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Factors associated with human visceral leishmaniasis cases during urban epidemics in Brazil: a systematic review

Published online by Cambridge University Press:  12 January 2021

Cleya da Silva Santana Cruz*
Affiliation:
Programa de Pós-graduação em Infectologia e Medicina Tropical, Faculdade de Medicina, Universidade Federal de Minas Gerais, 30130-100, Belo Horizonte, MG, Brazil
David Soeiro Barbosa
Affiliation:
Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, 31270-901, Belo Horizonte, MG, Brazil
Vinícius Cunha Oliveira
Affiliation:
Pós-graduação em Reabilitação e Desempenho Funcional, Universidade Federal dos Vales do Jequitinhonha e Mucuri, 39100-000, Diamantina, MG, Brazil
Diogo Tavares Cardoso
Affiliation:
Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, 31270-901, Belo Horizonte, MG, Brazil
Nathália Sernizon Guimarães
Affiliation:
Programa de Pós-graduação em Infectologia e Medicina Tropical, Faculdade de Medicina, Universidade Federal de Minas Gerais, 30130-100, Belo Horizonte, MG, Brazil
Mariângela Carneiro*
Affiliation:
Programa de Pós-graduação em Infectologia e Medicina Tropical, Faculdade de Medicina, Universidade Federal de Minas Gerais, 30130-100, Belo Horizonte, MG, Brazil Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, 31270-901, Belo Horizonte, MG, Brazil
*
Authors for correspondence: Cleya da Silva Santana Cruz, E-mail: [email protected]; Mariângela Carneiro, E-mail: [email protected]
Authors for correspondence: Cleya da Silva Santana Cruz, E-mail: [email protected]; Mariângela Carneiro, E-mail: [email protected]

Abstract

Visceral leishmaniasis (VL) is endemic in 70 countries and has been reported in 12 countries of Latin America, with over 90% of the cases reported in Brazil, where epidemics have occurred since 1980. The objective of this review is to describe the factors associated with the occurrence of VL epidemics in humans in urban areas. A systematic review was conducted according to the PRISMA-P guidelines. The databases PubMed (by Medline), Cochrane Library, Embase, Amed, LILACS and grey literature [Google Scholar and handsearch of the database of the Information System for Notifiable Diseases (SINAN) of Brazil's Unified Health System] were used. The protocol was registered under PROSPERO (CRD42019128998). Climatic, environmental factors and indicators of urban social structure were described as influencing the outbreaks in the North and Northeast regions. Gender and age characteristics were related to a greater chance of developing VL in the Central-West, Northeast and Southeast regions. Vector indicators showed a positive correlation with the incidence of VL in studies in the Northeast region. In the Southeast and Northeast regions, studies revealed the presence of dogs with positive correlation with VL. Knowledge gaps remain regarding the contribution to the increase in the risk factors described in ecological approaches, as no analysis was performed at the individual level, and it is still necessary to discuss the influence of other associated elements in epidemic episodes in the spread of VL.

