Squirrel Zoonoses J. Jill Heatley DVM MS DABVP (Avian), DACZM Associate Professor, Zoological Medicine College of Veterinary Medicine & Biomedical Sciences Texas A&M University, College Station

Tree SquirrelS Gray... Tassel-eared...Sciurus aberti Fox Tamiascirus Western - Sciurus griseus Eastern – Sciuris carolinensis Arizona ...Sciurus arizonensis Tassel-eared...Sciurus aberti Fox Eastern Fox....Sciurus niger Apache Fox.....Sciurus apache Tamiascirus American Red.....Tamiasciurus hudsonicus Chickaree......Tamiasciurus douglasi Flying Squirrels – Northern Southern and Glaucomys volans

What is a Squirrel ? Order Rodentia All continents Family Sciuridae Except Antarctica, Australia 50 genera, 273 species Subfamily Cyonomys – Prairie Dogs Spermophilus – Ground squirrels Marmota – Marmots Ammospermophilus – Antelope Squirrels Tamias – Chipmunks Tamiasciurus – Chickarees Sciurus – Tree Squirrels Glaucomys – New World flying squirrels

Interface Expanding urban communities Parks, neighborhoods Bird feeders Nature Vacation Exotic Pets Research Rehabilitation Hunting

Zoonotic Disease Bacterial Fungal Parasitic Viral Prion Literature review

Parasitic zoonoses Toxoplasma gondii Intermediate not definitive host Cryptosporidium parvum Eastern gray squirrel Chipmunk Red squirrel California Gray squirrel Hymenolepis nana Dwarf tapeworm of hamsters Human enteric disease Praziquantel Mange in squirrels is generally notoedric or demodectic and not transmissable to humans

Bacterial Zoonoses Squirrel Bite fever Lyme Disease Epidemic Typhus Tularemia Plague Leptospirosis Rat Bite fever Squirrel Bite fever Streptobaccillus moniliformis Spirillum minus Red legged ground squirrel Xerus erythropus Nigeria Campylobacter spp. Salmonellosis Pasteurella multocida Red squirrel Yersinia pseudotuberculosis White tailed antelope squirrel Citellus lecurus Yersinia enterocolitica Grey squirrel Zoonoses Squirrel Disease

Tularemia Isolated in 1912 Zoonoses Plague like disease of rodents Plague foci search Bacterium tularense Francisella tularensis Tulare county of origin, CA Ground squirrels Spermophilus beecheyii Zoonoses Sciurus carolinensis Infant Bite Arkansas Prairie Dog (BT Cyonomys ludovicianus) Titer positive 3 y with bite Fox Squirrel Skinned/dressed Alcala Minagorre, PJ [Francisella tularensis infection transmitted by prairie dog An.Pediatrics (Barc)2004 Jun 60(6) 583-4 Tularemia is a zoonosis caused by Francisella tularensis; it mainly affects wild animals and only occasionally affects human beings. Uncontrolled trade involving "exotic" animals could become a new route of acquisition. We report the case of a 3-year-old boy who contracted the disease through a bite from a prairie dog. Outbreaks of tularemia have recently been described in some of these animals captured in Texas (USA) and subsequently sold to other countries. Infection due to Yersinia pestis has also been described in humans through contact with prairie dogs with the disease. Streptomycin and gentamicin are currently the drugs of choice against tularemia infection. Citellus columbianus columbianus Columbian ground squirrel Citellus beecheyi Beechey ground squirrel Eutamia sp. Chipmunk Citellus richardsonii Richardson ground squirrel Citellus pygmaeus Little ground squirrel Magee JS et al. Tularemia trans by Squirrel Bite. Pediatric Infect Dis J.1989Feb8(2):123-5. Avashia SB at al Emerging Infec Dis 10(3) March 2004 Kirkwood T. Tularemia from the Fox Squirrel JAMA 1931; 96(12);941-942

