Prevalence of neurological disorders in French bulldog: A retrospective study of 343 cases (2002-2016)

Abstract

Background
French Bulldog (FB) has significantly gained in popularity over the last few years, and seems to be frequently affected by various neurological conditions. The purpose of this retrospective study was to report the prevalences of neurological diseases in a large population of FB, presented with neurological signs between 2002 and 2016, and for which a definitive diagnosis was established. A secondary objective was to identify epidemiological characteristics regarding specific diseases in this singular breed.

Results
During the study period, 533 FBs were presented for neurological signs, representing 18.7% of all admitted FBs (N = 2846). In total, 343 FBs with definitive diagnosis were included in this descriptive epidemiological study. Hansen type I intervertebral disk herniation (IVDH) was by far the most common neurological disorder (45.5% of all cases). The IVDH location was cervical in 39.8%, and thoracolumbar in 60.2% of cases. The median ages for cervical and thoracolumbar IVDH were 4.2 and 4 years, respectively. C3-C4 was the most commonly affected disk (57.8% of cervical IDVH) all locations combined. Spinal arachnoid diverticulum (SAD) was detected in 25 FBs, representing the second most common myelopathy (11.3%). A concurrent spinal abnormality was identified in 64.0% of SAD cases. Brain tumours represented 36.8% of encephalopathies, with glioma (confirmed or suspected) being the most common. Meningoencephalitis of unknown origin (MUO) represented 25.0% of brain disorders, females less than 5.5 years being more likely to be affected. Aside from central nervous system conditions, otitis interna associated with peripheral vestibular signs and bilateral congenital deafness (associated with white coat) were also common.

Conclusions
The findings of this study suggest that FB seems to be prone to several neurological diseases. IVDH is clearly predominant in FB and cervical location seems more represented than in other breeds. FBs affected by IVDH tend to be younger than previously described, either for both cervical and thoracolumbar locations. Thoracic SAD was the second most common myelopathy, with a concurrent spinal anomaly identified in two thirds of the cases. MUO was more likely to affect young to middle-aged females. These findings could be of interest for owners, breeders, practicing veterinarians and insurance companies.

Full text

R E S E A R C H A R T I C L E Open Access
Prevalence of neurological disorders in
French bulldog: a retrospective study of
343 cases (2002–2016)
Vincent Mayousse
1,3,5*
, Loïc Desquilbet
2
, Aurélien Jeandel
1,4
and Stéphane Blot
1,3,5
Abstract
Background: French Bulldog (FB) has significantly gained in popularity over the last few years, and seems to be
frequently affected by various neurological conditions. The purpose of this retrospective study was to report the
prevalences of neurological diseases in a large population of FB, presented with neurological signs between 2002
and 2016, and for which a definitive diagnosis was established. A secondary objective was to identify epidemiological
characteristics regarding specific diseases in this singular breed.
Results: During the study period, 533 FBs were presented for neurological signs, representing 18.7% of
all admitted FBs (N= 2846). In total, 343 FBs with definitive diagnosis were included in this descriptive
epidemiological study. Hansen type I intervertebral disk herniation (IVDH) was by far the most common
neurological disorder (45.5% of all cases). The IVDH location was cervical in 39.8%, and thoracolumbar in
60.2% of cases. The median ages for cervical and thoracolumbar IVDH were 4.2 and 4 years, respectively.
C3-C4 was the most commonly affected disk (57.8% of cervical IDVH) all locations combined. Spinal
arachnoid diverticulum (SAD) was detected in 25 FBs, representing the second most common myelopathy
(11.3%). A concurrent spinal abnormality was identified in 64.0% of SAD cases. Brain tumours represented
36.8% of encephalopathies, with glioma (confirmed or suspected) being the most common. Meningoencephalitis of
unknown origin (MUO) represented 25.0% of brain disorders, females less than 5.5 years being more likely to be
affected. Aside from central nervous system conditions, otitis interna associated with peripheral vestibular signs and
bilateral congenital deafness (associated with white coat) were also common.
Conclusions: The findings of this study suggest that FB seems to be prone to several neurological diseases. IVDH is
clearly predominant in FB and cervical location seems more represented than in other breeds. FBs affected by IVDH
tend to be younger than previously described, either for both cervical and thoracolumbar locations. Thoracic SAD was
the second most common myelopathy, with a concurrent spinal anomaly identified in two thirds of the cases. MUO
was more likely to affect young to middle-aged females. These findings could be of interest for owners, breeders,
practicing veterinarians and insurance companies.
