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Nanoliposomes Containing Carvacrol and Carvacrol-Rich Essential Oils as Effective Mosquitoes Larvicides

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Abstract

The low efficacy of essential oil-based larvicides and their components’ volatility have challenged their use as green alternatives. In this study, the larvicidal effect of essential oils of Satureja khuzestanica and Zataria multiflora with their ingredients, carvacrol, was first investigated against two medically important mosquitoes. After confirming each sample’s successful loading in the nanoliposomes with a vesicle size of 110 ± 8, 70 ± 5, and 76 ± 5 nm, their larvicidal effects were also evaluated. These effects of nanoliposomal forms were greater than that of non-formulated states. The best-observed LC50 against Anopheles stephensi and Culex quinquefasciatus were related to nanoliposomes containing essential oils of Z. multiflora (10.88 µg/mL) and S. khuzestanica (16.74 µg/mL). These samples could be used as green larvicides for investigation against other mosquito populations.

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Abbreviations

GC-MS:

Gas chromatography-mass spectrometry

DLS:

Dynamic light scattering

ATR-FTIR:

Attenuated total reflection-Fourier transform infrared

EO:

Essential oil

CarLipo:

Nanoliposomes containing carvacrol

SKEO:

Satureja khuzestanica Essential oil

SKLipo:

Nanoliposomes containing Satureja khuzestanica essential oil

ZMEO:

Zataria multiflora Essential oil

ZMLipo:

Nanoliposomes containing Zataria multiflora essential oil

References

  1. Calzolari, M. (2016). Mosquito-borne diseases in Europe: An emerging public health threat. Reports in Parasitology, 5, 1–12. https://doi.org/10.2147/rip.s56780.

    Article  Google Scholar 

  2. Corby-Harris, V., Drexler, A., De Jong, L. W., Antonova, Y., Pakpour, N., Ziegler, R., et al. (2010). Activation of Akt signaling reduces the prevalence and intensity of malaria parasite infection and lifespan in Anopheles stephensi mosquitoes. PLoS Pathogens, 6(7), e1001003. https://doi.org/10.1371/journal.ppat.1001003.

    Article  Google Scholar 

  3. Akbarzadeh, M., Soltani, A., Moemenbellah-Fard, M. D., Khoshnoud, M. J., & Azizi, K. (2020). Larvicidal, repellent, and histopathologic effects of Citrullus colocynthis against the malaria vector. Toxicological and Environmental Chemistry, 102(1–4), 92–104. https://doi.org/10.1080/02772248.2020.1770254.

    Article  Google Scholar 

  4. WHO (2019) World malaria report 2019. https://www.who.int/malaria/publications/world_malaria_report/en/. Accessed Dec 2020

  5. Ghahremani, L., Azizi, M., Moemenbellah-Fard, M. D., & Ghaem, H. (2019). Malaria preventive behaviors among housewives in suburbs of Bandar-Abbas City, south of Iran: Interventional design based on PRECEDE model. Pathog Glob Health, 113(1), 32–38. https://doi.org/10.1080/20477724.2019.1583847.

    Article  Google Scholar 

  6. Kent, R. J., Crabtree, M. B., & Miller, B. R. (2010). Transmission of West Nile virus by Culex quinquefasciatus say infected with Culex Flavivirus Izabal. PLoS Neglected Tropical Diseases, 4(5), e671. https://doi.org/10.1371/journal.pntd.0000671.

    Article  Google Scholar 

  7. Arensburger, P., Megy, K., Waterhouse, R. M., Abrudan, J., Amedeo, P., Antelo, B., et al. (2010). Sequencing of Culex quinquefasciatus establishes a platform for mosquito comparative genomics. Science, 330(6000), 86–88. https://doi.org/10.1126/science.1191864.

    Article  Google Scholar 

  8. Hemingway, J., Beaty, B. J., Rowland, M., Scott, T. W., & Sharp, B. L. (2006). The innovative vector control consortium: Improved control of mosquito-borne diseases. Trends in parasitology, 22(7), 308–312. https://doi.org/10.1016/j.pt.2006.05.003.

