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Zoonoses and Public Health

SHORT COMMUNICATION

Survey of Zoonotic Dermatoses in Client-Owned Exotic Pet


Mammals in Southern Italy
D. d’Ovidio1 and D. Santoro2
1
Private Practitioner, Napoli, Italy
2
Department of Veterinary Clinical Medicine, University of Illinois at Urbana-Champaign, Urbana, IL, USA

Impacts

• Several ‘exotic’ mammalian species (e.g. rabbits, rodents, ferrets and


hedgehogs) live in close proximity to humans as companion pets.
• Exotic pet mammals may serve as active carriers for many highly contagious
pathogens with zoonotic potential.
• An active routine screening examination and preventative treatments are
strongly recommended for every newly purchased pet mammal.

Keywords: Summary
Exotic pet mammals; zoonotic dermatoses;
parasitic and fungal infections Several ‘exotic’ mammalian species (e.g. rabbits, rodents, ferrets and hedge-
hogs) live in close proximity to humans as companion pets. Skin diseases (SD)
Correspondence: are frequent causes of morbidity in exotic pet mammals, and most of those
D. Santoro. Department of Small Animal SDs have a zoonotic potential. The purpose of this study was to determine the
Clinical Sciences, University of Florida,
frequencies and types of zoonotic dermatosis (ZD) in client-owned, exotic pet
Gainesville, FL, USA. Tel.: +1 352 392 2235;
mammals in Southern Italy. Six-hundred and fifty-five medical records of exo-
Fax: +1 352 846 2445;
E-mail: dsantoro@ufl.edu
tic pet mammals examined between 2011 and 2012, across twenty private prac-
tice veterinary clinics around the Naples area (Italy), were retrospectively
Received for publication March 23, 2013 evaluated and screened for animals diagnosed with SDs (rabbits n = 455, gui-
nea pigs n = 93, ferrets n = 64, hedgehogs n = 19, chinchillas n = 13 and rats
doi: 10.1111/zph.12100 n = 11). The records of animals diagnosed with SD, whose causative agents
had a zoonotic potential, were selected for analysis. The Mann–Whitney inde-
pendent test was used for statistical analysis. A P value ≤0.05 was considered
statistically significant. Eighty-two records (12.5%) of animals with ZD were
identified. Of those, 56.1% (46/82) were affected by fungal infections and
42.7% (35/82) by parasitic infections. No zoonotic bacterial or viral infections
were diagnosed. Dermatophytosis was significantly diagnosed more frequently
in younger animals. The results of this survey indicate that exotic pet mam-
mals may serve as active carriers for many highly contagious pathogens with
zoonotic potential. Awareness and vigilance by the veterinary practitioner is
crucial in the prevention of occurrences of ZDs. Children frequently come in
close contact with exotic pets. To prevent the unplanned transmission of path-
ogen from pet to human, an active routine screening examination and preven-
tative treatments are strongly recommended for every newly purchased pet
mammal.

dermatoses with zoonotic potential and zoonotic derma-


Introduction
tosis (ZD) have a high health impact on the pet owner
Exotic companion mammals (e.g. rabbits, rodents, ferrets, population (Scott and Horn, 1987; Hoppmann and Bar-
hedgehogs) are very popular household pets. As with ron, 2007; Kim et al., 2008; Rosen, 2011; Mitchell and
dogs and cats, they are a potential source of zoonotic Tully, 2012).
infections transmissible to their owners (Mitchell and The most common zoonoses with dermatological mani-
Tully, 2012). It has been previously demonstrated that festation in exotic companion mammals include parasitic

100 © 2014 Blackwell Verlag GmbH  Zoonoses and Public Health, 2015, 62, 100–104
D. d’Ovidio and D. Santoro Exotic Pet Mammals Skin Diseases with Zoonotic Potential