Type
Review Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Albuquerque, PLMM, da Silva Júnior, GB, Freire, CCF, Oliveira, SBC, Daniel Medeiros Almeida, DM, da Silva, HF, Cavalcante, MS and Sousa, AQ (2009) Urbanization of visceral leishmaniasis (kala-azar) in Fortaleza, Ceará, Brazil. Revista Panamericana de Salud Pública 26, 330336.CrossRefGoogle Scholar
Alvar, J, Vélez, ID, Bern, C, Herrero, M, Desjeux, P, Cano, J, Jannin, J and de Boer, M (2012) Leishmaniasis worldwide and global estimates of its incidence. PLoS ONE 7, e35671.CrossRefGoogle ScholarPubMed
Araújo, WS, de Freitas-Neta, MSB, Teixeira, VJCL, e Silva-Neto, JAL, Monteiro, MA, Alves, JWL, Cândido, ELC and Firmino, PRA (2018) Correlação entre leishmaniose visceral e indicadores socioeconômicos. Revista Multidisciplinar e de Psicologia 12, 817824.Google Scholar
Badaro, R, Jones, TC, Carvalho, EM, Sampaio, D, Reed, SG, Barral, A, Teixeira, R and Johnson WD, JR (1986) New perspectives on a subclinical form of visceral leishmaniasis. The Journal of Infectious Diseases 154, 10031011.CrossRefGoogle ScholarPubMed
Barata, RA, França-Silva, JC, Mayrink, W, Silva, JC, Prata, A, Lorosa, ES, Fiúza, JA, Gonçalves, CM, de Paula, KM and Dias, ES (2005) Aspectos da ecologia e do comportamento de flebotomíneos em área endêmica de leishmaniose visceral, Minas Gerais. Revista da Sociedade Brasileira de Medicina Tropical 38, 421425.CrossRefGoogle Scholar
Bavia, ME, Carneiro, DD, Gurgel, HC, Madureira Filho, C and Barbosa, MG. (2005) Remote sensing and geographic information systems and risk of American visceral leishmaniasis in Bahia, Brazil. Parasitologia 47, 165169.Google ScholarPubMed
Belo, VS, Werneck, GL, Barbosa, DS, Simões, TC, Nascimento, BWL, Silva, ES, da Silva, ES and Struchiner, CJ (2013) Factors associated with visceral leishmaniasis in the Americas: a systematic review and meta-analysis. PLoS Neglected Tropical Diseases 7, e2182.CrossRefGoogle ScholarPubMed
Borges, BKA, Silva, JA, Haddad, JPA, Moreira, EC, Magalhães, DF, Ribeiro, LML and Fiúza, VOP (2008) Assessment of knowledge and preventive attitudes concerning visceral leishmaniasis in Belo Horizonte, Minas Gerais State, Brazil. Cadernos de Saúde Pública 24, 777784.CrossRefGoogle Scholar
Borges, BKA, Silva, JA, Haddad, JPA, Moreira, EC, Magalhães, DF, Ribeiro, LML and Fiúza, VOP (2009) Animal presence and the risk for transmission of visceral leishmaniasis in Belo Horizonte, Brazil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 61, 10351043.CrossRefGoogle Scholar
Braga, J and Werneck, GL (2008) Vigilância epidemiológica. In RA, Medronho, Bloch KV, Luiz RR, Werneck GL (ed.), Epidemiologia. São Paulo: Atheneu, pp 103121.Google Scholar
Braga, RR, Lainson, R, Shaw, JJ, Ryan, L and Silveira, FT (1986) Leishmaniasis in Brazil. XXII: characterization of Leishmania from man, dogs and the sandfly Lutzomyia longipalpis (Lutz & Neiva, 1912) isolated during an outbreak of visceral leishmaniasis in Santarém, Pará state. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 143145.CrossRefGoogle ScholarPubMed
Brazuna, JCM, e Silva, EA, Brazuna, JM, Domingos, IH, Chaves, N, Honer, MR, van Onselen, VJ and de Oliveira, ALL (2012) Profile and geographic distribution of reported cases of visceral leishmaniasis in Campo Grande, State of Mato Grosso do Sul, Brazil, from 2002 to 2009. Revista da Sociedade Brasileira de Medicina Tropical 45, 601606.CrossRefGoogle Scholar
