Aggeu Magalhães Research Centre, Oswaldo Cruz Foundation (Fiocruz), Recife, Pernambuco, Brazil
Introduction
The leishmaniases are diseases caused by protozoa (Leishmania spp.), which are transmitted through the bite of phlebotomine sand flies (flebótomos). Only females are capable of transmitting these protozoa and they do so because they need to feed on blood to get the necessary nutrients for egg production. This is an important concept, as it teaches us that the best way to prevent Leishmania infection is through the use of personal protection measures (e.g., repellents) to reduce or eliminate the contact with the vectors. Nonetheless, even if veterinarians and medical physicians may know "what to do," the prevention of leishmaniasis remains a difficult task, considering the complexities involved in the disease epidemiology.
The objective of this state-of-the-art lecture is to provide a comprehensive overview on leishmaniasis from a One Health perspective.
Animals: From Hosts to Patients
Animals of different orders and species may be infected by Leishmania spp. It is pertinent to grasp this opportunity to emphasize that finding an animal infected by a given Leishmania sp. does not imply a reservoir role. Indeed, many domestic animals (e.g., horses) have been found infected by Leishmania spp., but are mere accidental hosts.
Primary hosts of Leishmania spp. include, for example, rodents, marsupials, sloths, forest primates, foxes, anteaters and armadillos. For instance, forest rodents are implicated as the primary hosts of Leishmania braziliensis, Leishmania mexicana and Leishmania amazonensis, while Leishmania panamensis is primarily a parasite of sloths.1
Although predominantly associated to wild animals, Leishmania spp. have adapted to the peridomestic environment, with domestic animals acting as potential reservoirs. Dogs are considered to be the principal reservoirs of Leishmania infantum in several countries in the Old and New Worlds2 and Leishmania peruviana in high Andean valleys in Peru. Dogs are frequently infected by L. braziliensis in rural areas in Latin America,3 but their role as reservoirs is probably negligible.
Most Leishmania spp.-infected animals exhibit no apparent clinical sign, but a small proportion of them may develop overt disease. This may happen with both wild and domestic animals. For instance, dogs and cats may be affected by different Leishmania spp., developing from self-healing skin ulcers to systemic, life-threatening disease. Veterinary practitioners working in endemic areas are familiarised with canine and, sometimes, feline patients with leishmaniasis. From a One Health perspective, veterinary practitioners dealing with leishmaniasis patients should always dedicate their time to instruct the owners regarding the disease and its prevention.
People at Risk
From a global perspective, it is estimated that more than 12 million people are infected with Leishmania spp. and 350 million are at risk. Recent estimates suggest that up to 0.4 million VL cases and 1.2 million CL cases occur each year. While present in 98 countries and three territories, over 90% of VL cases are concentrated in only six countries (i.e., India, Bangladesh, Sudan, South Sudan, Ethiopia, and Brazil) and most cases (70–75%) of CL occur in ten countries (i.e., Afghanistan, Algeria, Colombia, Brazil, Iran, Syria, Ethiopia, North Sudan, Costa Rica, and Peru).4
About 90% of the leishmaniasis cases reported in Latin America are from Brazil. The risk of infection by different Leishmania spp. varies widely. For instance, people living in rural areas, close to forest environments, are at risk of infection by Leishmania braziliensis, which occurs in all leishmaniasis endemic countries in the Americas except Guyana, Surinam and the United States. Leishmania guyanensis occurs in the Guyanas and northern Brazil, being mostly associated to forest workers. Leishmania amazonensis is rarely reported in humans, mainly because its phlebotomine vector (Lutzomyia flaviscutelata) prefers rodents as hosts and lives in swampy areas of the forest that are seldom frequented by people. As another example, Leishmania panamensis is found in Colombia, Costa Rica, Ecuador, Guatemala, Honduras, Nicaragua, and Panama. The disease it causes is common in agricultural workers and in military personnel during incursions into the jungle.
The Environment
The environment plays an important role with the transmission cycle of Leishmania spp., because it is where primary hosts, vectors and susceptible hosts encounter each other and where the transmission occurs. Herein, the "environment" should be intended as any place where the transmission may occur, including a forest, a crop plantation, the backyard of a house, and so on.5-7
Leishmania spp. infections are usually acquired in rural areas and natural environments (e.g., tropical rainforests), where Leishmania spp. may be maintained enzootically among wild animals. Indeed, in a recent past, leishmaniasis was considered to be a typical "rural disease" in Brazil, as it was almost exclusively found among agricultural workers, frequently associated with areas of deforestation and with land use changes. Nowadays, the disease is also prevalent in large urban centres, particularly among poor people living on urban periphery in shantytown settlements. The classical example is visceral leishmaniasis caused by L. infantum, a parasite that used to be restricted to poor rural areas, but nowadays is commonly found in urban areas in Brazil.
Another important aspect is that the environment is strongly influenced by the climate and vice versa. Climate changes currently in place on Earth may increase the risk of transmission of vector-borne diseases, including leishmaniasis. Indeed, phlebotomine sand flies are directly dependent on and influenced by climate variables.6,7 Increasing annual average temperatures may result in increases in vector populations in some areas where they are present and allow the establishment of permanent populations in areas where the low temperatures are currently limiting factors.
Conclusion
In the past century, we have witnessed profound changes in the environment where we live, being many of these changes produced by ourselves. For instance, structural changes in the 20th century have transformed Latin America from a largely rural region to a largely urban society in the first decade of the 21st century. This urbanization phenomenon has caused profound changes in our societies, as well as in the epidemiology of diseases like leishmaniasis.
The growing world population is increasingly demanding for more food, water and houses. As a result, we are destroying more forests, producing more waste, polluting more and so forth. By destroying natural habitats, we are pressuring wild animals to adapt to man-modified environments. This close contact between humans and wild animals may increase the opportunity of parasite transmission to both animals and people. For example, 13 out of the 21 human-infective Leishmania spp. have also been detected in domestic dogs.8 From a comparative medicine viewpoint, this fact suggests that dogs are probably susceptible to several Leishmania species, just as humans do.
From a One Health perspective, any attempt to control leishmaniasis should take into account animals, people and the environment. It is crucial to avoid or to reduce the contact with phlebotomine sand fly vectors, by using repellents on dogs (e.g., collars or spot-on pipettes)9 and also on humans, particularly in high-risk situations, such as during nocturnal stays in tropical rainforests in Latin America. Public health authorities in high-risk areas should promote the use of individual (e.g., avoidance of risk exposure, use of bed nets and repellents) and collective measures (e.g., indoor residual spraying) to reduce the burden of leishmaniasis in endemic areas.
References
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7. Miranda DE, Sales KG, Faustino MA, Alves LC, Brandão-Filho SP, Dantas-Torres F, de Carvalho GA. Ecology of sand flies in a low-density residential rural area, with mixed forest/agricultural exploitation, in north-eastern Brazil. Acta Trop. 2015;146:89–94.
8. Cantacessi C, Dantas-Torres F, Nolan MJ, Otranto D. The past, present, and future of Leishmania genomics and transcriptomics. Trends Parasitol. 2015;31(3):100–8.
9. Otranto D, Dantas-Torres F. The prevention of canine leishmaniasis and its impact on public health. Trends Parasitol. 2013;29(7):339–45.