Wright et al. Parasites Vectors (2020) 13:546 https://doi.org/10.1186/s13071-020-04407-5 Parasites & Vectors LETTER TO THE EDITOR Open Access Parasites and vector‑borne diseases disseminated by rehomed dogs Ian Wright1*, Frans Jongejan2, Mary Marcondes3, Andrew Peregrine4, Gad Baneth5, Patrick Bourdeau6, Dwight D. Bowman7, Edward B. Breitschwerdt8, Gioia Capelli9, Luís Cardoso10, Filipe Dantas‑Torres11, Michael J. Day12, Gerhard Dobler13, Lluis Ferrer14, Luigi Gradoni15, Peter Irwin12, Volkhard A. J. Kempf16, Barbara Kohn17, Friederike Krämer18, Michael Lappin19, Maxime Madder20, Ricardo G. Maggi8, Carla Maia21, Guadalupe Miró22, Torsten Naucke23, Gaetano Oliva24, Domenico Otranto25, Maria Grazia Pennisi26, Barend L. Penzhorn2, Martin Pfeffer27, Xavier Roura28, Angel Sainz22, SungShik Shin29, Laia Solano‑Gallego14, Reinhard K. Straubinger30, Séverine Tasker31, Rebecca Traub32 and Susan Little33 Abstract The Companion Vector-Borne Diseases (CVBD) World Forum is a working group of leading international experts who meet annually to evaluate current scientific findings and future trends concerning the distribution, pathogenesis, clin‑ ical presentation, diagnosis and prevention of vector-borne infections of dogs and cats. At the 14th Symposium of the CVBD World Forum in Trieste, Italy (March 25–28, 2019), we identified the need to (i) bring attention to the potential spread of parasites and vectors with relocated dogs, and (ii) provide advice to the veterinary profession regarding the importance of surveillance and treatment for parasites and vector-borne infections when rehoming dogs. This letter shares a consensus statement from the CVBD World Forum as well as a summary of the problem faced, including the role of veterinary professionals in parasite surveillance, causal issues, and the importance of interdisciplinary coopera‑ tion in addressing the problem. To limit opportunities for dissemination of parasites and vectors, whenever possible, underlying problems creating the need for dog rehoming should be addressed. However, when it is necessary to rehome dogs, this should ideally take place in the country and national region of origin. When geographically distant relocation occurs, veterinary professionals have a vital role to play in public education, vigilance for detection of exotic vectors and infections, and alerting the medical community to the risk(s) for pathogen spread. With appropriate veterinary intervention, dog welfare needs can be met without inadvertently allowing global spread of parasites and their vectors. Keywords: Relocation, Canine, Importation, Animal welfare, Zoonosis, Parasites, Prevention, Adoption, Shelter Letter to the Editor 2019, it was acknowledged that the veterinary profes- The continuous relocation of dogs both within and sion faces considerable challenges in dealing with these between countries represents a global veterinary and issues. Specifically, there is confusion among veterinary public health concern. At the 14th Symposium of the professionals regarding the role they play in international Companion Vector-Borne Diseases (CVBD) World rehoming advice, surveillance, and control of parasites Forum, held in Trieste, Italy, from March 25th to 28th, and pathogens for imported and exported dogs. It was agreed that a consensus statement would be beneficial in clarifying the view of the group and the role of the vet- *Correspondence: hammondia@hotmail.com 1 erinary profession regarding relocation of dogs and the The Mount Veterinary Practice, Fleetwood, UK Full list of author information is available at the end of the article associated potential spread of pathogens, vectors and © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat​iveco​ mmons​.org/licen​ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat​iveco​mmons​.org/publi​cdoma​in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Wright et al. Parasites Vectors (2020) 13:546 Page 2 of 4 diseases. Here, the consensus statement is presented authors acknowledge that in many parts of the world alongside a summary of the problem faced, including the problems are linked to economic factors and cultural role of veterinary professionals in parasite surveillance, attitudes [20]. For example, profit from export of dogs causative issues, and the importance of interdisciplinary is essential for some communities and, in some cases, cooperation in addressing the problem. meets market demand for rescue dogs in countries where there is incomplete knowledge of the welfare implications Consensus statement of importation. In many countries where canine welfare Economic, cultural and environmental factors are causing is compromised, human poverty and suffering can make global relocation of domestic dogs, which is associated allocation of resources towards animals less of a priority with the risk of dissemination of parasites, pathogens [20]. Although improving human welfare and infrastruc- and vectors. Where possible, the underlying problems ture will help animals indirectly, this process can be slow. should be addressed. However, when it is necessary to Where canine rehoming must occur, dogs should remain rehome dogs, this should ideally take place in the coun- in their region of origin whenever possible to reduce try and national