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Infectious threats from exotic pets: dermatological implications
Dermatol Clin 21 (2003) 229 – 236
Infectious threats from exotic pets: dermatological implications Ted Rosen, MDa,*, Jennifer Jablon, MDb b
a Department of Dermatology, Baylor College of Medicine, 2815 Plumb, Houston, TX 77005, USA Department of Internal Medicine, St. Joseph’s Mercy Hospital, 5301 E. Huron Drive, Ann Arbor, MI 48106, USA
During the past five decades, a considerable body of information regarding exotic animals has been generated. Such information has largely been utilized to study survival skills, migrating habits, or causes for a decline in species number; however, this body of information has also become important for a new reason: many Americans are inviting these exotic animals into their homes as pets. Neither pet owners nor non-veterinary health care providers are sufficiently knowledgeable about the possible medical problems caused by these animals. Hedgehogs, flying squirrels, iguanas, chinchillas, and cockatoos comprise a major part of this trend toward novel exotic pets residing in American households. Such animals can be associated with cutaneous infections, acute and chronic systemic illness with skin signs, and even fatality. Moreover, such animals have been found to harbor dangerous microorganisms that, although not yet directly linked to human infection, have the potential to cause devastating disease. Health care providers need to be more aware of the risks entailed by exotic pet ownership and to remember to inquire about such pets while obtaining a medical history or formulating a differential diagnosis.
Hedgehog There are eleven species of hedgehog, the most prevalent being the European hedgehog, the Pruner’s
* Corresponding author. E-mail address: [email protected] (T. Rosen).
(or Cape) hedgehog, the Egyptian (or long-eared) hedgehog, and the species Atelerix albiverntris, better known as the African pygmy hedgehog [1 – 3]. The African pygmy hedgehog has become a common household addition, with an estimated 40,000 households in the United States harboring this pet [4]. Although hedgehogs are often considered to be benign, easily maintained, small versions of porcupines, they can pose some rather unique threats to their human owners, including fungal and salmonella infections, contact urticaria, and possibly mycobacterium infections. The African pygmy hedgehog has recently been strongly implicated as a cause of moderate to severe cutaneous dermatophytosis [3]. The three individuals described in this report were in contact with an African pygmy hedgehog, and lesional cultures yielded an organism (Trichophyton mentagrophytes), which is known to be frequently carried on the quills and the underbelly in this particular species of hedgehog [5]. One of the patients reported merely handling the hedgehog in a pet store for a period of 1 to 2 minutes, indicating that this infection might be highly contagious if the animal is heavily colonized (Fig. 1). Additional cases of tinea corporis [6 – 9] and tinea capitis [10,11] have been reported following contact with wild European hedgehogs and their natural habitat, further suggesting that hedgehog pets might truly be a viable source of dermatophytosis in their unsuspecting owners. The hedgehog has also been implicated in one case of contact urticaria, which was most likely caused by a hypersensitivity response to hedgehog saliva, which the animal deposits on its quills [12]. The worst hazard to human owners of hedgehogs has been salmonellosis. The African pygmy hedgehog has
0733-8635/03/$ – see front matter D 2003, Elsevier Science (USA). All rights reserved. doi:10.1016/S0733-8635(02)00090-6
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Fig. 1. Massive tinea manum following exposure to an African pygmy hedgehog.
been clearly implicated in human salmonellosis in the United States and Canada [13,14]. Although it has been presumed that this infection results from ingestion of food inadvertently contaminated by hedgehog feces, the actual mechanism of salmonellosis acquired from hedgehogs has not been clearly established. Human salmonellosis can vary from dehydrating dysentery to meningitis and toxic bacteremia. It can be a serious illness, especially in the young, old, and immunocompromised. Although the African pygmy hedgehog has not yet been documented to carry any mycobacterial diseases, the European hedgehog has been found to carry the Mycobacterium species M. marinum and M. avium – intracellulare [15,16], which suggests that it is possible for the former variety to do so as well. Such organisms readily cause infection—even of a fatal nature—in immunocompromised patients [17]. Such patients should strictly avoid any potential sources of these organisms, and hedgehogs are not recommended pets for patients with HIV disease.
