Nina Marano DVM MPH Dipl ACVPM

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Where the Wild Things Are Public
Health Implications of the Exotic Animal Trade

Nina Marano DVM MPH Dipl ACVPM Division of
Global Migration and Quarantine Centers for
Disease Control and Prevention
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The Global Movement of Animals

• Exhibition at zoos
• Education and research
• Scientific conservation programs
• Incidental/Accidental
• Use as food and products
• Tourism and Immigration
• Commercial pet trade

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CDC Regulatory Authority for Importation
of Animals and Animal Products 42 CFR 71
(Foreign Quarantine)
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Smith et al 2009 Science
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Zoonoses in Pocket Pets

• Enteric pathogens
• Salmonella
• Lymphocytic choriomeningitis virus
• Tularemia
• Monkeypox

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Exotics Trade Show / Swap Meet, Georgia 2003
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2003 Outbreak of Monkeypox

• 72 human cases investigated, 37 confirmed
• Spread by African rodents imported for the
  commercial pet trade
• First human monkeypox cases reported outside
  Africa

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Movement of Imported African Rodents to Animal
Distributors and Distribution of Prairie Dogs
from Point of Infection
Rodent Shipment from Accra, Ghana
4/9/03
MMWR July 2003
4/9/03
TX 1 50 Gambian rats (GR)53 rope squirrels
(RS) 2 brush-tailed porcupines (BTP) 47 sun
squirrels (SS)100 striped mice (SM)510 dormice
(DM)
?
4/11/03
42 PDs traced
14 PDs traced
4/16/03
4/17/03
24 PDs traced
4/21/03
1 PDs traced
1 PD traced
4/26/03
4/28/03
?
11 PDs traced
4/28/03
5/12/03
4/29/03
5/18/03
June 2003 lab confirmation diseased animals
derived from shipment
6/1/03
6/1/03
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42 CFR 71.56 African Rodents Prairie Dogs

• Restrictions followed a 2003 monkeypox outbreak
  in the U.S. linked to importation of infected
  African rodents
• November 2003 Joint FDA-CDC Interim Final Rule
• Banned interstate movement of African rodents and
  prairie dogs
• Banned importation of African rodents
• September 2008
• FDA portion of ban on interstate movement of
  prairie dogs lifted
• CDCs import restrictions still in place

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Bacterial, Viral and Parasitic Zoonoses
Associated with Rodents
Crimean-Congo fever Dugbe virus Ebola
virus Hantavirus (HFRS) Hantavirus (HPS) Ippy
fever Lassa fever Machupo virus Mayaro
fever Marburg virus Mengo fever Omsk
fever Oropouche virus Monkeypox Q
fever Rabies Rift Valley fever Thogoto
virus Rocky Mountain spotted fever Tick-borne
encephalitis Typhus Amebiasis Babesiosis Capillari
asis Chagas disease Cryptosporidiosis Cysticercos
is
Brucellosis Coccidioidomycosis Corynebacteriosis D
ermatophytosis Nontuberculous mycobacteria Erysipe
las Leptospirosis Listeriosis Lyme
disease Plague Rat-bite fever Tick-borne
fever Salmonellosis Sporotrichosis Tuberculosis Tu
laremia Yersiniosis Asian ixodo-rickettsiosis Bhan
ja fever Borna virus Boutonneuse
fever Bunyaviruses Lymphocytic
choriomeningitis Cowpox
Dermatitis Echinococcus Eyeworms Giardiasis Hymeno
lepiasis Larva migrans Leishmaniasis Malaria Schis
tosomiasis Toxoplasmosis Trichinosis Trypanosomias
is
Zoonoses, Vol I, II, III. Acha and Szyfres,
PAHO 2003
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Risky Rodent Zoonoses
Crimean-Congo fever Dugbe virus Ebola
virus Hantavirus (HFRS) Hantavirus (HPS) Ippy
fever Lassa fever Machupo virus Mayaro
fever Marburg virus Mengo fever Omsk
fever Oropouche virus Monkeypox Q fever Rift
Valley fever Thogoto virus Tick-borne
encephalitis Rocky Mountain spotted
fever Typhus Amebiasis Babesiosis Capillariasis Ch
agas disease Cryptosporidiosis Cysticercosis
Brucellosis Coccidioidomycosis Corynebacteriosis D
ermatophytosis Nontuberculous mycobacteria Erysipe
las Leptospirosis Listeriosis Lyme
disease Plague Rat-bite fever Tick-borne
fever Salmonellosis Sporotrichosis Tuberculosis Tu
laremia Yersiniosis Asian ixodo-rickettsiosis Bhan
ja fever Borna virus Boutonneuse
fever Bunyaviruses Lymphocytic
choriomeningitis Cowpox
Dermatitis Echinococcus Eyeworms Giardiasis Hymeno
lepiasis Malaria Larva migrans Leishmaniasis Schis
tosomiasis Toxoplasmosis Trichinosis Trypanosomias
is
Zoonoses, Vol I, II, III. Acha and Szyfres,
PAHO 2003
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Cowpox in Europe Related to Pet Rodents