Keywords: Canine, Neurology, Epidemiology, Intervertebral disk disease, Referral centre, France
* Correspondence: vincent.mayousse@vet-alfort.fr
1
Université Paris-Est, Ecole Nationale Vétérinaire d’Alfort (EnvA), Unité de
Neurologie, 7 avenue du général de Gaulle, 94700 Maisons-Alfort, France
3
Inserm, IMRB U955-E10, 8 rue du général Sarrail, 94000 Créteil, France
Full list of author information is available at the end of the article
© The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Mayousse et al. BMC Veterinary Research (2017) 13:212
DOI 10.1186/s12917-017-1132-2
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Background
The French Bulldog (FB) is a canine breed originating
from France. The numbers of FBs have markedly
increased in recent decades. In Europe, FB has signifi-
cantly gained in popularity over the last few years. For
example, annual registrations of FBs have quadrupled
over the past 15 years in France [1], and in the United
Kingdom, 14,607 new registrations to the Kennel Club
were recorded in 2015 versus 526 in 2006 [2]. In North
America, FB was the 6th most popular breed in the
United States in 2014 [3], and the 9th most popular
breed in Canada in 2015 [4]. Due to the brachycephalic
and chondrodystrophic body conformation resulting
from selective inbreeding, a high prevalence of vari-
ous diseases has been described in this breed, includ-
ing several neurological conditions [5]. These include
not only myelopathies such as compressive vertebral
malformations [6], spinal arachnoid diverticula [7]
and intervertebral disc disease [8], but also encephal-
opathies such as brain tumours [9] or non-infectious
encephalitides [10]. To the authors’knowledge, no
study has yet reported the prevalences and distribu-
tions of different neurological disorders in FB or has
described a specific neurological condition in this
emerging breed. The primary objective of this
epidemiological study was therefore to report the
prevalences of different neurological conditions in a
large population of FBs presented for neurological
signs at a major referral centre. A secondary objective
was to identify epidemiological characteristics regar-
ding specific diseases in this singular breed.
Methods
Case selection
Case records of all French bulldogs presented for neuro-
logical signs (including spinal pain) at our institution
between January 1st, 2002 and January 1st, 2016 were
retrospectively reviewed. Dogs were included if they met
all the following inclusion criteria: (i) neurological clin-
ical signs, including isolated spinal pain, (ii) complete
available records and (iii) a definitive etiological diagno-
sis. The only exception was the inclusion of young dogs
presented for an auditory function screening, as several
animals were asymptomatic. Dogs that did not present
actual neurological clinical signs or signs mimicking a
neurological condition but related to another cause (e.g.
orthopaedic or ophthalmic conditions) were otherwise
excluded. Similarly, animals with only a neuroanatomical
diagnosis (e.g. “T2-L2 myelopathy”,or“cauda equina
syndrome”) were not included in the study.
Neurological diseases classification
When a dog was presented at our institution two times
or more for neurological conditions, only the first one
for which the dog was presented was taken into account.
Similarly, when two concomitant neurological diseases
were diagnosed at the same time on the same dog (i.e.
with one being an incidental finding), only the one re-
sponsible for the clinical signs was retained. To facilitate
data processing, each case was assigned to one of the
following neuroanatomical categories, according to the
definitive diagnosis: encephalopathy, myelopathy, per-
ipheral nervous system (PNS) & muscles disorder, and
unclassified neurological condition. Diseases unrelated
to one of the above-listed categories, such as paroxysmal
dyskinesia, tremors syndromes and congenital deafness
were grouped together under “unclassified neurological
conditions”.
Criteria used for the diagnosis of specific diseases
Definitive diagnoses for each patient were then estab-
lished by a board-certified neurologist based on patient’s
signalment and history, clinical findings and appropriate
ancillary tests, according to the current knowledge for
each condition. Ancillary tests comprised miscellaneous
blood testing (including biochemical analyses, serum bile
acids measurement, complete blood count, electrolytes,
hormonal testing, serology), cerebrospinal fluid (CSF)
analysis, PCR screening for various endemic infectious
agents of the nervous system, cytology and histology of
various tissues, otoscopy, bacterial culture on various
materials, muscles and nerves biopsies, myelography,
cross-sectional imaging (Computed tomography [CT]
and magnetic resonance imaging [MRI] scans), and elec-
trodiagnostics (electromyography, nerve conduction
studies and brainstem auditory evoked response
[BAER]). Two MRI devices were used during the study
period: a low-field (0.2 T) device prior to 2013, and a
high-field device (1.5 T) after 2013. Criteria allowing
diagnoses of diseases the most frequently expected are
listed in the following sections.
Brain diseases
When available, brain tumours were diagnosed based on
histological examination. In cases where a histological
examination was not performed, MRI criteria were used.
An intracranial glioma was defined as an intra-axial soli-
tary lesion, more or less enhancing after paramagnetic
intravenous contrast media administration, accompanied
or not by surrounding oedema and/or mass effect [11].
Similarly, pituitary neoplasia diagnosis was based upon
histological analysis and/or CT or MRI imaging features
(masses well-delineated in the pituitary area, more or
less invading the surrounding parenchyma with contrast
enhancement), along with consistent biochemical or
ultrasonographic abnormalities (hypercortisolism, bila-
teral adrenal enlargement etc. [12]). When the diagnosis
was achieved through imaging criteria, the term
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“suspected neoplasia”was therefore used to refer to
these diseases.