Bruhn, FRP, Morais, MHF, Bruhn, NCP, Cardoso, DL, Ferreira, F and Rocha CM, BM (2018) Human visceral leishmaniasis: factors associated with deaths in Belo Horizonte, Minas Gerais state, Brazil from 2006 to 2013. Epidemiology and Infection 146, 565570.CrossRefGoogle Scholar
Carneiro, D, Bavia, ME, Rocha, W, Lobão, J, Madureira-Filho, C, de Oliveira J, B, da Silva, CE, Barbosa, MG and Rios, R (2004) Identification of risk areas for visceral leishmaniasis through epidemiological studies and remote sensing data in Feira de Santana, Bahia, Brazil (2000–2002). Revista Baiana Saúde Pública 28, 1932.CrossRefGoogle Scholar
Carranza-Tamayo, CO, Werneck, GL and Romero, GAS (2016) Are opossums a relevant factor associated with asymptomatic Leishmania infection in the outskirts of the largest Brazilian cities? Brazilian Journal of Infectious Diseases 20, 119126.CrossRefGoogle ScholarPubMed
Carvalho, ML, Rebêlo, JMM, Araújo, JC and Barros, VLL (2000) Aspectos ecológicos dos flebotomíneos (Diptera: Psychodidae) do município de São José de Ribamar, MA, Brasil. Área endêmica de leishmanioses. Entomologia y Vectores 7, 1932.Google Scholar
Cerbino-Neto, J, Werneck, GL and Costa, CHN (2009) Factors associated with the incidence of urban visceral leishmaniasis: an ecological study in Teresina, Piauí State, Brazil. Cadernos de Saúde Pública 25, 15431551.CrossRefGoogle ScholarPubMed
Costa, CHN, Pereira, HF and Araújo, MV (1990) Visceral leishmaniasis epidemic in Piaui state, Brazil, 1980–1986. Revista de Saúde Pública 24, 361372.CrossRefGoogle Scholar
Costa, CHN, Werneck, GL, Rodrigues, L JR, Santos, MV, Araújo, IB, Moura, LS, Moreira, S, Gomes, RBB and Lima, SS (2005) Household structure and urban services: neglected targets in the control of visceral leishmaniasis. Annals of Tropical Medicine & Parasitology 99, 229236.CrossRefGoogle Scholar
Cunha, S, Freire, M, Eulalio, C, Cristovao, J, Netto, J, Johnson, WD, Reed, SG and Badaro, R (1995) Visceral leishmaniasis in a new ecological niche near a major metropolitan area of Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 89, 155158.CrossRefGoogle Scholar
da Silva, AR, Tauil, PL, Cavalcante, MNS, Medeiros, MN, Pires, BN and Gonçalves, EGR (2008) Situação epidemiológica da leishmaniose visceral, na Ilha de São Luís, Estado do Maranhão. Revista da Sociedade Brasileira de Medicina Tropical 41, 358364.CrossRefGoogle Scholar
da Silva, LB, de Aquino, DMC, Bezerra, JMT, Melo, MN, Leonardo, FS, e Silva, ASG and Pinheiro, VCS (2016) Factors associated with Visceral Leishmaniasis in an endemic area of Codó, State of Maranhão, Brazil. Revista de Epidemiologia e Controle de Infecção 6, 7480.Google Scholar
de Almeida, AS, Medronho, RA and Werneck, GL (2011) Identification of risk areas for visceral leishmaniasis in Teresina, Piauí State, Brazil. American Journal of Tropical Medicine and Hygiene 84, 681687.CrossRefGoogle ScholarPubMed
de Araújo, VEM, Pinheiro, LC, Almeida, MCM, de Menezes, FC, Morais, MHF, Reis, IA, Assunção, RM and Carneiro, M (2013) Relative risk of visceral Leishmaniasis in Brazil: a spatial analysis in urban area. PLoS Neglected Tropical Diseases 7, e2540.CrossRefGoogle ScholarPubMed
de Delgado, O, Feliciangeli, MD, Gomez, B, Alvarado, J, Garcia, I and Bello, C (1998) The re-emergence of American visceral leishmaniasis in an old focus in Venezuela: present situation of human and canine infections. Parasite 5, 317323.CrossRefGoogle Scholar
de Freitas, JCC, Sampaio-Filho, AP, Santos, GJLS, Lima, AL and Nunes-Pinheiro, DCS (2013) Analysis of seasonality, tendencies and correlations in human and canine visceral leishmaniasis. Acta Scientiae Veterimariae 41, 1151.Google Scholar
