The Primary Prevention of Atopy: Does Early Exposure to Cats and Dogs Prevent the Development of Allergy and Asthma in Children? A Comprehensive Analysis of the Literature
Abstract
:1. Introduction
2. Materials and Methods
2.1. Structured Clinical Question
2.2. Literature Search
3. Results
Summary of the Included Study
4. Discussion
4.1. Exposure to a Cat or Dog and the Protection against Allergies
4.2. The Role of Early Exposure to a Cat or Dog on the Development of Cat or Dog Allergy Later in Life
4.3. The Combination of Cat/Dog Exposure and Farming
4.4. The Role of other Environmental and Genetic Factors on the Development of Allergy
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Apelberg, B.J.; Aoki, Y.; Jaakkola, J.J.K. Systematic review: Exposure to pets and risk of asthma and asthma-like symptoms. J. Allergy Clin. Immunol. 2001, 107, 455–460. [Google Scholar] [CrossRef] [PubMed]
- Ownby, D.R.; Johnson, C.C. Does exposure to dogs and cats in the first year of life influence the development of allergic sensitization? Curr. Opin. Allergy Clin. Immunol. 2003, 3, 517–522. [Google Scholar] [CrossRef] [PubMed]
- Chan, S.K.; Leung, D.Y.M. Dog and Cat Allergies: Current State of Diagnostic Approaches and Challenges. Allergy Asthma Immunol. Res. 2018, 10, 97–105. [Google Scholar] [CrossRef] [PubMed]
- Man’s Best Friend: Global Pet Ownership and Feeding Trends—GfK. Available online: https://www.gfk.com/insights/mans-best-friend-global-pet-ownership-and-feeding-trends (accessed on 15 July 2023).
- van Hage, M.; Käck, U.; Asarnoj, A.; Konradsen, J.R. An update on the prevalence and diagnosis of cat and dog allergy—Emphasizing the role of molecular allergy diagnostics. Mol. Immunol. 2023, 157, 1–7. [Google Scholar] [CrossRef] [PubMed]
- Rapporto Assalco Zoomark 2019. Available online: https://www.assiteca.it/wp-content/uploads/2019/07/rapporto-assalco-zoomark-2019.pdf (accessed on 15 July 2023).
- Sander, I.; Lotz, A.; Neumann, H.D.; Czibor, C.; Flagge, A.; Zahradnik, E.; Raulf, M. Indoor allergen levels in settled airborne dust are higher in day-care centers than at home. Allergy 2018, 73, 1263–1275. [Google Scholar] [CrossRef] [PubMed]
- Amr, S.; Bollinger, M.E.; Myers, M.; Hamilton, R.G.; Weiss, S.R.; Rossman, M.; Osborne, L.; Timmins, S.; Kimes, D.S.; Levine, E.R.; et al. Environmental allergens and asthma in urban elementary schools. Ann. Allergy Asthma Immunol. 2003, 90, 34–40. [Google Scholar] [CrossRef] [PubMed]
- Custovic, A.; Fletcher, A.; Pickering, C.A.; Francis, H.C.; Green, R.; Smith, A.; Chapman, M.; Woodcock, A. Domestic allergens in public places III: House dust mite, cat, dog, and cockroach allergens in British hospitals. Clin. Exp. Allergy 1998, 28, 53–59. [Google Scholar] [CrossRef]
- Berge, M.; Munir, A.K.; Dreborg, S. Concentrations of cat (Fel d1), dog (Can f1) and mite (Der f1 and Der p1) allergens in the clothing and school environment of Swedish schoolchildren with and without pets at home. Pediatr. Allergy Immunol. 1998, 9, 25–30. [Google Scholar] [CrossRef]
- Bonnet, B.; Messaoudi, K.; Jacomet, F.; Michaud, E.; Fauquert, J.L.; Caillaud, D.; Evrard, B. An update on molecular cat allergens: Fel d 1 and what else? Chapter 1: Fel d 1, the major cat allergen. Allergy Asthma Clin. Immunol. 2018, 14, 14. [Google Scholar] [CrossRef] [PubMed]
- Lei, D.K.; Grammer, L.C. An overview of allergens. Allergy Asthma Proc. 2019, 40, 362–365. [Google Scholar] [CrossRef] [PubMed]
- Ingram, J.M.; Sporik, R.; Rose, G.; Honsinger, R.; Chapman, M.D.; Platts-Mills, T.A. Quantitative assessment of exposure to dog (Can f 1) and cat (Fel d 1) allergens: Relation to sensitization and asthma among children living in Los Alamos, New Mexico. J. Allergy Clin. Immunol. 1995, 96, 449–456. [Google Scholar] [CrossRef] [PubMed]
- Tedner, S.G.; Söderhäll, C.; Konradsen, J.R.; Bains, K.E.S.; Borres, M.P.; Carlsen, K.H.; Carlsen, K.C.L.; Färdig, M.; Gerdin, S.W.; Gudmundsdóttir, H.K.; et al. Extract and molecular-based early infant sensitization and associated factors—A PreventADALL study. Allergy 2021, 76, 2730–2739. [Google Scholar] [CrossRef] [PubMed]
