Halliday JEB , Hampson K , Hanley N , Lembo T , Sharp JP , Haydon DT , Cleaveland S , 2017. Driving improvements in emerging disease surveillance through locally relevant capacity strengthening. Science 357: 146–148.
Jayatilleke K , 2020. Challenges in implementing surveillance tools of high-income countries (HICs) in low middle income countries (LMICs). Curr Treat Options Infect Dis 123: 191–201.
Grubaugh ND et al., 2015. Xenosurveillance: a novel mosquito-based approach for examining the human-pathogen landscape. PLoS Negl Trop Dis 9: e0003628.
Fauver JR , Gendernalik A , Weger-Lucarelli J , Grubaugh ND , Brackney DE , Foy BD , Ebel GD , 2017. The use of xenosurveillance to detect human bacteria, parasites, and viruses in mosquito bloodmeals. Am J Trop Med Hyg 97: 324–329.
Yang Y , Garver LS , Bingham KM , Hang J , Jochim RC , Davidson SA , Richardson JH , Jarman RG , 2015. Feasibility of using the mosquito blood meal for rapid and efficient human and animal virus surveillance and discovery. Am J Trop Med Hyg 93: 1377–1382.
Fauver JR , Weger-Lucarelli J , Fakoli LS III , Bolay K , Bolay FK , Diclaro JW , Brackney DE , Foy BD , Stenglein MD , Ebel GD , 2018. Xenosurveillance reflects traditional sampling techniques for the identification of human pathogens: a comparative study in West Africa. PLoS Negl Trop Dis 12: 0006348.
Asturias EJ et al., 2016. The Center for Human Development in Guatemala: an innovative model for global population health. Adv Pediatr 63: 357–387.
Olson D et al., 2017. Performance of a mobile phone app-based participatory syndromic surveillance system for acute febrile illness and acute gastroenteritis in rural Guatemala. J Med Internet Res 19. e368.
World Health Organization , 2005. Handbook: IMCI Integrated Management of Childhood Illness. Geneva, Switzerland: WHO. Available at: https://apps.who.int/iris/handle/10665/42939. Accessed July 28, 2021.
Cark-Gil S , Darsie F , 1983. The mosquitoes of Guatemala. Their identification, distribution and bionomics, with keys to adult females and larvae in English and Spanish. Mosq Syst 15: 151–284.
Hemmerter S , Šlapeta J , Van Den Hurk AF , Cooper RD , Whelan PI , Russell RC , Johansen CA , Beebe NW , 2007. A curious coincidence: mosquito biodiversity and the limits of the Japanese encephalitis virus in Australasia. BMC Evol Biol 7, doi: 10.1186/1471-2148-7-100.
Ivanova NV , Zemlak TS , Hanner RH , Hebert PDN , 2007. Universal primer cocktails for fish DNA barcoding. Mol Ecol Notes 7: 544–548.
Ratnasingham S , Hebert PDN , 2016. BOLD: the barcode of life data system (www.barcodinglife.org). Mol Ecol Notes 2007: 355–364.
Fauver JR , Akter S , Morales AIO , Black WC , Rodriguez AD , Stenglein MD , Ebel GD , Weger-Lucarelli J , 2019. A reverse-transcription/RNase H based protocol for depletion of mosquito ribosomal RNA facilitates viral intrahost evolution analysis, transcriptomics and pathogen discovery. Virology 528: 181–197.
Chrzastek K , Lee DH , Smith D , Sharma P , Suarez DL , Pantin-Jackwood M , Kapczynski DR , 2017. Use of sequence-independent, single-primer-amplification (SISPA) for rapid detection, identification, and characterization of avian RNA viruses. Virology 509: 159–166.
Cross S , Kapuscinski ML , Perino J , Maertens BL , Weger-Lucarelli J , Ebel GD , Stenglein MD , 2018. Co-infection patterns in individual Ixodes scapularis ticks reveal associations between viral, eukaryotic and bacterial microorganisms. Viruses 10: 388.