Leptospirosis Multiple species Zoonosis Isolations - serovars Gray squirrel - ballum Fox squirrel - grippotyphosa Zoonosis Leptospira kirschneri Southern Flying squirrel Glaucomys volans Exported to Japan 28 29 yo males Leptospirosis in Squirrels Imported from United States to Japan. Masuzawa T Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 12, No. 7, July 2006 J Am Vet Med Assoc. 1975 Oct 1;167(7):587-9. Leptospirosis in selected wild mammals of the Florida panhandle and southwestern Georgia. Shotts EB Jr, Andrews CL, Harvey TW. 144 wild mammals, white-tailed deer, cottontail rabbits, fox squirrels, gray squirrels, raccoons, opossums, a bobcat, and various small rodents was examined for cultural or serologic evidence of leptospiral infection. Leptospires were isolated from 1 of 25 rabbits, 1 of 27 fox squirrels, 1 of 26 gray squirrels, 4 of 18 mice and rats, 8 of 21 raccoons, 7 of 17 opossums, and a bobcat.. Serotypes isolated were Leptospira interrogans, serotype grippotyphosa and L interrogans, serotype ballum. New host-serotype relationships were noticed in the following instances: bobcat: grippotyphosa, and gray squirrel: ballum. These studies further confirm the occurrence of grippotyphosa in the fox squirrel. Serologic response in these animals did not necessarily correlate with isolations, although some relationship was noticed in raccoons and opossums N Engl J Med. 1967 Apr 13;276(15):838-42. Human leptospirosis acquired from squirrels. Diesch SL, Crawford RP, McCulloch WF, Top FH Incidence of Leptospirosis in Wild Mammals from Southwestern Georgia, with a Report of New Hosts for Six Serotypes of Leptospires S. McKeever, G. W. Gorman, J. F. Chapman, M. M. Galton AND D. K. Powers From November 4, 1954, to March 20, 1956, 1,091 mammals were trapped in southwestern Georgia. Of these, 820 were tested for leptospires by culturing kidney tissue, and 44 (5.4%) were found positive. The leptospires involved were identified by agglutination and cross-agglutinin-adsorption tests as serologically homologous to L. ballum, L. pomona, L. australis A, L. grippotyphosa, and serotype members of the L. hebdomadis and L. mitis-hyos serogroups. The hosts were as follows: opossum for L. ballum and members of the L. mitis-hyos serogroup; gray fox for L. ballum; raccoon for L. ballum, L. pomona, L. australis A, L. grippotyphosa, and a member of the L. hebdomadis serogroup; striped skunk for L. ballum and L. pomona; and wildcat for L. ballum and L. pomona. No correlation was found between the incidence of infection by a given serotype of leptospires and density of the various species of mammals or the total mammalian population. The isolation of L. australis A., L. grippotyphosa, and organisms belonging to the L. mitis-hyos and L. hebdomadis serogroups is of primary significance. Only a few reference laboratories are routinely testing for the presence of antibodies to these pathogens in either man or domestic animals. There is a need for inclusion of antigens of these serotypes of leptospires in routine agglutination tests and for more intensive efforts to isolate leptospires from suspected cases in humans and domestic animals. The following new host records were established: gray fox for L. ballum; raccoon for L. ballum, L. pomona, L. australis A, L. grippotyphosa, and a member of the L. hebdomadis serogroup; striped skunk for L. ballum and L. pomona; wildcat for L. ballum and L. pomona; and opossum for members of the L. mitis-hyos serogroup.

Lyme disease Borrelia burgdorferi sensu latu Reservoirs Spirochetal bacteria Most common tick borne disease Debilitating chronic infection Tick intermediate Reservoirs Western Gray squirrel Eastern chipmunk Tamias straitus – eastern & upper midwestern US Persistent infection, no clinical signs Ixodes scapularis European reservoir potential Gray squirrel Sciurus carolinensis European tree squirrel – S. vulgaris

Epidemic or Louse Borne Typhus Bacterium Rickettsia prowazekii Clinical Signs Fever, Headache, Muscle pain Rash – trunk spreads to extremities Doesn’t involve the palms or soles (cf RMSF) Mort ~ 40% if untreated Primary Vector Human Body Louse

Epidemic Typhus Sporadic cases in Eastern US since 1970s Most cases in winter when squirrels nest in attics All non fatal, humans faster recovery with antibiotics Flying squirrels Glaucomys volans Handled, squirrels nests, pets in home Capable reservoirs Transient inapparent infection Squirrel human transmission unknown Sucking lice (Neohematopinus sciuropteri) Fleas transmit to squirrels in lab Direct contact, inhalation of dried squirrel excretions bites of squirrel ectoparasites Sucking lice Flea

Plague Bacterium - Yersinia pestis Complex flea rodent cycle Sylvatic reservoir Human clinical signs Severe disease Fatality rate > 50% if untreated Rare - Dozen cases / year Semiarid West New Mexico Arizona Colorado California

