Neurological Disorders in Pug Dogs: a Retrospective Study of 285 Cases (2013 – 2020) from a Single Referral Hospital in the United Kingdom

Introduction

Pugs were among the 10 most popular breeds in the UK in 2020 [1]. Compared to other breeds, pugs were identified at higher risk for a variety of health conditions, raising welfare concerns [2, 3]. In particular, neurological disorders were recently included in the 30 most common disorders of pugs [2]. Nonetheless, 93% of owners of brachycephalic breeds, including pugs, were recently found likely to own the same breed again in the future, and over 70% of pug owners would recommend this breed to first-time dog owners [4].

Consequently, the authors feel that widening the knowledge and literature about this breed would be useful for veterinary surgeons, breeders and dog owners. To the authors’ knowledge, the prevalence and localisation of neurological disorders among pugs has yet to be evaluated. Therefore, with this retrospective observational study, we aimed to report and analyse the neurological disorders diagnosed in a cohort of pugs presented to a single referral hospital in the UK, including their clinical presentation and the diagnostics test that were performed. As stated above, a better understanding of their distribution and characteristics could be useful to veterinary surgeons working in primary care and referral hospitals, and could be used as baseline for future studies in larger populations.

Methods

The medical records of pugs presented to Dick White Referrals (UK) from 1st January 2013 to 31st December 2020, for which a neurological condition was diagnosed, were retrieved from the electronical database. All medical records were reviewed by the main investigator and cases were included in the study if: (1) the medical record was complete, (2) the clinical signs were compatible with a neurological disease, (3) a final diagnosis was achieved. For some conditions (such as meningoencephalitis of unknown aetiology, MUA), a definitive diagnosis via histopathology was not available in all cases, in these cases additional criteria were used as described below. If a patient was admitted on several occasions, but always for the same medical condition, only the first visit was considered. Instead, if a patient was admitted on different occasions because of different medical conditions, each admission was considered as a separate medical record. If multiple findings were identified during investigations, only the findings responsible for the neurological clinical signs (according to clinician’s judgement) were recorded and considered for the final diagnosis. If a pug was presented solely for a radiographic screening of vertebral malformations (VMs), the medical record was excluded.

Clinical data including signalment (age, gender, and body weight), presenting complaint, presence or absence of pain, diagnostic investigations, and final diagnosis were recorded in an electronic spread sheet (Microsoft Excel for MAC version 16.60). A dog was considered painful at presentation if this was clearly stated on the animal’s initial neurological examination or based on the kennel sheet if an analgesic was administered upon hospital admission.

Final diagnoses were grouped into three categories: encephalopathies, myelopathies and diseases affecting the peripheral nervous system (PNS). All cases were under the primary care of a board-certified neurologist or a neurology resident under direct supervision.

A single low field magnetic resonance imaging (MRI) machine (Aperto/Lucente Hitachi 0.4 Tesla) was used throughout the study period. Analysis of cerebrospinal fluid (CSF) was performed by a board-certified clinical pathologist or resident under direct supervision.

Results

A total of 466 medical records of pugs presenting to the Neurology and Neurosurgery Service were retrieved, of which 281 were excluded due to one of the following reasons (Figure 1): incomplete medical records (n = 30), diagnosis of a non-neurological condition (n = 16), final diagnosis not reached (n = 20), presenting solely for radiographic screening for vertebral malformations (n = 58), or re-presenting for a previously diagnosed neurological condition (n = 157). From the 285 pugs included in the study, 236/285 (91%) presented once, while 23/285 (8.7%) and 1/285 (0.3%) presented twice and three times for different conditions, respectively.

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Figure 1: The Consolidated Standards of Reporting Trials (CONSORT) flow diagram of pug dogs referred to the Neurology & Neurosurgery department of Dick White Referrals (UK) from January 2013 to December 2020. A. Incomplete medical records; B. Diagnosis of a non-neurological condition; C. Final diagnosis not reached; D. Radiographic screening for vertebral malformations; E. Re-presenting for a previously diagnosed neurological condition.

Patient signalment including age, gender, neuter status and body weight was analysed for each diagnoses group separately (Table 1) and is described in the specific sections below.

