You are on page 1of 9

Vet Dermatol 2018 DOI: 10.1111/vde.

12708

Comparison of demographic data, disease severity and


response to treatment, between dogs with atopic
dermatitis and atopic-like dermatitis: a retrospective
study
Larissa S. Botoni* , Sheila M. F. Torres†, Sandra N. Koch† , Marcos B. Heinemann‡ and
Adriane P. Costa-Val*
*Department of Veterinary Clinical Sciences and Surgery, Universidade Federal de Minas Gerais, 6627 Anto^nio Carlos Ave, Belo Horizonte, 31270-
901, Brazil
†Department of Veterinary Clinical Sciences, University of Minnesota, 1365 Gortner Avenue, Saint Paul, MN 55108, USA
‡Department of Preventive Veterinary Medicine and Animal Health, Universidade de S~ ao Paulo, 87 Prof. Dr. Orlando Marques de Paiva Ave, S~ao
Paulo, 05508-270, Brazil
Correspondence: Sheila M. F. Torres, Department of Veterinary Clinical Sciences, University of Minnesota, 1365 Gortner Avenue, Saint Paul, MN
55108, USA. E-mail: torre009@umn.edu

Background – Limited information is available describing the features of canine atopic-like dermatitis (ALD) com-
pared with atopic dermatitis (AD).
Objectives – To compare demographic data, disease severity and response to therapy between ALD and AD
dogs.
Animals – Two hundred and fifty-three atopic dogs with intradermal and serum allergen-specific IgE test results
were selected retrospectively.
Methods and materials – Dogs were enrolled into the ALD group if both IgE tests were negative and into the
AD group if at least one test was positive. Demographic data, pruritus level and number of body sites affected
before and during therapy, in addition to maintenance therapy protocols, were compared between groups.
Results – There were 216 (85.38%) dogs in the AD group and 37 (14.62%) in the ALD group. The soft-coated
wheaten terrier, American Staffordshire terrier, English bulldog and Labrador retriever were over-represented in
the AD group. No significant differences between the groups were noted regarding the other demographic vari-
ables evaluated. There were no differences in the mean pruritus scores and number of affected body sites at the
first visit or during treatment. Furthermore, no significant differences between the groups were noted for the
maintenance treatment scores and reduction of pruritus level and number of body sites affected during treat-
ment.
Conclusions and clinical significance – The soft-coated wheaten terrier, American Staffordshire terrier, Eng-
lish bulldog and Labrador retriever were over-represented in the AD group. No significant differences in the other
demographic data and clinical features were noted between dogs with ALD and AD in the present study.

common environmental and food allergens, in the serum


Introduction
and skin prick test.1–4 The extrinsic type of AD (EAD) or
In humans, atopic dermatitis (AD) has been traditionally allergic atopic eczema/AD is characterized by high serum
classified into two subtypes according to the level of total IgE levels and positive allergen-specific IgE to com-
serum total IgE and the presence of specific IgE against mon environmental and food allergens.1,2 It has been
environmental and food allergens. The intrinsic type (IAD), hypothesized that IAD and EAD are different stages of
also named nonallergic AD, nonatopic eczema, atopiform AD. The condition in infancy may begin as nonallergic
dermatitis or nonallergic atopic eczema/dermatitis syn- (IAD) and progress to atopy (EAD) overtime.5–7 This
drome,1 is characterized by low or normal serum total IgE hypothesis has been supported by two studies that
levels and negative allergen-specific IgE reactions to reported allergen sensitization with positive allergen-spe-
cific IgE in a number of patients initially diagnosed as
IAD.1,8
Accepted 10 September 2018 Canine atopic-like dermatitis (ALD) has been defined as
This study was presented at the North American Veterinary Der- an inflammatory and pruritic skin disease with clinical fea-
matology Forum, 2018, Maui, Hawaii. Vet Dermatol 2018; 29: tures identical to those seen in canine AD, in which an
274 (Abstract). IgE response to environmental or other allergens cannot
Source of funding: This study was self-funded. be documented.9,10 Because total serum IgE levels have
Conflict of interests: No conflicts of interest have been a poor correlation with the atopic status in dogs,11–13 this
declared.

© 2018 ESVD and ACVD, Veterinary Dermatology 1


Botoni et al.

