[go: up one dir, main page]
More Web Proxy on the site http://driver.im/ Skip to main content

Advertisement

Springer Nature Link
Log in

Insecticidal activity of an essential oil of Tagetes patula L. (Asteraceae) on common bed bug Cimex lectularius L. and molecular docking of major compounds at the catalytic site of ClAChE1

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Emerging resistance to insecticides has influenced pharmaceutical research and the search for alternatives to control the common bed bug Cimex lectularius. In this sense, natural products can play a major role. Tagetes patula, popularly known as dwarf marigold, is a plant native to North America with biocide potential. The aim of this work was to evaluate the biological activity of T. patula essential oil (EO) against adult common bed bugs via exposure to dry residues by the Impregnated Paper Disk Test (IPDT) using cypermethrin as a positive control. We selected the enzyme acetylcholinesterase as a target for modeling studies, with the intent of investigating the molecular basis of any biological activity of the EO. Chemical analysis of the EO was performed using gas chromatography coupled to mass spectrometry (GC-MS). Additionally, oral and dermal acute toxicity tests were performed according to Organization for Economic Cooperation and Development (OECD) guidelines. The sulforhodamine B assay (SRB) was performed to verify the cytotoxicity of EO to HaCaT cells. The EO eliminated 100 % of the bed bugs at 100 mg mL−1 with an LC50 value of 15.85 mg mL−1. GC-MS analysis identified α-terpinolene, limonene, piperitenone, and piperitone as major components of the mixture. Molecular modeling studies of these major compounds suggested that they are acetylcholinesterase inhibitors with good steric and electronic complementarity. The in vitro cytotoxicity evaluation revealed a LC50 = 37.06 μg mL−1 and in vivo acute toxicity showed an LC50 >4000 mg kg−1, indicating that the EO presents low risk of toxic side effects in humans. The T. patula essential oil components provide a promising strategy for controlling bed bug populations with low mammalian toxicity. These findings pave the way for further in vivo studies aimed at developing a safe and effective insecticide.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
£29.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abbott WS (1925) A Method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267

    Article  CAS  Google Scholar 

  • Boase C (2001) Bed bugs-back from the brink. Pestic Outlook 12(4):159–162

    Article  Google Scholar 

  • Chang CL, Cho IK, Li QX (2009) Insecticidal activity of basil oil, trans-anethole, estragole, and linalool to adult fruit flies of Ceratitis capitata, Bactrocera dorsalis, and Bactrocera cucurbitae. J Econ Entomol 102(1):203–209

    Article  CAS  PubMed  Google Scholar 

  • Coats JR, Karr LL, Drewes CD (1991) Toxicity and neurotoxic effect of monoterpenoids in insects and earthworms. In: Hedin PA (ed) Naturally occurring pest bioregulators. ACS Symposium Series 449, American Chemical Society, Washington, pp 306–316

    Google Scholar 

  • Criado PR, Belda-Júnior W, Criado RF, Vasconcelose Silva R, Vasconcellos C (2011) Bedbugs (Cimicidae infestation): the worldwide renaissance of an old partner of human kind. Braz J Infect Dis 15(1):74–80

    Article  PubMed  Google Scholar 

  • Cruz MAS, Cedillo FD, Medina DH, Rodríguez AC (2014) Two agronomial aspects of Tagetes terniflora for essential oil production. JACEN 3(1):9–13

    Article  CAS  Google Scholar 

  • De Feo V, Soria EU, Soria RU, Pizza C (2004) Composition and in vitro toxicity of the essential oil of Tagetes terniflora HBK (Asteraceae). Flav Frag J 20(1):89–92

    Article  Google Scholar 

  • Delaunay P, Blanc V, Del Giudice P, Levy-Bencheton A, Chosidow O, Marty P, Brouqui F (2011) Bed bugs and infectious diseases. Clin Infect Dis 52:200–210

    Article  PubMed  PubMed Central  Google Scholar 

  • Doggett SL (2005) Bed bug ecology and control. In: Doggett SL (ed) Synopsis of papers. Westmead Hospital, Sydney

    Google Scholar 

  • Doggett SL, Russell RC (2009) Emerging challenges in bed bug management. In: Doggett SL (ed) Emerging Pest Management Challenges Symposium course notes. Westmead Hospital, Sydney

    Google Scholar 

  • Doggett SL, Geary MJ, Russell RC (2004a) The resurgence of bed bugs in Australia: with notes on their ecology and control. Environ Health 4:30–38

    Google Scholar 

  • Doggett SL, Geary MJ, Lamond P, Russell RC (2004b) Bed bug management: a case study. Profes Pest Manager 8(6):21–23

    Google Scholar 

  • Doggett SL, Orton CJ, Lilly D, Russell RC (2011) Bed bugs: the Australian response. Insects 2:96–111