Fauver JR et al., 2016. West African Anopheles gambiae mosquitoes harbor a taxonomically diverse virome including new insect-specific flaviviruses, mononegaviruses, and totiviruses. Virology 498: 288–299.
Babraham Bioinformatics FastQC. A Quality Control Tool for High Throughput Sequence Data. Available at: https://www.bioinformatics.babraham.ac.uk/projects/fastqc/. Accessed June 16, 2021.
Martin M , 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17: 10.
Li W , Godzik A , 2006. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658–1659.
Bankevich A et al., 2012. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19: 455–477.
Camacho C , Coulouris G , Avagyan V , Ma N , Papadopoulos J , Bealer K , Madden TL , 2009. BLAST+: architecture and applications. BMC Bioinformatics 10: 1–9.
Altschul SF , Gish W , Miller W , Myers EW , Lipman DJ , 1990. Basic local alignment search tool. J Mol Biol 215: 403–410.
Buchfink B , Xie C , Huson DH , 2014. Fast and sensitive protein alignment using DIAMOND. Nat Methods 12: 59–60.
Laue T , Emmerich P , Schmitz H , 1999. Detection of dengue virus RNA in patients after primary or secondary dengue infection by using the TaqMan automated amplification system. J Clin Microbiol 37: 2543–2547.
Gyawali N , Murphy AK , Hugo LE , Devine GJ , 2020. A micro-PRNT for the detection of Ross River virus antibodies in mosquito blood meals: a useful tool for inferring transmission pathways. PLoS One 15: e0229314.
Reeves LE , Gillett-Kaufman JL , Kawahara AY , Kaufman PE , 2018. Barcoding blood meals: New vertebrate-specific primer sets for assigning taxonomic identities to host DNA from mosquito blood meals. PLoS Negl Trop Dis 12: e0006767.
Abudurexiti A et al., 2019. Taxonomy of the order Bunyavirales: update 2019. Arch Virol 164: 1949–1965.
Cowling DW , Gardner IA , Johnson WO , 1999. Comparison of methods for estimation of individual-level prevalence based on pooled samples. Prev Vet Med 39: 211–225.
Barr AR et al., 1975. Review article: host-feeding patterns of mosquitoes, with a review of advances in analysis of blood meals by serology. J Med Entomol 11: 635–653.
Takken W , Verhulst NO , 2013. Host preferences of blood-feeding mosquitoes. Annu Rev Entomol 58: 433–453.
Kading RC , Biggerstaff BJ , Young G , Komar N , 2014. Mosquitoes used to draw blood for arbovirus viremia determinations in small vertebrates. PLoS One 9: e99342.
Guzman MG et al., 2010. Dengue: a continuing global threat. Nat Rev Microbiol 8: S7–S16.
Ramos-Nino ME , Fitzpatrick DM , Eckstrom KM , Tighe S , Hattaway LM , Hsueh AN , Stone DM , Dragon JA , Cheetham S , 2020. Metagenomic analysis of Aedes aegypti and Culex quinquefasciatus mosquitoes from Grenada, West Indies. PLoS One 15: e0231047.
da Silva Ferreira R et al., 2020. Insect-specific viruses and arboviruses in adult male culicids from midwestern Brazil. Infect Genet Evol 85: 104561.
Pauvolid-Corrêa C , Solberg A , Couto-Lima O , Nogueira DM , Langevin RM , Komar S , 2016. Novel viruses isolated from mosquitoes in Pantanal, Brazil. Genome Announc 4: 1195–1211.
Ribeiro GdO et al., 2019. Detection of RNA-dependent RNA polymerase of hubei reo-like virus 7 by next-generation sequencing in Aedes aegypti and Culex quinquefasciatus Mosquitoes from Brazil. Viruses 11: 147.
Vibin J , Chamings A , Collier F , Klaassen M , Nelson TM , Alexandersen S , 2018. Metagenomics detection and characterisation of viruses in faecal samples from Australian wild birds. Sci Rep 8: 8686
Vasilakis N , Tesh RB , 2015. Insect-specific viruses and their potential impact on arbovirus transmission. Curr Opin Virol 15: 69–74.
