One Health Approach to Leishmaniases: Understanding the Disease Dynamics Through Diagnostic Tools
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pathogens Review One Health Approach to Leishmaniases: Understanding the Disease Dynamics through Diagnostic Tools Ahyun Hong 1, Ricardo Andrade Zampieri 1 , Jeffrey Jon Shaw 2, Lucile Maria Floeter-Winter 1 and Maria Fernanda Laranjeira-Silva 1,* 1 Department of Physiology, Institute of Biosciences, University of São Paulo, São Paulo 05508-090, Brazil; [email protected] (A.H.); [email protected] (R.A.Z.); [email protected] (L.M.F.-W.) 2 Department of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo 05508-000, Brazil; jeff[email protected] * Correspondence: [email protected] Received: 28 July 2020; Accepted: 21 September 2020; Published: 1 October 2020 Abstract: Leishmaniases are zoonotic vector-borne diseases caused by protozoan parasites of the genus Leishmania that affect millions of people around the globe. There are various clinical manifestations, ranging from self-healing cutaneous lesions to potentially fatal visceral leishmaniasis, all of which are associated with different Leishmania species. Transmission of these parasites is complex due to the varying ecological relationships between human and/or animal reservoir hosts, parasites, and sand fly vectors. Moreover, vector-borne diseases like leishmaniases are intricately linked to environmental changes and socioeconomic risk factors, advocating the importance of the One Health approach to control these diseases. The development of an accurate, fast, and cost-effective diagnostic tool for leishmaniases is a priority, and the implementation of various control measures such as animal sentinel surveillance systems is needed to better detect, prevent, and respond to the (re-)emergence of leishmaniases. Keywords: Leishmania; protozoan parasite; epidemiology; environment; diagnosis 1. Introduction Leishmaniases are vector-borne diseases caused by protozoan parasites of the genus Leishmania and are transmitted amongst mammalian hosts by phlebotomine sandflies. They are endemic in 98 countries and are estimated to affect over 350 million people around the globe [1,2]. The diseases can be categorized into two types according to the primary reservoir hosts of the human infection: zoonosis and anthroponosis. Zoonosis refers to an infectious disease of animals that can be transmitted to humans, and anthroponosis refers to a naturally occurring infectious disease among humans [3,4]. The majority of the Leishmania species are involved in zoonotic transmission. Infected animal reservoir hosts are often introduced into the human population and spillover events result in zoonotic diseases (Figure1). Twenty-two Leishmania species belonging to the subgenera L. (Leishmania), L. (Mundinia), and L.(Viannia)[5] are found in humans. Among these, just two L. (L.) donovani and L. (L.) tropica are associated with an anthroponotic cycle (Table1). However, infections of both species have been reported in livestock animals in Nepal [6,7], and in hyraxes and dogs in the Mediterranean Basin and several countries in Africa [8]. Pathogens 2020, 9, 809; doi:10.3390/pathogens9100809 www.mdpi.com/journal/pathogens Pathogens 2020, 9, 809 2 of 24 Pathogens 2020, 9, x FOR PEER REVIEW 3 of 23 FigureFigure 1. 1.The The transmission transmission cycles cycles ofof zoonoticzoonotic leishmaniases. Sylvatic Sylvatic leishmaniases leishmaniases can can spill spill over over into into humanshumans living living in in proximity proximity to to forest forest focifoci ofof transmission,transmission, mainly due due to to deforestation deforestation or or other other factors factors affaffectingecting the the ecological ecological balance. balance. AsAs depicteddepicted by arrows, sand sand fly fly vectors, vectors, whose whose primary primary forests forests are are theirtheir natural natural breeding breeding sites, sites, adapt adapt toto peri-domesticperi-domestic and domestic domestic environments environments and and eventually eventually invade invade denselydensely populated populated urban urban environments environments (modified(modified fromfrom [[9]).9]). Table 1. Clinical manifestations, reservoir host, and geographical distribution of Leishmania species Leishmaniases present a broad spectrum of clinical manifestations, ranging from self-healing (modified from [1]). localized or multiple cutaneous lesions to mucosal lesions and potentially fatal visceral forms. These different formsSpecies are often associated Clinical Manifestation with a particul Reservoirar species Host or subgenus, nonetheless, Country/Region they are not unique to a species [10]. In most cases, cutaneous leishmaniasis (CL)VL: skin West and lesions Central are Asia, self-healing China, The Indian and subcontinent, The Mediterranean