Table Of ContentDermatolClin21(2003)xi–xii
Preface
Infectious diseases
TedRosen,MD
GuestEditor
Thisplaguehascomeuponusbyinfection,and mankind. The ability of unusual organisms such as
itwillspreadstillfurther,justasinthefieldsthe Vibrio species from sea water, achloric algae from
scab of one sheep or the mange of one pig, stagnant fresh water, tick-borne microbes, and sap-
destroystheentireherd.—Juvenal,fromSatires, rophyticfungifromsoiltoactashumanpathogensis
II.78,c.120A.D. discussed herein. The increasingly commonplace
You never win because microbes are part of practiceofkeepingexoticanimalsashouseholdpets
nature.Theywillconstantlyemerge.Ifwecome also has led to the real probability of acquiring
to terms with that and if we are smart and cutaneous and systemic disease. This subject is
quick...we’llbeaheadofthem.—Dr.MikeRyan explored in depth with an emphasis on the most
common unusual pets (hedgehog, chinchilla, iguana,
Inthenearly1900yearsthatelapsedbetweenthe flyingsquirrel,andcockatoo).
timeoftheRomansatiristandpoet,Juvenal,andthe Industrious and energetic pharmaceutical re-
current era, mankind has remained at constant risk searchershavecreatednewdrugstocombatdisease.
from infectious diseases. The virtual planetary erad- Cidofovir, ivermectin, albendazole, imiquimod, and
ication of smallpox has proven the potential power variousvaccineproductsaresuchmedications,allof
rationalbeingscanhaveovernature.Bycontrast,the which are summarized in this issue. New drugs
relatively recent emergence of the Human Immuno- exploredincludeagentsdesignedtocounterprimarily
deficiencyandEbolavirusesandthedevelopmentof viral and parasitic diseases. The host of choices
resistance to routine treatments (now manifested by awaiting the practitioner confronted with acyclovir-
lowlyheadlice)demonstratethenever-endingcapac- resistant herpetic infection is outlined along with
ity of microbes to maintain the upper hand in this some of the more promising anti-herpetic drugs of
epicstruggle. the future that arenotyet commercially available.
InthisissueofDermatologicClinicsIhaveused The expanding role of simple and complex cuta-
my position as guest editor to select topics that neoussurgeryperformedbydermatologistshasadded
highlight this constant battle between nature and yet another dimension to the potential for infectious
0733-8635/03/$ – seefrontmatterD2003,ElsevierScience(USA).Allrightsreserved.
doi:10.1016/S0733-8635(02)00091-8
xii T.Rosen/DermatolClin21(2003)xi–xii
disease.Thisissueaddresseswoundinfectionsandthe diseases. I hope this issue will fill in gaps in the
somewhatcontroversialroleofantibioticprophylaxis readers’informationbase.
associatedwithdermatologicsurgery.
ThefactthatBacillusanthracisrecentlywasused TedRosen, MD
as a weapon of bioterrorism, and that the correct Department of Dermatology
diagnosis was made by a dermatologist, underscores BaylorCollegeof Medicine
thenecessityforallhealthcareproviders—including Houston VAMedical Center
thoseofuswhopracticecutaneousmedicine—tohave Houston, TX,USA
a broad depth of knowledge regarding infectious E-mail address: [email protected]
DermatolClin21(2003)229–236
Infectious threats from exotic pets:
dermatological implications
Ted Rosen, MDa,*, Jennifer Jablon, MDb
aDepartmentofDermatology,BaylorCollegeofMedicine,2815Plumb,Houston,TX77005,USA
bDepartmentofInternalMedicine,St.Joseph’sMercyHospital,5301E.HuronDrive,AnnArbor,MI48106,USA
Duringthepastfivedecades,aconsiderablebody (or Cape) hedgehog, the Egyptian (or long-eared)
of information regarding exotic animals has been hedgehog,andthespeciesAtelerixalbiverntris,better
generated.Suchinformationhaslargelybeenutilized known as the African pygmy hedgehog [1–3]. The
tostudysurvivalskills,migratinghabits,orcausesfor African pygmy hedgehog has become a common
a decline in species number; however, this body of householdaddition,withanestimated40,000house-
information has also become important for a new holds in the United States harboring this pet [4].
