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Revista Pan-Amazônica de Saúde

versão impressa ISSN 2176-6215versão On-line ISSN 2176-6223

Rev Pan-Amaz Saude vol.14  Ananindeua  2023  Epub 27-Set-2023

http://dx.doi.org/10.5123/s2176-6223202301427 

ORIGINAL ARTICLE

List of sand fly (Diptera: Psychodidae) and spatial distribution of leishmaniasis main vector species in Mato Grosso State, Brazil

Sirlei Franck Thies (orcid: 0000-0003-2124-7603)1  , Jaqueline Aparecida Menegatti (orcid: 0000-0001-5134-7889)2  , Sinara Cristina de Moraes (orcid: 0000-0003-2558-5052)3  , Mirian Francisca Martins (orcid: 0000-0001-6288-7995)3 

1 Secretaria de Estado de Saúde de Mato Grosso, Escritório Regional de Saúde de Sinop, Sinop, Mato Grosso, Brasil

2 Secretaria de Estado de Saúde de Mato Grosso, Laboratório de Entomologia, Cuiabá, Mato Grosso, Brasil

3 Secretaria de Estado de Saúde de Mato Grosso, Escritório Regional de Saúde de Barra do Graças, Barra do Garças, Mato Grosso, Brasil

ABSTRACT

OBJECTIVES:

To update the sand fly species list (Diptera: Psychodidae) in Mato Grosso State, Brazil, and to demonstrate the spatial distribution of leishmaniasis main vector species in the state.

MATERIALS AND METHODS:

Data were obtained from academic publications on Mato Grosso phlebotomine fauna and entomological reports from the Mato Grosso State Health Department database from 2006 to 2021. The taxonomic nomenclature of the specimens followed recent updates by leading researchers in the field.

RESULTS:

Twenty-six new species were detected in the Mato Grosso phlebotomine fauna, with 132 species total: six of the genus Brumptomyia and 126 distributed among 16 other genera. The main vectors of American cutaneous leishmaniasis (Nyssomyia whitmani and Bichromomyia flaviscutellata) and visceral leishmaniasis (Lutzomyia (Lutzomyia) longipalpis and Lutzomyia (Lutzomyia) cruzi) were recorded in all three existing biomes in the state, especially in Cerrado.

CONCLUSION:

The phlebotomine fauna of Mato Grosso is one of the richest and most diversified in the country, with important species in leishmaniasis epidemiology distributed across all three biomes, a fact that reinforces the significance and necessity of entomological surveys to monitor the occurrence and distribution of leishmaniasis vectors in the region.

Keywords: Phlebotomus; Disease Vectors; Leishmaniasis; Entomology; Biomes

INTRODUCTION

Leishmaniases are infectious diseases of public health importance due to their high detection rate and ability to produce deformities1. They belong to the neglected tropical diseases group and are caused by protozoa of the genus Leishmania Ross, 1903 (Kinetoplastida: Trypanosomatidae) transmitted to humans by female hematophagous sand flies of the subfamily Phlebotominae (Diptera: Psychodidae)2,3,4. They comprise a spectrum of diseases classified as American tegumentary leishmaniasis (ATL) or cutaneous leishmaniasis (more common) and visceral leishmaniasis (VL), known as kala-azar, both widespread in tropical and subtropical regions of the world1.

In Brazil, ATL is considered a serious public health problem and has been recorded in all Brazilian states3,5. Between 2010 and 2019, Mato Grosso State recorded 23,980 disease cases, with autochthonous cases detected in all its cities5.

VL is a severe and potentially fatal disease that resurfaced in several Brazilian locations during the 1980s and has since spread to new areas, including the Midwest Region6. In Mato Grosso, VL is reported in urban and rural areas of the state's northern, central-southern, and southeastern regions, distributed in 34 cities, prevailing in the central-southern and southeastern regions6. Between 2010 and 2019, 258 disease cases were registered in the state5.

The transmission of etiological agents involves different phlebotomines in specific associations with the parasites and their hosts, with transmission cycles occurring throughout the Brazilian territory7,8. More than a thousand species are described worldwide, of which more than 530 come from the Neotropical region9. In the Americas, 40 species of sand flies are involved in transmitting the Leishmania sp. parasite10. In Brazil, the main vectors associated with ATL transmission are Bichromomyia flaviscutellata (Mangabeira, 1942), Nyssomyia umbratilis (Ward & Fraiha, 1977), Nyssomyia intermedia (Lutz & Neiva, 1912), Psychodopygus wellcomei Fraiha, Shaw & Lainson, 1971, Migonemyia (Migonemyia) migonei (France, 1920), and Nyssomyia whitmani (Antunes & Coutinho, 1939), the latter being the main species associated with ATL transmission and widely distributed in Brazil, as well as in Mato Grosso11,12,13,14,15.