- Wärnberg Gerdin, S.; Lie, A.; Asarnoj, A.; Borres, M.P.; Lødrup Carlsen, K.C.; Färdig, M.; Konradsen, J.R.; Monceyron Jonassen, C.; Olsson Mägi, C.A.; Rehbinder, E.M.; et al. Impaired skin barrier and allergic sensitization in early infancy. Allergy 2022, 77, 1464–1476. [Google Scholar] [CrossRef] [PubMed]
- Comberiati, P.; Costagliola, G.; D’Elios, S.; Peroni, D. Prevention of Food Allergy: The Significance of Early Introduction. Medicina 2019, 55, 323. [Google Scholar] [CrossRef] [PubMed]
- Trogen, B.; Jacobs, S.; Nowak-Wegrzyn, A. Early Introduction of Allergenic Foods and the Prevention of Food Allergy. Nutrients 2022, 14, 2565. [Google Scholar] [CrossRef] [PubMed]
- Caimmi, D.; Caffarelli, C.; Licari, A.; Miraglia Del Giudice, M.; Calvani, M.; Marseglia, G.L.; Marseglia, A.; Ricci, G.; Martelli, A.; Cravidi, C.; et al. Food allergy in primary care. Acta Biomed. 2021, 92, e2021521. [Google Scholar] [CrossRef] [PubMed]
- Kakieu Djossi, S.; Khedr, A.; Neupane, B.; Proskuriakova, E.; Jada, K.; Mostafa, J.A. Food Allergy Prevention: Early Versus Late Introduction of Food Allergens in Children. Cureus 2022, 14, e21046. [Google Scholar] [CrossRef]
- Calvani, M.; Anania, C.; Caffarelli, C.; Martelli, A.; Miraglia Del Giudice, M.; Cravidi, C.; Duse, M.; Manti, S.; Tosca, M.A.; Cardinale, F.; et al. Food allergy: An updated review on pathogenesis, diagnosis, prevention and management. Acta Biomed. 2020, 91, e2020012. [Google Scholar] [CrossRef]
- Liberati, A.; Altman, D.G.; Tetzlaff, J.; Mulrow, C.; Gøtzsche, P.C.; Ioannidis, J.P.; Clarke, M.; Devereaux, P.J.; Kleijnen, J.; Moher, D. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: Explanation and elaboration. PLoS Med. 2009, 6, e1000100. [Google Scholar] [CrossRef] [PubMed]
- Pinot de Moira, A.; Strandberg-Larsen, K.; Bishop, T.; Pedersen, M.; Avraam, D.; Cadman, T.; Calas, L.; Casas, M.; de Lauzon Guillain, B.; Elhakeem, A.; et al. Associations of early-life pet ownership with asthma and allergic sensitization: A meta-analysis of more than 77,000 children from the EU Child Cohort Network. J. Allergy Clin. Immunol. 2022, 150, 82–92. [Google Scholar] [CrossRef] [PubMed]
- Al-Tamprouri, C.; Malin, B.; Bill, H.; Lennart, B.; Anna, S. Cat and dog ownership during/after the first year of life and risk for sensitization and reported allergy symptoms at age 13. Immun. Inflamm. Dis. 2019, 7, 250–257. [Google Scholar] [CrossRef] [PubMed]
- Marrs, T.; Logan, K.; Craven, J.; Radulovic, S.; McLean, W.H.A.I.; Lack, G.; Flohr, C.; Perkin, M.R. Dog ownership at three months of age is associated with protection against food allergy. Allergy 2019, 74, 2212–2219, Correction in Allergy 2020, 75, 2428. [Google Scholar] [CrossRef] [PubMed]
- Okabe, H.; Hashimoto, K.; Yamada, M.; Ono, T.; Yaginuma, K.; Kume, Y.; Chishiki, M.; Sato, A.; Ogata, Y.; Imaizumi, K.; et al. Associations between fetal or infancy pet exposure and food allergies: The Japan Environment and Children’s Study. PLoS ONE 2023, 18, e0282725. [Google Scholar] [CrossRef]
- Kapszewicz, K.; Podlecka, D.; Polańska, K.; Stelmach, I.; Majak, P.; Majkowska-Wojciechowska, B.; Tymoniuk, B.; Jerzyńska, J.; Brzozowska, A. Home Environment in Early-Life and Lifestyle Factors Associated with Asthma and Allergic Diseases among Inner-City Children from the REPRO_PL Birth Cohort. Int. J. Environ. Res. Public Health 2022, 19, 11884. [Google Scholar] [CrossRef] [PubMed]
- Park, M.J.; Lee, S.Y.; Song, K.B.; Lee, S.H.; Choi, K.Y.; Lee, K.W.; Jung, S.; Suh, D.I.; Sheen, Y.H.; Kim, K.W.; et al. Dog Ownership in Early Life Increased the Risk of Nonatopic Asthma in Children. Int. Arch. Allergy Immunol. 2021, 182, 980–988. [Google Scholar] [CrossRef] [PubMed]
- Norbäck, D.; Zhang, X.; Tian, L.; Zhang, Y.; Zhang, Z.; Yang, L.; Chen, X.; Zeng, Z.; Lu, C.; Zhao, Z. Prenatal and perinatal home environment and reported onset of wheeze, rhinitis and eczema symptoms in preschool children in Northern China. Sci. Total Environ. 2021, 774, 145700. [Google Scholar] [CrossRef] [PubMed]