Öhlund P , Lundén H , Blomström AL , 2019. Insect-specific virus evolution and potential effects on vector competence. Virus Genes 55: 127.
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Surveillance methods that permit rapid detection of circulating pathogens in low-resource settings are desperately needed. In this study, we evaluated a mosquito bloodmeal-based surveillance method (“xenosurveillance”) in rural Guatemala. Twenty households from two villages (Los Encuentros and Chiquirines) in rural southwest Guatemala were enrolled and underwent weekly prospective surveillance from August 2019 to December 2019 (16 weeks). When febrile illness was reported in a household, recently blood-fed mosquitoes were collected from within dwellings and blood samples taken from each member of the household. Mosquitoes were identified to species and blood sources identified by sequencing. Shotgun metagenomic sequencing was used to identify circulating viruses. Culex pipiens (60.9%) and Aedes aegypti (18.6%) were the most abundant mosquitoes collected. Bloodmeal sources were most commonly human (32.6%) and chicken (31.6%), with various other mammal and avian hosts detected. Several mosquito-specific viruses were detected, including Culex orthophasma virus. Human pathogens were not detected. Therefore, xenosurveillance may require more intensive sampling to detect human pathogens in Guatemala and ecologically similar localities in Central America.
Financial support: This work was supported by a seed grant from the Colorado State University One Health Institute and by Colorado State University’s Office of the Vice President for Research. V. S. was partially supported by Colorado State University’s Office of the Vice President for Research. The content is solely the responsibility of the authors and does not necessarily represent the official views of the Office of the Vice President for Research. D. O. is supported by
Authors’ addresses: Rebekah J. McMinn, Valeria Scorza, Michael C. Young, Delaney Worthington, Emma K. Harris, Brian D. Foy, Mark D. Stenglein, and Gregory D. Ebel, Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, CO, E-mails: rebekah.mcminn@colostate.edu, andrea.scorza@colostate.edu, emceeyoung@gmail.com, delaney.worthington20@alumni.colostate.edu, emkate.harris@colostate.edu, brian.foy@colostate.edu, mark.stenglein@colostate.edu, and gregory.ebel@colostate.edu. Andrea Chacon, Fundacion para la Salud Integral de los Guatemaltecos, Retalhuleu, Guatemala, E-mail: chaconjuarez@gmail.com. Claudia Rückert, Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, CO, and Department of Biochemistry and Molecular Biology, University of Nevada, Reno, NV, E-mail: crueckert@unr.edu. Molly M. Lamb, Colorado School of Public Health, Aurora, CO, E-mail: molly.lamb@cuanschutz.edu. Ramon E. Medrano and Maria Renee Lopez, Centro de Estudios en Salud, Universidad del Valle de Guatemala, Guatemala City, Guatemala, E-mails: estuardomedranoe@gmail.com and mlopez@ces.uvg.edu.gt. Kareen Arias, Center for Human Development, Retalhuleu, Guatemala, E-mail: kareen.arias@gmail.com. Edwin J. Asturias and Daniel Olson, Colorado School of Public Health, Aurora, CO, Center for Human Development, Retalhuleu, Guatemala, and Department of Pediatrics, Section of Infectious Diseases, University of Colorado School of Medicine, Aurora, CO, E-mails: edwin.asturias@childrenscolorado.org and daniel.olson@childrenscolorado.org.
Halliday JEB , Hampson K , Hanley N , Lembo T , Sharp JP , Haydon DT , Cleaveland S , 2017. Driving improvements in emerging disease surveillance through locally relevant capacity strengthening. Science 357: 146–148.
Jayatilleke K , 2020. Challenges in implementing surveillance tools of high-income countries (HICs) in low middle income countries (LMICs). Curr Treat Options Infect Dis 123: 191–201.