The main species associated with VL transmission in Brazil is Lutzomyia (Lutzomyia) longipalpis (Lutz & Neiva, 1912). However, studies highlight the relevance of Lutzomyia (Lutzomyia) cruzi (Mangabeira, 1938) in the transmission process of VL3,11,16,17. In urban areas, dogs are considered important domestic reservoirs of Leishmania infantum due to their close contact with humans18,19.

Mato Grosso State has three distinct biomes: Cerrado, Pantanal, and Amazon Rainforest, with much of its territory in the Legal Amazon20. More than 50% of Mato Grosso cities have Amazon Rainforest territory, followed by Cerrado20,21. It shares borders with Amazonas and Pará States to the north, Tocantins and Goiás to the east, Mato Grosso do Sul to the south, and Rondônia and Bolivia to the west20.

The phlebotomine fauna diversity in Mato Grosso was first reported by Missawa and Maciel22, listing 106 relevant species to the ATL and VL epidemiology, such as Lu. (Lut.) cruzi, Lu. (Lut.) longipalpis, Bi. flaviscutellata, Ny. intermedia, Mg. (Mig.) migonei, and Ny. whitmani. Ribeiro et al.23 presented these vectors' distribution in the state's biomes (Amazon Rainforest, Cerrado, and Pantanal), reporting Lu. (Lut.) cruzi, Lu. (Lut.) longipalpis, and Ny. whitmani in all three biomes; and Bi. flaviscutellata is not found only in the Pantanal biome.

Environmental transformations resulting from rural migration to the outskirts of cities increase the irregular housing construction, resulting in a lack of basic sanitation and promoting social inequalities24. Thus, changes related to urbanization and the growing use of monoculture have avored phlebotomines in disease transmission25. The disease's spread to new frontiers likely follows deforestation between large cities, aiming to implement development projects26,27, crossed by an extensive network of access roads, promoting human-vector contact.

Knowledge of phlebotomine fauna and its geographical distribution according to the biome contributes to a better understanding of the leishmaniasis transmission dynamics. Therefore, this study aims to update the list of phlebotomine species found in Mato Grosso and show the spatial distribution of leishmaniasis's four main vector species in the state, according to the biome: Lu. (Lut.) longipalpis and Lu. (Lut.) cruzi, vectors of VL, and Bi. flaviscutellata and Ny. whitmani, vectors of ATL, to identify areas at risk of transmission and prone to entomological and epidemiological surveillance.

MATERIALS AND METHODS

STUDY AREA

Mato Grosso State is located in Brazil's Center-West Region, covering an area of 903,358 km², spread across 141 cities, with an estimated population of 3,658,813 inhabitants28. The state's geography is characterized by three biomes: the Amazon Rainforest, the Cerrado, and the Pantanal20.

The climate is hot tropical, with approximately five months of drought (May to September). The average annual rainfall is 1,750 mm, peaking from December to February. Summer months experience maximum temperatures around 40 °C, with an average of around 27 °C21.

DATA COLLECTION

Data on the vector species distribution in Mato Grosso was obtained using Google Scholar and the Scientific Electronic Library Online (SciELO - Brazil) platform for academic content, along with entomological reports from the Mato Grosso State Health Department (SES-MT) database from 2006 to 2021. The taxonomic nomenclature of the specimens adhered to recent updates by leading researchers in the field.

CAPTURE PROCEDURES AND TAXONOMIC IDENTIFICATION OF SPECIMENS

Capture techniques involved using CDC light traps29 and Shannon tents30, placed in intra-domicile, peridomicile, and extra-domicile areas. CDC traps were deployed at dusk and retrieved at dawn, lasting approximately 12 h, for three consecutive nights, while the Shannon tents were set up for one night at dusk and monitored for 4 h.

Captured specimens were sorted by city, date, and environment, duly labeled, preserved in 70% alcohol, and sent to the SES-MT Entomology Laboratory for clarification, assembly, identification, and quantification, according to Young and Duncan31, with a period of approximately eight days elapsed between capture and processing. The dichotomous keys of Young and Duncan31 and Galati32 were used for identification, following the taxonomic classification proposed by Galati32.

SPATIAL DISTRIBUTION OF LOCALITIES

For the phlebotomines spatial distribution in Mato Grosso, the studies by Missawa and Maciel22 and Mestre and Fontes6 were used as initial data sources, in addition to the studies by Missawa and Lima24, Ribeiro et al.23, Missawa et al.33, Zeilhofer et al.34, Missawa et al.35, Queiroz et al.36, Alves et al.37, Brito et al.17, Moraes38, and Thies et al.39. An unpublished database of species identified by the SES-MT Entomology Laboratory between 2006 and 2021 was used. This database provided a historical series of 16 years, serving as a faithful repository of specimen collections.

CLASSIFICATION OF CITIES ACCORDING TO BIOME

The 141 cities were classified according to biome using the ArcGIS program, considering the total area of each city (km²) included in the biome20,28. Coverage proportions were calculated for places encompassing multiple biomes, and the city was categorized into the biome with the greatest area coverage: Cerrado, Amazon Rainforest, or Pantanal.

