Acessibilidade / Reportar erro

You are what you eat: a systematic review exploring the interaction between Brazilian sand flies and their vertebrate food sources

Abstract

Sand flies play a crucial role as vectors of bacteria, viruses, and protists, with Leishmania being the most notable among them, transmitted to vertebrate hosts during blood feeding. Understanding the feeding behaviours of sand flies is imperative for gaining insights into their eco-epidemiological roles in the transmission of these infectious agents. This systematic review aimed to answer the question ‘What are the blood-feeding sources identified in Brazilian sand flies?’ to provide an analysis of their blood-feeding habits. The diverse range of at least 16 vertebrate orders identified as blood sources for 54 sand fly species across different geographic regions was summarised, and the factors potentially associated with the risk of bias in the included studies were analysed. The findings broaden the discussion concerning methods used to identify blood meal sources and shed light on the implications of sand fly feeding behaviours for the transmission dynamics of Leishmania.

Key words:
sand fly; blood-feeding habits; systematic review; Brazil


Vector-borne diseases present significant public health challenges globally, necessitating a thorough investigation of the intricate interactions between arthropod vectors and vertebrate hosts.11. Chen L, Chen S, Kong P, Zhou L. Host competence, interspecific competition and vector preference interact to determine the vector-borne infection ecology. Front Ecol Evol. 2022; 10: 993844. Among these vectors, sand flies (Diptera: Psychodidae) have garnered considerable attention due to their role in transmitting Leishmania, the causative agents of leishmaniasis, a widespread tropical disease with substantial global health implications.22. Álvarez-Hernández DA, Rivero-Zambrano L, Martínez-Juárez LA, García-Rodríguez-Arana R. Overcoming the global burden of neglected tropical diseases. Ther Adv Infect Dis. 2020; 7: 2049936120966449.,33. WHO - World Health Organization. Global leishmaniasis surveillance: 2019-2020, a baseline for the 2030 roadmap. Wkly Epidemiol Rec. 2021; 96(35): 401-19. The expanding geographical range of leishmaniasis, driven by factors such as urbanisation,44. Caldart ET, Seva AP, Pinto-Ferreira F, Pachoal ATP, de Oliveira JS, Cortela IB, et al. American cutaneous leishmaniasis associated with degradation of native forest, regardless of economic, social and infrastructure vulnerability. Zoonoses Public Health. 2021; 68(4): 327-43.,55. Rodrigues MGA, Sousa JDB, Dias ÁLB, Monteiro WM, Sampaio VS. The role of deforestation on American cutaneous leishmaniasis incidence: spatial-temporal distribution, environmental and socioeconomic factors associated in the Brazilian Amazon. Trop Med Int Health. 2019; 24(3): 348-55. climate change,66. de Carvalho BM, Perez LP, de Oliveira BFA, Jacobson LSV, Horta MA, Sobral A, et al. Vector-borne diseases in Brazil: climate change and future warming scenarios. SiD. 2020; 11(3): 361-404.,77. Mikery-Pacheco OF, Moo-Llanes DA, Rebollar-Téllez EA, Castillo-Vera A. Influence of climate change on leishmaniasis transmission in Latin America and the research status in Mexico. Rev Biomed. 2023; 34(1): 44-58. and human migration,88. Eroglu F, Ozgoztasi O. The increase in neglected cutaneous leishmaniasis in Gaziantep province of Turkey after mass human migration. Acta Trop. 2019; 192: 138-43.,99. Kumar A, Saurabh S, Jamil S, Kumar V. Intensely clustered outbreak of visceral leishmaniasis (kala-azar) in a setting of seasonal migration in a village of Bihar, India. BMC Infect Dis. 2020; 20: 1-13. underscores the urgent need to understand the determinants of disease transmission, as current control strategies have been inadequate in containing its spread.1010. Cota G, Erber AC, Schernhammer E, Simões TC. Inequalities of visceral leishmaniasis case-fatality in Brazil: a multilevel modeling considering space, time, individual and contextual factors. PLoS Negl Trop Dis. 2021; 15(7): e0009567.

Despite their significance as vectors of Leishmania, studies on the feeding behaviours of sand flies, particularly in Brazil, a biodiversity hotspot, have only gained attention in the last decades. This region offers a unique opportunity to investigate sand fly-host interactions. Understanding the feeding habits of sand flies is paramount, as these behaviours have been shown to be influential in vector longevity,1111. Schlein Y, Jacobson RL. Sugar meals and longevity of the sandfly Phlebotomus papatasi in an arid focus of Leishmania major in the Jordan Valley. Med Vet Entomol. 1999; 13(1): 65-71. fecundity,1212. Noguera P, Rondón M, Nieves E. Effect of blood source on the survival and fecundity of the sandfly Lutzomyia ovallesi Ortiz (Diptera: Psychodidae), vector of Leishmania. Biomedica. 2006; 26: 57-63. oviposition,1313. Moraes CS, Aguiar-Martins K, Costa SG, Bates PA, Dillon RJ, Genta FA. Second blood meal by female Lutzomyia longipalpis: enhancement by oviposition and its effects on digestion, longevity, and Leishmania infection. Biomed Res Int. 2018; 2018: 2472508. and vectorial capacity.1414. Sant'Anna MRV, Nascimento A, Alexander B, Dilger E, Cavalcante RR, Diaz-Albiter HM, et al. Chicken blood provides a suitable meal for the sand fly Lutzomyia longipalpis and does not inhibit Leishmania development in the gut. Parasit Vectors. 2010; 3(1): 1-11. Moreover, the intricate network of interactions between sand flies and vertebrates plays a crucial role in shaping the dynamics of Leishmania transmission.1515. Beattie L, Kaye PM. Leishmania-host interactions: what has imaging taught us? Cell Microbiol. 2011; 13(11): 1659-67.,1616. Posada-López L, Velez-Mira A, Cantillo O, Castillo-Castañeda A, Ramírez JD, Galati EAB, et al. Ecological interactions of sand flies, hosts, and Leishmania panamensis in an endemic area of cutaneous leishmaniasis in Colombia. PLoS Negl Trop Dis. 2023; 17(5): e0011316.

This systematic review aims to gather data on the analysis of the blood-feeding behaviour of Brazilian sand flies, with an emphasis on their role as putative vectors of Leishmania. Additionally, concerns regarding bias in the information within the included studies were evaluated using a specifically developed tool to assess this type of study.

MATERIALS AND METHODS

Protocol - This review was systematically conducted following the methodological principles outlined in the Cochrane Handbook,1717. Deeks JJ, Bossuyt PM, Leeflang MM, Takwoingi Y. Cochrane handbook for systematic reviews of diagnostic test accuracy. John Wiley & Sons; 2023. with adaptations for this type of study,1818. Tong A, Flemming K, McInnes E, Oliver S, Craig J. Enhancing transparency in reporting the synthesis of qualitative research: ENTREQ. BMC Med Res Methodol. 2012; 12(1): 1-8. and the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines.1919. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021; 372: n71.

Eligibility criteria - The systematic review was guided by the following research question: ‘What are the blood feeding sources identified in Brazilian sand flies?’ The article selection process and inclusion criteria followed the PICo framework (population, phenomenon of interest, and context): (P) Phlebotominae, (I) blood-feeding sources, and (Co) Brazil. Original research articles reporting the identification of blood sources in wild-caught female sand flies from Brazil were included. Articles describing techniques for identifying the blood sources of sand flies without field collections, outlining the attractiveness of sand flies to various baits (rodent, lizard, chicken, etc.), and/or reporting the identification of sand fly food sources outside Brazil were excluded.

Search strategy - Structured searches were conducted in three databases: MEDLINE (PubMed), Web of Science, and the Virtual Health Library (VHL). In each database, keywords associated with “Phlebotominae”, “Blood feeding”, and “Brazil” were combined using Boolean operators (AND, OR). Details about the search strategy employed in each database are available in the Supplementary data (Table). Articles published up to October 10, 2023, were included without any restrictions on the publication date. Furthermore, supplementary searches of the reference lists of the included articles were undertaken to ensure a thorough exploration of the literature.

Data retrieved from each database underwent initial processing in Mendeley Reference Management to identify and eliminate duplicate files (the same study found in different databases). Following this, the records were transferred to Rayyan for screening based on titles and abstracts.2020. Ouzzani M, Hammady H, Fedorowicz Z, Elmagarmid A. Rayyan-a web and mobile app for systematic reviews. Syst Rev. 2016; 5(1): 1-10. Two independent reviewers (MSS, API) conducted the screening process, following the predefined inclusion and exclusion criteria. Discrepancies were resolved through consensus, or by an additional reviewer (FDR) if an agreement was not reached. The full texts of selected studies were thoroughly examined to validate their eligibility, extract relevant data, and ensure that exclusion criteria were not applicable.

Data extraction - The primary characteristics of the studies, including details about the population, phenomenon of interest, and context, were independently extracted by three reviewers (FDR, MSS, API) and subsequently cross-referenced to confirm all obtained data. Extracted data included sand fly collections, the Brazilian states where sand flies were collected, the overall number of collected sand flies, the total count of collected and engorged females, the variety of vertebrate species identified as blood sources, and specific details concerning the methodology employed for blood meal identification. Sand fly nomenclature and genera abbreviations used here followed Galati2121. Galati EAB. Phlebotominae (Diptera, Psychodidae): classification, morphology and terminology of adults and identification of American Taxa. In: Rangel E, Shaw J, editors. Brazilian sand flies: biology, taxonomy, medical importance and control. 1st ed. Springer International Publishing; 2018. p. 9-212. and Marcondes,2222. Marcondes CB. A proposal of generic and subgeneric abbreviations for phlebtomine sandflies (Diptera: Psychodidae: Phelbotomina) of the world. Entomol News. 2007; 118(4): 351-6. respectively. Citations involving sand fly species complexes, specifically those morphologically indistinguishable, and synonyms were presented in accordance with the original records.

Risk of bias - To enable a critical and transparent analysis of the results obtained, an effort was made to examine potential sources of bias in the included articles related to three main domains: (I) Sand fly identification; (II) Sample quality; and (III) Methods for food source identification. For this analysis, signalling questions related to each domain were proposed (Table I) and analysed in all included articles.

TABLE I
Domains and signaling questions used to analyze the risk of bias in the included articles

RESULTS

Literature search - A total of 1,214 articles were initially identified from the databases, with 221 excluded due to duplication. After analysing titles and abstracts, 39 articles were selected for full-text reading. Among these, 36 articles were included, and a subsequent rigorous examination of reference lists did not yield the inclusion of any additional articles. Flow diagrams outlining each step of this systematic review, following the PRISMA guidelines, are presented in Fig. 1.

Fig. 1:
flow diagram illustrating the study selection process according to Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines.

Descriptive analysis of included studies - The characteristics of all included studies are presented in Table II, including information about the blood sources of sand flies from various Brazilian states. Light traps were utilised in most of the included studies (33/36), while manual collections (2/36) or Shannon traps (1/36) were less frequently employed. The total number of collected sand flies varied between 80 and 15,457, with the percentage of engorged females among the total collected females ranging from 0.4% to 100%. The results showed a slight tendency for engorged females to be captured using manual collection instead of Shannon or light traps.

TABLE II
Characteristics of the studies included in the systematic review

The food source data were recovered for 13 out of the 19 genera of Brazilian sand flies, encompassing a total of at least 54 species and subspecies out of about 280 species currently described in Brazil,2121. Galati EAB. Phlebotominae (Diptera, Psychodidae): classification, morphology and terminology of adults and identification of American Taxa. In: Rangel E, Shaw J, editors. Brazilian sand flies: biology, taxonomy, medical importance and control. 1st ed. Springer International Publishing; 2018. p. 9-212. corresponding to approximately 19% of the total. The following genera had information available: Bichromomyia, Evandromyia, Lutzomyia, Micropygomyia, Migonemyia, Nyssomyia, Pintomyia, Pressatia, Psathyromyia, Psychodopygus, Sciopemyia, Trichophoromyia, and Trichopygomyia. There is a lack of information regarding the blood food source for the remaining genera, including Brumptomyia, Deanemyia, Edentomyia, Expapillata, Martinsmyia, and Viannamyia. It is noteworthy that De. maruaga, a troglobite species, exhibits autogenic and parthenogenic behaviour,2323. Alves VR, de Freitas RA, Barrett T. Lutzomyia maruaga (Diptera: Psychodidae), a new bat-cave sand fly from Amazonas, Brazil. Mem Inst Oswaldo Cruz. 2008; 103(3): 251-3. but it is unclear whether this behaviour extends to all species within the genus.

Most of the studies (58%) demonstrated a predominant orientation towards the use of DNA-based methods, in which information regarding at least 42 species was retrieved (Table III). Among the 21 studies utilising molecular markers, 20 (95%) exclusively employed mitochondrial targets. Notably, cytochrome b (cytb) was the preferred molecular marker in 94% of the cases. The remaining two studies (6%) utilised cytochrome oxidase I (COI),2424. Costa JCR, Marchi GH, Santos CS, Andrade MCM, Chaves Jr SP, Silva MAN, et al. First molecular evidence of frogs as a food source for sand flies (Diptera: Phlebotominae) in Brazilian caves. Parasitol Res. 2021; 120(5): 1571-82. and the nuclear gene prepronociceptin (PNOC) as molecular targets.2525. Baum M, de Castro EA, Pinto MC, Goulart TM, Baura W, Klisiowicz DD, et al. Molecular detection of the blood meal source of sand flies (Diptera: Psychodidae) in a transmission area of American cutaneous leishmaniasis, Parana State, Brazil. Acta Trop. 2015; 143: 8-12. For host identification, 16 articles (76%) employed Sanger sequencing, followed by polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) (four articles, 19%), and specific primers for each host (one article, 5%).