    Article  Google Scholar 

  9. Osanloo, M., Amini, S. M., Sedaghat, M. M., & Amani, A. (2019). Larvicidal activity of chemically synthesized silver nanoparticles against Anopheles stephensi. J Pharm Negat Results, 10(1), 69–72. https://doi.org/10.4103/jpnr.jpnr_18_17.

    Article  Google Scholar 

  10. Salim-Abadi, Y., Asadpour, M., Sharifi, I., Sanei-Dehkordi, A., Gorouhi, M. A., Paksa, A., et al. (2017). Baseline susceptibility of filarial vector Culex quinquefasciatus (Diptera: Culicidae) to five insecticides with different modes of action in southeast of Iran. Journal of Arthropod-Borne Diseases, 11(4), 453–462.

    Google Scholar 

  11. Esmaili, F., Sanei-Dehkordi, A., Amoozegar, F., & Osanloo, M. (2021). A review on the use of essential oil-based nanoformulations in control of mosquitoes. Biointerface Research Applied Chemistry, 11(5), 12516–12529. https://doi.org/10.33263/briac115.1251612529.

    Article  Google Scholar 

  12. Osanloo, M., Arish, J., & Sereshti, H. (2019). Developed methods for the preparation of electrospun nanofibers containing plant-derived oil or essential oil: A systematic review. Polymer Bulletin, 77(11), 6085–6104. https://doi.org/10.1007/s00289-019-03042-0.

    Article  Google Scholar 

  13. Sugumar, S., Clarke, S., Nirmala, M., Tyagi, B., Mukherjee, A., & Chandrasekaran, N. (2014). Nanoemulsion of eucalyptus oil and its larvicidal activity against Culex quinquefasciatus. Bulletin of Entomological Research, 104(3), 393–402. https://doi.org/10.1017/S0007485313000710.

    Article  Google Scholar 

  14. Jesser, E. N., Yeguerman, C. O., Gili, V. O., Santillan, G. O., Murray, A. P., & DOMINI C, Werdin González JO. (2020). Optimization and characterization of essential oil nanoemulsions using ultrasound for new ecofriendly insecticides. ACS Sustain Chem Eng, 8(21), 7981–7992. https://doi.org/10.1021/acssuschemeng.0c02224.

    Article  Google Scholar 

  15. Osanloo, M., Sedaghat, M. M., Sereshti, H., & Amani, A. (2019). Chitosan nanocapsules of tarragon essential oil with low cytotoxicity and long-lasting activity as a green nano-larvicide. Journal Nanostructured, 9(4), 723–735. https://doi.org/10.22052/JNS.2019.04.014.

    Article  Google Scholar 

  16. Pavela, R., Pavoni, L., Bonacucina, G., Cespi, M., Cappellacci, L., Petrelli, R., et al. (2021). Encapsulation of Carlina acaulis essential oil and carlina oxide to develop long-lasting mosquito larvicides: Microemulsions versus nanoemulsions. Journal of Pest Science. https://doi.org/10.1007/s10340-020-01327-2.

    Article  Google Scholar 

  17. Trucillo, P., Ferrari, P., Campardelli, R., Reverchon, E., & Perego, P. (2020). A supercritical assisted process for the production of amoxicillin loaded liposomes for anti-microbial applications. Journal of Supercritical Fluids, 163, 104842. https://doi.org/10.1016/j.supflu.2020.104842.

    Article  Google Scholar 

  18. Mishra, D. K., Shandilya, R., & Mishra, P. K. (2018). Lipid based nanocarriers: A translational perspective. Nanomedicine, 14(7), 2023–2050. https://doi.org/10.1016/j.nano.2018.05.021.

    Article  Google Scholar 

  19. Zahin, N., Anwar, R., Tewari, D., Kabir, M. T., Sajid, A., Mathew, B., & Uddin, M. S. (2020). Nanoparticles and its biomedical applications in health and diseases: Special focus on drug delivery. Environmental Science and Pollution Research, 27(16), 19151–19168. https://doi.org/10.1007/s11356-019-05211-0.