RESULTS

From 2006 to 2021, entomological surveys were conducted in 118/141 (83.69%) cities in Mato Grosso: Acorizal, Água Boa, Alta Floresta, Alto Araguaia, Alto Boa Vista, Alto Garças, Alto Paraguai, Apiacás, Araguaiana, Araguainha, Arenápolis, Aripuanã, Barão de Melgaço, Barra do Bugres, Barra do Garças, Brasnorte, Cáceres, Campinápolis, Campo Novo do Parecis, Campo Verde, Campos de Júlio, Canabrava do Norte, Canarana, Carlinda, Chapada dos Guimarães, Cláudia, Colíder, Colniza, Comodoro, Confresa, Cotriguaçu, Cuiabá, Denise, Diamantino, Dom Aquino, Feliz Natal, Gaúcha do Norte, General Carneiro, Guarantã do Norte, Guiratinga, Ipiranga do Norte, Itanhangá, Itiquira, Jaciara, Jangada, Juara, Juína, Juruena, Juscimeira, Lucas do Rio Verde, Luciara, Marcelândia, Matupá, Mirassol D'Oeste, Nobres, Nortelândia, Nossa Senhora do Livramento, Nova Bandeirantes, Nova Brasilândia, Nova Canaã do Norte, Nova Guarita, Nova Lacerda, Nova Marilândia, Nova Maringá, Nova Mutum, Nova Santa Helena, Nova Ubiratã, Nova Xavantina, Novo Horizonte do Norte, Novo Mundo, Novo Santo Antônio, Novo São Joaquim, Paranaíta, Paranatinga, Pedra Preta, Peixoto de Azevedo, Planalto da Serra, Poconé, Pontal da Araguaia, Ponte Branca, Pontes e Lacerda, Porto Alegre do Norte, Porto dos Gaúchos, Porto Esperidião, Porto Estrela, Poxoréo, Primavera do Leste, Querência, Reserva do Cabaçal, Ribeirão Cascalheira, Ribeirãozinho, Rondolândia, Rondonópolis, Rosário Oeste, Salto do Céu, Santa Carmem, Santa Rita do Trivelato, Santo Antônio do Leverger, São Félix do Araguaia, São José do Povo, São José do Rio Claro, São José do Xingu, São José dos Quatro Marcos, São Pedro da Cipa, Sapezal, Serra Nova Dourada, Sinop, Sorriso, Tabaporã, Tangará da Serra, Tapurah, Terra Nova do Norte, Torixoréu, União do Sul, Várzea Grande, Vera, Vila Bela da Santíssima Trindade, and Vila Rica (Figure 1).

List of cities: 1-Acorizal, 2-Água Boa, 3-Alta Floresta, 4-Alto Araguaia, 5-Alto Boa Vista, 6-Alto Garças, 7-Alto Paraguai, 8-Alto Taquari, 9-Apiacás, 10-Araguaiana, 11-Araguainha, 12-Araputanga, 13-Arenápolis, 14-Aripuanã, 15-Barão de Melgaço, 16-Barra do Bugres, 17-Barra do Garças, 18-Bom Jesus do Araguaia, 19-Brasnorte, 20-Cáceres, 21-Campinápolis, 22-Campo Novo do Parecis, 23-Campo Verde, 24-Campos de Júlio, 25-Canabrava do Norte, 26-Canarana, 27-Carlinda, 28-Castanheira, 29-Chapada dos Guimarães, 30-Cláudia, 31-Cocalinho, 32-Colíder, 33-Colniza, 34-Comodoro, 35-Confresa, 36-Conquista D'Oeste, 37-Cotriguaçu, 38-Cuiabá, 39-Curvelândia, 40-Denise, 41-Diamantino, 42-Dom Aquino, 43-Feliz Natal, 44-Figueirópolis D'Oeste, 45-Gaúcha do Norte, 46-General Carneiro, 47-Glória D'Oeste, 48-Guarantã do Norte, 49-Guiratinga, 50-Indiavaí, 51-Ipiranga do Norte, 52-Itanhangá, 53-Itaúba, 54-Itiquira, 55-Jaciara, 56-Jangada, 57-Jauru, 58-Juara, 59-Juína, 60-Juruena, 61-Juscimeira, 62-Lambari D'Oeste, 63-Lucas do Rio Verde, 64-Luciara, 65-Marcelândia, 66-Matupá, 67-Mirassol D'Oeste, 68-Nobres, 69-Nortelândia, 70-Nossa Senhora do Livramento, 71-Nova Bandeirantes, 72-Nova Brasilândia, 73-Nova Canaã do Norte, 74-Nova Guarita, 75-Nova Lacerda, 76-Nova Marilândia, 77-Nova Maringá, 78-Nova Monte Verde, 79-Nova Mutum, 80-Nova Nazaré, 81-Nova Olímpia, 82-Nova Santa Helena, 83-Nova Ubiratã, 84-Nova Xavantina, 85-Novo Horizonte do Norte, 86-Novo Mundo, 87-Novo Santo Antônio, 88-Novo São Joaquim, 89-Paranaíta, 90-Paranatinga, 91-Pedra Preta, 92-Peixoto de Azevedo, 93-Planalto da Serra, 94-Poconé, 95-Pontal do Araguaia, 96-Ponte Branca, 97-Pontes e Lacerda, 98-Porto Alegre do Norte, 99-Porto dos Gaúchos, 100-Porto Esperidião, 101-Porto Estrela, 102-Poxoréu, 103-Primavera do Leste, 104-Querência, 105-Reserva do Cabaçal, 106-Ribeirão Cascalheira, 107-Ribeirãozinho, 108-Rio Branco, 109-Rondolândia, 110-Rondonópolis, 111-Rosário Oeste, 112-Salto do Céu, 113-Santa Carmem, 114-Santa Cruz do Xingu, 115-Santa Rita do Trivelato, 116-Santa Terezinha, 117-Santo Afonso, 118-Santo Antônio de Leverger, 119-Santo Antônio do Leste, 120-São Félix do Araguaia, 121-São José do Povo, 122-São José do Rio Claro, 123-São José do Xingu, 124-São José dos Quatro Marcos, 125-São Pedro da Cipa, 126-Sapezal, 127-Serra Nova Dourada, 128-Sinop, 129-Sorriso, 130-Tabaporã, 131-Tangará da Serra, 132-Tapurah, 133-Terra Nova do Norte, 134-Tesouro, 135-Torixoréu, 136-União do Sul, 137-Vale de São Domingos, 138-Várzea Grande, 139-Vera, 140-Vila Bela da Santíssima Trindade, 141-Vila Rica.