parameter cannot be used to distinguish AD and ALD in Study population


dogs. Thus, in dogs, the differentiation has been made on Dogs were placed into the AD or ALD group based on their IDT and
the basis of the results of intradermal (IDT) and serum AST results. The dogs that did not show any positive reactions on
both the IDT and AST were classified as ALD. The ones that showed
allergen-specific IgE tests (AST).
one or more positive reactions on one or both tests were placed in
To the best of the authors’ knowledge, there is only
the AD group. To be considered positive on the IDT, any reaction had
one study, published as an abstract, contrasting the clini- to have a 2+ or higher score, and be associated with erythema and
cal and epidemiological features of canine AD versus skin turgidity.9 To be considered positive on the AST, the reaction
ALD.14 Several other studies15–17 have investigated dif- had to be ≥80 EAU (ELISA absorbance units) as reported by IDEXX
ferent aspects of ALD; however, the diagnosis was made Laboratories.
based on either IDT or serum test, not strictly both. The
primary aim of this retrospective study was to compare, Statistical analyses
in a population of dogs diagnosed with AD or ALD using All dogs were included in the demographic data analysis. However,
both the IDT and AST tests, the following: (i) demographic for all other analyses, only dogs with at least four follow-up visits
data; (ii) disease severity measured by pruritus level, were included because this was considered to be a reasonable mini-
number of body sites affected and treatment and (iii) mal number of visits necessary to determine the maintenance treat-
ment regimen and evaluate response to therapy. Means and
response to therapy measured by reduction in pruritus
standard deviations were used to report the time period to achieve
level and number of body sites affected during treatment. four follow-up visits, the maximum duration of the follow-up period
The secondary aim was to summarize the demographic and the number of follow-up visits.
data of all dogs included in the study. Descriptive statistics was used to characterize the demographic
variables in each group in addition to the groups combined.
Means were compared between the AD and ALD groups using
Methods and materials the chi-square test or Fisher’s exact test for the qualitative data
and the Wilcoxon–Mann–Whitney U-test for the quantitative data.
Medical record search and data collection
To determine whether there was breed predisposition to develop
Medical records of dogs seen in a veterinary teaching hospital
AD or ALD, breed frequency was compared between each group
from 2007 to 2015 were searched using the keywords as fol-
and the general canine hospital population seen during the study
lows: atopic dermatitis, atopy, allergy, dog and canine. Inclusion
period, using Fisher’s exact test.
criteria for eligible dogs were (i) diagnosis of AD; (ii) IDT and AST
In order to assess differences in disease severity, the mean pruri-
test results available, and (iii) IDT and AST tests performed on
tus level and number of body sites affected at the first visit were
the same day. Exclusion criteria were (i) dogs with nonseasonal
compared between the AD and ALD groups using the Wilcoxon–
clinical signs of AD with no records of an elimination diet trial
Mann–Whitney U-test. In order to standardize the information avail-
performed; and (ii) dogs assigned to the ALD group that had a
able in the medical records, the dog’s body surface was divided as
positive response to a food trial (because this could represent an
follows: face, ears, neck, thorax, dorsum, flanks, abdomen, axillae,
IgE-mediated allergic response). Data collected from each dog
groins, front legs, hind legs, front paws, hind paws, perineum and
included sex, breed, age of disease onset, seasonality, presence
tail. Each of these body sites was counted as one affected area, total-
of respiratory signs, presence of conjunctivitis, performance of
ling 16 sites. The pruritus level recorded in the medical records was
food trial, food trial response, percentage of time spent indoors,
based on a 0–10 scoring system using owner’s verbal assessment
body regions affected, pruritus level and treatment. A standard
(before 2009) or the pruritus Visual Analog Scale (pVAS) as reported
history questionnaire was part of the electronic medical record
previously (after 2009).19
(UVISâ, Universal Veterinary Information System, Ross Group
The dog’s pruritus level at the first visit also was evaluated by cat-
Inc.; Miamisbur, OH, USA); therefore, the listed information was
egorizing the scores in severity levels according to the recommenda-
documented consistently for all cases.
tions of the International Committee on Allergic Diseases of Animals
(ICADA) as follows: mild: 2.0–3.5; moderate: 3.6–5.5 and severe:
Intradermal and serum allergen-specific IgE test 5.6–10).20 The frequency of each severity score was compared
protocols between the groups using Fisher’s exact test. Additionally, to indi-
The IDT test was performed by clipping the dog’s lateral thorax and rectly assess disease severity, the maintenance treatment modalities
injecting in the dermis 0.1 mL of 60 environmental allergens (Staller- were scored and compared between the AD and ALD groups using
genes Greerâ; Lenoir, NC, USA). The reactions were evaluated Fisher’s exact test. The following empirical treatment scoring system
15 min after the injections and subjectively graded 0 to 4+ based on was developed and used in the analysis: 1 (antihistamines and/or
the negative (saline) and positive (1:100,000 histamine) controls. The essential fatty acids and/or allergen-specific immunotherapy); 2 [one
dogs were sedated for the test using dexmedetomidine hydrochlo- immunomodulatory agent (i.e. oral glucocorticoid, ciclosporin, oclac-
ride (Orion Corp.; Espoo, Finland) intravenously at the dose of itinib or lokivetmab) with or without one or more of the medications
0.004 mg/kg. Drug withdrawal time prior to IDT was as follows: two included in score 1] and 3 (two or more immunomodulatory drugs,
weeks for antihistamines, essential fatty acids and topical products with or without one or more of the medications included in score 1).
containing glucocorticoids, four weeks for oral glucocorticoids, ciclos- We considered maintenance treatment to be the most frequently
porin and oclacitinib and, six to eight weeks for injectable glucocorti- used protocol that controlled the disease and this was determined as
coids. the average treatment scores during four or more follow-up visits.
Approximately 3 mL of blood was collected for the AST and placed In order to assess differences in response to therapy, the
in serum separator glass tubes. The serum was separated by centrifu- mean pruritus scores and mean number of body sites affected
gation and stored refrigerated under 2–4°C until submission to the lab- during treatment were compared between the ALD and AD
oratory within 12 h of collection. The AST was performed by IDEXX groups using the Wilcoxon–Mann–Whitney U-test. The pruritus
reference laboratories (IDEXX Laboratories, Inc.; Westbrook, MA, scores were then categorized in severity levels as described
USA) using the Greer Aller-g-completeâ kit (Stallergenes Greerâ). A above, and the frequency of each severity score was compared
monoclonal antibody cocktail-based ELISA was used for the detection between the groups using Fisher’s exact test. Because there
of serum allergen-specific IgE, as described previously.18 were no significant differences between the groups in the num-
The allergen panel used in the IDT and AST included household ber of dogs in each of the maintenance treatment scores, the
allergens, moulds and pollens of trees, grasses and weeds (Tables analysis was not blocked by treatment scores. The reduction of
S1 & S2, respectively). pruritus scores and number of lesions overtime also were