TABLE III
Blood source identification of Brazilian sand fly species by polymerase chain reaction (PCR)

The precipitin test (Table IV) was featured in 8 out of 36 studies, accounting for 23% of the research, and provided information on the identification of blood sources for nine sand fly species. It generally utilised different antisera, including those for bird, armadillo, chicken, dog, goat, opossum, equine, feline, human, sheep, rodent, and pig, or employed family-specific antisera. Conversely, enzyme-linked immunosorbent assay (ELISA) was employed in 7 out of 36 included studies (19%) (Table V), and the identification of blood sources for 17 sand fly species was obtained through the test with the same spectrum of antisera used in the precipitin test. In addition to the detection of a single food source, fourteen studies (38%) employing ELISA and precipitin techniques also reported sand flies with mixed feeding, in which two or more blood sources were simultaneously detected in the same sand fly. In contrast, only two studies identified multiple feedings through PCR-RFLP targeted to the cytb gene.2626. Quaresma PF, Carvalho GML, Ramos MCNF, Andrade Filho JD. Natural Leishmania sp. reservoirs and phlebotomine sandfly food source identification in Ibitipoca State Park, Minas Gerais, Brazil. Mem Inst Oswaldo Cruz. 2012; 107(4): 480-5.,2727. Guimarães-E-Silva AS, Silva SO, Ribeiro da Silva RC, Pinheiro VCS, Rebêlo JMM, Melo MN, et al. Leishmania infection and blood food sources of phlebotomines in an area of Brazil endemic for visceral and tegumentary leishmaniasis. PLoS One. 2017; 12(8): e0179052. A total of 15 sand fly species within seven genera were found engorged with mixed feeding (Fig. 2). The genus Nyssomyia was the most prevalent, with four species reported with mixed feeding, followed by Evandromyia (3), Psychodopygus (2), Lutzomyia (2), Pressatia (2), Micropygomyia (1), and Psathyromyia (1). Notably, a total of at least eight vertebrate orders have been associated with Lutzomyia longipalpis, Nyssomyia intermedia, and Nyssomyia whitmani, demonstrating a high plasticity of these species in feeding habits.

TABLE IV
Blood source identification of Brazilian sand fly species by Precipitin test
TABLE V
Blood source identification of Brazilian sand fly species by enzyme-linked immunosorbent assay (ELISA)

Fig. 2:
radial tree showing the relationship between the sand fly species and the vertebrate orders serving as blood source in mixed feeding reports

A complex interaction matrix was observed between the sand fly genera and the orders of vertebrates identified in the blood meal (Fig. 3). For all sand fly genera, except Trichopygomyia, more than one vertebrate order has been associated. The Nyssomyia genus accounted for 94 single blood meal identifications, with Ny. whitmani, Ny. intermedia, and Nyssomyia umbratilis being the most representative species. The Lutzomyia genus followed, with a high number of blood meal identifications attributed mainly to Lu. longipalpis. Notably, Psychodopygus also contributed significantly with 42 single blood meal identifications for at least ten species.

Fig. 3:
interaction matrix (Sankey diagram) between sand fly genera and vertebrates identified as the food source.

Risk of bias - Considering the three domains evaluated, a high risk of bias was mainly observed in the domain related to the selection and preservation of engorged females (Fig. 4). This is primarily associated with the lack of information regarding the female’s level of engorgement (partial or full) and the stage of the digestive process (recent or late). The risk of bias observed regarding the methodology used to identify the food source is mainly associated with the absence of controls (e.g., male sand flies as endogenous controls) and the lack of a predefined cut-off point for ELISA and precipitin techniques, or minimal similarity criteria attributed to the amplicon compared to the GenBank database. A low risk of bias was found in the domain of identifying sand flies, as few studies did not report using a specific classification key.

Fig. 4:
potential risk of bias identified in the included studies

DISCUSSION

Although leishmaniasis has been known to occur in Brazil since the early 1900s,2828. Benchimol JL, Gualandi FC, Barreto DCS, Pinheiro LA. Leishmaniasis: historical configuration in Brazil with an emphasis on the visceral disease, from the 1930s to the 1960s. Bol Mus Para Emílio Goeldi Cienc Hum. 2019; 14: 611-26. it was predominantly in the last two decades that blood source identification of sand flies emerged as a subject of study in the country. Understanding the feeding habits of sand flies is of utmost relevance, as it provides indirect data regarding the presence of vertebrates that may act as potential reservoirs/hosts of Leishmania.2929. Ready PD. Biology of phlebotomine sand flies as vectors of disease agents. Annu Rev Entomol. 2013; 58: 227-50. The intricate relationship between sand flies and vertebrates can also be used as evidence to suspect the role of sand flies as vectors.3030. Killick-Kendrick R. Phlebotomine vectors of the leishmaniases: a review. Med Vet Entomol. 1990; 4(1): 1-24. This is also applicable to sand flies that feed exclusively on animals not hosting Leishmania, as knowledge of their ecological habits is of interest. This systematic review gathered data on at least 54 sand fly species distributed across 17 Brazilian states (65%), underscoring the need for continuous study, particularly in the Southern region of the country, where only one study has been conducted.3131. Baum M, Ribeiro M, Lorosa ES, Damasio GAC, de Castro EA. Eclectic feeding behavior of Lutzomyia (Nyssomyia) intermedia (Diptera, Psychodidae, Phlebotominae) in the transmission area of American cutaneous leishmaniasis, State of Parana, Brazil. Rev Soc Bras Med Trop. 2013; 46(5): 560-5.

Light traps were the most utilised method in studies focusing on identifying female blood sources (91.6%) compared to other collection types such as manual or Shannon traps. This fact caught our attention since fed females are not typically attracted by light and are often observed resting after blood feeding.3232. Forattini OP. Entomologia médica: Psychodidae, Phlebotominae, leishmanioses, bartonelose. São Paulo: Ed. Edgard Blücher / Ed. Univ. São Paulo; 1973. v. 4, 658pp. This may account for the discrepancies between the total number of females collected and the total number of engorged females collected in the included studies (Table II). Regarding Shannon traps, in addition to light, the collector may also act as an attractant, leading to the capture of species nearby or attempting to feed on humans, mainly due to body temperature and the release of carbon dioxide through breathing. However, this attractiveness may not necessarily represent efficient feeding behaviour. Overall, it is evident that the sand fly collection method used to assess the blood meal source of females warrants further discussion.

Various techniques for identifying blood sources in sand flies have been employed, with molecular methods predominating alongside precipitin and ELISA techniques. The detection of mixed feedings underscores the need for careful consideration of the techniques used, particularly in assessing specificity and cross-reactivity. Overall, blood source identification is especially pertinent as a complementary tool in entomological studies aiming to identify and characterise potential vectors in endemic areas. In this regard, based on the results obtained here, we aim to explore and discuss two crucial points: methods for identifying blood sources and ecological inferences derived from blood sources.

Blood source identification in sand flies: methodological considerations - Similar to other dipterans, sand flies generally exhibit gonotrophic concordance, wherein each blood meal is followed by oviposition.3232. Forattini OP. Entomologia médica: Psychodidae, Phlebotominae, leishmanioses, bartonelose. São Paulo: Ed. Edgard Blücher / Ed. Univ. São Paulo; 1973. v. 4, 658pp. The duration of this process may vary among species, but it typically occurs within 5-7 days.3333. de Oliveira EF, Oshiro ET, Fernandes WS, Ferreira AMT, de Oliveira AG, Galati EAB. Vector competence of Lutzomyia cruzi naturally demonstrated for Leishmania infantum and suspected for Leishmania amazonensis. Am J Trop Med Hyg. 2017; 96(1): 178-81. Complete blood meal digestion usually takes place within 72-96 hours after blood feeding, and the degree of digestion can be a crucial factor in identifying the food source. Blood digestion is commonly categorised into three levels: 1) fresh blood (bright red content in the midgut with intact erythrocytes visible under the microscope), 2) partially digested blood (dark red), and 3) extensively digested blood (brown).3434. Svobodová M, Sádlová J, Chang KP, Volf P. Distribution and feeding preference of the sand flies Phlebotomus sergenti and P. papatasi in a cutaneous leishmaniasis focus in Sanliurfa, Turkey. Am J Trop Med Hyg. 2003; 68(1): 6-9. Interestingly, only four studies within the selected articles have characterised the level of engorgement or the stage of the digestive process.3535. Afonso MMDS, Duarte R, Miranda JC, Caranha L, Rangel EF. Studies on the feeding habits of Lutzomyia (Lutzomyia) longipalpis (Lutz & Neiva, 1912) (Diptera: Psychodidae: Phlebotominae) populations from endemic areas of American Visceral Leishmaniasis in Northeastern Brazil. J Trop Med. 2012; 2012: 1-6.,3636. de Brito VN, de Almeida ABPF, Nakazato L, Duarte R, Souza CO, Sousa VRF. Phlebotomine fauna, natural infection rate and feeding habits of Lutzomyia cruzi in Jaciara, state of Mato Grosso, Brazil. Mem Inst Oswaldo Cruz. 2014; 109(7): 899-904.,3737. Nery LCR, Lorosa ES, Franco AMR. Feeding preference of the sand flies Lutzomyia umbratilis and L. spathotrichia (Diptera: Psychodidae, Phlebotominae) in an urban forest patch in the city of Manaus, Amazonas, Brazil. Mem Inst Oswaldo Cruz. 2004; 99(6): 571-4.,3838. Neitzke-Abreu HC, Andrade GMC, de Almeida PS, Ribeiro GC, Ribeiro TA, Barrios D, et al. Natural infection of Lutzomyia longipalpis (Lutz & Neiva, 1912) by Leishmania infantum in a municipality with a high incidence of visceral leishmaniasis in the Brazilian Midwest. Rev Soc Bras Med Trop. 2023; 56: e0259-2023. This lack of information is particularly noteworthy because, in general, the studies reported a higher number of females assumed to be engorged compared to females in which the food source was identified. This discrepancy may be attributed to the amount of blood ingested or the level of blood digestion, which, if extensively digested, could lead to the failure to identify the food source.3939. Sant'Anna MR V, Jones NG, Hindley JA, Mendes-Sousa AF, Dillon RJ, Cavalcante RR, et al. Blood meal identification and parasite detection in laboratory-fed and field-captured Lutzomyia longipalpis by PCR using FTA databasing paper. Acta Trop. 2008; 107(3): 230-7. However, studies are necessary to ascertain the optimum range for detecting the blood source using different methodologies, such as ELISA and the precipitin test, even though estimating this variable for wild-caught females is challenging.

One of the primary challenges posed by sand flies as a molecular study model is the size of their tissue/body, which hampers the isolation of sufficient DNA for amplifying specific molecular targets. The amount of blood ingested by a female in a single feeding is not well-established; however, it is suggested to be equivalent to the insect’s own weight, which can vary from 0.1 to 0.6 mg.4040. Chaniotis BN. The biology of California phlebotomus (Diptera: Psychodidae) under laboratory conditions. J Med Entomol. 1967; 4(2): 221-33. Typically, full engorgement occurs in a single feeding, but occasionally a partly engorged sand fly may relocate to another site and continue feeding. Therefore, when considering sand flies that have fed on various vertebrates, the amount of blood ingested from each source can vary, influencing DNA recovery and consequently limiting the ability to identify mixed feedings. Conversely, the reactivity of blood containing multiple IgG from distinct hosts to antisera used in both the precipitin and ELISA tests appears to be more sensitive, allowing for the identification of mixed feedings.

Concerning ELISA and precipitin techniques, all studies utilised antisera from various vertebrates (e.g., cattle, horse, pig, rodent, human, chicken, etc.) to detect specific antibodies for identifying the blood source. However, a high risk of bias was observed in most studies due to the absence of specificity evaluations, potentially impacting cross-reactivity and consequently allowing the detection of mixed feedings. Notably, no instances of mixed feeding were observed when Sanger sequencing was employed. A potential explanation for this phenomenon could be the challenge of identifying polymorphic sites within the amplicon or the quantity of DNA obtained after the DNA extraction step. In either scenario, cloning the PCR product might be a useful strategy to enhance the detection of multiple blood feedings.