Figure 1 - Distribution of phlebotomine entomological surveys conducted in Mato Grosso cities, Brazil, from 2006 to 2021 

As for the cities' distribution by biome, the adopted classification revealed a predominance of the Amazon Rainforest biome, covering 53.19% of the geographical area and present in 75 cities; followed by the Cerrado, with coverage of 43.97%, reaching 62 cities; and the Pantanal, present in four cities, occupying 2.84% of Mato Grosso's territory.

Entomological collections took place in 100% (4/4) of cities in the Pantanal biome, in 77.33% (58/75) of those belonging to the Amazon Rainforest biome, and in 90.32% (56/62) of cities in the Cerrado biome.

A total of 132 phlebotomine species were recorded (26 had not yet been described for Mato Grosso State), distributed in 17 genera: Evandromyia (20); Psathyromyia (19); Psychodopygus (19); Lutzomyia (13); Micropygomyia (11); Nyssomyia (10); Pintomyia (7); Brumptomyia (6); Trichophoromyia (6); Bichromomyia (3); Migonemyia (3); Pressatia (3); Sciopemyia (3); Trichopygomyia (3); Viannamyia (3); Martinsmyia (2); and Expapillata (1) (Table 1).

Table 1 - List of phlebotomine species identified in Mato Grosso State, from 2006 to 2021 

Ny. whitmani and Bi. flaviscutellata, considered the main ATL vectors in Brazil and Mato Grosso, were found in 105/118 (88.98%) and 54/118 (45.76%) cities in Mato Grosso, respectively. Sympatry between these species was recorded in 53/118 (44.91%) of them (Figure 2).