de Oliveira, SS and de Araújo, TM (2003) Evaluation of control measures for visceral leishmaniasis (kala azar) in an endemic area in Bahia, Brazil (1995–2000). Cadernos de Saúde Pública 19, 16811690.Google Scholar
de Oliveira, ALL, Paniago, AMM, Sanches, MA, Dorval, MEC, Oshiro, ET, Leal, CRB, de Paula, FH, Pereira, LG, da Cunha, RV and Bóia, MN (2008) Asymptomatic infection in family contacts of patients with human visceral leishmaniasis in Três Lagoas, Mato Grosso do Sul State, Brazil. Cadernos de Saúde Pública, 24, 28272833.CrossRefGoogle Scholar
Desjeux, P. (2001) The increase in risk factors for leishmaniasis worldwide. Transactions of the Royal Society of Tropical Medicine and Hygiene 95, 239243.CrossRefGoogle ScholarPubMed
de Toledo, CRS, de Almeida, AS, Chaves, SAM, Sabroza, PC, Toledo, LM and Caldas, JP (2017) Vulnerability to the transmission of human visceral leishmaniasis in a Brazilian urban area. Revista de Saúde Pública 51, 49.CrossRefGoogle Scholar
dos Reis, LL, Balieiro, AAS, Fonseca, FR and Gonçalves, MJF (2019) Visceral leishmaniasis and its relationship with climate and environmental factors in the State of Tocantins, Brazil, from 2007 to 2014. Cadernos de Saúde Pública 35, e00047018.Google Scholar
Evans, TG, Teixeira, MJ, McAuliffe, IT, Vasconcelos, I, Vasconcelos, AW, Sousa, AA, Lima, JW and Pearson, RD (1992) Epidemiology of visceral leishmaniasis in northeast Brazil. The Journal of Infectious Diseases 166, 11241132.CrossRefGoogle ScholarPubMed
Falqueto, A, Ferreira, AL, dos Santos, CB, Porrozzi, R, da Costa, MVS, Teva, A, Cupolillo, E, Campos-Neto, A and Grimaldi, G JR (2009) Cross-sectional and longitudinal epidemiologic surveys of human and canine Leishmania infantum visceral infections in an endemic rural area of southeast Brazil (Pancas, Espírito Santo). The American Journal of Tropical Medicine and Hygiene 80, 559565.CrossRefGoogle Scholar
Feliciangeli, MD, Delgado, O, Suarez, B and Bravo, B (2006) Leishmania and sand flies: proximity to woodland as a risk factor for infection in a rural focus of visceral leishmaniasis in west central Venezuela. Tropical Medicine and International Health 11, 17851791.CrossRefGoogle Scholar
Gouvêa, MV, Werneck, GL, Costa, CHN and Carvalho, FAA (2007) Factors associated to Montenegro skin test positivity in Teresina, Brazil. Acta Tropica 104, 99107.CrossRefGoogle ScholarPubMed
Imamura, H, Downing, T, den Broeck, FV, Sanders, MJ, Rijal, S, Sundar, S, An Mannaert, A, Vanaerschot, M, Berg, M, Muylder, GD, Dumetz, F, Cuypers, B, Maes, I, Domagalska, M, Decuypere, S, Rai, K, Uranw, S, Bhattarai, NR, Khanal, B, Prajapati, VK, Sharma, S, Stark, O, Schönian, G, Koning, HPD, Settimo, L, Vanhollebeke, B, Roy, S, Ostyn, B, Boelaert, M, Maes, L, Berriman, M, Dujardin, JC and Cotton, JA (2016) Evolutionary genomics of epidemic visceral leishmaniasis in the Indian subcontinent. eLife 5, e12613.CrossRefGoogle ScholarPubMed
Jerônimo, SMB, Duggal, P, Braz, FSR, Cheng, C, Monteiro, GRG, Nascimento, ET, Martins, DRA, Karplus, TM, Ximenes, MFFM, Oliveira, CCG, Pinheiro, VG, Pereira, W, Peralta, JM, Sousa, J, Medeiros, IM, Pearsoni, RD, Burns, TL, Pugh, EW and Wilson, ME (2004) An emerging peri-urban pattern of infection with Leishmania chagasi, the protozoan causing visceral leishmaniasis in northeast Brazil. Scandinavian Journal of Infectious Diseases 36, 443449.CrossRefGoogle ScholarPubMed