The volume of blood available for DNA extractions serves as a clear indicator of DNA yield.4141. Chacon-Cortes D, Griffiths LR. Methods for extracting genomic DNA from whole blood samples: current perspectives. J Bio Sci Appl Med. 2014; 2: 1-9. Long-term storage conditions of sand fly tissue/blood, a crucial factor in molecular studies,4242. Depaquit J, Ferte H, Léger N, Killick-Kendrick R, Rioux J, Killick-Kendrick M, et al. Molecular systematics of the phlebotomine sandflies of the subgenus Paraphlebotomus (Diptera, Psychodidae, Phlebotomus) based on ITS2 rDNA sequences. Hypotheses of dispersion and speciation. Insect Mol Biol. 2000; 9(3): 293-300. can impact DNA integrity.4343. Holland NT, Smith MT, Eskenazi B, Bastaki M. Biological sample collection and processing for molecular epidemiological studies. Mutat Res. 2003; 543(3): 217-34. Appropriate storage conditions depend on various factors, including the intended analyses and the duration of specimen storage. Generally, blood samples stored at 4ºC for a short period still yield DNA of acceptable quality if the correct blood collection tubes are used,4444. Nederhand RJ, Droog S, Kluft C, Simoons ML, De Maat MPM; Investigators of the EUROPA trial. Logistics and quality control for DNA sampling in large multicenter studies. J Thromb Haemost. 2003; 1(5): 987-91.,4545. Richardson AJ, Narendran N, Guymer RH, Vu H, Baird PN. Blood storage at 4 C -factors involved in DNA yield and quality. J Lab Clin Med. 2006; 147(6): 290-4. although this practice is not standard in entomological studies. The preferred temperature for long-term DNA isolation from whole blood samples is -80ºC.4343. Holland NT, Smith MT, Eskenazi B, Bastaki M. Biological sample collection and processing for molecular epidemiological studies. Mutat Res. 2003; 543(3): 217-34. While whole blood samples can also be frozen at -20°C for long-term storage,4343. Holland NT, Smith MT, Eskenazi B, Bastaki M. Biological sample collection and processing for molecular epidemiological studies. Mutat Res. 2003; 543(3): 217-34.,4646. Steinberg KK, Sanderlin KK, Ou CY, Hannon WH, McQuillan G, Sampson EJ. DNA banking in epidemiologic studies. Epidemiol Rev. 1997; 19(1): 156-62.,4747. AlRokayan SAH. Effect of storage temperature on the quality and quantity of DNA extracted from blood. Pak J Biol Sci. 2000; 3(3): 392-4. some studies have reported lower DNA yields with this approach.4444. Nederhand RJ, Droog S, Kluft C, Simoons ML, De Maat MPM; Investigators of the EUROPA trial. Logistics and quality control for DNA sampling in large multicenter studies. J Thromb Haemost. 2003; 1(5): 987-91.,4747. AlRokayan SAH. Effect of storage temperature on the quality and quantity of DNA extracted from blood. Pak J Biol Sci. 2000; 3(3): 392-4. Regarding the blood content within sand flies, there is no evidence suggesting the optimal storage method, which makes the risk of bias related to this aspect unclear. However, it appears that temperatures higher than -80ºC may compromise blood integrity during long-term storage, potentially affecting the determination of the food source using both molecular methods and specific antibodies.

The storage method appears to be a concern in blood-feeding studies; however, seven articles (19%) did not specify the preservation method. Twelve studies (33%) reported that sand flies were stored dry after dissection at various temperatures, such as -7ºC, -15ºC, and -20ºC. In these cases, long-term storage may affect blood quality and, consequently, DNA recovery.4343. Holland NT, Smith MT, Eskenazi B, Bastaki M. Biological sample collection and processing for molecular epidemiological studies. Mutat Res. 2003; 543(3): 217-34. Ethanol was employed to preserve sand fly samples, with varying concentrations, including 70%,2424. Costa JCR, Marchi GH, Santos CS, Andrade MCM, Chaves Jr SP, Silva MAN, et al. First molecular evidence of frogs as a food source for sand flies (Diptera: Phlebotominae) in Brazilian caves. Parasitol Res. 2021; 120(5): 1571-82.,2525. Baum M, de Castro EA, Pinto MC, Goulart TM, Baura W, Klisiowicz DD, et al. Molecular detection of the blood meal source of sand flies (Diptera: Psychodidae) in a transmission area of American cutaneous leishmaniasis, Parana State, Brazil. Acta Trop. 2015; 143: 8-12.,4848. Pimentel AC, Uzcátegui YDS, de Lima ACS, Silveira FT, dos Santos TV, Ishikawa EAY. Blood Feeding Sources of Nyssomyia antunesi (Diptera: Psychodidae): A Suspected Vector of Leishmania (Kinetoplastida: Trypanosomatidae) in the Brazilian Amazon. J Med Entomol. 2022; 59(5): 1847-52.,4949. Rodrigues BL, Costa GD, Shimabukuro PHF. Identification of bloodmeals from sand flies (Diptera: Psychodidae) collected in the Parque Nacional do Virua, State of Roraima, Brazil. J Med Entomol. 2021; 58(6): 2488-94. 80%,5050. de Araujo-Pereira T, de Pita-Pereira D, Baia-Gomes SM, Boité M, Silva F, Pinto IS, et al. An overview of the sandfly fauna (Diptera: Psychodidae) followed by the detection of Leishmania DNA and blood meal identification in the state of Acre, Amazonian Brazil. Mem Inst Oswaldo Cruz. 2020; 115: 1-17. 90%,5151. de Ávila MM, Brilhante AF, de Souza CF, Bevilacqua PD, Galati EAB, Brazil RP, et al. Ecology, feeding and natural infection by Leishmania spp. of phlebotomine sand flies in an area of high incidence of American tegumentary leishmaniasis in the municipality of Rio Branco, Acre, Brazil. Parasit Vectors. 2018; 11: 64. and 96%.5252. da Silva MS, Pereira Jr AM, Costa NVC, Costa GS, Rodrigues MMS, Medeiros JF, et al. Use of light emitting diodes (LEDs) are effective and useful for sand fly ecoepidemiology studies in an Amazonian environment. Acta Trop. 2022; 233: 106550.,5353. Pereira Jr AM, Souza ABN, Castro TS, da Silva MS, de Paulo PFM, Ferreira GEM, et al. Diversity, natural infection and blood meal sources of phlebotomine sandflies (Diptera, Psychodidae) in the western Brazilian Amazon. Mem Inst Oswaldo Cruz. 2019; 114(6): 1-9.,5454. Leão PO, Pereira Jr AM, de Paulo PFM, Carvalho LPC, Souza ABN, da Silva MS, et al. Vertical stratification of sand fly diversity in relation to natural infections of Leishmania sp. and blood-meal sources in Jamari National Forest, Rondonia State, Brazil. Parasit Vectors. 2020; 13(1): 422. The stability of ethanol in stored blood is of immense entomological interest, as there is often a need for the analysis of such blood samples months after collection. Although some authors stored sand flies preserved in ethanol at different temperatures (-10ºC and -20ºC), the quality of blood in alcohol samples appears not to be affected at these temperatures for at least six months.5555. Meyer T, Monge PK, Sakshaug J. Storage of blood samples containing alcohol. Acta Pharmacol Toxicol (Copenh). 1979; 45(4): 282-6. Dimethyl sulfoxide (DMSO) at 6% was used to preserve engorged females in two studies2626. Quaresma PF, Carvalho GML, Ramos MCNF, Andrade Filho JD. Natural Leishmania sp. reservoirs and phlebotomine sandfly food source identification in Ibitipoca State Park, Minas Gerais, Brazil. Mem Inst Oswaldo Cruz. 2012; 107(4): 480-5.,5656. Carvalho GML, Rêgo FD, Tanure A, Silva ACP, Dias TA, Paz GF, et al. Bloodmeal identification in field-collected sand flies from Casa Branca, Brazil, using the cytochrome b PCR Method. J Med Entomol. 2017; 54(4): 1049-54. and seems to be an efficient and cost-effective preservative method, as it protects cells from intracellular ice formation-induced damage, acting as a cryoprotective agent.5757. Lovelock JE, Bishop MWH. Prevention of freezing damage to living cells by dimethyl sulphoxide. Nature. 1959; 183(4672): 1394-5.

In summary, these findings emphasise the need for standardised methodologies and meticulous consideration of storage conditions in future entomological studies to enhance the accuracy and reliability of blood source identification in sand flies.

Ecological inferences based on blood sources - Over time, numerous studies have explored the feeding tendencies of sand flies, often relying on attractiveness to vertebrates as a proxy for feeding preferences. However, such studies are limited as they do not always identify the actual blood sources, making the data fragile due to the potential for misinterpretation. For instance, while it has been suggested that species within the Martinsmyia genus are attracted to rodents based on bait studies, the blood sources of these species remain unidentified. Similarly, species within the Micropygomyia and Sciopemyia genera, traditionally believed to be exclusively attracted to cold-blooded animals, have been found feeding on warm-blooded animals, indicating variable feeding habits. The association between sand fly feeding habits and the detection of Leishmania parasites further complicates our understanding of their role in disease transmission. Although human blood has been detected in sand fly species from the Micropygomyia and Sciopemyia genera, the observed anthropophilic behaviour does not necessarily confirm their role as vectors, emphasising the necessity for more comprehensive studies. Furthermore, the possibility of cross-contamination of samples with human DNA during sand fly processing should be taken into consideration. In the risk of bias assessment, studies reporting descriptions regarding the use of sterile materials during sand fly dissection were considered as having a low risk of bias in the Sample Quality domain.

Human blood was detected in at least 35 sand fly species, making it the most identified vertebrate, followed by Gallus gallus blood, detected in 25 species. Chickens are refractory to Leishmania infection; however, their presence in peridomestic areas is often suggested as a risk factor of visceral leishmaniasis (VL). Belo et al.5858. Belo VS, Werneck GL, Barbosa DS, Simões TC, Nascimento BWL, da Silva ES, et al. Factors associated with visceral leishmaniasis in the Americas: a systematic review and meta-analysis. PLoS Negl Trop Dis. 2013; 7(4): e2182. conducted a meta-analysis of factors associated with VL and found conflicting data. On one hand, the presence of a chicken coop may attract sand flies,1414. Sant'Anna MRV, Nascimento A, Alexander B, Dilger E, Cavalcante RR, Diaz-Albiter HM, et al. Chicken blood provides a suitable meal for the sand fly Lutzomyia longipalpis and does not inhibit Leishmania development in the gut. Parasit Vectors. 2010; 3(1): 1-11. thereby increasing the chances of dogs (the main L. infantum reservoir) being bitten by them. On the other hand, if the vector feeds on chickens, it could reduce the proportion of effective bites on dogs. Given these contradictory results, further studies are needed to clarify this relationship. Moreover, the fact that sand flies have fed on various bird orders may indicate their ecological habits, such as utilising tree canopies for opportunistic blood feeding.

Additionally, while certain vertebrates like Artiodactyls and Equines may not be considered primary hosts of Leishmania parasites, their presence can influence sand fly density and human-sand fly exposure, thereby impacting disease transmission dynamics.5959. Bern C, Courtenay O, Alvar J. Of cattle, sand flies and men: a systematic review of risk factor analyses for South Asian visceral leishmaniasis and implications for elimination. PLoS Negl Trop Dis. 2010; 4(2): e599. Noteworthy, Leishmania (Mundinia) orientalis has been reported in bovines from Switzerland6060. Lobsiger L, Müller N, Schweizer T, Frey CF, Wiederkehr D, Zumkehr B, et al. An autochthonous case of cutaneous bovine leishmaniasis in Switzerland. Vet Parasitol. 2010; 169(3-4): 408-14. and descriptions of a horse infected by Leishmania braziliensis in South America was in the first half of the last century.6161. Mazza S. Leishmaniasis cutánea en el caballo y nueva observación de la misma en el perro. Bol Inst Clin Quir. 1927; 3: 462-4. Since then, several studies have suggested the presence of this parasite in horses and donkeys from Brazil.6262. Aguilar CM, Rangel EF, Grimaldi Filho G, Momem H. Human, canine and equine leishmaniasis caused by Leishmania braziliensis braziliensis in an endemic area in the State of Rio de Janeiro. Mem Inst Oswaldo Cruz. 1987; 82(1): 143.,6363. Falqueto A, Varejão JBM, Sessa PA. Cutaneous leishmaniasis in a horse (Equus caballus) from endemic area in the state of Espírito Santo, Brazil. Mem Inst Oswaldo Cruz.1987; 82(3): 443.,6464. Vexenat JA, Barretto AC, Rosa ACO, Sales CC, Magalhães AV. [Natural infection of Equus asinus by Leishmania braziliensis braziliensis - Bahia, Brazil]. Mem Inst Oswaldo Cruz. 1986; 81(2): 237-8.Leishmania infantum infection has also been reported in equines, causing skin lesions and locomotor problems,6565. Soares IR, Silva SO, Moreira FM, Prado LG, Fantini P, Maranhão RPA, et al. First evidence of autochthonous cases of Leishmania (Leishmania) infantum in horse (Equus caballus) in the Americas and mixed infection of Leishmania infantum and Leishmania (Viannia) braziliensis. Vet Parasitol. 2013; 197(3-4): 665-9. but it is also associated with asymptomatic disease.6666. Leonel JAF, Tannihão B, Arantes JA, Vioti G, Benassi JC, Brandi RA, et al. Detection of Leishmania infantum DNA in blood samples of horses (Equus caballus) and donkeys (Equus asinus) by PCR. Rev Inst Med Trop São Paulo. 2021; 63.,6767. Benassi JC, Benvenga GU, Ferreira HL, Soares RM, Silva DT, Pereira VF, et al. Molecular and serological detection of Leishmania spp. in horses from an endemic area for canine visceral leishmaniasis in southeastern Brazil. Pes Vet Bras. 2018; 38(6): 1058-63. Representative species of the subgenus Mundinia6868. Espinosa OA, Serrano MG, Camargo EP, Teixeira MMG, Shaw JJ. An appraisal of the taxonomy and nomenclature of trypanosomatids presently classified as Leishmania and Endotrypanum. Parasitology. 2018; 145(4): 430-42. have been identified in horses from Florida (USA) and Rio de Janeiro (Brazil),6969. Reuss SM, Dunbar MD, Mays MBC, Owen JL, Mallicote MF, Archer LL, et al. Autochthonous Leishmania siamensis in horse, Florida, USA. Emerg Infect Dis. 2012; 18(9): 1545.,7070. Mendes Junior AAV, Filgueira CPB, Miranda LFC, de Almeida AB, Cantanhêde LM, Fagundes A, et al. First report of Leishmania (Mundinia) martiniquensis in South American territory and confirmation of Leishbunyavirus infecting this parasite in a mare. Mem Inst Oswaldo Cruz. 2023; 118: 1-7. indicating that this vertebrate should sporadically represent a relevant role as a host of these parasites. However, studies assessing the competence of these animals as reservoirs should be conducted.