List of cities: 1-Acorizal, 2-Água Boa, 3-Alta Floresta, 4-Alto Araguaia, 5-Alto Boa Vista, 6-Alto Garças, 7-Alto Paraguai, 8-Alto Taquari, 9-Apiacás, 10-Araguaiana, 11-Araguainha, 12-Araputanga, 13-Arenápolis, 14-Aripuanã, 15-Barão de Melgaço, 16-Barra do Bugres, 17-Barra do Garças, 18-Bom Jesus do Araguaia, 19-Brasnorte, 20-Cáceres, 21-Campinápolis, 22-Campo Novo do Parecis, 23-Campo Verde, 24-Campos de Júlio, 25-Canabrava do Norte, 26-Canarana, 27-Carlinda, 28-Castanheira, 29-Chapada dos Guimarães, 30-Cláudia, 31-Cocalinho, 32-Colíder, 33-Colniza, 34-Comodoro, 35-Confresa, 36-Conquista D'Oeste, 37-Cotriguaçu, 38-Cuiabá, 39-Curvelândia, 40-Denise, 41-Diamantino, 42-Dom Aquino, 43-Feliz Natal, 44-Figueirópolis D'Oeste, 45-Gaúcha do Norte, 46-General Carneiro, 47-Glória D'Oeste, 48-Guarantã do Norte, 49-Guiratinga, 50-Indiavaí, 51-Ipiranga do Norte, 52-Itanhangá, 53-Itaúba, 54-Itiquira, 55-Jaciara, 56-Jangada, 57-Jauru, 58-Juara, 59-Juína, 60-Juruena, 61-Juscimeira, 62-Lambari D'Oeste, 63-Lucas do Rio Verde, 64-Luciara, 65-Marcelândia, 66-Matupá, 67-Mirassol D'Oeste, 68-Nobres, 69-Nortelândia, 70-Nossa Senhora do Livramento, 71-Nova Bandeirantes, 72-Nova Brasilândia, 73-Nova Canaã do Norte, 74-Nova Guarita, 75-Nova Lacerda, 76-Nova Marilândia, 77-Nova Maringá, 78-Nova Monte Verde, 79-Nova Mutum, 80-Nova Nazaré, 81-Nova Olímpia, 82-Nova Santa Helena, 83-Nova Ubiratã, 84-Nova Xavantina, 85-Novo Horizonte do Norte, 86-Novo Mundo, 87-Novo Santo Antônio, 88-Novo São Joaquim, 89-Paranaíta, 90-Paranatinga, 91-Pedra Preta, 92-Peixoto de Azevedo, 93-Planalto da Serra, 94-Poconé, 95-Pontal do Araguaia, 96-Ponte Branca, 97-Pontes e Lacerda, 98-Porto Alegre do Norte, 99-Porto dos Gaúchos, 100-Porto Esperidião, 101-Porto Estrela, 102-Poxoréu, 103-Primavera do Leste, 104-Querência, 105-Reserva do Cabaçal, 106-Ribeirão Cascalheira, 107-Ribeirãozinho, 108-Rio Branco, 109-Rondolândia, 110-Rondonópolis, 111-Rosário Oeste, 112-Salto do Céu, 113-Santa Carmem, 114-Santa Cruz do Xingu, 115-Santa Rita do Trivelato, 116-Santa Terezinha, 117-Santo Afonso, 118-Santo Antônio de Leverger, 119-Santo Antônio do Leste, 120-São Félix do Araguaia, 121-São José do Povo, 122-São José do Rio Claro, 123-São José do Xingu, 124-São José dos Quatro Marcos, 125-São Pedro da Cipa, 126-Sapezal, 127-Serra Nova Dourada, 128-Sinop, 129-Sorriso, 130-Tabaporã, 131-Tangará da Serra, 132-Tapurah, 133-Terra Nova do Norte, 134-Tesouro, 135-Torixoréu, 136-União do Sul, 137-Vale de São Domingos, 138-Várzea Grande, 139-Vera, 140-Vila Bela da Santíssima Trindade, 141-Vila Rica.

Figure 2 - Ny. whitmani and Bi. flaviscutellata spatial distribution in Mato Grosso State, Brazil, from 2006 to 2021 

Ny. whitmani was the predominant species in all three biomes. Bi. flaviscutellata, although also detected in the same biomes, was less frequent in the Pantanal (1/4 cities), being found for the first time in Barão do Melgaço, corresponding to the first record of this species in this biome.

In the Amazon Rainforest biome, Ny. whitmani was recorded in 86.21% (50/58) of the cities, while Bi. flaviscutellata was present in 44.83% (26/58).

In cities with the Cerrado biome, Ny. whitmani occurred in 91.07% (51/56) and Bi. flaviscutellata in 50.00% (28/56).

Of the species important in the VL epidemiology, Lu. (Lut.) longipalpis was detected in 48.31% (57/118) of the cities and Lu. (Lut.) cruzi in 34.75% (41/118). These species were found in sympatry in 25.42% (30/118) of the cities analyzed (Figure 3).