    Article  Google Scholar 

  20. Sebaaly, C., Jraij, A., Fessi, H., Charcosset, C., & Greige-Gerges, H. (2015). Preparation and characterization of clove essential oil-loaded liposomes. Food Chemistry, 178, 52–62. https://doi.org/10.1016/j.foodchem.2015.01.067.

    Article  Google Scholar 

  21. Wen, Z., Liu, B., Zheng, Z., You, X., Pu, Y., & Li, Q. (2010). Preparation of liposomes entrapping essential oil from Atractylodes macrocephala Koidz by modified RESS technique. Chemical Engineering Research and Design, 88(8), 1102–1107. https://doi.org/10.1016/j.cherd.2010.01.020.

    Article  Google Scholar 

  22. Kayedi, M. H., Haghdoost, A. A., Salehnia, A., & Khamisabadi, K. (2014). Evaluation of repellency effect of essential oils of Satureja khuzestanica (Carvacrol), Myrtus communis (Myrtle), Lavendula officinalis and Salvia sclarea using standard WHO repellency tests. Journal of Arthropod-Borne Diseases, 8(1), 60–68.

    Google Scholar 

  23. Lucia, A., & Guzmán, E. (2020). Emulsions containing essential oils, their components or volatile semiochemicals as promising tools for insect pest and pathogen management. Advances in Colloid and Interface Science, 287, 102330. https://doi.org/10.1016/j.cis.2020.102330.

    Article  Google Scholar 

  24. Farahani, S., Bandani, A. R., & Amiri, A. (2020). Toxicity and repellency effects of three essential oils on two populations of Tetranychus urticae (Acari: Tetranychidae). Persian Journal Acarol, 9(1), 67–81. https://doi.org/10.22073/pja.v9i1.55853.

    Article  Google Scholar 

  25. Amirinezhad, M., Yousefzadi, M., Arman, M., & Rahimzadeh, M. (2018). Comparison of essential oils toxicity of Satureja khuzistanica and Satureja rechingeri on larvae of the barnacle Amphibalanus amphitrite. Modares Journal of Biotechnology, 9(3), 435–440.

    Google Scholar 

  26. Bassole, I., Guelbeogo, W., Nebie, R., Costantini, C., Sagnon, N., Kabore, Z., & Traore, S. (2003). Ovicidal and larvicidal activity against Aedes aegypti and Anopheles gambiae complex mosquitoes of essential oils extracted from three spontaneous plants of Burkina Faso. Parassitologia, 45(1), 23–26.

    Google Scholar 

  27. Kelidari, H. R., Moemenbellah-Fard, M. D., Morteza-Semnani, K., Amoozegar, F., Shahriari-Namadi, M., Saeedi, M., & Osanloo, M. (2021). Solid-lipid nanoparticles (SLN) s containing Zataria multiflora essential oil with no-cytotoxicity and potent repellent activity against Anopheles stephensi. Journal of Parasitic Diseases, 45(1), 101–108. https://doi.org/10.1007/s12639-020-01281-x.

    Article  Google Scholar 

  28. Chegini, S. G., Abbasipour, H., Karimi, J., & Askarianzadeh, A. (2018). Toxicity of Shirazi thyme, Zataria multiflora essential oil to the tomato leaf miner, Tuta absoluta (Lepidoptera: Gelechiidae). International Journal of Tropical Insect Science, 38(4), 340–347. https://doi.org/10.1017/S1742758418000097.

    Article  Google Scholar 

  29. Youssefi, M. R., Tabari, M. A., Esfandiari, A., Kazemi, S., Moghadamnia, A. A., Sut, S., & Dall’Acqua, S. (2019). Efficacy of two monoterpenoids, carvacrol and thymol, and their combinations against eggs and larvae of the West Nile vector Culex pipiens. Molecules, 24(10), 1867. https://doi.org/10.3390/molecules24101867.