- Lu, C.; Norbäck, D.; Zhang, Y.; Li, B.; Zhao, Z.; Huang, C.; Zhang, X.; Qian, H.; Sun, Y.; Wang, J.; et al. Furry pet-related wheeze and rhinitis in pre-school children across China: Associations with early life dampness and mould, furry pet keeping, outdoor temperature, PM10 and PM2.5. Environ. Int. 2020, 144, 106033. [Google Scholar] [CrossRef] [PubMed]
- Li, C.; Chen, Q.; Zhang, X.; Li, H.; Liu, Q.; Fei, P.; Huang, L.; Yao, Z. Early Life Domestic Pet Ownership, and the Risk of Pet Sensitization and Atopic Dermatitis in Preschool Children: A Prospective Birth Cohort in Shanghai. Front. Pediatr. 2020, 8, 192. [Google Scholar] [CrossRef]
- Ojwang, V.; Nwaru, B.I.; Takkinen, H.M.; Kaila, M.; Niemelä, O.; Haapala, A.M.; Ilonen, J.; Toppari, J.; Hyöty, H.; Veijola, R.; et al. Early exposure to cats, dogs and farm animals and the risk of childhood asthma and allergy. Pediatr. Allergy Immunol. 2020, 31, 265–272. [Google Scholar] [CrossRef]
- Gallant, M.J.; Ellis, A.K. Prenatal and early-life exposure to indoor air-polluting factors and allergic sensitization at 2 years of age. Ann. Allergy Asthma Immunol. 2020, 124, 283–287. [Google Scholar] [CrossRef]
- Smejda, K.; Polanska, K.; Stelmach, W.; Majak, P.; Stelmach, I. Dog keeping at home before and during pregnancy decreased the risk of food allergy in 1-year-old children. Postepy Dermatol. Alergol. 2020, 37, 255–261. [Google Scholar] [CrossRef] [PubMed]
- Fall, T.; Ekberg, S.; Lundholm, C.; Fang, F.; Almqvist, C. Dog characteristics and future risk of asthma in children growing up with dogs. Sci. Rep. 2018, 8, 16899. [Google Scholar] [CrossRef] [PubMed]
- Bedolla-Barajas, M.; Morales-Romero, J.; Bedolla-Pulido, T.I.; Bedolla-Pulido, T.R.; Meza-López, C.; Pulido-Guillén, N.A. Exposure to dogs but not cats is associated to a decrease in the prevalence in atopic dermatitis amongst school-children. Allergol. Immunopathol. 2018, 46, 431–437. [Google Scholar] [CrossRef] [PubMed]
- Luo, S.; Sun, Y.; Hou, J.; Kong, X.; Wang, P.; Zhang, Q.; Sundell, J. Pet keeping in childhood and asthma and allergy among children in Tianjin area, China. PLoS ONE 2018, 13, e0197274. [Google Scholar] [CrossRef] [PubMed]
- O’Connor, G.T.; Lynch, S.V.; Bloomberg, G.R.; Kattan, M.; Wood, R.A.; Gergen, P.J.; Jaffee, K.F.; Calatroni, A.; Bacharier, L.B.; Beigelman, A.; et al. Early-life home environment and risk of asthma among inner-city children. J. Allergy Clin. Immunol. 2018, 141, 1468–1475. [Google Scholar] [CrossRef] [PubMed]
- Hesselmar, B.; Hicke-Roberts, A.; Lundell, A.C.; Adlerberth, I.; Rudin, A.; Saalman, R.; Wennergren, G.; Wold, A.E. Pet-keeping in early life reduces the risk of allergy in a dose-dependent fashion. PLoS ONE 2018, 13, e0208472. [Google Scholar] [CrossRef] [PubMed]
- Cukrowska, B.; Bierła, J.B.; Zakrzewska, M.; Klukowski, M.; Maciorkowska, E. The Relationship between the Infant Gut Microbiota and Allergy. The Role of Bifidobacterium breve and Prebiotic Oligosaccharides in the Activation of Anti-Allergic Mechanisms in Early Life. Nutrients 2020, 12, 946. [Google Scholar] [CrossRef] [PubMed]
- Fujimura, K.E.; Lynch, S.V. Microbiota in allergy and asthma and the emerging relationship with the gut microbiome. Cell Host Microbe 2015, 17, 592–602. [Google Scholar] [CrossRef]
- Gensollen, T.; Blumberg, R.S. Correlation between early-life regulation of the immune system by microbiota and allergy development. J. Allergy Clin. Immunol. 2017, 139, 1084–1091. [Google Scholar] [CrossRef]
- Heinrich, J.; Gehring, U.; Douwes, J.; Koch, A.; Fahlbusch, B.; Bischof, W.; Wichmann, H.E. Pets and vermin are associated with high endotoxin levels in house dust. Clin. Exp. Allergy 2001, 31, 1839–1845. [Google Scholar] [CrossRef]
- Williams, L.K.; Ownby, D.R.; Maliarik, M.J.; Johnson, C.C. The role of endotoxin and its receptors in allergic disease. Ann. Allergy Asthma Immunol. 2005, 94, 323–332. [Google Scholar] [CrossRef] [PubMed]