region of origin. Where geographically pathogen spread but also to keep the dogs in as familiar distant relocation is occurring, veterinary professionals conditions as possible. Street dogs may experience social have a vital role to play in public education, vigilance for stress, for instance, when denied free outdoor access. detection of exotic vectors and infections, and alerting Some communities keep community dogs that are likely the medical community to the risks for pathogen spread. to be less stressed free roaming than in a domestic house- This includes the implementation of appropriate diagnos- hold, as long as overall welfare via interventions such as tic tests and parasite or pathogen preventative measures, vaccination, quality of diet and parasite prevention can ideally before relocation, where necessary. be improved. The authors acknowledge that addressing underlying issues that affect canine welfare and increas- Summary of the problem ing education regarding these issues are long-term objec- Multiple drivers affect canine welfare worldwide includ- tives. In the meantime, export of dogs will continue to ing natural disasters [1], persecution of street dogs [2], occur, and veterinary professionals have a vital role to the canine meat trade [3], the practice of acquiring pet play. dogs as puppies bred in high production, commercial facilities, often in geographically remote locations [4, 5] and travelling dogs brought for mating [6]. Public desire The role of veterinary professionals to adopt dogs from abroad that have often had their Veterinary professionals have an important role to play welfare compromised by these events is increasing. In in maintaining biosecurity, reducing zoonotic risk to pet part, this is driven by social media channels in affluent owners and the wider public, and improving the health of regions [1], and increased awareness of geographically stray dogs. It is essential that veterinary professionals distant homeless dogs. As a result, dogs are often relo- (i) educate the public about the risks of adopting dogs cated over large geographical distances [7, 8]. However, from abroad or distant regions within a country and dog relocation can cause dissemination of pathogen and inform them about the benefits of adopting dogs locally. vector populations [9]. Increased human migration, cli- This communication should be compassionate as most mate change and pet travel are other factors that favour charities working in this field, and people adopting pets, this expansion [10–12]. Other risks associated with geo- do so with the best of intentions but may be unaware of graphically distant rehoming of dogs include behavioural the risks. Social media, practice websites, waiting room issues and spread of zoonotic parasitic, viral and bacte- leaflets and posters, and discussions can all be utilised to rial infections, such as Leishmania spp. [6, 13], rabies disseminate the message. [14], Brucella spp. [15] or Leptospira spp. [16]. Spread (ii) ask about travel history for any recently acquired of drug-resistant pathogens is an additional concern, pet and advise appropriate diagnostic testing and pre- e.g. drug-resistant heartworm (Dirofilaria immitis) and ventative treatments depending on parasites and other hookworms (Ancylostoma caninum) in North America pathogens present in the country of origin and relevant [17, 18]. clinical signs. Further information can be found at the following websites: https​://www.escca​p.org; https​://capcv​ Addressing causal issues et.org; https​://www.trocc​ap.com; currently https​://cvbd. Ideally, driving factors that lead to dog welfare con- bayer​.com – in the future https​://cvbd.elanc​o.com; https​ cerns and increased stray dog populations should be ://iscai​d.org; directly addressed. Such an approach has a range of ben- (iii) are vigilant in looking for exotic ticks or other efits beyond a reduction in dog displacement [19]. The arthropods on imported dogs and clinical signs that may Wright et al. Parasites Vectors (2020) 13:546 Page 3 of 4 indicate infection with pathogens not known to be locally encourage them to relax their requirements for rehom- endemic in the region of origin; ing where welfare will not be compromised as a result. If (iv) report all findings of unusual ticks or arthro- rehoming requirements are too stringent, this may deter pods and unusual infections to local health authorities, potential owners from adopting dogs from within their universities, independent organisations such as those own country. The members of the CVBD World Forum mentioned in point (ii) and through peer-reviewed pub- pledge their support to continue to provide data and lications. This helps generate an up-to-date picture of evidence-based advice on reducing parasites and vector- where vectors and pathogens may be emerging. Examples borne pathogens spread through provision of informa- of published reports include Haemaphysalis longicornis tion on optimal testing, preventative treatments, and ticks in North America [21], Rhipicephalus sanguineus increased veterinary and public education. ticks in northern European households [22], Babesia Acknowledgements canis in the UK [23, 24], heartworm (D. immitis) in Colo- We thank Bayer Animal Health for organizing and