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Feature
Feature Veterinary
Record
125 years
SMALL ANIMAL DERMATOLOGY
Feature
Feature
An outside-in dermatitis?
Skin barrier function
It is now thought that altered skin barrier
function plays an important role in the
FIG 2: (a) Histopathology of non-lesional atopic
pathogenesis of canine atopic dermatitis
skin. This skin is not normal; there is mild epidermal
(Marsella and others 2011). Regular bathing, spongiosis with a sparse superficial perivascular
which may disrupt the skin barrier, is a risk infiltrate of lymphocytes and other monocytes. This
factor for atopic dermatitis (Picco and others shows why regular ongoing treatment of affected
2008), and tape-stripping of Maltese-beagle dogs is important even if they look clinically healthy.
atopic dogs enhanced Dermatophagoides (b) Histopathology of lesional atopic skin, with
farinae allergen-specific responses compared severe epidermal spongiosis, acanthosis and hyperkeratosis, and infiltration of lymphocytes, monocytes,
eosinophils, neutrophils, mast cells and plasma cells. This dog needs specific anti-inflammatory
to non-treated controls (Olivry and others treatment to resolve the inflammation; simple emollients or allergen-specific immunotherapy will not be
2011). Furthermore, transepidermal water effective in these cases. Haematoxylin and eosin. x 400
loss is higher in atopic beagles than in
healthy controls (Marsella and Samuelson
2009, Hightower and others 2010). Other spongiosis, acanthosis and hyperkeratosis, 1999a, Hayashiya and others 2002, Maeda
studies have shown changes in the stratum and infiltration of CD4+ and CD8+ T and others 2002, 2004, 2005, Nuttall and
corneum, the epidermal lipid layer, and cells, monocytes, eosinophils, neutrophils, others 2002, Pucheu-Haston and others
in ceramide profiles in atopic compared mast cells and plasma cells (Fig 2b). The 2006, 2008). However, it was subsequently
to healthy dogs (Piekutowska and others key role of the mast cell was recognised demonstrated that there is a TH1-dominant
2008, Reiter and others 2009, Shimada and early. Allergen exposure triggers the release pattern, which mediates cell mediated
others 2009, Marsella and others 2010, Popa of preformed and stored mediators that inflammation, in chronic lesions (Olivry
and others 2011). Altered filaggrin (which initiate immediate phase inflammatory and others 1999a, Nuttall and others
is essential for skin barrier function and responses and late phase reactions. Mast 2002, 2004, Maeda and others 2005,
is strongly associated with human atopic cells concentrate in the pinnae, ventral 2008, Pucheu-Haston and others 2006,
dermatitis) expression and loss-of-function and interdigital skin (Auxilia and Hill 2008). Rather than reflecting a TH2/TH1
mutations have also been associated with 2000), which are all predilection sites for imbalance, canine atopic dermatitis appears
canine atopic dermatitis (Marsella and atopic dermatitis. Mast cells express the to show a progression from early humoral
others 2009, Chervet and others 2010). high affinity IgE receptor FceRI, which TH2-type inflammation to chronic TH1-
However, there are again breed differences; enables stable binding of IgE in the skin and type cell mediated inflammation. This may
for example, filaggrin gene mutations have increases the sensitivity of allergen-mediated be associated with a failure of regulation,
been associated with atopic dermatitis in activation (Zeman and others 2002). IgE as studies have demonstrated altered T
British labrador retrievers (Wood and others binding to FceRI on epidermal Langerhans’ regulatory (Treg) cell and immunoregulatory
2010, Salzmann and others 2011, Roque cells also increases the efficiency of allergen cytokine function (particularly transforming
and others 2012) and Thai small breed dogs presentation. The presence of FceRI allows growth factor-b1 and interleukin [IL]-10)
(Suriyaphol and others 2011) but not in West atopic dogs to become sensitised and react to in canine atopic dermatitis (Hayashiya
Highland white terriers (Wood and others trace amounts of allergen. and others 2002, Nuttall and others 2002,
2010, Salzmann and others 2011, Roque and Advances in molecular biology have Maeda and others 2007). Furthermore,
others 2012). Recent studies have shown allowed more recent studies to look successful allergen-specific immunotherapy