In cases of absent histopathological diagnosis, meningo-
encephalitis of unknown (MUO) origin was diagnosed
based on the following previously described criteria: Focal
or multifocal clinical signs of brain disease, T2-weighted
multifocal intra-axial hyperintense lesions with variable
T1-weighted contrast enhancement on MRI, mononucle-
ated pleocytosis on CSF analysis, and exclusion of
endemic infectious diseases [13]. Idiopathic epilepsy
diagnosis was based upon the International Veterinary
Epilepsy Task Force consensus, and included normal
inter-ictal examination, normal brain MRI and CSF ana-
lysis, as well as a normal comprehensive biochemistry pro-
file investigating metabolic causes of seizures, including
serum bile acid and electrolytes [14]. Criteria allowing
diagnosis of otogenic bacterial encephalitis included
consistent central nervous system (CNS) clinical sings,
middle/inner ear MRI and/or CT abnormalities, T1-
weighted meningeal and/or brain parenchyma enhance-
ment on MRI, inflammatory CSF (with or without bacter-
ial culture), and a positive response to antibiotic
treatment. The diagnosis of metabolic encephalopathies
was based on clinical signs suggestive of brain disease,
consistent MRI findings and an identified metabolic origin
on blood analysis (e.g. hepatic or renal failure) [15].
Myelopathies
Intervertebral disk herniation was diagnosed either by
CT, MRI or myelography associated with consistent
clinical signs and onset. The distinction between Hansen
type I and type II IVDH was based upon a combination
of clinical and imaging criteria and the perioperative ap-
pearance of herniated material in dogs that underwent
surgical treatment, as described in previous studies.
Hansen type I IVDH was suspected on CT if hyperdense
presumed disk material was observed in the interverte-
bral space and/or within the vertebral canal, along with
subsequent spinal cord compression on transverse
planes and/or epidural fat displacement [16]. It was sus-
pected on MRI if the disk had extruded through the an-
nulus fibrosus, and appeared as a compressive extradural
hypointense (either in T2 or T1-weighted) single lesion,
mostly lateralized and dispersed from either side of the
intervertebral space [17]. Hansen type I was suspected
during surgery if calcified/mineralized nucleus pulposus
was extruded in the vertebral canal and/or under the
dorsal longitudinal ligament [18].
Spinal arachnoid diverticulum (SAD) was defined on
myelography or CT-myelography as contrast-filled, tear-
drop shaped expansion of the subarachnoid space, with
a possible abrupt interruption of the contrast column
immediately after the lesion. On MRI, it was defined as
a T2-weighted hyperintense, T1-weighted and/or FLAIR
hypointense lesion of the subarachnoid space [19].
When histological examination was not performed,
usual previously described imaging criteria were used
to diagnose spinal tumours, especially regarding the
relationship between the lesion and the subarachnoid
space [20].
PNS & muscle disorders
Otitis interna was defined as the combination of clinical
signs suggestive of a peripheral vestibular syndrome,
evocative imaging findings either with CT (fluid-filled
tympanic bulla) or MRI (fluid-filled tympanic bulla and
loss of the normal T2-weighted hypersignal of the inner
ear), and evidence of inflammation/infection on bulla
cytology. Congenital deafness was defined as hearing loss
or deficits since birth, confirmed by a consistent BAER
study [21].
Data acquisition and statistical analysis
The clinical database of the institution was searched
using the clinical software (CLOVIS, 4Dv13) and appro-
priate keywords. When information was missing from
numerical records, the paper files were retrieved if avail-
able. For each case fulfilling the inclusion criteria, data
were recorded using a form created with EpiData v3.1
Software (Lauritsen J.M., Bruus M. & Myatt M., UK/
Denmark). Information regarding file number, age, sex,
body weight, duration of clinical signs, and definitive
diagnosis were collected. Complete data were then
exported into an Excel 2010 spreadsheet (Microsoft
Office 2010, Excel 2010) for further statistical evaluation.
Percentages for each subpopulation were calculated with
a 95% confidence interval, using the asymptotic/Wald
method (for groups in which n x p> 5, where n is the
number of individuals in the concerned subpopulation,
and p the estimate prevalence rate), or the exact bino-
mial/Clopper-Pearson method (for groups in which n x
p< 5, EpiTools, AusVet Animal Health Services). The χ
2
statistical test (or Fisher’s exact test when appropriate)
was used to assess the statistical association between age
(taken as a binary variable with appropriate cut-off ) or
sex, and the occurrence of IVDH or meningoencephalitis
of unknown origin. Odds Ratio (OR) were calculated to
quantify the association between sex and occurrence of
MUO, age and occurrence of IVDH, and were provided
with their 95% confidence interval (CI). A P-value < 0.05
was considered significant. Statistical tests were per-
formed using a website dedicated to statistical analysis
(BiostaTGV, http://marne.u707.jussieu.fr/biostatgv/). A
receiver operating characteristic (ROC) curve analysis
was performed to determine a cut-off value for the age
that best discriminated the presence (versus absence) of
meningoencephalitis of unknown origin. The optimum
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cut-off value was determined with Youden’s index
criteria. An appropriate statistical software was used for
the ROC analysis (SAS Software, version 9.3).
Results
Study population
Between 2002 and 2016, 2846 FBs were presented at
our institution (representing 3.1% of all dog breeds),
all chief complaints and all departments combined.
Over this period of time, FB was the sixth most
popular breed after standard poodle (4.1% of all dogs
breeds), German shepherd (4.2%), Labrador retriever
(6.2%), Yorkshire terrier (6.8%) and mixed-breed dogs
(10.1%). A total of 533 FBs (18.7% of the 2846 FBs)
were presented for suspected neurological signs.
During the same period, a total of 88,863 dogs (FB ex-
cluded) were presented at our institution, of which 10,150
(11.4%) were admitted for neurological clinical signs.
