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Repellent activity of the non-host semiochemical (E)-2-octenal against Amblyomma sculptum and Amblyomma dubitatum ticks under field conditions

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Abstract

Amblyomma ticks pose a significant public health threat due to their potential to transmit pathogens associated with rickettsial diseases. (E)-2-octenal, a compound found in donkeys (Equus asinus), exhibits strong repellent properties against Amblyomma sculptum nymphs under laboratory conditions. This study assessed the effectiveness of the (E)-2-octenal in wearable slow-release devices for personal human protection against Amblyomma ticks under natural conditions. Slow-release devices treated with (E)-2-octenal and untreated controls were prepared and tested on two volunteers walking through a tick-infested area in Goiania, Brazil. The experiment was conducted twice daily for three series of 10 days, with each volunteer wearing two devices attached to each leg, one on the ankle and one just above the thigh. Volunteers with control and treated devices exchanged them between rounds. Also, the daily release rate of (E)-2-octenal from the slow-release devices was determined in the laboratory, increasing significantly from 0.77 ± 0.14 µg/day on the first day to 9.93 ± 1.92 µg/day on the 4th day and remaining constant until the 16th day. A total of 5409 ticks were collected from both volunteers. Treated devices resulted in recovering fewer ticks (n = 1,666; 31%) compared to untreated devices (control: n = 3,743; 69%). (E)-2-octenal effectively repelled Amblyomma spp. larvae, A. sculptum adults, and exhibited pronounced repellency against A. dubitatum nymphs and adults. These findings suggest the potential of (E)-2-octenal delivered by wearable slow-release devices as a green-based repellent. Further improvements, however, are necessary to provide better protection for humans against A. sculptum and A. dubitatum in field conditions.

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References

  • Acke S, Couvreur S, Bramer WM, Schmickler MN, De Schryver A, Haagsma JA (2022) Global infectious disease risks associated with occupational exposure among non-healthcare workers: a systematic review of the literature. Occup Environ Med 79:63–71. https://doi.org/10.1136/oemed-2020-107164

    Article  PubMed  Google Scholar 

  • Almeida AP, Cunha LM, Bello AC, da Cunha AP, Domingues LN, Leite RC, Labruna MB (2011) A novel Rickettsia infecting Amblyomma dubitatum ticks in Brazil. Ticks Tick Borne Dis 2:209–212. https://doi.org/10.1016/j.ttbdis.2011.08.003

    Article  PubMed  Google Scholar 

  • Alvares CA, Stape JL, Sentelhas PC, De Moraes Gonçalves JL, Sparovek G (2013) Köppen’s climate classification map for Brazil. Meteorol Zeitschrift 22:711–728. https://doi.org/10.1127/0941-2948/2013/0507

    Article  Google Scholar 

  • Araújo RP, Navarro MBMA, Cardoso TAO (2015) Febre maculosa no Brasil: estudo da mortalidade para a vigilância epidemiológica. Cad Saúde Colet 23:354–361. https://doi.org/10.1590/1414-462X201500040094

    Article  Google Scholar 

  • Barbieri ARM, Szabó MPJ, Costa FB, Martins TF, Soares HS, Pascoli G, Torga K, Saraiva DG, Ramos VN, Osava C, Gerardi M, Dias RA, Moraes EA Jr, Ferreira F, Castro MB, Labruna MB (2019) Species richness and seasonal dynamics of ticks with notes on rickettsial infection in a Natural Park of the Cerrado biome in Brazil. Ticks Tick Borne Dis 10:442–453

    Article  PubMed  Google Scholar 

  • Barreto LP, Ribeiro-Silva CS, Machado LDC, Lima VH, Pinto SMN, Pereira-Junior RA, Carreira DN, Mascarin GM, Fernandes ÉKK, Borges LMF (2021) Efficacy of collars with allomones on dogs to control Rhipicephalus sanguineus sensu lato infestations under field conditions. Ticks Tick Borne Dis 12:101769. https://doi.org/10.1016/j.ttbdis.2021.101769

    Article  PubMed  Google Scholar 

  • Benelli G, Pavela R, Canale A, Mehlhorn H (2016) Tick repellents and acaricides of botanical origin: a green roadmap to control tick-borne diseases? Parasitol Res 115:2545–2560

    Article  PubMed  Google Scholar 

  • Bissinger BW, Roe RM (2010) Tick repellents: past, present, and future. Pesticide Biochem Physiol 96:63–79

