Allergic sensitization to common pets (cats/dogs) according to different possible modalities of exposure: an Italian Multicenter Study
- G. Liccardi1, 2Email author,
- L. Calzetta2, 3,
- G. Baldi4,
- A. Berra5,
- L. Billeri6,
- M. Caminati7,
- P. Capano8,
- E. Carpentieri9,
- A. Ciccarelli10,
- M. A. Crivellaro11,
- M. Cutajar12,
- M. D’Amato13,
- I. Folletti14,
- F. Gani15,
- D. Gargano16,
- D. Giannattasio17,
- M. Giovannini18,
- C. Lombardi19,
- M. Lo Schiavo20,
- F. Madonna21,
- M. Maniscalco22,
- A. Meriggi23,
- C. Micucci24,
- M. Milanese25,
- C. Montera20,
- G. Paolocci14,
- R. Parente26,
- A. Pedicini27,
- R. Pio20,
- F. Puggioni28,
- M. Russo1,
- A. Salzillo1,
- P. Scavalli29,
- N. Scichilone30,
- B. Sposato31,
- A. Stanziola13,
- G. Steinhilber32,
- A. Vatrella33,
- P. Rogliani2, 3,
- G. Passalacqua34 and
- On behalf of Italian Allergic Respiratory Diseases Task Force
© The Author(s) 2018
Received: 4 December 2017
Accepted: 22 January 2018
Published: 2 February 2018
The query “are there animals at home?” is usually administered for collecting information on anamnesis. This modality to consider exposure to pet allergens constitutes a potential bias in epidemiological studies and in clinical practice. The aim of our study was to evaluate/quantify different modalities of exposure to cat/dog in inducing allergic sensitization.
Thirty Italian Allergy units participated in this study. Each centre was required to collect the data of at least 20 consecutive outpatients sensitized to cat/dog allergens. A standardized form reported all demographic data and a particular attention was paid in relieving possible modalities of exposure to cat/dog.
A total 723 patients sensitized to cat/dog were recorded, 359 (49.65%) reported direct pet contact, 213 patients (29.46%) were pet owners, and 146 subjects (20.19%) were exposed to pets in other settings. Other patients were sensitized by previous pet ownership (150–20.75%) or indirect contact (103–14.25%), in 111 subjects (15.35%) any contact was reported.
Only 213 patients (29.46%) would be classified as “exposed to animals” and 510 (70.54%) as “not exposed” according to usual query. Our classification has shown that many “not-exposed” subjects (399–55.19%) were “really exposed”. The magnitude of exposure to pet allergens at home is not related exclusively to pet ownership. These considerations should be taken into account during the planning of epidemiological studies and in clinical practice for the management of pet allergic individuals.
Exposure to animal allergens constitutes a relevant risk factor for the development of allergic sensitization and respiratory allergic diseases, such as asthma and rhino-conjunctivitis in susceptible individuals . In all developed countries cats and dogs are the most common pets living in indoor environments and the frequency of their ownership is highly variable, according to cultural differences and environmental factors [2, 3]. Cat and dog allergens should be considered ubiquitous because they are found not only in indoor environments, where these animals are kept, but also in other indoor private or public places where cats/dogs have been never kept . Although the presence of a pet at home is considered usually the main risk factor for allergic sensitization, dynamic distribution of the main pet allergens indoors is complex and depends by production, aero-dispersion, sedimentation and passive transport through clothes and other items [5–9]. These variables determine a diffuse presence of pet allergens (indirect exposure) also in indoor environments without pets and in environments where pets are no longer present for a long time (e.g. voluntary removal or re-location, natural death etc.) [10–12]. The query “are there animals at home?” is common and usually administered by researchers, physicians and pulmonologists/allergologists to patients for collecting information on anamnesis . This prevalent modality to consider exposure to pet allergens constitutes a potential bias in large epidemiological studies on the relationship between pet-exposure and allergic sensitization . We believe that an accurate medical history on pet exposure is essential also in clinical practice for an objective evaluation of the risk and the clinical significance of the skin-prick-test (SPT) positivity to pet (cat/dog) allergens, as well as for the management of sensitized patients (pet-avoidance measures, allergen immunotherapy, pharmacological treatment of respiratory symptoms etc.) . The aim of our study was to evaluate and quantify the role of different modalities of exposure to cat/dog in inducing allergic sensitization in a consistent population of cat and/or dog sensitized individuals living in Italy.
