- Open Access
Gender aspects in allergies of pets – A secondary publication and update
© The Author(s). 2017
- Received: 13 July 2017
- Accepted: 1 November 2017
- Published: 27 December 2017
Allergies need not only affect humans; this multifactorial and complex disease can also affect animals. Comparative allergology investigates the many similarities between the pathogenesis, clinics, diagnosis, and therapy of the disorders in humans and pet animals. In contrast to human allergy research, the veterinary field lacks access to a central database, which means there are no cohort studies published. This limits not only the research on breed and regional differences in allergies, but also further studies on the impact of gender in allergies of domestic animals. Moreover, domestic cats, dogs and male horses are castrated in most cases, which neutralises any effects of sexual hormones. In this review article a few interesting findings regarding gender aspects in companion animals were extracted from current literature. In summary, there is a lack of data on gender effects on allergies in cats, dogs or horses.
- Atopic dermatitis
Comparative medicine is an interdisciplinary field in which researchers transfer knowledge from the basic research into clinical implications to improve the health of humans and animals. The dog is known as a spontaneous model for atopic dermatitis and many of our companion animals exhibit spontaneous signs of allergic diseases . Moreover, our pet animals are often neutered or spayed to prevent reproduction and/or diseases or to influence their behavior. In this way, some effect of sex hormones on the allergic diseases in this population can be explored. Even if the databases in veterinary medicine are not extensive yet, there is data and some evidence of the influence of sex hormones on the allergic diseases. The purpose of this review was to collect the current evidence of the gender aspects in dogs, cats and horses and their impact on the developement of the allergic diseases.
Canine atopic dermatitis (CAD) is the most investigated and most common allergic disease in companion animals. Due to its similarities to human atopic dermatitis, comparative allergology investigates and compares CAD and atopic disease in humans . In contrast to human medicine, veterinary medicine is far behind with regard to both centralized databases and broad access to medical records of populations of affected animals, or any standardization of allergen testing.
An extreme bias in most of these previously described studies is caused by the fact that companion animals are often neutered, although regional differences occur. In 2016, a retrospective study evaluated the effect of gonadectomy on immune-mediated diseases in dogs and for the first time revealed some interesting insights into this topic . Under the investigated diseases, CAD was the most common disease in 90.090 dogs, presented between 1995 and 2010 to a veterinary teaching hospital in California. In the population of 1638 dogs with CAD, 83 were intact females, 745 neutered females, 169 intact males and 641 neutered males, resulting in a greater relative risk of disease in both neutered sexes. In addition, neutered females were at a 1.5–2 fold higher danger of developing atopic dermatitis . A possible explanation is the role of gonadal steroids on the immune response, especially on the TH2 type hypersensitivity. Estradiol seemed to accelerate the progression of humoral immune response via enhancing the TH2 pathway, while androgen has a protective effect . These findings could indeed explain the results in the California study, but more data is required to suggest any clear evidence for a gender impact on CAD. Nevertheless, dogs present an interesting model of evaluation of the gender aspect in AD due to their classification as non-neutered female and male, and neutered female and male animal groups.
Interestingly enough, even in human literature where significantly more data from birth-control studies, cohort studies and central databases are available, the evidence for a clear gender difference in AD is conflicting . On the other hand, even if human atopic dermatitis (AD) and CAD are compatible in regard to the pathogenesis and clinical presentation, their treatment differs considerably. Causative allergens can be found in most of the dogs with CAD (intradermal test and/or serum IgE test), and in most of the treated dogs, allergen-specific immunotherapy (ASIT) reduces the symptoms . Therefore, a direct comparison should be made carefully.
Other allergies in dogs are flea allergy dermatitis (FAD) and food induced atopic dermatitis (FIAD). At the moment, FIAD is considered to be the same disease as CAD and its main clinical symptoms are comparable to CAD. Only the trigger allergens differ, hence the name food induced atopic dermatitis (FIAD). Although in theory the influence of sex hormones should have an impact on the pathogenesis, there is currently no evidence of gender differences present in FIAD and FAD studies [19, 20].
As is the case with dogs, cats are not registered in a central database system either, with the exception of Switzerland. Central registration of cats, along with systemic data collection by veterinarians, would facilitate cohort population studies in feline allergology and dermatology.