Flying squirrel There are two distinct groups of rodents that are often referred to as ‘‘flying squirrels.’’ Members of the first group, consisting of African rodents with scaly tails in the family Anomaluridae, are not sold as pets. The second group contains the more familiar North American and Eurasian flying squirrels and the Australian sugar glider from the subfamily Petauristinae of the family Sciuridae. The term ‘‘flying squirrel’’ is somewhat of a misnomer because these animals actually make gliding leaps of up to 150 feet
utilizing parachute-like membranes that are connected on each side to their forelegs and hindlegs. There are 35 species of flying squirrels in the family Sciuridae, but only two are found in North America, Glaucomys volans and Glaucomys sabrinus [18]. These animals are known to nest in birdhouses or buildings. These closely related species, collectively known as New World flying squirrels, have recently become popular household pets, with the estimated 5000 to 8000 owners in the United States [4]. Although the flying squirrel has been proclaimed to be a friendly and intelligent pet, especially when domesticated as a newborn, it should be noted that such animals might be the source of a number of dangerous infections. Some flying squirrels have been reported to harbor the proliferative stages of Toxoplasma gondii, the organism responsible for potentially fatal toxoplasmosis in humans [19]. It is not known how the squirrels were infected; it is hypothesized that Toxoplasma gondii might be a congenitally acquired infection because the squirrel is an herbivore and the main method of parasite acquisition is ingestion of raw meat containing cysts. Although there are no documented reports of human toxoplasmosis from flying squirrels, the fact that a herbivore such as the flying squirrel can acquire this disease leaves open the possibility that owners could be at risk. Other potentially dangerous microorganisms harbored by flying squirrels are unusual and aggressive species of the bacterium Staphylococcus. In one study, virtually all of the flying squirrels captured in Raleigh, North Carolina carried three atypical strains of staphylococcus on their skin: Staphylococcus sp. 3, S. sciuri, and S. xylosus [20]. In the same study, these three strains were found
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(uncommonly) on human skin, with the prevalence being 0%, 10%, and 42% respectively. S. sciuri and S. xylosus grow poorly on agar at pH 5.3 or below, explaining why they are rare on human skin (pH 5.0); however, these species grow well at pH 7.0 or above, making them a danger if, as a human skin contaminant, they enter the bloodstream through a wound. The in vivo pH of human tissues is between 7.35 and 7.45, an ideal environment for this organism to proliferate. In this same study, Staphylococcus sp. 3 was isolated only from the flying squirrel, raccoon, opossum, and the eastern gray squirrel, but not from human skin. Considering its novelty, this species would pose a threat to a human who would have little to no immunity against it. There is evidence Glaucomys species serve as an extrahuman reservoir for typhus. Epidemic typhus is caused by infection with Rickettsia prowazekii and is usually transmitted from person-to-person by way of the human body louse. The last major outbreak of louse-borne typhus in the United States was in the 1920s, but sporadic cases of a milder form of typhus occurring in people living in rural environments have been attributed to contact with flying squirrels [21 – 24]. The mode of transmission between flying squirrel and human has not been firmly established, although experimental work suggests that transmission to humans might occur through inhalation of aerosolized ectoparasite feces or directly by way of the bite of an infected ectoparasite [25]. In one study, serological evidence of typhus infection was established only in flying squirrels, not the lice or ticks found on their skin [22], whereas another study found that commensal fleas and lice—and their host flying squirrels—were infected [24]. Although such disease has been a milder form of typhus, all patients presented with one or more of the following symptoms: fever, typical louse-born epidemic typhus rash (blanchable erythematous macules spreading to the trunk and extremities from the axillary folds), nausea, vomiting, headache, myalgia, photophobia, malaise, and dizziness. One woman died from renal complications [23]. Thus, the combination of fever, rash, and systemic toxicity in an owner of a flying squirrel should suggest typhus as a possible diagnosis.
Iguana There are thirteen iguana species within the larger members of the lizard family Iguanidae. The best known and most common is the reptile Iguana iguana, which naturally inhabits Southern Mexico and Brazil. This particular lizard is inexpensive to
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purchase, and there are now some 700,000 such pets in the United States [4]. Other well-known species include I. delicatissima of the Caribbean islands, Cyclura cornuta of Haiti, Dipsosaurus dorsalis, the desert iguana of Mexico and the United States, Amblyrhynchus cristatus, the marine iguana, and the Conolophus iguanas of the Galapagos Islands. I. iguana is a greenish-colored animal with overlaid brown bands. It usually eats fruit and leaves, but it will also eat small birds and mammals. This 20-pound reptile can grow up to 6 feet long and poses a domicilliary challenge that is often met by allowing it to reside/sleep in an extra household bathtub! Many potentially pathogenic bacteria have been isolated from the iguana pharynx, including Staphylococcus sp, Streptococcus sp, Serratia sp, Corynebacterium sp, Alcaligenes sp, and from the cloaca, including Micrococcus sp, Bacillus subtilis, Salmonella marina, Salmonella chameleon, Escherichia coli, and Hafnialike species [26]. The organisms from the pharynx have the potential to cause serious cellulitis if the iguana bites. In fact, there are several such reports in the literature [27 – 29]. Serratia marcescens infection, as determined by wound culture in one reported case [27], is particularly difficult in that it might manifest as rapidly progressive, bullous cellulitis associated with extreme systemic toxicity (Fig. 2). Iguanas are commonly treated by breeders with broad-spectrum prophylactic antibiotics to prevent disease and discoloration [30]. Although this practice is frequently unsuccessful, it might result in the development of drug-resistant bacteria, further complicating the management of cellulitis following an iguana bite. A series of investigations in the 1970s led to the discovery of a new herpes-type virus isolated from the pharynx of the common pet iguana [31,32]. This virus was the first to be isolated from reptiles, and it appeared to possess a capability for causing latent or unapparent infections consistent with mammalian herpesviruses. This virus has not been implicated in human infection to date, but it remains another potential complication of an iguana bite. Most allergic responses to pets occur in association with the fur (dander) of the implicated animal; however, at least one well-documented case of allergic rhinitis, asthma, and urticaria has been reported to be caused by an iguana [33]. The allergic nature of this reaction was verified by demonstrating a positive intradermal skin test to an aqueous extract prepared from iguana scale. The iguana is best known for its potential for transmitting salmonella to humans. There has been a significant increase in nontyphoidal salmonellosis, which is generally acquired from animals. Approx-
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Fig. 2. Serratia marcescens cellulitis following an iguana bite.