  • Bissinger BW, Apperson CS, Watson DW, Arellano C, Sonenshine DE, Roe RM (2011) Novel field assays and the comparative repellency of BioUD®, DEET and permethrin against Amblyomma americanum. Med Vet Entomol 25:217–226

    Article  CAS  PubMed  Google Scholar 

  • Borges LMF, Oliveira Filho JG, Ferreira LL, Louly CCB, Pickett JA, Birkett MA (2015) Identification of non-host semiochemicals for the brown dog tick, Rhipicephalus sanguineus sensu lato (Acari: Ixodidae), from tick-resistant beagles, Canis lupus familiaris. Ticks Tick Borne Dis 6:676–682

    Article  PubMed  Google Scholar 

  • Brugman VA, Smallegange RC, Logan JG (2018) Semiochemical tools for a new generation of livestock pest control. Ecol Control Vector Borne Dis 5:389–434

    Google Scholar 

  • Castagnolli KC, Figueiredo LB, Santana DA, Castro MB, Romano MA, Szabó MPJ (2003) Acquired resistance of horses to Amblyomma cajennense (Fabricius, 1787) ticks. Vet Parasitol 117:271–283

    Article  PubMed  Google Scholar 

  • CDC - Centers for Disease Control and Prevention (2022) Preventing tick bites. https://www.cdc.gov/ticks/avoid/on_people.html. Accessed 24 Nov 2022

  • Dantas-Torres F, Onofrio VC, Barros-Battesti DM (2009) The ticks (Acari: Ixodida: Argasidae, Ixodidae) of Brazil. Syst Appl Acarol 14:30–46

    Google Scholar 

  • Dantas-Torres F, Martins TF, Muñoz-Leal S, Onofrio VC, Barros-Battesti DM (2019) Ticks (Ixodida: Argasidae, Ixodidae) of Brazil: updated species checklist and taxonomic keys. Ticks Tick Borne Dis 10:101252. https://doi.org/10.1016/j.ttbdis.2019.06.012

    Article  PubMed  Google Scholar 

  • Dantas-Torres F, Melo MF, Sales KGDS, Sousa-Paula LCD, da Silva FJ, Figueredo LA, Labruna MB (2021) Seasonal dynamics and rickettsial infection in free-living Amblyomma dubitatum in the Atlantic Forest biome in north-eastern Brazil. Acta Trop 217:1–7. https://doi.org/10.1016/j.actatropica.2021.105854

    Article  CAS  Google Scholar 

  • Dautel H, Dippel C, Werkhausen A, Diller R (2013) Efficacy testing of several Ixodes ricinus tick repellents: different results with different assays. Ticks Tick Borne Dis 4:256–263

    Article  PubMed  Google Scholar 

  • de la Fuente J, Estrada-Pena A, Venzal JM, Kocan KM, Sonenshine DE (2008) Overview: ticks as vectors of pathogens that cause disease in humans and animals. Front Biosci 13:6938–6946. https://doi.org/10.2741/3200

    Article  PubMed  Google Scholar 

  • de Paula LGF, Zeringóta V, Sampaio ALN, Bezerra GP, Barreto ALG, dos Santos AA, Miranda VC, Paula WVF, Neves LC, Secchis MV, Alves SGA, Sevá AP, Borges LMF, Monteiro C, Dantas-Torres F, Krawczak FS (2021) Seasonal dynamics of Amblyomma sculptum in two areas of the Cerrado biome midwestern Brazil, where human cases of rickettsiosis have been reported. Exp Appl Acarol 84:215–225

    Article  PubMed  Google Scholar 

  • Donalisio MR, Souza CE, Angerami RN, Samy AM (2020) Mapping Brazilian spotted fever: linking etiological agent, vectors, and hosts. Acta Trop 207:105496. https://doi.org/10.1016/j.actatropica.2020.105496

    Article  CAS  PubMed  Google Scholar 

  • Eisen L, Stafford KC (2021) Barriers to effective tick management and tick-bite prevention in the United States (Acari: Ixodidae). J Med Entomol 58:1588–1600

    Article  PubMed  Google Scholar 

  • Faccini-Martínez AA, Krawczak FS, Oliveira SV, Labruna MB, Angerami RN (2021) Rickettsioses in Brazil: distinct diseases and new paradigms for epidemiological surveillance. Rev Soc Bras Med Trop 54:e07322020. https://doi.org/10.1590/0037-8682-0732-2020

    Article  PubMed  PubMed Central  Google Scholar 

  • Falce HC, Flechtmann CH, Fernandes BF (1983) Ixodidae (Acari) on horses, mules and asses in the State of Paraná, Brazil. Rev Facul Med Vet Zoo 20:103–106