2 © 2018 ESVD and ACVD, Veterinary Dermatology


Canine atopic dermatitis and atopic-like dermatitis

compared between the groups to measure differences in therapy >80% of the time indoors (ALD: 87.0%; AD: 83.5%;
responses using a marginal linear regression model. P = 0.385).
All statistical analyses were performed using the software R
A strict food elimination diet trial followed by challenge
v.3.2.4 (R Core Team. R: A Language and Environment for Statis-
tical Computing. http://www.R-project.org; R Foundation for Statis-
was performed in 222 of 253 dogs (87.7%), and a partial
tical Computing, Vienna, Austria, 2014). A P-value ≤0.05 was positive response was observed in 25 of 253 dogs
considered significant. (11.3%), all from the AD group. The 31 dogs that did not
have a food trial performed (26 AD and 5 ALD) had strictly
seasonal clinical signs (Table 1).
Results There were 34 of 216 (13.4%) dogs with positive serol-
Demographic data ogy and negative intradermal test results in the AD group.
A total of 2,691 cases were initially retrieved, and 253 When all study dogs were compared to the general
were considered eligible for the study based on the inclu- hospital population seen during 2007 and 2015, the soft-
sion and exclusion criteria. Two hundred and sixteen coated wheaten terrier (P < 0.000; OR = 5.8), American
(85.38%) dogs were included in the AD group and 37 Staffordshire terrier (P < 0.000; OR = 4.76), English bull-
(14.62%) in the ALD group. There were no significant dif- dog (P = 0.005; OR = 3.49) and the Labrador retriever
ferences between the groups in the demographic vari- (P = 0.037; OR = 1.40) were predisposed to developing
ables presented in Table 1. The proportion of males AD. Breeds over-represented in the AD group also
(51.4%; 51.4%) and females (48.6%; 48.6%), respec- included the soft-coated wheaten terrier (P < 0.001;
tively, in the ALD and AD groups was identical OR = 5.8), American Staffordshire terrier (P < 0.000;
(P = 0.997). There were no significant differences in the OR = 5.61), English bulldog (P = 0.002; OR = 4.11) and
age of disease onset (ALD: 16.2 months; AD: the Labrador retriever (P = 0.024; OR = 1.46). There
20.9 months; P = 0.232). The respiratory signs recorded were no over-represented breeds in the ALD group when
in the medical records were sneezing, coughing and run- compared to the general hospital population seen during
ning nose. The most common respiratory sign in the ALD the study period.
and AD groups was sneezing. The proportion of dogs For the analyses of disease severity and response to
with respiratory signs was low in both groups (ALD: therapy, 171 dogs with records of at least four follow-
24.3%; AD: 19.0%; P = 0.317), as was the frequency of up visits were included. The mean time period to
dogs with conjunctivitis (ALD: 21.6%; AD: 18.1%; achieve four follow-up visits was 5.1 months (SD: 1.7;
P = 0.648). Clinical signs of AD were predominantly year- range: 2–11), and the maximum duration of the follow-
round in the ALD and AD groups (70.3%; 60.2%; up period was eight years (mean: 3.0 years; SD:
P = 0.244) and the dogs in each group spent on average 1.9 years; range: four months to eight years). The

Table 1. Comparison of epidemiological variables between the atopic-like dermatitis (ALD) and atopic dermatitis (AD) groups
All dogs ALD AD

Variables N % N % N % OR CI - 95% P-value*


Sex
Female 123 48.6 18 48.6 105 48.6 1.00 - 0.997†
Male 130 51.4 19 51.4 111 51.4 1.00 [0.5;2.01]
Respiratory signs
None 203 80.2 28 75.7 175 81 1.00 - 0.317‡
Sneezes 43 17 7 18.9 36 16.7 0.72 [0.33; 1.91]
Cough 5 1.9 1 2.7 4 1.9 0.32 [0.07; 3.22]
Nose discharge 2 0.7 1 2.7 1 0.5 0.08 [0.02; 1.62]
Conjunctivitis
No 206 81.4 29 78.4 177 81.9 1.00 - 0.648†
Yes 47 18.6 8 21.6 39 18.1 0.64 [0.33; 1.78]
Seasonality
Seasonal 97 38.3 11 29.7 86 39.8 1.00 - 0.244†
Year-round 156 61.6 26 70.3 130 60.2 0.64 [0.3; 1.36]
Food trial
No 31 12.2 5 13.5 26 12 1.00 - 0.788†
Yes 222 87.7 32 86.5 190 88 1.07 [0.45; 3.28]
Partial response to food trial
No 197 88.7 32 100 165 86.9 1.00 - 1.000‡
Yes 25 11.3 0 0 25 13.1 0.99 [0.36; 3.88]
Age at onset in month – mean (SD) 20.2 (17.4) 16.2 (11.6) 20.9 (18.2) 0.98 [0.95; 1.01] 0.232§
% Indoors – mean (SD) 84.2 (15.5) 87 (9.8) 83.5 (16.3) 0.15 [0.01; 2.84] 0.385§
*P < 0.05 was considered significant.
†chi-square test.
‡Fisher’s exact test.
§Wilcoxon–Mann–Whitney U-test.
C.I. confidence interval, OR odds ratio, SD standard deviation.
N = 269 (all selected dogs were included).

© 2018 ESVD and ACVD, Veterinary Dermatology 3


Botoni et al.

Figure 1. Box plot showing the pruritus scores of the dogs with atopic dermatitis (AD) and atopic-like dermatitis (ALD) at the first visit.
The box represents the interquartile range (i.e. 25th to 75th percentile range). The dark horizontal line represents the median. For each box, the T-
bars represent the main body of data. The open circles represent outliers. (b) Frequency of dogs in each categorized pruritus score at the first visit.
Pruritus scores grouped into mild, moderate and severe. N = 171.

mean number of follow-up visits was 6.7 (SD: 2.39;


range four to 18).