    Article  Google Scholar 

  30. Novato, T. P., Araújo, L. X., de Monteiro, C. M., Maturano, R., Senra Tde, O., da Silva, M. R., et al. (2015). Evaluation of the combined effect of thymol, carvacrol and (E)-cinnamaldehyde on Amblyomma sculptum (Acari: Ixodidae) and Dermacentor nitens (Acari: Ixodidae) larvae. Veterinary Parasitology, 212(3–4), 331–335. https://doi.org/10.1016/j.vetpar.2015.08.021.

    Article  Google Scholar 

  31. Traboulsi, A. F., Taoubi, K., & el-Haj S, Bessiere JM, Rammal S. (2002). Insecticidal properties of essential plant oils against the mosquito Culex pipiens molestus (Diptera: Culicidae). Pest Management Science, 58(5), 491–495. https://doi.org/10.1002/ps.486.

    Article  Google Scholar 

  32. Govindarajan, M., Rajeswary, M., Hoti, S. L., & Benelli, G. (2016). Larvicidal potential of carvacrol and terpinen-4-ol from the essential oil of Origanum vulgare (Lamiaceae) against Anopheles stephensi, Anopheles subpictus, Culex quinquefasciatus and Culex tritaeniorhynchus (Diptera: Culicidae). Research in Veterinary Science, 104, 77–82. https://doi.org/10.1016/j.rvsc.2015.11.011.

    Article  Google Scholar 

  33. Andrade-Ochoa, S., Sánchez-Aldana, D., Chacón-Vargas, K. F., Rivera-Chavira, B. E., & Sánchez-Torres, L. E. (2018). Oviposition deterrent and larvicidal and pupaecidal activity of seven essential oils and their major components against Culex quinquefasciatus Say (Diptera: Culicidae): Synergism-antagonism effects. Insects, 9(1), 25. https://doi.org/10.3390/insects9010025.

    Article  Google Scholar 

  34. Suntres, Z. E., Coccimiglio, J., & Alipour, M. (2015). The bioactivity and toxicological actions of carvacrol. Critical Reviews in Food Science and Nutrition, 55(3), 304–318. https://doi.org/10.1080/10408398.2011.653458.

    Article  Google Scholar 

  35. Abedinpour, N., Ghanbariasad, A., Taghinezhad, A., & Osanloo, M. (2021). Preparation of nanoemulsions of Mentha piperita essential oil and investigation of their cytotoxic effect on human breast cancer lines. BioNanoScience. https://doi.org/10.1007/s12668-021-00827-4.

    Article  Google Scholar 

  36. Siria, D. J., Batista, E. P. A., Opiyo, M. A., Melo, E. F., Sumaye, R. D., Ngowo, H. S., et al. (2018). Evaluation of a simple polytetrafluoroethylene (PTFE)-based membrane for blood-feeding of malaria and dengue fever vectors in the laboratory. Parasites & Vectors, 11(1), 236. https://doi.org/10.1186/s13071-018-2823-7.

    Article  Google Scholar 

  37. WHO (2005) Guidelines for laboratory and field testing of mosquito larvicides. https://whqlibdoc.who.int/hq/2005/WHO_CDS_WHOPES_GCDPP_2005.13.pdf. AccessedDec2020

  38. Finney, D. J. (1971). Probit analysis (3rd ed.). Cambridge University Press.

    MATH  Google Scholar 

  39. Can, B. K. (2008). Biological and pharmacological activities of carvacrol and carvacrol bearing essential oils. Current Pharmaceutical Design, 14(29), 3106–3119. https://doi.org/10.2174/138161208786404227.

    Article  Google Scholar 

  40. Veldhuizen, E. J., Tjeerdsma-van Bokhoven, J. L., Zweijtzer, C., Burt, S. A., & Haagsman, H. P. (2006). Structural requirements for the antimicrobial activity of carvacrol. Journal of Agriculture and Food Chemistry, 54(5), 1874–1879. https://doi.org/10.1021/jf052564y.