    Article  Google Scholar 

  • Faraone N, MacPherson S, Hillier NK (2019) Behavioral responses of Ixodes scapularis tick to natural products: development of novel repellents. Exp Appl Acarol 79(2):195–207. https://doi.org/10.1007/s10493-019-00421-0

    Article  CAS  PubMed  Google Scholar 

  • Ferreira LL, Sarria ALF, Oliveira Filho JG, Silva FO, Powers SJ, Caulfield JC, Pickett JA, Birkett MA, Borges LMF (2019) Identification of a non-host semiochemical from tick-resistant donkeys (Equus asinus) against Amblyomma sculptum ticks. Ticks Tick Borne Dis 10:621–627

    Article  PubMed  PubMed Central  Google Scholar 

  • Garira W, Chirove F (2020) A general method for multiscale modelling of vector-borne disease systems. Interface Focus 10:20190047

    Article  PubMed  Google Scholar 

  • Jongejan F, Uilenberg G (2004) The global importance of ticks. Parasitology 129(Suppl):S3-14. https://doi.org/10.1017/s0031182004005967

    Article  PubMed  Google Scholar 

  • Krawczak FS, Martins TF, Oliveira CS, Binder LC, Costa FB, Nunes PH, Gregori F, Labruna MB (2015) Amblyomma yucumense n. sp. (Acari: Ixodidae), a parasite of wild mammals in Southern Brazil. J Med Entomol 52:28–37

    Article  PubMed  Google Scholar 

  • Labruna MB (2009) Ecology of rickettsia in South America. Ann N Y Acad Sci 1166:156–166. https://doi.org/10.1111/j.1749-6632.2009.04516.x.PMid:19538276

    Article  PubMed  Google Scholar 

  • Labruna MB, Pinter A, Castro MB, Castagnolli KC, Szabó MJP (2002) Some records on host questing behavior of Amblyomma cajennense (Acari: Ixodidae) larvae. Rev Bras Parasitol Vet 11:91–93

    Google Scholar 

  • Labruna MB, Whitworth T, Horta MC, Bouyer DH, McBride JW, Pinter A, Popov V, Gennari SM, Walker DH (2004a) Rickettsia species infecting Amblyomma cooperi ticks from an area in the state of São Paulo, Brazil, where Brazilian spotted fever is endemic. J Clin Microbiol 42:90–98

    Article  PubMed  PubMed Central  Google Scholar 

  • Labruna MB, Whitworth T, Bouyer DH, McBride J, Camargo LM, Camargo EP, Popov V, Walker DH (2004b) Rickettsia bellii and Rickettsia amblyommii in Amblyomma ticks from the state of Rondônia, Western Amazon, Brazil. J Med Entomol 41:1073–1081

    Article  PubMed  Google Scholar 

  • Labruna MB, Pacheco RC, Ataliba AC, Szabó MPJ (2007) Human parasitism by the capybara tick Amblyomma dubitatum (Acari: Ixodidae). Entomol News 118:77–80

    Article  Google Scholar 

  • Labruna MB, Krawczak FS, Gerardi M, Binder LC, Barbieri ARM, Paz GF, Rodrigues DS, Araújo RN, Bernardes ML, Leite RC (2017) Isolation of Rickettsia rickettsii from the tick Amblyomma sculptum from a Brazilian spotted fever-endemic area in the Pampulha Lake region, southeastern Brazil. Vet Parasitol Reg Stud Rep 8:82–85. https://doi.org/10.1016/j.vprsr.2017.02.007

    Article  Google Scholar 

  • Luz HR, Costa FB, Benatti HR, Ramos VNA, Serpa MC, Martins TF, Acosta ICL, Ramirez DG, Muñoz-Leal S, Ramirez-Hernandez A, Binder LC, Carvalho MP, Rocha V, Dias TC, Simeoni CL, Brites-Neto J, Brasil J, Nievas AM, Monticelli PF, Moro MEG, Lopes B, Aguiar DM, Pacheco RC, Souza CE, Piovezan U, Juliano R, Ferraz KMPMB, Szabó MPJ, Labruna MB (2019) Epidemiology of capybara associated Brazilian spotted fever. PLOS Negl Trop Dis 13:e0007734. https://doi.org/10.1371/journal.pntd.0007734

    Article  PubMed  PubMed Central  Google Scholar 

  • Martins TF, Onofrio VC, Barros-Battesti DM, Labruna MB (2010) Nymphs of the genus Amblyomma (Acari: Ixodidae) of Brazil: descriptions, redescriptions, and identification key. Ticks Tick Borne Dis 1:75–99