reason: many Americans are inviting these exotic Although hedgehogs are often considered to be
animalsintotheirhomesaspets.Neitherpetowners benign, easily maintained, small versions of porcu-
nor non-veterinary health care providers are suffi- pines, they can pose some rather unique threats to
ciently knowledgeable about the possible medical theirhumanowners,includingfungalandsalmonella
problemscausedbytheseanimals.Hedgehogs,flying infections,contacturticaria,andpossiblymycobacte-
squirrels, iguanas, chinchillas, and cockatoos com- rium infections. The African pygmy hedgehog has
prise a major part of this trend toward novel exotic recently been strongly implicated as a cause of
pets residing in American households. Such animals moderate to severe cutaneous dermatophytosis [3].
can be associated with cutaneous infections, acute Thethreeindividualsdescribedinthisreportwerein
andchronicsystemicillnesswithskinsigns,andeven contact with an African pygmy hedgehog, and
fatality. Moreover, such animals have been found to lesional cultures yielded an organism (Trichophyton
harbor dangerous microorganisms that, although not mentagrophytes), which is known to be frequently
yet directly linked to human infection, have the carried on the quills and the underbelly in this
potential to cause devastating disease. Health care particular species of hedgehog [5]. One of the
providersneedtobemoreawareoftherisksentailed patients reported merely handling the hedgehog in a
by exotic pet ownership and to remember to inquire petstoreforaperiodof1to2minutes,indicatingthat
aboutsuchpetswhileobtainingamedical historyor this infection might be highly contagious if the
formulatingadifferential diagnosis. animalisheavilycolonized(Fig.1).Additionalcases
oftineacorporis[6–9]andtineacapitis[10,11]have
been reported following contact with wild European
Hedgehog hedgehogs and their natural habitat, further suggest-
ingthathedgehogpetsmighttrulybeaviablesource
There are eleven species of hedgehog, the most ofdermatophytosisintheirunsuspectingowners.The
prevalentbeingtheEuropeanhedgehog,thePruner’s hedgehog has also been implicated in one case of
contact urticaria, which was most likelycaused bya
hypersensitivity response to hedgehog saliva, which
the animal deposits on its quills [12]. The worst
* Correspondingauthor. hazard to human owners of hedgehogs has been
E-mailaddress:[email protected](T.Rosen). salmonellosis. The African pygmy hedgehog has
0733-8635/03/$ – seefrontmatterD2003,ElsevierScience(USA).Allrightsreserved.
doi:10.1016/S0733-8635(02)00090-6
230 T.Rosen,J.Jablon/DermatolClin21(2003)229–236
Fig.1.MassivetineamanumfollowingexposuretoanAfricanpygmyhedgehog.
beenclearlyimplicatedinhumansalmonellosisinthe utilizing parachute-like membranes that are con-
United States and Canada [13,14]. Although it has nected on each side to their forelegs and hindlegs.
beenpresumedthatthisinfectionresultsfrominges- Thereare35speciesofflyingsquirrelsinthefamily
tionoffoodinadvertentlycontaminatedbyhedgehog Sciuridae,butonlytwoarefoundinNorthAmerica,
feces, the actual mechanism of salmonellosis Glaucomys volans and Glaucomys sabrinus [18].
acquiredfromhedgehogshasnotbeenclearlyestab- These animals are known to nest in birdhouses or
lished. Human salmonellosis can vary from dehy- buildings. These closely related species, collectively
dratingdysenterytomeningitisandtoxicbacteremia. known as New World flying squirrels, have recently
It can be a serious illness, especially in the young, become popular household pets, with the estimated
old,andimmunocompromised.AlthoughtheAfrican 5000to 8000owners inthe UnitedStates [4].
