Insecticide-impregnated netting as a potential surface treatment: an alternative to insecticide spraying for control of the leishmaniasis vector Lutzomyia longipalpis (Diptera: Psychodidae)?

Abstract Background: The sand fly, Lutzomyia longipalpis, is the main vector of Leishmania infantum in Brazil. A previous laboratory study showed that covering surfaces with insecticide-impregnated netting may provide an alternative method for killing sand flies. Synthetic male Lu. longipalpis sex/aggregation pheromone co-located with micro-encapsulated l-cyhalothrin demonstrated the potential of “lure-and-kill” to significantly reduce canine infection and sand fly densities. In this study we were interested to determine if insecticide impregnated netting could replace sprayed insecticide for Lu. longipalpis control.Methods: We placed synthetic pheromone in experimental and real chicken sheds treated with a 1m2 surface of either sprayed insecticide or insecticide-impregnated netting. Two experiments in experimental chicken sheds were carried out to determine the effect of the insecticide treatments on Lu. longipalpis over 1-week and 16-week periods. We counted the number of Lu. longipalpis collected overnight and dead at 24 hours. Two longitudinal intervention studies were carried in real chicken sheds and compared the numbers of Lu. longipalpis (collected and dead at 24h) before adding the intervention (either the netting or sprayed insecticide treatments) with the numbers collected 24h after the intervention. Results: In the first experiment all flies caught in the spray treated experimental chicken sheds were dead at 24 hours and in netting treated sheds 97% of females and 88% of males were dead at 24 hours (257 vs 225, Wilcoxon Signed Ranks Test P=0.043). The netting and spray treated traps were equally effective at killing both female and male Lu. longipalpis over the first 8-weeks however after 16-weeks both treatments killed a significantly lower proportion of females (64%vs 96%; P=0.000) and males 89%vs 100%; P=0.000) compared to the beginning. In the first of the longitudinal studies in real chicken sheds only the netting intervention significantly increased the proportion of females dead after 24h (60%vs81%; P=0.042). The subsequent study showed that both netting and spraying treatments had similarly significant impacts on the proportion of females dead after 24h (netting: 60%vs80%: P=0.0194 and spraying: 43%vs72%: P=0.0004).Conclusions: The netting and spray insecticide interventions (with synthetic sex/aggregation pheromone) have similar impacts on the Lu. longipalpis population.

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Odour of domestic dogs infected with Leishmania infantum is attractive to female but not male sand flies: Evidence for parasite manipulation

PLoS Pathogens ◽

10.1371/journal.ppat.1009354 ◽

2021 ◽

Vol 17 (3) ◽

pp. e1009354

Author(s):

Monica E. Staniek ◽

James G. C. Hamilton

Keyword(s):

Leishmania Infantum ◽

Etiologic Agent ◽

Human Infection ◽

T Test ◽

Sand Fly ◽

Lutzomyia Longipalpis ◽

Sand Flies ◽

Control Female ◽

Behavioural Experiments ◽

Paired T Test

Globally visceral leishmaniasis (VL) causes thousands of human deaths every year. In South America, the etiologic agent, Leishmania infantum, is transmitted from an infected canine reservoir to human hosts by the bite of the sand fly vector; predominantly Lutzomyia longipalpis. Previous evidence from model rodent systems have suggested that the odour of infected hosts is altered by the parasite making them more attractive to the vector leading to an increased biting rate and improved transmission prospects for the pathogen. However, there has been no assessment of the effect of Le infantum infection on the attractiveness of dogs, which are the natural reservoirs for human infection. Hair collected from infected and uninfected dogs residing in a VL endemic city in Brazil was entrained to collect the volatile chemical odours present in the headspace. Female and male Lu. longipalpis sand flies were offered a choice of odour entrained from infected and uninfected dogs in a series of behavioural experiments. Odour of uninfected dogs was equally attractive to male or female Lu. longipalpis when compared to a solvent control. Female Lu. longipalpis were significantly more attracted to infected dog odour than uninfected dog odour in all 15 experimental replicates (average 45.7±0.87 females attracted to infected odour; 23.9±0.82 to uninfected odour; paired T-test, P = 0.000). Male Lu. longipalpis did not significantly prefer either infected or uninfected odour (average 36.1±0.4 males to infected odour; 35.7±0.6 to uninfected odour; paired T-test, P = 0.722). A significantly greater proportion of females chose the infected dog odour compared to the males (paired T-test, P = 0.000). The results showed that the odour of dogs infected with Le. infantum was significantly more attractive to blood-seeking female sand flies than it was to male sand flies. This is strong evidence for parasite manipulation of the host odour in a natural transmission system and indicates that infected dogs may have a disproportionate significance in maintaining infection in the canine and human population.