    Article  PubMed  PubMed Central  Google Scholar 

  • Doggett SL, Dwyer DE, Penas PF, Russel RC (2012) Bed Bugs: Clinical Relevance and Control Options. Clin Microbiol Rev 25(1):164-192

  • Ferrer MVF, Sainz-Elipe S (2005) La chinche de cama. Un ectoparasito emergente? Enf Emerg 7(3):87–101

    Google Scholar 

  • Gangloff-Kaufmann J, Shultz J (2003) Bed bugs are back! An IPM answer. New York State Integrated Pest Management Program, Cornell University, New York

    Google Scholar 

  • Goddard J, deShazo R (2009) Bed Bugs (Cimex lectularius) and clinical consequences of their bites. JAMA 301(13):1358–1366

    Article  CAS  PubMed  Google Scholar 

  • Harlan HJ (2006) Bed bugs 101: the basics of Cimex lectularius. Am Entomol 52(2):99–101

    Article  Google Scholar 

  • Hirao M (2010) Recent resurgence of bed bug and its management. Med Entomol Zool 61:211–221

    Article  Google Scholar 

  • Hwang CE, Kim YH, Kwon DH, Seong KM, Choi JY, Je YH, Lee SH (2014) Biochemical and toxicological properties of two acetylcholinesterases from the common bed bug, Cimex lectularius. Pest Biochem Physiol 110:20–26

    Article  CAS  Google Scholar 

  • Jain AN (2003) Surflex: fully automatic flexible molecular docking using a molecular similarity-based search engine. J Med Chem 46:499–511

    Article  CAS  PubMed  Google Scholar 

  • Kilpinen O, Karl-Martin VJ, Kristensen M (2008) Bed bug problems in Denmark, with a European perspective. In: Robinson WH, Bajomi D (eds) Proceedings of the 6th International Conference on Urban Pests. OOK-Press, Budapest, pp 395–399

    Google Scholar 

  • Kilpinen O, Kristensen M, Jensen KMV (2011) Resistance differences between chlorpyrifos and synthetic pyrethroids in Cimex lectularius population from Denmark. Parasitol Res 109:1461–1464

    Article  PubMed  Google Scholar 

  • Kostyukovsky M, Rafaeli A, Gileadi C, Demchenko N, Shaaya E (2002) Activation of octopaminergic receptors by essential oil constituents isolated from aromatic plants: possible mode of action against insect pests. Pest Manag Sci 58:1101–1106

    Article  CAS  PubMed  Google Scholar 

  • Kweka EJ, Mwang’onde BJ, Kimaro EE, Msangi S, Tenu F, Mahande AM (2009) Insecticides susceptibility status of the bed bugs (Cimex lectularius) in a rural area of Magugu, Northern Tanzania. J Glob Infect Dis 1(2):102–106

    Article  PubMed  PubMed Central  Google Scholar 

  • Lai O, Ho D, Glick S, Jaqdeo J (2016) Bed bugs and possible transmission of human pathogens: a systematic review. Arch Dermatol Res 308(8):531–538

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee IY, Ree HI, An SJ, Linton JA, Yong TS (2008) Reemergence of the bed bug Cimex lectularius in Seoul, Korea. Korean J Parasitol 46(4):269–271

    Article  PubMed  PubMed Central  Google Scholar 

  • Leulmi H, Bitam I, Berenger JM, Lepidi H, Rolain JM, Almeras L, Raoult D, Parola P (2015) Competence of Cimex lectularius bed bugs for the transmission of Bartonella quintana, the agent of Trench Fever. PLoS Negl Trop Dis 9(5):e0003789

    Article  PubMed  PubMed Central  Google Scholar 

  • Lilly DG, Doggett SL, Zalucki MP, Orton C, Russell RC (2009) Bed bugs that bite back, confirmation of insecticide resistance in the common bed bug, Cimex lectularius. Prof Pest Manager 13:22–24

    Google Scholar 

  • López MD, Pascual-Villalobos MJ (2010) Mode of inhibition of acetylcholinesterase by monoterpenoids and implications. Ind Crop Prod 31:284–288

    Article  Google Scholar 

  • Masetti M, Bruschi F (2007) Bed bug infestations recorded in Central Italy. Parasitol Intern 56(1):81–83

    Article  Google Scholar 

  • Naqqash MN, Gökçe A, Bakhsh A, Salim M (2016) Insecticide resistance and its molecular basis in urban insect pests. Parasitol Res 115(4):1363–1373

    Article  PubMed  Google Scholar 

  • Nascimento LGG (2010) Investigação da ocorrência de infestação por Cimicidae (Heteroptera: Cimicomorpha) na Região Metropolitana de São Paulo, no período de 2004 a 2009. Universidade de São Paulo (USP), São Paulo, p 144