Plague Periodic plague outbreaks More susceptible rodent hosts Flea vector (Flea control!!!) CS: nonspecific: lethargy, depression, respiratory distress, lymphadenopathy, anorexia Serologic testing More susceptible rodent hosts Prairie dogs Known reservoir Ground squirrels Fox squirrels Human exposure occurs during outbreaks Flea bites Direct contact w nonrodent hosts Trend of eastward expansion Epizootic fox squirrels central Texas

Fungal Zoonoses Dermatophytosis Sporotrichosis Sporothrix schenckii Unknown Sciurid, not captured Bite 1.5 months earlier in the park Severe arm lesion responded to 3 months of antibiotic and antifungal therapy Lymphocutaneous Sporotrichosis Associated with a Squirrel Bite: Case Report and Review PS Saravanakumar, P Eslami FA Zar Clinical Infectious Diseases, 23(3)3 Sep 1996) 647-648.

Dermatophytosis Gray Squirrels Dermatomycoses, Tinea, “Ringworm” May accompany parapox fibromas Systemic Phycomycosis Circular shape, scaly raised border Patchy hair loss Neck , head ,armpits, abdomen Skin reddening, thin layer serous exudate, crusts, skin nodules Hair broken off at skin surface, Fine stubble broken hair Lewis et al. JWD Oct 1975 Urban Gray squirrel mycology Lesions Etiologies

Dermatophytosis Gray Squirrels Trichophyton mentagrophytes Mucor Candida albicans Microsporum gypseum, Scopulaiopsis brevicaulis Microsporum cookei Systemic Phycomycosis Dermatiaceous Fungi – pigmented Phaeoannellomyces wernecklii Damp weather conditions Prevalence > 50%

Rule out Alopecia Histology Zoonotic Sciurus carolinensis Glaucomys volans Dietary, heritable? Congenital Alopecia Dermatophytosis Louse Bite Lesions Notoedric Mange Larval Harvest Mite Lesions Histology Fungal organisms in superficial skin, in and around hairs History, Lesions Direct examination Culture Identify specific fungus Zoonotic Young animals more commonly affected One researcher developed lesions after handling squirrels Use gloves, wash with soap after handling

Viral Zoonoses Lymphocytic Choriomeningitis Virus Gray squirrels serologically positive UK 4/19 Snowshoe hare virus (SSHV) Arboviruses West Nile Virus Western Equine Encephalitis Lacross Virus Eastern Equine Encephalitis Rabies Gray squirrel No human cases associated with squirrel bite Monkeypox Virus Encephalomyocarditis virus Serological evidence of murine pathogens in wild grey squirrels (Sciurus carolinensis)in North Wales A. G. GREENWOOD, S. SANCHEZ The Veterinary Record, April 27, 2002 White et al. Micro Study of Urban Gray squirrel 1975 JAVMA 167

WEE EEE VEE Alphaviruses, Togaviridae WEE rare disease in people Lacrosse Virus, EEE (mort 50%), VEE rare serious disease Mosquito vector Hosts (Black tailed jack rabbit, White footed mouse?, ?) Lacrosse Encephalitis – Tree squirrels and chipmunks primary amplifying hosts WEE Viremia – Gray squirrels (Sciurus carolinensis), California ground squirrels, San Joachin antelope ground squirrels, Aggressive, bite people, Usu fatal, may survive overwinter Richardson’s ground squirrels (Spermophilus richardsonii) contaminated urine, cannibalism Experimental Infection Weak, depressed, ataxic, limb paralysis prior to death Some became hyperexcitable Brain, brainstem Necrosis & edema EEE - Gray squirrels Peripheral inoculation: Encephalitis & death VEE – Significant viremia, > 50% mort Mexican ground squirrel - Spermophilus mexicanus Gray squirrel

SnowShoe Hare Virus Bunyaviridae Antibodies Variant of the La Crosse virus Encephalitis occasional - NY, Eastern Canada Antibodies Experimental infection ground squirrels Symptomless viremia Artic ground squirrels Spermophilus parryii Golden mantled ground squirrels Spermophilus lateralis Yellow-pine chipmunks Eutamias amoenus Red squirrels Newhouse 1967 Field and lab studies on the hosts and vectors of the SSHV Mosquito news 31:401-408

