Distinct healthy and atopic canine gut microbiota is influenced by diet and antibiotics

Abstract

The rising trend in non-communicable chronic inflammatory diseases coincides with changes in Western lifestyle. While changes in the human microbiota may play a central role in the development of chronic diseases, estimating the contribution of associated lifestyle factors remains challenging. We studied the influence of lifestyle-diet, antibiotic use, and residential environment with housing and family-on the gut microbiota of healthy and owner-reported atopic pet dogs, searching for associations between the lifestyle factors, atopy and microbiota. The results showed that atopic and healthy dogs had contrasting gut microbial composition. The gut microbiota also differed between two breeds, Labrador Retriever and Finnish Lapphund, selected for our study. Among all lifestyle factors studied, diet was most significantly associated with gut microbiota but only weakly with atopic symptoms. Thus, diet- and atopy-associated changes in the microbiota were not interrelated. Instead, the severity of symptoms was positively associated with the usage of antibiotics, which in turn was associated with the microbiota composition. Urban lifestyle was significantly associated with the increased prevalence of allergies but not with the gut microbiota. Our results from pet dogs supported previous evidence from humans, demonstrating that antibiotics, gut microbiota and atopic manifestation are interrelated. This congruence suggests that canine atopy might be a promising model for understanding the aetiology of human allergy.

Keywords: Western lifestyle; allergic diseases; canine model; diet; gut microbiome; pet dogs.

Figure 1.

Relationships between breed, allergic symptoms and microbiota. (a) Compositional variation in microbiota between healthy and atopic Finnish Lapphund and Labrador Retrievers studied by distance-based redundancy analysis that used dogs' atopy status (atopic or healthy) and breed as constraining factors, and Bray–Curtis index to measure sample-wise differences. The ellipses show 0.75 confidence intervals of the group centroids. (b) Differently abundant (p ≤ 0.05) bacterial OTUs between healthy and atopic individuals. For visualization, CSS normalized OTU abundances were transformed by natural logarithm. Prevotella_9 (Otu 66) was marginally significant (p = 0.11) but the pattern between atopic and healthy was distinct.

Figure 2.

The gut microbiota of Finnish Lapphunds in relation to diet. (a) Changes in microbiota, which were due to differences in the content of non-heat-processed low-carbohydrate raw (NHeP-LC-R) items in dogs’ diet, were determined by distance-based redundancy analysis. Bray–Curtis index was used to measure sample-wise differences in the microbiota. The ellipses show 0.75 confidence intervals of the group centroids. The effects of other dietary factors such as probiotics, fats and heat-processed high-carbohydrate moist food on microbiota were minor but were taken into consideration. In practice, residual variation remaining from the fitting of these background factors were constrained by the percentage of NHeP-LC-R food. (b,c) Differently abundant (p < 0.05) OTUs that increased concurrently with the content of (b) heat-processed high carbohydrate dry (HeP-HC-D) items and (c) NHeP-LC-R items in diet. The colours of three groups are the same as in panel (a). Mean abundances of OTUs are based on the square-root-transformed CSS-normalized read counts.

Figure 3.

The gut microbiota of atopic and healthy Labrador Retrievers in relation to diet and antibiotic use. Compositional variation in microbiota was constrained by distance-based redundancy analysis that used severity of symptoms as an explanatory variable and Bray–Curtis index to measure sample-wise differences in the microbiota. An increasing size of a symbol indicates more severe atopy symptoms of the corresponding dog. Collinear factors, i.e. the percentage of non-heated low carbohydrate raw (NHeP-LC-R) items in dogs' diet and especially use of antibiotics increased along with the atopy symptoms.