ONLINE REPORT Canine Leishmaniasis Control in the Context of One Health Filipe Dantas-Torres, Guadalupe Miró, Gad Baneth, Patrick Bourdeau, Edward Breitschwerdt, Gioia Capelli, Luís Cardoso, Michael J. Day, Gerhard Dobler, Luis Ferrer, Peter Irwin, Frans Jongejan, Volkhard A.J. Kempf, Barbara Kohn, Michael Lappin, Susan Little, Maxime Madder, Ricardo Maggi, Carla Maia, Mary Marcondes, Torsten Naucke, Gaetano Oliva, Maria Grazia Pennisi, Barend L. Penzhorn, Andrew Peregrine, Martin Pfeffer, Xavier Roura, Angel Sainz, SungShik Shin, Laia Solano-Gallego, Reinhard K. Straubinger, Séverine Tasker, Rebecca Traub, Ian Wright, Dwight D. Bowman, Luigi Gradoni, Domenico Otranto Author affiliations: Aggeu Magalhães Institute, Fundação Oswaldo Dogs are the main reservoir of Leishmania infantum and in Cruz (Fiocruz), Recife, Brazil (F. Dantas-Torres); Universidad some countries have been regularly culled as part of govern- Complutense de Madrid, Madrid, Spain (G. Miró, A. Sainz); ment policy to control visceral leishmaniasis. At the 13th Sym- Hebrew University of Jerusalem, Rehovot, Israel (G. Baneth); posium of the Companion Vector-Borne Diseases World Fo- Ecole Nationale Vétérinaire, Nantes, France (P. Bourdeau); North rum in Windsor, UK, March 19–22, 2018, we consolidated a Carolina State University, Raleigh, North Carolina, USA consensus statement regarding the usefulness of dog culling as a means of controlling visceral leishmaniasis. The state- (E. Breitschwerdt, R. Maggi); Istituto Zooprofilattico Sperimentale ment highlighted the futility of culling infected dogs, whether delle Venezie, Legnaro, Italy (G. Capelli); University of healthy or sick, as a measure to control the domestic reservoir Trás-os-Montes e Alto Douro (UTAD), Vila Real, Portugal of L. infantum and reduce the risk for visceral leishmaniasis. (L. Cardoso); Murdoch University, Murdoch, Western Australia, Australia (M.J. Day, P. Irwin); Bundeswehr Institute of Microbiology, Munich, Germany (G. Dobler); Universitat Autònoma de Barcelona, Bellaterra, Spain (L. Ferrer, X. Roura, V isceral leishmaniasis (VL), caused by Leishmania donovani in Asia and Africa and by L. infantum in the Mediterranean Basin, the Middle East, Central Asia, L. Solano-Gallego); Utrecht University, Utrecht, the Netherlands (F. Jongejan); Goethe-University, Frankfurt am Main, Germany South America, and Central America, is a life-threatening (V.A.J. Kempf ); Freie Universität Berlin, Berlin, Germany disease that affects ≈200,000–400,000 persons annually (B. Kohn); Colorado State University, Fort Collins, Colorado, USA and causes an estimated ≈20,000–40,000 deaths per year (M. Lappin); Oklahoma State University, Stillwater, Oklahoma, (1,2). Although an increasing number of other mammalian USA (S. Little); Clinglobal, Tamarin, Mauritius (M. Madder); hosts, including infected humans, have served as effective Universidade NOVA de Lisboa, Lisbon, Portugal (C. Maia); reservoirs by infecting phlebotomine sand fly vectors, dogs São Paulo State University, São Paulo, Brazil (M. Marcondes); remain a pivotal indirect source in many situations where LABOKLIN GmbH, Bad Kissingen, Germany (T. Naucke); the transmission cycle of L. infantum occurs (3,4). University of Naples Federico II, Naples, Italy (G. Oliva); Over the years, millions of dogs have been killed as University of Messina, Messina, Italy (M.G. Pennisi); University of part of government policies to control human VL caused Pretoria, Onderstepoort, South Africa (B.L. Penzhorn); University by L. infantum, also known as zoonotic VL (5). The na- of Guelph, Guelph, Ontario, Canada (A. Peregrine); Universität tional public health policies of Central Asian, Caucasian, Leipzig, Leipzig, Germany (M. Pfeffer); Chonnam National and some Balkan countries still recommend culling any University, Gwangju, South Korea (S. Shin); Ludwig-Maximilians- L. infantum–positive dog (1). In rural areas of China, the Universität München, Munich, Germany (R.K. Straubinger); Maghreb countries (North Africa), and parts of the Middle University of Bristol, Bristol, UK (S. Tasker); University of East, dog culling remains common practice (1), although Melbourne, Parkville, Victoria, Australia (R. Traub); The Mount medical therapy is