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Leishmania infantum Infection Modulates the Jak-STAT Pathway in Lutzomyia longipalpis LL5 Embryonic Cells and Adult Females, and Affects Parasite Growth in the Sand Fly

Frontiers in Tropical Diseases ◽

10.3389/fitd.2021.747820 ◽

2021 ◽

Vol 2 ◽

Author(s):

Erich Loza Telleria ◽

Daisy Aline Azevedo-Brito ◽

Barbora Kykalová ◽

Bruno Tinoco-Nunes ◽

André Nóbrega Pitaluga ◽

...

Keyword(s):

Post Infection ◽

Leishmania Infantum ◽

Janus Kinase ◽

Sand Fly ◽

Lutzomyia Longipalpis ◽

Sand Flies ◽

Embryonic Cells ◽

Adult Females ◽

Parasite Survival ◽

Stat Pathway

Phlebotomine sand flies (Diptera, Psychodidae) belonging to the Lutzomyia genus transmit zoonoses in the New World. Lutzomyia longipalpis is the main vector of Leishmania infantum, which is the causative agent of visceral leishmaniasis in Brazil. To identify key molecular aspects involved in the interaction between vector and pathogens and contribute to developing disease transmission controls, we investigated the sand fly innate immunity mediated by the Janus kinase/signal transducer and activator of transcription (Jak-STAT) pathway in response to L. infantum infection. We used two study models: L. longipalpis LL5 embryonic cells co-cultured with L. infantum and sand fly females artificially infected with the parasite. We used qPCR to follow the L. longipalpis gene expression of molecules involved in the Jak-STAT pathway. Also, we modulated the Jak-STAT mediated immune response to understand its role in Leishmania parasite infection. For that, we used RNAi to silence the pathway regulators, protein inhibitor of activated STATs (PIAS) in LL5 cells, and STAT in adult females. In addition, the pathway suppression effect on parasite development within the vector was assessed by light microscopy in late-phase infection. The silencing of the repressor PIAS in LL5 cells led to a moderate increase in a protein tyrosine phosphatase 61F (PTP61F) expression. It suggests a compensatory regulation between these two repressors. L. infantum co-culture with LL5 cells upregulated repressors PIAS, suppressor of cytokine signaling (SOCS), and PTP61F. It also downmodulated virus-induced RNA-1 (VIR-1), a pathway effector, indicating that the parasite could repress the Jak-STAT pathway in LL5 cells. In Leishmania-infected L. longipalpis females, STAT and the antimicrobial peptide attacin were downregulated on the third day post-infection, suggesting a correlation that favors the parasite survival at the end of blood digestion in the sand fly. The antibiotic treatment of infected females showed that the reduction of gut bacteria had little effect on the Jak-STAT pathway regulation. STAT gene silencing mediated by RNAi reduced the expression of inducible nitric oxide synthase (iNOS) and favored Leishmania growth in sand flies on the first day post-infection. These results indicate that STAT participated in the iNOS regulation with subsequent effect on parasite survival.

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Leishmania infantum xenodiagnosis from vertically infected dogs reveals significant skin tropism

PLoS Neglected Tropical Diseases ◽

10.1371/journal.pntd.0009366 ◽

2021 ◽

Vol 15 (10) ◽

pp. e0009366

Author(s):

Breanna M. Scorza ◽

Kurayi G. Mahachi ◽

Arin C. Cox ◽

Angela J. Toepp ◽

Adam Leal-Lima ◽

...