Most of the blood feeding reports on Carnivora were represented by feedings on Canis lupus familiaris (domestic dog), widely known to be the primary reservoir of L. infantum in urban areas of Brazil,7171. Gontijo CMF, Melo MN. Leishmaniose visceral no Brasil: quadro atual, desafios e perspectivas. Rev Bras Epidemiol. 2004; 7(3): 338-49. and the remaining were associated with Felis silvestris catus (domestic cat), in which L. infantum infections have also been sporadically reported.7272. Santos NS, Pinho FA, Hlavac NRC, Nunes TL, Almeida NR, Solcà MS, et al. Feline leishmaniasis caused by Leishmania infantum: parasite sequencing, seropositivity, and clinical characterization in an endemic area from Brazil. Front Vet Sci. 2021; 8: 1-12. Other sylvatic Carnivora, like the crab-eating fox (Cerdocyon thous) and the bush dog (Speothos venaticus), have also been suggested as reservoirs of L. infantum.7373. Roque ALR, Jansen AM. Wild and synanthropic reservoirs of Leishmania species in the Americas. Int J Parasitol Parasites Wildl. 2014; 3(3): 251-62. Several sand fly species, such as Bichromomyia flaviscutellata, Lutzomyia cruzi, Lu. longipalpis, Migonemyia migonei, Ny. intermedia, Nyssomyia neivai, Ny. umbratilis, and Ny. whitmani, have been found feeding on dogs, and there is ongoing debate regarding their role as vectors of Leishmania.7474. Brazil RP, Rodrigues AAF, Andrade-Filho JD. Sand fly vectors of Leishmania in the Americas - A mini review. Entomol Ornithol Herpetol. 2015; 4(2): 1-4.,7575. Akhoundi M, Kuhls K, Cannet A, Votýpka J, Marty P, Delaunay P, et al. A historical overview of the classification, evolution, and dispersion of Leishmania parasites and sandflies. PLoS Negl Trop Dis. 2016; 10(3): e0004349. However, the presence of other species feeding on dogs, such as Evandromyia cortelezzii, Evandromyia evandroi, Evandromyia termitophila, and Pressatia choti, opens perspectives on the capacity and competence of vectorial studies to ascertain their involvement in the epidemiological cycle, particularly of L. infantum.

The nine-banded armadillo (Dasypus novemcinctus) is considered a potential reservoir of Leishmania naiffi in Brazil.7676. Naiff RD, Freitas RA, Naiff MF, Arias JR, Barret TV, Momen H, et al. Epidemiological and nosological aspects of Leishmania naiffi Lainson & Shaw, 1989. Mem Inst Oswaldo Cruz. 1991; 86(3): 317-21.,7777. Lainson R, Shaw JJ. Leishmania (Viannia) naiffi sp. n., a parasite of the armadillo, Dasypus novemcinctus (L.) in Amazonian Brazil. Ann Parasitol Hum Comp. 1989; 64(1): 3-9. At least five sand fly species have been found feeding on this vertebrate (Evandromyia sp.; Psychodopygus ayrozai, Chagasi series of Psychodopygus genus, Psychodopygus paraensis, and Psychodopygus carrerai carrerai) in studies conducted in Roraima and Acre, both in the Northern region of Brazil,4949. Rodrigues BL, Costa GD, Shimabukuro PHF. Identification of bloodmeals from sand flies (Diptera: Psychodidae) collected in the Parque Nacional do Virua, State of Roraima, Brazil. J Med Entomol. 2021; 58(6): 2488-94.,5050. de Araujo-Pereira T, de Pita-Pereira D, Baia-Gomes SM, Boité M, Silva F, Pinto IS, et al. An overview of the sandfly fauna (Diptera: Psychodidae) followed by the detection of Leishmania DNA and blood meal identification in the state of Acre, Amazonian Brazil. Mem Inst Oswaldo Cruz. 2020; 115: 1-17. consistent with the geographical distribution of L. naiffi. Of these sand fly species, only Ps. ayrozai has been suggested as a putative vector of this parasite.7474. Brazil RP, Rodrigues AAF, Andrade-Filho JD. Sand fly vectors of Leishmania in the Americas - A mini review. Entomol Ornithol Herpetol. 2015; 4(2): 1-4. Other Cingulata have also been found as blood sources for sand flies, such as Dasypus sabanicola,7878. Torchitte APA, Pereira Jr AM, Paulo PFM, Costa GS, Castro TS, Ferreira RGM, et al. Identification of sand flies (Diptera: Psychodidae) and blood meal sources in periurban areas of Ji-Paraná municipality, Western Brazilian Amazon. Braz J Biol. 2021; 81(1): 225-7. and the six-banded armadillo Euphractus sexcinctus;7979. Macedo-Silva VP, Martins DRA, De Queiroz PVS, Pinheiro MPG, Freire CCM, Queiroz JW, et al. Feeding preferences of Lutzomyia longipalpis (Diptera: Psychodidae), the sand fly vector, for Leishmania infantum (Kinetoplastida: Trypanosomatidae). J Med Entomol. 2014; 51(1): 237-44. however, there is a lack of information regarding their role as hosts/reservoirs of Leishmania.

The participation of other infected mammals, rather than dogs, in the transmission cycle of L. infantum in urban areas, has already been proposed for opossums (Didelphimorphia).8080. Santiago MEB, Vasconcelos RO, Fattori KR, Munari DP, Michelin AF, Lima VMF. An investigation of Leishmania spp. in Didelphis spp. from urban and peri-urban areas in Bauru (São Paulo, Brazil). Vet Parasitol. 2007; 150(4): 283-90. A total of eight sand fly species, within five genera (Lutzomyia, Nyssomyia, Pressatia, Psathyromyia, and Psychodopygus), have been found feeding on at least four species of opossums: Philander canus, Didelphis albiventris, Didelphis marsupialis, and Marmosops noctivagus.5050. de Araujo-Pereira T, de Pita-Pereira D, Baia-Gomes SM, Boité M, Silva F, Pinto IS, et al. An overview of the sandfly fauna (Diptera: Psychodidae) followed by the detection of Leishmania DNA and blood meal identification in the state of Acre, Amazonian Brazil. Mem Inst Oswaldo Cruz. 2020; 115: 1-17.,8181. Costa GD, Pereira Jr AM, Castro TS, de Paulo PFM, Ferreira GEM, Medeiros JF. Sand fly fauna and molecular detection of Leishmania species and blood meal sources in different rural environments in western Amazon. Acta Trop. 2021; 224: 106150.,8282. Oliveira-Pereira YN, Moraes JLP, Lorosa ES, Rebêlo JMM. Feeding preference of sand flies in the Amazon, Maranhão State, Brazil. Cad Saude Publica. 2008; 24(9): 2183-6. Of these, only D. albiventris and D. marsupialis are considered potential reservoirs of L. infantum and Leishmania guyanensis, respectively.8383. Sherlock IA, Miranda JC, Sadigursky M, Grimaldi Jr G. Natural infection of the opossum Didelphis albiventris (Marsupialia, Didelphidae) with Leishmania donovani, in Brazil. Mem Inst Oswaldo Cruz. 1984; 79(4): 511.,8484. Sherlock IA. Ecological interactions of visceral leishmaniasis in the State of Bahia, Brazil. Mem Inst Oswaldo Cruz. 1996; 91(6): 671-83.,8585. Arias JR, Naiff RD, Miles MA, De Souza AA. The opossum, Didelphis marsupialis (Marsupialia: Didelphidae), as a reservoir host of Leishmania braziliensis guyanensis in the Amazon Basin of Brazil. Trans R Soc Trop Med Hyg. 1981; 75(4): 537-41. However, other species of the genera Philander and Marmosops have also been suspected of sustaining Leishmania amazonensis and L. guyanensis infection, respectively.8686. Lainson R, Shaw JJ, Ready PD, Miles MA, Póvoa M. Leishmaniasis in Brazil: XVI. Isolation and identification of, Leishmania species from sandflies, wild mammals and man in north Pará State, with particular reference to L. braziliensis guyanensis causative agent of "pian-bois". Trans R Soc Trop Med Hyg. 1981; 75(4): 530-6.,8787. Quaresma PF, Rêgo FD, Botelho HA, da Silva SR, Moura AJ, Neto RGT, et al. Wild, synanthropic and domestic hosts of Leishmania in an endemic area of cutaneous leishmaniasis in Minas Gerais State, Brazil. Trans R Soc Trop Med Hyg. 2011; 105(10): 579-85. In general, opossums are synanthropic and are frequently found in peridomiciliary areas, where they may serve as a source of infection to vectors, such as Lu. longipalpis, Ny. intermedia, and Ny. whitmani, which have been found feeding on opossums.2727. Guimarães-E-Silva AS, Silva SO, Ribeiro da Silva RC, Pinheiro VCS, Rebêlo JMM, Melo MN, et al. Leishmania infection and blood food sources of phlebotomines in an area of Brazil endemic for visceral and tegumentary leishmaniasis. PLoS One. 2017; 12(8): e0179052.,3131. Baum M, Ribeiro M, Lorosa ES, Damasio GAC, de Castro EA. Eclectic feeding behavior of Lutzomyia (Nyssomyia) intermedia (Diptera, Psychodidae, Phlebotominae) in the transmission area of American cutaneous leishmaniasis, State of Parana, Brazil. Rev Soc Bras Med Trop. 2013; 46(5): 560-5.,3535. Afonso MMDS, Duarte R, Miranda JC, Caranha L, Rangel EF. Studies on the feeding habits of Lutzomyia (Lutzomyia) longipalpis (Lutz & Neiva, 1912) (Diptera: Psychodidae: Phlebotominae) populations from endemic areas of American Visceral Leishmaniasis in Northeastern Brazil. J Trop Med. 2012; 2012: 1-6.,8181. Costa GD, Pereira Jr AM, Castro TS, de Paulo PFM, Ferreira GEM, Medeiros JF. Sand fly fauna and molecular detection of Leishmania species and blood meal sources in different rural environments in western Amazon. Acta Trop. 2021; 224: 106150.,8888. Fonteles RS, Vasconcelos GCE, Azevêdo PCB, Lopes GN, Moraes JLP, Lorosa ES, et al. Blood feeding preference of Lutzomyia whitmani (Diptera, Psychodidae) in a transmission area for American cutaneous leishmaniasis in the State of Maranhão, Brazil. Rev Soc Bras Med Trop. 2009; 42(6): 647-50.,8989. Missawa NA, Lorosa ES, Dias ES. Feeding preference of Lutzomyia longipalpis (Lutz & Neiva, 1912) in transmission area of visceral leishmaniasis in Mato Grosso. Rev Soc Bras Med Trop. 2008; 41(4): 365-8.