imately 4 million such cases were tabulated in 1995; these infections were believed to be caused by infected eggs and poultry and pet iguanas [6]. There have been many reports of enteric salmonellosis acquired from pet iguanas in the United States [34 – 36], an 83% rate of fecal shedding of salmonella from pet iguanas [37], and scattered reports of salmonella meningitis associated with iguana ownership [38]. From a dermatological standpoint, nontyphoidal salmonella infection can be associated with a nondescript, generalized erythematous papular eruption. Thus, the clinical situation of diarrhea and a rash in an iguana owner should strongly suggest salmonellosis as the etiology.
Chinchilla The chinchilla is a small South American herbivore of the family Chinchilladae of the order Rodentia. There is some debate regarding whether the chinchilla is one species (Chinchilla laniger) or two species, the long-tailed C. laniger and the short-tailed C. brevicaudata. These animals, long known for soft, attractive fur, naturally inhabit the rocky regions of the Chilean and Bolivian Andes and subsist on grain, herbs, and moss. Once hunted almost to extinction and still scarce in the wild, chinchillas are now raised commercially in ‘‘farms.’’ Almost all of the chinchillas in captivity used for commercial breeding are descended from a few animals introduced into the United States in the 1920s. Some 80,000 chinchillas are kept as household pets [4]. The skin and fur of the chinchilla often harbors several common superficial fungi. Trychophyton
mentagrophytes and Microsporum gypseum have been recovered from chinchillas; these organisms have actually been responsible for symptomatic animal dermatophytosis [39 – 42]. Because these organisms are well established as etiologic for human disease, it is not unreasonable to suspect the chinchilla as the source of infection in an owner who presents with acute, inflammatory tinea corporis or tinea capitis (Fig. 3). Several nondermatophytes have also been isolated from the chinchilla, including Aspergillus niger, Cladosporium spp, and Rhizopus species [43]. Such saprophytes might become opportunistic pathogens in select individuals such as diabetics, organ transplant patients, bone marrow transplant recipients, and leukemia patients. Hence, the chinchilla might not be a good choice for a pet in these circumstances. Chinchillas also have a predilection for harboring Klebsiella pneumoniae and Pseudomonas aeruginosa [44,45]. These organisms can be isolated from chinchillas with unapparent disease, or they might be discovered after the chinchilla’s demise from bacterial sepsis. Because these organisms are well recognized as potential human pathogens, signs and symptoms suggestive of Gram-negative sepsis in a chinchilla owner (especially an owner who is immunocompromised or diabetic) should be heeded carefully.
Cockatoo The colorful cockatoo is among the most popular of ornamental pet birds. There are 18 distinct species falling into the overall category of ‘‘cockatoo.’’ The majority of these parrot relatives are native to Aus-
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Fig. 3. Inflammatory tinea corporis in a chinchilla owner.
tralia, Indonesia, and the Philippine Islands. Though not possessing as prolific a vocabulary retention as a parrot, the cockatoo offers the singular advantage of being a long-lived pet; birds in this category survive 30 to 80 years in a comfortable home environment. In common with pigeons, the cockatoo is a potential source of infection caused by Cryptococcus neoformans serotypes A and D. Generally, the bird remains well, but sheds the fungus in its feces, contaminating the birdcage and ambient air in close proximity to the cage [46,47]. On rare occasions, the cockatoo itself can develop cryptococcal disease [48]. A recent case report elegantly demonstrated that cryptococcosis can be transmitted from an infected
pet cockatoo to a susceptible human owner, in this instance an elderly renal transplant patient [49]. In the report cited, patient and cockatoo isolates were indistinguishable based upon biochemical profiles, monoclonal antibody binding patterns, restriction fragment length polymorphism analysis, and karyotyping. From the dermatologist’s viewpoint, cryptococcosis can present in many fashions, including cellulitis, lesions resembling molluscum and herpes, and Kaposi’s sarcoma-like papulonodules (Fig. 4). The close association of the cockatoo with cryptococcal disease has led to the strong suggestion that immunosuppressed and immunocompromised patients should avoid choosing this bird as a pet [49,50].
Fig. 4. Nodular cutaneous cryptococcosis in an HIV+ cockatoo owner.