Characteristics of the patients sensitized to dog/cat allergens (total no. = 723)
Age range (years)
Family history of atopy (yes/no)a
Intermittent/mild persistent asthmab
Moderate/severe persistent asthmab
Intermittent/mild persistent rhinitisb
Moderate/severe persistent rhinitisb
Allergic sensitization to common pets
Allergic sensitization only to cat/dog
Age of onset of respiratory symptoms (years)
Passive smoke only
Yes (none for pets)
Possible modalities of exposure to pet allergens in 723 pet-sensitized patients (no and %)
Possible modalities of exposure to pets
DOG, no (%)
CAT, no (%)
DOG/CAT, no (%)
150 (20.75 %)
Direct domestic contact
213 (29.46 %)
Direct contact elsewhere
146 (20.19 %)
103 (14.25 %)
No apparent contact
111 (15.35 %)
Triggering of respiratory symptoms after exposure to pet allergens in 723 pet-sensitized patients (no and %)
Type of response
Total, no (%)
DOG, no (%)
CAT, no (%)
DOG/CAT, no (%)
Are allergic respiratory symptoms triggered by direct pet contact?
(*) All pets
Patients no (%)
Discussion and conclusions
Common pet ownership with a stable presence of the animal indoors is usually considered the main index of exposure to cat/dog, with the consequent risk of inducing allergic sensitization. “Are there animals at home?” is the common query administered by doctors to patients in order to collect information on anamnesis during epidemiological studies on the relationship between exposure to pets and development of allergic sensitization (e.g. during the first phase of life to evaluate a “protective effect” of early exposure to cat/dog). The same query is commonly used also in clinical practice to establish the clinical significance of a SPT positivity to cat/dog allergens and, thus, to manage the sensitized patients (pet-avoidance measures, allergen immunotherapy, pharmacological treatment of respiratory symptoms etc.). This commonly used question should not be considered the main factor of exposure to pet allergens and, consequently, the main risk factor for allergic sensitization either in clinical practice and large epidemiological studies [12, 20, 21]. In fact, Fig. 1 shows that only the condition b is reported usually in the questionnaires utilized for large epidemiological studies as well as in clinical practice for collecting data on anamnesis. In the conditions a, c and d the presence of a pet at home should be considered “formally negative” in the questionnaires or anamnestic report, but the level of direct/indirect exposure to pet allergens could be significant [4–7]. Only the condition e should be considered at the lower risk of pet allergen exposure after having excluded any direct/indirect contact with pets. Therefore, the simple answer “yes or no” on the question regarding the presence of pet at home can lead to misleading interpretation of the clinical significance of positive SPTs as well as the real risk of exposure to allergens of dog/cat in epidemiological studies. Consequently, we have previously suggested a new, more realistic, classification of modalities of exposure to pet allergens in “real life” based on the five possible conditions reported in Fig. 1. We have used this classification of exposure either for common pets and large animal such as horse, for which we have provided some specific modifications [10, 21–27]. To the best of our knowledge, this is the first study on the application of these new queries on the modality of exposure to pet allergens. As shown by Table 2, only a limited amount of patients sensitized to pets should be classified as “exposed to animals”, whereas the majority of patients should be classified as “not exposed” as a consequence of usual query “are there animals at home?. On the other hand and in agreement with our classification, a high percentage of formally “not-exposed” subjects were “really exposed” to pets. As a consequence of the present classification, only few patients were really “not-exposed” because no apparent direct/indirect exposure to pets or pet-derived materials. Another important finding of our study is that only half of our pet-sensitized individuals reported a clinically relevant symptoms worsening as a consequence of a close contact with pets, especially with cats. If we consider the modality of exposure, it is likely that these individuals belong to the groups directly exposed to pets at home or elsewhere . These findings confirm that in already pet-sensitized patients a direct and prolonged exposure to animals may represent a relevant risk factor for exacerbations of respiratory symptoms . It is important to note that 338 individuals (46.7%) failed to respond presumably because the symptoms were considered negligible, or not related with the contact of animals.
