Pet rabbits and guinea pigs can be potential vehicles for zoonotic or allergenic fungi to their tutors. Results revealed that the cutaneous mycobiota of the rabbits and guinea pigs under study was mainly composed by environmental filamentous saprophytic fungi and yeasts, as described in other studies performed in these animal species (6, 7, 21, 22), as well as in others, such as dogs and cats (21, 22, 25–32). Saprophytic fungi were expected to be found in these animals because of their permanent contact with organic matter present in the hay, food and substrate and with the environment. The yeast species identified were also expected, as they are commensals of animals and humans microbiota (Candida) (33) or humid environments (Rhodotorula) (34). As far as we know, this study allowed the isolation of three fungal genera in rabbits and guinea pigs for the first time, namely Chaetomium sp., Phoma sp. and Rhodotorula sp., which were already isolated from dogs and cats (25, 26, 29, 30, 35).
It was not possible to isolate dermatophytes from the animals under study; however, the other fungi identified were already reported as responsible for cutaneous lesions in humans, dogs and cats. In humans, Aspergillus sp., Alternaria sp., Candida sp., Chaetomium sp., Cladosporium sp., Mucor sp., Penicillium sp., Phoma sp., Rhizopus sp. and Scopulariopsis sp. have been reported to be responsible for cutaneous infections (36–42). In dogs and cats, Alternaria sp., Aspergillus sp., Candida sp., Cladosporium sp., Mucor sp. and Penicillium sp. have also been reported as responsible for cutaneous infections (36, 43–46). Most of them were not previously associated with infections in pet rabbits and guinea pigs, except for Aspergillus sp., that was already related with cutaneous infections in rabbits (12). However, it is important to refer that Scopulariopsis sp. was isolated from one animal under study, which had alopecia and crusting lesions on the extremities. Several factors need to be taken into consideration before relating this species to infection, namely the concentration of isolated fungi, the clinical status of the animal and the possibility of contamination of the sample or culture (47). Although the hypothesis of colonization of a pre-existing wound cannot be ruled out, results seem to indicate that this fungus may have been responsible for this lesion, especially since its association with lesions very similar to dermatophytosis in humans has been described (41). In fact, identified species may have the ability to cause disease in rabbits and guinea pigs, not only in animals with immunosuppression or deficient nutritional status, but also in healthy individuals after abrasive or perforating injury (36). Therefore, veterinarians should consider non-dermatophytic fungal infections as a differential diagnosis for cutaneous lesions.
Many of the variables under study are frequently referred as predisposing factors for dermatophytosis in guinea pigs and rabbits (4). Dermatophytes were not isolated, but the association between positive mycological cultures and number of fungal species isolated with several independent variables was evaluated.
It was possible to observe that samples collected from guinea pig are likely to originate cultures with a higher number of fungal species than those from rabbits, which seems to indicate that the self-cleaning habits of guinea pigs are less efficient than the ones from rabbits; also, unlike rabbits, mutual grooming is less frequent between different guinea pigs (48). Self-cleaning allows the maintenance of animal hygiene by removing dirt and parasites (49). If not performed, the skin surface presents a higher probability of fungi colonization and dermatological disease development, which may also explain the higher tendency of guinea pigs for dermatophytosis (4, 6, 8, 20, 21, 50). In fact, a study in cats with dermatophytosis reported that collared cats show more generalized lesions comparing with animals without Elizabethan collar that could perform their self-cleaning, suggesting that the cleaning behaviour may limit the development of lesions (51).
Age was found to be related with positive mycological cultures. Older animals may suffer from diseases that could impair cleaning behaviours, such as dental disease associated with oral pain, or musculoskeletal disorders that reduce mobility and cause pain (52, 53).
Regarding outdoor access, it was already reported that fungal species present in cats’ hair may vary depending on the environment (54). Considering that the organic matter present in gardens and backyards constitutes a relevant substrate for saprophytic fungi, it is expected that samples collected from animals with outdoor access to originate cultures with a higher number of fungal species.
Prolonged antimicrobial therapy can influence the composition of the commensal microbiota of mucosa and facilitate yeast proliferation (33), being reported that the skin and hair microbiota may vary according to the immune state (54). In this study, samples from animals which were under drug therapy (anti-inflammatory, antinematodal drugs and antibiotic) presented a higher probability of originating positive cultures. These animals were mainly diagnosed with advanced dental disease or presented neurological signs compatible with Encephalitozoon cuniculi. These two situations generally promote a decrease in body condition, poor nutritional status, and an altered degree of activity (51–53), which may explain this result.
Concluding, this is the first study regarding cutaneous mycobiota of pet rabbits and guinea pigs performed in Portugal. Despite of not being possible to isolate dermatophytes, results showed that these animals can carry several filamentous fungi and yeasts in their hair and skin. Three of these genera were isolated for the first time in these animals, namely Chaetomium, Phoma and Rhodotorula. All the isolated fungi are frequently present in the environment and usually do not cause disease. However, infections related with most of the identified fungi were already described in animals and humans, especially in immunocompromised individuals. Therefore, these animals can represent a zoonotic risk, which may be related with animals age, species, ongoing medication and outdoor access.