VECTOR BORNE PARASITIC AND VIRAL DISEASES – Module 1

Leishmaniases: Reservoir hosts

Carla Maia DVM, MSc, PhD, DipEVPC, EBVS® European Veterinary Specialist in Parasitology Global Health and Tropical Medicine. Medical Parasitology Unit. Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa [email protected]

C. Maia

C. Maia The aim of this presentation is to learn:

 Definition of a reservoir host of Leishmania sp.

 Identify the proven (and some of the suspected) reservoir hosts of visceral and cutaneous leishmaniases in the Old and New Worlds

Leishmaniases

• Worldwide phlebotomine sand fly-borne diseases

caused by protozoa belonging to genus Leishmania

• 21 Leishmania spp. pathogenic for humans

• Diverse clinical manifestations:

(In: http://www.parasitologie.univ-montp1.fr/leishmania.htm)

 Visceral leishmaniasis (VL) caused by parasites of the L. donovani J. Oliveira

complex (L. donovani Old World, L. infantum Old + New Worlds)

 Cutaneous (CL) or mucocutaneous (MCL) leishmaniasis caused by

Leishmania spp.

• Endemic in >100 countries; 1 billion people at risk

• Incidence of 0.2 to 0.4 million VL cases and 0.7 to 1.3 million CL cases L. Varandas Reservoir host of leishmaniases = a in which Leishmania survives persistently in a way that it may serve as a source of parasites to the vectors

Leishmaniases can be grouped into two broad epidemiological categories according to the source of human infection:

 Zoonotic leishmaniases → reservoir hosts are wild or domestic and humans play a

role of an accidental host

 Anthroponotic leishmaniases → man is the sole reservoir host and source of vector’s infection A “good” reservoir host should:

 Be susceptible to the parasites

 Live in close contact with man (or any other reservoir host)

 Be a good source of parasites to the vectors  Provide a significant food source for the vectors and both should rest and breed in the same habitat

 Infection should present a chronic evolution allowing the to survive at least until the next transmission season

 Leishmania parasites identified in reservoir hosts biochemically and genetically the same as those in

humans Be aware that:

 The mere presence of the infection in a particular mammal

species, even in large numbers Does not indicate that it is a reservoir host  The mere detection of Leishmania DNA in the tissues of a

particular mammal species

In order to incriminate a reservoir host → demonstration that the parasite population depends on that particular mammal for its long-term maintenance When more than one host species can be infected, they can be divided on epidemiological grounds:

 Primary reservoir host → responsible for maintaining the parasite indefinitely in nature. Infection is

normally without clinical signs

 Secondary (or minor) reservoir host → can transmit infection but cannot maintain parasite

transmission in the absence of the primary host(s)

 Accidental (or incidental) host → can be infected but has no role in the maintenance of the

ecological system Anthroponosis Anthroponotic Leishmaniases

Humans are reservoir hosts in two forms of the disease:

 VL caused by L. donovani in Indian subcontinent (Bangladesh, and Nepal) and East Africa

(Djibouti, Ethiopia, Eritrea, Kenya, Somalia, South Sudan, Sudan and Uganda)

 CL caused by L. tropica in semi-arid subtropical regions from south-east Turkey to north-west of India

Small foci: Arabia, Ethiopia, Greece, Namibia, North Africa (Algeria, Egypt, Morocco and Tunisia) and Central Asia Boelaert & Sundar, 2017  Foci with few/sporadic cases, disease known/suspected to be zoonotic:

Rock hyraxes (Procavia North African gundi (Ctenodactylus

capensis) in Israel gundi) in the Maghreb

https://en.wikipedia.org/wiki/Rock_hyrax https://en.wikipedia.org/wiki/Comm on_gundi Zoonotic Visceral Leishmaniasis

L. infantum (syn. of L. chagasi) in Central and South America, the Mediterranean basin, Middle East and

Asia

Primary domestic reservoir hosts: Dogs (Canis lupus familiaris)

C. Maia C. Maia C. Maia Secondary reservoir hosts → Transmission of infection confirmed by xenodiagnoses: black rats, hares and wild rabbits ?

Zoonotic Visceral Leishmaniasis

Suggested sylvatic reservoir hosts : Wild carnivores (i.e. foxes (Vulpes spp. and Cerdocyon thous), jackals (Canis aureus), wolves (Canis lupus) and raccoon dogs (Nyctereutes procyonoides)) → no strong evidence as an important source of infection → infectiousness to the vectors to be confirmed ?

