- The incidence of clinical fungal disease is low in the small mammal patient, however Trichophyton mentagrophytes is the most common cause of dermatitis in these species.
- Fungal pathogens are generally more important for their zoonotic potential. Rodents are frequently asymptomatic carriers of ringworm, and transmission of disease to human caretakers is not uncommon.
Dermatophytosis is a superficial invasion of the stratum corneum. Infection is usually confined to the skin, fur, and nails (Fig 1). Although the overall incidence of disease is low, dermatophytes are the most important fungal pathogen of small mammals. Certain genetic lines may be predisposed to the development of dermatophytosis, and the incidence of disease may also increase with stressors such as overcrowding, heat, humidity, ectoparasitism, old age, youth, and/or pregnancy.
Among rodents, dermatophytosis or ringworm is most commonly reported in the guinea pig (Cavia porcellus). Reports are uncommon in the rat (Rattus norvegicus), chinchilla (Chinchilla laniger), prairie dog (Cynomys ludovicianus), and mouse (Mus musculus) although occasional outbreaks do occur. There are also sporadic reports in the ferret (Mustela putorius furo), European hedgehog (Erinaceus europaeus) and European rabbit (Oryctolagus cuniculus). Ringworm is extremely rare in the golden hamster (Mesocricetus auratus) and Djungarian hamster (Phodopus sungorus), and there are no reports of naturally occurring or experimental disease in the Mongolian gerbil (Meriones unguiculatus).
The most common cause of ringworm in rabbits and rodents is the zoophilic organism, Trichophyton mentagrophytes var. mentagrophytes. Trichophyton mentagrophytes var. quinckeanum has been associated with ringworm in free-ranging mice (Peromyscus maniculatus). There are reports of ringworm in the European hedgehog caused by Trichophyton erinacei.
The saprophytic organism, Microsporum gypseum is a less frequent cause of clinical disease in rabbits and rodents. Microsporum canis infection has been reported in the guinea pig, and in rare cases the prairie dog and chinchilla. Reported causes of ringworm in ferrets also include M. canis and T. mentagrophytes.
The appearance and location of ringworm will vary with the species affected. Common lesions include irregular patches of alopecia, broken hairs, and variable amounts of redness, crust, and scale. Pruritus is usually minimal to absent. In severe cases, large regions of inflammation and scab formation may develop.
Lesions may be found on any part of the body, however they are most common on or around the head.
- Oval patches of alopecia, crust, scale, and inflammation often begin on the nose in the guinea pig before spreading to the forehead, pinnae, and around the eyes (Fig 2). Lesions may then extend over the back and limbs, but are rarely found on the ventrum. Rare nail bed infections have also been reported in the guinea pig.
- Disease in the chinchilla frequently involves the face, particularly around the eyes, behind the ears, and the forelimbs. Lesions may also be found around the mammary glands. Historically, dermatophytosis has also been implicated as a possible cause of fur chewing in the chinchilla.
- In the rat, lesions are most commonly found over the back and neck, while lesions in the mouse are often on the head, neck, and tail. The most well known clinical disease of free-ranging rodents is “mouse favus”, a severe form of ringworm caused by Trichophyton mentagrophytes var. quinckeanum. Scutula or thick, yellow, saucer-shaped crusted lesions up to 1 cm in diameter may be found on the head and body. These lesions contain large amounts of fungal mycelium and inflammatory cells, and are associated with erythema, papules, pustules, pruritus, and occasionally scarring.
- In rabbits, lesions are often located on the ears and face, particularly around the eyes and on the nose.
- Lesions may be found on the head, in the nail bed, and under the pads in the European hedgehog. Lesions between spines are difficult to observe.
Diagnosis of fungal disease
Important differential diagnoses for dermatophytosis include parasitic alopecia caused by fleas, mites or lice, and barbering often secondary to stressors. Concurrent dermatophytosis and ectoparasitism may be particularly likely in rats, mice, and guinea pigs.
Confirmation of fungal disease typically relies upon cytology and culture (Fig 3). Pluck or scrape from the periphery of skin lesions. For cytologic evaluation, mount samples in 10% KOH under a petrolatum ringed coverslip. Collect samples for culture with a sterile toothbrush, hemostat or surgical scrub brush to dislodge hair and cellular debris. Place the sample directly onto the agar surface, and leave the samples in culture medium for a minimum of 10 days. In an experimental guinea pig model, Saunte et al found that cytology was less sensitive than culture, but that culture was as sensitive the new rapid dermatophyte PCR.