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As is true of almost any bird, the cockatoo can carry avian mites such as the northern fowl mite (Ornithonyssus sylvarium) and the chicken mite (Dermanyssus gallinae). Although such ectoparasites are more commonly associated with the commercial poultry industry or with wild nesting birds (eg, starlings and pigeons), they can also infest various birds used as house pets (eg, canaries, doves, finches, parakeets, and other psitticine species) [51,52]. Avian mites can cause an intensely pruritic, localized to generalized, papular to papulovesicular eruptions in an unsuspecting and incidental human host. Avian mites can be introduced into the environment not only by affected birds but also by other pets that seemingly acquired acariasis from birds housed at the same pet store. For example, two cases of avian mite dermatitis were recently reported to arise from infested pet gerbils [53]. Because avian mites cannot reproduce on a human host, infection with this type of organism is self-limiting if the source of the mites is permanently removed, or if the birdcage is cleaned and the pet bird disinfected with acaricide; temporary relief from pruritus in the incidental human host can be obtained with application of potent topical steroids.
Summary Zoonoses are diseases that can be transmitted from animals to humans. More than 250 distinct zoonoses have been described in the literature. It is estimated that 56% of United States households contain at least one pet, and although considerable research has been performed regarding the more common household animals including dogs, cats, small birds, and rodents, surprisingly little is known about the zoonotic hazards of owning the more exotic pets [54 – 57]. According to the 1997 USPHS/IDSA Report on the Prevention of Opportunistic Infections in Persons Infected with Human Immunodeficiency Virus, the immunocompromised patient should avoid contact with feces-laden soil, litter boxes, reptiles, most pet birds, and any animal less than 6 months old [58]. It has also been documented that because of their inquisitive nature, children are at even higher risk for infection from animals than adolescents or immunocompetent adults [54]. In this article the authors have reviewed the available data regarding hazards associated with the hedgehog, flying squirrel, iguana, chinchilla, and cockatoo. With the growing popularity of such exotic pets, further observation and research is warranted. Physicians need to be aware of the possibility of
zoonotic disease related to exotic pet ownership, and they should address this issue when obtaining a history and formulating a differential diagnosis of cutaneous lesions suggestive of such illnesses.
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T. Rosen, J. Jablon / Dermatol Clin 21 (2003) 229–236 [19] Cross J, Lien J, Hsu M. Toxoplasma isolated from the Formosan giant flying squirrel. Taiwan I Hsueh Hui Tsa Chih 1969;68:678 – 83. [20] Kloos WE, Zimmerman RJ, Smith RF. Preliminary studies on the characterization and distribution of Staphylococcus and Micrococcus species on animal skin. App Environ Microbiol 1976;31:53 – 9. [21] Anonymous. Centers for Disease Control. Current trends: epidemic typhus associated with flying squirrels—United States. MMWR 1982;31:555 – 61. [22] Duma RJ, Sonenshine DE, Bozeman FM, et al. Epidemic typhus in the United States associate with flying squirrels. JAMA 1981;245:2318 – 23. [23] McDade JE, Shepard CC, Redus MA, et al. Evidence of Rickettsia prowazekii infections in the United States. Am J Trop Med Hyg 1980;29:277 – 84. [24] Sonenshine DE, Bozeman FM, Williams MS, et al. Epizootiology of epidemic typhus (Rickettsia prowazekii) I flying squirrels. Am J Trop Med Hyg 1978;27: 339 – 49. [25] Bozeman FM, Soneshine DE, Williams MS, et al. Experimental infection of ectoparasite arthropods with Rickettsia prowazekii (GvF-16 strain) and transmission to flying squirrels. Am J Trop Med Hyg 1981; 30:253 – 63. [26] Boam GW, Sanger VL, Cowan DF, et al. The pathogenicity for mice of two species of salmonella isolated from the green iguana (Iguana iguana). J Am Vet Med Assoc 1970;157:689 – 90. [27] Hsieh S, Babl FE. Serratia marcescens cellulitis following an iguana bite. Clin Infect Dis 1999;28: 1181 – 2. [28] Kelsey J, Ehrlich M, Henderson SO. Exotic reptile bites. Am J Emerg Med 1997;15:536 – 7. [29] Teitel AD. Bite of the iguana [letter]. Am J Emerg Med 1990;8:567 – 8. [30] Barten SL. The medical care of iguanas and other common pet lizards. Vet Clin N Am Small Anim Pract 1993;23:1213 – 49. [31] Clark HF, Karzon DT. Iguana virus, a herpes-like virus isolated from cultured cells of a lizard, Iguana iguana. Infect Immun 1972;5:559 – 69. [32] Zeigel RF, Clark HF. Electron microscopy observation on a new herpes-type virus isolated from Iguana iguana and propagated in reptilian cells in vitro. Infec Immun 1972;5:570 – 82. [33] Kelso JM, Fox RW, Jones RT, et al. Allergy to iguana. J Allergy Clin Immunol 2000;106:369 – 72. [34] Dalton C, Hoffman R, Pape J. Iguana-associated salmonellosis in children. Pediatr Infect Dis J 1995;14: 319 – 20. [35] Mermin J, Hoar B, Angulo FJ. Iguanas and Salmonella marina infection in children: a reflection of the increasing incidence of reptile-associated salmonellosis in the United States. Pediatrics 1997;99:399 – 402. [36] Mitchell MA, Shane SM. Preliminary findings of Salmonella spp. in captive green iguanas (Iguana iguana) and their environment. Prev Vet Med 2000;45: 297 – 304.