Not unlike dogs, cats frequently show allergic skin symptoms that necessitate a visit at veterinary clinics. Due to the decrease in investigation into the pathogenesis of allergies in cats, the nomenclature of allergic skin diseases in felines has yet to be standardized. Additionally, limited diagnostic methods for allergic feline diseases contribute to a confusing nomenclature, which makes differentiating the three main allergic skin diseases a complex problem. Consequently, queries in medical databases (keywords: feline/cat Atopy, feline/cat Atopic Dermatitis, cat/feline Allergic Dermatitis and Dog/Canine Atopic Dermatitis, Dog/Canine Atopy and Dog/Canine Allergic Dermatitis) result in 4 times fewer references to studies on feline allergies compared to studies on canines.
Itching and excoriations on the head and neck area (head and neck pruritus)
Symmetrical self-induced ventral alopecia
Eosinophilic granuloma complex (eosinophilic granuloma, eosinophilic plaques and indolent/eosinophilic ulcer)
Miliary dermatitis and others.
Feline cutaneous reactive patterns are neither pathognomonic of environmental allergies (atopic dermatitis, or "non-flea, non-food hypersensitivity disorder", [NFNFHD]), nor specific to allergies in cats in general (flea allergy, food allergy and atopic dermatitis — NFNFHD). The field of research that is focused on feline allergies lacks bigger cohort studies, as in the past only small studies (with a few patients) and studies in restricted geographical areas have been published.
In terms of the influence of sexual hormones on the development, duration and severity of feline atopic dermatitis, the following aspects have to be considered. Regardless of sex, the majority of cats in western countries, where most of the published studies about atopic dermatitis or the eosinophilic granuloma complex in cats are being carried out, are castrated early (at 4–12 months of age). Only a few individuals, usually pedigree cats used for breeding, remain intact. As a consequence, less information about family and breed predispositions is available. Only a few case reports show breed and family relation in feline allergy, e.g., in the Abyssinian [21–23] and Devon Rex . Further bias in feline studies is caused by the fact that the intact “barn cats” are rarely taken to a veterinarian, let alone to a specialist, to diagnose the disorder. A multicentric study, however, reported a predisposition for atopic dermatitis (non-flea/non-food hypersensitivity dermatitis [HD]) in young-adult, purebred and female cats. More precisely, 59% of 161 cats with atopic dermatitis were females . Another Australian retrospective study of 45 atopic cats resulted in no gender predisposition when compared to the animal population at the university hospital . The eosinophilic granuloma complex, which in felines is not identical with hypersensitive skin disease, was investigated in 17 Norwegian wildcats – 6 males (2 intact and 4 castrated) and 11 females (20 intact and 1 spayed) . Atopic dermatitis and allergies were underlying the eosinophilic granuloma complex only in some of these cats, but gender effects were not reported. Collectively, to this day it has been impossible to conclude whether female, male or neutered cats are more frequently afflicted with allergies (especially atopic dermatitis) or with the eosinophilic granuloma complex. In a recent prospective clinical trial with 800 shelter kittens that focused on the investigation of the influence of early (at the age of 8–12 weeks) and late (at the age of 6–8 months) gonadectomy on different diseases (including dermatologic conditions), no statistical difference was observed as regards the development of these different diseases . In this study, all kittens were adopted shortly after being neutered and then followed-up until 24 months of age. 1Speaking of feline asthma or feline bronchial disease, few studies with some contradictory results of sexual status on the disease are published. Female predispositions have previously been reported [27, 28], yet in a study by Fosters and others there was no sex predisposition noted .
In general, information about the influence of sex hormones in allergic disorder in companion animals is very limited. A recent study evaluating the neuter status and the sex of dogs with AD found a higher risk of disease development in neutered individuals (males and females) and in neutered female dogs when compared to neutered male dogs. The impact of sexual hormones on canine, feline or equine allergic diseases is an interesting research field and can help in finding comparative aspects in relation to human allergies, due to the neutering performed in companion animals. Therefore, more data are needed to investigate this field. The foundation of central databases, where research centers or universities would document and share their patients’ records would be very helpful. In North America, a central database collecting data of volunteering universities and centers of veterinary patients does exist (veterinary medical databases, VMDB), but it is not freely accessible.
Additionally, central state registers of all small animals (dogs and cats) and possibly horses, documenting species, date of birth, breed, gender, status/age of neutering, and diseases would be the next useful step in understanding hormonal influences. Data from commercial veterinary laboratories performing allergy testing may also – to a certain degree – be valuable. These institutions usually collect a complete signalment including the status of neutering and a rather detailed history.
In addition, longitudinal studies that would follow the relationship between the neutering of allergic dogs or cats and the amount of medication needed to control their AD might, to some degree, address our question.