Grubaugh ND et al., 2015. Xenosurveillance: a novel mosquito-based approach for examining the human-pathogen landscape. PLoS Negl Trop Dis 9: e0003628.
Fauver JR , Gendernalik A , Weger-Lucarelli J , Grubaugh ND , Brackney DE , Foy BD , Ebel GD , 2017. The use of xenosurveillance to detect human bacteria, parasites, and viruses in mosquito bloodmeals. Am J Trop Med Hyg 97: 324–329.
Yang Y , Garver LS , Bingham KM , Hang J , Jochim RC , Davidson SA , Richardson JH , Jarman RG , 2015. Feasibility of using the mosquito blood meal for rapid and efficient human and animal virus surveillance and discovery. Am J Trop Med Hyg 93: 1377–1382.
Fauver JR , Weger-Lucarelli J , Fakoli LS III , Bolay K , Bolay FK , Diclaro JW , Brackney DE , Foy BD , Stenglein MD , Ebel GD , 2018. Xenosurveillance reflects traditional sampling techniques for the identification of human pathogens: a comparative study in West Africa. PLoS Negl Trop Dis 12: 0006348.
Asturias EJ et al., 2016. The Center for Human Development in Guatemala: an innovative model for global population health. Adv Pediatr 63: 357–387.
Olson D et al., 2017. Performance of a mobile phone app-based participatory syndromic surveillance system for acute febrile illness and acute gastroenteritis in rural Guatemala. J Med Internet Res 19. e368.
World Health Organization , 2005. Handbook: IMCI Integrated Management of Childhood Illness. Geneva, Switzerland: WHO. Available at: https://apps.who.int/iris/handle/10665/42939. Accessed July 28, 2021.
Cark-Gil S , Darsie F , 1983. The mosquitoes of Guatemala. Their identification, distribution and bionomics, with keys to adult females and larvae in English and Spanish. Mosq Syst 15: 151–284.
Hemmerter S , Šlapeta J , Van Den Hurk AF , Cooper RD , Whelan PI , Russell RC , Johansen CA , Beebe NW , 2007. A curious coincidence: mosquito biodiversity and the limits of the Japanese encephalitis virus in Australasia. BMC Evol Biol 7, doi: 10.1186/1471-2148-7-100.
Ivanova NV , Zemlak TS , Hanner RH , Hebert PDN , 2007. Universal primer cocktails for fish DNA barcoding. Mol Ecol Notes 7: 544–548.
Ratnasingham S , Hebert PDN , 2016. BOLD: the barcode of life data system (www.barcodinglife.org). Mol Ecol Notes 2007: 355–364.
Fauver JR , Akter S , Morales AIO , Black WC , Rodriguez AD , Stenglein MD , Ebel GD , Weger-Lucarelli J , 2019. A reverse-transcription/RNase H based protocol for depletion of mosquito ribosomal RNA facilitates viral intrahost evolution analysis, transcriptomics and pathogen discovery. Virology 528: 181–197.
Chrzastek K , Lee DH , Smith D , Sharma P , Suarez DL , Pantin-Jackwood M , Kapczynski DR , 2017. Use of sequence-independent, single-primer-amplification (SISPA) for rapid detection, identification, and characterization of avian RNA viruses. Virology 509: 159–166.
Cross S , Kapuscinski ML , Perino J , Maertens BL , Weger-Lucarelli J , Ebel GD , Stenglein MD , 2018. Co-infection patterns in individual Ixodes scapularis ticks reveal associations between viral, eukaryotic and bacterial microorganisms. Viruses 10: 388.
Fauver JR et al., 2016. West African Anopheles gambiae mosquitoes harbor a taxonomically diverse virome including new insect-specific flaviviruses, mononegaviruses, and totiviruses. Virology 498: 288–299.
Babraham Bioinformatics FastQC. A Quality Control Tool for High Throughput Sequence Data. Available at: https://www.bioinformatics.babraham.ac.uk/projects/fastqc/. Accessed June 16, 2021.
Martin M , 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17: 10.
