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VMX 2018 Small Animal | Forensics &

INTERNATIONAL SHELTER ADOPTIONS: SAVING LIVES OR SPREADING DISEASE? Katherine Polak, DVM, MPH, MS, DACVPM REASONS FOR INTERNATIONAL ADOPTIONS Four Paws International In areas with a signifcant stray and overpopula- Bangkok, Thailand tion, there are often simply not enough adoptive homes or interest locally in rescued animals. In many cultures, a stray OVERVIEW mixed-breed dog is viewed much differently than a purebred While estimates vary, the population of worldwide dog or cat; therefore, when seeking a , most local people may be as high as 500 million, with the majority living much will typically visit a pet store rather than adopt from a shelter. differently than traditionally-owned by Western stan- Adopting animals internationally helps animal shelters re- dards1. Most are classifed as free-roaming or ‘communi- duce overcrowding, relieve stress on staff, and ultimately ty-owned’, and are frequently subject to malnutrition, save more animals in communities where local adoptions abuse, poisoning, and road traffc accidents. During the are limited. Performing international adoptions may also in- last decade, increasing numbers of animal welfare organi- crease the profle of the organization. zations have begun working in poorly resourced areas in On the receiving end, shelters that receive imported dogs an effort to improve animal welfare. In areas with little local and may also reap certain benefts. In the US, the arriv- capacity for local adoptions, sheltering organizations have al of internationally rescued dogs often generates so much started investigating whether international pet transport community interest that every animal is quickly adopted might be a viable option to increase their live release rates. from the facility through adoption events. The novelty of im- This practice, while a life-saving mechanism for many ani- ported rescued dogs also increases the public awareness mals, is not with inherit risks and controversy. Animals surrounding important international animal welfare issues. must be appropriately selected, screened for infectious disease, and the necessary processes followed for trans- CONTROVERSY port. Pet transport programs must comply with local and There is considerable controversy involving the transport international regulations of both the importing and export- of dogs and cats internationally to communities where there ing country to protect both human and animal health. While is already an overabundance of animals in shelters. saving animals lives is a noble goal, it must be done re- Furthermore, international transport can facilitate disease sponsibly to mitigate the risk of disease introduction and transmission. Given the public health risk posed by the im- transmission. portation of animals for adoption and the euthanasia of adoptable animals in certain countries, many suggest that TRENDS IN ANIMAL TRANSPORT organizations frst consider improving their local capacity Transport programs vary considerably. Some are small, through spay/neuter and community engagement before loosely organized grassroots efforts performed by local res- sending animals abroad. cuers while others are conducted by large international ani- mal welfare organizations using a network of overseas shel- RISKS TO ANIMAL WELFARE ter partners. The transportation of dogs for commercial The transportation of animals is not with inherit risk to purposes also accounts for a signifcant number of dogs the individual animal. While small dogs and cats may be and cats transported each year, but is largely outside the able to travel in an aircraft cabin with a passenger, most scope of discussion here. typically fy under the cabin in cargo, a pressurized hold. In most countries, pet transportation is on the rise yet no While cargo holds are pressurized, they can be dark, noisy, formalized system exists to track exactly how many ani- and have fuctuating temperatures and air pressures. mals are transported internationally for adoption purposes. While most airlines have time and temperature restrictions, The growth in pet transportation has increased largely due undoubtedly such environments can be stressful. While to the growing awareness of various international animal animal deaths in cargo are relatively rare, injuries can be welfare issues such as the dog and trade in Asia. common. The most frequent injuries observed result from This has created a unique adoption market in countries biting and scratching at kennels and respiratory distress, such as the US and Canada. Korean Air and Asiana most likely attributable to stress, particularly at the time of Airlines transported pets 24,741 and 12,595 times in 2016, loading. The risk of transport is signifcantly higher for respectively2. The combined number increased 19.2% brachycephalic breeds. The stress of transport may also from the year prior (2015) to reach an all-time high. lead to immune compromise and/or recrudescence of Considerable expansion in animal transportation is ex- disease and increased viral shedding. pected in the coming years. Soi Dog Foundation, a non-proft based in Phuket, Thailand, routinely adopts and Disease transmission transports up to 50 dogs and cats monthly into homes into A major argument against international adoptions is the the US, UK, and Canada. potential introduction of foreign animal diseases, particularly

