Introduction

Canine leishmaniasis is a vector-borne disease of great medico-veterinary relevance, which affects dogs from all continents, except Oceania.¹ From an epidemiological point of view, canine leishmaniasis is a multifaceted disease and, for this reason, its control is not easy to achieve² and requires a holistic approach focused on both dogs and phlebotomine vectors. Novel and cost-effective strategies against canine leishmaniasis have been developed and made available in the veterinary market. Nowadays, different tools are available for the prevention of canine leishmaniasis, including vaccines and repellents. In this seminar, the current knowledge on the prevention and control of canine leishmaniasis is summarized.

Preventing the Infection: Vector Control

The control of phlebotomine vectors involves the use of insecticides and repellents on dogs or in the environment. Indoors residual spraying may be useful in particular situations, such as when a high density of phlebotomine sand flies is found near or in human habitations. Similarly, chicken coops, pigsties, corrals, and dog shelters may concentrate large number of phlebotomine vectors and should be targeted by control activities. The application of insecticides on the walls and roofs of human habitations and in animal shelters has been shown to be effective in reducing the population of phlebotomine sand flies.³ However, environmental and human health hazard concerns around the employment of organochlorides and other chemical groups (e.g., organophosphates and carbamates) have progressively led to their substitution by synthetic pyrethroids (e.g., a-cypermethrin, cypermethrin, deltamethrin, and l-cyhalothrin), which are currently used by public health authorities in several countries. Nonetheless, the application of insecticides in the environment may eventually have only a transitory effect and may be unsustainable in the long term for several technical and economic reasons. In addition, information on vector population dynamics is fundamental to optimize timing and modalities of insecticide applications.

The use of repellents on dogs has become the most effective tool for prevention of L. infantum infection in these animals. They cause insect disorientation and sudden abandonment of the host, followed by death soon after the landing of an insect on the coat of a treated animal. Hence, blood feeding usually does not occur and the infection is usually prevented. The effect of synthetic pyrethroids in spot-on formulations or collars may last from 1 to approximately 8 months, respectively.^4–6

When a spot-on formulation is applied, it usually takes 24 h for the insecticide to spread throughout the stratum corneum. On the contrary, powders and sprays have an immediate effect but a short residual activity. For example, the insecticidal effect of deltamethrin and permethrin, alone or in combination with other insecticides (e.g., imidacloprid), was experimentally tested against different sand fly vectors by evaluating the number of unfed female sand flies collected soon after contact with a treated animal and their mortality within 24 h after exposure to treated dogs. The results of laboratory studies were generally positive, with an antifeeding effect ranging from 84% to 96% of sand flies and an insecticidal activity of near 100% in the few fed females. Indeed, the use of pyrethroids with repellent properties in impregnated collars and spot-on formulations showed to be a suitable approach to reduce the risk of L. infantum infection in dogs. Specifically, collars containing 4% deltamethrin (Scalibor, Intervet)^4,7 or 10% imidacloprid and 4.5% flumethrin (Seresto, Bayer Animal Health),⁶ and a spot-on formulation containing 10% imidacloprid and 50% permethrin (Advantix, Bayer)⁵ have been used for reducing the biting rate of sand fly vectors, exhibiting protection rates ranging from 50% to 100% over two consecutive transmission seasons.

Preventing the Disease: Vaccines

Vaccination is an approach for preventing canine leishmaniasis, which is now available in Brazil and Europe. A vaccine prepared with a glycoprotein known as the fucose mannose ligand of Leishmania donovani (Leishmune, Fort Dodge Animal Health) has been licensed for use in Brazil, and it showed an efficacy of 76% and a protection of 92%.⁸ Another vaccine using ES antigen purified from culture supernatant of L. infantum promastigotes and Quillaja saponaria (QA21) as an adjuvant (CaniLeish, Virbac Animal Health) has been licensed recently in Europe and displayed 68.4% efficacy in protecting animals against the appearance of clinical signs under field conditions.⁹ Analogously, a vaccine using a recombinant A2-antigen of Leishmania amastigotes with saponin as an adjuvant (Leish-Tec, Hertape Calier) showed an efficacy ranging from 58.1% to 80.8%, depending on diagnostic criteria used.¹⁰

Conclusion

Based on current knowledge, topical products with repellent activity represent a powerful tool for reducing the transmission of infection to dogs. Currently, the use of repellents in different formulations may induce a high degree of protection in dogs at individual and population level.