    Google Scholar 

  • Neves DP (2005) Parasitologia Humana, 11th edn. Atheneu, São Paulo

    Google Scholar 

  • Omudu EA, Kuse CN (2010) Bed bug infestation and its control practices in Gbajimba: a rural settlement in Benue state, Nigeria. J Vector Borne Dis 47:222–227

    CAS  PubMed  Google Scholar 

  • Organization for Economic Co-operation and Development (OECD) (2001) Guideline for testing of chemicals 420. Acute oral toxicity—fixed dose procedure

  • Organization for Economic Co-operation and Development (OECD) (2004) Guideline for testing of chemicals, 402. Acute dermal toxicity—fixed dose procedure, 1st version

  • Oyedele AO, Gbolade AA, Sosan MB, Adewoyin FB, Soyelu OL, Orafidiya OO (2002) Formulation of an effective mosquito-repellent topical product from lemongrass oil. Phytomedicine 9(3):259–262

    Article  CAS  PubMed  Google Scholar 

  • Pavela R (2008) Insecticidal properties of several essential oils on the house fly (Musca domestica L.). Phytother Res 22:274–278

    Article  CAS  PubMed  Google Scholar 

  • Politi FAS, Souza-Moreira TM, Rodrigues ER, Queiroz GM, Figueira GM, Januário AH, Berenger JM, Socolovschi C, Parola P, Pietro RCLR (2013) Chemical characterization and acaricide potential of essential oil from aerial parts of Tagetes patula L. (Asteraceae) against engorged adult females of Rhipicephalus sanguineus (Latreille, 1806). Parasitol Res 112(6):2261–2268

    Article  PubMed  Google Scholar 

  • Puckett RT, McDonald DL, Gold RE (2013) Comparison of multiple steam treatment durations for control of bed bugs (Cimex lectularius L.). Pest Manag Sci 69(9):1061–1065

    Article  CAS  PubMed  Google Scholar 

  • Re L, Barocci S, Sonnino S, Mencarelli A, Vivani C (2000) Linalool modifies the nicotinic receptor-ion channel kinetics at the mouse neuromuscular junction. Pharmacol Res 42:177–182

    Article  CAS  PubMed  Google Scholar 

  • Rey L (2002) Bases da Parasitologia Médica, 2nd edn. Guanabara-Koogan, Rio de Janeiro

    Google Scholar 

  • Romero A, Potter MF, Potter DA, Haynes KF (2007) Insecticide resistance in the bed bug: a factor in the pest’s sudden resurgence? J Med Entomol 44(2):175–178

    PubMed  Google Scholar 

  • Seong KM, Kim YH, Kwon DH, Lee SH (2012) Identification and characterization of three cholinesterases from the common bed bug, Cimex lectularius. Insect Mol Biol 21(2):149–159

    Article  CAS  PubMed  Google Scholar 

  • Singh N, Wang C, Cooper R (2014) Potential of essential oil-based pesticides and detergents for bed bug control. J Econ Entomol 107(6):2163–2170

    Article  PubMed  Google Scholar 

  • Skehan P, Storeng R, Scudiero D, Monges A, McMahon J, Vistica D, Warren JT, Bokesch H, Kenney S, Boyd MR (1990) New colorimetric cytotoxicity assay for anticancer-drug screening. J Natl Cancer Inst 82:1107–1112

    Article  CAS  PubMed  Google Scholar 

  • Solomon B, Sahle FF, Gebre-Mariam T, Asres K, Neubert RH (2012) Microencapsulation of citronella oil for mosquito-repellent application: formulation and in vitro permeation studies. Eur J Pharm Biopharm 80(1):61–66

    Article  CAS  PubMed  Google Scholar 

  • Tawatsin A, Thavara U, Chompoosri J, Phusup Y, Jonjang N, Khumsawads C, Bhakdeenuan P, Sawanpanyalert P, Asavadachanukorn P, Mulla MS, Siriyasatien P, Debboun M (2011) Insecticide resistance in bed bugs in Thailand and laboratory evaluation of insecticides for the control of Cimex hemipterus and Cimex lectularius (Hemiptera: Cimicidae). J Med Entomol 48:1023–1030

    Article  CAS  PubMed  Google Scholar 

  • Ter Poorten MC, Prose NS (2005) The return of common bed bug. Pediatr Dermatol 22(3):183–187

    Article  PubMed  Google Scholar 

  • Toutant JP (1989) Insect acetylcholinesterase: catalytic properties, tissue distribution and molecular forms. Prog Neurobiol 32:423–446

    Article  CAS  PubMed  Google Scholar 

  • Tripathi AK, Prajapati V, Kumar S (2003) Bioactivities of l-carvone, d-carvone, and dihydrocarvone toward three stored product beetles. J Econ Entomol 96(5):1594–1601