This is a possible limitation of this study. Other limitations are the lack of data on the presence of pet allergens at home for the reasons previously reported, and the lack of data on the general population regarding the exposure to pets in the first years of life.
GL conceived the idea, designed this study and wrote manuscript first draft. BG, BA, CM, CP, CE, CA, CMA, CMAR, DAM, FI, GF, GD, GDOM, MC, MM, MC, PG, PR, PA, PR, PF, SA, SP, SN, SB, SA, SG and VA recruited pet-sensitized patients. CL, RP, PG, collected the data and RM performed the statistical analyses. All co-authors drafted the manuscript and gave input and agreed to the final submitted version. All authors read and approved the final manuscript.
The authors would like to thank the veterinarian doctor Dr. Giovanni Menna as pet consultant and Mr. Gaetano Francesco Salzillo for technical assistance in the preparation of tables and figures.
Italian Allergic Respiratory Diseases Task Force (other components) Ilaria Baiardini, Caterina Bucca, Giorgio Walter Canonica, Maria Teresa Costantino, Stefano Del Giacco, Enrico Heffler, Stefania La Grutta, Vincenzo Patella, Erminia Ridolo, Giovanni Rolla, Oliviero Rossi, Eleonora Savi, Gianenrico Senna, Carlo Filippo Tesi, Giovanni Viegi.
The authors declare that they have no competing interests.
Availability of data
Data supporting our findings is stored on a database in the Department of Pulmonology, Haematology and Oncology. Division of Pneumology and Allergology. High Speciality “A. Cardarelli” Hospital, Naples Italy.
Ethics approval and consent to participate
Informed consent was obtained from the patients or their parents before performing skin prick tests in ambulatory settings. Ethics approval was not required because diagnostic tests have been carried out during routine outpatient activity.
No funding to declare.
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.
- Konradsen JR, Fujisawa T, van Hage M, Hedlin G, Hilger C, Kleine-tebbe J, Matsui EC, Roberts G, Ronmark E, Platts-Mills TAE. Allergy to furry animals: new insights, diagnostic approaches, and challenges. J Allergy Clin Immunol. 2015;135:616–25.View ArticlePubMedGoogle Scholar
- Eller E, Roll S, Chen CM, Herbarth O, Wichman HE, Berg A, Krämer U, Mommers M, Thijs C, Wijga A, Brunekreef B, Fantini MP, Bravi F, Forastiere F, Porta D, Sunyer J, Torrent M, Høst A, Halken S, Lødrup Carlsen KC, Carlsen KH, Wickman M, Kull I, Wahn U, Willich SN, Lau S, Keil T, Heinrich J. Meta-analysis of determinants for pet ownership in 12 European birth cohort on asthma and allergies: a GA2LEN initiative. Allergy. 2008;63:1491–8.View ArticlePubMedGoogle Scholar
- Sheikh SI, Pitts J, Ryan-Wenger NA, McCoy KS, Hayes D. Racial differences in pet ownership in families of children with asthma. World J Pediatr. 2016;12:343–6.View ArticlePubMedGoogle Scholar
- Liccardi G, D’Amato G, D’Amato L, Salzillo A, Piccolo A, De Napoli I, Dente B, Cazzola M. The effect of pet ownership on the risk of allergic sensitization and bronchial asthma. Respir Med. 2005;99:227–33.View ArticlePubMedGoogle Scholar
- Chan-Yeung M, McClean PA, Sandell PR, Slutsky AS, Zamel N. Sensitization to cat without direct cat exposure. Clin Exp Allergy. 1999;29:762–5.View ArticlePubMedGoogle Scholar
- Munir AKM, Einarsson R, Schou C, Dreborg SKG. Allergens in school dust.I. The amount of the major cat (Fel d 1) and dog (Can f 1) allergens in dust from Swedish schools is high enough to probably cause perennial symptoms in most children with asthma who are sensitized to cat and dog. J Allergy Clin Immunol. 1993;91:1067–74.View ArticlePubMedGoogle Scholar