The effectiveness of the combined use of vaccines plus repellents in preventing L. infantum infection and subsequent disease development should be assessed by means of large-scale, randomized controlled field trials. This combined strategy may become the next frontier in the control of canine leishmaniasis. Finally, synergism between medical physicians, veterinary practitioners, researchers, public health authorities, and politicians is central to find a one-base platform for planning sustainable control strategies against canine leishmaniasis, and also from a one-health perspective.

References

1.  Dantas-Torres F, Solano-Gallego L, Baneth G, Ribeiro VM, de Paiva-Cavalcanti M, Otranto D. Canine leishmaniosis in the Old and New Worlds: unveiled similarities and differences. Trends Parasitol. 2012;28(12):531–538.

2.  Otranto D, Dantas-Torres F. The prevention of canine leishmaniasis and its impact on public health. Trends Parasitol. 2013;29(7):339–345.

3.  Maroli M, Gradoni L, Oliva G, Castagnaro M, Crotti A, Lubas G, Paltrinieri S, Roura X, Zini E, Zatelli A. Guidelines for prevention of leishmaniasis in dogs. J Am Vet Med Assoc. 2010;236(11):1200–1206.

4.  Killick-Kendrick R, Killick-Kendrick M, Focheux C, Dereure J, Puech MP, Cadiergues MC. Protection of dogs from the bites of phlebotomine sandflies by deltamethrin collars for the control of canine leishmaniasis. Med Vet Entomol. 1997;11(2):105–111.

5.  Otranto D, de Caprariis D, Lia RP, Tarallo V, Lorusso V, Testini G, Dantas-Torres F, Latrofa S, Diniz PP, Mencke N, Maggi RG, Breitschwerdt E, Capelli G, Stanneck D. Prevention of endemic canine vector-borne diseases using imidacloprid 10% and permethrin 50% in young dogs: a longitudinal field study. Vet Parasitol. 2010;172(3–4):323–332.

6.  Otranto D, Dantas-Torres F, de Caprariis D, Di Paola G, Tarallo VD, Latrofa MS, Lia RP, Annoscia G, Breitshwerdt EB, Cantacessi C, Capelli G, Stanneck D. Prevention of canine leishmaniosis in a hyper-endemic area using a combination of 10% imidacloprid/4.5% flumethrin. PLoS One. 2013;8(2):e56374.

7.  Maroli M, Mizzon V, Siragusa C, D'Oorazi A, Gradoni L. Evidence for an impact on the incidence of canine leishmaniasis by the use of deltamethrin-impregnated dog collars in southern Italy. Med Vet Entomol. 2001;15(4):358–363.

8.  Borja-Cabrera GP, Correia Pontes NN, da Silva VO, Paraguai de Souza E, Santos WR, Gomes EM, Luz KG, Palatnik M, Palatnik de Sousa CB. Long lasting protection against canine kala-azar using FML-QuilA saponin vaccine in an endemic area of Brazil (São Gonçalo do Amaranto, RN). Vaccine. 2002;20(27–28):3277–3284.

9.  Regina-Silva S, Feres AM, França-Silva JC, Dias ES, Michalsky ÈM, de Andrade HM, Coelho EA, Ribeiro GM, Fernandes AP, Machado-Coelho GL. Field randomized trial to evaluate the efficacy of the Leish-Tec® vaccine against canine visceral leishmaniasis in an endemic area of Brazil. Vaccine. 2016;34(19):2233–2239.

10. Oliva G, Nieto J, Foglia Manzillo V, Cappiello S, Fiorentino E, Di Muccio T, Scalone A, Moreno J, Chicharro C, Carrillo E, Butaud T, Guegand L, Martin V, Cuisinier AM, McGahie D, Gueguen S, Cañavate C, Gradoni L. A randomised, double-blind, controlled efficacy trial of the LiESP/QA-21 vaccine in naïve dogs exposed to two Leishmania infantum transmission seasons. PLoS Negl Trop Dis. 2014;8(10):e3213.