    Article  CAS  PubMed  Google Scholar 

  • Vasudevan P, Kashyap S, Sharna S (1997) Tagetes: a multipurpose plant. Biores Technol 62:29–35

    Article  CAS  Google Scholar 

  • Viegas-Júnior C (2003) Terpenos com atividade inseticida: uma alternativa para o controle químico de insetos. Quim Nov. 26(3):390–400

  • Wang JL, Li Y, Lei CL (2009) Evaluation of monoterpenes for the control of Tribolium castaneum (Herbst) and Sitophilus zeamais Motschulsky. Nat Prod Res 23B:1080–1088

    Article  Google Scholar 

  • Wang C, Singh N, Cooper R (2014) Efficacy of an essential oil-based pesticide for controlling bed bug (Cimex lectularius) infestations in apartment buildings. Insects 5(4):849–859

    Article  PubMed  PubMed Central  Google Scholar 

  • Yunes RA, Pedrosa RC, Cechinel-Filho V (2001) Fármacos e fitoterápicos: a necessidade do desenvolvimento da indústria de fitoterápicos e fitofármacos no Brasil. Quim Nov. 24(1):147–152

  • Zhu F, Wigginton J, Romero A, Moore A, Ferguson K, Palli R, Potter MF, Haynes KF, Palli SR (2010) Widespread distribution of knockdown resistance mutations in the bed bug, Cimex lectularius (Hemiptera: Cimicidae), populations in the United States. Arch Insect Biochem Physiol 73:245–257

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the Collection of Medicinal and Aromatic Plants (CPMA) of the Multidisciplinary Center for Chemical, Biological and Agricultural Research (CPQBA) for supplying the plant material; Prof. Dr. Norberto Peporine Lopes of the Research Support Center in Natural and Synthetic Products (NPPNS), the School of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo (USP), for chromatographic equipment; Prof. Dr. João Aristeu da Rosa, for the colony of C. lectularius maintained at the School of Pharmaceutical Sciences (UNESP), Araraquara (SP), Brazil; and Prof. Dr. Christiane Pienna Soares of the Laboratory of Cytology and Cell Biology (UNESP), Araraquara (SP), for HaCat cells.

Author information

Authors and Affiliations

  1. Department of Organic Chemistry, Institute of Chemistry, University Estadual Paulista-UNESP, Rua Prof. Francisco Degni 55, Quitandinha, Araraquara, SP, CEP 14800-060, Brazil

    Flávio Augusto Sanches Politi, Alexander Alves da Silva & Maysa Furlan

  2. Faculdade de Ciências Farmacêuticas, University Estadual Paulista-UNESP, Rod. Araraquara-Jaú Km 01, Araraquara, SP, 14801-902, Brazil

    Juliana Damieli Nascimento, Isabela Jacob Moro & Rosemeire Cristina Linhari Rodrigues Pietro

  3. Centro de Pesquisa e Inovação em Biodiversidade e Fármacos, Instituto de Física de São Carlos, Universidade de São Paulo, São Carlos, SP, 13563-120, Brazil

    Mariana Lopes Garcia & Rafael Victório Carvalho Guido

  4. Centro de Assistência Toxicológica (CEATOX), University Estadual Paulista-UNESP, Distrito de Rubião Júnior s/n, Botucatu, SP, 18618-970, Brazil

    Antônio Francisco Godinho

Authors
  1. Flávio Augusto Sanches Politi
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Juliana Damieli Nascimento
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Alexander Alves da Silva
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Isabela Jacob Moro
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. Mariana Lopes Garcia
    View author publications

    You can also search for this author inPubMed Google Scholar

  6. Rafael Victório Carvalho Guido
    View author publications

    You can also search for this author inPubMed Google Scholar

  7. Rosemeire Cristina Linhari Rodrigues Pietro
    View author publications

    You can also search for this author inPubMed Google Scholar

  8. Antônio Francisco Godinho
    View author publications

    You can also search for this author inPubMed Google Scholar

  9. Maysa Furlan
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Flávio Augusto Sanches Politi.

Additional information

Highlights

• Tagetes patula essential oil showed similar insecticidal effects to cypermethrin.

• Major compounds of essential oil acting as competitive inhibitors of ClAChE1.

• Assays of acute toxicity and cytotoxicity showed that the essential oil is safe.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Politi, F.A.S., Nascimento, J.D., da Silva, A.A. et al. Insecticidal activity of an essential oil of Tagetes patula L. (Asteraceae) on common bed bug Cimex lectularius L. and molecular docking of major compounds at the catalytic site of ClAChE1. Parasitol Res 116, 415–424 (2017). https://doi.org/10.1007/s00436-016-5305-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-016-5305-x

Keywords