List of cities: 1-Acorizal, 2-Água Boa, 3-Alta Floresta, 4-Alto Araguaia, 5-Alto Boa Vista, 6-Alto Garças, 7-Alto Paraguai, 8-Alto Taquari, 9-Apiacás, 10-Araguaiana, 11-Araguainha, 12-Araputanga, 13-Arenápolis, 14-Aripuanã, 15-Barão de Melgaço, 16-Barra do Bugres, 17-Barra do Garças, 18-Bom Jesus do Araguaia, 19-Brasnorte, 20-Cáceres, 21-Campinápolis, 22-Campo Novo do Parecis, 23-Campo Verde, 24-Campos de Júlio, 25-Canabrava do Norte, 26-Canarana, 27-Carlinda, 28-Castanheira, 29-Chapada dos Guimarães, 30-Cláudia, 31-Cocalinho, 32-Colíder, 33-Colniza, 34-Comodoro, 35-Confresa, 36-Conquista D'Oeste, 37-Cotriguaçu, 38-Cuiabá, 39-Curvelândia, 40-Denise, 41-Diamantino, 42-Dom Aquino, 43-Feliz Natal, 44-Figueirópolis D'Oeste, 45-Gaúcha do Norte, 46-General Carneiro, 47-Glória D'Oeste, 48-Guarantã do Norte, 49-Guiratinga, 50-Indiavaí, 51-Ipiranga do Norte, 52-Itanhangá, 53-Itaúba, 54-Itiquira, 55-Jaciara, 56-Jangada, 57-Jauru, 58-Juara, 59-Juína, 60-Juruena, 61-Juscimeira, 62-Lambari D'Oeste, 63-Lucas do Rio Verde, 64-Luciara, 65-Marcelândia, 66-Matupá, 67-Mirassol D'Oeste, 68-Nobres, 69-Nortelândia, 70-Nossa Senhora do Livramento, 71-Nova Bandeirantes, 72-Nova Brasilândia, 73-Nova Canaã do Norte, 74-Nova Guarita, 75-Nova Lacerda, 76-Nova Marilândia, 77-Nova Maringá, 78-Nova Monte Verde, 79-Nova Mutum, 80-Nova Nazaré, 81-Nova Olímpia, 82-Nova Santa Helena, 83-Nova Ubiratã, 84-Nova Xavantina, 85-Novo Horizonte do Norte, 86-Novo Mundo, 87-Novo Santo Antônio, 88-Novo São Joaquim, 89-Paranaíta, 90-Paranatinga, 91-Pedra Preta, 92-Peixoto de Azevedo, 93-Planalto da Serra, 94-Poconé, 95-Pontal do Araguaia, 96-Ponte Branca, 97-Pontes e Lacerda, 98-Porto Alegre do Norte, 99-Porto dos Gaúchos, 100-Porto Esperidião, 101-Porto Estrela, 102-Poxoréu, 103-Primavera do Leste, 104-Querência, 105-Reserva do Cabaçal, 106-Ribeirão Cascalheira, 107-Ribeirãozinho, 108-Rio Branco, 109-Rondolândia, 110-Rondonópolis, 111-Rosário Oeste, 112-Salto do Céu, 113-Santa Carmem, 114-Santa Cruz do Xingu, 115-Santa Rita do Trivelato, 116-Santa Terezinha, 117-Santo Afonso, 118-Santo Antônio de Leverger, 119-Santo Antônio do Leste, 120-São Félix do Araguaia, 121-São José do Povo, 122-São José do Rio Claro, 123-São José do Xingu, 124-São José dos Quatro Marcos, 125-São Pedro da Cipa, 126-Sapezal, 127-Serra Nova Dourada, 128-Sinop, 129-Sorriso, 130-Tabaporã, 131-Tangará da Serra, 132-Tapurah, 133-Terra Nova do Norte, 134-Tesouro, 135-Torixoréu, 136-União do Sul, 137-Vale de São Domingos, 138-Várzea Grande, 139-Vera, 140-Vila Bela da Santíssima Trindade, 141-Vila Rica.

Figure 3 - Lu. (Lut.) longipalpis and Lu. (Lut.) cruzi spatial distribution in Mato Grosso State, Brazil, from 2006 to 2021 

Lu. (Lut.) longipalpis and Lu. (Lut.) cruzi were found in all three biomes. In the Amazon Rainforest biome, Lu. (Lut.) longipalpis occurred in 36.84% (21/57) and Lu. (Lut.) cruzi in 15.79% (9/57) of the cities predominantly in this biome. For the Cerrado, Lu. (Lut.) longipalpis was detected in 32/56 (57.14%) and Lu. (Lut.) cruzi in 28/56 (50.00%) of the cities in this biome. Both species were recorded in all cities (4/4) of the Pantanal biome.

Among the 118 cities analyzed in this study, only 10 (8.47%) did not have the main species of epidemiological importance for ATL and VL (Figure 1).

DISCUSSION

The findings of this study reveal the expansion of entomological surveillance for phlebotomines in Mato Grosso, from the 68 cities surveyed by Missawa and Lima24 (1996-2004) to 118 (2006-2021). However, there is still a need to expand entomological surveillance actions to the other cities that have not been surveyed/silenced (Alto Taquari, Araputanga, Bom Jesus do Araguaia, Castanheira, Cocalinho, Conquista D'Oeste, Curvelândia, Figueirópolis D'Oeste, Glória D'Oeste, Indiavaí, Itaúba, Jauru, Lambari D'Oeste, Nova Monte Verde, Nova Nazaré, Nova Olímpia, Rio Branco, Santa Cruz do Xingu, Santo Afonso, Santo Antônio do Leste, Santa Terezinha, Tesouro, and Vale de São Domingos), in order to encompass the entire state.

In addition to the increase in the number of cities surveyed, there was an increase in the number of phlebotomine species recorded, from 106 species described by Missawa and Maciel22 to 132. This growth may be due to the expansion of entomological monitoring carried out by health services and research groups, revealing the importance of these activities for understanding the phlebotomine fauna. This information is necessary for planning prevention and control measures to reduce the risk of leishmaniasis transmission in Mato Grosso since the presence of vectors and their spatial density are associated with the lower or higher risk of leishmaniasis occurrence in each geographical area. Thus, this study contributes to identifying locations at risk of disease transmission in the state.