 Naturally susceptible to infection by L. infantum, normally without development of clinical signs

(when present usually cutaneous; systemic involvement also recorded)

 Blood source for some Leishmania vectors

 Present parasites in an available way to infect the vector Maia et al. 2015  Among the most popular pets, present in peri/domestic transmission cycles occur

 Parasites isolated from infected cats biochemically and genetically identical to the ones obtained

from humans and dogs with leishmaniases

 Epidemiological importance in leishmaniasis poorly understood

https://www.writelikenooneswatching.com/2014/02/cats-and- children.html/ Leishmania (Mundinia) martiniquensis Zoonosis?

 Previously known as “Leishmania siamensis” (nomen nudum)

Sporadic autochthonous equine and bovine CL has been reported in Germany, Switzerland and in the USA

→ wide geographical distribution

 Human cases of VL and CL with/out other co-immunosupressive states in Thailand and Myanmar

 Zoonotic potential has been suggested → parasite DNA in liver and spleen samples of black rats

collected in an area where VL cases have been reported Zoonotic Cutaneous Leishmaniases – Old World

L. major from India through Central Asia, the Middle East, to North and West Africa

Reservoir hosts: species

(Rhombomys opimus) in central Asia, northern Afghanistan and Iran

( hurrianae) in India

• Fat sand-rat (Psammomyus obesus) and Sundevall's jird (Meriones crassus) in northern Africa and

Middle East; Shaw's jird (Meriones shawi) in Morocco and Tunisia

(Meriones libycus) in the Arabian peninsula and central Asia

• Short-tailed bandicoot rat (Nesokia indica) in Iran

• Arvicanthis, Tatera, Mastomys or Xerus spp. in sub-Saharan Africa

• Voles (Microtus tristrami and Microtus guentheri) in Israel Zoonotic Cutaneous Leishmaniases – Old World Boelaert & Sundar, 2017

L. aethiopica highlands of East Africa (Ethiopia, Kenya and Uganda)

Reservoir hosts: hyraxes (Procavia capensis and Heterohyrax brucei)

L. infantum throughout the Mediterranean Basin C. Maia

Reservoir hosts: dogs https://en.wikipedia.org/wiki/Rock_hyrax

L. Campino Zoonotic Cutaneous Leishmaniases – New World

L. amazonensis (syn. of L. garnhami) in Argentina, Bolivia, Brazil, Colombia,

Costa Rica, Ecuador, French Guyana, Peru, Suriname and Venezuela

Reservoir hosts: ground-dwelling

Suspected/putative secondary reservoir hosts: several wild

Hairy-tailed bolo mouse (Necromys lasiurus)

https://en.wikipedia.org/wiki/Hairy-tailed_bolo_mouse

Boelaert & Sundar, 2017 Zoonotic Cutaneous and Mucocutaneous Leishmaniases – New World

L. braziliensis countries of Central and South America

Sylvatic reservoir hosts: bats, edentates, marsupials, wild rodents

Tate’s woolly mouse opossum (Marmosa Flat-faced fruit-eating bat (Artibeus paraguayana) planirostris)

https://www.who.int/leishmaniasis/mucocutaneous_leishmaniasis/en/ Common opossum (Didelphis marsupialis)

https://www.pinterest.fr/pin/346917977525671665

https://www.sarem.org.ar/en/conservation-committee/artibeus-planirostris-en/ https://en.wikipedia.org/wiki/Common_opossum

Suspected domestic reservoir hosts (rural areas): equids, dogs and cats ?

Suspected reservoir hosts (outbreaks): humans Zoonotic Cutaneous Leishmaniases – New World

L. colombiensis in Colombia, Panama and Venezuela

Reservoir host: Hoffmann's two-toed sloth (Choloepus hoffmanni)

https://en.wikipedia.org/wiki/Hoffmann%27s_two-toed_sloth

L. guyanensis in Argentina, Bolivia, Brazil (some states), Colombia, Ecuador, French Guiana, Guyana,

Peru, Suriname and Venezuela

Reservoir host: Linnaeus's two-toed sloth (Choloepus didactylus)

https://en.wikipedia.org/wiki/Linnaeus%27s_two-toed_sloth Zoonotic Cutaneous Leishmaniases – New World