usually allowed for dogs that are owned. Veterinary Practice, Fleetwood, UK (I. Wright); Cornell In Central and South America, dog culling has been rec- University, Ithaca, New York, USA (D.D. Bowman); Istituto ommended and practiced in several countries, including Superiore di Sanità, Rome, Italy (L. Gradoni); University of Bari Argentina, Brazil, Colombia, Uruguay, and Venezuela (1). Aldo Moro, Bari, Italy (D. Otranto) Nonetheless, this practice has been replaced by more effec- tive approaches, even in countries like Brazil, where thou- DOI: https://doi.org/10.3201/eid2512.190164 sands of dogs used to be culled every year (5). e1 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 25, No. 12, December 2019 ONLINE REPORT The Companion Vector-Borne Diseases (CVBD) indirect source, but also the parasite and, importantly, the World Forum is a group of scientists working on canine sand fly vector (13). Thus, the use of dog culling as a strat- and feline vectorborne diseases (6). This group contributes egy to reduce the incidence of VL in humans cannot be to an ongoing discussion and update on vectorborne dis- justified and should no longer be used. eases from around the world and their effects on dogs, cats, and humans. Because the topic of canine leishmaniasis is Alternative and More Effective Solutions for Better of global importance and thus frequently discussed, a con- Control of Canine Leishmaniasis sensus was reached that we should be more proactive in our A plethora of scientific evidence demonstrates that the position toward controlling this disease. At the 13th Sym- regular use of topical repellent insecticides is highly ef- posium of the CVBD World Forum, held in Windsor, UK, fective in preventing phlebotomine sand fly bites (13–15) during March 19–22, 2018, we discussed the control of ca- and, therefore, L. infantum transmission (16,17). The con- nine leishmaniasis caused by L. infantum in the context of stant use of repellent insecticides not only protects the One Health and consolidated a consensus statement about dogs from sand flies infected on other hosts (and thus from the usefulness of dog culling as a means of controlling VL. becoming infected and acting as sources of infection) but This statement targets areas where VL caused by L. infan- also enables a reduction of these vectors in the vicinity of tum is endemic and dog culling has been a common prac- humans, potentially resulting in a reduction of human in- tice. We present this consensus statement and highlight the fections and clinical VL incidence (18,19). Vaccines (i.e., futility of culling infected dogs, whether clinically healthy Leish-Tec, Ceva Saúde Animal Ltda, https://www. or sick, as a measure to control the domestic reservoir of L. ceva.com.br/Produtos/Lista-de-Produtos/LEISH-TEC; infantum and reduce the risk for VL in humans. CaniLeish, Virbac Schweiz AG, https://www.virbac.ch/ de/kleintiere-produkte/impfstoffe/canileish; and LetiFend, Scientific Reasons Why Dog Culling Laboratorios LETI, Lda., https://saludanimal.leti.com/ Is Unacceptable en/letifend-vaccine-against-canine-leishmaniasis_3944) In areas of Asia (e.g., China) where government regimes are also available in some countries for reducing the risk have promoted massive culling of all dogs (regardless of for appearance of clinical signs and disease progression seropositive status), in association with widespread use of in infected dogs (15,20). Chemotherapy (e.g., allopurinol DDT for vector control (7), the disease incidence declined plus meglumine antimoniate or allopurinol plus miltefos- for many years. However, whether this was an effect of dog ine) and immune therapy (e.g., domperidone, and dietary elimination, vector control, or both is difficult to say (5,7). In nucleotides plus active hexose correlated compound) also fact, during the past 20 years, a mass of scientific evidence may reduce the infectiousness of treated dogs, leading to a has accumulated from around the world and under different decrease of infected phlebotomine sand flies under experi- ecologic scenarios that demonstrates the failure of dog cull- mental conditions (15,21–25). ing as a control strategy, particularly in Brazil (5,7). A dog culling strategy is not