Keyword(s):

Leishmania Infantum ◽

Severe Disease ◽

Clinical Status ◽

Parasite Burden ◽

Parasite Load ◽

Sand Fly ◽

Lutzomyia Longipalpis ◽

Sand Flies ◽

Feeding Site ◽

Transmission Potential

Background Dogs are the primary reservoir for human visceral leishmaniasis due to Leishmania infantum. Phlebotomine sand flies maintain zoonotic transmission of parasites between dogs and humans. A subset of dogs is infected transplacentally during gestation, but at what stage of the clinical spectrum vertically infected dogs contribute to the infected sand fly pool is unknown. Methodology/Principal findings We examined infectiousness of dogs vertically infected with L. infantum from multiple clinical states to the vector Lutzomyia longipalpis using xenodiagnosis and found that vertically infected dogs were infectious to sand flies at differing rates. Dogs with mild to moderate disease showed significantly higher transmission to the vector than dogs with subclinical or severe disease. We documented a substantial parasite burden in the skin of vertically infected dogs by RT-qPCR, despite these dogs not having received intradermal parasites via sand flies. There was a highly significant correlation between skin parasite burden at the feeding site and sand fly parasite uptake. This suggests dogs with high skin parasite burden contribute the most to the infected sand fly pool. Although skin parasite load and parasitemia correlated with one another, the average parasite number detected in skin was significantly higher compared to blood in matched subjects. Thus, dermal resident parasites were infectious to sand flies from dogs without detectable parasitemia. Conclusions/Significance Together, our data implicate skin parasite burden and earlier clinical status as stronger indicators of outward transmission potential than blood parasite burden. Our studies of a population of dogs without vector transmission highlights the need to consider canine vertical transmission in surveillance and prevention strategies.

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Phlebotomine sand flies and canine infection in areas of human visceral leishmaniasis, Cuiabá, Mato Grosso

Revista Brasileira de Parasitologia Veterinária ◽

10.1590/s1984-29612011000300010 ◽

2011 ◽

Vol 20 (3) ◽

pp. 228-234 ◽

Cited By ~ 7

Author(s):

Gustavo Leandro da Cruz Mestre ◽

Ana Lúcia Maria Ribeiro ◽

Rosina Djunko Miyazaki ◽

Jorge Senatore Vargas Rodrigues ◽

Arleana do Bom Parto Ferreira de Almeida ◽

...

Keyword(s):

Visceral Leishmaniasis ◽

Urban Areas ◽

Sand Fly ◽

Lutzomyia Longipalpis ◽

Sand Flies ◽

Mato Grosso ◽

Human Visceral Leishmaniasis ◽

Life Threatening ◽

Canine Infection ◽

The City

Visceral leishmaniasis is a systemic infectious disease that can cause to a severe, potentially life-threatening chronic condition in humans. Risk factors for infection in urban areas have been associated with poor living conditions, the presence of sand fly vectors and infected pets. This study aimed to describe sand fly and canine infection in the neighborhoods of human visceral leishmaniasis occurrence in the city of Cuiabá, Mato Grosso State, central-western Brazil, reported between January 2005 and December 2006. A total of 1,909 sand flies were collected. They were predominantly males and the most frequent species were Lutzomyia cruzi (81.25%), Lutzomyia whitmani (13.88%) and Lutzomyia longipalpis (2.62%). The sand fly density was not significantly correlated with the variation of environmental factors. The prevalence of canine visceral leishmaniasis in the neighborhoods studied was 26.82% and it was found that areas with high density of vectors coincided with areas of high prevalence of dogs and those with the highest rates of human cases. The study of vectors and other potential hosts are essential for a good understanding of visceral leishmaniasis and the related public health concerns, aiming at the prevention and control of leishmaniasis in the city of Cuiabá, Mato Grosso State.

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Binding of Leishmania infantum Lipophosphoglycan to the Midgut Is Not Sufficient To Define Vector Competence in Lutzomyia longipalpis Sand Flies

mSphere ◽

10.1128/msphere.00594-20 ◽

2020 ◽

Vol 5 (5) ◽

Author(s):

Iliano V. Coutinho-Abreu ◽

James Oristian ◽

Waldionê de Castro ◽

Timothy R. Wilson ◽

Claudio Meneses ◽

...