- Gern, J.E.; Reardon, C.L.; Hoffjan, S.; Nicolae, D.; Li, Z.; Roberg, K.A.; Neaville, W.A.; Carlson-Dakes, K.; Adler, K.; Hamilton, R.; et al. Effects of dog ownership and genotype on immune development and atopy in infancy. J. Allergy Clin. Immunol. 2004, 113, 307–314. [Google Scholar] [CrossRef] [PubMed]
- Noval Rivas, M.; Chatila, T.A. Regulatory T cells in allergic diseases. J. Allergy Clin. Immunol. 2016, 138, 639–652. [Google Scholar] [CrossRef] [PubMed]
- Stark, J.M.; Liu, J.; Tibbitt, C.A.; Christian, M.; Ma, J.; Wintersand, A.; Dunst, J.; Kreslavsky, T.; Murrell, B.; Adner, M.; et al. Recombinant multimeric dog allergen prevents airway hyperresponsiveness in a model of asthma marked by vigorous TH2 and TH17 cell responses. Allergy 2022, 77, 2987–3001. [Google Scholar] [CrossRef] [PubMed]
- Schröder, P.C.; Illi, S.; Casaca, V.I.; Lluis, A.; Böck, A.; Roduit, C.; Depner, M.; Frei, R.; Genuneit, J.; Pfefferle, P.I.; et al. A switch in regulatory T cells through farm exposure during immune maturation in childhood. Allergy 2017, 72, 604–615. [Google Scholar] [CrossRef] [PubMed]
- Lluis, A.; Depner, M.; Gaugler, B.; Saas, P.; Casaca, V.I.; Raedler, D.; Michel, S.; Tost, J.; Liu, J.; Genuneit, J.; et al. Increased regulatory T-cell numbers are associated with farm milk exposure and lower atopic sensitization and asthma in childhood. J. Allergy Clin. Immunol. 2014, 133, 551–559. [Google Scholar] [CrossRef]
- Schaub, B.; Liu, J.; Hoppler, S.; Haug, S.; Sattler, C.; Lluis, A.; Illi, S.; von Mutius, E. Impairment of tregulatory cells in cord blood of atopic mothers. J. Allergy Clin. Immunol. 2008, 121, 1491–1499. [Google Scholar] [CrossRef]
- Zhang, H.; Kong, H.; Zeng, X.; Guo, L.; Sun, X.; He, S. Subsets of regulatory T cells and their roles in allergy. J. Transl. Med. 2014, 12, 125. [Google Scholar] [CrossRef]
- Zhang, Y.; Tan, M.; Qian, X.; Li, C.; Yue, L.; Liu, Y.; Shi, S. Interaction between early-life pet exposure and methylation pattern of ADAM33 on allergic rhinitis among children aged 3–6 years in China. Allergy Asthma Clin. Immunol. 2021, 17, 44. [Google Scholar] [CrossRef]
- Liccardi, G.; Calzetta, L.; Baldi, G.; Berra, A.; Billeri, L.; Caminati, M.; Capano, P.; Carpentieri, E.; Ciccarelli, A.; Crivellaro, M.A.; et al. Allergic sensitization to common pets (cats/dogs) according to different possible modalities of exposure: An Italian Multicenter Study. Clin. Mol. Allergy 2018, 16, 3. [Google Scholar] [CrossRef]
- 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, 61–64. [Google 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. 2016, 44, 387–388. [Google Scholar] [CrossRef] [PubMed]
- van Leent, M.M.T.; Priem, B.; Schrijver, D.P.; de Dreu, A.; Hofstraat, S.R.J.; Zwolsman, R.; Beldman, T.J.; Netea, M.G.; Mulder, W.J.M. Regulating trained immunity with nanomedicine. Nat. Rev. Mater. 2022, 7, 465–481. [Google Scholar] [CrossRef]
- Martín-Cruz, L.; Sevilla-Ortega, C.; Angelina, A.; Domínguez-Andrés, J.; Netea, M.G.; Subiza, J.L.; Palomares, O. From trained immunity in allergy to trained immunity-based allergen vaccines. Clin. Exp. Allergy 2023, 53, 145–155. [Google Scholar] [CrossRef] [PubMed]
- Wanka, L.; Jappe, U. Trained immunity and allergy: State of the art and future perspectives. Allergy 2021, 76, 1265–1267. [Google Scholar] [CrossRef] [PubMed]
- Indolfi, C.; Dinardo, G.; Klain, A.; Contieri, M.; Umano, G.R.; Decimo, F.; Abbadessa, S.; Vitulano, C.; Ciprandi, G.; Miraglia Del Giudice, M. Sensitization to nsLTP: A Retrospective Study in An Italian Pediatric Population over the Last Decade. J. Immunol. Res. 2023, 2023, 4053799. [Google Scholar] [CrossRef] [PubMed]
- Allergy Season Is about to Get Worse—National Geographic. Available online: https://www.nationalgeographic.com/environment/article/allergy-season-could-be-much-longer-with-climate-change#:~:text=The%20World%20Health%20Organization%20estimates,to%2040%20percent%20of%20children (accessed on 15 July 2023).