Biopsy specimens stained with periodic acid Schiff or silver stain may also be indicated for diagnosis in rare cases. Use of an ultraviolet Wood’s lamp is generally non-diagnostic. Hairs infected with Microsporum canis will fluoresce yellow-green, however most pathogenic dermatophytes in small mammal do not fluoresce.
The route of antifungal drug administration should cause as little stress as possible, and the medication chosen must also be safe and efficacious. A good rule of thumb is to avoid any treatment that is not considered kitten-safe. Since small mammals are frequently used as laboratory animal models, there may also be reports in the literature on the use of antifungal agents in these species. Although most of these reports cannot be directly extrapolated for clinical care, they do serve to document drug efficacy.
In all cases of dermatophytosis, vacuum the environment and disinfect caging. The disinfectants, sodium hypochlorite (1:10 dilution), benzalkonium chloride, 0.2% enilconazole solution (Imaverol, Janssen), and glutaraldehyde are all effective against ringworm. Be sure to destroy or discard all substrate material and cage furniture that are porous and cannot be disinfected as they may serve as potential sources of reinfection.
Topical antifungal therapy
There are many options for topical therapy of cutaneous fungal disease (Table 1), however proceed with caution since the patient may groom off and ingest creams or lotions. Carefully clip wide margins around focal lesions and avoid nicking the skin. Topical treatments, particularly baths and dips, may require sedation or anesthesia for some small mammals.
Topical antiseptics such as 2% chlorhexidine or povidone-iodine are also considered safe and effective. Povidone-iodine is a better choice for facial lesions, since concentrated chlorhexidine can damage the corneal surface. To destroy fungal nail bed infections, use antiseptic solution as a dip several times daily over several weeks. Griseofulvin (Fulvicin, Schering-Plough) as a 1.5% solution in dimethylsulfoxide has also been applied topically once or twice daily over 7 to 14 days. Studies have found that rat skin is 14-times more permeable to griseofulvin than human skin, therefore a much smaller amount of drug was needed to achieve adequate drug levels. Treatment of ringworm in the chinchilla may include the addition of an antifungal agent to the dust bath. One teaspoon of captan (Ortho) mixed with 2 cups of dust has been reported to be effective against dermatophytosis. The successful use of clotrimazole powder in dust has also been described. In a recent paper by Al-Janabi, ibuprofen cream was reportedly effective in rabbits in a clinical trial. Relatively new products that have been empirically shown to improve or eliminate dermatophyte lesions in guinea pigs include a terbinafine nail solution (TNS) containing a nail penetration enhancer (DDAIP HCl, trade name NexACT-88), eugenol, clove essential oil obtained from Syzygium aromaticum, and nerolidol isolated from Japanese cypress oil. Eugenol and nerolidol were adjusted to 10% concentration with a base of Vaseline petroleum jelly and were applied topically to the skin lesions in guinea pigs empirically infected with M. gypseum daily for 3 weeks.
Systemic antifungal therapy
Due to the danger of overdosage and adverse effects, oral antifungals are generally indicated for the treatment of multiple or widespread cutaneous lesions or severe, resistant infections. Oral griseofulvin (Fulvin P/G, Schering-Plough) 15-25 mg/kg PO SID for 4 to 8 weeks has been reported to be effective in guinea pigs and chinchillas with ringworm. Avoid griseofulvin in any pregnant rodent as death, stillbirth, and failure to thrive were reported in pregnant chinchillas given griseofulvin at 25 mg/kg for 10 weeks. Other adverse effects that may be seen with griseofulvin administration include diarrhea, anorexia, and leukopenia. The azole derivative, fluconazole (Diflucan, Roerig) (10-20 mg/kg PO SID) was used to successfully treat experimental Trichophyton mentagrophytes infection in guinea pigs. Ketoconazole (Nizoral, Janssen) (10-15 mg/kg PO SID) has also been recommended in the rodent. Although ketoconazole is much less expensive, there is less risk of adverse effects such as anorexia, vomiting, diarrhea, and elevations in liver enzymes with itraconazole (Sporanox, Janssen)(5-10 mg/kg PO SID). Ketoconazole is also contraindicated in pregnant animals. Itraconazole (10 mg/kg PO SID for 12 days) significantly reduced lesions and redness in guinea pigs. Infections with M. canis responded better than those caused by T. mentagrophytes. The allylamine derivative, terbinafine is reportedly more efficacious than fluconazole and itraconazole against Trichophyton spp. in the guinea pig. Recommended dosages range from 8-20 mg/kg PO SID.