The order Pilosa, a clade of xenarthran placental mammals, includes anteaters and sloths.9090. Möller-Krull M, Delsuc F, Churakov G, Marker C, Superina M, Brosius J, et al. Retroposed elements and their flanking regions resolve the evolutionary history of xenarthran mammals (armadillos, anteaters, and sloths). Mol Biol Evol. 2007; 24(11): 2573-82. Together with marsupials, these ancient Leishmania hosts are also native American fauna and possess a peculiar blood vessel structure that allows for an extremely low metabolic rate, conserving energy.9191. Bugge J. Cephalic arterial pattern in New World edentates and Old World pangolins with special reference to their phylogenetic relationships and taxonomy. Acta Anat (Basel). 1979; 105(1): 37-46. Regarding anteaters, only Tamandua tetradactyla, a putative host of L. amazonensis, L. guyanensis, and L. infantum,9292. Araújo A, Reinhard K, Ferreira LF, Pucu E, Chieffi PP. Paleoparasitology: the origin of human parasites. Arq Neuropsiquiatr. 2013; 71: 722-6.,9393. Lainson R, Shaw JJ, Povoa M. The importance of edentates (sloth and anteaters) as primary reservoirs of Leishmania braziliensis guyanensis, causative agent of "pian-bois" in north Brazil. Trans R Soc Trop Med Hyg. 1981; 75(4): 611-2.,9494. Mimori T, Grimaldi Jr G, Kreutzer RD, Gomez EA, McMahon-Pratt D, Tesh RB, et al. Identification, using isoenzyme electrophoresis and monoclonal antibodies, of Leishmania isolated from humans and wild animals of Ecuador. Am J Trop Med Hyg. 1989; 40(2): 154-8. has been reported as a blood source for Evandromyia, Nyssomyia, Psathyromyia, and Psychodopygus.4848. Pimentel AC, Uzcátegui YDS, de Lima ACS, Silveira FT, dos Santos TV, Ishikawa EAY. Blood Feeding Sources of Nyssomyia antunesi (Diptera: Psychodidae): A Suspected Vector of Leishmania (Kinetoplastida: Trypanosomatidae) in the Brazilian Amazon. J Med Entomol. 2022; 59(5): 1847-52.,5050. de Araujo-Pereira T, de Pita-Pereira D, Baia-Gomes SM, Boité M, Silva F, Pinto IS, et al. An overview of the sandfly fauna (Diptera: Psychodidae) followed by the detection of Leishmania DNA and blood meal identification in the state of Acre, Amazonian Brazil. Mem Inst Oswaldo Cruz. 2020; 115: 1-17.,5252. da Silva MS, Pereira Jr AM, Costa NVC, Costa GS, Rodrigues MMS, Medeiros JF, et al. Use of light emitting diodes (LEDs) are effective and useful for sand fly ecoepidemiology studies in an Amazonian environment. Acta Trop. 2022; 233: 106550.,5353. Pereira Jr AM, Souza ABN, Castro TS, da Silva MS, de Paulo PFM, Ferreira GEM, et al. Diversity, natural infection and blood meal sources of phlebotomine sandflies (Diptera, Psychodidae) in the western Brazilian Amazon. Mem Inst Oswaldo Cruz. 2019; 114(6): 1-9.,5454. Leão PO, Pereira Jr AM, de Paulo PFM, Carvalho LPC, Souza ABN, da Silva MS, et al. Vertical stratification of sand fly diversity in relation to natural infections of Leishmania sp. and blood-meal sources in Jamari National Forest, Rondonia State, Brazil. Parasit Vectors. 2020; 13(1): 422.,8181. Costa GD, Pereira Jr AM, Castro TS, de Paulo PFM, Ferreira GEM, Medeiros JF. Sand fly fauna and molecular detection of Leishmania species and blood meal sources in different rural environments in western Amazon. Acta Trop. 2021; 224: 106150. The two genera of sloths (Bradypus and Choloepus) have representatives considered putative reservoirs of Leishmania in Brazil. Bradypus tridactylus has been associated with L. shawi infections, and Choloepus didactylus has been associated with L. guyanensis in the Northern region.9595. Lainson R, Braga RR, De Souza AAA, Povoa MM, Ishikawa EAY, Silveira FT. Leishmania (Viannia) shawi sp. n., a parasite of monkeys, sloths and procyonids in Amazonian Brazil. Ann Parasitol Hum Comp. 1989; 64(3): 200-7. Moreover, C. hoffmanni has been associated with Leishmania colombiensis and Leishmania equatoriensis (syn = Endotrypanum colombiensis and Endotrypanum equatoriensis, respectively)6868. Espinosa OA, Serrano MG, Camargo EP, Teixeira MMG, Shaw JJ. An appraisal of the taxonomy and nomenclature of trypanosomatids presently classified as Leishmania and Endotrypanum. Parasitology. 2018; 145(4): 430-42. in South America.9696. Darling ST. The Endotrypanum of Hoffman's sloth. J Med Res. 1914; 31(2): 195.,9797. Shaw JJ. A possible vector of Endotrypanum schaudinni of the sloth Choloepus hoffmanni, in Panama. Nature. 1964; 201(4917): 417-8. Six sand fly species (Lutzomyia spathotrichia, Nyssomyia anduzei, Ny. umbratilis, Ny. antunesi, Pintomyia fiocruzi, and Trichopygomyia sp.) have been found feeding on sloths, and among these species, Ny. anduzei and Ny. umbratilis have been reported as naturally infected with Endotrypanum9797. Shaw JJ. A possible vector of Endotrypanum schaudinni of the sloth Choloepus hoffmanni, in Panama. Nature. 1964; 201(4917): 417-8.,9898. Rogers WO, Burnheim PF, Wirth DF. Detection of Leishmania within sand flies by kinetoplast DNA hybridization. Am J Trop Med Hyg. 1988; 39(5): 434-9. and may be considered putative vectors of these parasites.

Among primates, sand flies feeding on humans suggest anthropophilic tendencies, but their role as vectors remains debated. Notably, Micropygomyia trinidadensis and Sciopemyia sordellii, frequently associated with cold-blooded animals, have been found feeding on humans.2727. Guimarães-E-Silva AS, Silva SO, Ribeiro da Silva RC, Pinheiro VCS, Rebêlo JMM, Melo MN, et al. Leishmania infection and blood food sources of phlebotomines in an area of Brazil endemic for visceral and tegumentary leishmaniasis. PLoS One. 2017; 12(8): e0179052.,5050. de Araujo-Pereira T, de Pita-Pereira D, Baia-Gomes SM, Boité M, Silva F, Pinto IS, et al. An overview of the sandfly fauna (Diptera: Psychodidae) followed by the detection of Leishmania DNA and blood meal identification in the state of Acre, Amazonian Brazil. Mem Inst Oswaldo Cruz. 2020; 115: 1-17. Molecular analysis has shown the presence of L. amazonensis, L. infantum, and L. braziliensis DNA in Mi. trinidadensis9999. Carvalho-Silva R, Ribeiro-da-Silva RC, Cruz LNPD, Oliveira MS, Amoedo PM, Rebêlo JMM, et al. Predominance of Leishmania (Leishmania) amazonensis DNA in Lutzomyia longipalpis sand flies (Diptera: Psychodidae) from an endemic area for leishmaniasis in Northeastern Brazil. Rev Inst Med Trop São Paulo. 2022; 64: e32. and L. braziliensis, L. infantum, and L. naiffi in Sc. sordellii.100100. Pereira-Filho AA, Fonteles RS, Bandeira MCA, Moraes JLP, Rebêlo JMM, Melo MN. Molecular Identification of Leishmania spp. in Sand Flies (Diptera: Psychodidae: Phlebotominae) in the Lençóis Maranhenses National Park, Brazil. J Med Entomol. 2018; 55(4): 989-94.,101101. Da Silva YY, Sales KGDS, Miranda DEDO, Figueredo LA, Brandão-Filho SP, Dantas-Torres F. Detection of Leishmania DNA in sand flies (Diptera: Psychodidae) from a cutaneous Leishmaniasis outbreak area in Northeastern Brazil. J Med Entomol. 2020; 57(2): 529-33. Until today, the role of members of Micropygomyia and Scyopemia as vectors of Leishmania is debated. The presence of blood from Alouatta seniculus (Venezuelan red howler) and Plecturocebus bernhardi (zog-zog monkey) was also detected in Psychodopygus hirsutus, Ny. antunesi complex, and Ny. umbratilis; however, these vertebrates are not yet considered hosts/reservoirs of Leishmania.

Nine species of rodents belonging to six genera have been detected as blood sources for sand flies. Blood from three species of agouti (Dasyprocta azarae, Dasyprocta leporina, and Dasyprocta fuliginosa) has been detected in Lu. cruzi, Ny. antunesi, Psychodopygus davisi, and the Chagasi series of the Psychodopygus genus, with only D. azarae considered a putative host of L. infantum.7373. Roque ALR, Jansen AM. Wild and synanthropic reservoirs of Leishmania species in the Americas. Int J Parasitol Parasites Wildl. 2014; 3(3): 251-62. The lowland paca (Cuniculus paca) is considered a putative host of Leishmania lainsoni,102102. Silveira FT, Lainson R, Shaw JJ, Braga RR, Ishikawa EE, Souza AA. Cutaneous leishmaniasis in Amazonia: isolation of Leishmania (Viannia) lainsoni from the rodent Agouti paca (Rodentia: Dasyproctidae), in the state of Pará, Brazil. Rev Inst Med Trop São Paulo. 1991; 33(1): 18-22. and its blood was detected within Ny. antunesi,4848. Pimentel AC, Uzcátegui YDS, de Lima ACS, Silveira FT, dos Santos TV, Ishikawa EAY. Blood Feeding Sources of Nyssomyia antunesi (Diptera: Psychodidae): A Suspected Vector of Leishmania (Kinetoplastida: Trypanosomatidae) in the Brazilian Amazon. J Med Entomol. 2022; 59(5): 1847-52.Pintomyia serrana and Chagasi series of Psychodopygus genus.4949. Rodrigues BL, Costa GD, Shimabukuro PHF. Identification of bloodmeals from sand flies (Diptera: Psychodidae) collected in the Parque Nacional do Virua, State of Roraima, Brazil. J Med Entomol. 2021; 58(6): 2488-94.,5050. de Araujo-Pereira T, de Pita-Pereira D, Baia-Gomes SM, Boité M, Silva F, Pinto IS, et al. An overview of the sandfly fauna (Diptera: Psychodidae) followed by the detection of Leishmania DNA and blood meal identification in the state of Acre, Amazonian Brazil. Mem Inst Oswaldo Cruz. 2020; 115: 1-17. However, although Ny. antunesi has been found associated with several Leishmania (Viannia) parasites,5050. de Araujo-Pereira T, de Pita-Pereira D, Baia-Gomes SM, Boité M, Silva F, Pinto IS, et al. An overview of the sandfly fauna (Diptera: Psychodidae) followed by the detection of Leishmania DNA and blood meal identification in the state of Acre, Amazonian Brazil. Mem Inst Oswaldo Cruz. 2020; 115: 1-17.,5454. Leão PO, Pereira Jr AM, de Paulo PFM, Carvalho LPC, Souza ABN, da Silva MS, et al. Vertical stratification of sand fly diversity in relation to natural infections of Leishmania sp. and blood-meal sources in Jamari National Forest, Rondonia State, Brazil. Parasit Vectors. 2020; 13(1): 422.,103103. Carneiro ACG, de Souza EA, Barroso EP, de Ávila MM, Melchior LAK, Rocha RC, et al. Phlebotomine fauna (Diptera: Psychodidae) and infection by Leishmania spp. in forest fragments of a university campus, Western Amazon. J Med Entomol. 2023; 60(1): 218-23.,104104. Silveira FT, Ishikawa EAY, De Souza AAA, Lainson R. An outbreak of cutaneous leishmaniasis among soldiers in Belém, Pará State, Brazil, caused by Leishmania (Viannia) lindenbergi n. sp. A new leishmanial parasite of man in the Amazon region. Parasite. 2002; 9(1): 43-50. the presence of L. lainsoni has never been detected in these sand flies, only in Evandromyia evandroi, Lu. longipalpis, Ny. whitmani, Trichophoromyia brachipyga, and Trichophoromyia ubiquitalis,100100. Pereira-Filho AA, Fonteles RS, Bandeira MCA, Moraes JLP, Rebêlo JMM, Melo MN. Molecular Identification of Leishmania spp. in Sand Flies (Diptera: Psychodidae: Phlebotominae) in the Lençóis Maranhenses National Park, Brazil. J Med Entomol. 2018; 55(4): 989-94.,105105. Lainson R, Shaw JJ, Souza AAA, Silveira FT, Falqueto A. Further observations on Lutzomyia ubiquitalis (Psychodidae: Phlebotominae), the sandfly vector of Leishmania (Viannia) lainsoni. Mem Inst Oswaldo Cruz. 1992; 87(3): 437-9.,106106. Silveira FT, Souza AAA, Lainson R, Shaw JJ, Braga RR, Ishikawa EEA. Cutaneous leishmaniasis in the Amazon Region: natural infection of the sandfly Lutzomyia ubiquitalis (Psychodidae: Phlebotominae) by Leishmania (Viannia) lainsoni in Pará State, Brazil. Mem Inst Oswaldo Cruz. 1991; 86(1): 127-30.,107107. Pereira Jr AM, Teles CBG, dos Santos APA, Rodrigues MS, Marialva EF, Pessoa FAC, et al. Ecological aspects and molecular detection of Leishmania DNA Ross (Kinetoplastida: Trypanosomatidae) in phlebotomine sandflies (Diptera: Psychodidae) in Terra Firme and Várzea environments in the Middle Solimões Region, Amazonas State, Brazil. Parasit Vectors. 2015; 8(1): 1-11.,108108. Uzcátegui YDVS, Dos Santos TV, Silveira FT, Ramos PKS, Dos Santos EJM, Póvoa MM. Phlebotomines (Diptera: Psychodidae) from a urban park of Belém, Pará State, northern Brazil and potential implications in the transmission of American cutaneous leishmaniasis. J Med Entomol. 2020; 57(1): 281-8. highlighting the necessity of further studies to understand the transmission dynamics of this parasite. Coendu prehensilis (Brazilian porcupine), whose blood was detected in Pi. serrana and Ps. davisi,5050. de Araujo-Pereira T, de Pita-Pereira D, Baia-Gomes SM, Boité M, Silva F, Pinto IS, et al. An overview of the sandfly fauna (Diptera: Psychodidae) followed by the detection of Leishmania DNA and blood meal identification in the state of Acre, Amazonian Brazil. Mem Inst Oswaldo Cruz. 2020; 115: 1-17. is considered a putative host of L. infantum in Bolivia.109109. Le Pont F, Mouchet J, Desjeux P. Leishmaniasis in Bolivia. VII. Infection of sentinel porcupines (Coendou prehensilis, L.) by Leishmania (Le.) chagasi. Mem Inst Oswaldo Cruz. 1989; 84(4): 575.Leishmania hertigi [syn. Porcisia hertigi6868. Espinosa OA, Serrano MG, Camargo EP, Teixeira MMG, Shaw JJ. An appraisal of the taxonomy and nomenclature of trypanosomatids presently classified as Leishmania and Endotrypanum. Parasitology. 2018; 145(4): 430-42.] has been described from this vertebrate in Panama;110110. Herrer A, Telford Jr SR, Christensen HA. Enzootic cutaneous leishmaniasis in eastern Panama: I: Investigation of the infection among forest mammals. Ann Trop Med Parasitol. 1971; 65(3): 349-58. however, in Brazil, there is no data regarding its putative role in the transmission cycle of trypanosomatids. Rattus rattus (black rat) blood was found in Lu. spathotrichia, Ny. umbratilis, Pa. Shannoni complex, and Mg. migonei. This rodent is known to be a reservoir of L. braziliensis, and these sand flies should be investigated as putative vectors. Among these sand flies, at least Mg. migonei is considered a permissive vector, able to sustain late-stage infections of L. braziliensis.111111. Guimarães VCFV, Pruzinova K, Sadlova J, Volfova V, Myskova J, Brandão-Filho SP, et al. Lutzomyia migonei is a permissive vector competent for Leishmania infantum. Parasit Vectors. 2016; 9(1): 1-6. Blood from the house mouse (Mus musculus) was found within females of Chagasi series of Psychodopygus genus,4949. Rodrigues BL, Costa GD, Shimabukuro PHF. Identification of bloodmeals from sand flies (Diptera: Psychodidae) collected in the Parque Nacional do Virua, State of Roraima, Brazil. J Med Entomol. 2021; 58(6): 2488-94. and this vertebrate is considered a putative host of L. braziliensis in peridomestic areas.112112. de Freitas TPT, D'Andrea PS, de Paula DAJ, Nakazato L, Dutra V, Bonvicino CR, et al. Natural infection of Leishmania (Viannia) braziliensis in Mus musculus captured in Mato Grosso, Brazil. Vector-Borne and Zoonotic Diseases. 2012; 12(1): 81-3. In sylvatic areas, representatives of Proechimys seem to be hosts of L. amazonensis and L. guyanensis,8585. Arias JR, Naiff RD, Miles MA, De Souza AA. The opossum, Didelphis marsupialis (Marsupialia: Didelphidae), as a reservoir host of Leishmania braziliensis guyanensis in the Amazon Basin of Brazil. Trans R Soc Trop Med Hyg. 1981; 75(4): 537-41.,8686. Lainson R, Shaw JJ, Ready PD, Miles MA, Póvoa M. Leishmaniasis in Brazil: XVI. Isolation and identification of, Leishmania species from sandflies, wild mammals and man in north Pará State, with particular reference to L. braziliensis guyanensis causative agent of "pian-bois". Trans R Soc Trop Med Hyg. 1981; 75(4): 530-6. and blood from Proechimys gardneri was found in Bi. flaviscutellata,5252. da Silva MS, Pereira Jr AM, Costa NVC, Costa GS, Rodrigues MMS, Medeiros JF, et al. Use of light emitting diodes (LEDs) are effective and useful for sand fly ecoepidemiology studies in an Amazonian environment. Acta Trop. 2022; 233: 106550. the primary vector of L. amazonensis in Brazil,7474. Brazil RP, Rodrigues AAF, Andrade-Filho JD. Sand fly vectors of Leishmania in the Americas - A mini review. Entomol Ornithol Herpetol. 2015; 4(2): 1-4. evidencing a close relationship between hosts and vectors.

