Most cited article - PubMed ID 30740304
Host competence of African rodents Arvicanthis neumanni, A. niloticus and Mastomys natalensis for Leishmania major
BACKGROUND: Several new species of Leishmania have recently emerged in Europe, probably as the result of global changes and increased human migration from endemic areas. In this study, we tested whether two sand fly species, the Western Mediterranean Phlebotomus perniciosus and the Eastern Mediterranean P. tobbi, are competent vectors of L. donovani, L. major and L. martiniquensis. METHODOLOGY/PRINCIPAL FINDINGS: Sand flies were infected through the chick skin membrane using Leishmania species and strains of various geographical origins. Leishmania infections were evaluated by light microscopy and qPCR, and the representation of morphological forms was assessed from Giemsa-stained gut smears. Neither P. perniciosus nor P. tobbi supported the development of L. martiniquensis, but L. major and L. donovani in both species survived defecation of blood meal remnants, colonized the stomodeal valve and produced metacyclic stages. The results with L donovani have shown that infection rates in sand flies can be strain-specific; therefore, to determine vector competence or refractoriness, it is optimal to test at least two strains of Leishmania. CONCLUSIONS, SIGNIFICANCE: Both sand fly species tested are potential vectors of L. donovani and L. major in Mediterranean area. However, further studies will be needed to identify European vectors of L. martiniquensis and to test the ability of other European sand fly species to transmit L. major, L. donovani, L. tropica and L. infantum.
- MeSH
- Insect Vectors * parasitology physiology MeSH
- Chickens parasitology MeSH
- Leishmania * physiology classification genetics MeSH
- Leishmaniasis transmission parasitology MeSH
- Humans MeSH
- Phlebotomus * parasitology physiology MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Geographicals
- Europe MeSH
Leishmania, the dixenous trypanosomatid parasites, are the causative agents of leishmaniasis currently divided into four subgenera: Leishmania, Viannia, Sauroleishmania, and the recently described Mundinia, consisting of six species distributed sporadically all over the world infecting humans and/or animals. These parasites infect various mammalian species and also cause serious human diseases, but their reservoirs are unknown. Thus, adequate laboratory models are needed to enable proper research of Mundinia parasites. In this complex study, we compared experimental infections of five Mundinia species (L. enriettii, L. macropodum, L. chancei, L. orientalis, and four strains of L. martiniquensis) in three rodent species: BALB/c mouse, Chinese hamster (Cricetulus griseus) and steppe lemming (Lagurus lagurus). Culture-derived parasites were inoculated intradermally into the ear pinnae and progress of infection was monitored for 20 weeks, when the tissues and organs of animals were screened for the presence and quantity of Leishmania. Xenodiagnoses with Phlebotomus duboscqi were performed at weeks 5, 10, 15 and 20 post-infection to test the infectiousness of the animals throughout the experiment. BALB/c mice showed no signs of infection and were not infectious to sand flies, while Chinese hamsters and steppe lemmings proved susceptible to all five species of Mundinia tested, showing a wide spectrum of disease signs ranging from asymptomatic to visceral. Mundinia induced significantly higher infection rates in steppe lemmings compared to Chinese hamsters, and consequently steppe lemmings were more infectious to sand flies: In all groups tested, they were infectious from the 5th to the 20th week post infection. In conclusion, we identified two rodent species, Chinese hamster (Cricetulus griseus) and steppe lemming (Lagurus lagurus), as candidates for laboratory models for Mundinia allowing detailed studies of these enigmatic parasites. Furthermore, the long-term survival of all Mundinia species in steppe lemmings and their infectiousness to vectors support the hypothesis that some rodents have the potential to serve as reservoir hosts for Mundinia.
- MeSH
- Arvicolinae * parasitology MeSH
- Cricetulus MeSH
- Cricetinae MeSH
- Leishmania * classification MeSH
- Leishmaniasis * parasitology MeSH
- Disease Models, Animal * MeSH
- Mice, Inbred BALB C * MeSH
- Mice MeSH
- Animals MeSH
- Check Tag
- Cricetinae MeSH
- Mice MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Leishmaniases are neglected diseases caused by protozoans of the genus Leishmania that threaten millions of people worldwide. Cutaneous leishmaniasis (CL) caused by L. major is a typical zoonosis transmitted by phlebotomine sand flies and maintained in rodent reservoirs. The female sand fly was assumed to become infected by feeding on the skin lesion of the host, and the relative contribution of asymptomatic individuals to disease transmission was unknown. In this study, we infected 32 Meriones shawi, North African reservoirs, with a natural dose of L. major obtained from the gut of infected sand flies. Skin manifestations appeared in 90% of the animals, and xenodiagnosis with the proven vector Phlebotomus papatasi showed transmissibility in 67% of the rodents, and 45% were repeatedly infectious to sand flies. Notably, the analysis of 113 xenodiagnostic trials with 2189 sand flies showed no significant difference in the transmissibility of animals in the asymptomatic and symptomatic periods; asymptomatic animals were infectious several weeks before the appearance of skin lesions and several months after their healing. These results clearly confirm that skin lesions are not a prerequisite for vector infection in CL and that asymptomatic animals are an essential source of L. major infection. These data are important for modeling the epidemiology of CL caused by L. major.