Missawa and Maciel22, using Young and Duncan31 for taxonomic classification, identified Lutzomyia goiana (Martins, Falcão & Silva, 1962) and Migonemyia baityi Damasceno, Causey & Arouck, 1945 in Mato Grosso. Using the taxonomic classification proposed by Galati32, these species were reclassified as Micropygomyia (Sauromyia) vonatzingeni (Galati, 2007) and Migonemyia (Blancasmyia) bursiformis (Floch & Abonnenc, 1944), respectively, qualitatively altering the list of phlebotomine species found in Mato Grosso (Table 1).

Queiroz et al.36 and Moraes38 identified Ps. wellcomei and Micropygomyia (Sauromyia) ferreirana (Barreto, Martins & Pellegrino, 1956) in Barra do Garças city, respectively, marking the first records of these species in Mato Grosso. In Cáceres, Alves et al.37 detected: Brumptomyia avellari (Costa Lima, 1932); Brumptomyia mangabeirai (Barreto & Coutinho, 1941); Evandromyia (Aldamyia) aldafalcaoae (Santos, Andrade Filho & Honer, 2001); Psathyromyia (Forattiniella) campograndensis (Oliveira, Andrade Filho, Falcão & Brazil, 2001); Expapillata cerradincola (Galati, Nunes, Oshiro & Dorval, 1995); and Micropygomyia (Silvamyia) echinatopharynx Andrade Filho, Galati, Andrade & Falcão, 2004. Thies et al.39 reported Viannamyia caprina (Osorno-Mesa, Morales & Osorno, 1972) and Psychodopygus dorlinsis (Le Pont & Desjeux, 1982) in Sinop, marking the first record of these species in the state.

In addition to the main species involved in leishmaniasis epidemiology1,12, others also implicated in the dissemination cycle were recorded in Mato Grosso, such as Bichromomyia olmeca bicolor (Fairchild & Theodor, 1971), Bichromomyia olmeca nociva (Young & Arias, 1982), Ny. umbratilis, Nyssomyia yuilli yuilli (Young & Porter, 1972), Trichophoromyia ubiquitalis (Mangabeira, 1942), Mg. (Mig.) migonei, Nyssomyia antunesi (Coutinho, 1939), among others.

The diversity of phlebotomine species recorded in Mato Grosso (132 species) quantitatively surpasses its neighboring states such as Pará (130)40, Amazonas (131)41, Tocantins (43)42, Goiás (47)43, and Mato Grosso do Sul (54)14; except for Rondônia, which surpassed this record, with 143 species44. In Bolivia, a country bordering Mato Grosso, 121 species were recorded45.

This diversity demonstrates the adaptation of these vectors to different environments (ecotopes, biomes), with varying levels of anthropogenic interference, whether through forms of land use and occupation, deforestation, fires, or resource extraction, factors that can cause changes in phlebotomine ecology26,46. The size of Mato Grosso's geographical area and the variety of biomes (Cerrado, Amazon Rainforest, and Pantanal), as well as transition zones, can favor the diversification of the phlebotomine fauna, as has already been observed for triatomine species47. Knowing the phlebotomine fauna is important, as it is estimated that 10% of them are incriminated or suspected of transmitting the agents that cause leishmaniasis48.

Brazil is a vast country with five biomes, which may explain the diversity of phlebotomines43. Mato Grosso has three biomes throughout its territorial area, which may have contributed to a greater richness of recorded species compared to other Brazilian states20,21.

Regarding the importance of recording vectors in ATL epidemiology, this study highlighted the wide distribution of Ny. whitmani in Mato Grosso, found in 88.98% of the surveyed cities, results that corroborate the Zeilhofer et al.34 and Missawa et al.33 findings.

The wide distribution of Ny. whitmani is reflected in the widespread occurrence of human cases in all Mato Grosso cities, as well as the maintenance and growth of ATL cases in the state26. Ny. whitmani is involved in ATL transmission in both old colonization areas and recent urbanization areas49. According to Souza et al.50, this species is adapted to urban areas and can transmit ATL both in the peridomicile and intradomicile, often found in chicken coops, suggesting a process of adaptation to the anthropic environment36,51; it is opportunistic and has eclectic feeding habits, adjusting its habits to the availability of hosts in anthropic environments52.

Ny. whitmani can be found in five regions of Brazil, associated with a variety of vegetation types, such as forests, cerrado, and caatinga, widely distributed in Roraima, Acre, Tocantins, and Mato Grosso do Sul53. This wide distribution and association with Leishmania braziliensis in different regions show the importance of this species in ATL epidemiology, reinforcing its status as the main vector in Mato Grosso, corroborating its findings in other areas54,55,56.

These vector findings demonstrate the relevance of entomological research and reinforce the need to develop public health policies aimed at preventing and promoting health, as well as timely diagnosis and treatment of ATL human cases.