Lima, ALM, de Lima, ID, Coutinho, JFV, de Sousa, UPST and Rodrigues, MAG (2017) Changing epidemiology of visceral leishmaniasis in northeastern Brazil: a 25-year follow-up of an urban outbreak. Transactions of the Royal Society of Tropical Medicine and Hygiene 111, 440447.CrossRefGoogle ScholarPubMed
Menezes, JA, Luz, TCB, de Sousa, FF, Verne, RN, Lima, FP and Margonari, C (2016) Peridomiciliary risk factors and knowledge concerning visceral leishmaniasis in the population of Formiga, Minas Gerais, Brazil. Revista Brasileira de Epidemiologia 19, 362374.CrossRefGoogle ScholarPubMed
Menon, SS, Rossi, R, Nshimyumukiza, L and Zinszer, K (2016) Decentralized control of human visceral leishmaniasis in endemic urban areas of Brazil: a literature review. Tropical Medicine and Health 44, 9.CrossRefGoogle ScholarPubMed
Missawa, NA and Dias, ES (2007) Phlebotomine sand flies (Diptera: Psychodidae) in the municipality of Várzea Grande: an area of transmission of visceral leishmaniasis in the state of Mato Grosso, Brazil. Memória do Instituto Oswaldo Cruz 102, 913918.CrossRefGoogle ScholarPubMed
Moher, D, Liberati, A, Tetzlaff, J, Altman, DG and Group, PRISMA (2015) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Open Medicine 3 123130.Google Scholar
Moreno, EC, Melo, MN, Genaro, O, Lambertucci, JR, Serufo, JC, Andrade, ASR, Antunes, CMF and Carneiro, M (2005) Risk factors for Leishmania chagasi infection in an urban area of Minas Gerais state. Revista da Sociedade Brasileira de Medicina Tropical 38, 456463.CrossRefGoogle Scholar
Nascimento, MD, Alcântara-Neves, NM, Muniz, ME, Nunes, SF, Paranhos, M and Carvalho, LC (1993) Induction and modulation of the immune response to Leishmania by Montenegro's skin test. Transactions of the Royal Society of Tropical Medicine and Hygiene 87, 9193.CrossRefGoogle ScholarPubMed
Oliveira, CL, Assunção, RM, Reis, IA and Proietti, FA (2001) Distribuição espacial da leishmaniose visceral humana e canina em Belo Horizonte, Minas Gerais, Brasil, 1994–1997. Cadernos de Saúde Pública 17, 12311239.CrossRefGoogle Scholar
Oliveira, CL, Diez-Roux, A, César, CC and Projetti, FA (2006) A case-control study of microenvironmental risk factors for urban visceral leishmaniasis in a large city of Brazil, 1999–2000. Revista Panamericana de Salud Publica 20, 369376.CrossRefGoogle Scholar
Oliveira, IBB, Batista, HL, Peluzio, JM, Pfrimer, IAH, Rodrigues, FM and Carmo-Filho, JR (2014) Epidemiological and environmental aspects of visceral leishmaniasis in children under 15 years of age between 2007 and 2012 in the City of Araguaína, State of Tocantins, Brazil. Revista da Sociedade Brasileira de Medicina Tropical 47, 476482.CrossRefGoogle ScholarPubMed
Otranto, D, Testini, G, Buonavoglia, C, Parisi, A, Brandonisio, O, Circella, H, Dantas-Torres, F and Camarda, A (2010) Experimental and field investigations on the role of birds as hosts of Leishmania infantum, with emphasis on the domestic chicken. Acta Tropica 113, 8083.CrossRefGoogle ScholarPubMed
Ponte, CB, Souza, NC, Cavalcante, MN, Barral, AMP, de Aquino, DMC and Caldas, AJM (2011) Risk factors for Leishmania chagasi infection in an endemic area in Raposa, State of Maranhão, Brazil. Revista da Sociedade Brasileira de Medicina Tropical 44, 712721.CrossRefGoogle Scholar
Rêgo, FD, Souza, GD, Miranda, JB, Peixoto, LV and Andrade-Filho, JD (2020) Potential vectors of Leishmania parasites in a recent focus of visceral Leishmaniasis in neighborhoods of Porto Alegre, State of Rio Grande do Sul, Brazil. Journal of Medical Entomology 57, 12861292.CrossRefGoogle Scholar