Among the 533 FBs presented for neurological clin-
ical signs, 25 were excluded because the clinical
examination failed to identify a neurological disorder.
A further 165 animals were excluded because of in-
complete files and/or absence of definitive diagnosis.
In the end, 343 FBs with a confirmed neurological
disease and a precise diagnosis were included in the
statistical analysis, representing 12% of all FBs pre-
sented to the institution during the study period. The
whole case selection procedure is detailed in Fig. 1.
Two concomitant neurological conditions were diag-
nosed in only 9 dogs at the time of presentation.
Overall distribution of neurological diseases
In total, 64.7% of the 343 dogs presented a myelopathy
(n= 222 dogs, 95% CI 59.7–69.8%), 19.8% presented an
encephalopathy (n= 68, 95% CI 15.6–24.0%), 9.3% pre-
sented an unclassified condition (n= 32, 95% CI 6.5–
12.9%) and 6.1% presented a PNS/muscle disorder
(n= 21, 95% CI 3.8–9.2%). The median age of the FBs in
this study was 4.0 years (range from 0.2 to 14.5 years).
There were 188 males (including 19 castrated dogs) and
155 females (including 64 spayed females). All the
results are detailed in Table 1.
Myelopathies distribution
Hansen type I intervertebral disk herniation was the
most common myelopathy, with 70.3% documented
cases (n= 156 dogs, 95% CI 64.3–76.3%). IVDH
accounted for 45.5% (95% CI 40.2–50.8%) of all the
neurological conditions, and for 5.5% of all FBs pre-
sented to our institution during the study period (95%
CI 4.6–6.3%). Five dogs presented two IVDH at the time
of presentation, representing a total of 161 sites of disk
herniation. Cervical IVDH accounted for 39.8% of all
IVDH (n= 64, 95% CI 32.2–47.3%), whereas thoracol-
umbar and lumbar locations represented 60.2% of IVDH
(n= 97, 95% CI 52.7–67.8%). There was no significant
association between sex and IVDH (p= 0.95). When
cervical and thoracic/lumbar IVDH were taken together,
most dogs (80.8%, 95% CI 74.6–87.0%) were more than
3 years old. Age was significantly associated with IVDH,
since 81% of FBs affected by IVDH were 3 years old or
533 eligible FB presented for
neurological clinical signs
508 FB presenting
actual neurological
clinical signs
343 FB with a
definitive diagnosis
165 FB excluded because
of incomplete file or lack
of definitive diagnosis
91 709 dogs presented to
the institution between
01/01/2002 and 01/01/2016
88 863 Non-FBs presented to
the institution during the
study period
10 150 Non-FBs presented
for neurological clinical
signs
11.4%
18.7%
2 846 FB presented to the
institution during the study
period
25 FB excluded because
of clinical signs due to
non-neurological
condition
Fig. 1 Data flow diagram illustrating the case selection procedure of the 343 French bulldogs (FB) selected from the general hospital population
between 2002 and 2016, and presenting neurological clinical signs and a definitive diagnosis
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more, compared to 64% of dogs affected by another
myelopathy (OR = 2.4, 95% CI 1.2–4.5, p< 0.01).
Spinal arachnoid diverticulum was the second most
common myelopathy, with 11.3% of dogs affected by this
condition (n=25,95%CI7.4–16.2%). SAD represented
7.3% of all diseases of the study (95% CI 4.5–10.0%). Com-
pressive vertebral malformation was diagnosed in 8.6% of
dogs with myelopathy (n=19,95%CI5.2–13.0%),
followed by a neoplastic condition (either spinal or verte-
bral neoplasia) in 3.2% of dogs (n= 7, 95% CI 1.3–6.4%),
syringomyelia in 2.7% of dogs (n= 6, 95% CI 1.0–5.8%),
and ischemic myelopathy in 1.8% of dogs (n=4,95%CI
0.05–4.5%). The remaining disorders of the spinal cord
were acute non-compressive nucleus pulposus extrusion
(n= 3), immune-mediated myelitis (n= 1), and lumbosa-
cral spinal cord dermoid sinus (n=1).
Cervical intervertebral disk herniation
The median age of dogs affected by cervical IVDH
was 4.2 years (range from 1.5 to 10 years), and the
median weight was 12.4 kg (range from 8 to 19 kg).
Cervical hyperesthesia, often pronounced, was
observed in 82.8% of dogs presenting cervical IVDH
(n= 53, 95% CI 73.5–92.0%). The most commonly af-
fected site in the cervical region was C3-C4 (57.8% of
cervical IVDH, n= 37, 95% CI 45.7–69.9%) followed
by C4-C5 (18.8%, n= 12, 95% CI 10.1–30.5%) and
C2-C3 (17.2%, n= 11, 95% CI 8.9–28.7%). An epi-
dural hematoma/haemorrhage was observed in 3 cases
that underwent cervical ventral slot surgery.