- Riedler, J.; Braun-Fahrländer, C.; Eder, W.; Schreuer, M.; Waser, M.; Maisch, S.; Carr, D.; Schierl, R.; Nowak, D.; von Mutius, E. Exposure to farming in early life and development of asthma and allergy: A cross-sectional survey. Lancet 2001, 358, 1129–1133. [Google Scholar] [CrossRef] [PubMed]
- Tizek, L.; Redlinger, E.; Ring, J.; Eyerich, K.; Biedermann, T.; Zink, A. Urban vs rural—Prevalence of self-reported allergies in various occupational and regional settings. World Allergy Organ. J. 2022, 15, 100625. [Google Scholar] [CrossRef] [PubMed]
- Leonardi, S.; Miraglia del Giudice, M.; La Rosa, M.; Bellanti, J.A. Atopic disease, immune system, and the environment. Allergy Asthma Proc. 2007, 28, 410–417. [Google Scholar] [CrossRef] [PubMed]
- Hakanen, E.; Lehtimäki, J.; Salmela, E.; Tiira, K.; Anturaniemi, J.; Hielm-Björkman, A.; Ruokolainen, L.; Lohi, H. Urban environment predisposes dogs and their owners to allergic symptoms. Sci. Rep. 2018, 8, 1585. [Google Scholar] [CrossRef]
- Song, M.; Hwang, S.; Son, E.; Yeo, H.J.; Cho, W.H.; Kim, T.W.; Kim, K.; Lee, D.; Kim, Y.H. Geographical Differences of Risk of Asthma and Allergic Rhinitis according to Urban/Rural Area: A Systematic Review and Meta-analysis of Cohort Studies. J. Urban Health 2023, 100, 478–492. [Google Scholar] [CrossRef]
- Garn, H.; Potaczek, D.P.; Pfefferle, P.I. The Hygiene Hypothesis and New Perspectives-Current Challenges Meeting an Old Postulate. Front. Immunol. 2021, 12, 637087. [Google Scholar] [CrossRef] [PubMed]
- Prokopakis, E.; Vardouniotis, A.; Kawauci, H. The pathophysiology of the hygiene hypothesis. Int. J. Pediatr. Otorhinolaryngol. 2013, 77, 1065–1071. [Google Scholar] [CrossRef] [PubMed]
- Weber, J.; Illi, S.; Nowak, D. Asthma and the hygiene hypothesis. Does cleanliness matter? Am. J. Respir. Crit. Care Med. 2015, 191, 522–529. [Google Scholar] [CrossRef] [PubMed]
- Indolfi, C.; Klain, A.; Di Nardo, G.; Gitto, E.; Cuppari, C.; Ceravolo, A.; Concolino, D.; De Sarro, R.; Salpietro, A.; Decimo, F.; et al. Is there a link between infections and asthma? J. Biol. Regul. Homeost. Agents 2022, 36, 159–169. [Google Scholar]
- Klain, A.; Indolfi, C.; Dinardo, G.; Licari, A.; Cardinale, F.; Caffarelli, C.; Manti, S.; Ricci, G.; Pingitore, G.; Tosca, M.; et al. United airway disease. Acta Biomed. 2021, 92, e2021526. [Google Scholar] [CrossRef] [PubMed]
- Krzych-Fałta, E.; Furmańczyk, K.; Piekarska, B.; Raciborski, F.; Tomaszewska, A.; Walkiewicz, A.; Samel-Kowalik, P.; Borowicz, J.; Namysłowski, A.; Samoliński, B.K. Extent of protective or allergy-inducing effects in cats and dogs. Ann. Agric. Environ. Med. 2018, 25, 268–273. [Google Scholar] [CrossRef] [PubMed]
- Burbank, A.J.; Sood, A.K.; Kesic, M.J.; Peden, D.B.; Hernandez, M.L. Environmental determinants of allergy and asthma in early life. J. Allergy Clin. Immunol. 2017, 140, 1–12. [Google Scholar] [CrossRef]
- López-Cervantes, J.P.; Lønnebotn, M.; Jogi, N.O.; Calciano, L.; Kuiper, I.N.; Darby, M.G.; Dharmage, S.C.; Gómez-Real, F.; Hammer, B.; Bertelsen, R.J.; et al. The Exposome Approach in Allergies and Lung Diseases: Is It Time to Define a Preconception Exposome? Int. J. Environ. Res. Public Health 2021, 18, 12684. [Google Scholar] [CrossRef] [PubMed]
- González-Pérez, R.; Poza-Guedes, P.; Pineda, F.; Galán, T.; Mederos-Luis, E.; Abel-Fernández, E.; Martínez, M.J.; Sánchez-Machín, I. Molecular Mapping of Allergen Exposome among Different Atopic Phenotypes. Int. J. Mol. Sci. 2023, 24, 10467. [Google Scholar] [CrossRef]
- O’Regan, G.M.; Sandilands, A.; McLean, W.H.I.; Irvine, A.D. Filaggrin in atopic dermatitis. J. Allergy Clin. Immunol. 2008, 122, 689–693. [Google Scholar] [CrossRef] [PubMed]
- Klain, A.; Indolfi, C.; Dinardo, G.; Bifulco, D.; Quaranta, G.; Bencivenga, C.L.; Decimo, F.; Miraglia del Giudice, M. Marcia Atopica: Ci sono nuove evidenze? Riv. Immunol. Allergol. Pediatr. 2021, 35, 17–22. [Google Scholar]
- Maiello, N.; Giannetti, A.; Ricci, G.; Cinicola, B.; Carello, R.; Indolfi, C.; Caffarelli, C.; Marseglia, A.; Calvani, M.; Miraglia Del Giudice, M.; et al. Atopic dermatitis and atopic march: Which link? Acta Biomed. 2021, 92, e2021525. [Google Scholar] [CrossRef] [PubMed]
- Miraglia del Giudice, M.; Decimo, F.; Leonardi, S.; Maioello, N.; Amelio, R.; Capasso, A.; Capristo, C.; Capristo, A.F. Immune dysregulation in atopic dermatitis. Allergy Asthma Proc. 2006, 27, 451–455. [Google Scholar] [CrossRef]
- Simpson, A.; Brough, H.A.; Haider, S.; Belgrave, D.; Murray, C.S.; Custovic, A. Early-life inhalant allergen exposure, filaggrin genotype, and the development of sensitization from infancy to adolescence. J. Allergy Clin. Immunol. 2020, 145, 993–1001. [Google Scholar] [CrossRef] [PubMed]
- Sherenian, M.G.; Kothari, A.; Biagini, J.M.; Kroner, J.W.; Baatyrbek Kyzy, A.; Johannson, E.; Atluri, G.; He, H.; Martin, L.J.; Khurana Hershey, G.K. Sensitization to peanut, egg or pets is associated with skin barrier dysfunction in children with atopic dermatitis. Clin. Exp. Allergy 2021, 51, 666–673. [Google Scholar] [CrossRef] [PubMed]
- Panzer, A.R.; Sitarik, A.R.; Fadrosh, D.; Havstad, S.L.; Jones, K.; Davidson, B.; Finazzo, S.; Wegienka, G.R.; Woodcroft, K.; Lukacs, N.W.; et al. The impact of prenatal dog keeping on infant gut microbiota development. Clin. Exp. Allergy, 2023; ahead of print. [Google Scholar] [CrossRef]
