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Volume 25, Number 12—December 2019
Online Report

Canine Leishmaniasis Control in Context of One Health

Filipe Dantas-Torres, Guadalupe Miró, Gad Baneth, Patrick Bourdeau, Edward Breitschwerdt, Gioia Capelli, Luís Cardoso, Michael J. Day, Gerhard Dobler, Lluis 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, and Domenico OtrantoComments to Author 
Author affiliations: Aggeu Magalhães Institute, Fundação Oswaldo Cruz (Fiocruz),; Recife, Brazil (F. Dantas-Torres); Universidad Complutense de Madrid, Madrid, Spain (G. Miró, A. Sainz); Hebrew University of Jerusalem, Rehovot, Israel (G. Baneth); Ecole Nationale Vétérinaire, Nantes, France (P. Bourdeau); North Carolina State University, Raleigh, North Carolina, USA (E. Breitschwerdt, R. Maggi); Istituto Zooprofilattico Sperimentale delle Venezie, Legnaro, Italy (G. Capelli); University of Trás-os-Montes e Alto Douro (UTAD), Vila Real, Portugal (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, L. Solano-Gallego); Utrecht University, Utrecht, the Netherlands (F. Jongejan); Goethe-University, Frankfurt am Main, Germany (V.A.J. Kempf ); Freie Universität Berlin, Berlin, Germany (B. Kohn); Colorado State University, Fort Collins, Colorado, USA (M. Lappin); Oklahoma State University, Stillwater, Oklahoma, USA (S. Little); Clinglobal, Tamarin, Mauritius (M. Madder); Universidade NOVA de Lisboa, Lisbon, Portugal (C. Maia); São Paulo State University, São Paulo, Brazil (M. Marcondes); LABOKLIN GmbH, Bad Kissingen, Germany (T. Naucke); University of Naples Federico II, Naples, Italy (G. Oliva); U; niversity of Messina, Messina, Italy (M.G. Pennisi); University of Pretoria, Onderstepoort, South Africa (B.L. Penzhorn); University of Guelph, Guelph, Ontario, Canada (A. Peregrine); Universität Leipzig, Leipzig, Germany (M. Pfeffer); Chonnam National University, Gwangju, South Korea (S. Shin); Ludwig-Maximilians-Universität München, Munich, Germany (R.K. Straubinger); University of Bristol, Bristol, UK (S. Tasker); University of Melbourne, Parkville, Victoria, Australia (R. Traub); The Mount Veterinary Practice, Fleetwood, UK (I. Wright); Cornell University, Ithaca, New York, USA (D.D. Bowman); Istituto Superiore di Sanità, Rome, Italy (L. Gradoni); University of Bari Aldo Moro, Bari, Italy (D. Otranto)

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Abstract

Dogs are the main reservoir of Leishmania infantum and in some countries have been regularly culled as part of government policy to control visceral leishmaniasis. At the 13th Symposium of the Companion Vector-Borne Diseases World Forum in Windsor, UK, March 19–22, 2018, we consolidated a consensus statement regarding the usefulness of dog culling as a means of controlling visceral leishmaniasis. The statement highlighted the futility of culling infected dogs, whether healthy or sick, as a measure to control the domestic reservoir of L. infantum and reduce the risk for visceral leishmaniasis.

Visceral leishmaniasis (VL), caused by Leishmania donovani in Asia and Africa and by L. infantum in the Mediterranean Basin, the Middle East, Central Asia, South America, and Central America, is a life-threatening disease that affects ≈200,000–400,000 persons annually and causes an estimated ≈20,000–40,000 deaths per year (1,2). Although an increasing number of other mammalian hosts, including infected humans, have served as effective reservoirs by infecting phlebotomine sand fly vectors, dogs remain a pivotal indirect source in many situations where the transmission cycle of L. infantum occurs (3,4).

Over the years, millions of dogs have been killed as part of government policies to control human VL caused by L. infantum, also known as zoonotic VL (5). The national public health policies of Central Asian, Caucasian, and some Balkan countries still recommend culling any L. infantum –positive dog (1). In rural areas of China, the Maghreb countries (North Africa), and parts of the Middle East, dog culling remains common practice (1), although medical therapy is usually allowed for dogs that are owned. In Central and South America, dog culling has been recommended and practiced in several countries, including Argentina, Brazil, Colombia, Uruguay, and Venezuela (1). Nonetheless, this practice has been replaced by more effective approaches, even in countries like Brazil, where thousands of dogs used to be eliminated every year (5).