Li W , Godzik A , 2006. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658–1659.
Bankevich A et al., 2012. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19: 455–477.
Camacho C , Coulouris G , Avagyan V , Ma N , Papadopoulos J , Bealer K , Madden TL , 2009. BLAST+: architecture and applications. BMC Bioinformatics 10: 1–9.
Altschul SF , Gish W , Miller W , Myers EW , Lipman DJ , 1990. Basic local alignment search tool. J Mol Biol 215: 403–410.
Buchfink B , Xie C , Huson DH , 2014. Fast and sensitive protein alignment using DIAMOND. Nat Methods 12: 59–60.
Laue T , Emmerich P , Schmitz H , 1999. Detection of dengue virus RNA in patients after primary or secondary dengue infection by using the TaqMan automated amplification system. J Clin Microbiol 37: 2543–2547.
Gyawali N , Murphy AK , Hugo LE , Devine GJ , 2020. A micro-PRNT for the detection of Ross River virus antibodies in mosquito blood meals: a useful tool for inferring transmission pathways. PLoS One 15: e0229314.
Reeves LE , Gillett-Kaufman JL , Kawahara AY , Kaufman PE , 2018. Barcoding blood meals: New vertebrate-specific primer sets for assigning taxonomic identities to host DNA from mosquito blood meals. PLoS Negl Trop Dis 12: e0006767.
Abudurexiti A et al., 2019. Taxonomy of the order Bunyavirales: update 2019. Arch Virol 164: 1949–1965.
Cowling DW , Gardner IA , Johnson WO , 1999. Comparison of methods for estimation of individual-level prevalence based on pooled samples. Prev Vet Med 39: 211–225.
Barr AR et al., 1975. Review article: host-feeding patterns of mosquitoes, with a review of advances in analysis of blood meals by serology. J Med Entomol 11: 635–653.
Takken W , Verhulst NO , 2013. Host preferences of blood-feeding mosquitoes. Annu Rev Entomol 58: 433–453.
Kading RC , Biggerstaff BJ , Young G , Komar N , 2014. Mosquitoes used to draw blood for arbovirus viremia determinations in small vertebrates. PLoS One 9: e99342.
Guzman MG et al., 2010. Dengue: a continuing global threat. Nat Rev Microbiol 8: S7–S16.
Ramos-Nino ME , Fitzpatrick DM , Eckstrom KM , Tighe S , Hattaway LM , Hsueh AN , Stone DM , Dragon JA , Cheetham S , 2020. Metagenomic analysis of Aedes aegypti and Culex quinquefasciatus mosquitoes from Grenada, West Indies. PLoS One 15: e0231047.
da Silva Ferreira R et al., 2020. Insect-specific viruses and arboviruses in adult male culicids from midwestern Brazil. Infect Genet Evol 85: 104561.
Pauvolid-Corrêa C , Solberg A , Couto-Lima O , Nogueira DM , Langevin RM , Komar S , 2016. Novel viruses isolated from mosquitoes in Pantanal, Brazil. Genome Announc 4: 1195–1211.
Ribeiro GdO et al., 2019. Detection of RNA-dependent RNA polymerase of hubei reo-like virus 7 by next-generation sequencing in Aedes aegypti and Culex quinquefasciatus Mosquitoes from Brazil. Viruses 11: 147.
Vibin J , Chamings A , Collier F , Klaassen M , Nelson TM , Alexandersen S , 2018. Metagenomics detection and characterisation of viruses in faecal samples from Australian wild birds. Sci Rep 8: 8686
Vasilakis N , Tesh RB , 2015. Insect-specific viruses and their potential impact on arbovirus transmission. Curr Opin Virol 15: 69–74.
Öhlund P , Lundén H , Blomström AL , 2019. Insect-specific virus evolution and potential effects on vector competence. Virus Genes 55: 127.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 1381 | 1028 | 82 |
Full Text Views | 1139 | 77 | 9 |
PDF Downloads | 249 | 58 | 5 |