In conclusion, ecological inferences drawn from blood sources, in association with the presence of Leishmania in putative hosts, shed light on the complex dynamics of sand fly ecology. This underscores the importance of comprehensive studies to elucidate the role of sand flies in disease transmission cycles. By further investigating these ecological relationships, researchers can contribute to the development of more effective vector control strategies, ultimately helping to mitigate the burden of leishmaniasis in endemic regions.

Concluding remarks

In summary, this study underscores the critical importance of blood source identification in sand fly research to elucidate the intricate dynamics of vector-host-parasite interactions. The implementation of standardised methodologies, coupled with meticulous attention to storage conditions and the level of blood digestion in females, is paramount for advancing our comprehension of sand fly feeding ecology and its implications for Leishmania transmission dynamics. By confronting these methodological challenges head-on, future investigations may make significant strides in unravelling the nuanced roles of sand fly species as vectors, and by extension, their potential hosts/reservoirs, within the complex epidemiological network of Leishmania in Brazil.

REFERENCES

  • 1
    Chen L, Chen S, Kong P, Zhou L. Host competence, interspecific competition and vector preference interact to determine the vector-borne infection ecology. Front Ecol Evol. 2022; 10: 993844.
  • 2
    Álvarez-Hernández DA, Rivero-Zambrano L, Martínez-Juárez LA, García-Rodríguez-Arana R. Overcoming the global burden of neglected tropical diseases. Ther Adv Infect Dis. 2020; 7: 2049936120966449.
  • 3
    WHO - World Health Organization. Global leishmaniasis surveillance: 2019-2020, a baseline for the 2030 roadmap. Wkly Epidemiol Rec. 2021; 96(35): 401-19.
  • 4
    Caldart ET, Seva AP, Pinto-Ferreira F, Pachoal ATP, de Oliveira JS, Cortela IB, et al. American cutaneous leishmaniasis associated with degradation of native forest, regardless of economic, social and infrastructure vulnerability. Zoonoses Public Health. 2021; 68(4): 327-43.
  • 5
    Rodrigues MGA, Sousa JDB, Dias ÁLB, Monteiro WM, Sampaio VS. The role of deforestation on American cutaneous leishmaniasis incidence: spatial-temporal distribution, environmental and socioeconomic factors associated in the Brazilian Amazon. Trop Med Int Health. 2019; 24(3): 348-55.
  • 6
    de Carvalho BM, Perez LP, de Oliveira BFA, Jacobson LSV, Horta MA, Sobral A, et al. Vector-borne diseases in Brazil: climate change and future warming scenarios. SiD. 2020; 11(3): 361-404.
  • 7
    Mikery-Pacheco OF, Moo-Llanes DA, Rebollar-Téllez EA, Castillo-Vera A. Influence of climate change on leishmaniasis transmission in Latin America and the research status in Mexico. Rev Biomed. 2023; 34(1): 44-58.
  • 8
    Eroglu F, Ozgoztasi O. The increase in neglected cutaneous leishmaniasis in Gaziantep province of Turkey after mass human migration. Acta Trop. 2019; 192: 138-43.
  • 9
    Kumar A, Saurabh S, Jamil S, Kumar V. Intensely clustered outbreak of visceral leishmaniasis (kala-azar) in a setting of seasonal migration in a village of Bihar, India. BMC Infect Dis. 2020; 20: 1-13.
  • 10
    Cota G, Erber AC, Schernhammer E, Simões TC. Inequalities of visceral leishmaniasis case-fatality in Brazil: a multilevel modeling considering space, time, individual and contextual factors. PLoS Negl Trop Dis. 2021; 15(7): e0009567.
  • 11
    Schlein Y, Jacobson RL. Sugar meals and longevity of the sandfly Phlebotomus papatasi in an arid focus of Leishmania major in the Jordan Valley. Med Vet Entomol. 1999; 13(1): 65-71.
  • 12
    Noguera P, Rondón M, Nieves E. Effect of blood source on the survival and fecundity of the sandfly Lutzomyia ovallesi Ortiz (Diptera: Psychodidae), vector of Leishmania. Biomedica. 2006; 26: 57-63.
  • 13
    Moraes CS, Aguiar-Martins K, Costa SG, Bates PA, Dillon RJ, Genta FA. Second blood meal by female Lutzomyia longipalpis: enhancement by oviposition and its effects on digestion, longevity, and Leishmania infection. Biomed Res Int. 2018; 2018: 2472508.
  • 14
    Sant'Anna MRV, Nascimento A, Alexander B, Dilger E, Cavalcante RR, Diaz-Albiter HM, et al. Chicken blood provides a suitable meal for the sand fly Lutzomyia longipalpis and does not inhibit Leishmania development in the gut. Parasit Vectors. 2010; 3(1): 1-11.
  • 15
    Beattie L, Kaye PM. Leishmania-host interactions: what has imaging taught us? Cell Microbiol. 2011; 13(11): 1659-67.
  • 16
    Posada-López L, Velez-Mira A, Cantillo O, Castillo-Castañeda A, Ramírez JD, Galati EAB, et al. Ecological interactions of sand flies, hosts, and Leishmania panamensis in an endemic area of cutaneous leishmaniasis in Colombia. PLoS Negl Trop Dis. 2023; 17(5): e0011316.
  • 17
    Deeks JJ, Bossuyt PM, Leeflang MM, Takwoingi Y. Cochrane handbook for systematic reviews of diagnostic test accuracy. John Wiley & Sons; 2023.
  • 18
    Tong A, Flemming K, McInnes E, Oliver S, Craig J. Enhancing transparency in reporting the synthesis of qualitative research: ENTREQ. BMC Med Res Methodol. 2012; 12(1): 1-8.
  • 19
    Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021; 372: n71.
  • 20
    Ouzzani M, Hammady H, Fedorowicz Z, Elmagarmid A. Rayyan-a web and mobile app for systematic reviews. Syst Rev. 2016; 5(1): 1-10.
  • 21
    Galati EAB. Phlebotominae (Diptera, Psychodidae): classification, morphology and terminology of adults and identification of American Taxa. In: Rangel E, Shaw J, editors. Brazilian sand flies: biology, taxonomy, medical importance and control. 1st ed. Springer International Publishing; 2018. p. 9-212.
  • 22
    Marcondes CB. A proposal of generic and subgeneric abbreviations for phlebtomine sandflies (Diptera: Psychodidae: Phelbotomina) of the world. Entomol News. 2007; 118(4): 351-6.
  • 23
    Alves VR, de Freitas RA, Barrett T. Lutzomyia maruaga (Diptera: Psychodidae), a new bat-cave sand fly from Amazonas, Brazil. Mem Inst Oswaldo Cruz. 2008; 103(3): 251-3.
  • 24
    Costa JCR, Marchi GH, Santos CS, Andrade MCM, Chaves Jr SP, Silva MAN, et al. First molecular evidence of frogs as a food source for sand flies (Diptera: Phlebotominae) in Brazilian caves. Parasitol Res. 2021; 120(5): 1571-82.
  • 25
    Baum M, de Castro EA, Pinto MC, Goulart TM, Baura W, Klisiowicz DD, et al. Molecular detection of the blood meal source of sand flies (Diptera: Psychodidae) in a transmission area of American cutaneous leishmaniasis, Parana State, Brazil. Acta Trop. 2015; 143: 8-12.
  • 26
    Quaresma PF, Carvalho GML, Ramos MCNF, Andrade Filho JD. Natural Leishmania sp. reservoirs and phlebotomine sandfly food source identification in Ibitipoca State Park, Minas Gerais, Brazil. Mem Inst Oswaldo Cruz. 2012; 107(4): 480-5.
  • 27
    Guimarães-E-Silva AS, Silva SO, Ribeiro da Silva RC, Pinheiro VCS, Rebêlo JMM, Melo MN, et al. Leishmania infection and blood food sources of phlebotomines in an area of Brazil endemic for visceral and tegumentary leishmaniasis. PLoS One. 2017; 12(8): e0179052.
  • 28
    Benchimol JL, Gualandi FC, Barreto DCS, Pinheiro LA. Leishmaniasis: historical configuration in Brazil with an emphasis on the visceral disease, from the 1930s to the 1960s. Bol Mus Para Emílio Goeldi Cienc Hum. 2019; 14: 611-26.
  • 29
    Ready PD. Biology of phlebotomine sand flies as vectors of disease agents. Annu Rev Entomol. 2013; 58: 227-50.
  • 30
    Killick-Kendrick R. Phlebotomine vectors of the leishmaniases: a review. Med Vet Entomol. 1990; 4(1): 1-24.
  • 31
    Baum M, Ribeiro M, Lorosa ES, Damasio GAC, de Castro EA. Eclectic feeding behavior of Lutzomyia (Nyssomyia) intermedia (Diptera, Psychodidae, Phlebotominae) in the transmission area of American cutaneous leishmaniasis, State of Parana, Brazil. Rev Soc Bras Med Trop. 2013; 46(5): 560-5.
  • 32
    Forattini OP. Entomologia médica: Psychodidae, Phlebotominae, leishmanioses, bartonelose. São Paulo: Ed. Edgard Blücher / Ed. Univ. São Paulo; 1973. v. 4, 658pp.
  • 33
    de Oliveira EF, Oshiro ET, Fernandes WS, Ferreira AMT, de Oliveira AG, Galati EAB. Vector competence of Lutzomyia cruzi naturally demonstrated for Leishmania infantum and suspected for Leishmania amazonensis. Am J Trop Med Hyg. 2017; 96(1): 178-81.
  • 34
    Svobodová M, Sádlová J, Chang KP, Volf P. Distribution and feeding preference of the sand flies Phlebotomus sergenti and P. papatasi in a cutaneous leishmaniasis focus in Sanliurfa, Turkey. Am J Trop Med Hyg. 2003; 68(1): 6-9.
  • 35
    Afonso MMDS, Duarte R, Miranda JC, Caranha L, Rangel EF. Studies on the feeding habits of Lutzomyia (Lutzomyia) longipalpis (Lutz & Neiva, 1912) (Diptera: Psychodidae: Phlebotominae) populations from endemic areas of American Visceral Leishmaniasis in Northeastern Brazil. J Trop Med. 2012; 2012: 1-6.
  • 36
    de Brito VN, de Almeida ABPF, Nakazato L, Duarte R, Souza CO, Sousa VRF. Phlebotomine fauna, natural infection rate and feeding habits of Lutzomyia cruzi in Jaciara, state of Mato Grosso, Brazil. Mem Inst Oswaldo Cruz. 2014; 109(7): 899-904.
  • 37
    Nery LCR, Lorosa ES, Franco AMR. Feeding preference of the sand flies Lutzomyia umbratilis and L. spathotrichia (Diptera: Psychodidae, Phlebotominae) in an urban forest patch in the city of Manaus, Amazonas, Brazil. Mem Inst Oswaldo Cruz. 2004; 99(6): 571-4.
  • 38
    Neitzke-Abreu HC, Andrade GMC, de Almeida PS, Ribeiro GC, Ribeiro TA, Barrios D, et al. Natural infection of Lutzomyia longipalpis (Lutz & Neiva, 1912) by Leishmania infantum in a municipality with a high incidence of visceral leishmaniasis in the Brazilian Midwest. Rev Soc Bras Med Trop. 2023; 56: e0259-2023.
  • 39
    Sant'Anna MR V, Jones NG, Hindley JA, Mendes-Sousa AF, Dillon RJ, Cavalcante RR, et al. Blood meal identification and parasite detection in laboratory-fed and field-captured Lutzomyia longipalpis by PCR using FTA databasing paper. Acta Trop. 2008; 107(3): 230-7.
  • 40
    Chaniotis BN. The biology of California phlebotomus (Diptera: Psychodidae) under laboratory conditions. J Med Entomol. 1967; 4(2): 221-33.
  • 41