341 VMX 2018 Small Animal | Forensics & Animal Welfare those with zoonotic potential. If animals are shipped, careful transport. To learn about quarantine policies, documentation management is required to minimize the risk of disease. and other requirements, organizations must check with the This risk is magnifed when animals of unknown disease appropriate agency, typically the Department of Agriculture, in status are co-mingled or group-housed prior to or during their country. It is particularly important that all health condi- transport. While poses the greatest risk, the trans- tions of the animal are properly documented. Animal welfare mission of other zoonotic diseases (e.g., brucellosis, leish- organizations must carefully screen and choose animals maniasis, campylobacteriosis, leptospirosis, giardiasis, and based on both medical and behavioral examinations. Animals cutaneous or visceral larva migrans) is also a real threat. should ideally be chosen based on the lowest risk of disease. While there is often emphasis placed on adopting Case study - Canine parvovirus and distemper virus and due to their high adoptability, they are immunolog- In August 2010, 221 rescued dogs ranging in age from 4 ically naïve and the most susceptible to disease. Dogs should weeks to > 1 year were transported by cargo plane from be assessed behaviorally as well as physically. Puerto Rico to Orlando, Florida. The dogs were destined for After selecting an animal for adoption, the organization or a national adoption event in New York following a 4-day lay- individual shipping an animal internationally carries the bur- over in Florida. Unfortunately, several of the imported dogs den of ensuring that animal is free of disease and eligible for were incubating parvovirus and distemper virus at the time travel into the desired country. Ideally the shelter or facility of transport which led to the Florida State Veterinarian de- should have a preventive care program already in exis- claring an offcial quarantine due to the diseased dogs, the tence. Prior to travel, it is recommended that the following frst ever state-mandated quarantine for dogs. be performed noting that import restrictions may vary de- pending on the country of import and export. Case study - Canine influenza Spay/neuter surgery – Sterilization should ideally be per- Until March 2015, the canine infuenza (CIV) strain H3N2 formed prior to travel. Spay/neuter surgery may allow for the appeared to be limited to Asia, specifcally Korea, China, identifcation of underlying conditions such as pyometra. and Thailand. However, an outbreak originating in Chicago Adequate time should be allowed between surgery and was believed to have been due to a H3N2 strain3. While it transport to allow for proper incisional healing. In interna- was speculated that the virus was introduced to the U.S. via tional settings where veterinary training may be poor, it dogs rescued and imported from Asia, there was no evi- might be necessary to confrm the removal of all ovarian dence to substantiate this claim. Dogs must be screened for tissue in female animals prior to transport. any signs of respiratory disease prior to transport. Comprehensive physical examination – This should be Researchers at the University of Wisconsin found that CIV performed when deciding whether or not an animal is a H3N2 can shed for more than 20 days4. sound candidate for transportation, and repeated within 24 hours of transport to detect signs of infectious disease. RISKS TO PUBLIC HEALTH Vaginal and penile exams should also be performed to de- The most signifcant zoonotic risk is the importation of a tect potential signs of canine transmissible venereal tumor. dog or cat incubating rabies. Rabies, the deadliest of all Identifcation – Microchips are preferred and required by zoonotic diseases accounts for over 50,000 human deaths most countries for import. around the world annually. The introduction of any non-en- Heartworm antigen testing – Many animals are transport- demic rabies viruses into a naïve animal population has the ed from heartworm endemic areas to areas typically consid- potential to change the epizootiology of rabies in-country ered free of the disease. It is important to ascertain whether leading to severe health consequences and economic or not a dog has detectable antigen near the time of trans- losses. port. The American Heartworm Society recommends that In June of 2015, a free roaming dog and her were dogs with a positive heartworm test be started on doxycy- captured in Cairo, Egypt. Her vaccination certifcates were cline therapy prior to transport6. Dogs with a negative heart- forged to avoid exclusion of the dog from entry under the US worm antigen test should be re-tested six months following CDC’s current dog importation regulations, and she was relocation. Some organizations may choose to treat infect- transported to the U.S. by an animal rescue organization in ed dogs with either a two- or split-dose melarsomine proto- a shipment that included seven other dogs and 27 cats5. col prior to transport due to the cost of treatment in the im- Following her arrival and placement in a foster home in port country. Ideally, the transporting agency should allow Virginia, the rescue dog developed signs and symptoms 4-6 months to complete heartworm treatment prior to trans- classic of rabies. The dog was quickly euthanized and trace- port to reduce the risk of thromboembolism. All dogs regard- back steps were implemented to assess exposure and risk. less of antigen status should be started on macrocyclic lac- tone therapy prior to transport. RESPONSIBILITIES OF THOSE INVOLVED Endoparasiticide – A broad spectrum deworming produc- It is critical that those involved in transport are familiar with tive effective against hookworms and roundworms should the import and export requirements for all relevant countries be administered. Certain countries also require tapeworm as well as airline requirements to ensure safe and responsible treatment days before transport.