Thoracolumbar intervertebral disk herniation
Among these non-cervical IVDH (n= 97), 68 were lo-
cated in the thoracolumbar (T3-L3) region and 29 were
located in the lumbosacral (L4-S) region. The median
age of FBs affected by thoracic and lumbar IVDH was
4 years (range from 1.7 to 13 years). The median weight
was 12.4 (range from 4.5 to 18 kg). The most commonly
affected intervertebral spaces in this group of dog were
T13-L1 (20.6%, n= 20 95% CI 12.6–28.7%), followed by
L2-L3 (17.5%, n= 17, 95% CI 10.0–25.1%), L3-L4
(16.5%, n= 16, 95% CI 9.1–23.9%) and L1-L2 (14.5%,
n= 14, 95% CI 7.4–21.4%). Finally, T12-T13, L4-L5 and
other intervertebral locations regrouped 10 dogs each
(representing 10.3% of thoracolumbar IVDH each, 95%
CI 4.3–16.4%). An extradural haemorrhage and/or
hematoma was observed during cross-sectional imaging
and/or surgery in 27.8% (n= 27, 95% CI 18.9–36.8%) of
all cases diagnosed with thoracic or lumbar IVDH,
regardless of the affected disk location.
Spinal arachnoid diverticulum
Concerning SAD, 88.0% (n= 22, 95% CI 75.3–100%)
were located in the thoracolumbar (T3-L3) region. More
Table 1 Distibution of the different neurological diseases in the
343 FBs from the study, with a definitive diagnosis
Category/Diseases N= 343 (%)
Myelopathies 222/343 (64.7%)
IVDH 156/222 (70.3%),
representing 161 IV sites
Cervical IVDH 64/161 (39.8%)
C3-C4 37/64 (57.8%)
C4-C5 12/64 (18.8%)
C2-C3 11/64 (17.2%)
C5-C6 4/64 (6.2%)
Non-cervical IVDH 97/161 (60.2%)
T13-L1 20/97 (20.6%)
L2-L3 17/97 (17.5%)
L3-L4 16/97 (16.5%)
L1-L2 14/97 (14.5%)
T12-T13 10/97 (10.3%)
L4-L5 10/97 (10.3%)
Other locations 10/97 (10.3%)
Spinal arachnoid diverticulum 25/222 (11.3%)
Thoracic 22/25 (88%)
Cervical 3/25 (12%)
Compressive vertebral malformations 19/222 (8.6%)
Hemivertebra + kyphosis 17/19 (89.5%)
Other CVM 2/19 (10.5%)
Spinal neoplasia 7/222 (3.1%)
Syringohydromyelia 6/222 (2.7%)
Other myelopathies 9/222 (4%)
Encephalopathies 68/343 (19.8%)
Brain neoplasia 25/68 (36.8%)
Glioma 17/25 (68%)
Pituitary neoplasia 5/25 (20%)
Other neoplasias 3/25 (12%)
MUO/optic neuritis 17/68 (25%)
Idiopathic epilepsy 9/68 (13.2%)
Infectious encephalitis 8/68 (11.8%)
Metabolic 3/68 (4.4%)
Other encephalopathies 6/68 (8.8%)
Unclassified neurological conditions 32/343 (9.3%)
Congenital deafness 29/32 (90.6%)
Bilateral 21/29 (72.4%)
Unilateral 8/29 (27.6%)
Other unclassified conditions 3/32 (9.4%)
PNS/muscle disorders 21/343 (6.1%)
Otitis interna/PVS 14/21 (66.7%)
Myopathies 3/21 (14.3%)
Idiopathic vestibular syndrome 2/21 (9.5%)
Others PNS/muscle disorders 2/21 (9.5%)
FB French bulldog, IVDH intervertebral disk herniation, IV intervertebral, CVM
compressive vertebral malformation, MUO meningoencephalitis of unknown
origin, PNS peripheral nervous system, PVS peripheral vestibular syndrome
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than three quarters of the thoracolumbar SAD cases
were located between T9 and T12 (77.3%, n= 17, 95%
CI 59.8–94.8%). In the remaining 12.0% (n=3,95%CI
0.0–24.7%) of animals affected by this condition, a
cervical (C1-C5) location of the SAD was observed. No
SAD was found in the caudal cervical (C6-T2) or lumbo-
sacral (L4-S) segments. In addition, a vertebral malfor-
mation (n= 12) or a mild IVDH (n= 4), at the level or
distant from maximum 2 to 3 vertebral bodies to the
SAD, was identified in 64.0% (n= 16, 95% CI 45.2–
82.8%) of all cases. The median age of FBs affected by
SAD was 4.5 years (range from 1 to 10.7 years).
Compressive vertebral malformations
Concerning the 19 dogs clinically affected by congenital
vertebral malformations, 17 presented with hemiverteb-
rae (89.5%, 95% CI 75.7–100%) associated with a major
kyphosis responsible for a compression of the spinal
cord. The most commonly affected vertebrae were T6,
T7, T8, and T10 (with 3 abnormal vertebrae for each).
Five FB presented with two or more malformations. One
dog presented with a wedge-shaped vertebrae and one
dog presented with L6-L7 spina bifida.
Encephalopathies distribution
Brain neoplasia
A suspected brain neoplasia was observed in 36.8% of
FBs affected by an encephalopathy (n= 25, 95% CI
28.6–53.3%), with a glioma, either suspected or con-
firmed, being the most common (n= 17, 68% of all
neoplasias 95% CI 49.7–86.3%). Five FBs presented a
pituitary macroadenoma (n= 5, 20.0% of neoplasias
95% CI 6.8–40.7%). The three remaining animals were
affected by intracranial lymphoma, malignant intracra-
nial peripheral nerve sheath tumour of cranial nerve
III, or suspected osteosarcoma of the calvarium.