- Liccardi G, D’Amato G, Russo M, Canonica GW, D’Amato L, Passalacqua G. Focus on cat allergen (Fel d 1): immunological and aerodynamic characteristics, modality of airway sensitization and avoidance strategies. Int Arch Allergy Immunol. 2003;132:1–12.View ArticlePubMedGoogle Scholar
- D’Amato G, Liccardi G, Russo M, Barber D, D’Amato M, Carreira J. Clothing is a carrier of cat allergens. J Allergy Clin Immunol. 1997;99:577–8.View ArticlePubMedGoogle Scholar
- Liccardi G, Barber D, Russo M, D’Amato M, D’Amato G. Human hair: an unexpected source of cat allergen exposure. Int Arch Allergy Immunol. 2005;137:141–4.View ArticlePubMedGoogle Scholar
- Liccardi G, Salzillo A, Calzetta L, Piccolo A, Menna G, Rogliani P. Can the presence of cat/dog at home be considered the only criterion of exposure to cat/dog allergens? A likely underestimated bias in clinical practice and in large epidemiological studies. Eur Ann Allergy Clin Immunol. 2016;48:61–4.PubMedGoogle Scholar
- Liccardi G, Salzillo A, Calzetta L, Pignatti P, Rogliani P. Can pet keeping be considered the only criterion of exposure toc at/dog allergens in the first year of life ? Allergol Immunopathol (Madr). 2016;44:387–8.View ArticlePubMedGoogle Scholar
- Liccardi G, Salzillo A, Cecchi L, D’Amato M, D’Amato G. Is cat-keeping the main determinant of new-onset adulthood cat sensitization ? J Allergy Clin Immunol. 2012;129:1689–90.View ArticlePubMedGoogle Scholar
- Apfelbacher C, Frew E, Xiang A, Apfel A, Smith H. Assessment of pet exposure by self-report in epidemiological studies of allergy and asthma: a systematic review. J Asthma. 2016;53:363–73.View ArticlePubMedGoogle Scholar
- Liccardi G, Salzillo A, Calzetta L, Piccolo A, Rogliani P. Assessment of pet exposure by questionnaires in epidemiological studies (but also in clinical practice!): why the questions should be simplified? J Asthma. 2016;53:879–81.View ArticlePubMedGoogle Scholar
- Bousquet J, Michel FB. Precision of prick and puncture tests. J Allergy Clin Immunol. 1992;90:870–2.View ArticlePubMedGoogle Scholar
- Bousquet J, The ARIA, Workshop Group. Allergic rhinitis and its impact on asthma. J Allergy Clin Immunol. 2001;108:S147–336.View ArticlePubMedGoogle Scholar
- Global Initiative for Asthma. http://ginasthma.com.
- Bousquet J, Heinzerling L, Bachert C, Papadopoulos NG, Bousquet PJ, Burney PG, Canonica GW, Carlsen KH, Cox L, Haahtela T, Lodrup Carlsen KC, Price D, Samolinski B, Simons FE, Wickman M, Annesi-Maesano I, Baena-Cagnani CE, Berg-mann KC, Bindslev-Jensen C, Casale TB, Chiriac A, Cruz AA, Dubakiene R, Durham SR, Fokkens WJ, Gerth-van-Wijk R, Ka-layci O, Kowalski ML, Mari A, Mullol J, Nazamova-Baranova L, O’Hehir RE, Ohta K, Panzner P, Passalacqua G, Ring J, Rogala B, Romano A, Ryan D, Schmid-Grendelmeier P, Todo-Bom A, Valenta R, Woehrl S, Yusuf OM, Zuberbier T, Demoly P. Global allergy and asthma european network; allergic rhinitis and its impact on asthma. Practical guide to skin prick tests in allergy to aeroallergens. Allergy. 2012;67:18–24.View ArticlePubMedGoogle Scholar
- Galvão CES, Graudenz GS, Kalil J, Castro FFM. Sensitization to cat allergen and its association with respiratory allergies: cross-sectional study. Sao Paulo Med J. 2017;135:488–90.View ArticlePubMedGoogle Scholar