Comparison of disease severity between the AD and


ALD groups
The pruritus scores and number of affected body sites of
dogs at the first visit and the maintenance therapy proto-
cols across visits were used as parameters to assess dis-
ease severity in the groups. There was no significant
difference (Wilcoxon–Mann–Whitney U-test, P = 0.433)
in the mean pruritus score of dogs in the AD (6.5  2.1;
range: 0–10) and ALD (6.87  1.86; range: 2–9) groups
(Figure 1a). When pruritus scores were categorized in
severity levels, most dogs in the AD (70.4%) and ALD
(81.2%) groups had severe pruritus. There were no signif-
icant differences between the groups (Fisher’s exact test;
P = 0.908) in the frequencies of cases classified as hav- Figure 2. Box plot showing the number of body sites affected in
ing mild, moderate or severe pruritus levels (Figure 1b). dogs with atopic dermatitis (AD) and atopic-like dermatitis (ALD) at
There was no significant difference (Wilcoxon–Mann– the first visit.
Whitney U-test; P = 0.474) in the mean number of The box represents the interquartile range (i.e. 25th to 75th per-
affected body sites between the AD (3.8  1.8; range: 0– centile range). The dark horizontal line represents the median. For
each box, the T-bars represent the main body of data. The open cir-
11) and the ALD (3.7  2.6; range = 0–8) groups (Fig-
cles represent outliers. N = 171.
ure 2).
No significant differences (Fisher’s exact test;
P = 0.796) in the frequencies of dogs receiving each in severity levels, most dogs in the AD (51.6%) and
of the categorized maintenance treatment modality ALD (68.8%) had moderate pruritus. There were no
was noted between the AD and ALD groups (Fig- significant differences between the groups (Fisher’s
ure 3). exact test; P = 0.528) in the frequencies of cases clas-
sified as having mild, moderate or severe pruritus
Comparison of response to therapy between the AD levels (Figure 4b).
and ALD groups There was no significant difference (Wilcoxon–Mann–
The pruritus scores and number of affected body sites Whitney U-test; P = 0.093) in the mean number of
of the dogs taken across at least four revisits (i.e. dur- affected body sites between the AD (3.0  1.2; range:
ing treatment) were used as parameters to assess 0.4–8.5) and the ALD (3.0  1.4; range = 1–5.8) groups
response to therapy between the groups. There was during treatment (Figure 5).
no significant difference (Wilcoxon–Mann–Whitney U- No significant difference was noted between the
test; P = 0.949) in the mean pruritus score of the dogs groups in the reduction of pruritus level (marginal linear
in the AD (4.7  1.4; range: 1.1–10) and ALD regression model; P = 0.061) or number of body sites
(4.7  1.9; range = 2.8–7.1) groups during treatment affected (marginal linear regression model; P = 0.365)
(Figure 4a). When the pruritus scores were categorized during treatment.

4 © 2018 ESVD and ACVD, Veterinary Dermatology


Canine atopic dermatitis and atopic-like dermatitis

however, this difference was not statistically significant.


A previous study reports the mean age of onset to be
identical in both groups.14 In contrast, human patients
with IAD are known to have a later disease onset com-
pared to EAD, even though IAD remains more common in
children than adults.1,3,8,24
In humans, IAD is typically not associated with other
atopic diseases, such as asthma, rhino-conjunctivitis and
contact dermatitis.1,2,6,24 No differences were found
between the groups regarding the presence of respiratory
signs and conjunctivitis, which were infrequent in our
canine patients. Conjunctivitis was observed in 18.6% of
all enrolled dogs and similar results have been reported
elsewhere.26 In another study, the frequency of allergic
conjunctivitis in atopic dogs was 60%, suggesting that
conjunctivitis could in fact be underdiagnosed in this dis-
Figure 3. Frequency of dogs in each treatment score.
Scores: 1 (antihistamines and/or essential fatty acids and/or allergen-
ease.27
specific immunotherapy), 2 [one immunomodulatory agent (i.e. oral Studies evaluating breed predisposition to AD show
glucocorticoid, ciclosporin, oclacitinib, or lokivetmab) with or without marked regional variations,28–34 yet the Labrador retrie-
one or more of the medications included in score 1] and, 3 (two or ver has been frequently reported in various studies
more immunomodulatory agents, with or without one or more of the from different locations,28,32–34 so our results are in
medications included in score 1). AD, atopic dermatitis; ALD, atopic- accordance with previous studies. The other over-
like dermatitis. N = 171.
represented breeds in our study were the soft-coated
wheaten terrier, English bulldog and American
Staffordshire terrier. In one study performed in Aus-
tralia, the English bulldog and American Staffordshire
Discussion
terrier also were shown to be at increased risk for
In the present study, ALD comprised 14.62% of the developing AD;33 in a worldwide multicentre study,
enrolled population. This incidence is lower than a previ- bulldogs (English and French combined) were over-
ous report of 25.6% for dogs;14 by comparison, the represented.35 In addition, one study from Switzerland
reported incidence is 10–45% in humans with IAD.2,21–24 reported an over-representation of soft-coated whea-
Moreover, in contrast to humans where females appear ten terriers and American Staffordshire terriers.34 Not
to be at increased risk for developing both, IAD and surprisingly, the breeds over-represented in the AD
EAD,1,3,23–25 neither our study nor a previous study14 group were the same ones observed in the whole
found a significant difference in sex distribution within study population because this group accounted for
the groups. We observed an earlier mean age of onset in 85.38% of the cases. The French bulldog was over-
ALD dogs compared to AD (16.2 versus 20.9 months); represented in an ALD cohort investigated

Figure 4. (a) Box plot showing the mean pruritus scores of dogs with and atopic dermatitis (AD) and atopic-like dermatitis (ALD) during four or
more follow-up visits.
The box represents the interquartile range (i.e. 25th to 75th percentile range). The dark horizontal line represents the median. For each box, the
T-bars represent the main body of data. The open circles represent outliers. (b) Frequency of dogs in each categorized pruritus score during four or
more follow-up visits. The pruritus scores were categorized as follows: mild: 2.0–3.5; moderate: 3.6–5.5 and severe: 5.6–10. N = 171.