- Tun, H.M.; Konya, T.; Takaro, T.K.; Brook, J.R.; Chari, R.; Field, C.J.; Guttman, D.S.; Becker, A.B.; Mandhane, P.J.; Turvey, S.E.; et al. Exposure to household furry pets influences the gut microbiota of infants at 3–4 months following various birth scenarios. Microbiome 2017, 5, 40. [Google Scholar] [CrossRef]
- Pavord, I.D.; Beasley, R.; Agusti, A.; Anderson, G.P.; Bel, E.; Brusselle, G.; Cullinan, P.; Custovic, A.; Ducharme, F.M.; Fahy, J.V.; et al. After asthma: Redefining airways diseases. Lancet 2018, 391, 350–400. [Google Scholar] [CrossRef]
Reference | Study Group | Study Type | Aim | Age of Outcome Assessment | Key Results |
---|---|---|---|---|---|
[22] | In the European Union Child Cohort Network, information was collected from 77,434 mother–child pairs from 9 birth cohorts. | Meta-analysis | To investigate whether early ownership of cats and dogs is associated with asthma in school-aged children. | The outcomes were evaluated in school-age children employing the International Study of Asthma and Allergy in Childhood (ISAAC) questionnaire. | No significant correlation was found between owning cats or dogs and the likelihood of developing asthma. The duration and the degree of ownership did not significantly affect these associations. Likewise, owning cats or dogs did not show a significant association with allergic sensitization specific to cats or dogs. However, there was a strong relation between allergic sensitization specific to cats or dogs and the presence of asthma in school-age children. |
[23] | Data from 1231 children born in 1996–1997 at Östersund Hospital in Sweden were collected. | Observational study | To determine the relationship between dog and cat ownership during and after the first year of life and the likelihood of sensitization and allergy symptoms at age 13. | At 13 years of age, diagnoses of dog and cat allergies and asthma were made based on parental reports of allergic symptoms in a sample size of 834 individuals. | Keeping a dog or a cat during the first 12 months of life was found to decrease the risk of sensitization to dog or cat allergens, respectively, as well as sensitization to birch and other allergens (Timothy, Cat, Birch, Horse, Dog, Soy, Wheat, Fish, Egg, Milk). Furthermore, owning a cat during and after the first year of life decreased the likelihood of developing cat allergies and hay fever. Dog ownership beyond the first year of life had no effect on allergic symptoms, however, having a dog at home during the first 12 months of life lowered the likelihood of developing dog and cat allergies. |
[24] | A randomized trial was conducted on 1303 infants aged three months to evaluate the prevention of food allergy. A survey was administered to determine pet ownership, and the patients were assessed for AD at the time of enrolment. | Randomized control study | To research how having a pet in the house might safeguard against food allergies. | Analyses of serum and skin were performed at 3 months, 1, and 3 years to evaluate sensitization to food and aeroallergens. Additionally, food allergy status was determined through double-blind, placebo-controlled food challenges conducted between 1 and 3 years of age. | Infants who lived with dogs exhibited a 90% lower likelihood of developing a food allergy. Notably, none of the 49 newborns who had at least two dogs in their household experienced food allergies, raising the possibility of a dose–response link. Specifically, for each additional dog owned, the odds of developing a food allergy decreased. However, no significant association was observed between owning dogs or cats and the development of AD. |
[25] | Data from Japan Environment and Children’s Study, including 97,413 mother–child dyads, were evaluated. | Prospective study | To investigate the impact of pet exposure on the likelihood of developing food allergies. | The prevalence of food allergy in pre-schoolers was assessed based on questionnaires. | Exposure to dogs or cats during fetal development or the first years of life reduced the chance of developing food allergies up to the age of 3. Specifically, dog ownership was associated with a lower risk of developing egg, milk, and nut allergies, while cat ownership was linked with a lower risk of developing wheat and egg allergies. |
[26] | Data from the Polish Mother and Child Cohort (REPRO_PL) were gathered. | Prospective study | The objective of the study was to investigate if early-life lifestyle variables and indoor allergen exposure affected a child’s chance of developing asthma, AD, and allergic rhinitis by the age of 10. | Data were collected at 10 years of age, using questionnaires during interviews. | Among the children included in the study, cat and dog allergens were the most commonly detected allergens in their homes, present in all of the households. A higher concentration of the cat allergen Fel d1 in house dust was found to be significantly associated with an increased risk of developing asthma at the age of 10 years. However, no significant associations were observed between allergen concentrations and the development of AD or allergic rhinitis. For AD and allergic rhinitis, no significant associations were observed. |