facilitating our discussion at rado [8], Ehrlichia canis in Australia [25] and Leishma- the 14th Symposium of the CVBD World Forum in Trieste, Italy, in March 2019. nia spp. transmission to untraveled dogs in the absence Bayer Animal Health is now part of Elanco. We thank in memoriam Michael Day for all of his work and commitment to the CVBD World Forum and of sand fly vectors in the Czech Republic [6] and in the towards the furtherment of parasite knowledge, understanding and control. UK [13, 26]. To many of us he was more than a brilliant colleague but a friend. Authorsʼ contributions Importance of interdisciplinary and international IW, FJ, SL, MM and AP drafted the initial statement. All other co-authors worked on the initial manuscript and contributed to the final document. All cooperation authors read and approved the final manuscript. Government legislation regarding dog importation and exportation varies but has an impact by potentially lim- Funding FD-T received a research fellowship from CNPq (Bolsa de Produtividade; iting the numbers of imported dogs and ensuring com- grant no. 313118/2018-3). FK is working in a project funded by Bayer Animal pulsory vaccine and parasite/pathogen preventative Health (TransMIT; Z 2079), which is now part of Elanco, at TransMIT GmbH, treatment requirements are followed before entry. Dog Germany. CM has the support of the Fundação para a Ciência e a Tecnologia/ Ministério da Ciência, Tecnologia e Ensino Superior (Investigator Starting Grant importation requirements can also vary depending on IF/01302/2015). whether the dog is classified as personal or commercial. Personal import usually has fewer requirements, which Availability of data and materials are why rescue groups sometimes translocate dogs as Not applicable. owned pets [27]. In both cases, if the administration of Ethics approval and consent to participate highly effective preventative measures such as anti-rabies Not applicable. vaccination, tick control, testing for vector-borne agents, Consent for publication or praziquantel treatment for Echinococcus multilocu- Not applicable. laris is adequately followed, biosecurity against specific Competing interests pathogens can potentially be maintained. For exam- The authors declare that they have no competing interests. The authors are ple, modelling has demonstrated that the introduction members of the CVBD World Forum. The CVBD World Forum was founded of E. multilocularis into countries free of the parasite during the 1st International CVBD Symposium from April 18th to 20th, 2006, in Billesley, UK, as a consequence of the increasing global threats through would be inevitable without the compulsory treatment vector-borne diseases. The CVBD World Forum is supported by Bayer Animal of dogs that have visited or been imported from endemic Health, which is now part of Elanco. countries [28]. Other examples include compulsory anti-rabies vaccination of travelling and imported dogs Author details keeping many countries rabies-free, and the success until 1 The Mount Veterinary Practice, Fleetwood, UK. 2 Department of Veterinary recently of screening dogs imported into Australia for E. Tropical Diseases, University of Pretoria, Onderstepoort, South Africa. 3 School of Veterinary Medicine, São Paulo State University, São Paulo, Brazil. 4 Depart‑ canis in preventing its introduction in that country. ment of Pathobiology, University of Guelph, Guelph, ON, Canada. 5 Koret Financial aid for projects associated with canine wel- School of Veterinary Medicine, Hebrew University of Jerusalem, Rehovot, Israel. 6 fare supported by governments and by international Ecole Nationale Vétérinaire, Nantes, France. 7 Department Microbiology & Immunology, Cornell University, Ithaca, NY, USA. 8 Department of Clinical Sci‑ charities is helpful in tackling canine welfare issues in ences, North Carolina State University, Raleigh, NC, USA. 9 Istituto Zooprofilat‑ countries of origin [19]. This funding, together with tico Sperimentale delle Venezie, Legnaro, Italy. 10 Department of Veterinary increased policing of existing animal welfare laws, is Sciences and Animal and Veterinary Research Centre (CECAV), University of Trás-os-Montes e Alto Douro (UTAD), Vila Real, Portugal. 11 Aggeu Magalhães important for implementation of these measures, but it is Institute, Fundação Oswaldo Cruz (Fiocruz), Recife, Brazil. 12 College of Veteri‑ critically important to be sensitive to accepted norms in nary Medicine, Murdoch University, Murdoch, WA, Australia. 13 Bundeswehr different cultures [3]. 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Retrospective lished maps and institutional affiliations. analysis of vector-borne infections in dogs after travelling to endemic areas (2007–2018). Vet Parasitol X. 2019;2:100015. Ready to submit your research ? Choose BMC and benefit from: • fast, convenient online submission • thorough peer review by experienced researchers in your field • rapid publication on acceptance • support for research data, including large and complex data types • gold Open Access which fosters wider collaboration and increased citations • maximum visibility for your research: over 100M website views per year At BMC, research is always in progress. Learn more biomedcentral.com/submissions