pygmy hedgehog has not yet been documented to Although the flying squirrel has beenproclaimed
carry any mycobacterial diseases, the European to be a friendly and intelligent pet, especially when
hedgehoghasbeenfoundtocarrytheMycobacterium domesticated as a newborn, it should be noted that
species M. marinum and M. avium–intracellulare such animals might be the source of a number of
[15,16], which suggests that it is possible for the dangerous infections. Some flying squirrels have
former variety to do so as well. Such organisms been reported to harbor the proliferative stages of
readily cause infection—even of a fatal nature—in Toxoplasma gondii, the organism responsible for
immunocompromised patients [17]. Such patients potentially fatal toxoplasmosis in humans [19]. It is
should strictly avoid any potential sources of these not known how the squirrels were infected; it is
organisms,andhedgehogsarenotrecommendedpets hypothesized that Toxoplasma gondii might be a
for patientswith HIV disease. congenitally acquired infection because the squirrel
is an herbivore and the main method of parasite
acquisitionisingestionofrawmeatcontainingcysts.
Flyingsquirrel Althoughtherearenodocumentedreportsofhuman
toxoplasmosis from flying squirrels, the fact that a
There are two distinct groups of rodents that are herbivoresuchastheflyingsquirrelcanacquirethis
often referred to as ‘‘flying squirrels.’’ Members of diseaseleavesopenthepossibilitythatownerscould
the first group, consisting of African rodents with be at risk. Other potentially dangerous microorga-
scalytailsinthefamilyAnomaluridae,arenotsoldas nisms harbored by flying squirrels are unusual and
pets. The second group contains the more familiar aggressive species of the bacterium Staphylococcus.
NorthAmericanandEurasianflyingsquirrelsandthe In one study, virtually all of the flying squirrels
Australian sugar glider from the subfamily Petau- captured in Raleigh, North Carolina carried three
ristinae of the family Sciuridae. The term ‘‘flying atypical strains of staphylococcus on their skin:
squirrel’’ is somewhat of a misnomer because these Staphylococcus sp. 3, S. sciuri, and S. xylosus [20].
animalsactuallymakeglidingleapsofupto150feet In the same study, these three strains were found
T.Rosen,J.Jablon/DermatolClin21(2003)229–236 231
(uncommonly) on human skin, with the prevalence purchase,andtherearenowsome700,000suchpets
being 0%, 10%, and 42% respectively. S. sciuri and in the United States [4]. Other well-known species
S. xylosus grow poorly on agar at pH 5.3 or below, include I. delicatissima of the Caribbean islands,
explainingwhytheyarerareonhumanskin(pH5.0); Cyclura cornuta of Haiti, Dipsosaurus dorsalis, the
however,thesespeciesgrowwellatpH7.0orabove, desert iguana of Mexico and the United States,
making them a danger if, as a human skin contam- Amblyrhynchuscristatus, the marine iguana, andthe
inant, they enter the bloodstream through a wound. Conolophus iguanas ofthe Galapagos Islands.
TheinvivopHofhumantissuesisbetween7.35and I. iguana is a greenish-colored animal with
7.45, an ideal environment for this organism to overlaidbrownbands.Itusuallyeatsfruitandleaves,
proliferate. In this same study, Staphylococcus sp. 3 but it will also eat small birds and mammals. This
was isolated only from the flying squirrel, raccoon, 20-poundreptilecangrowupto6feetlongandposes
opossum,andtheeastern graysquirrel, butnotfrom adomicilliarychallengethatisoftenmetbyallowing
human skin. Considering its novelty, this species ittoreside/sleepinanextrahouseholdbathtub!Many
would pose a threat to a human who would have potentially pathogenic bacteria have been isolated
little tonoimmunity against it. from the iguana pharynx, including Staphylococcus
There is evidence Glaucomys species serve as an sp, Streptococcus sp, Serratia sp, Corynebacterium
extrahuman reservoir for typhus. Epidemictyphus is sp, Alcaligenes sp, and from the cloaca, including
causedbyinfectionwithRickettsiaprowazekiiandis Micrococcussp,Bacillussubtilis,Salmonellamarina,
usuallytransmittedfromperson-to-personbywayof Salmonellachameleon,Escherichiacoli,andHafnia-
the human body louse. The last major outbreak of like species [26]. The organisms from the pharynx
louse-borne typhus in the United States was in the have the potential to cause serious cellulitis if the
1920s,butsporadiccasesofamilderformoftyphus iguanabites.Infact,thereareseveralsuchreportsin
occurringinpeoplelivinginruralenvironmentshave theliterature[27–29].Serratiamarcescensinfection,
been attributed to contact with flying squirrels [21– asdeterminedbywoundcultureinonereportedcase
24].Themodeoftransmissionbetweenflyingsquir- [27],isparticularlydifficultinthatitmightmanifest
rel and human has not been firmly established, as rapidly progressive, bullous cellulitis associated
although experimental work suggests that transmis- with extreme systemic toxicity (Fig. 2). Iguanas are
sion to humans might occur through inhalation of commonly treated by breeders with broad-spectrum
aerosolized ectoparasite feces or directly by way of prophylactic antibiotics to prevent disease and dis-
thebiteofaninfectedectoparasite[25].Inonestudy, coloration [30]. Although this practice is frequently
serological evidence of typhus infection was estab- unsuccessful, it might result in the development of
lished only in flying squirrels, not the lice or ticks drug-resistantbacteria,furthercomplicatingtheman-
foundontheirskin[22],whereasanotherstudyfound agement of cellulitis following aniguanabite.