Although recorded in all studied biomes, Bi. flaviscutellata was more prevalent in the Cerrado cities of Mato Grosso, reinforcing the need for attention to its dispersion and importance in the state's ATL epidemiology. This species is zoophilic and feeds on small rodents of the genera Oryzomys and Proechimys and is considered a vector of Leishmania amazonensis57. It inhabits forest areas, found in openings of fallen trees that offer conditions for both the development of immature forms and the permanence of vertebrate hosts58. Occasionally, it invades the peridomestic habitats59 and shelters of domestic animals60,61, exploiting degraded areas usually occupied by human populations, facilitating human-vector contact42,59.

When assessing the dispersion of important species for VL in Mato Grosso, its primary vector, Lu. (Lut.) longipalpis, occurred in all the Pantanal biome cities and in 57.14% of those in Cerrado. Missawa and Lima24 reported the association of this species with the Amazon Rainforest and Cerrado biomes. The maintenance of Lu. (Lut.) longipalpis is possibly associated with its dietary eclecticism7,62,63,64,65,66.

Lu. (Lut.) cruzi was also found in 100% of the cities with the Pantanal biome and in 50% of the Cerrado cities, corroborating the Ribeiro and Missawa67 and Missawa and Lima24 findings, who reported a higher frequency of this species in Cerrado and Pantanal cities, suggesting the Cerrado as the preferential environment for this species.

Lu. (Lut.) cruzi is important to VL epidemiology in Mato Grosso35 and Mato Grosso do Sul68. Cases of VL and ATL have been reported in the absence of the main vector species, Lu. (Lut.) longipalpis, and there are already records of natural infection of Lu. (Lut.) cruzi by Leishmania chagasi in both states35,68, demonstrating that this species may be part of the leishmaniasis transmission chain.

The occurrence of Lu. (Lut.) longipalpis and Lu. (Lut.) cruzi, with a wide distribution in the different biomes of Mato Grosso, confirms the generalist nature of these species, adapted to diversified habitats69.

Another species constantly present in ATL endemic areas is Ny. umbratilis70, considered one of the main vectors of Leishmania (Viannia) guyanensis in most of Latin American countries, such as Brazil, Bolivia, Colombia, Peru, Venezuela, Suriname, and French Guiana, and in the Amazon Region71. Mg. (Mig.) migonei is a permissive vector, capable of being infected with various species of Leishmania72, also found in the state.

A species of Leishmania can be transmitted by different species of sand flies (Diptera: Psychodidae: Phlebotominae) in different geographical regions and biomes43. The presence of medically important phlebotomine species in the state's different biomes reveals vulnerable and/or receptive areas for transmitting leishmaniasis in all the Mato Grosso cities surveyed.

CONCLUSION

This study revealed a high diversity of phlebotomines in Mato Grosso, ranking it the second Brazilian state with the highest number of distinct species.

It was possible to verify the expansion of entomological surveillance in the state over the years and an increase in the number of identified species that may be involved and/or incriminated in the transmission of leishmaniasis in Mato Grosso.

Thus, entomological and epidemiological surveillance studies, especially those focused on the knowledge of phlebotomine fauna and its behavior, will provide subsidies to support health services in effective prevention and health promotion activities aimed at controlling leishmaniasis.

The importance of integrated work between the Municipal Health Departments and the State Health Department is also emphasized. This allows the optimization of resources and the prompt effectiveness of vector control actions, thereby reducing the risk of disease transmission and ensuring the improvement of the population's quality of life.

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6Article originally published in Portuguese (http://dx.doi.org/10.5123/S2176-6223202301427)

7Translated by: Vera Maria Segurado Pimentel

8Reviewed by: Isabella Mateus

How to cite this article / Como citar este artigo: Thies SF, Menegatti JA, Moraes SC, Martins MF. List of sand fly (Diptera: Psychodidae) and spatial distribution of leishmaniasis main vector species in Mato Grosso State, Brazil. Rev Pan Amaz Saude. 2023;14:e202301427. Doi: http://dx.doi.org/10.5123/S2176-6223202301427

Received: December 13, 2022; Accepted: July 04, 2023

Correspondence / Correspondência: Sirlei Franck Thies. Rua das Avencas, 2072. Bairro: Setor Residencial Norte. Zip code: 78550-300 - Sinop, Mato Grosso, Brazil - Phone #: +55 (66) 3531-2418. E-mail: sirleithies@ses.mt.gov.br

CONFLICTS OF INTEREST

The authors declare no conflicts of interest related to the study.

AUTHORS' CONTRIBUTION

SFT was responsible for conceiving the study, data collection, analysis, and interpretation, manuscript writing and revision. JAM contributed to data collection, analysis, and manuscript revision. SCM contributed to data analysis, interpretation, and manuscript revision. MFM contributed to data analysis and interpretation, manuscript writing and revision. All authors reviewed and approved the final manuscript.

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