Chemosphere xxx (2013) xxx–xxx
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Larvicidal activity of Mentha x villosa Hudson essential oil, rotundifolone and derivatives Tamires Cardoso Lima a, Tayane Kayne Mariano da Silva a, Fabiana Lima Silva b, José Maria Barbosa-Filho b, Márcia Ortiz Mayo Marques c, Roseli La Corte Santos d, Sócrates Cabral de Holanda Cavalcanti a, Damião Pergentino de Sousa b,⇑ a
Department of Pharmacy, Federal University of Sergipe, CEP 49100-000 São Cristóvão, Sergipe, Brazil Department of Pharmaceutical Sciences, Federal University of Paraíba, CEP 58051-970 João Pessoa, Paraíba, Brazil Center of Genetics, Molecular Biology and Phytochemistry, Agronomic Institute, CEP 13001-970 Campinas, São Paulo, Brazil d Department of Morphology, Federal University of Sergipe, CEP 49100-000 São Cristóvão, Sergipe, Brazil b c
h i g h l i g h t s The Mentha x villosa Hudson essential oil exhibited toxic effects against Aedes aegypti mosquitoes larvae. Rotundifolone, the major constituent of the Mentha x villosa Hudson essential oil, exhibited larvicidal activity. The study showed the structural characteristics which may contribute to the larvicidal activity of rotundifolone and its analogues.
a r t i c l e
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Article history: Received 3 July 2013 Received in revised form 6 October 2013 Accepted 8 October 2013 Available online xxxx Keywords: Larvicidal activity Essential oil Aedes aegypti Terpene Dengue
a b s t r a c t The aim of this study was to evaluate the larvicidal activity of Mentha x villosa essential oil (MVEO) and its major constituent, rotundifolone, against larvae of Aedes aegypti. Additionally, a set of 15 analogues of the rotundifolone were evaluated to identify the molecular characteristics which contribute to the larvicidal effect. The results from the present study showed that the MVEO exhibited outstanding toxic effects against Ae. aegypti larvae (LC50 = 45.0 ppm). Rotundifolone exhibited reasonable larvicidal activity (LC50 = 62.5 ppm). With respect to comparative study of rotundifolone and its analogues, all tested compounds were less potent than rotundifolone, except ()-limonene. In general, replacement of C–C double bonds by epoxides groups decreases the larvicidal potency. The presence of a,b-unsaturated carbonyls contributes to the larvicidal toxicity. The addition of hydroxyl groups in the chemical structure resulted in less potent compounds. Furthermore, the enantioselectivity seems to play an important role for the larvicidal toxicity. Ó 2013 Published by Elsevier Ltd.
1. Introduction Dengue is an infectious disease caused by an arbovirus transmitted to humans by the bite of female mosquitoes of the genus Aedes. Among many vectors, Aedes aegypti L. (Diptera: Culicidae) is the one of utmost epidemiological importance (Ligon, 2005; Coelho et al., 2009). Over the past 60 years the incidence, distribution, and clinical severity of dengue have increased dramatically; resulting in the most important viral disease transmitted by arthropod vectors in terms of mortality and morbidity (Rigau-Pérez et al., 1998; Rosen, 1999). In the absence of effective and safe vaccines for dengue prevention, the epidemics control is accomplished by monitoring ⇑ Corresponding author. Tel.: +55 7988329710. E-mail address: [email protected] (D.P. de Sousa).