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[37] Burnham BR, Atchley DH, DeFusco RP, et al. Prevalence of fecal shedding of Salmonella organisms among captive green iguanas and potential public health implications. J Am Vet Med Assoc 1998; 213:48 – 50. [38] Sam WI, Mackay AD. Salmonella meningitis and a green iguana. J R Soc Med 2000;93:318 – 9. [39] Cabanas FJ, Abarca ML, Bragulat MR. Dermatophytes from domestic animals in Barcelona, Spain. Mycopathologia 1997;137:107 – 13. [40] Hagen KW, Gorham JR. Dermatomycoses in fur animals: chinchilla, ferret, mink, and rabbit. Vet Med Small Anim Clin 1972;67:43 – 8. [41] Male O, Fritsch P. Trychophyton mentagrophytes caused epidemic and enzootic disease in a chinchilla farm. Mykosen 1966;4:74 – 84. [42] Morganti L, Gomez Portugal EA. Microsporum gypseum infection in chinchillas. Sabouraudia 1970;8: 39 – 40. [43] Aho R. Saprophytic fungi isolated from the hair of domestic and laboratory animals with suspected dermatophytosis. Mycopathologia 1983;83:65 – 73. [44] Bartoszcze M, Matras J, Palec S, et al. Klebsiella pneumoniae infection in chinchillas. Vet Rec 1990; 127:119. [45] Doerning BJ, Brammer DW, Rush HG. Pseudomonas aeruginosa infection in a Chinchilla lanigera. Lab Anim 1993;27:131 – 3. [46] Staib F. Sampling and isolation of Cryptococcus neoformans from indoor air with the aid of the Reuter Centrifugal Sampler and guizotia abyssinica creatinine agar. Zentralbl Bakteriol Mikrobiol Hyg 1985;180: 567 – 75. [47] Staib F, Schulz-Dieterich J. Cryptococcus neoformans in fecal matter of birds kept in cages. Control of Cr. Neoformans habitats. Zentralbl Bakteriol Mikrobiol Hyg 1984;179:179 – 86. [48] Fenwick B, Takeshita K, Wong A. A moluccan cockatoo with disseminated cryptococcosis. J Am Vet Med Assoc 1985;187:1218 – 9. [49] Nosanchuk JD, Shoham S, Fries BC, et al. Evidence of zoonotic transmission of Cryptococcus neoformans from a pet cockatoo to an immunocompromised patient. Ann Intern Med 2000;132:205 – 8. [50] Blaschke-Hellmessedn R. Cryptococcus species—etiological agents of zoonoses or sapronosis? Mycoses 2000;43(Suppl 1):48 – 60. [51] Jeffrey JS, McCrea B. Identification and treatment of common mites and lice of birds. 1999. Available at: http://www.animal science.ucdavis.edu/Avian/ pfs31.htm. Accessed March 31, 1999. [52] Schulze KE, Cohen PR. Dove-associated gamasoidosis: a case of avian mite dermatitis. J Am Acad Dermatol 1994;30:278 – 80. [53] Lucky AW, Sayers C, Argus JD, et al. Avian mites acquired from a new source-pet gerbils. Report of two cases and review of the literature. Arch Dermatol 2001;137:167 – 70. [54] Chomel BB. Zoonoses of house pets other than
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Infectious threats from exotic pets: dermatological implications Ted Rosen, MDa,*, Jennifer Jablon, MDb b
a Department of Dermatology, Baylor College of Medicine, 2815 Plumb, Houston, TX 77005, USA Department of Internal Medicine, St. Joseph’s Mercy Hospital, 5301 E. Huron Drive, Ann Arbor, MI 48106, USA
During the past five decades, a considerable body of information regarding exotic animals has been generated. Such information has largely been utilized to study survival skills, migrating habits, or causes for a decline in species number; however, this body of information has also become important for a new reason: many Americans are inviting these exotic animals into their homes as pets. Neither pet owners nor non-veterinary health care providers are sufficiently knowledgeable about the possible medical problems caused by these animals. Hedgehogs, flying squirrels, iguanas, chinchillas, and cockatoos comprise a major part of this trend toward novel exotic pets residing in American households. Such animals can be associated with cutaneous infections, acute and chronic systemic illness with skin signs, and even fatality. Moreover, such animals have been found to harbor dangerous microorganisms that, although not yet directly linked to human infection, have the potential to cause devastating disease. Health care providers need to be more aware of the risks entailed by exotic pet ownership and to remember to inquire about such pets while obtaining a medical history or formulating a differential diagnosis.
Hedgehog There are eleven species of hedgehog, the most prevalent being the European hedgehog, the Pruner’s
* Corresponding author. E-mail address: [email protected] (T. Rosen).