Keyword(s):

Leishmania Infantum ◽

Vector Competence ◽

Sand Fly ◽

Parasite Development ◽

Lutzomyia Longipalpis ◽

Sand Flies ◽

Content Type ◽

Survival And Development ◽

Blood Meal Digestion ◽

Insect Gut

It is well established that the presence of LPG is sufficient to define the vector competence of restrictive sand fly vectors with respect to Leishmania parasites. However, the permissiveness of other sand flies with respect to multiple Leishmania species suggests that other factors might define vector competence for these vectors. In this study, we investigated the underpinnings of Leishmania infantum survival and development in its natural vector, Lutzomyia longipalpis. We found that LPG-mediated midgut binding persists in late-stage parasites. This observation is of relevance for the understanding of vector-parasite molecular interactions and suggests that only a subset of infective metacyclic-stage parasites (metacyclics) lose their ability to attach to the midgut, with implications for parasite transmission dynamics. However, our data also demonstrate that LPG is not a determining factor in Leishmania infantum retention in the midgut of Lutzomyia longipalpis, a permissive vector. Rather, LPG appears to be more important in protecting some parasite strains from the toxic environment generated during blood meal digestion in the insect gut. Thus, the relevance of LPG in parasite development in permissive vectors appears to be a complex issue and should be investigated on a strain-specific basis.

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Modelling Sand Fly Lutzomyia longipalpis Attraction to Host Odour: Synthetic Sex-Aggregation Pheromone Dominates the Response

Microorganisms ◽

10.3390/microorganisms9030602 ◽

2021 ◽

Vol 9 (3) ◽

pp. 602

Author(s):

Renata Retkute ◽

Erin Dilger ◽

James G. C. Hamilton ◽

Matt J. Keeling ◽

Orin Courtenay

Keyword(s):

Aggregation Pheromone ◽

Blood Feeding ◽

Sand Fly ◽

Lutzomyia Longipalpis ◽

Animal Reservoir ◽

Modelling Framework ◽

Synthetic Pheromone ◽

Host Seeking ◽

Dead End ◽

Relative Attractiveness

Zoontic visceral leishmaniasis (ZVL) due to Leishmania infantum is a potentially fatal protozoan parasitic disease of humans and dogs. In the Americas, dogs are the reservoir and the sand fly, Lutzomyia longipalpis, the principal vector. A synthetic version of the male sand fly produced sex-aggregation pheromone attracts both female and male conspecifics to co-located insecticide, reducing both reservoir infection and vector abundance. However the effect of the synthetic pheromone on the vector’s “choice“ of host (human, animal reservoir, or dead-end host) for blood feeding in the presence of the pheromone is less well understood. In this study, we developed a modelling framework to allow us to predict the relative attractiveness of the synthetic pheromone and potential alterations in host choice. Our analysis indicates that the synthetic pheromone can attract 53% (95% CIs: 39%–86%) of host-seeking female Lu. longipalpis and thus it out-competes competing host odours. Importantly, the results suggest that the synthetic pheromone can lure vectors away from humans and dogs, such that when co-located with insecticide, it provides protection against transmission leading to human and canine ZVL.

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The sand fly (Diptera: Psychodidae) fauna of the urban area of Lassance, Northeast Minas Gerais, Brazil

PLoS ONE ◽

10.1371/journal.pone.0257043 ◽

2021 ◽

Vol 16 (10) ◽

pp. e0257043

Author(s):

Gabriel Barbosa Tonelli ◽

Camila Binder ◽

Victoria Laporte Carneiro Nogueira ◽

Marina Henriques Prado ◽

Gabriela Gonçalves Theobaldo ◽

...

Keyword(s):

Leishmania Infantum ◽

Abundant Species ◽

Minas Gerais ◽

Sand Fly ◽

Canine Leishmaniasis ◽

Lutzomyia Longipalpis ◽

Scaling Analysis ◽

Sand Flies ◽

Risk Area ◽

Risk Areas

The present study aimed to check the sand flies’ fauna on the municipality of Lassance, Minas Gerais, Brazil and detect the presence of Leishmania DNA on the female captured and determine the risk areas of the municipality. Sand flies were collected monthly from May 2018 to April 2019 using automatic light traps for 3 consecutive nights. Eight houses were selected as sample points due its previous reports of tegumentary leishmaniasis and/or canine leishmaniasis. The sand fly’s fauna found on the present study it’s represented by several medical importance species and the most abundant species found were Lutzomyia longipalpis (77.09%) and Nyssomyia intermedia (10.06%). Leishmania infantum DNA was detected in a pool of Lu. longipalpis resulting on a 2.81% of infection rate. By the frequency of the two most abundant species on this study, we developed a risk area map and it draws attention to sample point 6 due to disparate abundance of sand flies at this site (81.81%). Statistical overview shows Lu. longipalpis as dominant species and, still, Non-Metric Multidimensional Scaling analysis reveal high similarity on fauna’s diversity on the study area. Our findings suggest that the diversity of sand flies from the municipality of Lassance may promote the circulation of Leishmania infantum parasites putting in risk the habitants and other mammal’s species. Still, our study reinforces the necessity of specific studies focused on breed sites of phlebotomine and its’ ecology to expand the knowledge about the behaviour of this group of insects applying directly to leishmaniases’ epidemiology.