Three gliomas and 2 pituitary macroadenomas were
confirmed histologically (either with biopsies or post
mortem examinations). The median age of FBs with
brain neoplasia was 9.0 years old (range from 5 to
14.5 years).
Meningoencephalitis of unknown origin
Meningoencephalitis of unknown origin represented
25.0% of the encephalopathies (n= 17, 95% CI 15.3–
37.0%). The median age of FBs affected by MUO was
2.25 years (range from 0.8 to 6.5 years). Among the 68
(19.8%) FBs that presented an encephalopathy, MUO
was more frequently observed in females than in males
(OR = 7.1, 95% CI 2.0–25.2, p< 0.01). ROC curve ana-
lysis enabled us to determine that the cut-off age that
best discriminated the presence versus the absence of
MUO was 5.5 years, with a sensitivity of 60.7% and a
specificity of 94.1% (Area under the curve = 0.76).
Therefore, by using this cut-off, 94.1% of FBs less than
5.5 years old presented with clinical signs related to an
encephalopathy were affected by MUO, whereas 60.7%
of FBs of 5.5 years old or more presented with the same
clinical signs were not affected by this condition.
Other encephalopathies
Regarding other conditions, idiopathic epilepsy repre-
sented 13.2% of encephalopathies (n= 9, 95% CI 6.2–
23.6%), and bacterial encephalitis associated with otitis
media/interna 11.8% (n= 8, 95% CI 5.2–21.9%). The
remaining encephalopathies were metabolic encephalop-
athies (n= 3, two hepatic encephalopathies, and one
uraemic encephalopathy), congenital hydrocephalus
(n= 2), cannabinoid intoxications (n= 2), ischemic
stroke and degenerative encephalopathy (n= 1 for each
condition).
Other neurological conditions distribution
Among the unclassified neurological disorders (n= 32),
90.6% of FBs presented congenital deafness (n= 29, 95%
CI 80.5–100.0%). Bilateral deafness was detected in
72.4% (n= 21, 95% CI 56.1–88.7%) of animals presenting
congenital deafness, versus 27.6% for the unilateral form
of the condition. Among all FBs presented with congeni-
tal deafness, 79.3% were white or had white in their coat
(n= 23, 95% CI 64.6–94.1%). Idiopathic head tremors
were observed in 2 animals, and narcolepsy/cataplexy in
a single case.
Among PNS/muscles disorders (n= 21), 66.7% of
animals presented an otitis interna with neurological
signs (see below, n= 14, 95% CI 46.5–86.8%), 14.3%
presented a myopathy (n= 3, 95% CI 3.0–36.3%),
withonecaseofeachthefollowingconditions:
immune-mediated polymyositis, ischaemic neuromyo-
pathy and corticosteroids-induced myopathy. Two
animals presented an idiopathic acute vestibular
syndrome, one case presented a chronic steroid-
responsive polyneuropathy, and one case presented a
malignant peripheral nerve sheath tumour. Among
the FBs affected by otitis media/interna, all animals
were presented with a peripheral vestibular syndrome,
eight cases had concurrent ipsilateral facial paralysis,
and four cases had a concurrent Horner syndrome.
Discussion
This study revealed that 18.7% of FBs admitted in our
institution during the study period presented with
neurological clinical signs, 12% when only dogs with
definitive diagnosis are considered. Although the
hospital population of FBs in this study roughly re-
flects the general FB population (mostly in good
health), this percentage is probably overestimated as a
large majority of dog are presented to our institution
Mayousse et al. BMC Veterinary Research (2017) 13:212 Page 6 of 10
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

for health issues. However, the objective of the
current study was not to estimate the prevalence rate
of neurological disorders in the general FB popula-
tion, but rather among FBs presented to a veterinary
hospital.
This study showed that the FB breed is affected by
various neurological conditions, even if disorders of the
central nervous system (CNS) were clearly predominant
in this population. Hansen type I IVDH was by far the
most prevalent neurological disease of FBs in this study,
as it represented nearly half the overall conditions of the
whole nervous system (45.5%), and 5.5% of all FBs pre-
sented to our institution during the study period. In a
large American study evaluating inherited disorders in
pure-breed and mixed-breed dogs, FB was found to be
the second breed most frequently affected by IVDH after
the Dachshund [8].
An important finding is that nearly 40% of IVDH in
FBs from this study occurred in the cervical area. In
other breeds, several studies demonstrated a lower
percentage of cervical IVDH in comparison to
thoracic-lumbar IVDH, rather located around 20–
25%, especially in Dachshund [22–24].However,an
almost similar cervical versus thoracic-lumbar IVDH
repartition has been reported in Beagle or Cocker
Spaniel in a older study, even if the number of dogs
in these breeds was limited [24].
Regarding IVDH position, the C3-C4 intervertebral
space was the most frequently involved site, all locations
combined. This contrasts either with recent [25] or older
[26] findings indicating that C2-C3 was the most
commonly affected disk in chondrodystrophic dogs pre-
senting cervical IVDH, although only a small number of
FBs were mentioned in the most recent report (n= 5).