L. lainsoni in Bolivia (subtropical areas), Brazil (some states), Ecuador,

French Guiana, Peru (tropical areas) and Suriname

Suspected reservoir host: Lowland paca (Cuniculus paca)

By Marcos Antonio Vieira de Freitas - Own work, CC BY-SA 4.0, https://commons.wikimedia.org/w/index.php?curid=60064430 L. mexicana (syn. of L. pifanoi) in Belize, Colombia, Costa Rica, Ecuador, Guatemala, Mexico, southern USA and Venezuela

Reservoir hosts: Ground-dwelling rodents (Heteromys, Neotoma, Nyctomys, Ototylomys and Sigmodon Big-eared climbing rat (Ototylomys phyllotis) spp.)

Boelaert & Sundar, 2017 https://www.inaturalist.org/taxa/45025-Ototylomys-phyllotis

Zoonotic Cutaneous Leishmaniases – New World

L. naiffi in Brazil (Rondônia state), Ecuador, Suriname and French Guiana

banded_armadillo

- Nine

Reservoir host: Nine-banded armadillo (Dasypus novemcinctus) /wiki/ https://en.wikipedia.org

L. panamensis in Colombia, Costa Rica, Ecuador (Pacific littoral), Guatemala, Honduras, Nicaragua and

South American coati (Nasua Panama nasua)

Reservoir hosts: sloths Saguinus Saguinus

Suspected reservoir hosts: coatis, monkeys, rodents

https://pt.wikipedia.org/wiki/Quati-de-cauda-anelada )

Suspected reservoir hosts (outbreaks): humans

Geoffroy’s tamarin( Geoffroy’s geoffroyi

https://pt.wikipedia.org/wiki/Saguinus_geoffroyi ? Zoonotic Cutaneous Leishmaniases – New World

L. peruviana in Peruvian Andes ? Suspected sylvatic reservoir hosts: marsupials and rodents

Suspected peri/domestic reservoir host: dog

L. shawi in Brazil (Atlantic rainforest of Pará State)

Sylvatic reservoir hosts: coatis, monkeys and sloths

L. venezuelensis in Venezuela ?

Suspected domestic reservoir host: cat Take home message:

 Reservoir host of leishmaniases = a mammal in which Leishmania survives persistently in a way that it

may serve as a source of parasites to the vectors

. Primary reservoir host → responsible for maintaining the parasite indefinitely in nature

. Secondary reservoir host → can transmit infection but cannot maintain parasite transmission in the

absence of the primary host(s)

 The mere presence of the infection in a particular mammal species

 The mere detection of Leishmania DNA in the tissues of a particular mammal species

 Does not indicate that this mammal is a reservoir host Take home message:

 Leishmania spp. have been found in a variety of wild and domestic animals but their role in the life

cycle of the parasite is unknown

 To determine the role of a suspected reservoir host in the maintenance and transmission of Leishmania

spp. pathogenic to humans:

 Isolation and genetical and biochemical characterization of the parasites from samples

accessible to the vectors

 Evaluation of their infectiousness to vectors (i.e. xenodiagnosis)

→ Other factors: food sources, longevity, movement and migration activities Selected references

. Alvar J et al. (2012) Leishmaniasis worldwide and global estimates of its incidence. PLoS ONE 7(5):e35671

. Aoun K, Bouratbine A (2014) Cutaneous leishmaniasis in North Africa: a review. Parasite 21:14

. Ashford RW (2000) The leishmaniases as emerging and reemerging zoonoses. Int J Parasitol 30(12–13):1269-81

. Gramiccia M, Gradoni L (2005) The current status of zoonotic leishmaniases and approaches to disease control. Int J Parasitol

35(11-12):1169-80

. Maia C, Dantas-Torres F, Campino L (2018) Parasite Biology: The Reservoir Hosts. In: The Leishmaniases: Old Neglected

Tropical Diseases. Ed: F. Bruschi, L. Gradoni. Springer International Publishing. Viena. Austria, pp 79-106

. Quinnell R, Courtenay O (2009) Transmission, reservoir hosts and control of zoonotic visceral leishmaniasis. Parasitology

136(14):1915-34

. WHO (2010) Control of the Leishmaniasis: Report of the WHO Expert Committee on the Control of Leishmaniases, World

Health Organization. http://www.who.int/neglected_diseases/resources/who_trs_949/en