- Liccardi G, Salzillo A, Calzetta L, Piccolo A, Rogliani P. Chronic cat allergen exposure and low sensitization: possible limitations in patients’ selection? J Allergy Clin Immunol. 2016;137:1621–2.View ArticlePubMedGoogle Scholar
- Liccardi G, D’Amato G, Canonica GW, Dente B, Passalacqua G. Severe respiratory allergy induced by indirect exposure to rabbit dander: a case report. Allergy. 2004;59:1237–8.View ArticlePubMedGoogle Scholar
- Liccardi G, Piccolo A, Dente B, Salzillo A, Gilder JA, Russo M, D’Amato G. Rabbit allergens: a significant risk for allergic sensitization in subjects without occupational exposure. Respir Med. 2007;101:333–9.View ArticlePubMedGoogle Scholar
- Liccardi G, Passalacqua G, on behalf of the Allergy Study Group of the Italian Society of Respiratory Medicine (SIMeR). Sensitization to rabbit allergens in Italy—a multicentre study in atopic subjects without occupational exposure. Int Arch Allergy Immunol. 2006;141:295–9.View ArticlePubMedGoogle Scholar
- Liccardi G, Salzillo A, Dente B, Piccolo A, Lobefalo G, Russo M, Gilder JA, D’Amato G. Horse allergens: an underestimated risk for allergic sensitization in an urban atopic population without occupational exposure. Respir Med. 2009;103:414–20.View ArticlePubMedGoogle Scholar
- Liccardi G, Salzillo A, Sofia M, Piccolo A, Dente B, Russo M, D’Amato M, Stanziola A, D’Amato G. Sensitization to rodents (mouse/rat) in an urban atopic population without occupational exposure living in Naples. Italy. Eur Ann Allergy Clin Immunol. 2012;44:200–4.PubMedGoogle Scholar
- Liccardi G, Salzillo A, Piccolo A, Russo M, D’Amato G. Sensitization to furry animals in an urban atopic population living in Naples, Italy. Allergy. 2011;66:1500–1.View ArticlePubMedGoogle Scholar
- Liccardi G, D’Amato G, Antonicelli L, Berra A, Billeri L, Canoni-ca GW, Casino G, Cecchi L, Folletti I, Gani F, Lombardi C, Lo Schiavo M, Meriggi A, Milanese M, Passalacqua G, Pio R, Rolla G, Russo M, Scaccianoce S, Senna GE, Scavalli P, Scichilone N, Sposato B, Siracusa A, Ventura MT, Allergy Study Group of the Italian Society of Respiratory Medicine (SIMeR). Sensitization to horse allergens in Italy: a multicentre study in urban atopic subjects without occupational exposure. Int Arch Allergy Immunol. 2011;155:1103–14.View ArticleGoogle Scholar
- Heinrich J, Bedada GB, Zock JP, Chinn S, Norbäck D, Olivieri M, Svanes C, Ponzio M, Verlato G, Villani S, Jarvis D, Luczynska C, Indoor Working Group of the European Community Respiratory Health Survey II. Cat allergen level: its determinants and relationship to specific IgE to cat across European centers. J Allergy Clin Immunol. 2006;118:674–81.View ArticlePubMedGoogle Scholar
- Zeidler MR, Goldin JG, Kleerup EC, Kim HJ, Truong DA, Gjertson DW, Kennedy NJ, Newman KB, Tashkin DP, Silverman JM, Corren J. Small airways response to naturalistic cat allergen exposure in subjects with asthma. J Allergy Clin Immunol. 2006;118:1075–81.View ArticlePubMedGoogle Scholar
- Liccardi G, Passalacqua G, Salzillo A, Piccolo A, Falagiani P, Russo M, Canonica GW, D’Amato G. Is sensitization to furry animals an independent allergic phenotype in non-occupationally exposed individuals ? J Investig Allergol Clin Immunol. 2011;21:137–41.PubMedGoogle Scholar
- Liccardi G, Meriggi A, Russo M, Croce S, Salzillo A, Pignatti P. The risk of sensitization to furry animals in patients already sensitized to cat/dog: a in vitro evaluation using molecular-based allergy diagnostics. J Allergy Clin Immunol. 2015;135:1664–6.View ArticlePubMedGoogle Scholar