The main problem considering the correct evaluation of gender effects on atopic and/or allergic diseases in cats, dogs and horses is the lack of a central registry/database inhibiting the analysis of large data sets. The often practiced castration of domestic animals at different ages represents another complexity in approaching this question. Overall, more evidence is needed to document clinical importance of gender in allergies of domestic animals. Deeper knowledge could lead to practical recommendations for animal owners.
We would like to acknowledge Brett Whitley for English proof reading this article.
Herrmann I, Panakova L. Genderaspekte bei den Allergien unserer Haustiere. Allergologie 2017; 40: 128-132.
This work was supported by grants of the Austrian Science Fund FWF, W1248-B30 (MCCA) and in part SFB F4606-B28.
Availability of data and materials
IH and LP designed the original article. IH, LE and LP wrote the updated article and searched the literature. All authors read and approved the final manuscript.
Ethics approval and consent to participate
Consent for publication
All authors have seen and approved the last version.
The authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Open AccessThis 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.
- Jensen-Jarolim E, Einhorn L, Herrmann I, Thalhammer JG, Panakova L. Pollen allergies in humans and their dogs, cats and horses: differences and similarities. Clin Transl Allergy. 2015;5:15.View ArticlePubMedPubMed CentralGoogle Scholar
- Olivry T. What can dogs bring to atopic dermatitis research? Chem Immunol Allergy. 2012;96:61–72.View ArticlePubMedGoogle Scholar
- Griffin C, DeBoer D. The ACVD task force on canine atopic dermatitis (XIV): clinical manifestations of canine atopic dermatitis. Vet Immunol Immunopathol. 2001;81:255–69.View ArticlePubMedGoogle Scholar
- Scott DW. Observations on canine atopy. J Am Anim Hosp Assoc 1981;14:766–79.Google Scholar
- Willemse A, van den Brom WE. Investigations of the symptomatology and the significance of immediate skin test reactivity in canine atopic dermatitis. Res Vet Sci. 1983;34:261–5.PubMedGoogle Scholar
- Bizikova P, Santoro D, Marsella R, Nuttall T, Eisenschenk MNC, Pucheu-Haston CM. Review: clinical and histological manifestations of canine atopic dermatitis. Vet Dermatol. 2015;26:79–e24.View ArticlePubMedGoogle Scholar
- Favrot C, Steffan J, Seewald W, Picco F. A prospective study on the clinical features of chronic canine atopic dermatitis and its diagnosis. Vet Dermatol. 2010;21:23–31.View ArticlePubMedGoogle Scholar
- Jaeger K, Linek M, Power HT, Bettenay SV, Zabel S, Rosychuk RAW, et al. Breed and site predispositions of dogs with atopic dermatitis: a comparison of five locations in three continents. Vet Dermatol. 2010;21:118–22.View ArticlePubMedGoogle Scholar
- Bruet V, Bourdeau PJ, Roussel A, Imparato L, Desfontis J-C. Characterization of pruritus in canine atopic dermatitis, flea bite hypersensitivity and flea infestation and its role in diagnosis. Vet Dermatol. 2012;23:487–e93.View ArticlePubMedGoogle Scholar
- Wilhem S, Kovalik M, Favrot C. Breed-associated phenotypes in canine atopic dermatitis. Vet Dermatol. 2011;22:143–9.View ArticlePubMedGoogle Scholar
- Nødtvedt A, Bergvall K, Sallander M, Egenvall A, Emanuelson U, Hedhammar Å. A case?Control study of risk factors for canine atopic dermatitis among boxer, bullterrier and west highland white terrier dogs in Sweden. Vet Dermatol. 2007;18:309–15.View ArticlePubMedGoogle Scholar
- Salzmann CA, Olivry TJM, Nielsen DM, Paps JS, Harris TL, Olby NJ. Genome-wide linkage study of atopic dermatitis in west highland white terriers. BMC Genet. 2011;12:37.View ArticlePubMedPubMed CentralGoogle Scholar
- Wood SH, Ke X, Nuttall T, McEwan N, Ollier WE, Carter SD. Genome-wide association analysis of canine atopic dermatitis and identification of disease related SNPs. Immunogenetics. 2009;61:765–72.View ArticlePubMedGoogle Scholar
