Distribution of Lutzomyia ayacuchensis, the vector of Andean-type cutaneous leishmaniasis, at different altitudes on the Andean slope of Ecuador
Graphical abstract
Introduction
Leishmaniasis is a vector-borne parasitic disease caused by an obligate intracellular protozoan of the genus Leishmania. The disease is one of the most neglected diseases worldwide, having strong and complex associations with poverty, and it affects at least 12 million people (Alvar et al., 2012). Approximately 20 species of Leishmania are reported to be pathogenic to humans, and the parasites produce a wide range of clinical infections in both humans and vertebrate animals as zoonoses. In humans, the disease occurs in three distinct manifestations, cutaneous, mucocutaneous and visceral forms, and these clinical forms are largely associated with the Leishmania species responsible. The parasites are transmitted by female sand flies of the genus Phlebotomus in the Old World and Lutzomyia in the New World. At present, approximately 800 sand fly species have been recorded; however, less than 10% of them transmit each particular Leishmania species (Munstermann, 2004, Bates, 2007, Kato et al., 2010). Therefore, investigations on the prevalent parasite and vector species at given endemic areas is important for risk assessment and appropriate treatment of the disease.
Since 1982, we have been conducting epidemiological studies in the New World, especially in Ecuador. In this country, transmission of cutaneous and mucocutaneous leishmaniases occurs in rural populations living in bilateral regions of the Andes Mountains from the lowlands to the highlands up to an elevation of 2500 m. The disease is widely spread in most provinces and is a considerable public health problem in Ecuador (Gomez and Hashiguchi, 1991). In the endemic areas, however, adequate epidemiological studies have not been done on a community basis, and no control measures have been applied to reduce or interrupt the transmission of the disease.
During our research activities, we have discovered a form of the disease in people living on the Andean plateau/valleys; the disease form is very similar to ‘Peruvian uta’ but the causative agent and vector are completely different (Takaoka et al., 1990, Hashiguchi et al., 1991, Gomez and Hashiguchi, 1991, Kato et al., 2005, Kato et al., 2008a). These findings have increased the known distribution of Andean leishmaniasis in the Andes regions. Until very recently, the only form of leishmaniasis in the Andes was thought to be ‘Peruvian uta’ caused by Leishmania (Viannia) peruviana. In Peru, the causative agent of the disease is L. (V.) peruviana and the suspected vectors are Lutzomyia (Lu.) verrucarum, Lu. peruensis, and Lu. ayacuchensis (Davies et al., 1993, Perez et al., 1991, Perez et al., 2007, Caceres et al., 2004, Kato et al., 2008a, Kato et al., 2011). In Ecuador, on the other hand, two species of the genus Leishmania, Leishmania (Leishmania) mexicana and L. (L.) major-like, seemed to be involved in Andean highland leishmaniasis (Hashiguchi et al., 1991). The only incriminated vector species is Lu. ayacuchensis, and the ratio infected by L. (L.) mexicana is high (1–8%) in highland areas, which is uncommon in most endemic areas of Ecuador (Takaoka et al., 1990, Gomez and Hashiguchi, 1991, Hashiguchi et al., 1991, Kato et al., 2005, Kato et al., 2008a). Therefore, distribution of the vector species is a major risk factor for the endemicity of leishmaniasis. In the present study, the vertical distribution of Lu. ayacuchensis and other man-biting sand fly species were surveyed at different altitudes (300–2500 m above sea level (a.s.l.)) of the Andean slope, and the genetic divergence of Lu. ayacuchensis was analyzed by targeting the cytochrome oxidase I gene.
Section snippets
Study sites
The main study sites are located in Chimborazo Province on the south east of Ecuador, and located on the Andean slope, ranging from 300 m to 2500 m a.s.l. along a railway, which was recently reconstructed and restarted after an approximately 20-year break (Fig. 1). The study area Canton Alausi has a population of ca. 4000 and lies at 2300–2500 m a.s.l. (Fig. 1). A small village, Chanchan, has only 37 villagers in total, and Canton Huigra has a population of ca. 2000 at an altitude of 1200–1300 m
Vertical distribution of sand flies along the Andean slope
Eight man-biting species of the genus Lutzomyia, Lu. ayacuchensis, Lu. maranonensis, Lu. robusta, Lu. hartmanni, Lu. gomezi, Lu. trapidoi, and Lu. panamensis were identified at different altitudes/sites of the present study areas (Table 1 and Fig. 2). The vector species of Andean-type cutaneous leishmaniasis, Lu. ayacuchensis, was identified at altitude of 650 m and higher areas, and a higher distribution ratio of the species was observed at higher altitudes; from 23.4% in Ochoa (650 m a.s.l.) to
Discussion
In the present study, sand fly species were surveyed at different altitudes of an Andean slope, and vertical distribution of Lu. ayacuchensis, the vector of L. (L.) mexicana in the Ecuadorian Andes, was elucidated. The distribution pattern was similar to that of 20 years ago. A haplotype analysis of Lu. ayacuchensis targeting the COI gene showed no apparent difference among populations at different localities where the infection ratio of the sand flies by L. (L.) mexicana is markedly different.