    Article  Google Scholar 

  41. Pavela, R., Morshedloo, M. R., Mumivand, H., Khorsand, G. J., Karami, A., Maggi, F., et al. (2020). Phenolic monoterpene-rich essential oils from Apiaceae and Lamiaceae species: Insecticidal activity and safety evaluation on non-target earthworms. Entomologia Generalis, 40, 421–435. https://doi.org/10.1127/entomologia/2020/1131.

    Article  Google Scholar 

  42. Khakzad, S., Rahmani, F., Hojjati, M., & Tabandeh, M. R. (2019). Anti-carcinogenic effects of Satureja khuzistanica and Zataria multiflora essential oils on K562 cell line proliferation. Journal of Food and Bioprocess Engineering, 2(2), 127–132.

    Google Scholar 

  43. Saidi, M. (2014). Antioxidant activities and chemical composition of essential oils from Satureja khuzestanica, Oliveria decumbens and Thymus daenensis. Journal of Essential Oil-Bear Plants, 17(3), 513–521. https://doi.org/10.1080/0972060X.2014.901607.

    Article  Google Scholar 

  44. Zandi-Sohani, N., & Ramezani, L. (2015). Evaluation of five essential oils as botanical acaricides against the strawberry spider mite Tetranychus turkestani Ugarov and Nikolskii. International Biodeterioration & Biodegradation, 98, 101–106. https://doi.org/10.1016/j.ibiod.2014.12.007.

    Article  Google Scholar 

  45. Raeisi, M., GhorbaniBidkorpeh, F., Hashemi, M., Tepe, B., Moghaddam, Z., AmanMohammadi, M., & Noori, S. M. A. (2019). Chemical composition and antibacterial and antioxidant properties of essential oils of Zataria multiflora, Artemisia deracunculus and Mentha piperita. Medical Laboratory Journal, 13(2), 1–7. https://doi.org/10.29252/mlj.13.2.1.

    Article  Google Scholar 

  46. Ardekani, N. T., Khorram, M., Zomorodian, K., Yazdanpanah, S., Veisi, H., & Veisi, H. (2019). Evaluation of electrospun poly (vinyl alcohol)-based nanofiber mats incorporated with Zataria multiflora essential oil as potential wound dressing. International Journal of Biological Macromolecules, 125, 743–750. https://doi.org/10.1016/j.ijbiomac.2018.12.085.

    Article  Google Scholar 

  47. Khatibi, S., Misaghi, A., Moosavy, M., AkhondzadehBasti, A., Mohamadian, S., & Khanjari, A. (2018). Effect of nanoliposomes containing Zataria multiflora Boiss. Essential oil on gene expression of Shiga toxin 2 in Escherichia coli O157: H7. Journal Applied Microbiology, 124(2), 389–397. https://doi.org/10.1111/jam.13641.

    Article  Google Scholar 

  48. Khatibi, S. A., Misaghi, A., Moosavy, M.-H., Amoabediny, G., & Basti, A. A. (2014). Effect of preparation methods on the properties of Zataria multiflora Boiss. Essential oil loaded: nanoliposomes Characterization of size, encapsulation efficiency and stability. Pharmaceutical Sciences, 20(4), 141–148. https://doi.org/10.5681/PS.2015.003.

    Article  Google Scholar 

  49. Liolios, C. C., Gortzi, O., Lalas, S., Tsaknis, J., & Chinou, I. (2009). Liposomal incorporation of carvacrol and thymol isolated from the essential oil of Origanum dictamnus L. and in vitro antimicrobial activity. Food Chemistry, 112(1), 77–83. https://doi.org/10.1016/j.foodchem.2008.05.060.

    Article  Google Scholar 

  50. Engel, J. B., Heckler, C., Tondo, E. C., Daroit, D. J., & da Silva, M. P. (2017). Antimicrobial activity of free and liposome-encapsulated thymol and carvacrol against Salmonella and Staphylococcus aureus adhered to stainless steel. International Journal of Food Microbiology, 252, 18–23. https://doi.org/10.1016/j.ijfoodmicro.2017.04.003.