- Shaw SC, Wood JLN, Freeman J, Littlewood JD, Hannant D. Estimation of heritability of atopic dermatitis in Labrador and golden retrievers. Am J Vet Res. 2004;65:1014–20.View ArticlePubMedGoogle Scholar
- Sundburg CR, Belanger JM, Bannasch DL, Famula TR, Oberbauer AM. Gonadectomy effects on the risk of immune disorders in the dog: a retrospective study. BMC Vet Res. 2016;12:278.View ArticlePubMedPubMed CentralGoogle Scholar
- Tanriverdi F, Silveira LFG, Maccoll GS, Bouloux PMG. The hypothalamic – pituitary – gonadal axis : immune function and autoimmunity. J Endocrinol. 2003;176:293–304.View ArticlePubMedGoogle Scholar
- Chen W, Mempel M, Schober W, Behrendt H, Ring J. Gender difference, sex hormones, and immediate type hypersensitivity reactions. Allergy Eur J Allergy Clin Immunol. 2008;63:1418–27.View ArticleGoogle Scholar
- Loewenstein C, Mueller RS. A review of allergen-specific immunotherapy in human and veterinary medicine. Vet Dermatol. 2009;20:84–98.View ArticlePubMedGoogle Scholar
- Picco F, Zini E, Nett C, Naegeli C, Bigler B, Rüfenacht S, et al. A prospective study on canine atopic dermatitis and food-induced allergic dermatitis in Switzerland. Vet Dermatol. 2008;19:150–5.View ArticlePubMedGoogle Scholar
- Verlinden A, Hesta M, Millet S, Janssens GPJ. Food allergy in dogs and cats: a review. Crit Rev Food Sci Nutr. 2006;46:259–73.View ArticlePubMedGoogle Scholar
- Moriello KA. Feline atopy in three littermates. Vet Dermatol. 2001;12:177–81.View ArticlePubMedGoogle Scholar
- Hobi S, Linek M, Marignac G, Olivry T, Beco L, Nett C, et al. Clinical characteristics and causes of pruritus in cats: a multicentre study on feline hypersensitivity-associated dermatoses. Vet Dermatol. 2011;22:406–13.View ArticlePubMedGoogle Scholar
- Foster AP. Diagnosing and treating feline atopy. Vet Med. 2002;97:226–40.Google Scholar
- Ravens PA, Xu BJ, Vogelnest LJ. Feline atopic dermatitis: a retrospective study of 45 cases (2001-2012). Vet Dermatol. 2014;25:95–102.View ArticlePubMedGoogle Scholar
- Leistra WHG, van Oost BA, Willemse T. Non-pruritic granuloma in Norwegian forest cats. Vet Rec. 2005;156:575–7.View ArticlePubMedGoogle Scholar
- Porters N, Polis I, Moons CPH, Van de Maele I, Ducatelle R, Goethals K, et al. Relationship between age at gonadectomy and health problems in kittens adopted from shelters. Vet Rec. 2015;176:572.View ArticlePubMedGoogle Scholar
- Adamama-Moraitou KK, Patsikas MN, Koutinas AF. Feline lower airway disease: a retrospective study of 22 naturally occurring cases from Greece. J Feline Med Surg. 2004;6:227–33.View ArticlePubMedGoogle Scholar
- Moise NS, Wiedenkeller D, Yeager AE, Blue JT, Scarlett J. Clinical, radiographic, and bronchial cytologic features of cats with bronchial disease: 65 cases (1980-1986). J Am Vet Med Assoc. 1989;194:1467–73.PubMedGoogle Scholar
- Foster SF, Allan GS, Martin P, Robertson ID, Malik R. Twenty-five cases of feline bronchial disease (1995-2000). J Feline Med Surg. 2004;6:181–8.View ArticlePubMedGoogle Scholar
- Stepnik CT, Outerbridge CA, White SD, Kass PH. Equine atopic skin disease and response to allergen-specific immunotherapy: a retrospective study at the University of California-Davis (1991-2008). Vet Dermatol. 2012;23:29–36.View ArticlePubMedGoogle Scholar
- Vostrá-Vydrová H, Vostrý L, Hofmanová B, Krupa E, Zavadilová L. Pedigree analysis of the endangered old Kladruber horse population. Livest Sci. 2016;185:17–23.View ArticleGoogle Scholar
- Lange S, Hamann H, Deegen E, Ohnesorge B, Distl O. Investigation of the prevalence of summer eczema in Icelandic horses in northern Germany. Berl Munch Tierarztl Wochenschr. 2005;118:481–9.PubMedGoogle Scholar
- Couëtil LL, Ward MP. Analysis of risk factors for recurrent airway obstruction in north American horses: 1,444 cases (1990-1999). J Am Vet Med Assoc. 2003;223:1645–50.View ArticlePubMedGoogle Scholar