(or Cape) hedgehog, the Egyptian (or long-eared) hedgehog, and the species Atelerix albiverntris, better known as the African pygmy hedgehog [1 – 3]. The African pygmy hedgehog has become a common household addition, with an estimated 40,000 households in the United States harboring this pet [4]. Although hedgehogs are often considered to be benign, easily maintained, small versions of porcupines, they can pose some rather unique threats to their human owners, including fungal and salmonella infections, contact urticaria, and possibly mycobacterium infections. The African pygmy hedgehog has recently been strongly implicated as a cause of moderate to severe cutaneous dermatophytosis [3]. The three individuals described in this report were in contact with an African pygmy hedgehog, and lesional cultures yielded an organism (Trichophyton mentagrophytes), which is known to be frequently carried on the quills and the underbelly in this particular species of hedgehog [5]. One of the patients reported merely handling the hedgehog in a pet store for a period of 1 to 2 minutes, indicating that this infection might be highly contagious if the animal is heavily colonized (Fig. 1). Additional cases of tinea corporis [6 – 9] and tinea capitis [10,11] have been reported following contact with wild European hedgehogs and their natural habitat, further suggesting that hedgehog pets might truly be a viable source of dermatophytosis in their unsuspecting owners. The hedgehog has also been implicated in one case of contact urticaria, which was most likely caused by a hypersensitivity response to hedgehog saliva, which the animal deposits on its quills [12]. The worst hazard to human owners of hedgehogs has been salmonellosis. The African pygmy hedgehog has
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Fig. 1. Massive tinea manum following exposure to an African pygmy hedgehog.
been clearly implicated in human salmonellosis in the United States and Canada [13,14]. Although it has been presumed that this infection results from ingestion of food inadvertently contaminated by hedgehog feces, the actual mechanism of salmonellosis acquired from hedgehogs has not been clearly established. Human salmonellosis can vary from dehydrating dysentery to meningitis and toxic bacteremia. It can be a serious illness, especially in the young, old, and immunocompromised. Although the African pygmy hedgehog has not yet been documented to carry any mycobacterial diseases, the European hedgehog has been found to carry the Mycobacterium species M. marinum and M. avium – intracellulare [15,16], which suggests that it is possible for the former variety to do so as well. Such organisms readily cause infection—even of a fatal nature—in immunocompromised patients [17]. Such patients should strictly avoid any potential sources of these organisms, and hedgehogs are not recommended pets for patients with HIV disease.
Flying squirrel There are two distinct groups of rodents that are often referred to as ‘‘flying squirrels.’’ Members of the first group, consisting of African rodents with scaly tails in the family Anomaluridae, are not sold as pets. The second group contains the more familiar North American and Eurasian flying squirrels and the Australian sugar glider from the subfamily Petauristinae of the family Sciuridae. The term ‘‘flying squirrel’’ is somewhat of a misnomer because these animals actually make gliding leaps of up to 150 feet
utilizing parachute-like membranes that are connected on each side to their forelegs and hindlegs. There are 35 species of flying squirrels in the family Sciuridae, but only two are found in North America, Glaucomys volans and Glaucomys sabrinus [18]. These animals are known to nest in birdhouses or buildings. These closely related species, collectively known as New World flying squirrels, have recently become popular household pets, with the estimated 5000 to 8000 owners in the United States [4]. Although the flying squirrel has been proclaimed to be a friendly and intelligent pet, especially when domesticated as a newborn, it should be noted that such animals might be the source of a number of dangerous infections. Some flying squirrels have been reported to harbor the proliferative stages of Toxoplasma gondii, the organism responsible for potentially fatal toxoplasmosis in humans [19]. It is not known how the squirrels were infected; it is hypothesized that Toxoplasma gondii might be a congenitally acquired infection because the squirrel is an herbivore and the main method of parasite acquisition is ingestion of raw meat containing cysts. Although there are no documented reports of human toxoplasmosis from flying squirrels, the fact that a herbivore such as the flying squirrel can acquire this disease leaves open the possibility that owners could be at risk. Other potentially dangerous microorganisms harbored by flying squirrels are unusual and aggressive species of the bacterium Staphylococcus. In one study, virtually all of the flying squirrels captured in Raleigh, North Carolina carried three atypical strains of staphylococcus on their skin: Staphylococcus sp. 3, S. sciuri, and S. xylosus [20]. In the same study, these three strains were found
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(uncommonly) on human skin, with the prevalence being 0%, 10%, and 42% respectively. S. sciuri and S. xylosus grow poorly on agar at pH 5.3 or below, explaining why they are rare on human skin (pH 5.0); however, these species grow well at pH 7.0 or above, making them a danger if, as a human skin contaminant, they enter the bloodstream through a wound. The in vivo pH of human tissues is between 7.35 and 7.45, an ideal environment for this organism to proliferate. In this same study, Staphylococcus sp. 3 was isolated only from the flying squirrel, raccoon, opossum, and the eastern gray squirrel, but not from human skin. Considering its novelty, this species would pose a threat to a human who would have little to no immunity against it. There is evidence Glaucomys species serve as an extrahuman reservoir for typhus. Epidemic typhus is caused by infection with Rickettsia prowazekii and is usually transmitted from person-to-person by way of the human body louse. The last major outbreak of louse-borne typhus in the United States was in the 1920s, but sporadic cases of a milder form of typhus occurring in people living in rural environments have been attributed to contact with flying squirrels [21 – 24]. The mode of transmission between flying squirrel and human has not been firmly established, although experimental work suggests that transmission to humans might occur through inhalation of aerosolized ectoparasite feces or directly by way of the bite of an infected ectoparasite [25]. In one study, serological evidence of typhus infection was established only in flying squirrels, not the lice or ticks found on their skin [22], whereas another study found that commensal fleas and lice—and their host flying squirrels—were infected [24]. Although such disease has been a milder form of typhus, all patients presented with one or more of the following symptoms: fever, typical louse-born epidemic typhus rash (blanchable erythematous macules spreading to the trunk and extremities from the axillary folds), nausea, vomiting, headache, myalgia, photophobia, malaise, and dizziness. One woman died from renal complications [23]. Thus, the combination of fever, rash, and systemic toxicity in an owner of a flying squirrel should suggest typhus as a possible diagnosis.