Basin, leave permanentL. (L.) donovani scars. However,AVL, PKDL, some CL species Humancan lead to moreEast Africa; severe CL: The pathologies Mediterranean Basin; such ML: as North Africa; PKDL: The Indian subcontinent, East mucocutaneous (MCL), diffuse (DCL), or disseminated (DL) cutaneous andleishmaniases. North Africa Visceral VL: Central and West Asia, China, leishmaniasis (VL), also known as kala-azar, is Human,the most Dog, Fox,severe Jackal, form of leishmaniases and can be fatal The Mediterranean Basin, Africa; CL: L. (L.) infantum AVL, ZVL, CL Badger, Rodent, Cat, unless treated. Common clinical signs include non-tender splenomegaly,The Mediterranean Basin, with West Asia,or China,without Opossum West Africa hepatomegaly, and individuals with pre-existing health conditionsWest and may Central develop Asia, The Indian post-kala-azar subcontinent, L. (L.) major ZCL Rodent dermal leishmaniasis (PKDL) consequent to the treatment [1]. The Mediterranean Basin, Africa Central, South and West Asia, The Mediterranean Eurasia (Old World) Due toL. the (L.) tropicacomplex relationshipACL, ZCLAVL between Human,human, HyraxHuman animal hosts, parasites,Basin, and East Africasand fly vectors, the transmission of Leishmania spp. is intricate. Moreover, vector-borne diseasesWest Asiaare influenced by L. (L.) killicki CL Unknown The Mediterranean Basin environmentalL. (L.) aethiopicachanges and socioeconomicZCL, DCL, ML factors Hyrax, su Rodentch as poorCL: housing East Africa (Ethiopiaand sanitary and Kenya); conditions, ML: Ethiopia L. (M.) orientalis CL, DL, VL Unknown Thailand malnutrition,L. (L.) infantum or population chagasi movement.ZVL, CL Anthropogeni Dog, Cat, Fox,c Opossumfactors tend to South reorient and Central the America, composition Mexico and behavior ofL. sand (L.) mexicana fly vectors. ToZCL, date, MCL, there DCL are at Rodent,least Opossum50 different sand fly species Americas known to transmit L. (L.) pifanol DCL Unknown Venezuela leishmaniases.L. (L.) venezuelensis In general, each sandCL fly species has Unknown its preferred ecological Venezuelaniche and transmits a L. (L.) garnhami ZCL Unknown Central America, Venezuela certain LeishmaniaL. (L.) amazonensis species (reviewedZCL, DCL, CLin [11]). Furthermore, Rodent zoonotic leishmaniases South America have a broad Dog, Horse, Donkey, mammalianL. (V.) reservoir braziliensis diversityZCL, in MCL, different DL parts of the world [12].South The and sylvatic Central America, transmission Mexico is Mule, Rodent, Opossum affected byL. the (L.) waltoniwildlife populationDCL in and around human Unknown settlements. Divergent Dominican species Republic of sylvatic, Sloth, Anteater, domestic, L.and (V.) guyanesissynanthropic animalsZCL, MCL have been reported as reservoir hostsSouth for Americavarious Leishmania Opossum Dog, Sloth, Opossum, species aroundL. (V.) panamensis the globe—rodents,ZCL, MCL foxes, dogs, cats, primates, hyraxes,South and and bats Central are America among those Tamandua maintainingL. the (V.) shawi transmission of LeishmaniaZCL [1] (Figure Sloth, Primate 1). Leishmania species may Brazil infect a distinct mammalianL. host, (V.) nai yet,ffi in the northeastZCL region of Brazil, Armadillo a mosaic of different Brazil,sylvatic French and Guiana synanthropic Americas (New World) L. (V.) lainsoni ZCL Rodent South America rodents appearL. (V.) lindenbergi to be reservoirs ZCLof L. (V.) braziliensis Unknown [12]. Events such as deforestation Brazil due to L. (V.) peruviana ZCL, MCL Dog, Opossum, Rodent Peru urbanizationL. (M.) martiniquensiscan create new breedingCL habitats for Unknown vectors, which can lead French to Guiana spillovers across ecosystemEndotrypanum boundaries colombiensis [13,14]. WiZCLth over 60% of human Sloth infectious diseases Colombia, Venezuela, being Panamazoonotic [15], recognizingACL, anthroponotic the interdependence cutaneous leishmaniasis; and connections AVL, anthroponoticbetween humans, visceral animals, leishmaniasis; and the CL, environment cutaneous thatleishmaniasis; the hosts and DL, vectors disseminated inhabit cutaneous is indisputably leishmaniasis; essential. DCL, di Hence,ffuse (anergic) adopting cutaneous a ‘One leishmaniasis; Health’ approach MCL, mucocutaneous leishmaniasis; ML, mucosal leishmaniasis; PKDL, post-kala-azar dermal leishmaniasis; VL, visceral becomesleishmaniasis; imperative ZCL, zoonotic to control cutaneous leishmaniases. leishmaniasis; ZVL, zoonotic visceral leishmaniasis. Pathogens 2020, 9, 809 3 of 24 Leishmaniases present a broad spectrum of clinical manifestations, ranging from self-healing localized or multiple cutaneous lesions to mucosal lesions and potentially fatal visceral forms. These different forms are often associated with a particular species or subgenus, nonetheless, they are not unique to a species [10]. In most cases, cutaneous