[27] | The Cohort for Childhood Origin of Asthma and Allergic Diseases was used to provide information. | Prospective study | To examine the relationship between dog ownership at any point between pregnancy and the age of 1 year and sensitivity to airborne allergens at ages 3 and 7, bronchial hyperresponsiveness (BHR), and asthma at age 7. | At 36 weeks of gestation, at delivery, at 6 months, at 1 year, and then once a year, regular follow-up visits for medical examinations and self-report questionnaires were carried out. At 3 and 7 years old, BHR and asthma were evaluated, as well as sensitization to aeroallergens. | No significant differences in sensitization to dogs at ages 3 and 7 were observed between children who owned dogs and those who did not. However, owning a dog during early life was found to reduce the risk of sensitization to aeroallergens at age 7. On the other hand, dog ownership was associated with a significant increase in the risk of nonatopic BHR. Furthermore, dog ownership was linked to the development of nonatopic asthma at 7 years of age. |
[28] | Parents of children aged 3 to 6 years (N = 3606) reported data on home environment and symptoms using ISAAC questionnaire in Taiyuan. The survey collected information on symptoms experienced during the first 2 years of life and symptoms reported within the past year. | Retrospective study | The study aimed to examine the reported appearance of childhood wheeze, rhinitis, and eczema symptoms concerning the prenatal, perinatal, and postnatal home environment. | Information on symptoms experienced during the first 2 years of life and symptoms reported within the past year were collected in preschool children. | The prevalence of wheezing and eczema was increased in households with dogs. |
[29] | The study involved the participation of children aged 3 to 6 years from daycare centers in seven Chinese cities, with a total sample size of 39,782 children. Parents of children completed a questionnaire regarding the home environment and their children’s health, which included questions about rhinoconjunctivitis and wheezing in the presence of furry pets, as well as diagnosed rhinitis. Additionally, data from monitoring stations were used. | Retrospective study | To investigate how early-life exposure to hairy pets affects a child’s respiratory symptoms. | Outcomes were evaluated in preschool children aged 3 to 6 years. | Children who lived in rural or suburban regions and whose mothers worked as farmers during pregnancy had lower rates of other diagnosed rhinitis (unrelated to furry pets). Both perinatal and postnatal ownership of dogs and cats were associated with symptoms related to furry pets and diagnosed rhinitis specifically related to furry pets. In contrast, owning cats and dogs appeared to have a protective effect against other forms of diagnosed rhinitis. |
[30] | Data from Shanghai Allergy Cohort were collected. Information on furry pet ownership was collected through questionnaires. | Prospective study | To research how having pets early in life affects children’s pet AD and sensitization. | Pet sensitization and AD were diagnosed at 5 years old. | Domestic pet ownership during infancy and preschool years was positively linked with a higher risk of dog sensitization. A greater risk of AD at age 5 was inversely related to pet ownership during infancy. |
[31] | Information from 3781 children, including in the Finnish Type 1 Diabetes Prediction and Prevention (DIPP) Nutrition Study, was collected at age 5 using ISAAC questionnaire. Data on allergic disease and asthma and exposure to pets during the first 12 months of life were gathered. | Retrospective study | To examine whether exposure to farm and indoor pets in infancy affects the chance of developing asthma and allergies by age 5. | Asthma and allergy were assessed by age 5. | Asthma, allergic rhinitis, and atopic sensitization risk were found to be inversely correlated with the presence of dogs in the home. On the other hand, owning a cat was linked to a lower chance of developing atopic eczema. |
[32] | From birth through to age 2 years, 108 mother–child couples included in the Kingston Allergy Birth Cohort were monitored. | Prospective study | To assess the impact of exposure to seven air pollution variables during pregnancy and the first 2 years of life on allergy sensitization. | A skin prick test (SPT) was performed on the 2-year-old children. | Exposure to cats during the 6-month period resulted in a significant increase in the OR of having a positive SPT result. No statistically significant associations between a positive SPT and dog exposure were found. |
[33] | 539 mother–child pairs included in the study were part of the Polish Mother and Child Cohort (REPRO_PL), a multicentre prospective cohort established in 2007. Mothers in each trimester of pregnancy and 1 year after childbirth completed a questionnaire on animal exposure. | Prospective study | To evaluate the association between prenatal and postnatal exposure to pet ownership and the development of AD, food allergy, and wheezing in children at the ages of 1 and 2. | Children’s health status was assessed at around one year and two years of age. | Keeping a dog at home before and during pregnancy decreased the risk of food allergy in the first year of life. On the other hand, keeping any animal other than a dog (cat, hamster, guinea pig, or rabbit) before and during pregnancy increased the risk of food allergy in the first year of life for children. |