Table 1: Signalment and presence of pain at neurological examination for each the three final diagnoses obtained in a cohort of pug dogs referred to the Neurology & Neurosurgery department a single referral centre in the UK. PNS: peripheral nervous system; M: male entire; MN: male neutered; F: female entire; FN: female neutered; BW: body weight; n = number of cases. P value refers to the comparison between the three groups. In the same row, same superscript letter refers to p < 0.05 between groups.

Ambulatory paraparesis was the most common presenting symptom in 79 cases (27.6%), followed by seizures (n = 58, 20.3%), ataxia (n = 47, 16.4%) and spinal pain (n = 29, 10.1%). The remaining cases were referred for investigation of vestibular signs (n = 16, 5.6%), non-ambulatory paraparesis (n = 12; 4.2%), ambulatory tetraparesis (n = 9; 3.15%), behavioural changes / involuntary movements (n = 9; 3.15%), monoparesis (n = 7; 2.5%), paraplegia (n = 4; 1.4%), non-ambulatory tetraparesis (n = 3; 1.05%), muscle atrophy (n = 3; 1.05%), head trauma (n = 3; 1.05%), facial nerve paralysis (n = 2; 0.7%), hemiparesis (n = 2; 0.7%), visual deficits (n = 1; 0.35%) and generalized weakness (n = 1; 0.35%).

Investigations were performed according to clinician’s recommendation and owner’s consent; a total of 278 cases (97.5%) underwent MRI scan. CSF was collected in 89 (31.2%) cases. Serology for Toxoplasma gondii and Neospora caninum was performed in 49 (17.5%) cases.

Myelopathies were the most common diagnosis, followed by encephalopathies, and PNS diseases were the least common (Table 1). Pugs diagnosed with encephalopathies were younger (p = 0.0003) than those diagnosed with myelopathies. Pugs with myelopathies were more likely to be painful than both those with encephalopathies [reciprocal OR 13.45 (4.23 – 41.94), p < 0.0001] or PNS disease [OR 6.89. (1.08 – 74.24), p = 0.04].

Discussion

This is the largest study reporting a wide range of neurological conditions in a large sample of pugs from a single referral centre in the UK to the authors’ knowledge. Myelopathies were overrepresented, with IVDE, IVDP, ANNPE, SAD and VMs comprising almost 60% of all diagnosed conditions. Conditions of the PNS were rarely reported in this population. In accordance with the previously reported high prevalence of gait abnormalities in pug dogs [9], the most frequent presenting complaints were: ambulatory paraparesis and ataxia, when referring to myelopathies and seizures, when referring to encephalopathies.

A recent study reporting the prevalence of neurological conditions in French bulldogs, found that IVDDs and SAD were the most frequent diagnoses [10], results similar to those of the present study, supporting possible predisposition of both breeds to develop myelopathies. Approximately one third of the total population of pugs in this study were affected by IVDDs. Whilst previous studies into IVDDs in dogs have included pugs, their prevalence was low compared to other breeds such as Dachshund, Pembroke Welsh Corgi and French Bulldog [11, 12]. The present study supports that IVDDs should be included amongst the main differentials for pugs presenting with myelopathies. According to our results, IVDDs are more likely to be painful than other myelopathies, and are more commonly localised at thoracolumbar level. In the present study, when a pug was comfortable on analgesia at the time of presentation, then the referring notes were used to record the presence or absence of pain. This may explain the high proportion of painful pugs diagnosed with ANNPE, since vocalisation and spinal hyperaesthesia are common at initial presentation [13].

SAD was diagnosed on 14.4% (41/285) of the total population of pugs included in this study. Mauler, et al. [6] found that pugs were the most commonly affected breed in a population of dogs presenting with SAD. SAD is generally described as a non-painful condition in dogs [6, 14], and the present study supports this statement having found only one case experiencing pain at neurological examination.