© 2018 ESVD and ACVD, Veterinary Dermatology 5


Botoni et al.

to ciclosporin compared to ALD dogs (92% and 50%,


respectively).14
Finally, in humans, IAD has been shown to be a
dynamic disease where individuals could develop aller-
gen-specific antibody at a latter disease phase.5–8,36 The
ALD patients included in the study were not retested,
thus we do not know if this phenomenon occurs in dogs
and it will be interesting to investigate this further.
This study has some limitations inherent to its retro-
spective nature, including the inability to assess and
compare lesion severity and disease phenotype
between the groups due to the lack of standardization
in the lesion description portion of the medical records.
Moreover, the small number of dogs in the ALD could
have impacted the results. Furthermore, it could be
contended that ideally all of the dogs in the AD group
Figure 5. Box plot showing the mean number of body sites affected
should have had positive tests to both IDT and AST,
for dogs with atopic dermatitis (AD) and atopic-like dermatitis (ALD)
and that this may have provided a more precise com-
after four or more follow-up visits.
The box represents the interquartile range (i.e. 25th to 75th percentile parison of the groups. Likewise, it could be contended
range). The dark horizontal line represents the median. For each box, that comparison of the two groups in which no cases
the T-bars represent the main body of data. The open circles represent showed a partial response to food trials (as in the AD
outliers. N = 171. group), may have given a more precise assessment of
AD versus ALD.
In summary, in the present study, the soft-coated
previously.14 The present study did not find any over-
wheaten terrier, American Staffordshire terrier, English
represented breeds in the ALD group, again indicating
bulldog and Labrador retriever were over-represented
regional differences.
in the AD group. No significant differences in age of
Human patients with IAD have been reported to have
disease onset, sex, presence of respiratory and ocular
significantly lower SCORAD scores, which measures the
signs, percentage of time spent indoors, disease
severity of skin lesions, compared to EAD.1,8 Moreover,
severity and response to therapy were observed
in a study, IAD patients used tacrolimus, emollients and
between AD and ALD subtypes. The lack of differ-
antihistamines significantly less frequently and reported a
ences could suggest that there are no real differences
better quality of life than EAD patients, suggesting less
between the proposed subtypes and, that in fact, they
severe disease in this subtype.1 In the present study, we
are part of the same dynamic disease. However,
used number of body sites affected and pruritus scores at
future prospective studies including a larger cohort of
the first visit and maintenance treatment scores as surro-
dogs with AD, and especially with ALD, are needed to
gates of disease severity. No significant differences in
support our findings. In addition, such studies should
any of these variables were found between the groups.
evaluate carefully any differences in disease pheno-
Likewise, a previous study did not find any significant dif-
type, barrier integrity and immunological responses
ferences in clinical scores between the ALD and AD
between the subtypes which could help tailor therapy
groups, but no specific information on the scores used
more effectively.
was provided.14 These results suggest that, in contrast to
humans, disease severity is similar in dogs with AD and
ALD. However, prospective studies including larger num- References
bers of dogs, especially with ALD, are needed to corrobo-
1. Brenninkmeijer EEA, Spuls PI, Legierse CM et al. Clinical differ-
rate this hypothesis.
ences between atopic and atopiform dermatitis. J Am Acad Der-
In humans, IAD patients seem to present more fre- matol 2008; 58: 407–414.
quently with Dennie–Morgan infraorbital folds, orbital 2. Kulthanan K, Boochangkool K, Tuchinda P et al. Clinical features
darkening, cheilitis and anterior neck folds than EAD of the extrinsic and intrinsic types of adult-onset atopic dermati-
patients.1,2,6 Because of the retrospective nature of the tis. Asia Pac Allergy 2011; 1: 80–86.
study, we were not able to evaluate if certain disease fea- 3. Karimkhani C, Silverberg JI, Dellavalle RP. Defining intrinsic vs.
extrinsic atopic dermatitis. Dermatol Online J 2015; 21: pii:
tures occur more frequently in one group than the other,
13030/qt14p8p404
nevertheless, this should be evaluated in prospective 4. Mori T, Ishida K, Mukumoto Y et al. Comparison of skin barrier
studies. function and sensory nerve electric current perception threshold
Pruritus scores and body sites affected also were eval- between IgE-high extrinsic and IgE-normal intrinsic types of ato-
uated following treatment as indirect indicators of pic dermatitis. Br J Dermatol 2010; 162: 83–90.
response to therapy. No significant differences between 5. Roguedas-Contios AM, Misery L. What is intrinsic atopic der-
the groups were noted in mean pruritus scores and num- matitis? Clin Rev Allergy Immunol 2011; 41: 233–236.
6. Roz_ alski M, Rudnicka L, Samochocki Z. Atopic and non-atopic
ber of body sites affected or reduction of pruritus and
eczema. Acta Dermatovenerol Croat 2016; 24: 110–115.
affected areas during treatment. A previous study did not 7. Ton ci
c RJ, Marinovic B. The role of impaired epidermal barrier
observe any difference in response to glucocorticoids but function in atopic dermatitis. Acta Dermatovenerol Croat 2016;
noted that significantly more AD dogs had good response 24: 95–109.