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Binding of Leishmania infantum LPG to the midgut is not sufficient to define vector competence in Lutzomyia longipalpis sand flies

10.1101/2020.06.10.145342 ◽

2020 ◽

Author(s):

Iliano V. Coutinho-Abreu ◽

James Oristian ◽

Waldionê de Castro ◽

Timothy R. Wilson ◽

Claudio Meneses ◽

...

Keyword(s):

Late Stage ◽

Leishmania Infantum ◽

Vector Competence ◽

Sand Fly ◽

Parasite Development ◽

Lutzomyia Longipalpis ◽

Sand Flies ◽

Survival And Development ◽

Sand Fly Vectors

AbstractThe major surface lipophosphoglycan (LPG) of Leishmania parasites is critical to vector competence in restrictive sand fly vectors by mediating Leishmania attachment to the midgut epithelium, considered essential to parasite survival and development. However, the relevance of LPG for sand flies that harbor multiple species of Leishmania remains elusive. We tested binding of Leishmania infantum wild type (WT), LPG-defective (Δlpg1 mutants) and add-back lines (Δlpg1 + LPG1) to sand fly midguts in vitro and their survival in Lutzomyia longipalpis sand flies in vivo. Le. infantum WT parasites attached to the Lu. longipalpis midgut in vitro with late-stage parasites binding to midguts in significantly higher numbers compared to early-stage stage promastigotes. Δlpg1 mutants did not bind to Lu. longipalpis midguts, and this was rescued in the Δlpg1 + LPG1 lines, indicating that midgut binding is mediated by LPG. When Lu. longipalpis sand flies were infected with either Le. infantum WT, Δlpg1, or Δlpg1 + LPG1 of the BH46 or BA262 strains, the BH46 Δlpg1 mutant, but not the BA262 Δlpg1 mutant, survived and grew to similar numbers as the WT and Δlpg1 + LPG1 lines. Exposure of BH46 and BA262 Δlpg1 mutants to blood engorged midgut extracts led to the mortality of the BA262 Δlpg1 but not the BH46 Δlpg1 parasites. These findings suggest that Le. infantum LPG protects parasites on a strain-specific basis early in infection, likely against toxic components of blood digestion, however, it is not necessary to prevent Le. infantum evacuation along with the feces in the permissive vector Lu. longipalpis.IMPORTANCEIt is well established that LPG is sufficient to define the vector competence of restrictive sand fly vectors to Leishmania parasites. However, the permissiveness of other sand flies to multiple Leishmania species suggests that other factors might define vector competence for these vectors. In this study, we investigated the underpinnings of Leishmania infantum survival and development in its natural vector Lutzomyia longipalpis. We found out that LPG-mediated midgut binding persists in late-stage parasites. This observation is paradigm-changing and suggests that only a subset of infective metacyclics lose their ability to attach to the midgut with implications for parasite transmission dynamics. However, our data also demonstrate that LPG is not a determining factor in Leishmania infantum retention in the midgut of Lutzomyia longipalpis, a permissive vector. Rather, LPG appears to be more important in protecting some parasite strains from the toxic environment generated during blood meal digestion in the insect gut. Thus, the relevance of LPG in parasite development in permissive vectors appears to be complex and should be investigated on a strain-specific basis.

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Molecular signatures of sexual communication in the phlebotomine sand flies

PLoS Neglected Tropical Diseases ◽

10.1371/journal.pntd.0008967 ◽

2020 ◽

Vol 14 (12) ◽

pp. e0008967

Author(s):

Paul V. Hickner ◽

Nataliya Timoshevskaya ◽

Ronald J. Nowling ◽

Frédéric Labbé ◽

Andrew D. Nguyen ◽

...