    Article  Google Scholar 

  51. Liu, H., Xu, Q., Zhang, L., & Liu, N. (2005). Chlorpyrifos resistance in mosquito Culex quinquefasciatus. Journal of Medical Entomology, 42(5), 815–820. https://doi.org/10.1093/jmedent/42.5.815.

    Article  Google Scholar 

  52. Lima, E. P., Paiva, M. H. S., de Araújo, A. P., da Silva, ÉV. G., da Silva, U. M., de Oliveira, L. N., et al. (2011). Insecticide resistance in Aedes aegypti populations from Ceará. Brazil. Parasites & vectors, 4(1), 1–12. https://doi.org/10.1186/1756-3305-4-5.

    Article  Google Scholar 

  53. Casimiro, S., Coleman, M., Hemingway, J., & Sharp, B. (2014). Insecticide resistance in Anopheles arabiensis and Anopheles gambiae from Mozambique. Journal of Medical Entomology, 43(2), 276–282. https://doi.org/10.1603/0022-2585(2006)043[0276:iriaaa]2.0.co;2.

    Article  Google Scholar 

  54. Baek, S. H., Kang, J. H., Hwang, Y. H., Ok, K. M., Kwak, K., & Chun, H. S. (2016). Detection of methomyl, a carbamate insecticide, in food matrices using terahertz time-domain spectroscopy. J Infrared Millim Terahertz Waves, 37(5), 486–497. https://doi.org/10.1007/s10762-015-0234-9.

    Article  Google Scholar 

  55. Schulze, H., Scherbaum, E., Anastassiades, M., Vorlová, S., Schmid, R. D., & Bachmann, T. T. (2002). Development, validation, and application of an acetylcholinesterase-biosensor test for the direct detection of insecticide residues in infant food. Biosensors & Bioelectronics, 17(11–12), 1095–1105. https://doi.org/10.1016/s0956-5663(02)00104-5.

    Article  Google Scholar 

  56. Damalas, C. A., & Eleftherohorinos, I. G. (2011). Pesticide exposure, safety issues, and risk assessment indicators. International Journal of Environmental Research and Public Health, 8(5), 1402–1419. https://doi.org/10.3390/ijerph8051402.

    Article  Google Scholar 

  57. Isman, M. B. (2000). Plant essential oils for pest and disease management. Crop protection, 19(8–10), 603–608. https://doi.org/10.1016/s0261-2194(00)00079-x.

    Article  Google Scholar 

  58. Osanloo, M., Sedaghat, M. M., Esmaeili, F., & Amani, A. (2018). Larvicidal activity of essential oil of Syzygium aromaticum (Clove) in comparison with its major constituent, eugenol, against Anopheles stephensi. Journal of Arthropod-Borne Diseases, 12(4), 361–369.

    Google Scholar 

  59. Silva, V. B., Travassos, D. L., Nepel, A., Barison, A., Costa, E. V., Scotti, L., et al. (2017). Synthesis and chemometrics of thymol and carvacrol derivatives as larvicides against Aedes aegypti. Journal of Arthropod-Borne Diseases, 11(2), 315–330.

    Google Scholar 

  60. Lima, T. C., Kweka, E. J., Marciale, C. M., & de Sousa, D. P. (2016). Larvicidal activity of essential oil constituents against malaria vector, Anopheles gambiae (Diptera: Culicidae). Natural Products Communications, 11(10), 1539–1540.

    Google Scholar 

  61. Vatandoost, H., & Vaziri, V. (2004). Larvicidal activity of a neem tree extract [Neemarin] against mosquito larvae in the Islamic Republic of Iran. Eastern Mediterranean Health Journal, 10(4–5), 573–581.

    Article  Google Scholar 

  62. Hadjiakhoondi, A., Vatandoost, H., Abousaber, M., Khanavi, M., & Abdi, L. (2008). Chemical composition of the essential oil of Tagetes minuta L. and its effects on Anopheles stephensi larvae in Iran. Journal Medicinal Plants, 7(26), 33–39.