- Keywords
- Leishmania, Meriones, Phlebotomus, asymptomatic infection, reservoir host, xenodiagnosis,
- Publication type
- Journal Article MeSH
BACKGROUND: Sergentomyia minuta (Diptera: Phlebotominae) is an abundant sand fly species in the Mediterranean basin and a proven vector of reptile parasite Leishmania (Sauroleishmania) tarentolae. Although it feeds preferentially on reptiles, blood meal analyses and detection of Leishmania (Leishmania) infantum DNA in wild-caught S. minuta suggest that occasional feeding may occur on mammals, including humans. Therefore, it is currently suspected as a potential vector of human pathogens. METHODS: A recently established S. minuta colony was allowed to feed on three reptile species (i.e. lizard Podarcis siculus and geckos Tarentola mauritanica and Hemidactylus turcicus) and three mammal species (i.e. mouse, rabbit and human). Sand fly mortality and fecundity were studied in blood-fed females, and the results were compared with Phlebotomus papatasi, vector of Leishmania (L.) major. Blood meal volumes were measured by haemoglobinometry. RESULTS: Sergentomyia minuta fed readily on three reptile species tested, neglected the mouse and the rabbit but took a blood meal on human. However, the percentage of females engorged on human volunteer was low in cage (3%) and feeding on human blood resulted in extended defecation times, higher post-feeding mortality and lower fecundity. The average volumes of blood ingested by females fed on human and gecko were 0.97 µl and 1.02 µl, respectively. Phlebotomus papatasi females readily fed on mouse, rabbit and human volunteer; a lower percentage of females (23%) took blood meal on the T. mauritanica gecko; reptilian blood increased mortality post-feeding but did not affect P. papatasi fecundity. CONCLUSIONS: Anthropophilic behaviour of S. minuta was experimentally demonstrated; although sand fly females prefer reptiles as hosts, they were attracted to the human volunteer and took a relatively high volume of blood. Their feeding times were longer than in sand fly species regularly feeding on mammals and their physiological parameters suggest that S. minuta is not adapted well for digestion of mammalian blood. Nevertheless, the ability to bite humans highlights the necessity of further studies on S. minuta vector competence to elucidate its potential role in circulation of Leishmania and phleboviruses pathogenic to humans.
- Keywords
- Feeding preferences, Leishmania, Phlebotomus, Sand flies, Sergentomyia,
- MeSH
- DNA genetics MeSH
- Lizards * MeSH
- Rabbits MeSH
- Leishmania * genetics MeSH
- Humans MeSH
- Mice MeSH
- Phlebotomus * parasitology MeSH
- Psychodidae * parasitology MeSH
- Mammals genetics MeSH
- Animals MeSH
- Check Tag
- Rabbits MeSH
- Humans MeSH
- Mice MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- DNA MeSH
The clinical manifestation of leishmaniases depends on parasite species, host genetic background, and immune response. Manifestations of human leishmaniases are highly variable, ranging from self-healing skin lesions to fatal visceral disease. The scope of standard model hosts is insufficient to mimic well the wide disease spectrum, which compels the introduction of new model animals for leishmaniasis research. In this article, we study the susceptibility of three Asian rodent species (Cricetulus griseus, Lagurus lagurus, and Phodopus sungorus) to Leishmania major and L. donovani. The external manifestation of the disease, distribution, as well as load of parasites and infectiousness to natural sand fly vectors, were compared with standard models, BALB/c mice and Mesocricetus auratus. No significant differences were found in disease outcomes in animals inoculated with sand fly- or culture-derived parasites. All Asian rodent species were highly susceptible to L. major. Phodopus sungorus showed the non-healing phenotype with the progressive growth of ulcerative lesions and massive parasite loads. Lagurus lagurus and C. griseus represented the healing phenotype, the latter with high infectiousness to vectors, mimicking best the character of natural reservoir hosts. Both, L. lagurus and C. griseus were also highly susceptible to L. donovani, having wider parasite distribution and higher parasite loads and infectiousness than standard model animals.
- Keywords
- Cricetulus griseus, Lagurus lagurus, Phlebotomus, Phodopus sungorus, cutaneous leishmaniasis, infectiousness, model animals, sand fly, visceral leishmaniasis, xenodiagnosis,
- Publication type
- Journal Article MeSH
Visceral leishmaniasis caused by Leishmania donovani is regarded as mostly anthroponotic, but a role for animal reservoir hosts in transmission has been suggested in East Africa. Field studies in this region have shown the presence of this parasite in several mammalian species, including rodents of the genera Arvicanthis and Mastomys. Further, the natural reservoirs of Leishmania (Mundinia) sp. causing human cutaneous disease in Ghana, West Africa, are unknown. This study assessed the potential role of the Sub-Saharan rodents Arvicanthis neumanni, A. niloticus and Mastomys natalensis as hosts of L. donovani and L. sp. from Ghana, based on experimental infections of animals and xenodiagnoses. The distribution and load of parasites were determined post mortem using qPCR from the blood, skin and viscera samples. The attractiveness of Arvicanthis and Mastomys to Phlebotomus orientalis was tested by pair-wise comparisons. None of the animals inoculated with L. donovani were infectious to P. orientalis females, although, in some animals, parasites were detected by PCR even 30 weeks post infection. Skin infections were characterized by low numbers of parasites while high parasite burdens were present in spleen, liver and lymph nodes only. Therefore, wild Arvicanthis and Mastomys found infected with L. donovani, should be considered parasite sinks rather than parasite reservoirs. This is indirectly supported also by results of host choice experiments with P. orientalis in which females preferred humans over both Arvicanthis and Mastomys, and their feeding rates on rodents ranged from 1.4 to 5.8% only. Therefore, the involvement of these rodents in transmission of L. donovani by P. orientalis is very unlikely. Similarly, poor survival of Leishmania parasites in the studied rodents and negative results of xenodiagnostic experiments do not support the involvement of Arvicanthis and Mastomys spp. in the transmission cycle of L. sp. from Ghana.
- Keywords
- Grass rats, Multimammate mice, Mundinia, Reservoir hosts, Visceral leishmaniasis, Xenodiagnosis,
- Publication type
- Journal Article MeSH