342 VMX 2018 Small Animal | Forensics & Animal Welfare

Rabies and DHPP/FVRCP vaccination – A rabies vacci- While the US requires that animals form rabies-endemic nation is legally required for all dogs and cats, with minor countries not be imported until one month after they receive exceptions which vary per country. All dogs should be ap- their rabies vaccination (3 months of age), puppies younger propriately vaccinated for canine distemper and canine par- than 3 months can sell for a higher price. As a result, import- vovirus and cats for panleukopenia. ers may falsify documents to make the dogs’ age older than CBC/Chemistry – Bloodwork can be used to rule out un- what they really are. There are also reports of falsifying derlying disease that may not be evident on physical exam- breed registration and birth location. ination, including thrombocytopenia for tick-borne disease Rabies titer tests can also be falsifed. Serum can be which is prevalent in free-roaming dogs. banked for animals already known to have adequate anti- IDEXX 4DX SNAP test – Screens for exposure to tick- body titers and submitted in the place of another dog who borne disease and heartworm infection. Some organiza- may have failed the titer test previously. tions may elect to administer a 21-28 day course of doxycy- cline to dogs who test positive for E. canis and Anaplasma SUMMARY spp. antibodies. The risks and benefts of transport programs both in the Ectoparasiticide – Animal should be free of ectoparasites area of export and import must be carefully considered. It is during their time spent in the organization’s care. the author’s opinion that international transport programs Advanced diagnostics – Further diagnostics may be war- should be a last resort after all efforts for local adoption, ranted depending on clinical signs. Certain infectious dis- transfer, and welfare promotion in the local community have ease including dermatophytosis, parvovirus, and distemper been exhausted. must be ruled out through diagnostics (DTM culture, SNAP test, blood smears), clinical signs, and keeping animals REFERENCES separated from those that might be carrying infectious dis- 1. Hsu Y., Severinghaus L, Serpell J. Dog keeping in ease. Radiographs may be warranted depending on physi- Taiwan: Its contribution to the problem of free-roaming cal examination fndings. FeLV/FIV tests should be per- dogs. Journal of Applied Animal Welfare Science. 2003; formed to ascertain the retroviral status of cats going into 6(1): 1–23. adoption programs. For dogs originating from shelters in 2. Min-hee J. Pet transport by air doubled in six years Asia, PCR for infuenza may be advised if respiratory dis- [Internet]. Business Korea. 2017 [cited 3 May 2017]. ease is endemic in the population. Available from http://www.businesskorea.co.kr/english/ Rabies titer test (Fluorescent Antibody Virus Neutralization news/insight/17848-travel-pet-pet-transport-air- (FAVN)) – FAVN testing is often required by many ra- doubled-six-years. bies-free countries and some rabies-controlled countries for 3. Kang Y, Kim H, Ku K, Park E, Yum J, Seo S. H3N2 ca- dogs and cats to qualify for a reduced quarantine period or nine infuenza virus causes severe morbidity in dogs no quarantine at all when they are traveling from particular with induction of genes related to infammation and countries. The test consists of a three-fold serum dilution apoptosis. Veterinary Research. 2013;44(1):92. series and is used to detect rabies virus neutralizing anti- 4. Newbury S, Godhardt-Cooper J, Poulsen K, Cigel F, body after vaccination. Balanoff L, Toohey-Kurth K. Prolonged intermittent virus shedding during an outbreak of canine infuenza A H3N2 FALSIFICATION OF DOCUMENTATION virus infection in dogs in three Chicago area shelters: 16 The US CDC and state agencies have received reports of cases (March to May 2015). Journal of the American invalid or questionable health and rabies vaccination certif- Veterinary Medical Association. 2016;248(9):1022-1026. cates for imported dogs. Further complicating matters is the 5. Sinclair J, Wallace R, Gruszynski K, Freeman M, fact that importation regulations may be diffcult to enforce in Campbell C, Semple S et al. Rabies in a dog imported certain countries due to limited resources at ports of entry to from Egypt with a falsifed rabies vaccination certifcate inspect dog shipments. In May 2014, the US CDC issued — Virginia, 2015. MMWR Morbidity and Mortality the health alert notifcation “Imported Dogs with Questionable Weekly Report. 2015;64(49):1359-1362. Documents” due to ongoing concerns with dogs’ entry doc- 6. Current canine guidelines for the prevention, diagnosis uments listing incorrect ages and rabies vaccination status. and management of heartworm (Diroflaria immitis) in- Similarly, falsifed documents have been reported in rela- fection in dogs [Internet]. American Heartworm Society. tion to the sale of puppies from intensive breeding opera- [cited 1 May 2017]. Available from: http://www.heart- tions to supply the demand for certain pure breed dogs. wormsociety.org/pdf/2014-AHS- Canine-Guidelines.pdf.

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