6 © 2018 ESVD and ACVD, Veterinary Dermatology


Canine atopic dermatitis and atopic-like dermatitis

8. Folster-Holst R, Pape M, Buss YL et al. Low prevalence of the 23. Ponyai G, Hidve gi B, Nemeth I et al. Contact and aeroallergens
intrinsic form of atopic dermatitis among adult patients. Allergy in adulthood atopic dermatitis. J Eur Acad Dermatol Venerol
2006; 61: 629–632. 2008; 22: 1,346–1,355.
9. Hensel P, Santoro D, Favrot C. Canine atopic dermatitis: detailed 24. Schmid P, Simon D, Simon H. Epidemiology, clinical features,
guidelines for diagnosis and allergen identification. BMC Vet Res and immunology of the “intrinsic” (non-IgE-mediated) type of
2015; 11: 196. atopic dermatitis (constitutional dermatitis). Allergy 2001; 56:
10. Pucheu-Haston CM, Bizikova P, Eisenschenk MNC et al. 841–849.
Review: The role of antibodies, autoantigens and food aller- 25. Yamaguchi H, Hirasawa N, Asakawa S et al. Intrinsic atopic der-
gens in canine atopic dermatitis. Vet Dermatol 2015; 26: matitis shows high serum nickel concentration. Allergol Int
115–e30. 2015; 64: 282–284.
11. Roque JB, O’Leary CA, Kyaw-Tanner M et al. High allergen-spe- 26. Wilhem S, Kovalik M, Favrot C. Breed-associated phenotypes in
cific serum immunoglobulin E levels in nonatopic West Highland canine atopic dermatitis. Vet Dermatol 2011; 22: 143–149.
white terriers. Vet Dermatol 2011; 22: 257–266. 27. Lourencßo-Martins AM, Delgado E, Neto I et al. Allergic conjunc-
12. Lauber B, Molitor V, Meury S et al. Total IgE and allergen-speci- tivitis and conjunctival provocation tests in atopic dogs. Vet
fic IgE and IgG antibody levels in sera of atopic dermatitis Ophthalmol 2011; 14: 248–256.
affected and non-affected Labrador- and Golden retrievers. Vet 28. Zur G, White SD, Ihrke PJ et al. Canine atopic dermatitis : a ret-
Immunol Immunopathol 2012; 149: 112–118. rospective study of 266 cases examined at the University of Cali-
13. Zwickl LLMN, Joekel DE, Fischer NM et al. Total and Toxocara fornia, Davis, 1992 – 1998. Part I. Clinical features and allergy
canis larval excretory/secretory antigen- and allergen-specific testing results.. Vet Dermatol 2002; 13: 89–102.
IgE in atopic and non-atopic dogs. Vet Dermatol 2018; 29: 222– 29. Tarpataki N, Papa K, Reiczigel J et al. Prevalence and features of
e80. canine atopic dermatitis in Hungary. Acta Vet Hung 2006; 54:
14. Prelaud N, Cochet-Faivre N. A retrospective study of 21 353–366.
cases of canine atopic-like dermatitis. Vet Dermatol 2007; 18: 30. Picco F, Zini E, Nett C et al. A prospective study on canine atopic
385. (Abstract) dermatitis and food-induced allergic dermatitis in Switzerland.
15. Suto A, Suto Y, Onohara N et al. Food allergens inducing a lym- Vet Dermatol 2008; 19: 150–155.
phocyte-mediated immunological reaction in canine atopic-like 31. Jaeger K, Linek M, Power HT et al. Breed and site predispo-
dermatitis. J Vet Med Sci 2015; 77: 251–254. sitions of dogs with atopic dermatitis: a comparison of five
16. Fujimura M, Nakatsuji Y, Ishimaru H. Cyclosporin A treatment in locations in three continents. Vet Dermatol 2010; 21: 118–
intrinsic canine atopic dermatitis (atopic-like dermatitis): open 122.
trial study. Pol J Vet Sci 2016; 19: 567–572. 32. Bruet V, Bourdeau PJ, Roussel A et al. Characterization of pruri-
17. Kawano K, Oumi K, Ashida Y et al. The prevalence of dogs tus in canine atopic dermatitis, flea bite hypersensitivity and flea
with lymphocyte proliferative responses to food allergens in infestation and its role in diagnosis. Vet Dermatol 2014; 23: 487–
canine allergic dermatitis. Pol J Vet Sci 2013; 16: 735– e93.
739. 33. Mazrier H, Vogelnest LJ, Thomson PC et al. Canine atopic der-
18. Lee KW, Blankenship KD, McCurry ZM et al. Performance char- matitis: breed risk in Australia and evidence for a susceptible
acteristics of a monoclonal antibody cocktail-based ELISA for clade. Vet Dermatol 2016; 27: 167–e42.
detection of allergen-specific IgE in dogs and comparison with a 34. Nødtvedt A, Egenvall A, Bergval K et al. Incidence of and risk
high affinity IgE receptor-based ELISA. Vet Dermatol 2009; 20: factors for atopic dermatitis in a Swedish population of insured
157–164. dogs. Vet Rec 2006; 159: 241–246.
19. Rybnıcek J, Lau-Gillard PJ, Harvey R et al. Further validation of a 35. Favrot C, Steffan J, Seewald W et al. A prospective study on the
pruritus severity scale for use in dogs. Vet Dermatol 2009; 20: clinical features of chronic canine atopic dermatitis and its diag-
115–122. nosis. Vet Dermatol 2010; 21: 23–31.
20. Olivry T, Bensignor E, Favrot C et al. Development of a core 36. Novembre E, Cianferoni A, Lombardi E et al. Natural history of
outcome set for therapeutic clinical trials enrolling dogs with “intrinsic” atopic dermatitis. Allergy 2001; 56: 452–453.
atopic dermatitis (COSCAD’18). BMC Vet Res 2018; 14:
238.
21. Ott H, Stanzel S, Ocklenburg C et al. Total serum IgE as a Supporting Information
parameter to differentiate between intrinsic and extrinsic ato-
pic dermatitis in children. Acta Derm Venerol 2009; 89: 257–
Additional Supporting Information may be found in the
261. online version of this article.
22. Ott H, Wilke J, Baron JM et al. Soluble immune receptor serum Table S1. Panel of allergens used in the intradermal test.
levels are associated with age, but not with clinical phenotype or Table S2. Panel of allergens used for allergen-specific
disease severity in childhood atopic dermatitis. J Eur Acad Der- serum IgE test.
matol Venerol 2010; 24: 395–402.