    Article  PubMed  Google Scholar 

  • Martins TF, Barbieri ARM, Costa FB, Terassini FA, Camargo LMA, Peterka CRL, De C Pacheco R, Dias RA, Nunes PH, Marcili A, Scofield A, Campos AK, Horta MC, Guilloux AGA, Benatti HR, Ramirez DG, Barros-Battesti DM, Labruna MB (2016) Geographical distribution of Amblyomma cajennense (sensu lato) ticks (Parasitiformes: Ixodidae) in Brazil, with description of the nymph of A. cajennense (sensu stricto). Parasit Vectors 9:186. https://doi.org/10.1111/mve.12406

  • Nava S, Venzal JM, Labruna MB, Mastropaolo M, González EM, Mangold AJ, Guglielmone AA (2010) Hosts, distribution and genetic divergence (16S rDNA) of Amblyomma dubitatum (acari: Ixodidae). Exp Appl Acarol 51:335–351. https://doi.org/10.1007/s10493-009-9331-6

    Article  PubMed  Google Scholar 

  • Nava S, Beati L, Labruna MB, Cáceres AG, Mangold AJ, Guglielmone AA (2014) Reassessment of the taxonomic status of Amblyomma cajennense (Fabricius, 1787) with the description of three new species, Amblyomma tonelliae n. sp., Amblyomma interandinum n. sp. and Amblyomma patinoi n. sp., and reinstatement of Amblyomma mixtum Koch, 1844, and Amblyomma sculptum Berlese, 1888 (Ixodida: Ixodidae). Ticks Tick Borne Dis 5:252–276. https://doi.org/10.1016/j.ttbdis.2013.11.004

    Article  PubMed  Google Scholar 

  • Oliveira SV, Angerami RN (2018) Timeliness in the notification of spotted fever in Brazil: Evaluating compulsory reporting strategies and digital disease detection. Int J Infect Dis 72:16–18. https://doi.org/10.1016/j.ijid.2018.04.4317

    Article  Google Scholar 

  • Oliveira Filho JG, Ferreira LL, Sarria ALF, Pickett JA, Birkett MA, Mascarin GM, Pérez de León AA, Borges LMF (2017) Brown dog tick, Rhipicephalus sanguineus sensu lato, infestation of susceptible dog hosts is reduced by slow release of semiochemicals from a less susceptible host. Ticks Tick Borne Dis 8:139–145

    Article  PubMed  Google Scholar 

  • Oliveira Filho JG, Ferreira LL, Silva FO, Menezes KMF, Muniz ER, Paula LGF, Sarria ALF, Pickett JA, Birkett MA, Mascarin GM, Borges LMF (2018) Persistence and efficacy of a new formulation based on dog allomonal repellents against Rhipicephalus sanguineus sensu lato tick. Rev Bras Parasitol Vet 27:1–6

    Google Scholar 

  • Pajuaba Neto AA, Ramos VDN, Martins MM, Osava CF, Pascoal JO, Suzin A, Yokosawa J, Szabó MPJ (2018) Influence of microhabitat use and behavior of Amblyomma sculptum and Amblyomma dubitatum nymphs (Acari: Ixodidae) on human risk for tick exposure, with notes on Rickettsia infection. Ticks Tick Borne Dis 9:67–71

    Article  PubMed  Google Scholar 

  • R Core Team (2020) R: A Language and Environment for statistical computing. R foundation for statistical computing, Vienna, Austria. https://www.R-project.org

  • Ramos VN, Osava CF, Piovezan U, Szabó MPJ (2014) Ticks on humans in the Pantanal wetlands, Brazil. Ticks Tick Borne Dis 5:497–499

    Article  PubMed  Google Scholar 

  • Ramos VN, Osava CF, Piovezan U, Szabó MPJ (2017) Ambush behavior of the tick Amblyomma sculptum (Amblyomma cajennense complex) (Acari: Ixodidae) in the Brazilian Pantanal. Ticks Tick Borne Dis 8:506–510

    Article  PubMed  Google Scholar 

  • Sakai RK, Costa FB, Ueno T, Ramirez DG, Soares JF, Fonseca AH, Labruna MB, Barros-Battesti DM (2014) Experimental infection with Rickettsia rickettsii in an Amblyomma dubitatum tick colony, naturally infected by Rickettsia bellii. Ticks Tick Borne Dis 5:917–923. https://doi.org/10.1016/j.ttbdis.2014.07.003