West Nile Virus Encephalitis virus Fox squirrel (Sciurus niger) Seroconversion late summer early fall None in urine, fleas Exp: feces and oral cavity Experimental infection suggests amplifying host High seroprevalence Western gray squirrel (S. griseus) Eastern gray squirrel (S. carolinensis) 3/36 live neurologic tree squirrels viremia similar to WNV-infected birds. Most squirrels no virus in serum S. carolinensis not amplifying hosts low viremias, lack of mortality Low seroprevalence 2% Useful as sentinels Pull papers do better contrast comparison

Kyansur Forest Disease Tick borne encephalitis flavivirus complex 1956 epidemic of people and monkeys Fever, hypotension hepatomegaly, hemorrhage/neuro/bronchopneumonia recovery/late fever Southern india - 2500 m radius Striped palm squirrels Funambulus tristriatus Antibodies Viremic infective for Ticks

MonkeyPox Virus Orthopox virus Main host African tree squirrels Broad primate host range includes humans Fever rash resembles small pox Low mortality high morbidity Infection via direct contact Main host African tree squirrels Tree squirrels Heliosciurus rufobrachium H. gambianus Rope Squirrels Funisciuris anerythrus F. lemniscatus Prairie dogs Poorly competent host Effective transmitters for veterinary staff

Diseases Infectious Monkey Pox Humans 1-10% mortality Contact, respiratory droplets CS: fever, cough, conjunctivitis, lymphadenopathy, nodular rash No treatment Strict biosecurity, humane euthanasia CDC website www.cdc.gov/ncidod/monkeypox Final rule prohibits capture, offers to capture, transport, sale, barter, exchange, distribution, or release of a listed animal into the environment. Prairie dogs (Cynomys sp.) African Tree squirrels (Heliosciurus sp.), Rope squirrels (Funisciurus sp.), Gambian giant pouched rats Cricetomys sp.

EMCV Encephalomyocarditis Virus Genus cardiovirus AKA: Mengovirus Worldwide/Ubiquitous disease of rodents Human: suspected neurologic disease Now thought to be asymptomatic Isolated from feces/intestinal contents Sciurus spp. Red squirrels Wild squirrels (Vizoso et al 1964) Where/ how viral persistence between epidemics unclear Acute death due to cardiac necrosis Important for zoo collection, elephants Chimpanzee, Orangutan Poorly infectious for people

Squirrel brains Creutzfeldt-Jakob disease (CJD) “burgoo” Squirrel brain stew 5 patients 56-78y Unrelated, Different towns Rural Kentucky Don’t eat brain unless you want be a zombie Creutzfeldt-Jakob Disease and eating squirrel brains. The LANCET Vol 350 • August 30, 1997 642 Berger JR et al.

Summary Squirrels are harbor a plethora of zoonoses Sentinel Is it the cute factor? Thanks for your attention

Recommended Readings Field Manual of Wildlife Diseases in the Southeastern United States, 3rd ed Davidson, WR Zoo & Wild Animal Medicine 5th ed Sainsbury, Rodent Chapter Infectious Diseases of Wild Mammals ES Wiliams, IK Barker Smithsonian Museum of Natural History North American Mammals http://www.mnh.si.edu/mna/main.cfm

Clostridium botulinum Saravanakuma PS Eslami P Zar FA Lymphocutaneous sporotrichosis associated with a squirrel bite: case report and review. Clin Infect Dise 1996 sep 23(3) 647-8

Squirrel Fibroma AKA Squirrel Pox Range Host Squirrel Pox Virus 1953 Leporipoxvirus Related to Shope’s Fibroma of rabbits Range Range: Maryland, New York, Virginia, Michigan, North Carolina, Ontario Host Gray squirrel Fox Squirrel Red squirrel Significant cause of decline Experimental infections Woodchucks, rabbits

Squirrel Fibroma Lesions Clinical Signs Limited to skin Metastasis to the lungs, liver, kidney, and lymph nodes has been reported. Secondary infection Vision obstruction Raised flattened nodules Light colored, little fur 1/16- 1 inch diameter Single or wide dissemination Epizootic Lesions on the eyelid Swelling, discoloration, necrosis of leg or foot Clinical Signs Most infections self limiting, spontaneously regress Debilitation, emaciation, death Rare epizootics Morbidity, mortality many squirrels Florida www.michigan.gov/dnr

Parasite-mediated competition Parapoxvirus: Grey & Red Squirrels Mosquito spread