    Chacon-Cortes D, Griffiths LR. Methods for extracting genomic DNA from whole blood samples: current perspectives. J Bio Sci Appl Med. 2014; 2: 1-9.
  • 42
    Depaquit J, Ferte H, Léger N, Killick-Kendrick R, Rioux J, Killick-Kendrick M, et al. Molecular systematics of the phlebotomine sandflies of the subgenus Paraphlebotomus (Diptera, Psychodidae, Phlebotomus) based on ITS2 rDNA sequences. Hypotheses of dispersion and speciation. Insect Mol Biol. 2000; 9(3): 293-300.
  • 43
    Holland NT, Smith MT, Eskenazi B, Bastaki M. Biological sample collection and processing for molecular epidemiological studies. Mutat Res. 2003; 543(3): 217-34.
  • 44
    Nederhand RJ, Droog S, Kluft C, Simoons ML, De Maat MPM; Investigators of the EUROPA trial. Logistics and quality control for DNA sampling in large multicenter studies. J Thromb Haemost. 2003; 1(5): 987-91.
  • 45
    Richardson AJ, Narendran N, Guymer RH, Vu H, Baird PN. Blood storage at 4 C -factors involved in DNA yield and quality. J Lab Clin Med. 2006; 147(6): 290-4.
  • 46
    Steinberg KK, Sanderlin KK, Ou CY, Hannon WH, McQuillan G, Sampson EJ. DNA banking in epidemiologic studies. Epidemiol Rev. 1997; 19(1): 156-62.
  • 47
    AlRokayan SAH. Effect of storage temperature on the quality and quantity of DNA extracted from blood. Pak J Biol Sci. 2000; 3(3): 392-4.
  • 48
    Pimentel AC, Uzcátegui YDS, de Lima ACS, Silveira FT, dos Santos TV, Ishikawa EAY. Blood Feeding Sources of Nyssomyia antunesi (Diptera: Psychodidae): A Suspected Vector of Leishmania (Kinetoplastida: Trypanosomatidae) in the Brazilian Amazon. J Med Entomol. 2022; 59(5): 1847-52.
  • 49
    Rodrigues BL, Costa GD, Shimabukuro PHF. Identification of bloodmeals from sand flies (Diptera: Psychodidae) collected in the Parque Nacional do Virua, State of Roraima, Brazil. J Med Entomol. 2021; 58(6): 2488-94.
  • 50
    de Araujo-Pereira T, de Pita-Pereira D, Baia-Gomes SM, Boité M, Silva F, Pinto IS, et al. An overview of the sandfly fauna (Diptera: Psychodidae) followed by the detection of Leishmania DNA and blood meal identification in the state of Acre, Amazonian Brazil. Mem Inst Oswaldo Cruz. 2020; 115: 1-17.
  • 51
    de Ávila MM, Brilhante AF, de Souza CF, Bevilacqua PD, Galati EAB, Brazil RP, et al. Ecology, feeding and natural infection by Leishmania spp. of phlebotomine sand flies in an area of high incidence of American tegumentary leishmaniasis in the municipality of Rio Branco, Acre, Brazil. Parasit Vectors. 2018; 11: 64.
  • 52
    da Silva MS, Pereira Jr AM, Costa NVC, Costa GS, Rodrigues MMS, Medeiros JF, et al. Use of light emitting diodes (LEDs) are effective and useful for sand fly ecoepidemiology studies in an Amazonian environment. Acta Trop. 2022; 233: 106550.
  • 53
    Pereira Jr AM, Souza ABN, Castro TS, da Silva MS, de Paulo PFM, Ferreira GEM, et al. Diversity, natural infection and blood meal sources of phlebotomine sandflies (Diptera, Psychodidae) in the western Brazilian Amazon. Mem Inst Oswaldo Cruz. 2019; 114(6): 1-9.
  • 54
    Leão PO, Pereira Jr AM, de Paulo PFM, Carvalho LPC, Souza ABN, da Silva MS, et al. Vertical stratification of sand fly diversity in relation to natural infections of Leishmania sp. and blood-meal sources in Jamari National Forest, Rondonia State, Brazil. Parasit Vectors. 2020; 13(1): 422.
  • 55
    Meyer T, Monge PK, Sakshaug J. Storage of blood samples containing alcohol. Acta Pharmacol Toxicol (Copenh). 1979; 45(4): 282-6.
  • 56
    Carvalho GML, Rêgo FD, Tanure A, Silva ACP, Dias TA, Paz GF, et al. Bloodmeal identification in field-collected sand flies from Casa Branca, Brazil, using the cytochrome b PCR Method. J Med Entomol. 2017; 54(4): 1049-54.
  • 57
    Lovelock JE, Bishop MWH. Prevention of freezing damage to living cells by dimethyl sulphoxide. Nature. 1959; 183(4672): 1394-5.
  • 58
    Belo VS, Werneck GL, Barbosa DS, Simões TC, Nascimento BWL, da Silva ES, et al. Factors associated with visceral leishmaniasis in the Americas: a systematic review and meta-analysis. PLoS Negl Trop Dis. 2013; 7(4): e2182.
  • 59
    Bern C, Courtenay O, Alvar J. Of cattle, sand flies and men: a systematic review of risk factor analyses for South Asian visceral leishmaniasis and implications for elimination. PLoS Negl Trop Dis. 2010; 4(2): e599.
  • 60
    Lobsiger L, Müller N, Schweizer T, Frey CF, Wiederkehr D, Zumkehr B, et al. An autochthonous case of cutaneous bovine leishmaniasis in Switzerland. Vet Parasitol. 2010; 169(3-4): 408-14.
  • 61
    Mazza S. Leishmaniasis cutánea en el caballo y nueva observación de la misma en el perro. Bol Inst Clin Quir. 1927; 3: 462-4.
  • 62
    Aguilar CM, Rangel EF, Grimaldi Filho G, Momem H. Human, canine and equine leishmaniasis caused by Leishmania braziliensis braziliensis in an endemic area in the State of Rio de Janeiro. Mem Inst Oswaldo Cruz. 1987; 82(1): 143.
  • 63
    Falqueto A, Varejão JBM, Sessa PA. Cutaneous leishmaniasis in a horse (Equus caballus) from endemic area in the state of Espírito Santo, Brazil. Mem Inst Oswaldo Cruz.1987; 82(3): 443.
  • 64
    Vexenat JA, Barretto AC, Rosa ACO, Sales CC, Magalhães AV. [Natural infection of Equus asinus by Leishmania braziliensis braziliensis - Bahia, Brazil]. Mem Inst Oswaldo Cruz. 1986; 81(2): 237-8.
  • 65
    Soares IR, Silva SO, Moreira FM, Prado LG, Fantini P, Maranhão RPA, et al. First evidence of autochthonous cases of Leishmania (Leishmania) infantum in horse (Equus caballus) in the Americas and mixed infection of Leishmania infantum and Leishmania (Viannia) braziliensis. Vet Parasitol. 2013; 197(3-4): 665-9.
  • 66
    Leonel JAF, Tannihão B, Arantes JA, Vioti G, Benassi JC, Brandi RA, et al. Detection of Leishmania infantum DNA in blood samples of horses (Equus caballus) and donkeys (Equus asinus) by PCR. Rev Inst Med Trop São Paulo. 2021; 63.
  • 67
    Benassi JC, Benvenga GU, Ferreira HL, Soares RM, Silva DT, Pereira VF, et al. Molecular and serological detection of Leishmania spp. in horses from an endemic area for canine visceral leishmaniasis in southeastern Brazil. Pes Vet Bras. 2018; 38(6): 1058-63.
  • 68
    Espinosa OA, Serrano MG, Camargo EP, Teixeira MMG, Shaw JJ. An appraisal of the taxonomy and nomenclature of trypanosomatids presently classified as Leishmania and Endotrypanum. Parasitology. 2018; 145(4): 430-42.
  • 69
    Reuss SM, Dunbar MD, Mays MBC, Owen JL, Mallicote MF, Archer LL, et al. Autochthonous Leishmania siamensis in horse, Florida, USA. Emerg Infect Dis. 2012; 18(9): 1545.
  • 70
    Mendes Junior AAV, Filgueira CPB, Miranda LFC, de Almeida AB, Cantanhêde LM, Fagundes A, et al. First report of Leishmania (Mundinia) martiniquensis in South American territory and confirmation of Leishbunyavirus infecting this parasite in a mare. Mem Inst Oswaldo Cruz. 2023; 118: 1-7.
  • 71
    Gontijo CMF, Melo MN. Leishmaniose visceral no Brasil: quadro atual, desafios e perspectivas. Rev Bras Epidemiol. 2004; 7(3): 338-49.
  • 72
    Santos NS, Pinho FA, Hlavac NRC, Nunes TL, Almeida NR, Solcà MS, et al. Feline leishmaniasis caused by Leishmania infantum: parasite sequencing, seropositivity, and clinical characterization in an endemic area from Brazil. Front Vet Sci. 2021; 8: 1-12.
  • 73
    Roque ALR, Jansen AM. Wild and synanthropic reservoirs of Leishmania species in the Americas. Int J Parasitol Parasites Wildl. 2014; 3(3): 251-62.
  • 74
    Brazil RP, Rodrigues AAF, Andrade-Filho JD. Sand fly vectors of Leishmania in the Americas - A mini review. Entomol Ornithol Herpetol. 2015; 4(2): 1-4.
  • 75
    Akhoundi M, Kuhls K, Cannet A, Votýpka J, Marty P, Delaunay P, et al. A historical overview of the classification, evolution, and dispersion of Leishmania parasites and sandflies. PLoS Negl Trop Dis. 2016; 10(3): e0004349.
  • 76
    Naiff RD, Freitas RA, Naiff MF, Arias JR, Barret TV, Momen H, et al. Epidemiological and nosological aspects of Leishmania naiffi Lainson & Shaw, 1989. Mem Inst Oswaldo Cruz. 1991; 86(3): 317-21.
  • 77
    Lainson R, Shaw JJ. Leishmania (Viannia) naiffi sp. n., a parasite of the armadillo, Dasypus novemcinctus (L.) in Amazonian Brazil. Ann Parasitol Hum Comp. 1989; 64(1): 3-9.
  • 78
    Torchitte APA, Pereira Jr AM, Paulo PFM, Costa GS, Castro TS, Ferreira RGM, et al. Identification of sand flies (Diptera: Psychodidae) and blood meal sources in periurban areas of Ji-Paraná municipality, Western Brazilian Amazon. Braz J Biol. 2021; 81(1): 225-7.
  • 79
    Macedo-Silva VP, Martins DRA, De Queiroz PVS, Pinheiro MPG, Freire CCM, Queiroz JW, et al. Feeding preferences of Lutzomyia longipalpis (Diptera: Psychodidae), the sand fly vector, for Leishmania infantum (Kinetoplastida: Trypanosomatidae). J Med Entomol. 2014; 51(1): 237-44.
  • 80
    Santiago MEB, Vasconcelos RO, Fattori KR, Munari DP, Michelin AF, Lima VMF. An investigation of Leishmania spp. in Didelphis spp. from urban and peri-urban areas in Bauru (São Paulo, Brazil). Vet Parasitol. 2007; 150(4): 283-90.
  • 81
    Costa GD, Pereira Jr AM, Castro TS, de Paulo PFM, Ferreira GEM, Medeiros JF. Sand fly fauna and molecular detection of Leishmania species and blood meal sources in different rural environments in western Amazon. Acta Trop. 2021; 224: 106150.
  • 82
    Oliveira-Pereira YN, Moraes JLP, Lorosa ES, Rebêlo JMM. Feeding preference of sand flies in the Amazon, Maranhão State, Brazil. Cad Saude Publica. 2008; 24(9): 2183-6.
  • 83
    Sherlock IA, Miranda JC, Sadigursky M, Grimaldi Jr G. Natural infection of the opossum Didelphis albiventris (Marsupialia, Didelphidae) with Leishmania donovani, in Brazil. Mem Inst Oswaldo Cruz. 1984; 79(4): 511.
  • 84
    Sherlock IA. Ecological interactions of visceral leishmaniasis in the State of Bahia, Brazil. Mem Inst Oswaldo Cruz. 1996; 91(6): 671-83.
  • 85
    Arias JR, Naiff RD, Miles MA, De Souza AA. The opossum, Didelphis marsupialis (Marsupialia: Didelphidae), as a reservoir host of Leishmania braziliensis guyanensis in the Amazon Basin of Brazil. Trans R Soc Trop Med Hyg. 1981; 75(4): 537-41.
  • 86
    Lainson R, Shaw JJ, Ready PD, Miles MA, Póvoa M. Leishmaniasis in Brazil: XVI. Isolation and identification of, Leishmania species from sandflies, wild mammals and man in north Pará State, with particular reference to L. braziliensis guyanensis causative agent of "pian-bois". Trans R Soc Trop Med Hyg. 1981; 75(4): 530-6.