    Article  PubMed  Google Scholar 

  • Szabó MPJ, Castagnolli KC, Figueiredo LB, Santana DA, Castro MB, Romano MA (2004) Amblyomma cajennense ticks induce immediate hypersensitivity in horses and donkeys. Exp App Acarol 33:109–117

    Article  Google Scholar 

  • Szabó MP, Labruna MB, Garcia MV, Pinter A, Castagnolli KC, Pacheco RC, Castro MB, Veronez VA, Magalhães GM, Vogliotti A, Duarte JM (2009) Ecological aspects of the free-living ticks (Acari: Ixodidae) on animal trails within Atlantic rainforest in south-eastern Brazil. Ann Trop Med Parasitol 103(1):57–72. https://doi.org/10.1179/136485909X384956

    Article  PubMed  Google Scholar 

  • Szabó MPJ, Pinter A, Labruna MB (2013) Ecology, biology and distribution of spotted-fever tick vectors in Brazil. Front Cell Infect Microbiol 3:27. https://doi.org/10.3389/fcimb.2013.00027

    Article  PubMed  PubMed Central  Google Scholar 

  • Szabó MPJ, Martins TF, Barbieri ARM, Costa FB, Soares HS, Tolesano-Pascoli GV, Torga K, Saraiva DG, Ramos VDN, Osava CF, de Castro MB, Labruna MB (2020) Ticks biting humans in the Brazilian savannah: Attachment sites and exposure risk in relation to species, life stage and season. Ticks Tick Borne Dis 11(2):101328. https://doi.org/10.1016/j.ttbdis.2019.101328

    Article  PubMed  Google Scholar 

  • Valente JDM, Silva PW, Arzua M, Barros-Battesti DM, Martins TF, Silva AM, Vieira TSWJ, Labruna MB, Vieira RFC (2020) Records of ticks (Acari: Ixodidae) on humans and distribution of spotted-fever cases and its tick vectors in Paraná State, southern Brazil. Ticks Tick Borne Dis 11:101510. https://doi.org/10.1016/j.ttbdis.2020.101510

    Article  PubMed  Google Scholar 

  • Zeringóta V, Oliveira Filho JG, Borges LMF (2020) Activation of the ambusher tick Rhipicephalus microplus (Acari: Ixodidae) exposed to different stimuli. Med Vet Entomol 34:236–239

    Article  PubMed  Google Scholar 

  • Zeringóta V, Pereira-Junior RA, Sarria ALF, Henrique ACC, Birkett MA, Borges LMF (2021) Identification of a non-host semiochemical from miniature pinscher, Canis lupus familiaris, that repels Rhipicephalus sanguineus sensu lato (Acari: Ixodidae). Ticks Tick Borne Dis 12:101582. https://doi.org/10.1016/j.ttbdis.2020.101582

    Article  PubMed  Google Scholar 

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Funding

This research was supported by grants from the Fundação de Amparo à Pesquisa do Estado de Goiás (FAPEG, 201710267000515) and Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil (INCT-EM, 465678/2014-9). The Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) of Brazil provided a Ph.D. scholarship for V.H.Lima, and the grant PQ 306319/2018-7 for É.K.K.Fernandes. The Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) of Brazil provided PhD scholarship for S.M.N.Pinto (CAPES Finance code 001).

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Valesca H. Lima: Conceptualization, Methodology, Investigation, Writing—original draft, Writing—review & editing, Visualization, Project administration. Salorrane M. N. Pinto: Methodology, Investigation, Writing—original draft, Writing—review & editing. Lucas P. Barreto: Methodology, Investigation, Writing—review & editing. André L. F. Sarria: Methodology, Investigation, Writing—review & editing. Gabriel M. Mascarin: Formal analysis, Writing—original draft, Writing—review & editing, Visualization. Éverton K. K. Fernandes: Resources, Writing—original draft, Writing—review & editing, Funding acquisition, Visualization. Lígia M. F. Borges: Conceptualization, Methodology, Formal analysis, Resources, Writing—original draft, Writing—review & editing, Funding acquisition, Visualization.

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Correspondence to Éverton Kort Kamp Fernandes.

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Lima, V.H., do Nascimento Pinto, S.M., Barreto, L.P. et al. Repellent activity of the non-host semiochemical (E)-2-octenal against Amblyomma sculptum and Amblyomma dubitatum ticks under field conditions. Exp Appl Acarol 92, 423–437 (2024). https://doi.org/10.1007/s10493-023-00880-6

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