Iguana There are thirteen iguana species within the larger members of the lizard family Iguanidae. The best known and most common is the reptile Iguana iguana, which naturally inhabits Southern Mexico and Brazil. This particular lizard is inexpensive to
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purchase, and there are now some 700,000 such pets in the United States [4]. Other well-known species include I. delicatissima of the Caribbean islands, Cyclura cornuta of Haiti, Dipsosaurus dorsalis, the desert iguana of Mexico and the United States, Amblyrhynchus cristatus, the marine iguana, and the Conolophus iguanas of the Galapagos Islands. I. iguana is a greenish-colored animal with overlaid brown bands. It usually eats fruit and leaves, but it will also eat small birds and mammals. This 20-pound reptile can grow up to 6 feet long and poses a domicilliary challenge that is often met by allowing it to reside/sleep in an extra household bathtub! Many potentially pathogenic bacteria have been isolated from the iguana pharynx, including Staphylococcus sp, Streptococcus sp, Serratia sp, Corynebacterium sp, Alcaligenes sp, and from the cloaca, including Micrococcus sp, Bacillus subtilis, Salmonella marina, Salmonella chameleon, Escherichia coli, and Hafnialike species [26]. The organisms from the pharynx have the potential to cause serious cellulitis if the iguana bites. In fact, there are several such reports in the literature [27 – 29]. Serratia marcescens infection, as determined by wound culture in one reported case [27], is particularly difficult in that it might manifest as rapidly progressive, bullous cellulitis associated with extreme systemic toxicity (Fig. 2). Iguanas are commonly treated by breeders with broad-spectrum prophylactic antibiotics to prevent disease and discoloration [30]. Although this practice is frequently unsuccessful, it might result in the development of drug-resistant bacteria, further complicating the management of cellulitis following an iguana bite. A series of investigations in the 1970s led to the discovery of a new herpes-type virus isolated from the pharynx of the common pet iguana [31,32]. This virus was the first to be isolated from reptiles, and it appeared to possess a capability for causing latent or unapparent infections consistent with mammalian herpesviruses. This virus has not been implicated in human infection to date, but it remains another potential complication of an iguana bite. Most allergic responses to pets occur in association with the fur (dander) of the implicated animal; however, at least one well-documented case of allergic rhinitis, asthma, and urticaria has been reported to be caused by an iguana [33]. The allergic nature of this reaction was verified by demonstrating a positive intradermal skin test to an aqueous extract prepared from iguana scale. The iguana is best known for its potential for transmitting salmonella to humans. There has been a significant increase in nontyphoidal salmonellosis, which is generally acquired from animals. Approx-
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Fig. 2. Serratia marcescens cellulitis following an iguana bite.
imately 4 million such cases were tabulated in 1995; these infections were believed to be caused by infected eggs and poultry and pet iguanas [6]. There have been many reports of enteric salmonellosis acquired from pet iguanas in the United States [34 – 36], an 83% rate of fecal shedding of salmonella from pet iguanas [37], and scattered reports of salmonella meningitis associated with iguana ownership [38]. From a dermatological standpoint, nontyphoidal salmonella infection can be associated with a nondescript, generalized erythematous papular eruption. Thus, the clinical situation of diarrhea and a rash in an iguana owner should strongly suggest salmonellosis as the etiology.