  • 87
    Quaresma PF, Rêgo FD, Botelho HA, da Silva SR, Moura AJ, Neto RGT, et al. Wild, synanthropic and domestic hosts of Leishmania in an endemic area of cutaneous leishmaniasis in Minas Gerais State, Brazil. Trans R Soc Trop Med Hyg. 2011; 105(10): 579-85.
  • 88
    Fonteles RS, Vasconcelos GCE, Azevêdo PCB, Lopes GN, Moraes JLP, Lorosa ES, et al. Blood feeding preference of Lutzomyia whitmani (Diptera, Psychodidae) in a transmission area for American cutaneous leishmaniasis in the State of Maranhão, Brazil. Rev Soc Bras Med Trop. 2009; 42(6): 647-50.
  • 89
    Missawa NA, Lorosa ES, Dias ES. Feeding preference of Lutzomyia longipalpis (Lutz & Neiva, 1912) in transmission area of visceral leishmaniasis in Mato Grosso. Rev Soc Bras Med Trop. 2008; 41(4): 365-8.
  • 90
    Möller-Krull M, Delsuc F, Churakov G, Marker C, Superina M, Brosius J, et al. Retroposed elements and their flanking regions resolve the evolutionary history of xenarthran mammals (armadillos, anteaters, and sloths). Mol Biol Evol. 2007; 24(11): 2573-82.
  • 91
    Bugge J. Cephalic arterial pattern in New World edentates and Old World pangolins with special reference to their phylogenetic relationships and taxonomy. Acta Anat (Basel). 1979; 105(1): 37-46.
  • 92
    Araújo A, Reinhard K, Ferreira LF, Pucu E, Chieffi PP. Paleoparasitology: the origin of human parasites. Arq Neuropsiquiatr. 2013; 71: 722-6.
  • 93
    Lainson R, Shaw JJ, Povoa M. The importance of edentates (sloth and anteaters) as primary reservoirs of Leishmania braziliensis guyanensis, causative agent of "pian-bois" in north Brazil. Trans R Soc Trop Med Hyg. 1981; 75(4): 611-2.
  • 94
    Mimori T, Grimaldi Jr G, Kreutzer RD, Gomez EA, McMahon-Pratt D, Tesh RB, et al. Identification, using isoenzyme electrophoresis and monoclonal antibodies, of Leishmania isolated from humans and wild animals of Ecuador. Am J Trop Med Hyg. 1989; 40(2): 154-8.
  • 95
    Lainson R, Braga RR, De Souza AAA, Povoa MM, Ishikawa EAY, Silveira FT. Leishmania (Viannia) shawi sp. n., a parasite of monkeys, sloths and procyonids in Amazonian Brazil. Ann Parasitol Hum Comp. 1989; 64(3): 200-7.
  • 96
    Darling ST. The Endotrypanum of Hoffman's sloth. J Med Res. 1914; 31(2): 195.
  • 97
    Shaw JJ. A possible vector of Endotrypanum schaudinni of the sloth Choloepus hoffmanni, in Panama. Nature. 1964; 201(4917): 417-8.
  • 98
    Rogers WO, Burnheim PF, Wirth DF. Detection of Leishmania within sand flies by kinetoplast DNA hybridization. Am J Trop Med Hyg. 1988; 39(5): 434-9.
  • 99
    Carvalho-Silva R, Ribeiro-da-Silva RC, Cruz LNPD, Oliveira MS, Amoedo PM, Rebêlo JMM, et al. Predominance of Leishmania (Leishmania) amazonensis DNA in Lutzomyia longipalpis sand flies (Diptera: Psychodidae) from an endemic area for leishmaniasis in Northeastern Brazil. Rev Inst Med Trop São Paulo. 2022; 64: e32.
  • 100
    Pereira-Filho AA, Fonteles RS, Bandeira MCA, Moraes JLP, Rebêlo JMM, Melo MN. Molecular Identification of Leishmania spp. in Sand Flies (Diptera: Psychodidae: Phlebotominae) in the Lençóis Maranhenses National Park, Brazil. J Med Entomol. 2018; 55(4): 989-94.
  • 101
    Da Silva YY, Sales KGDS, Miranda DEDO, Figueredo LA, Brandão-Filho SP, Dantas-Torres F. Detection of Leishmania DNA in sand flies (Diptera: Psychodidae) from a cutaneous Leishmaniasis outbreak area in Northeastern Brazil. J Med Entomol. 2020; 57(2): 529-33.
  • 102
    Silveira FT, Lainson R, Shaw JJ, Braga RR, Ishikawa EE, Souza AA. Cutaneous leishmaniasis in Amazonia: isolation of Leishmania (Viannia) lainsoni from the rodent Agouti paca (Rodentia: Dasyproctidae), in the state of Pará, Brazil. Rev Inst Med Trop São Paulo. 1991; 33(1): 18-22.
  • 103
    Carneiro ACG, de Souza EA, Barroso EP, de Ávila MM, Melchior LAK, Rocha RC, et al. Phlebotomine fauna (Diptera: Psychodidae) and infection by Leishmania spp. in forest fragments of a university campus, Western Amazon. J Med Entomol. 2023; 60(1): 218-23.
  • 104
    Silveira FT, Ishikawa EAY, De Souza AAA, Lainson R. An outbreak of cutaneous leishmaniasis among soldiers in Belém, Pará State, Brazil, caused by Leishmania (Viannia) lindenbergi n. sp. A new leishmanial parasite of man in the Amazon region. Parasite. 2002; 9(1): 43-50.
  • 105
    Lainson R, Shaw JJ, Souza AAA, Silveira FT, Falqueto A. Further observations on Lutzomyia ubiquitalis (Psychodidae: Phlebotominae), the sandfly vector of Leishmania (Viannia) lainsoni. Mem Inst Oswaldo Cruz. 1992; 87(3): 437-9.
  • 106
    Silveira FT, Souza AAA, Lainson R, Shaw JJ, Braga RR, Ishikawa EEA. Cutaneous leishmaniasis in the Amazon Region: natural infection of the sandfly Lutzomyia ubiquitalis (Psychodidae: Phlebotominae) by Leishmania (Viannia) lainsoni in Pará State, Brazil. Mem Inst Oswaldo Cruz. 1991; 86(1): 127-30.
  • 107
    Pereira Jr AM, Teles CBG, dos Santos APA, Rodrigues MS, Marialva EF, Pessoa FAC, et al. Ecological aspects and molecular detection of Leishmania DNA Ross (Kinetoplastida: Trypanosomatidae) in phlebotomine sandflies (Diptera: Psychodidae) in Terra Firme and Várzea environments in the Middle Solimões Region, Amazonas State, Brazil. Parasit Vectors. 2015; 8(1): 1-11.
  • 108
    Uzcátegui YDVS, Dos Santos TV, Silveira FT, Ramos PKS, Dos Santos EJM, Póvoa MM. Phlebotomines (Diptera: Psychodidae) from a urban park of Belém, Pará State, northern Brazil and potential implications in the transmission of American cutaneous leishmaniasis. J Med Entomol. 2020; 57(1): 281-8.
  • 109
    Le Pont F, Mouchet J, Desjeux P. Leishmaniasis in Bolivia. VII. Infection of sentinel porcupines (Coendou prehensilis, L.) by Leishmania (Le.) chagasi. Mem Inst Oswaldo Cruz. 1989; 84(4): 575.
  • 110
    Herrer A, Telford Jr SR, Christensen HA. Enzootic cutaneous leishmaniasis in eastern Panama: I: Investigation of the infection among forest mammals. Ann Trop Med Parasitol. 1971; 65(3): 349-58.
  • 111
    Guimarães VCFV, Pruzinova K, Sadlova J, Volfova V, Myskova J, Brandão-Filho SP, et al. Lutzomyia migonei is a permissive vector competent for Leishmania infantum. Parasit Vectors. 2016; 9(1): 1-6.
  • 112
    de Freitas TPT, D'Andrea PS, de Paula DAJ, Nakazato L, Dutra V, Bonvicino CR, et al. Natural infection of Leishmania (Viannia) braziliensis in Mus musculus captured in Mato Grosso, Brazil. Vector-Borne and Zoonotic Diseases. 2012; 12(1): 81-3.
  • 113
    Afonso MMDS, Gomes AC, Meneses CRV, Rangel EF. Studies on the feeding habits of Lutzomyia (N.) intermedia (Diptera, Psychodidae), vector of cutaneous leishmaniasis in Brazil. Cad Saude Publica. 2005; 21(6): 1816-20.
  • 114
    Barata RA, França-Silva JC, Mayrink W, Silva JC, Prata A, Lorosa ES, et al. Aspects of the ecology and behaviour of phlebotomines in endemic area for visceral leishmaniasis in State of Minas Gerais. Rev Soc Bras Med Trop. 2005; 38(5): 421-5.
  • 115
    Christensen HA, Arias JR, de Vasquez AM, de Freitas RA. Hosts of sandfly vectors of Leishmania braziliensis guyanensis in the central Amazon of Brazil. Am J Trop Med Hyg. 1982; 31(2): 239-42.
  • 116
    Dutra-Rêgo F, Lima MA, Almeida GLP, de Almeida PS, Bastos GKSV, Alexandre LVN, et al. Molecular detection of Leishmania and blood meal analysis in sand flies from Corumbá, Mato Grosso do Sul, Brazil. Acta Trop. 2023; 245: 106961.
  • 117
    Fonteles RS, Pereira AA, Moraes JLP, Pereira SRF, Rodrigues BL, Rebêlo JMM. Detection of Leishmania DNA and blood meal identification in sand flies (Diptera: Psychodidae) from Lençois Maranhenses National Park Region, Brazil. J Med Entomol. 2018; 55(2): 445-51.
  • 118
    Marassá AM, Consales CA, Galati EAB, Nunes VLB. Identificação do sangue ingerido por Lutzomyia (Lutzomyia) longipalpis (Lutz & Neiva, 1912) e Lutzomyia (Lutzomyia) almerioi (Galati & Nunes, 1999) pela técnica imunoenzimática do ELISA de captura, no sistema avidina-biotina. Rev Soc Bras Med Trop. 2006; 39(2): 183-6.
  • 119
    Marassá AM, Galati EAB, Bergamaschi DP, Consales CA. Blood feeding patterns of Nyssomyia intermedia and Nyssomyia neivai (Diptera, Psychodidae) in a cutaneous leishmaniasis endemic area of the Ribeira Valley, State of Sao Paulo, Brazil. Rev Soc Bras Med Trop. 2013; 46(5): 547-54.
  • 120
    de Oliveira AG, Marassá AM, Consales CA, Dorval MEC, Fernandes CE, de Oliveira GR, et al. Observations on the feeding habits of Lutzomyia longipalpis (Lutz & Neiva, 1912) (Diptera: Psychodidae: Phlebotominae) in Campo Grande, an endemic area of visceral leishmaniasis in Mato Grosso do Sul, Brazil. Acta Trop. 2008; 107(3): 238-41.
  • 121
    Pereira NCL, Michalsky ÉM, Alonso C, Pinheiro LC, Lara-Silva FO, Lima NA, et al. Survey of phlebotomine sand fly fauna in a public Zoo in Brazil: Species diversity, seasonality, and host variety. Vet Parasitol Reg Stud Reports. 2023; 44: 100917.
  • 122
    Soares VYR, da Silva JC, da Silva KR, Cruz MSP, Santos MPD, Ribolla PEM, et al. Identification of blood meal sources of Lutzomyia longipalpis using polymerase chain reaction-restriction fragment length polymorphism analysis of the cytochrome B gene. Mem Inst Oswaldo Cruz. 2014; 109(3): 379-83.
  • 123
    Tanure A, Peixoto JC, Afonso MMS, Duarte R, Pinheiro AC, Coelho SVB, et al. Identification of sandflies (Diptera: Psychodidae: Phlebotominae) blood meals in an endemic leishmaniasis area in Brazil. Rev Inst Med Trop São Paulo. 2015; 57: 321-4.
  • 124
    dos Santos TV, Prévot G, Ginouvès M, Duarte R, Silveira FT, Póvoa MM, et al. Ecological aspects of Phlebotomines (Diptera: Psychodidae) and the transmission of American cutaneous leishmaniasis agents in an Amazonian/Guianan bordering area. Parasit Vectors. 2018; 11(1): 1-13.

Publication Dates

  • Publication in this collection
    30 Aug 2024
  • Date of issue
    2024

History

  • Received
    04 Mar 2024
  • Accepted
    12 June 2024
Instituto Oswaldo Cruz, Ministério da Saúde Av. Brasil, 4365 - Pavilhão Mourisco, Manguinhos, 21040-900 Rio de Janeiro RJ Brazil, Tel.: (55 21) 2562-1222, Fax: (55 21) 2562 1220 - Rio de Janeiro - RJ - Brazil
E-mail: memorias@fiocruz.br