Re sume 
Contexte – Peu de donne es est disponible pour la description des caracte ristiques de la dermatite atopie-
like (ALD) compare  a la dermatite atopique (AD).
Objectifs – Comparer les donne es demographiques, la se  ve
rite
 de l’atteinte et la re
ponse au traitement
entre les chiens ALD et AD.
Sujets – Deux cent cinquante trois chiens atopiques avec des tests IgE spe cifiques d’allerge
nes seriques
ou intradermiques ont e  te
 se
lectionne
 s re
trospectivement.
Mate riel et methode – Les chiens ont e  te
 inclus dans le groupe ALD avec les deux tests ne gatifs et dans
le groupe AD si au moins un des tests e tait positif. Les donnees de mographiques, le niveau de prurit et le
nombre de sites corporels atteints avant et au cours du traitement, en plus des protocoles de traitement
de maintenance, ont e  te
 compare s entre les groupes.
Re sultats – Il y avait 216 (85.38%) chiens dans le groupe AD et 37 (14.62%) dans le groupe ALD. Dans le
groupe AD les races surrepre sentees e
taient : soft-coated wheaten terrier, American Staffordshire terrier,

© 2018 ESVD and ACVD, Veterinary Dermatology 7


Botoni et al.

English bulldog et Labrador retriever. Il n’y avait aucune diffe rence significative entre les groupes concer-
mographiques e
nant les autres variables de valuees. Il n’y avait pas de diffe
rence dans les scores moyens
de prurit et le nombre de sites corporels atteints  a la premiere visite ou au cours du traitement. En outre,
aucune difference entre les groupes n’a e te
 note
e pour les scores de traitement de maintenance et la dimi-
nution du niveau de prurit et le nombre de sites atteints au cours du traitement.
Conclusions et importance clinque – Les races soft-coated wheaten terrier, American Staffordshire ter-
rier, English bulldog et Labrador retriever etaient surrepre sentees dans le groupe AD. Aucune diffe rence
significative des donnees demographiques et des crite res cliniques n’a e
 te
 observe
e entre le chiens ALD
et AD dans cette e tude.

Resumen
Introduccio  n – se dispone de informacio n escasa describiendo las caracterısticas de la dermatitis similar a
pica canino (ALD) en comparacio
la dermatitis ato n con la dermatitis ato
pica propiamente dicha (AD).
Objetivos – comparar los datos demograficos, la gravedad de la enfermedad y la respuesta al tratamiento
entre perros con ALD y AD.
Animales – se seleccionaron retrospectivamente doscientos cincuenta y tres perros ato picos con resulta-
dos positivos especıficos de alergeno de pruebas intrade rmicos y de IgE se rica.
Me todos y materiales – los perros fueron incluidos en el grupo ALD si ambas pruebas de IgE fueron nega-
tivas y en el grupo AD si al menos una prueba fue positiva. Los datos demogr aficos, el nivel de prurito y la
cantidad de sitios corporales afectados antes y durante la terapia, adem as de los protocolos de terapia de
mantenimiento, se compararon entre los grupos.
Resultados – hubo 216 (85,38%) perros en el grupo de AD y 37 (14,62%) en el grupo de ALD. Las razas
Soft Coated Wheaten Terrier, American Staffordshire Terrier, English Bulldog y Labrador Retriever estaban
sobrerrepresentadas en el grupo AD. No se observaron diferencias significativas entre los grupos con res-
pecto a las otras variables demograficas evaluadas. No hubo diferencias en los valroes medios de prurito y
en el numero de sitios corporales afectados en la primera visita o durante el tratamiento. Adem as, no se
observaron diferencias significativas entre los grupos para los valores de tratamiento de mantenimiento y
la reduccion del nivel de prurito y la cantidad de sitios corporales afectados durante el tratamiento.
Conclusiones y significacio  n clınica – las razas Soft Coated Wheaten Terrier, American Staffordshire Ter-
rier, English Bulldog y Labrador Retriever estaban sobrerrepresentadas en el grupo de AD. No se observa-
ron diferencias significativas en los otros datos demogr aficos y caracterısticas clınicas entre los perros con
ALD y AD en el presente estudio.

Zusammenfassung
Hintergrund – Es gibt nur wenig Information u €ber die charakteristischen Merkmale von Atopie-€ ahnlicher
Dermatitis (ALD) beim Hund im Vergleich zur atopischen Dermatitis (AD).
Ziele – Ein Vergleich von ALD und AD bei Hunden in Bezug auf die demografischen Daten, die Schwere
der Erkrankung und die Reaktion auf eine Therapie.
Tiere – Zweihundertdreiundfu €nfzig atopische Hunde mit einem Intradermaltest Ergebnis und einem Aller-
gen-spezifischen IgE Serologietest Ergebnis wurden retrospektiv ausgew€ ahlt.
Methoden und Materialien – Die Hunde wurden der ALD Gruppe zugeteilt wenn beide IgE Tests negativ
waren und in die AD Gruppe wenn mindestens ein Test positiv war. Die demografischen Daten, das Juck-
reizlevel und die Anzahl der betroffenen Ko€rperstellen vor und w€ahrend der Therapie, sowie die Protokolle
der Erhaltungstherapie wurden zwischen den beiden Gruppen verglichen.
Ergebnisse – Es waren 216 (85,38%) Hunde in der AD Gruppe und 37 (14,62%) in der ALD Gruppe. Der
Soft-Coated Wheaten Terrier, der American Staffordshire Terrier, die Englische Bulldogge und der Labrador
Retriever waren in der AD Gruppe u €berrepr€asentiert. Es bestanden keine signifikanten Unterschiede zwis-
chen den Gruppen in Bezug auf die anderen untersuchten demografischen Variablen. Es gab keine Unter-
schiede zwischen den durchschnittlichen Juckreizwerten und der Anzahl der betroffenen Ko €rperstellen
beim Erstbesuch oder w€ahrend der Behandlung. Weiters gab es keine signifikanten Unterschiede zwis-
chen den Gruppen in Bezug auf die Werte der Erhaltungstherapie und der Reduktion der Juckreizlevels
und der Anzahl der betroffenen Ko €rperstellen w€
ahrend der Behandlung.
Schlussfolgerungen und klinische Bedeutung – Der Soft-Coated Wheaten Terrier, der American
Staffordshire Terrier, die Englische Bulldogge und der Labrador Retriever waren in der AD Gruppe u €ber-
repr€asentiert. Bei den anderen demografischen Daten und den klinischen Merkmalen gab es zwischen den
Hunden mit ALD und AD in der vorliegenden Studie keine signifikanten Unterschiede.