Although clinical disease is relatively uncommon in pets and laboratory animals, rodents are often asymptomatic carriers of ringworm. Dermatophytes are easily transmitted from asymptomatic rodents to humans, and often the first indication of disease in a laboratory is infection among the human workers. Mice and guinea pigs are the most important sources of human infection with Trichophyton mentagrophytes var. mentagrophytes or Microsporum gypseum. There are also reports of human infection secondary to subclinical infection in rabbits and rats. In a survey of farm rabbits, the risk of potential exposure to dermatophytes increased when the animal suffered from a concurrent disease. Dermatophyte prevalence also increased in areas with temperature exceeding 68°F (20°C) and relative humidity ranging from 62-65%. Non-domestic rodents may also be asymptomatic carriers of dermatophytosis. Although rare, human infection with Trichophyton mentagrophytes var. quinckeanum has been reported.
Although fungal disease is uncommon in small mammals, dermatophytosis is the most common mycosis seen in clinical practice. Trichophyton mentagrophytes is the most common etiologic agent, and the guinea pig is the most common species affected although there are reports in the literature in most pet and laboratory species except the gerbil. Despite the low incidence of clinical disease, rodents are common asymptomatic carriers of dermatophytes, and ringworm is the most common zoonotic disease transmitted from rodents to humans.
Table 1. Topical antifungal agents reported to be effective in small mammals
|0.2% Enilconazole||Imaverol, Janssen Animal Health||Dilute 1 part of 10% enilconazole in 50 parts water to create a 0.2% solution.|
|Lime-sulfur||LymDyp, DVM Pharmaceuticals||Dip animals with a 1:40 dilution of lime-sulfur once weekly for 6 weeks. This product is not available in most European countries.|
|2% Miconazole||Conofite, Schering-Plough||Use of miconazole shampoo two to three times weekly for at least 2 to 3 weeks has proved efficacious in guinea pigs with ringworm.|
|0.25% terbinafine cream||Lamisil, Novartis|
Al-Janabi AS. In vitro and in vivo therapeutic activity of ibuprofen against dermatophytes. Saudi Med J 30(5):624-628, 2009.
Bleich A, Nicklas W. Zoonoses transmitted by mouse and rat maintained as laboratory or pet animals. Berl Munch Tierarztl Wochenschr 121(7-8):241-255, 2008.
Bourne D. Enilconazole: with special reference to hedgehogs and lagamorphs. Wildlife1 website. Available at: http://wildlife1.wildlifeinformation.org/S/00Chem/ChComplex/Enilconazole.htm . Accessed May 26, 2010.
Brillowska-Dabrowska A, Swierkowska A, Lindhart SDM, Arendrup MC. Diagnostic PCR tests for Microsporum audouinii, M. canis, and Trichophyton infections. Med Mycol 48(3):486-490, 2010.
Cafarchia C, Camarda A, Coccioli C, et al. Epidemiology and risk factors for dermatophytoses in rabbit farms. Med Mycol 48(7):975-980, 2010.
Carpenter JW. Exotic Animal Formulary, 3rd ed. Philadelphia, Elsevier, 2005.
Chermette R, Ferreiro L, Guillot J. Dermatophytoses in animals. Mycopathologia 166(5-6):385-405, 2008.
Connole MD, Yamaguchi H, Elad D, et al. Natural pathogens of laboratory animals and their effects on research. Med Mycol 38 Suppl 1:59-65, 2000.
Donnelly TM, Rush EM, Lackner PA. Ringworm in small exotic pets. Seminars in Avian and Exotic Pet Medicine; 9(2):82-93, 2000.
Gallo MG, Tizzani P, Peano A, et al. Eastern cottontail (Sylvilagus floridanus) as carrier of dermatophyte fungi. Mycopathologia 160(2):163-166, 2005.