Resende, MC, Camargo, MC, Vieira, JR, Nobi, RC, Porto, MN, Oliveira, CD, Pessanha, JE, Cunga, MDA, Brandão, ST (2006) Seasonal variation of Lutzomyia longipalpis in Belo Horizonte, State of Minas Gerais Revista da Sociedade Brasileira de Medicina Tropical 39, 51-55..CrossRefGoogle Scholar
Rivas, GB, de Souza, NA, Peixoto, AA and Bruno, RV (2014) Effects of temperature and photoperiod on daily activity rhythms of Lutzomyia longipalpis (Diptera: Psychodidae). Parasites Vectors 7, 278.CrossRefGoogle Scholar
Rocha, ATF, de Espindola, GM, Soares, MRAS, Rocha, JRS and Costa, CHNC (2018) Visceral leishmaniasis and vulnerability conditions in an endemic urban area of northeastern Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 112, 317325.CrossRefGoogle Scholar
Romero, GA and Boelaert, M (2010) Control of visceral leishmaniasis in Latin America – a systematic review. PLoS Neglected Tropical Diseases 4, e584.CrossRefGoogle ScholarPubMed
Sevá, AP, Mao, L, Galvis-Ovallos, F, Lima, JMT and Valle, D (2017) Risk analysis and prediction of visceral leishmaniasis dispersion in São Paulo State, Brazil. PLoS Neglected Tropical Diseases 11, e0005353.CrossRefGoogle ScholarPubMed
Sharma, MC, Gupta, AK, Saran, R and Sinha, SP (1990) The effect of age and sex on the incidence of kala-azar. The Journal of Communicable Diseases 22, 277278.Google ScholarPubMed
Sherlock, IA 1996 Ecological interactions of visceral leishmaniasis in the State of Bahia, Brazil. Memórias do Instituto Oswaldo Cruz 91, 671683.CrossRefGoogle ScholarPubMed
Silva, LDA, Romero, HD, Prata, A, Costa, RT, Nascimento, E, Carvalho, SFG and Rodrigues, V (2006). Immunologic tests in patients after clinical cure of visceral leishmaniasis. American Journal of Tropical Medicine and Hygiene 75, 739743.CrossRefGoogle Scholar
Viana, GMC, Nascimento, MDSB, Rabelo, EMF, Diniz-Neto, JA, Binda-Júnior, JR, Galvão, CSS, dos Santos, AC, Santos-Júnior, OM, de Oliveira, RAS and Guimarães, RS (2011) Relationship between rainfall and temperature: observations on the cases of visceral leishmaniasis in São Luis Island, State of Maranhão, Brazil. Revista da Sociedade Brasileira de Medicina Tropical 44, 722724.CrossRefGoogle ScholarPubMed
Werneck, GL and Maguire, JH (2002) Spatial modelling using mixed models: an ecological study of visceral leishmaniasis in Teresina, Piauí State, Brazil. Cadernos de Saúde Pública 18, 633637.CrossRefGoogle Scholar
Werneck, GL, Rodrigue- Júnior, L, Santos, MV, Araújo, IB, Moura, LS, Lima, SS, Gomes, RBB, Maguire, JH and Costa, CHN (2002) The burden of Leishmania chagasi infection during an urban outbreak of visceral leishmaniasis in Brazil. Acta Tropica 83, 1318.CrossRefGoogle ScholarPubMed
Werneck, GL, Costa, CNH, Wlaker, AM, David, JR, Wand, M and Maguire, JH (2007) Multilevel modelling of the incidence of visceral leishmaniasis in Teresina, Brazil. Epidemiology and Infection 135, 195201.CrossRefGoogle ScholarPubMed
World Health Organization (2018) Status of endemicity of visceral leishmaniasis worldwide. Available at https://www.who.int/docs/default-source/ntds/leishmaniasis/gho-vl-2018.pdf?sfvrsn=b748935a_4 (Accessed 29 June 2019).Google Scholar
Ximenes, MFFM, e Silva, VPM, de Queiroz, PVS, Rego, MM, Cortez, AM, Batista, LMM, de Medeiros, AS and Jeronimio, SMB (2007) Flebotomíneos (Diptera: Psychodidae) e leishmanioses no Rio Grande do Norte, Nordeste do Brasil: reflexos do ambiente antrópico. Neotropical Entomology 36, 128137.CrossRefGoogle Scholar
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