    Google Scholar 

  63. Torabi Pour, H., Shayeghi, M., Vatandoost, H., & Abai, M. R. (2016). Study on larvicidal effects of essential oils of three Iranian native plants against larvae of Anopheles stephensi (Liston). Vector Biol J, 1(2), 2–6. https://doi.org/10.4172/2473-4810.1000109.

    Article  Google Scholar 

  64. Soonwera, M. (2015). Efficacy of essential oil from Cananga odorata (Lamk) Hook.f. & Thomson (Annonaceae) against three mosquito species Aedes aegypti (L.), Anopheles dirus (Peyton and Harrison), and Culex quinquefasciatus (Say). Parasitology Research, 114(12), 4531–4543. https://doi.org/10.1007/s00436-015-4699-1.

    Article  Google Scholar 

  65. Sharifi-Rad, J., Sureda, A., Tenore, G. C., Daglia, M., Sharifi-Rad, M., Valussi, M., et al. (2017). Biological activities of essential oils: From plant chemoecology to traditional healing systems. Molecules (Basel, Switzerland), 22(1), 70. https://doi.org/10.3390/molecules22010070.

    Article  Google Scholar 

  66. Turek, C., & Stintzing, F. C. (2013). Stability of essential oils: A review. Comprehensive Reviews in food Science and Food Safety, 12(1), 40–53. https://doi.org/10.1111/1541-4337.12006.

    Article  Google Scholar 

  67. Ashbaugh, H. S., & Paulaitis, M. E. (2001). Effect of solute size and solute–water attractive interactions on hydration water structure around hydrophobic solutes. Journal of the American Chemical Society, 123(43), 10721–10728. https://doi.org/10.1021/ja016324k.

    Article  Google Scholar 

  68. Carlsson, J., & Åqvist, J. (2006). Calculations of solute and solvent entropies from molecular dynamics simulations. Physical Chemistry Chemical Physics: PCCP, 8(46), 5385–5395. https://doi.org/10.1039/b608486a.

    Article  Google Scholar 

  69. Prakash, A., Baskaran, R., Paramasivam, N., & Vadivel, V. (2018). Essential oil based nanoemulsions to improve the microbial quality of minimally processed fruits and vegetables: A review. Food Research International, 111, 509–523. https://doi.org/10.1016/j.foodres.2018.05.066.

    Article  Google Scholar 

  70. Das, S., Singh, V. K., Dwivedy, A. K., Chaudhari, A. K., & Dubey, N. K. (2021). Nanostructured Pimpinella anisum essential oil as novel green food preservative against fungal infestation, aflatoxin B1 contamination and deterioration of nutritional qualities. Food Chemistry, 344, 128574. https://doi.org/10.1016/j.foodchem.2020.128574.

    Article  Google Scholar 

  71. Zou, Y., Priebe, W., & Perez-Soler, R. (1996). Lyophilized preliposomal formulation of the non-cross-resistant anthracycline annamycin: Effect of surfactant on liposome formation, stability and size. Cancer Chemotherapy and Pharmacology, 39(1–2), 103–108. https://doi.org/10.1007/s002800050544.

    Article  Google Scholar 

  72. Park, J.-B., Noh, H.-g, Jung, J.-H., Kim, J.-M., & Kang, C.-Y. (2012). Enhanced transdermal delivery and optimization of nano-liposome preparation using hydrophilic drug. Journal of Pharmaceutical Investigation, 42(2), 57–63. https://doi.org/10.1007/s40005-012-0009-4.

    Article  Google Scholar 

  73. Tcholakova, S., Mitrinova, Z., Golemanov, K., Denkov, N. D., Vethamuthu, M., & Ananthapadmanabhan, K. P. (2011). Control of Ostwald ripening by using surfactants with high surface modulus. Langmuir, 27(24), 14807–14819. https://doi.org/10.1021/la203952p.