Keyword(s):

Aggregation Pheromone ◽

Sexual Communication ◽

Gene Families ◽

Food Sources ◽

Sand Fly ◽

Gene Copy ◽

Lutzomyia Longipalpis ◽

Sand Flies ◽

Sympatric Populations ◽

Phlebotomine Sand Flies

Phlebotomine sand flies employ an elaborate system of pheromone communication wherein males produce pheromones that attract other males to leks (thus acting as an aggregation pheromone) and females to the lekking males (sex pheromone). In addition, the type of pheromone produced varies among populations. Despite the numerous studies on sand fly chemical communication, little is known of their chemosensory genome. Chemoreceptors interact with chemicals in an organism’s environment to elicit essential behaviors such as the identification of suitable mates and food sources. Thus, they play important roles during adaptation and speciation. Major chemoreceptor gene families, odorant receptors (ORs), gustatory receptors (GRs) and ionotropic receptors (IRs) together detect and discriminate the chemical landscape. Here, we annotated the chemoreceptor repertoire in the genomes of Lutzomyia longipalpis and Phlebotomus papatasi, major phlebotomine vectors in the New World and Old World, respectively. Comparison with other sequenced Diptera revealed a large and unique expansion where over 80% of the ~140 ORs belong to a single, taxonomically restricted clade. We next conducted a comprehensive analysis of the chemoreceptors in 63 L. longipalpis individuals from four different locations in Brazil representing allopatric and sympatric populations and three sex-aggregation pheromone types (chemotypes). Population structure based on single nucleotide polymorphisms (SNPs) and gene copy number in the chemoreceptors corresponded with their putative chemotypes, and corroborate previous studies that identified multiple populations. Our work provides genomic insights into the underlying behavioral evolution of sexual communication in the L. longipalpis species complex in Brazil, and highlights the importance of accounting for the ongoing speciation in central and South American Lutzomyia that could have important implications for vectorial capacity.

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Detection of Pintomyia fischeri (Diptera: Psychodidae) With Leishmania infantum (Trypanosomatida: Trypanosomatidae) Promastigotes in a Focus of Visceral Leishmaniasis in Brazil

Journal of Medical Entomology ◽

10.1093/jme/tjaa199 ◽

2020 ◽

Author(s):

Fredy Galvis-Ovallos ◽

Adriele Eiko Ueta ◽

Gabriella de Oliveira Marques ◽

Ana Maria Casagrande Sarmento ◽

Gabriela Araujo ◽

...

Keyword(s):

Visceral Leishmaniasis ◽

Leishmania Infantum ◽

Species Complex ◽

Natural Infection ◽

Metropolitan Region ◽

Sand Fly ◽

Surveillance Program ◽

Lutzomyia Longipalpis ◽

Sand Flies ◽

Vector Surveillance

Abstract Visceral leishmaniasis is spreading in Brazil where the main vector of its agent, Leishmania infantum Nicolle, 1908, is the Lutzomyia longipalpis (Lutz & Neiva, 1912) species complex (Diptera: Psychodidae: Phlebotominae), on which many of the activities of the visceral leishmaniasis surveillance program are based. However, there are areas where canine, and/or human cases have been occurring without the presence of this species complex as in the western part of the Greater São Paulo Metropolitan region, where Embu das Artes municipality is situated. In this area, Pintomyia fischeri (Pinto, 1926) has been implicated as potential vector of Le. infantum but so far its natural infection with this parasite has not yet been ascertained. Therefore, the present study sought to investigate the natural infection in sand flies of a CVL focus in Embu das Artes. The sand fly collections were undertaken with Shannon and CDC traps, monthly, between 1800 and 2100 hours from November 2018 to October 2019, inclusive. A total of 951 sand flies (457 males and 494 females), belonging to 10 species, were captured. Pintomyia fischeri was the predominant species (89.5%); of which 426 females were dissected and one of them (0.23%) was found to be harboring flagellates in its midgut. A sample of these flagellates was isolated in culture and characterized by a 234 base pair fragment of Leishmania heat-shock protein 70 gene (hsp70) and restriction fragment length polymorphism with Hae III restriction enzyme as Le. infantum. This finding reinforces previous evidence of Pi. fischeri as a vector of Le. infantum in foci of visceral leishmaniasis and highlights the importance of vector surveillance in areas where this species occurs.

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