supportable for several reasons. Our Consensus Advice and Practical Recommendations First, no reliable body of scientific evidence supports All veterinarians take an oath, an example of which is: “I the effectiveness of dog culling as a means of reducing solemnly swear to use my scientific knowledge and skills the incidence of VL (8,9). Second, alternative reservoir for the benefit of society through the protection of animal hosts may play a role in maintaining the life cycle of L. health and welfare, the prevention and relief of animal infantum (3,4) and must be taken into consideration when suffering, the conservation of animal resources, the pro- an integrated control strategy is formulated. Third, culled motion of public health, and the advancement of medical dogs are rapidly replaced with young dogs that are often knowledge” (https://www.avma.org/KB/Policies/Pages/ more susceptible to primary infection (10). Fourth, sero- veterinarians-oath.aspx). For the control of VL by L. in- logic diagnostic tools often used for screening dogs as part fantum, scientific data clearly align closely with the senti- of a culling program have limitations in terms of sensi- ments expressed by all veterinarians in adhering to their tivity and specificity (e.g., cross-reactivity where other oath, certain in the knowledge that preventive methods Leishmania spp. or trypanosomatids occur) (11,12). Fifth, should be used, rather than the practice of dog culling, dog culling is not a cost-effective, valid alternative from which we believe to be unethical and unjustifiable from a a socioeconomic perspective (e.g., effect of dog removal scientific viewpoint. on their owners and drugs for euthanasia) to government Using the basis of a One Health approach toward the institutions (7), particularly in developing countries, that prevention of zoonotic Leishmania infection in animals and promises a long-term solution to the problem. Finally, humans, the members of the CVBD World Forum advocate effective control of L. infantum transmission requires in- the following recommendations concerning L. infantum in- tegrated approaches focusing not only on the dog as an fection in companion animals: e2 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 25, No. 12, December 2019 Canine Leishmaniasis Control in Context of One Health 1. Companion animals should be protected from phle- Lutzomyia longipalpis and the influence of human immunodeficiency botomine sand fly bites to prevent either leishmanial virus infection. Am J Trop Med Hyg. 2018;98:126–33. https://doi.org/10.4269/ajtmh.16-0883 primary infection or spread from already infected 4. Maia C, Dantas-Torres F, Campino L. Parasite biology: the dogs. Additional control measures, including envi- reservoir hosts. In: Bruschi F, Gradoni L. editors. The ronmental vector control, vaccination, and prophylac- leishmaniases: old neglected tropical diseases. 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Vet I di Bari, Strada Provinciale per Casamassima km 3, 70010, Valenzano mmunol Immunopathol. 2002;88:13–20. https://doi.org/10.1016/ |S0165-2427(02)00128-9 70010, Italy; email: domenico.otranto@uniba.it prions Kaposi Eptesicus fuscus Plasmodium knowlesi cholera tularemia syncytium Klebsiella Vibrio vulnificus yaws Leptospira Quinine sapovirus Rickettsia variola Campylobacter Chagas disease rotavirus Lyssavirus Acinetobacter Aspergillus botulism Escherichia coli syphilis knemidocoptic mange Babesia hemozoin Naegleria fowlerii Ehrlichia Leishmaniasis etymologiarabies Bordetella Anopheles Verona integron Zika virus Herpesvirusvaccination Artemisinin Dengue Shigella Borna disease virus Ebola Franciscella tularensis typhus Rickettsia orf Coxiella burnetii kobuvirus Candida Orientia tsutsugamushi Norovirus tuberculosis Bocavirus chimera QBrucella fever Malaria measles quarantine Mange tetanus Chikungunya pertactin Borrelia Leprosyinfluenza Calcivirus quarantine Peste des petits ruminants meliodosis Diphtheria O’nyong-nyong virus Pseudoterranova Bonferroni correction azarasi pertussis Merkel cells Ignatzschineria Glanders Yersinia featured monthly in http://wwwnc.cdc.gov/eid/articles/etymologia e4 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 25, No. 12, December 2019