The Companion Vector-Borne Diseases (CVBD) World Forum is a group of scientists working on canine and feline vectorborne diseases (6). This group contributes to an ongoing discussion and update on vectorborne diseases from around the world and their effects on dogs, cats, and humans. Because the topic of canine leishmaniosis is of global importance and thus frequently discussed, a consensus was reached that we should be more proactive in our position toward controlling this disease. At the 13th Symposium of the CVBD World Forum, held in Windsor, UK, during March 19–22, 2018, we discussed the control of canine leishmaniosis caused by L. infantum in the context of One Health and consolidated a consensus statement about the usefulness of dog culling as a means of controlling VL. This statement targets areas where VL caused by L. infantum is endemic and dog culling has been a common practice. We present this consensus statement and highlight the futility of culling infected dogs, whether clinically healthy or sick, as a measure to control the domestic reservoir of L. infantum and reduce the risk for VL in humans.

Scientific Reasons Why Dog Culling Is Unacceptable

In areas of Asia (e.g., China) where government regimes have promoted massive culling of all dogs (regardless of seropositive status), in association with widespread use of DDT for vector control (7), the disease incidence declined for many years. However, whether this was an effect of dog elimination, vector control, or both is difficult to say (5,7). In fact, during the past 20 years, a mass of scientific evidence has accumulated from around the world and under different ecologic scenarios that demonstrates the failure of dog culling as a control strategy, particularly in Brazil (5,7). A dog culling strategy is not supportable for several reasons.

First, no reliable body of scientific evidence supports the effectiveness of dog culling as a means of reducing the incidence of VL (8,9). Second, alternative reservoir hosts may play a role in maintaining the life cycle of L. infantum (3,4) and must be taken into consideration when an integrated control strategy is formulated. Third, culled dogs are rapidly replaced with young dogs that are often more susceptible to primary infection (10). Fourth, serologic diagnostic tools often used for screening dogs as part of a culling program have limitations in terms of sensitivity and specificity (e.g., cross-reactivity where other Leishmania spp. or trypanosomatids occur) (11,12). Fifth, dog culling is not a cost-effective, valid alternative from a socioeconomic perspective (e.g., effect of dog removal on their owners and drugs for euthanasia) to government institutions (7), particularly in developing countries, that promises a long-term solution to the problem. Finally, effective control of L. infantum transmission requires integrated approaches focusing not only on the dog as an indirect source, but also the parasite and, importantly, the sand fly vector (13). Thus, the use of dog culling as a strategy to reduce the incidence of VL in humans cannot be justified and should no longer be used.

Alternative and More Effective Solutions for Better Control of Canine Leishmaniosis

A plethora of scientific evidence demonstrates that the regular use of topical repellent insecticides is highly effective in preventing phlebotomine sand fly bites (1315) and, therefore, L. infantum transmission (16,17). The constant use of repellent insecticides not only protects the dogs from sand flies infected on other hosts (and thus from becoming infected and acting as sources of infection) but also enables a reduction of these vectors in the vicinity of humans, potentially resulting in a reduction of human infections and clinical VL incidence (18,19). Vaccines (i.e., Leish-Tec, Ceva Saúde Animal Ltda, https://www.ceva.com.br/Produtos/Lista-de-Produtos/LEISH-TEC; CaniLeish, Virbac Schweiz AG, https://www.virbac.ch/de/kleintiere-produkte/impfstoffe/canileish; and LetiFend, Laboratorios LETI, Lda., https://saludanimal.leti.com/en/letifend-vaccine-against-canine-leishmaniasis_3944) are also available in some countries for reducing the risk for appearance of clinical signs and disease progression in infected dogs (15,20). Chemotherapy (e.g., allopurinol plus meglumine antimoniate or allopurinol plus miltefosine) and immune therapy (e.g., domperidone, and dietary nucleotides plus active hexose correlated compound) also may reduce the infectiousness of treated dogs, leading to a decrease of infected phlebotomine sand flies under experimental conditions (15,2125).

Our Consensus Advice and Practical Recommendations

All veterinarians take an oath, an example of which is: “I solemnly swear to use my scientific knowledge and skills for the benefit of society through the protection of animal health and welfare, the prevention and relief of animal suffering, the conservation of animal resources, the promotion of public health, and the advancement of medical knowledge” (https://www.avma.org/KB/Policies/Pages/veterinarians-oath.aspx). For the control of VL by L. infantum, scientific data clearly align closely with the sentiments expressed by all veterinarians in adhering to their oath, certain in the knowledge that preventive methods should be used, rather than the practice of dog culling, which we believe to be unethical and unjustifiable from a scientific viewpoint.

Based on a One Health approach toward the prevention of zoonotic Leishmania infection in animals and humans, the members of the CVBD World Forum advocate the following recommendations concerning L. infantum infection in companion animals:

1. Companion animals should be protected from phlebotomine sand fly bites to prevent either leishmanial primary infection or spread from already infected dogs. Additional control measures, including environmental vector control, vaccination, and prophylactic medications (14,15,26), may also be used where available.

2. Dog culling in areas where VL is endemic should be replaced with alternative nonterminal measures that can prevent infection in dogs.