Funding
This study was financially supported by the Ministry of Education, Culture and Sports, Science and Technology (MEXT) of Japan (Grant nos. 23256002 and 25257501), and the Prometeo Project of the Secretaria Nacional de Educacion Superior, Ciencia, Tecnologia e Innovacion (SENESCYT), Ecuador.
Conflict of interest
The authors have no conflicts of interest to declare.
Acknowledgements
We are indebted to Flavio-Valeriano Zambrano C. (Servicio Nacional de Erradicacion de la Malaria, Guayaquil, Ecuador), Kazue Hashiguchi (Centro de Biomedicina, Universidad Central del Ecuador, Quito, Ecuador), and Roberto Sud A. (Ministerio de Salud Publica y Asistencia Social, Guayaquil, Ecuador) for their technical assistance during the field phase of the present study.
References (23)
Transmission of Leishmania metacyclic promastigotes by phlebotomine sand flies
Int. J. Parasitol.
(2007)- et al.
Lutzomyia verrucarum can transmit Leishmania peruviana, the aetiological agent of Andean cutaneous leishmaniasis
Trans. R. Soc. Trop. Med. Hyg.
(1993) - et al.
First human cases of Leishmania (Viannia) naiffi infection in Ecuador and identification of its suspected vector species
Acta Trop.
(2013) - et al.
Leishmania (Viannia) peruviana isolated from the sandfly Lutzomyia peruensis (Diptera: Psychodidae) and a sentinel hamster in the Huayllacallán Valley, Ancash, Peru
Trans. R. Soc. Trop. Med. Hyg.
(1991) - et al.
Leishmaniasis worldwide and global estimates of its incidence
PLOS ONE
(2012) - et al.
Median-joining networks for inferring intraspecific phylogenies
Mol. Biol. Evol.
(1999) - et al.
Epidemiology of Andean cutaneous leishmaniasis: incrimination of Lutzomyia ayacuchensis (Diptera: Psychodidae) as a vector of Leishmania in geographically isolated, upland valleys of Peru
Am. J. Trop. Med. Hyg.
(2004) - et al.
DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates
Mol. Mar. Biol. Biotechnol.
(1994) - et al.
Monthly variation in natural infection of the sandfly Lutzomyia ayacuchensis with Leishmania mexicana in an endemic focus in the Ecuadorian Andes
Ann. Trop. Med. Parasitol.
(1991) - et al.
Andean leishmaniasis in Ecuador caused by infection with Leishmania mexicana and L. major-like parasites
Am. J. Trop. Med. Hyg.
(1991)
Molecular mass screening to incriminate sand fly vectors of Andean-type cutaneous leishmaniasis in Ecuador and Peru
Am. J. Trop. Med. Hyg.
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Anthropophilic phlebotomine sand fly Lutzomyia species and search for the natural Leishmania infections in an area endemic for cutaneous leishmaniasis in Ecuador
2020, Acta TropicaCitation Excerpt :tortura, and Lu. gomezi, were incriminated as probable vectors of the Leishmania parasites (Takaoka et al., 1990; Kato et al., 2005, 2008, 2013; Gomez et al., 2014a,b; Hashiguchi et al., 2017, 2018). Regarding the causative Leishmania parasites, on the other hand, there exist eight species; L. (V.) guyanensis/panamensis, L. (V.) braziliensis, L. (V.) naiffi, L. (V.) lainsoni, L. (L.) mexicana, L. (L.) amazonensis, L. (L.) major-like reported (Mimori et al., 1989; Armijos et al., 1990; Hashiguchi et al., 2017; Kato et al., 2016, 2019).
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2018, Acta TropicaCitation Excerpt :In Ecuador, the anthropophilic sand fly Lu. ayacuchensis, vector of the L. (L.) mexicana parasite, was reported from restricted areas in Ecuador, the provinces of Azuay and Chimborazo (Hashiguchi et al., 1991, 2017; Mimori et al., 2001; Kato et al., 2007, 2015; Gomez et al., 2014a,b). In the Ecuadorian Andes regions, the altitudinal distribution and species composition were investigated at six different localities with 300 m − 2300 m a.s.l., along the railways and the river Chanchan in Chimborazo Province (Gomez et al., 1994, 2014a).