In the thoracolumbar area, T13-L1 was the most fre-
quently affected site, followed by L2-L3 and L1-L2 in FB
of our study. This is in partial agreement with previous
publications revealing that the most often affected site in
canine thoracolumbar IVDH was T12-T13, followed by
T13-L1 and T11-T12 intervertebral spaces [27–29].
Note that the majority of dogs which constituted the
populations in these previous studies were Miniature
Dachshunds and not FBs. Conversely, IVDH were dis-
tributed more equitably between T13 and L4 in the FB
reported here, which is consistent with a previous publi-
cation demonstrating that FB present thoracolumbar
IVDH more caudally than Dachshund [28].
The median age of the FBs affected by cervical and
thoracic-lumbar IVDH in the present study was 4.2
and 4.0 years respectively, which tends to be younger
than in other breeds for both locations. Regarding
Hansen type I thoracic-lumbar IVDH, this is indeed
in contrast with the largest case series in which the
estimated mean and median age is around 6 years
old, all breeds combined [27–30]. Nonetheless, a sin-
gle study comparing thoracolumbar Hansen type I
IVDH in FB and Dachshunds showed that FBs were
younger at the time of surgery [28], even if the num-
ber of FBs was limited in this report (n= 47). Simi-
larly, studies addressing cervical IVDH revealed a
median age ranging between 6 and 8 years old in
chondrodystrophic dogs [25, 26, 31]. One hypothesis
for this difference could be the fact that intervertebral
disk degeneration occurs faster in FB than in other
chondrodystrophic breeds. However, no study has yet
compared the disk degeneration kinetic between
chondrodystrophic breeds. Another recent study dem-
onstrated that congenital vertebral malformations,
common in FB, could promote intervertebral disk
degeneration in the adjacent intervertebral spaces in
chondrodystrophic breeds [32].
SAD was the second most frequent myelopathy and
was identified in 25 dogs from this study, constituting
the largest published population of FBs diagnosed with
this condition. SAD was preponderant in the middle to
caudal thoracic area in the FBs of this study. These
findings regarding SAD location are consistent with a
previous publication [7], the thoracic region being the
most frequently affected in small chondrodystrophic
breeds, such as Pug or FB. In addition, a potential
underlying cause such as vertebral malformation or mild
IVDH was identified in 64.0% of the cases of SAD in this
study. This observation is also in agreement with the
publication by Mauler and colleagues [7], which revealed
that 61.5% of the 13 FBs reported in this study presented
a concurrent spinal disorder. This could therefore pre-
dispose FB for acquired SAD in the thoracic area of the
spinal cord. Compressive thoracic vertebral malforma-
tions resulting in a myelopathy were found in nearly 9%
of FBs in this report, mainly represented by mid to cau-
dal thoracic hemivertebrae. The true prevalence of verte-
bral malformation is however higher in FB, as
asymptomatic dogs may present this abnormality [33],
while only symptomatic FBs were included in the
present study. A recent study showed indeed that verte-
bral malformations in neurologically normal FBs were
detected in 93.5% of cases, and were more frequently
observed than in other chondrodystrophic brachy-
cephalic dog [34].
Encephalopathies were the second most frequently
observed condition of the nervous system in this FBs
population. Brain neoplasia appeared to be the
primary cause of encephalopathy within this subpopu-
lation, with glial tumour (either suspected or histolog-
ically confirmed) being the most frequent. This
finding is in agreement with a past study, which re-
vealed that FB, among other brachycephalic dogs,
seems predisposed to gliomas [9]. Nevertheless, the
Mayousse et al. BMC Veterinary Research (2017) 13:212 Page 7 of 10
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

diagnosis of glioma was not definitive in all cases in
our study, as necropsy or biopsies were not per-
formed in all animals presented with a brain tumour.
In these cases, the diagnosis was based mainly on
MRI characteristics. Even if several studies provided
interesting MRI features giving indications for the dif-
ferentiation in the tumour nature or subtype, these
parameters remain to be improved, as they lack sensi-
tivity and specificity [35–37]. The second most fre-
quent encephalopathy was meningoencephalitis of
unknown origin, which was found to be more com-
mon in small young to middle-aged female dogs ac-
cording to a meta-analysis from 2010 [13]. In the
present study too, FBs less than five and a half years
old seemed more likely to be affected by MUO than
other causes of encephalopathies, although the sensi-
tivity for the selected cut-off value was not optimal.
Similarly, females in the present population of FBs
appeared to be more likely affected by this condition
than male dogs, which is consistent with previous
data [13].
Congenital deafness was the more frequently detected
unclassified neurological disease, as 90.6% of FBs in this
subpopulation were affected by this condition. Congeni-
tal deafness has been described in many canine breeds,
including FB [38], and has been associated with the pres-
ence of white colour in coat or blue eyes in various
breeds [38, 39]. Deaf FBs from our study were either
white or contained white in their coat in nearly 80% of
cases. The prevalence of bilateral deafness is usually
lower than unilateral deafness according to several con-
cordant studies [39–42]. Surprisingly, bilateral deafness
was diagnosed more frequently than unilateral deafness
in the FBs of this study, as 72.4% of the dogs were
bilaterally deaf. This observation needs to be validated
by other referral centres as several individuals were
presented for auditory function screening purpose.