that some of the changes to the epidermal beyond the cells
lipid layer can be reversed using oral n3 and and investigate the TABLE 1: Suspected environmental factors that may be associated
n6 essential fatty acids and a topical skin cytokine milieu with the development of canine atopic dermatitis (Nodtvedt and
lipid complex (Popa and others 2011, 2012), in canine atopic others 2007a, b, Picco and others 2008, Meury and others 2011,
suggesting that improving the skin barrier is dermatitis. This has van Beeck and others 2011)
important in treatment. greatly increased our Risk of developing atopic dermatitis Environmental factor
understanding of
Increased Urban life
What’s happening in the skin? the disease, and led
High human population density
Cell, cytokine and chemokine to new approaches
Increased average annual rainfall
profiles to treatment. Adoption at the age of 8 to 12 weeks
Early studies were limited to phenotyping Initially, canine Regular bathing of young healthy dogs
cellular infiltration and histopathological atopic dermatitis Reduced Rural life
changes in atopic skin. Non-lesional atopic was assumed to Living with other animals
skin is characterised by mild epidermal be a T helper 2 Walking in forests
spongiosis with sparse superficial (TH2)-associated Feeding non-commercial foods to lactating bitches
perivascular infiltrates of lymphocytes, disease, as TH2 No effect Sex
monocytes, dendritic cells and mast cells responses mediate Season of birth
Home environment
(Fig 2a) (Olivry and others 1997, 1999b, IgE production and
Vaccination
Marsella and others 2006b). In lesional allergic reactions
De-worming
skin, there is progressive epidermal (Olivry and others
Feature
Feature
Box 3: Evidence-based medicine Box 4: Key recommendations from the 2010 ICADA Guidelines for the Treatment
recommendations for the treatment of Atopic Dermatitis (Olivry and others 2010a)
of canine atopic dermatitis (Olivry
and Mueller 2003, Olivry and others Treatment of acute flares of atopic dermatitis
2010b, Olivry and Bizikova 2013) n Avoidance of flare factors:
❒ Regular flea control
High quality evidence ❒ Evaluation of the role of food allergens
n Oral glucocorticoids ❒ Identification and avoidance of environmental factors (eg, temperature, humidity,
n Oral ciclosporin irritants and allergens)
Moderate quality evidence n Identification and treatment of secondary staphylococcal and Malassezia infections
n Subcutaneous allergen-specific n Bathing with emollient and anti-pruritic shampoos (eg, Allermyl; Virbac Animal
immunotherapy Health)
n Topical hydrocortisone aceponate n Topical glucocorticoids (eg, hydrocortisone aceponate or triamcinolone)
n Topical triamcinolone n Oral glucocorticoids
n Topical tacrolimus Treatment of chronic atopic dermatitis
n Oral essential fatty acids (as a steroid n Avoidance of flare factors:
sparing agent) ❒ Regular flea control
n Oral Chinese herbal therapy (as a ❒ Evaluation of the role of food allergens
steroid sparing agent) ❒ Identification and avoidance of environmental factors (eg, temperature, humidity,
n Oral pentoxifylline irritants and allergens)
n Oral misoprostol n Identification and treatment of secondary staphylococcal and Malassezia infections
Low quality evidence n Bathing with emollient and anti-pruritic shampoos
n Injectable interferon omega n Dietary supplementation with essential fatty acids or feeding essential fatty acid
n Budesonide leave-on conditioner enriched diets
n Topical ciclosporin nano-emulsion n Topical glucocorticoids (eg, hydrocortisone aceponate or triamcinolone)
n Oral fexofenadine n Topical tacrolimus
n Oral mastinib n Oral glucocorticoids
n Essential fatty acid containing diets n Oral ciclosporin
n Topical hydrocortisone aceponate n Allergen-specific immunotherapy:
(as intermittent therapy on two days/ ❒ To prevent future flares associated with allergen exposure, ie, to induce tolerance
week) to environmental allergens
been consistent (van Damme and others needed to make evidence-based clinical environmental allergens. Food trials should
2009, Fazakerley and others 2010, Santoro decisions. The results from these analyses be part of the investigation in all cases,
and others 2011, 2012, Leonard and others were recently summarised in the 2010 and avoidance of food allergens may be
2012, Mullin and others 2013). The role ICADA Guidelines for the Treatment of important in some dogs.