要約
背景 – アトピー性皮膚炎(AD)と比較して犬アトピー様皮膚炎(ALD)の特徴を記述した情報は限られてい
る。
目的 – 本研究の目的は、ALD及びAD犬間の人口統計学的データ、疾患の重症度および治療反応を比較す
ることである。
8 © 2018 ESVD and ACVD, Veterinary Dermatology
Canine atopic dermatitis and atopic-like dermatitis

被験動物 – 皮内および血清アレルゲン特異的IgE試験結果を有するアトピー性皮膚炎の犬253頭を遡及的
に選択した。
方法および材料 – 両検査が陰性であればALD群に、少なくとも1つの検査が陽性であればAD群に登録し
た。維持療法プロトコールに加えて、人口統計学的データ、掻痒レベルおよび治療前および治療中に罹
患部位数を群間比較した。
結果 – AD群の犬が216頭(85.38%)、ALD群の犬が37頭(14.62%)であった。ソフトコーテッド・ウィート
ン・テリア、アメリカン・スタッフォードシャー・テリア、イングリッシュ・ブルドッグ、ラブラドー
ル・レトリーバーは、AD群において過剰発現していた。評価した他の人口統計学的変数に関して、グル
ープ間の有意差を認めなかった。最初の訪問時または治療中の平均掻痒スコアおよび罹患部位数に差は
なかった。さらに、維持療法スコアおよび掻痒レベルの減少および治療中の罹患部位数に関して、群間
に有意差を認めなかった。
結論と臨床的意義 – ソフトコーテッド・ウィートン・テリア、アメリカン・スタッフォードシャー・テ
リア、イングリッシュ・ブルドッグ、ラブラドール・レトリーバーは、AD群において過剰発現してい
た。本研究では、他の人口統計学的データおよび臨床的特徴においてALDおよびAD犬間に有意差を認め
なかった。

摘要
背景 – 相比于异位性皮炎(AD),对犬异位样皮炎(ALD)特征信息的描述信息有限。
目的 – 比较ALD和AD患犬的数量统计学数据、疾病严重程度和对治疗的反应。
动物 – 回顾性分析253只异位性犬的皮内和血清过敏原特异性IgE检测结果。
方法和材料 – 如果两项IgE检测均为阴性,则将犬归入ALD组;如果至少一项检测为阳性,则将其归入AD组。
除了维持治疗方案之外,在两组之间比较数量统计学数据、瘙痒水平和治疗之前和期间身体发病部位的数
量。
结果 – AD组有216只犬(85.38%),ALD组有37只犬(14.62%)。在AD组中,大多是软毛小麦梗、美国斯塔福德
郡梗、英国斗牛犬和拉布拉多猎犬。两组的其它统计学变量方面评估,无显著差异。首次就诊或治疗期间,平
均瘙痒评分和发病部位的数目没有差异。此外,两组之间在维持治疗评分、瘙痒水平减少和治疗期间发病的
身体部位数量等方面无显著差异。
结论和临床意义 – AD组中,软毛小麦梗、美国斯塔福德郡梗、英国斗牛犬和拉布拉多猎犬的比例较高。本
研究中,ALD和AD患犬在其它统计资料和临床特征方面无显著差异。

Resumo
Contexto – Poucos dados foram publicados na literatura descrevendo as caracterısticas da dermatite
atopica-like (DAL) em c~aes e comparadas a dermatite ato pica canina (DA).
Objetivos – Comparar os dados demogr aficos, a gravidade da doencßa e a resposta ao tratamento entre
c~aes com DAL e DA.
Animais – Foram selecionados retrospectivamente duzentos e cinquenta e tre ^ s c~ picos que foram
aes ato
   
submetidos a ambos os testes de IgE alergeno-especıficas, intradermico e sorologico, e apresentavam os
resultados disponıveis.
Me todos e materiais – Os c~aes que apresentaram ambos os testes de IgE negativos foram alocados no
grupo DAL e os que apresentaram ao menos um dos testes positivo foram alocados no grupo DA. Os
dados demograficos, grau de prurido e nu mero de  areas corpo reas afetadas antes e durante o tratamento,
bem como os protocolos de tratamento de manutencß~ ao, foram comparados entre os grupos.
Resultados – Duzentos e dezesseis c~aes (85,38%) foram alocados no grupo DA e 37 (14,62%) no grupo
DAL. As racßas soft-coated wheaten terrier, American Staffordshire terrier, Labrador retriever e buldogue
^s estavam super-representadas no grupo DA. N~
ingle ao foram observadas diferencßas significativas entre os
grupos em relacß~ao a outras variaveis demogr aficas avaliadas. N~ao houve diferencßas significativas no grau
de prurido e no nu mero de areas corpo reas afetadas me dios na primeira consulta ou durante o tratamento.
Alem disso, n~ao foram observadas diferencßas significativas entre os grupos nos escores de tratamento de
manutencß~ao e na reducß~ao do grau de prurido e do nu mero de  areas corpo reas afetadas durante o trata-
mento.
Concluso ~ es e significa
^ncia clınica – As racßas soft-coated wheaten terrier, American Staffordshire terrier,
buldogue ingle ^s e Labrador retriever estavam super-representadas no grupo DA. N~ ao foram observadas
diferencßas significativas em outras variaveis demogr aficas ou caracterısticas clınicas entre os c~
aes com
DAL e DA no presente estudo.

© 2018 ESVD and ACVD, Veterinary Dermatology 9

You might also like