[34] | Records from 23585 Swedish children born from 2001 to 2004 were collected from national register. | Retrospective study | To evaluate if dog housekeeping during the first 12 months of life and different dog characteristics reduce the risk of asthma among school-age children. | The outcomes were evaluated at age 6. | Living with female dogs during the first year of life was associated with a lower risk of developing asthma compared to male dogs. Additionally, children who had 2 or more dogs had a decreased chance of asthma compared to those with only one dog. |
[35] | Data from 756 children, aged 6–7, about exposure to dogs and cats and allergic diseases were collected with the ISAAC questionnaire. | Cross-sectional retrospective study | To analyze the influence of early exposure to dogs or cats on the prevalence of asthma and allergy among school-aged children. | Data regarding the prevalence of allergic diseases were collected at the age of 6–7 years old. | Exposure to dogs, whether indoors or outdoors, showed a significant association with a reduced prevalence of AD. On the other hand, exposure to outdoor cats was linked to nocturnal coughing and ongoing rhinitis. |
[36] | Parental reports of 7360 children from birth to 8 years old in China were analyzed, using the ISAAC questionnaire. | Retrospective study | To find the relationship between pet keeping (cat, dog, rodent, bird, or fish) and asthma and allergy in infancy and childhood. | ISAAC questionnaire was used to assess the association between allergy and early-life pet exposure in children aged 0–8 years old. | Keeping pets, especially cats, was a notable risk factor for diagnosed asthma and AD. Exposure to a pet in early childhood notably heightened the risk of experiencing current wheeze, current dry cough, and diagnosed rhinitis. Even after accounting for avoidance behavior, the adverse impact of pet keeping on children’s health became even more evident. A dose–response relationship was observed between pet keeping and the prevalence of current wheeze and eczema. |
[37] | Data from 442 children belonging to a birth cohort of high-risk inner-city children were collected to examine the effects of prenatal and early-life factors on the risk of asthma in school-age individuals. | Prospective study | To discover early-life environmental risk factors for asthma in children. | Data were analyzed at 7 years of age. | In the first 3 years of life, a decreased asthma risk was linked to higher levels of cockroach, mouse, and cat allergens in household dust. |
[38] | Two Sweden cohorts were examined (n = 1029, n = 249). The first cohort consisted of 7- to 8-year-old children. The second cohort was a birth cohort. Data regarding asthma and allergy were collected through validated questionnaires in school-age children. | Cross-sectional and retrospective study | To determine if keeping cats and dogs throughout the first year of life was associated in a dose-dependent manner. | The onset of allergy and asthma disease was evaluated in school-age children (7–9 years old) | Between individuals without pets and those with five or more pets, the prevalence of allergy drastically dropped from 49 to 0%. Similarly, the prevalence of allergy in the last year decreased from 32% to zero with an increasing number of pets. |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Indolfi, C.; D’Addio, E.; Bencivenga, C.L.; Rivetti, G.; Bettini, I.; Licari, A.; Manti, S.; Mori, F.; Miraglia del Giudice, M.; Klain, A. The Primary Prevention of Atopy: Does Early Exposure to Cats and Dogs Prevent the Development of Allergy and Asthma in Children? A Comprehensive Analysis of the Literature. Life 2023, 13, 1859. https://doi.org/10.3390/life13091859
Indolfi C, D’Addio E, Bencivenga CL, Rivetti G, Bettini I, Licari A, Manti S, Mori F, Miraglia del Giudice M, Klain A. The Primary Prevention of Atopy: Does Early Exposure to Cats and Dogs Prevent the Development of Allergy and Asthma in Children? A Comprehensive Analysis of the Literature. Life. 2023; 13(9):1859. https://doi.org/10.3390/life13091859
Chicago/Turabian StyleIndolfi, Cristiana, Elisabetta D’Addio, Chiara Lucia Bencivenga, Giulio Rivetti, Irene Bettini, Amelia Licari, Sara Manti, Francesca Mori, Michele Miraglia del Giudice, and Angela Klain. 2023. "The Primary Prevention of Atopy: Does Early Exposure to Cats and Dogs Prevent the Development of Allergy and Asthma in Children? A Comprehensive Analysis of the Literature" Life 13, no. 9: 1859. https://doi.org/10.3390/life13091859
APA StyleIndolfi, C., D’Addio, E., Bencivenga, C. L., Rivetti, G., Bettini, I., Licari, A., Manti, S., Mori, F., Miraglia del Giudice, M., & Klain, A. (2023). The Primary Prevention of Atopy: Does Early Exposure to Cats and Dogs Prevent the Development of Allergy and Asthma in Children? A Comprehensive Analysis of the Literature. Life, 13(9), 1859. https://doi.org/10.3390/life13091859