The members of the CVBD World Forum recommend the following measures to reduce the risk for L. infantum infection in dogs and in humans:

1. Promote phlebotomine sand fly bite prevention to reduce the risk for L. infantum infection in noninfected dogs and its spread from already infected dogs.

2. Improve the general health and nutritional status of dogs.

3. Implement latest concepts regarding the clinical management of canine leishmaniosis, including approaches to diagnosis and treatment.

4. Improve environmental and housing conditions to enhance phlebotomine sand fly control and reduce the exposure of humans to the vectors.

Dr. Dantas-Torres is a public health researcher at Aggeu Magalhães Institute (Fiocruz) and a founding director and scientific guidelines coordinator of the Tropical Council for Companion Animal Parasites (TroCCAP). His research interests include epidemiology, diagnosis, and prevention of vector-borne diseases, including leishmaniasis.

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Acknowledgments

We thank Bayer Animal Health for organizing and facilitating our discussion at the 13th Symposium of the CVBD World Forum.

F.D.T. received a research fellowship from CNPq (Bolsa de Produtividade; grant no. 313118/2018-3). C.M. has the support of the Fundação para a Ciência e Tecnologia/Ministério da Ciência, Tecnologia e Ensino Superior (Investigator Starting Grant IF/01302/2015).

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References

  1. Alvar  J, Vélez  ID, Bern  C, Herrero  M, Desjeux  P, Cano  J, et al.; WHO Leishmaniasis Control Team. Leishmaniasis worldwide and global estimates of its incidence. PLoS One. 2012;7:e35671. DOIPubMed
  2. Burza  S, Croft  SL, Boelaert  M. Leishmaniasis. Lancet. 2018;392:95170. DOIPubMed
  3. Ferreira  GR, Castelo Branco Ribeiro  JC, Meneses Filho  A, de Jesus Cardoso Farias Pereira  T, Parente  DM, Pereira  HF, et al. Human competence to transmit Leishmania infantum to Lutzomyia longipalpis and the influence of human immunodeficiency virus infection. Am J Trop Med Hyg. 2018;98:12633. DOIPubMed
  4. Maia  C, Dantas-Torres  F, Campino  L. Parasite biology: the reservoir hosts. In: Bruschi F, Gradoni L. editors. The leishmaniases: old neglected tropical diseases. Cham (Switzerland): Springer International Publishing AG; 2018. p 79–106.
  5. Dantas-Torres  F, Miró  G, Bowman  DD, Gradoni  L, Otranto  D. Culling dogs for zoonotic visceral leishmaniasis control: the wind of change. Trends Parasitol. 2019;35:97101. DOIPubMed
  6. Baneth  G, Bourdeau  P, Bourdoiseau  G, Bowman  D, Breitschwerdt  E, Capelli  G, et al.; CVBD World Forum. Vector-borne diseases—constant challenge for practicing veterinarians: recommendations from the CVBD World Forum. Parasit Vectors. 2012;5:55. DOIPubMed
  7. Costa  CH. How effective is dog culling in controlling zoonotic visceral leishmaniasis? A critical evaluation of the science, politics and ethics behind this public health policy. Rev Soc Bras Med Trop. 2011;44:23242. DOIPubMed
  8. Romero  GA, Boelaert  M. Control of visceral leishmaniasis in latin america-a systematic review. PLoS Negl Trop Dis. 2010;4:e584. DOIPubMed
  9. González  U, Pinart  M, Sinclair  D, Firooz  A, Enk  C, Vélez  ID, et al. Vector and reservoir control for preventing leishmaniasis. Cochrane Database Syst Rev. 2015; (8):CD008736. DOIPubMed
  10. Nunes  CM, Pires  MM, da Silva  KM, Assis  FD, Gonçalves Filho  J, Perri  SH. Relationship between dog culling and incidence of human visceral leishmaniasis in an endemic area. Vet Parasitol. 2010;170:1313. DOIPubMed
  11. Silva  DA, Madeira  MF, Teixeira  AC, de Souza  CM, Figueiredo  FB. Laboratory tests performed on Leishmania seroreactive dogs euthanized by the leishmaniasis control program. Vet Parasitol. 2011;179:25761. DOIPubMed
  12. Travi  BL, Cordeiro-da-Silva  A, Dantas-Torres  F, Miró  G. Canine visceral leishmaniasis: Diagnosis and management of the reservoir living among us. PLoS Negl Trop Dis. 2018;12:e0006082. DOIPubMed
  13. Gálvez  R, Montoya  A, Fontal  F, Martínez De Murguía  L, Miró  G. Controlling phlebotomine sand flies to prevent canine Leishmania infantum infection: A case of knowing your enemy. Res Vet Sci. 2018;121:94103. DOIPubMed