    Article  Google Scholar 

  74. Shahzad, K., & Manzoor, F. (2021). Nanoformulations and their mode of action in insects: A review of biological interactions. Drug and Chemical Toxicology, 44(1), 1–11. https://doi.org/10.1080/01480545.2018.1525393.

    Article  Google Scholar 

  75. Ferreira, R., D’Haveloose, N. P., Cruz, R. A. S., Araujo, R. S., Carvalho, J. C. T., Rocha, L., et al. (2020). Nano-emulsification enhances the larvicidal potential of the essential oil of Siparuna guianensis (Laurales: Siparunaceae) against Aedes (Stegomyia) aegypti (Diptera: Culicidae). Journal of Medical Entomology, 57(3), 788–796. https://doi.org/10.1093/jme/tjz221.

    Article  Google Scholar 

  76. Osanloo, M., Sedaghat, M. M., Sereshti, H., Amani, A. (2019) Nano-encapsulated tarragon (Artemisia dracunculus) essential oil as a sustained release nano-larvicide. Journal of Contemporary Medical, 5 (2), 82–89. https://doi.org/10.22317/jcms.v5i2.570

  77. Kavallieratos, N. G., Nika, E. P., Skourti, A., Ntalli, N., Boukouvala, M. C., Ntalaka, C. T., et al. (2021). Developing a Hazomalania voyronii essential oil nanoemulsion for the eco-friendly management of Tribolium confusum, Tribolium castaneum and Tenebrio molitor larvae and adults on stored wheat. Molecules, 26(6), 1812. https://doi.org/10.3390/molecules26061812.

    Article  Google Scholar 

  78. Benelli, G., Pavoni, L., Zeni, V., Ricciardi, R., Cosci, F., Cacopardo, G., et al. (2020). Developing a highly stable Carlina acaulis essential oil nanoemulsion for managing Lobesia botrana. Nanomaterials, 10(9), 1867. https://doi.org/10.3390/nano10091867.

    Article  Google Scholar 

  79. Chen, J., Wang, W., Xu, Y., & Zhang, X. (2011). Slow-release formulation of a new biological pesticide, pyoluteorin, with mesoporous silica. Journal of Agriculture and Food Chemistry, 59(1), 307–311. https://doi.org/10.1021/jf103640t.

    Article  Google Scholar 

  80. Linxin, D., He, J., Borui, L., Nana, W., & Song, L. (2020). Study of a new 3D MOF and its adsorption, slow release and biological activity in water-soluble and oil-soluble pesticides. Polyhedron, 190, 114752. https://doi.org/10.1016/j.poly.2020.114752.

    Article  Google Scholar 

  81. Liu, B., Wang, Y., Yang, F., Wang, X., Shen, H., Cui, H., & Wu, D. (2016). Construction of a controlled-release delivery system for pesticides using biodegradable PLA-based microcapsules. Colloids and Surfaces B: Biointerfaces, 144, 38–45. https://doi.org/10.1016/j.colsurfb.2016.03.084.

    Article  Google Scholar 

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Funding

Fasa University of Medical Sciences supported this study, grant No. 97502.

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ASD performed larvicidal tests and performed probit analysis. RH interpreted ATR-FTIR spectra. MDMF wrote related discussion about the larvicidal assays. SS reviewed the literature and wrote the introduction. MO designed the study, prepared nanoformulations, and drafted the manuscript. All authors contributed to the drafting of the manuscript and approved the final version.

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Correspondence to Mahmoud Osanloo.

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This study has been approved by the ethics committee at Fasa University of Medical Sciences, IR.FUMS.REC.1400.114. Besides, this research did not involve in vivo or human study.

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Sanei-Dehkordi, A., Heiran, R., Moemenbellah-Fard, M.D. et al. Nanoliposomes Containing Carvacrol and Carvacrol-Rich Essential Oils as Effective Mosquitoes Larvicides. BioNanoSci. 12, 359–369 (2022). https://doi.org/10.1007/s12668-022-00971-5

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