autonomous signs, all with ictal salivation and for one (9%) of the cats ictal vocalisation was described.¹⁶ A previous study showed that ictal salivation was more common in cats with PIE than in cats with structural epilepsy, and that ictal vocalisation was more common in cats with structural epilepsy than in cats with PIE.¹⁶ All cats with focal epilepsy in this study (n = 7) showed salivation and three (75%) showed mydriasis, which agrees with a previous study reporting autonomous signs in cats with induced temporal lobe epilepsy.²⁸ Postictal signs were noted for 82% of the BSH cats with PIE in this study. Common signs included ataxia or fatigue lasting for minutes to hours before the cat returned to normal. In a previous study, ataxia was the most commonly described postictal sign in cats.⁵

Most cats (73%) in our study presented with fewer than one epileptic seizure a month, and for the majority (82%) of cats the frequency of epileptic seizures did not change over time. Although 71% of the BSH owners had consulted a veterinarian about the epileptic seizures, none of the cats was treated with AEDs at the time of the study. This might reflect the fact that the population of cats in this study was not from a referral hospital population and hence possibly included less severe cases, cases seen by veterinarians less familiar with treating epileptic seizures or owners less likely to want to medicate their cats. It has previously been shown that the handling of patients with epilepsy varies markedly depending on the population studied.^29,30 Previous studies have reported an epileptic seizure frequency for cats with PIE of 1–20 seizures/month before treatment with AEDs was instituted.^31–33

None of the cats with PIE in this study went into epilepsy seizure remission. Complete epilepsy seizure remission for cats with PIE has been reported in 42–44% of cases.^12,13 The use of AEDs most likely influenced the remission rate in previous studies.^12,13 Also, our inclusion criteria for PIE, with at least 6 months between the first and last epileptic seizure, excluded the majority of self-limiting conditions causing epileptic seizures.^13,16 Our results indicate that remission without AED therapy is an uncommon event in PIE in the BSH breed.

Interestingly, when asked about interictal abnormalities in their cats, four owners (36%) of BSH cats in the PIE group spontaneously described their cats as being more anxious, compared with their experience with other cats. Neurobehavioural comorbidities have not been described in cats but have been reported in people with IE.^34,35 Several studies in dogs with IE have proposed that behaviour changes are a common finding in IE.^36–42

Limitations of the study

The clinical characteristics of epileptic seizures in veterinary medicine are mainly based on the owners’ description of the events, which was also the case in our study. However, a report studying differences in how neurologists vs caregivers to human patients with epilepsy described seizures showed good inter-observer agreement.⁴³ This suggests that owners are capable of recognising epileptic seizure activity in their cats.

No clinical or neurological examination was performed in any of the cats included in the PIE group for this study and none underwent diagnostic work-up. Instead, stringent inclusion criteria, based on earlier data on feline epilepsy, were applied to be categorised as having PIE.^{5,12,13,16,44}

The inclusion of cats in this study was based on cats being registered in SVERAK. Although registration of cats is not mandatory in Sweden, the majority of Swedish breeders choose to register all their litters in SVERAK, suggesting that the vast majority of Swedish BSH cats were enrolled in this study.

Conclusions

The prevalence of epileptic seizures in Swedish BSH cats born between 2006 and 2016 was 0.9%, and the prevalence of PIE in the same population was 0.7%.

BSH cats with PIE presented with infrequent, but consistent, epileptic seizures often without progression. Some owners reported interictal behaviour changes, which might indicate a behavioural comorbidity in BSH cats with PIE. None of the cats with PIE received AEDs at the time of the study and none of the cats with PIE went into epileptic seizure remission.

Supplemental Material

Supplementary material 1

Questions asked in the general health survey translated from Swedish

Supplemental Material

Supplementary material 2

Information collected from each owner in the in-depth telephone interview

Footnotes

Acknowledgements

We thank SVERAK (The Swedish Cat Clubs’ National Association) for providing information from their register, all animal owners who kindly let us collect information about their pets, the breeder club for British Shorthair cats for their kind help and posting information about the study on their website and the Anicura Research Fund for funding the project.

Accepted: 13 July 2021

Supplementary material

The following files are available online:

Supplementary material 1: questions asked in the general health survey translated from Swedish.

Supplementary material 2: information collected from each owner in the in-depth telephone interview.

Conflict of interest

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

Funding

This research was funded by the AniCura Research Fund.

Ethical approval

This work did not involve the use of animals and therefore ethical approval was not necessarily required.

Informed consent

This work did not involve the use of animals (including cadavers) and therefore informed consent was not required. No animals or people are identifiable within this publication, and therefore additional informed consent for publication was not required.

ORCID iD

Marianne Tenger

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Klang

Epilepsy in cats: theory and practice.

J Vet Intern Med 2014; 28: 255–263.

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Epilepsy in British Shorthair cats in Sweden

Abstract

Objectives

Methods

Results

Conclusions and relevance

Keywords

Introduction

Materials and methods

Data collection

Phase 1: questionnaire

Phase 2: telephone interview

Phase 3: data analysis

Statistical analysis

Results

Prevalence of epileptic seizures and PIE

Clinical phenotype of BSH cats with PIE

Outcome

Discussion

Limitations of the study

Conclusions

Supplemental Material

Supplementary material 1

Supplemental Material

Supplementary material 2

Footnotes

Acknowledgements

Supplementary material

Conflict of interest

Funding

Ethical approval

Informed consent

ORCID iD

References

Supplementary Material