that commensal fleas and lice—and their host flying A series of investigations in the 1970s led to the
squirrels—wereinfected[24].Althoughsuchdisease discovery of a new herpes-type virus isolated from
has been a milder form of typhus, all patients pre- thepharynxofthecommonpetiguana[31,32].This
sentedwithoneormoreofthefollowingsymptoms: viruswasthefirsttobeisolatedfromreptiles,andit
fever, typical louse-born epidemic typhus rash appearedtopossessacapabilityforcausinglatentor
(blanchable erythematous macules spreading to the unapparent infections consistent with mammalian
trunkandextremitiesfromtheaxillaryfolds),nausea, herpesviruses. This virus has not been implicated in
vomiting, headache, myalgia, photophobia, malaise, human infection to date, but it remains another
and dizziness. One woman died from renal compli- potential complication ofaniguanabite.
cations [23]. Thus, the combination of fever, rash, Most allergic responses to pets occur in asso-
andsystemictoxicityinanownerofaflyingsquirrel ciationwiththefur(dander)oftheimplicatedanimal;
shouldsuggest typhus as apossiblediagnosis. however,atleastonewell-documentedcaseofaller-
gicrhinitis,asthma,andurticariahasbeenreportedto
be caused by an iguana [33]. The allergic nature of
Iguana thisreactionwasverifiedbydemonstratingapositive
intradermal skin test to an aqueous extract prepared
Therearethirteeniguanaspecieswithinthelarger from iguanascale.
members of the lizard family Iguanidae. The best The iguana is best known for its potential for
known and most common is the reptile Iguana transmittingsalmonellatohumans.Therehasbeena
iguana, which naturally inhabits Southern Mexico significant increase in nontyphoidal salmonellosis,
and Brazil. This particular lizard is inexpensive to which is generally acquired from animals. Approx-
232 T.Rosen,J.Jablon/DermatolClin21(2003)229–236
Fig.2.Serratiamarcescenscellulitisfollowinganiguanabite.
imately4millionsuchcasesweretabulatedin1995; mentagrophytes and Microsporum gypseum have
these infections were believed to be caused by been recovered from chinchillas; these organisms
infected eggsandpoultry andpet iguanas[6]. There have actually been responsible for symptomatic ani-
have been many reports of enteric salmonellosis mal dermatophytosis [39–42]. Because these orga-
acquired from pet iguanas in the United States nisms are well established as etiologic for human
[34–36], an 83% rate of fecal shedding of salmo- disease, it is not unreasonable to suspect the chin-
nella from pet iguanas [37], and scattered reports of chilla as the source of infection in an owner who
salmonella meningitis associated with iguana own- presents with acute, inflammatory tinea corporis or
ership [38]. From a dermatological standpoint, non- tineacapitis(Fig.3).Severalnondermatophyteshave
typhoidalsalmonellainfectioncanbeassociatedwith also been isolated from the chinchilla, including
a nondescript, generalized erythematous papular Aspergillus niger, Cladosporium spp, and Rhizopus
eruption. Thus, the clinical situation of diarrhea species[43].Suchsaprophytesmightbecomeoppor-
and a rash in an iguana owner should strongly tunistic pathogens in select individuals such as dia-
suggest salmonellosis as the etiology. betics, organ transplant patients, bone marrow
transplant recipients, and leukemia patients. Hence,
thechinchillamightnotbeagoodchoiceforapetin
Chinchilla these circumstances.