of antimicrobial peptides in canine atopic Canine Atopic Dermatitis (Box 4) (an open- n Canine atopic dermatitis is associated
dermatitis is therefore still unclear and access article and freely available in a number with characteristic historical features and
requires further study. of different languages). clinical signs, but these are not absolutely
Microorganisms and microbial extracts Groups have also been working to specific and other pruritic dermatoses must
are strongly proinflammatory, attracting improve the quality of clinical trials and be eliminated to confirm the diagnosis.
and activating inflammatory cells and facilitate comparison between studies. For n Canine atopic dermatitis is more than an
driving chronic cell-mediated immunity. example, it is now expected that clinical allergic disease. Canine atopic dermatitis is
Interestingly, recent research has shown that trials will report validated clinical lesion and a complex multifactorial disease involving
atopic dogs develop specific IgE antibodies pruritus scores (Hill and others 2007, Olivry flare factors, a poor skin barrier, allergic
to Malassezia and staphylococci (Morris and and others 2007). More recently, a quality sensitisation and cutaneous inflammation;
others 1998, 2002, Nuttall and Halliwell of life score has been validated (Favrot and all of these factors should be addressed for
2001, Morris and DeBoer 2003, Bexley and others 2010a). This represents a major successful long-term treatment.
others 2013). The clinical significance of advance in assessing clinical trials, as quality n Canine atopic dermatitis is a variable
this is uncertain, but if microorganisms act of life is probably the most important disease. There is breed and individual
as allergens, then specific immunotherapy outcome measure for affected dogs and their variation in clinical signs and response to
could be used to ameliorate their impact. owners (Linek and Favrot 2010). treatment; every dog should be treated as an
individual, and no one treatment is likely to
Evidence-based medicine in Relevance to veterinary practice be successful in all cases.
canine atopic dermatitis We can only provide a short overview of n Canine atopic dermatitis is a lifelong
Dermatology was one of the first veterinary the huge advances that have been made in disease. The best results are associated with
disciplines to embrace evidence-based understanding the pathogenesis, diagnosis consistent ongoing treatment that keeps the
medicine. ITFCAD and later ICADA groups and treatment of canine atopic dermatitis. clinical signs in remission.
reviewed the literature to identify clinical trials However, there are a number of key findings n Canine atopic dermatitis has a
for therapeutic interventions in canine atopic that are directly relevant to clinical practice: complex and dynamic pattern of cytokine
dermatitis. These were evaluated for quality expression involving TH2, TH1 and
and efficacy to produce recommendations n Canine atopic dermatitis is a genetically immunoregulatory cytokines. Atopic skin
for treatment (Box 3). Clinicians in first- mediated disease. Owners should be advised exhibits chronic relapsing inflammation,
opinion practice will rarely have the time to about the consequences of breeding from which is best managed with consistent
individually analyse clinical trials, and these affected dogs. proactive treatment, whether or not the skin
meta-analyses are an ideal way to access the n Canine allergic dermatitis may be looks normal, rather than reactively treating
high-quality data and recommendations associated with reactions to food as well as flares of inflammation.