(Cheyletiella parasitovorax, Leporacarus gibbus, Trixacarus medical records of exotic pet mammals with SD in which
caviae, Sarcoptes scabiei, Notoedres cati and Otodectes cyno- zoonotic potential aetiologies were proven were selected for
tis) and fungal infections (Trichophyton mentagrophytes and analysis. Cases with ZD were included only if information
Microsporum spp.). While not as common, bacterial (Staph- on the cutaneous and systemic clinical signs, as well as a
ylococcus aureus, Salmonella spp., Corynebacterium kutscheri definitive diagnosis of ZD, was documented in the patients’
and Francisella tularensis) (Beck and Pfister, 2006; Hill and records. From each medical record, the following data were
Brown, 2011; Pignon and Mayer, 2011; Rosen, 2011; Mitch- retrieved and analysed: sex, weight, age of onset of ZD,
ell and Tully, 2012) and viral infections (monkeypox virus general husbandry and feeding history.
and cowpox virus) have also been reported (Souza, 2011;
Mitchell and Tully, 2012).
Statistical analysis
Transmission of ZD from pets to humans primarily
occurs through direct contact with infected animals, but Median, range and the lowest and highest values were cal-
also by a contaminated environment or through ectopara- culated for all data sets. The Mann–Whitney independent
sites serving as vectors. The most common clinical signs, of test was used for the statistical analysis of age and weight.
the above-mentioned ZD in people, include vesicular or Ninety-five per cent confidence intervals (CI) were calcu-
papular dermatitis, wheals, localized pruritus, alopecia and lated. The chi-squared test was used for the statistical analy-
crusts (Mitchell and Tully, 2012). Dermatological signs sis of the mammals’ sex. Differences with a value of
associated with systemic manifestations (systemic hypereo- P ≤ 0.05 were considered statistically significant. Age, sex
sinophilia) have also been reported (Dobrosavljevic et al., and weight were the variables analysed in both groups
2007). (infected versus non-infected). The variables were analysed
To the authors’ knowledge, no epidemiological studies for each species to facilitate the interpretation of the data.
to determine the risk of zoonotic potential transmission Statistical analyses were performed using MEDCALC 12.0 sta-
from pet mammals to humans have been published. To tistical software (MedCalc Software, Mariakerke, Belgium).
address this lack of information, the purpose of this survey
was to evaluate the frequency and types of ZDs present in
Results
exotic companion mammals in Southern Italy.
All data for the animals included in this study are reported
in Table 1.
Materials and Methods
Medical records for 82 exotic pet mammals diagnosed
Study population with ZD were selected and analysed. Parasitic ZD occurred
Six-hundred and fifty-five medical records of exotic pet in 42.7% (35/82) of cases. Of those cases with parasitic ZD,
mammals seen across 20 private veterinary clinics around 51.4% (18/35) were pet rabbits in which the following para-
the Naples, Italy, area from 2011 to 2012 were retrospec- sites were identified: C. parasitovorax (12/18), L. gibbus (4/
tively reviewed. The exotic pet mammals included rabbits 18), S. scabiei (2/18). Ferrets comprised 25.7% (9/35) of
(Oryctolagus cuniculus) n = 455, guinea pigs (Cavia porcel- the cases with parasitic ZD, in which the following parasites
lus) n = 93, ferrets (Mustela putorius furo) n = 64, hedge- were identified: O. cynotis (5/9) and S. scabiei (4/9).
hogs (Ateletrix albiventris) n = 19, chinchillas (Chinchilla Twenty per cent (7/35) of cases with parasitic ZD were gui-
lanigera) n = 13 and rats (Rattus norvegicus) n = 11. The nea pigs, and all were infested by T. caviae. 2.9% (1/35) of

Table 1. Details of 82 exotic pet mammals diagnosed with zoonotic dermatosis (ZD) in Southern Italy

Sex
a
Total No. of No. of cases No. of cases No. of Average Average
Species cases enrolled affected parasites cases fungi age (years) weight (kgs) M F

Rabbits 455 33 18 15 2.2 1.5 20 13


Guinea pigs 93 30 7 23 1.5 0.7 12 18
Ferrets 64 12 9 3 1.5 1.0 4 8
Hedgehogs 19 1 1 0 1 0.4 0 1
Chinchillas 13 4 0 4 1.4 0.5 3 1
Rats 11 1 0 1 0.6 0.3 1 0
Total 655 82 35 46

F, female; M, male.
a
Age of animals when the skin disorder was diagnosed.

© 2014 Blackwell Verlag GmbH  Zoonoses and Public Health, 2015, 62, 100–104 101
Exotic Pet Mammals Skin Diseases with Zoonotic Potential D. d’Ovidio and D. Santoro