García-Sánchez MS, Pereiro M Jr, Pereiro MM, Toribio J. Favus due to Trichophyton mentagrophytes var. quinckeanum. Dermatology 194(2):177-179, 1997.
Ghannoum MA, Long L, Pfister WR. Determination of the efficacy of terbinafine hydrochloride nail solution in the topical treatment of dermatophytosis in a guinea pig model. Mycoses 52(1):35-43, 2009.
Harkness JE, Wagner JE. Specific diseases and conditions. In: The Biology and Medicine of Rabbits and Rodents, 4th ed. Baltimore, Williams and Wilkins, 1995. Pp. 202-204.
Hata Y, Amagai M, Naka W, et al. Two cases of Trichophyton mentagrophytes infection contracted from a hamster and a chinchilla. Japanese Journal of Medical Mycology 41(4):269-273, 2000.
Hoppmann E, Barron HW. Rodent dermatology. J Exotic Pet Med 16(4):238-255, 2007.
Kassem MA, Esmat S, Bendas ER, El-Komy MH. Efficacy of topical griseofulvin in treatment of tinea corporis. Mycoses 49(3):232-235, 2006.
Kushida T. Dermatophytosis caused by Trichophyton mentagrophytes in squirrels. Nippon Juigaku Zasshi 41:177-179, 1979.
Lee SJ, Han JI, Lee GS, et al. Antifungal effect of eugenol and nerolidolRefer against Microsporum gypseum in a guinea pig model. Biol Pharm Bull 30(1):184-188, 2007.
Mieth H, Leitner I, Meingassner JG. The efficacy of orally applied terbinafine, itraconazole and fluconazole in models of experimental trichophytoses. J Med Vet Mycol 32(3):181-188, 1994.
Nagino K, Shimohira H, Ogawa M, et al. Comparison of the therapeutic efficacy of oral doses of fluconazole and griseofulvin in a guinea pig model of dermatophytosis. J Antibiotics 53(2):207-210, 2000.
Nagino K, Shimohira H, Ogawa M, et al. Comparison of the therapeutic efficacy of oral doses of fluconazole and itraconazole in a guinea pig model of dermatophytosis. J Infect Chemother 6(1):41-44, 2000.
Quesenberry K, Carpenter JW. Ferrets, Rabbits, and Rodents: Clinical Medicine and Surgery, 2nd ed. Philadelphia, WB Saunders, 2003.
Pinto E, Vale-Silva L, Cavaleiro C, Salguiero L. Antifungal activity of the clove essential oil from Syzgium aromaticum on Candida, Aspergillus, and dermatophyte species. J Med Microbiol 58(Pt 11 ):1454-1462, 2009.
Pollock CG. Fungal diseases of laboratory rodents. Vet Clin North Am Exot Anim Pract 6(2):401-414, 2003.
Rycroft AN, McLay C. Disinfectants in the control of small animal ringworm due to Microsporum canis. Vet Rec 129(11):239-241, 1991.
Saunte DM, Hasselby JP, Brillowska-Dabrowska A, et al. Experimental guinea pig model of dermatophytosis: a simple and useful tool for the evaluation of new diagnostics and antifungals. Med Mycol 46(4):303-313, 2008.
Tabor E, Bostwick DC, Evans CC. Corneal damage due to eye contact with chlorhexidine gluconate. J Am Med Assoc 261(4):557-558, 1989.
Uchida K, Yamaguchi H. Effectiveness of oral treatment with terbinafine in a guinea pig model of tinea pedis. Jpn J Antibiotic 47:1401-1406, 1994.
Van Rooij P, Detandt M, Nolard N. Trichophyton mentagrophytes of rabbit origin causing family incidence of kerion: an environmental study. Mycoses 49:426-430, 2006.
Vangeel I, Pasmans F, Vanrobaeys M, et al. Prevalence of dermatophytes in asymptomatic guinea pigs and rabbits. Vet Rec 146(15):440-441, 2000.
Yamaguchi H, Uchida K, Tanaka T, et al. Therapeutic efficacy of a topical tolnaftate preparation in guinea pig model of tinea pedis. Jpn J Antibiot 54: 323-330, 2001.
Pollock C. Dermatophytosis in small mammals. January 4, 2011. LafeberVet Web site. Available at https://lafeber.com/vet/dermatophytosis-in-small-mammals/