  14. Wylie  CE, Carbonell-Antoñanzas  M, Aiassa  E, Dhollander  S, Zagmutt  FJ, Brodbelt  DC, et al. A systematic review of the efficacy of prophylactic control measures for naturally occurring canine leishmaniosis. Part II: topically applied insecticide treatments and prophylactic medications. [Erratum in: Prev Vet Med. 2015;120:250–1]. Prev Vet Med. 2014;117:1927. DOIPubMed
  15. Miró  G, Petersen  C, Cardoso  L, Bourdeau  P, Baneth  G, Solano-Gallego  L, et al. Novel areas for prevention and control of canine leishmaniosis. Trends Parasitol. 2017;33:718–30. [Erratum in: Novel Areas for Prevention and Control of Canine Leishmaniosis]. Trends Parasitol. 2017;33:71830.PubMed
  16. Otranto  D, Dantas-Torres  F, de Caprariis  D, Di Paola  G, Tarallo  VD, Latrofa  MS, et al. Prevention of canine leishmaniosis in a hyper-endemic area using a combination of 10% imidacloprid/4.5% flumethrin. PLoS One. 2013;8:e56374. DOIPubMed
  17. Brianti  E, Gaglio  G, Napoli  E, Falsone  L, Prudente  C, Solari Basano  F, et al. Efficacy of a slow-release imidacloprid (10%)/flumethrin (4.5%) collar for the prevention of canine leishmaniosis. Parasit Vectors. 2014;7:327. DOIPubMed
  18. Gavgani  AS, Hodjati  MH, Mohite  H, Davies  CR. Effect of insecticide-impregnated dog collars on incidence of zoonotic visceral leishmaniasis in Iranian children: a matched-cluster randomised trial. Lancet. 2002;360:3749. DOIPubMed
  19. Courtenay  O, Bazmani  A, Parvizi  P, Ready  PD, Cameron  MM. Insecticide-impregnated dog collars reduce infantile clinical visceral leishmaniasis under operational conditions in NW Iran: A community-wide cluster randomised trial. PLoS Negl Trop Dis. 2019;13:e0007193. DOIPubMed
  20. Solano-Gallego  L, Cardoso  L, Pennisi  MG, Petersen  C, Bourdeau  P, Oliva  G, et al. Diagnostic challenges in the era of canine Leishmania infantum vaccines. Trends Parasitol. 2017;33:70617. DOIPubMed
  21. Gradoni  L, Maroli  M, Gramiccia  M, Mancianti  F. Leishmania infantum infection rates in Phlebotomus perniciosus fed on naturally infected dogs under antimonial treatment. Med Vet Entomol. 1987;1:33942. DOIPubMed
  22. Guarga  JL, Moreno  J, Lucientes  J, Gracia  MJ, Peribáñez  MA, Castillo  JA. Evaluation of a specific immunochemotherapy for the treatment of canine visceral leishmaniasis. Vet Immunol Immunopathol. 2002;88:1320. DOIPubMed
  23. Miró  G, Gálvez  R, Fraile  C, Descalzo  MA, Molina  R. Infectivity to Phlebotomus perniciosus of dogs naturally parasitized with Leishmania infantum after different treatments. Parasit Vectors. 2011;4:52. DOIPubMed
  24. Courtenay  O, Carson  C, Calvo-Bado  L, Garcez  LM, Quinnell  RJ. Heterogeneities in Leishmania infantum infection: using skin parasite burdens to identify highly infectious dogs. PLoS Negl Trop Dis. 2014;8:e2583. DOIPubMed
  25. Segarra  S, Miró  G, Montoya  A, Pardo-Marín  L, Teichenné  J, Ferrer  L, et al. Prevention of disease progression in Leishmania infantum-infected dogs with dietary nucleotides and active hexose correlated compound. Parasit Vectors. 2018;11:103. DOIPubMed
  26. Wylie  CE, Carbonell-Antoñanzas  M, Aiassa  E, Dhollander  S, Zagmutt  FJ, Brodbelt  DC, et al. A systematic review of the efficacy of prophylactic control measures for naturally-occurring canine leishmaniosis, part I: vaccinations. Prev Vet Med. 2014;117:718. DOIPubMed

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Suggested citation for this article: Dantas-Torres F, Miró G, Baneth G, Bourdeau P, Breitschwerdt E, Capelli G, et al. Canine leishmaniasis control in context of One Health. Emerg Infect Dis. 2019 Dec [date cited]. https://doi.org/10.3201/eid2512.190164

DOI: 10.3201/eid2512.190164

Original Publication Date: 10/31/2019

Table of Contents – Volume 25, Number 12—December 2019

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Domenico Otranto, Università degli Studi di Bari, Strada Provinciale per Casamassima km 3, 70010, Valenzano 70010, Italy

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Page created: October 31, 2019
Page updated: October 31, 2019
Page reviewed: October 31, 2019
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
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