parasitic ZD were hedgehogs with only one case of N. cati hogs) represent one of the primary environmental host for
diagnosed. Compiling the results from all animals, the most dermatophytes as they can be asymptomatic carriers for
common parasites were C. parasitovorax (14.9%) and T. mentagrophytes (Chomel et al., 2007; Rovid-Spickler
T. caviae (8.6%), followed by S. scabiei (7.4%), O. cynotis and Dvorak, 2008; Kraemer et al., 2012). Asymptomatic
(6.2%), L. gibbus (4.9%) and N. cati (1.2%). Age was not exotic pet mammals represent a source for fungal infec-
statistically associated with parasitic SD in any of the tions in people where heavily colonized, even if the con-
species analysed. tact time is very short (Rosen and Jablon, 2003; Riley and
Fungal ZD occurred in 56.1% (46/82) of reviewed cases. Chomel, 2005).
Of those cases with fungal ZD, 50% (23/46) were guinea The age of onset was analysed to determine whether
pigs, 32.6% (15/46) were rabbits and 8.7% (4/46) were there was a statistically significant association between the
chinchillas. In all cases, T. mentagrophytes was the only der- age of animal and the development of fungal diseases. We
matophyte identified. The remaining 8.7% were composed found that dermatophytosis was more prominent in young
of ferrets [6.5% (3/46)], in which both Microsporum spp. animals. This finding fits with current immunological
(2/3) and T. mentagrophytes (1/3) were identified. 2.2% (1/ trends, as it is well known that younger and sick animals
46) were rats affected by dermatophytosis due to Microspo- are more pre-disposed to be affected by infectious diseases
rum spp. Compiling the results from all enrolled animals, (Moriello, 2003; Hess and Tater, 2012).
the most common dermatophyte identified was T. mentag- In this study, the most common parasitic ZD was chey-
rophytes (53.1%), whereas Microsporum spp. occurred only letiellosis (14.9%). C. parasitovorax is a common parasite
in 3.7% of cases. The age of animals infected with a derma- in rabbits, but can affect any mammalian species. In rab-
tophyte was significantly less (younger) than animals not bits, C. parasitovorax can cause subclinical disease or, more
infected with a dermatophyte [median ages: 0.7 (CI = 0.5– frequently, signs of pruritic dermatitis associated with scal-
0.77) versus 3.2 (CI = 3–3.6) years (rabbit) (P < 0.0001), ing, alopecia or broken hairs in several regions of the rab-
1.6 versus 3.6 (CI = 2.6–5.7) years (chinchillas) (P = bit’s body. In people, a large number of infestations by
0.0054), and 0.5 versus 2.4 (CI = 2–3) years (ferret) Cheyletiella spp. have been documented (Wagner and Stall-
(P = 0.0036)]. meister, 2000; Dobrosavljevic et al., 2007; Jofre et al.,
No bacterial or viral ZD was reported. Both sex and 2009), and it is estimated that in households with infested
weight were not statistically associated with the develop- animals, 20% of pet owners are also infected (Wagner and
ment of SD in any of the species analysed. Stallmeister, 2000). However, because the mites adopt the
commonly termed ‘bite and run’ behaviour, by biting peo-
ple and returning rapidly to their animal host, it is often
Discussion
difficult to find them on human patients (Wagner and
The results from the data reviewed in this survey indicate Stallmeister, 2000). Main clinical signs in people include
that the prevalence of ZD in exotic pet mammals in South- pruritus, erythematous papules, papulovesicles, urticaria,
ern Italy is 12.5%. The most common aetiological agent vesiculobullous eruptions and excoriations usually on fore-
was T. metagrophytes followed by C. parasitovorax. The arms, chest and abdomen (Parish and Schwartzman, 1993;
only ZDs observed in this study were parasitic and fungal Wagner and Stallmeister, 2000). Rarely, cheyletiellosis is
dermatoses involving all the species enrolled. Bacterial and also associated with severe and persistent peripheral eosino-
viral dermatoses were not present in any of the enrolled philia (Dobrosavljevic et al., 2007).
cases. The second most common parasitic ZD in this survey
Superficial fungal infections were the most common was caused by T. caviae followed by S. scabiei. In guinea
types of ZD identified in this study. Fungal infections were pigs, the main clinical signs include intense pruritus, alope-
diagnosed in 56.1% of the cases. T. mentagrophytes was cia, crusting and unthrifty-looking coat. Similarly, pruritic
the most prevalent dermatophyte isolated in almost all lesions produced in pets are also the main clinical signs
species analysed, whereas Microsporum spp. occurred only reported in people, predominantly children (Mitchell and
in 3.7% of the cases. Both of the fungi isolated are com- Tully, 2012). In both ZDs, T. caviae and S. scabiei, regular
monly diagnosed in both people and animals. They are routine clinical examination of the pet and a regular anti-
keratinophilic fungi affecting the stratum corneum, hair parasitic treatment is fundamental for the prevention of
shafts and nails (Canny and Gamble, 2003; Rosen, 2011). T. caviae or S. scabiei infections. In fact, due to the high
Dermatophytosis is considered one of the most common rate of false-negative skin scrapings, a definitive diagnosis
and important zoonotic skin diseases worldwide (Moriello, of T. caviae or S. scabiei can be highly challenging for both
2003). The prevalence of dermatophytosis in people is veterinarians and physicians (Aydıng€ oz and Mansur, 2011).
unknown as the disease is not reportable. Exotic compan- Proper pet examinations and preventative treatment are
ion mammals (rabbits, guinea pigs, chinchillas, hedge- most crucial for S. scabiei, as human scabies is a common

102 © 2014 Blackwell Verlag GmbH  Zoonoses and Public Health, 2015, 62, 100–104
D. d’Ovidio and D. Santoro Exotic Pet Mammals Skin Diseases with Zoonotic Potential

public health concern worldwide with an estimated


Source of Funding
300 million infected individuals (Burkhart, 2006).
Otodectes cynotis was detected in 6.2% of the animals in This study was self-funded.
this survey. This parasite is not host specific and may
affect many species of pets such as dogs, cats, rabbits,
Conflict of Interest
rodents and ferrets causing mild to severe otitis and pru-
ritic dermatitis. Occasional human infections have also None declared.
been reported, and primary signs included pruritic papu-
lar lesions on the skin or even true otic parasitic infesta-
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