Otitis media/interna associated with peripheral ves-
tibular syndrome was the most common disease in
dogs presented with PNS/muscles disorders. This is
in agreement with a previous study suggesting that
the primary cause of peripheral vestibular syndrome
in dog was otitis media/interna [43]. However, there
was no information regarding the predisposition of a
specific breed. To the authors’knowledge, no infor-
mation is available in the veterinary literature regard-
ing the potential predisposition of a particular canine
breed for otitis interna/vestibular neuritis. This
disease might eventually spread to the overlying brain
and/or meninges in some cases, thus resulting in
bacterial meningoencephalitis [44].
The study period was specifically chosen after 2002
in order to minimize the measurement bias regarding
conditions that required an MRI scan for accurate
diagnoses. This date corresponds in fact to the arrival
of a MRI device in our institution. However, a meas-
urement bias may still exist because MRI scans were
performed on a low-field device prior to 2013,
whereas a high-field device was used after 2013. This
may have affected the detection of certain disorders,
such as MUO, immune-mediated myelitis or idio-
pathic epilepsy, even if a study in people revealed
only subtle differences in the detection of brain le-
sions between low-field and high-field MRI devices
[45]. Indeed, mild brain anomalies may be missed
with a low-field MRI device, and a dog wrongly
classified has having idiopathic epilepsy for example.
Finally, the FBs population in this study may differ
from that encountered in other referral centres, as
the number of insured dogs is probably higher in UK
and North America than in France. This may have
hadadirectinfluenceoncaseselectionsinceitcould
have decreased the number of detailed clinical cases
with a definitive diagnosis, and thus the prevalence
rates of certain diseases.
Conclusion
This is the first study addressing neurological condi-
tions as a whole in a large cohort of FBs, and this
further confirms the general impression of many vet-
erinarians regarding the overall distribution of these
disorders. Hansen type I IVDH appeared to be by
far the most frequent neurological disease in middle-
aged FBs, representing 5.5% of all FBs presented
during the study period. FB tends to be more fre-
quently affected by cervical IVDH than other breeds,
and at a younger age. The topographical distribution
indicates a greater tendency for involvement of the
C3-C4 intervertebral disk.
SAD was the second most commonly diagnosed
myelopathy, with an associated spinal abnormality in
nearly two thirds of the cases. Suspected brain
tumours and MUO were the most frequent encephal-
opathies, the latter preferentially affecting young to
middle-aged female patients. Otitis interna with per-
ipheral vestibular signs and bilateral congenital deaf-
ness associated with white coat, were also frequently
observed, apart from CNS conditions. The high
prevalence of various neurological diseases identified
in this study might be explained by the specific body
conformation of FB. This hypothesis needs however
to be verified through comparative studies with other
breeds, further multicentric studies in European and
North American referral centres, and largest represen-
tative populations. Findings of the present study could
be of interest for FBs owners and breeders, practicing
veterinarians and pets insurance companies.
Mayousse et al. BMC Veterinary Research (2017) 13:212 Page 8 of 10
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Abbreviations
BAER: Brainstem auditory evoked response; CNS: Central nervous system;
CSF: Cerebrospinal fluid; CT: Computed tomography; FB: French Bulldog;
FLAIR: Fluid attenuated inversion recovery; IVDH: Intervertebral disk
herniation; MRI: Magnetic resonance imaging; MUO: Meningoencephalitis of
unknown origin; PNS: Peripheral nervous system; SAD: Spinal arachnoid
diverticulum
Acknowledgments
The authors want to thank TVM Laboratories.
Funding
The Neurology Unit is partially supported by TVM Laboratories. However,
TVM Laboratories did not directly fund this study.
Availability of data and materials
The datasets used and/or analysed during the current study are available
from the corresponding author on reasonable request.
Authors’contributions
VM, AJ and SB conceived the study. VM collected all data and write the
manuscript. LD designed and participated in the statistical analysis. AJ and
SB participated in the revision of the manuscript. All authors read and
approved the final manuscript.
Ethics approval and consent to participate
The retrospective analysis is exempt from ethics approval from the
institutional animal care and use committee.
Consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
Publisher’sNote
Springer Nature remains neutral with regard to jurisdictional claims in
published maps and institutional affiliations.
Author details
1
Université Paris-Est, Ecole Nationale Vétérinaire d’Alfort (EnvA), Unité de
Neurologie, 7 avenue du général de Gaulle, 94700 Maisons-Alfort, France.
2
Université Paris-Est, Ecole Nationale Vétérinaire d’Alfort (EnvA), Unité de
Biostatistiques et d’Epidémiologie Clinique, 7 avenue du général de Gaulle,
94700 Maisons-Alfort, France.
3
Inserm, IMRB U955-E10, 8 rue du général
Sarrail, 94000 Créteil, France.
4
Present adress: Davies Veterinary Specialists,
Manor Farm Buisiness Park, Higham Gobion, Herts SG5 3HR, United Kingdom.
5
UMR BNMS Neurobiologie, Ecole Nationale Veterinaire d’Alfort, 7 avenue du
General de Gaulle, 94700, Maisons Alfort, France.
Received: 26 January 2017 Accepted: 26 June 2017
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