Chinchilla The chinchilla is a small South American herbivore of the family Chinchilladae of the order Rodentia. There is some debate regarding whether the chinchilla is one species (Chinchilla laniger) or two species, the long-tailed C. laniger and the short-tailed C. brevicaudata. These animals, long known for soft, attractive fur, naturally inhabit the rocky regions of the Chilean and Bolivian Andes and subsist on grain, herbs, and moss. Once hunted almost to extinction and still scarce in the wild, chinchillas are now raised commercially in ‘‘farms.’’ Almost all of the chinchillas in captivity used for commercial breeding are descended from a few animals introduced into the United States in the 1920s. Some 80,000 chinchillas are kept as household pets [4]. The skin and fur of the chinchilla often harbors several common superficial fungi. Trychophyton
mentagrophytes and Microsporum gypseum have been recovered from chinchillas; these organisms have actually been responsible for symptomatic animal dermatophytosis [39 – 42]. Because these organisms are well established as etiologic for human disease, it is not unreasonable to suspect the chinchilla as the source of infection in an owner who presents with acute, inflammatory tinea corporis or tinea capitis (Fig. 3). Several nondermatophytes have also been isolated from the chinchilla, including Aspergillus niger, Cladosporium spp, and Rhizopus species [43]. Such saprophytes might become opportunistic pathogens in select individuals such as diabetics, organ transplant patients, bone marrow transplant recipients, and leukemia patients. Hence, the chinchilla might not be a good choice for a pet in these circumstances. Chinchillas also have a predilection for harboring Klebsiella pneumoniae and Pseudomonas aeruginosa [44,45]. These organisms can be isolated from chinchillas with unapparent disease, or they might be discovered after the chinchilla’s demise from bacterial sepsis. Because these organisms are well recognized as potential human pathogens, signs and symptoms suggestive of Gram-negative sepsis in a chinchilla owner (especially an owner who is immunocompromised or diabetic) should be heeded carefully.
Cockatoo The colorful cockatoo is among the most popular of ornamental pet birds. There are 18 distinct species falling into the overall category of ‘‘cockatoo.’’ The majority of these parrot relatives are native to Aus-
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Fig. 3. Inflammatory tinea corporis in a chinchilla owner.
tralia, Indonesia, and the Philippine Islands. Though not possessing as prolific a vocabulary retention as a parrot, the cockatoo offers the singular advantage of being a long-lived pet; birds in this category survive 30 to 80 years in a comfortable home environment. In common with pigeons, the cockatoo is a potential source of infection caused by Cryptococcus neoformans serotypes A and D. Generally, the bird remains well, but sheds the fungus in its feces, contaminating the birdcage and ambient air in close proximity to the cage [46,47]. On rare occasions, the cockatoo itself can develop cryptococcal disease [48]. A recent case report elegantly demonstrated that cryptococcosis can be transmitted from an infected
pet cockatoo to a susceptible human owner, in this instance an elderly renal transplant patient [49]. In the report cited, patient and cockatoo isolates were indistinguishable based upon biochemical profiles, monoclonal antibody binding patterns, restriction fragment length polymorphism analysis, and karyotyping. From the dermatologist’s viewpoint, cryptococcosis can present in many fashions, including cellulitis, lesions resembling molluscum and herpes, and Kaposi’s sarcoma-like papulonodules (Fig. 4). The close association of the cockatoo with cryptococcal disease has led to the strong suggestion that immunosuppressed and immunocompromised patients should avoid choosing this bird as a pet [49,50].
Fig. 4. Nodular cutaneous cryptococcosis in an HIV+ cockatoo owner.
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As is true of almost any bird, the cockatoo can carry avian mites such as the northern fowl mite (Ornithonyssus sylvarium) and the chicken mite (Dermanyssus gallinae). Although such ectoparasites are more commonly associated with the commercial poultry industry or with wild nesting birds (eg, starlings and pigeons), they can also infest various birds used as house pets (eg, canaries, doves, finches, parakeets, and other psitticine species) [51,52]. Avian mites can cause an intensely pruritic, localized to generalized, papular to papulovesicular eruptions in an unsuspecting and incidental human host. Avian mites can be introduced into the environment not only by affected birds but also by other pets that seemingly acquired acariasis from birds housed at the same pet store. For example, two cases of avian mite dermatitis were recently reported to arise from infested pet gerbils [53]. Because avian mites cannot reproduce on a human host, infection with this type of organism is self-limiting if the source of the mites is permanently removed, or if the birdcage is cleaned and the pet bird disinfected with acaricide; temporary relief from pruritus in the incidental human host can be obtained with application of potent topical steroids.
Summary Zoonoses are diseases that can be transmitted from animals to humans. More than 250 distinct zoonoses have been described in the literature. It is estimated that 56% of United States households contain at least one pet, and although considerable research has been performed regarding the more common household animals including dogs, cats, small birds, and rodents, surprisingly little is known about the zoonotic hazards of owning the more exotic pets [54 – 57]. According to the 1997 USPHS/IDSA Report on the Prevention of Opportunistic Infections in Persons Infected with Human Immunodeficiency Virus, the immunocompromised patient should avoid contact with feces-laden soil, litter boxes, reptiles, most pet birds, and any animal less than 6 months old [58]. It has also been documented that because of their inquisitive nature, children are at even higher risk for infection from animals than adolescents or immunocompetent adults [54]. In this article the authors have reviewed the available data regarding hazards associated with the hedgehog, flying squirrel, iguana, chinchilla, and cockatoo. With the growing popularity of such exotic pets, further observation and research is warranted. Physicians need to be aware of the possibility of
zoonotic disease related to exotic pet ownership, and they should address this issue when obtaining a history and formulating a differential diagnosis of cutaneous lesions suggestive of such illnesses.
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