Feature
n Allergen-specific immunotherapy is MCEWAN, N. A. (2009) Staphylococcal colonization K., KURATA, K., MASUDA, K., OHNO, K. &
of mucosal and lesional skin sites in atopic and healthy TSUJIMOTO, H. (2002) Lesional expression of thymus
safe and effective. Allergen testing and dogs. Veterinary Dermatology 20, 179-184 and activation-regulated chemokine in canine atopic
immunotherapy should be considered in all GONZALES, A. J., HUMPHREY, W. R., MESSAMORE, dermatitis. Veterinary Immunology and Immunopathology 88,
cases. J. E., FLECK, T. J., FICI, G. J., SHELLY, J. A. & 79-87
n Atopic skin is readily colonised by OTHERS (2013) Interleukin-31: its role in canine pru- MAEDA, S., OHMORI, K., YASUDA, N., KURATA,
ritus and naturally occurring canine atopic dermatitis. K., SAKAGUCHI, M., MASUDA, K., OHNO, K. &
staphylococci and Malassezia. Secondary Veterinary Dermatology 24, 48-e12 TSUJIMOTO, H. (2004) Increase of CC chemokine
infections should promptly identified and HALLIWELL, R. (1973) The localization of IgE in canine receptor 4-positive cells in the peripheral CD4+ cells
treated. skin: an immunofluorescent study. Journal of Immunology in dogs with atopic dermatitis or experimentally sen-
110, 422-430 sitized to Japanese cedar pollen. Clinical and Experimental
n Use evidence-based medicine for clinical
HALLIWELL, R. E. W. (2006) Revised nomencla- Allergy 34, 1467-1473
decision-making. Meta-analyses have ture for veterinary allergy. Veterinary Immunology and MAEDA, S., TSUCHIDA, H. & MARSELLA, R. (2007)
identified the most effective therapeutic Immunopathology 114, 207-208 Allergen challenge decreases mRNA expression of regu-
interventions, and these have been brought HALLIWELL, R., SCHWARTZMAN, R. & ROCKEY, latory cytokines in whole blood of high-IgE beagles.
J. (1972) Antigenic relationship between canine and Veterinary Dermatology 18, 422-426
together in clinical guidelines. human IgE. Clinical and Experimental Immunology 10, MAEDA, S., TSUCHIDA, H., SHIBATA, S.,
399-407 KAWAKAMI, T., TSUKUI, T., OHBA, Y., FUKATA,
Conclusion HALLIWELL, R., SCHWARTZMAN, R. M. & T. & KITAGAWA, H. (2008) Expression analysis of
There have been great changes in our MONTGOMERY, P. (1975) Physicochemical properties CCL27 and CCL28 mRNA in lesional and non-lesional
of canine IgE. Transplant Proceedings 7, 537-543 skin of dogs with atopic dermatitis. Journal of Veterinary
understanding of canine atopic dermatitis HARVEY, R. G. & NOBLE, W. C. (1994) A temporal Medical Science 70, 51-55
in the past 75 years. There have been huge study comparing the carriage of Staphylococcus intermedius MAEDA, S., TSUKUI, T., SAZE, K. I., MASUDA, K.,
advances in diagnosis and management, but on normal dogs with atopic dogs in clinical remission. OHNO, K., TSUJIMOTO, H. & IWABUCHI, S. (2005)
Veterinary Dermatology 5, 21-25 Production of a monoclonal antibody to canine thymus
canine atopic dermatitis remains a clinical HAYASHIYA, S., TANI, K., MORIMOTO, M., and activation-regulated chemokine (TARC) and detec-
challenge. It is a very common and very HAYASHI, T., HAYASAKI, M., NOMURA, T., UNE, tion of TARC in lesional skin from dogs with atopic
distressing condition that causes undoubted S., NAKAICHI, M. & TAURA, Y. (2002) Expression of dermatitis. Veterinary Immunology and Immunopathology
suffering for the affected dogs, and is T helper 1 and T helper 2 cytokine mRNAs in freshly 103, 83-92
isolated peripheral blood mononuclear cells from dogs MARSELLA, R., NICKLIN, C. & LOPEZ, J. (2006a)
frustrating for their owners and clinicians. with atopic dermatitis. Journal of Veterinary Medicine Series Studies on the role of routes of allergen exposure in
Nevertheless, we are confident that ongoing A: Physiology Pathology Clinical Medicine 49, 27-31 high IgE-producing beagle dogs sensitized to house dust
research will continue to reveal its mysteries HIGHTOWER, K., MARSELLA, R. & FLYNN-LURIE, mites. Veterinary Dermatology 17, 306-312
A. (2010) Effects of age and allergen exposure on tran- MARSELLA, R., OLIVRY, T., CARLOTTI, D-N. &
and lead to safer and more efficacious forms
sepidermal water loss in a house dust mite-sensitized International Task Force for Canine
of treatment. beagle model of atopic dermatitis. Veterinary Dermatology Atopic Dermatitis (2011) Current evidence of
21, 88-95 skin barrier dysfunction in human and canine atopic
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These include:
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Notes