VMs, most commonly affecting the thoracic vertebrae, were the cause for clinical signs in 14.4% (41/285) of the total population of pugs included. In the present study, only findings suspected responsible for the clinical signs were reported, thus it is likely that the prevalence of VMs was higher and in many cases incidental. A recent study investigated the presence of CAPD and its association with clinical signs of myelopathy, and failed to confirm the latter [15]. Similarly, a study on thoracolumbar VMs in pugs failed to reach an association between the presence of VMs and relevant clinical signs, although the majority of VMs were adjacent to an area of focal spinal cord pathology, suggesting a possible clinical impact [16]. Previously, clinically relevant thoracic VMs, such as hemivertebrae, were described in 5% of all pugs [17, 18], although most dogs were free from clinical signs. In our study, pugs diagnosed with VMs were younger compared to those diagnosed with myelopathies, suggesting that this condition should be included in the differentials for young pugs with gait abnormalities usually non-painful. One case of spinal cord gliosis and one case of spinal cord atrophy were documented. Spinal cord gliosis and atrophy could be considered features indicative of constrictive myelopathy [19], which is a differential in pugs presenting with progressive gait abnormalities and urinary and/or faecal incontinence [19, 20]. Recent literature suggests that the development of constrictive myelopathy is common in pugs and often a result of several coexisting conditions, including CAPD, IVDP, and SAD, whilst CAPD alone is often incidental and not responsible for clinical signs [21].

Idiopathic epilepsy was the most represented encephalopathy. Pugs diagnosed with encephalopathies were significantly younger when compared to myelopathies or PNS diseases. Although pugs are not among the breeds with an identified genetic background for idiopathic epilepsy [22], a high prevalence of seizures was documented among pugs presenting to primary veterinary care in the UK [23]. Further studies are required to evaluate a possible genetic background for idiopathic epilepsy in pugs. MUA was the second most prevalent encephalopathy found but the diagnosis was mainly antemortem. Therefore, it is possible that the prevalence of MUA cases has been over or underestimated. Post-mortem examination, performed in 5/29 of the MUA cases, revealed the presence of necrotizing meningoencephalitis (NME), also known as pug dog encephalitis. NME was first reported in 1989 [24] and its imaging and histopathological features have been better characterised since. Two specific risk loci have been also associated to the development of NME in pugs [25]. A predisposition for young adult female pugs has been described [26], which is supported by the findings of our study. The small population of pugs diagnosed with NME in this present study could have also been affected by the referral population setting, considering that pugs with clinical signs compatible with NME may have been euthanised at the primary care veterinary centres without referral on the suspicion for poor prognosis.

Otitis was frequently associated with signs suggestive of peripheral vestibular disease, as previously described [27]. Masticatory muscle myositis has been reported in pugs [28], although it is not among the most commonly reported breeds, in agreement to the findings of the present study only a small number of patients was diagnosed with this condition. Future studies regarding the most common diseases of the PNS in brachycephalic breed dogs are warranted.

There are several limitations in the present study arising mainly from its retrospective nature. The caseload might be biased by the topographical differences in the prevalence of neurological disorders in the UK compared to other countries, and the fact that only a single and referral hospital was included. Cases were managed by different neurologists over a period of several years and the diagnostic steps for each specific disease were not standardized. The presence or absence of pain was documented based on referring notes and administration of analgesic at the time of admission, and pain scores were not available. Only findings suspected to be responsible for the presenting clinical signs were reported, thus other, coexisting conditions may be underrepresented if considered incidental (such as CAPD or other VM). Cases without a final diagnosis were excluded from the study, which may have biased the frequency of some conditions over others. For example, pugs presenting in refractory status epilepticus, may have been euthanised prior to investigations, cases with mild neurological signs may have been discharged without pursuing further investigations, or financial factors may have precluded allowing investigations, thus not reaching a definitive diagnosis. Finally, histopathological confirmation was not available in most cases of MUA, leading to a suspected rather than confirmed diagnosis for this disease, and not allowing more specific classification of the type of MUA for each case.

Conclusion

This is the first study reporting various neurological conditions in a large population of pugs. Myelopathies are the most common group of neurological diseases diagnosed in pugs, and they tend to be more frequently localised at the thoracolumbar level. The presence or absence of pain at neurological examination might be useful to differentiate among different myelopathies. Encephalopathies are the second most common category of neurological diseases diagnosed in pugs, and those dogs present significantly younger than those with myelopathies. PNS diseases are uncommon in this breed. The results of the present study can form the basis for future studies and be of interest for veterinarians, pug breeders and owners.

Ethical Approval

Ethical approval was obtained from the School’s Committee for Animal Research and Ethics (CARE); School of Veterinary Medicine University of Nottingham. Signed informed owner consent to use clinical information for retrospective studies was granted at the time of the animal’s admission.