Allergies are prevalent in both humans and dogs, with higher incidence in urban settings. This urban-rural disparity is hypothesized to be linked to differences in microbial exposures. While previous research demonstrated an association between urban living and allergy risk in both species, the potential for shared microbial factors contributing to this risk in cohabiting dogs and owners remained unexplored. This study aimed to investigate this gap by examining skin and gut microbiota composition, along with lifestyle and environmental factors, in a large cohort of dog-owner pairs. The study hypothesized that shared living environments, lifestyles, and microbial exposures would similarly influence the risk of allergic traits in both dogs and their owners. The rationale behind this hypothesis stemmed from observations that various protective factors against allergies (frequent contact with other animals, larger family size) are believed to increase exposure to beneficial microbes, typically found in rural and farming environments. Furthermore, prior studies had indicated that dogs and humans with allergic symptoms exhibit distinct microbiota profiles compared to healthy individuals, suggesting a potential link between microbiota composition and allergic disease development. The unique contribution of this study lies in the simultaneous investigation of these factors in cohabiting dogs and their owners, allowing for a more comprehensive understanding of the interplay between environmental, lifestyle, and microbial influences on allergic disease susceptibility.

Existing literature indicates a strong correlation between urban living and increased allergy risk in both humans and dogs. Studies have highlighted the protective role of exposure to diverse microbial communities found in rural or farming environments. These environments often provide exposure to a range of beneficial microbes which are thought to modulate immune responses and reduce the risk of developing allergic diseases. In humans, factors like limited contact with farm animals, small family size, and Westernized diets have been linked to a higher risk of allergies. Conversely, in dogs, frequent exposure to other animals and larger family sizes have been associated with a decreased risk. These observations suggest that similar environmental factors may trigger comparable allergic responses across mammalian species. Several studies have shown that allergic dogs and humans display distinct skin and gut microbiota compared to healthy counterparts. These differences in microbial composition further strengthen the hypothesis that microbial exposures play a crucial role in allergy development.

This study utilized a cohort of 168 dog-owner pairs. Owners were recruited through Finnish Lapphund and Labrador Retriever breeders. Data collection included questionnaires on lifestyle, environment, and owner-reported allergic symptoms in both dogs and owners. Skin samples (inner side of front leg for dogs, volar forearm for owners) and fecal samples were collected. DNA was extracted from skin and gut samples for 16S rRNA gene sequencing to characterize microbiota composition. Aeroallergen sensitization in humans was assessed using Phadiatop tests. Allergy in dogs was based on the severity of owner-reported symptoms (a validated questionnaire was used because IgE levels in dogs don’t correlate well with symptom severity). Data were processed using established bioinformatic pipelines, including OTU clustering and annotation, contaminant removal, and normalization. Living environment and lifestyle data were simplified using PCA and PCoA, respectively. Statistical analyses included logistic regression (to assess the association between allergic traits and environmental factors), PERMANOVA (to compare microbiota diversity and structure across groups), Random Forest Regression (to predict environmental and lifestyle factors from microbiota data), and Bayesian source tracking (to determine the shared microbial components between dogs and owners). Ethical approvals were obtained from relevant committees before data collection.

The study revealed a significant association between urban living and increased risk of allergic symptoms in both dogs and their owners. Approximately 31% of owners showed aeroallergen sensitization, while about 20% of dogs exhibited owner-reported allergic symptoms. Logistic regression revealed a statistically significant association between urban living and owner-reported allergy in dogs (p=0.003) and a borderline association in humans (p=0.054). Similar associations were observed for lifestyle. Dogs and owners tended to be concurrently allergic or healthy; an allergic dog was more likely to have a sensitized owner, and vice versa. Analysis of microbiota data showed that skin microbiota, but not gut microbiota, was partially shared between dogs and their owners. Urban environments led to a homogenization of skin microbiota in both species. Random Forest Regression showed a stronger association between skin microbiota and living environment in dogs than in humans. While no universally shared bacterial taxa were found that correlated with allergic traits in both species, specific taxa linked to living environment and lifestyle differed between allergic and healthy individuals within each species. For example, Rhodopseudomonas (urban-associated) was enriched in allergic dogs, while Actinoplanes (rural lifestyle-associated) was enriched in healthy dogs. Source tracking indicated that urban lifestyle increased the proportion of human skin bacteria on dogs’ skin.

This study's findings support the hypothesis that environmental factors, particularly those related to microbial exposures, influence allergy development in both dogs and humans. The significant associations between urban living/lifestyle and allergy risk in both species, coupled with the homogenization of skin microbiota in urban environments, highlight the role of environmental microbial exposures. However, the lack of shared bacterial taxa universally associated with allergy in both species suggests that other factors, beyond shared microbial exposures, also contribute to the observed co-occurrence of allergic traits in dogs and owners. Differences in skin physiology and immune tolerance between dogs and humans likely account for the species-specific differences in allergy-associated taxa. The study’s observation of higher diversity in dog skin microbiota supports the idea that dogs act as microbial reservoirs in the home environment. The findings suggest that environmental microbes carried on dog fur/skin might exert stronger immuno-regulatory effects than solely resident dog-skin microbes. The increased proportion of human-associated skin microbes on allergic dogs could indicate reduced exposure to environmental microbes in urban or indoor environments.

This study provides evidence supporting the role of environmental factors, including microbial exposures, in the development of allergic traits in both dogs and their owners. Urban environments and lifestyles associated with reduced microbial diversity are linked to increased allergy risk in both species. While a partially shared skin microbiota was observed, the lack of universally shared allergy-associated taxa highlights the complexity of the allergy-microbiota relationship and the potential for other factors to play a role. Future research could focus on identifying specific microbial metabolites or pathways influencing immune responses and examining the role of other environmental factors beyond microbial exposures.

The study's relatively small number of allergic individuals might have limited statistical power. The reliance on owner-reported symptoms for diagnosing allergies in dogs, while using a validated questionnaire, could introduce some bias. Potential confounding factors, such as diet and medication in humans, and other environmental factors like air pollution, were not fully addressed in this study. Finally, participation bias might have influenced the results, although the participation rate was reasonably high.