• Cowpox is an orthopoxvirus (Variola - smallpox,
  Vaccinia - monkeypox) circulating among rodent
  populations indigenous in Europe
• Can be transmitted to humans, cats, pet rats, zoo
  animals
• Large amounts of virus are found in lungs of
  infected animals
• Rodents (voles and lemmings) are animal hosts
• Antibodies to Cowpoxvirus found in 66 (41.8 ) of
  158 voles
• Human infection is associated with direct contact
  with an infected animal
• Disease is self-limiting in immunocompetent
  hosts, but can be severe and fatal in
  immunocompromised hosts
• Jan 2009 - 18 cases of human cowpox in Germany
  and 12 in France
• Sequencing data from the human isolates traced
  back to rodents in pet trade originating from
  breeder in Czech Republic
• Source
  ECDC Feb 2009

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Exotic Small Mammals Bartonella

• Bartonella
• 11/20 species known to be human pathogens,
  causing endocarditis,
• and neuroretinitis
• Objective
• Determine the prevalence of Bartonella sp. in pet
  animals
• 546 exotic small mammals imported to Japan
• From US, Europe, Middle East Asia
• 28 species including mice, gerbils, squirrels,
  chipmunks, hedgehogs, sugar gliders
• 367 animals captured in the wild, 179 from
  breeding colonies
• Blood samples collected for culture and
  sequencing
• Results
• Overall prevalence of Bartonella
• 142/546 (26) animals bacteremic
• Prevalence by animal origin
• Wild animals 137/367 (37)
• Breeding colony animals 5/179 (2.8)
• 407 Bartonella isolates
• 4 known and 6 novel species

Inoue et al EID Vol 15, No. 4 April 2009
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Nonhuman Primate (NHP) Infectious
Disease Risks

• Tuberculosis
• Viral Hemorrhagic Fever
• Ebola, Marburg
• Herpes B virus
• Hepatitis
• Monkeypox
• Simian Immunodeficiency Virus (SIV)
• Yellow Fever reservoir

Credit iStockPhoto
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Current CDC NHP Importation Program

• Increased federal oversight
• Register with CDC
• Certify use for scientific, educational purposes,
  
• or exhibition
• Isolate and quarantine for 31 days
• Implement disease control measures
• Report suspected zoonotic disease to CDC
• Impact
• Improved detection and control of disease
  outbreaks
• Reduction in NHP mortality from 15 to lt1

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Herpes B virus

• Macaque monkeys Asia Northern Africa
• Temples in Nepal or India
• Human infection rare Since 1933, 50 cases, but
  high fatality rate (80 if untreated)
• Most cases occupational via bites or scratches
• Virus long lived on surfaces (up to 2 weeks)
• No cases in travelers, but travelers should be
  aware of potential risk
• Advice
• Dont feed or pet monkeys
• Obtain prompt first aid for wounds seek
  healthcare
• Follow up with physician on return from travel

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International Travel Trade in Animal
ProductsA Pathway for Hitchhiking Pathogens?

• In 2006 253,000 non-resident passenger arrivals
  to the U.S. from Africa
• Opportunities for pathogen Introduction via
  animal products
• Other routes of entry
• Cargo
• Mail
• Limited inspection capabilities given scope of
  trade and travel

Office of Travel Tourism Industries U.S.
Department of Commerce
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Travelers Visiting Friends and Relatives VFRs

• Foreign-born increased 57 since 1990 from 19.8
  million to 31.1 million1
• 20 of US population are first-generation
  immigrants or their children2
• VFRs comprised 43 of US overseas travelers in
  20073
• 1US Census Bureau, Census 2000 Brief, The
  Foreign-Born Population 2000, issued Dec 2003
  (Previous US Census Bureau, Profile of the Born
  Outside the United States Population 2000, issues
  Dec 2003
• 2 Angell Cetron, 2005
• 32007 Profile of U. S. Resident Travelers
  Visiting Overseas Destinations Reported From
  Survey of International Air Travelers, Office of
  travel and tourism Industries, USDOC