Chinchillasalsohaveapredilectionforharboring
The chinchilla is a small South American herbi- KlebsiellapneumoniaeandPseudomonasaeruginosa
voreofthefamilyChinchilladaeoftheorderRoden- [44,45]. These organisms can be isolated from chin-
tia. There is some debate regarding whether the chillas with unapparent disease, or they might be
chinchilla is one species (Chinchilla laniger) or two discoveredafterthechinchilla’sdemisefrombacterial
species,thelong-tailedC.lanigerandtheshort-tailed sepsis. Because these organisms are well recognized
C.brevicaudata.Theseanimals,longknownforsoft, as potential human pathogens, signs and symptoms
attractive fur, naturally inhabit the rocky regions of suggestive of Gram-negative sepsis in a chinchilla
theChileanandBolivianAndesandsubsistongrain, owner (especially an owner who is immunocompro-
herbs, and moss. Once hunted almost to extinction misedordiabetic)shouldbeheededcarefully.
andstillscarceinthewild,chinchillasarenowraised
commerciallyin‘‘farms.’’Almostallofthechinchil-
las in captivity used for commercial breeding are Cockatoo
descended from a few animals introduced into the
United States in the 1920s. Some 80,000 chinchillas Thecolorfulcockatooisamongthemostpopular
arekept as householdpets[4]. ofornamentalpetbirds.Thereare18distinctspecies
The skin and fur of the chinchilla often harbors falling into the overall category of ‘‘cockatoo.’’ The
several common superficial fungi. Trychophyton majority of these parrot relatives are native to Aus-
T.Rosen,J.Jablon/DermatolClin21(2003)229–236 233
Fig.3.Inflammatorytineacorporisinachinchillaowner.
tralia, Indonesia, and the Philippine Islands. Though pet cockatoo to a susceptible human owner, in this
notpossessingasprolificavocabularyretentionasa instanceanelderlyrenaltransplantpatient[49].Inthe
parrot, the cockatoo offers the singular advantage of reportcited,patientandcockatooisolateswereindis-
beingalong-livedpet;birds inthiscategorysurvive tinguishablebaseduponbiochemicalprofiles,mono-
30to 80yearsin acomfortable homeenvironment. clonalantibodybindingpatterns,restrictionfragment
In common with pigeons, the cockatoo is a length polymorphism analysis, and karyotyping.
potentialsourceofinfectioncausedbyCryptococcus From the dermatologist’s viewpoint, cryptococcosis
neoformans serotypes A and D. Generally, the bird can present in many fashions, including cellulitis,
remains well, but sheds the fungus in its feces, lesionsresemblingmolluscumandherpes,andKapo-
contaminating the birdcage and ambient air in close si’s sarcoma-like papulonodules (Fig. 4). The close
proximitytothecage[46,47].Onrareoccasions,the associationofthecockatoowithcryptococcaldisease
cockatooitselfcandevelopcryptococcaldisease[48]. has led to the strong suggestion that immunosup-
A recent case report elegantly demonstrated that pressed and immunocompromised patients should
cryptococcosis can be transmitted from an infected avoid choosingthis birdas apet [49,50].
Fig.4.NodularcutaneouscryptococcosisinanHIV+cockatooowner.
234 T.Rosen,J.Jablon/DermatolClin21(2003)229–236
As is true of almost any bird, the cockatoo can zoonoticdiseaserelatedtoexoticpetownership,and
carry avian mites such as the northern fowl mite they should address this issue when obtaining a
(Ornithonyssus sylvarium) and the chicken mite history and formulating a differential diagnosis of
(Dermanyssusgallinae).Althoughsuchectoparasites cutaneous lesionssuggestive of suchillnesses.
are more commonly associated with the commercial
poultry industry or with wild nesting birds (eg,
starlings and pigeons), they can also infest various
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