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Health Risks from Bushmeat

• HIV is most likely derived from
  chimpanzee-to-human transmission
• Through hunting butchering of bushmeat
• Adaptation to human host human-to-human
  transmission
• Ebola virus
• Detected in chimpanzees and duikers in the Ivory
  Coast
• Associated with hunter contact with dead
  chimpanzees
• Simian Immunodeficiency Virus (SIV)
• 131/788 samples from monkeys meat SIV
• in Cameroon
• Peeters et al EID Vol 8 No. 5, May
  2002
• Monkeypox virus
• Has been detected in monkeys, rodents humans

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Bushmeat Seizures at US AirportsOctober
2005- Sept 2006

• October 2005 - Sept 2006 50 seizures of
  CDC-prohibited bushmeat at US ports of entry
• Animal species
• Grasscutter/cane rat, nonhuman primate,
• porcupine, bat
• Ports of entry
• Newark, Detroit, Atlanta
• Countries of origin
• Ghana, Nigeria, Cameroon
• Transit Airport
• Netherlands

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Population Density of US Residents from
West African Countries, 2009
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42CFR 71.32(b) Haitian Goat-Hair Products

• Import restrictions on untanned goat-hair
  products from Haiti
• 1973 case of cutaneous anthrax
• Advisory memorandum No. 107
• Handicrafts (goatskin drums)

Credit iStockPhoto
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Anthrax in Animal Hides Imported to the US
http//www.erdunia.com/index.asp?cat_id5catname
'Musical20Instruments http//www.cdc.gov/MMWR/pr
eview/mmwrhtml/mm5510a4.htm
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Rabies Pre exposure Vaccination Recommendations
for Travelers
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Public Health Concerns about Dogs Imported to the
US from Rabies Endemic Areas

• Puppies imported for commercial pet trade
• Increasing trend in importation of purebred
  puppies from abroad for sale to US buyers
• Many too young to be vaccinated for rabies come
  from rabies endemic areas
• 2004-2007 3 instances of dogs imported from
  Puerto Rico, Thailand India positive for rabies
• Dogs imported as part of humanitarian rescue
  operations
• Animal rescue organization efforts to find homes
  in the US for stray dogs from Iraq, Puerto Rico
• June 2008 - dog imported from Iraq positive for
  rabies
• Opportunity for widespread exposure of public

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• Since Sept 2008
• 33 missions from Iraq
• 90 dogs cats
• All vaccinated healthy

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Screwworm Myiasis

• Gusanos, Mosca Verde, Gusano barrendor, Gusaneras

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Nonnative Species Established in Florida
Gambian Rat
African Snakehead Fish
Floridas invasive species strategic plan
http//iswgfla.org
Burmese Python
Red Eared Slider
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Proposed House Rule 669, April 2009
Non-Native Wildlife Prevention Act

• Risk assessment of all non-native wildlife
  species
• proposed for importation into the US, other
  than approved species
• Identity of the organism to the species level
• Geographic source
• Likelihood of spread and harm to other species or
  habitats
• Establishes prohibitions on
• Importation of nonnative species or viable eggs
• Possession, purchase, sale, barter, release, or
  breeding
• Allow imposition of fees to recover costs of
  assessing risks of
• Establishes a Nonnative Wildlife Invasion
  Prevention Fund

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Reducing Zoonotic Risks Associated with Trade
Movement of Animals

• Broker interagency cooperation to assess and
  close regulatory gaps
• Utilize regulatory mechanisms and education to
  decrease supply and demand for animals in the
  commercial pet trade
• Encourage partnerships between wildlife and
  public health to promote conservation and protect
  animal and human health especially in source
  countries
• Enhance surveillance of animals in commerce
• Build the capacity of existing systems to
  identify track imported animal species and
  quantity of shipments
• Conduct risk assessments of high risk animals,
  products, and vectors to better target control
  and prevention efforts

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Acknowledgements

• CDC
• Betsy Schroeder
• Gale Galland
• Sheryl Shapiro
• Bob Mullan
• Nancy Gallagher
• Heather Bair
• Kathryn Johnson
• Gary Brunette
• Kevin Liske
• Charles Rupprecht
• Margaret Carl
• Paul Arguin
• Marty Cetron