mosquitoes breeding sites and by the use of synthetic chemical insecticides to control the spreading of adult or larval forms of Ae. aegypti (Tauil, 2001; Porto et al., 2008). Although the chemical products are effective, the continuous use in large scale has contributed to the emergence of many negative consequences, such as, the appearance of insecticide resistance in dengue vectors leading to decreased efficacy and adverse effects on non-target species, including humans (Zahran and Abdelgaleil, 2011). These problems have persuaded numerous researches in order to develop alternative strategies using natural products to control Ae. aegypti proliferation. In this direction, the plant essential oils and their major constituents have received much attention as potential bioactive agents against mosquito vector (Cheng et al., 2009; Waliwitiya et al., 2009; Zahran and Abdelgaleil, 2011). The genus Mentha is represented by about 19 species and 13 natural hybrids and it is an important member of the family
0045-6535/$ - see front matter Ó 2013 Published by Elsevier Ltd. http://dx.doi.org/10.1016/j.chemosphere.2013.10.035
Please cite this article in press as: Lima, T.C., et al. Larvicidal activity of Mentha x villosa Hudson essential oil, rotundifolone and derivatives. Chemosphere (2013), http://dx.doi.org/10.1016/j.chemosphere.2013.10.035
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Lamiaceae (Kumar et al., 2011a). Various essential oils of Mentha have been described in the literature for its insecticidal properties, such as the essential oil of Mentha pulegium (Franzios et al., 1997), Mentha piperita (Ansari et al., 2000), Mentha spicata, Mentha longifolia, and Mentha suaveolens (Koliopoulos et al., 2010). The specie Mentha x villosa Hudson popularly known as ‘‘hortelã-da-folhamiúda’’ or Cuban mint is an herb largely cultivated in northeastern Brazil (Alencastro et al., 1965). The essential oil from M. x villosa Hudson possess several biological properties (Arruda et al., 2006; De Sousa et al., 2007, 2008), however, there are no studies about its insecticidal activity against Ae. aegypti. Therefore, the present study aims to evaluate the larvicidal activity of M. x villosa Hudson (MVEO) leaves essential oil and its main constituent, the monoterpene rotundifolone, against thirdinstar larvae of Ae. aegypti. Additionally, the Structure-Activity Relationships (SAR) involving a set of 15 analogues compounds of rotundifolone was investigated.
The compounds pulegone epoxide (Katsuhara, 1967), (+)- and ()-carvone epoxide (Santos et al., 1997), (+)- and ()-limonene epoxide (Thomas and Bessière, 1989), ()-perillaldehyde (Furniss et al., 1998), perillaldehyde epoxide (Kido et al., 1992), transisopulegone (Moreira and Corrêa, 2003), hydroxycarvone, hydroxydihydrocarvone (Büchi and Wuest, 1979), trans-dihydrocarvone (Faria et al., 2000) and acetoxycarvotanacetone (Andrade et al., 2011) were prepared in our laboratory according to the literature and analyzed by infrared, 1H and 13C NMR. (+)-Pulegone, ()-carvone, ()-limonene and Temephos was purchased from Sigma– Aldrich Co. (St. Louis, MO, USA). Chemical structures of the evaluated compounds are shown in Fig. 1.
2. Material and methods
2.6. Larvicidal assay
2.1. Plant material
The steam-distilled oil was analyzed by gas chromatographymass spectrometry (GC/MS) using a Hewlett Packard equipment, chromatograph model 5890 equipped with a mass spectrometer model 5988A and an OV-5 capillary column (30 m 0.25 mm 0.25 lm) using the following analytical conditions: electron impact, 70 eV; carrier gas, Helium; flow rate, 1.0 mL/min; oven temperature programmed from 60 to 240 °C at 3 °C/min; injector temperature, 240 °C; detector temperature, 230 °C; split ratio 1/20. The injected volume was 1.0 ll of a solution containing ca. 0.1 ll of oil in 1.0 mL of ethyl acetate. The identification of each component was performed by comparing their mass spectra with the database of the GC/MS (Nist 62 lib.) and Kovats retention indices (Adams, 2001).
Larval mortality bioassays were performed according to the methodology recommended by WHO and adapted by Santos et al. (2011). The larvicidal properties of the MVEO, rotundifolone and its analogues were evaluated on third-instar larvae and in all the experiments was used only the Rockefeller lineage. Eggs of Ae. aegypti were obtained from the insectary of the Federal University of Sergipe attached to paper stips. Paper strips (1000 eggs L1) were placed in a rectangular polyethylene container containing natural mineral water and cat food (whiskas) to allow regular development of the larvae. The container was kept in the insectary for hatching and monitoring of larvae development for 3–4 days. The concentration ranges were determined by a preliminary curve concentration–response with 20 larvae. Standard solutions (20,000 ppm) of the tested oil and compounds were prepared using MVEO (20 mg), Tween-80 (10% v/v) and natural mineral water (90% v/v) or each compound (20 mg), Tween-80 (10% v/v), dimethyl sulfoxide (30% v/v) and natural mineral water (60% v/v). From the standard solution, a series of dilutions was prepared ranging from 10 to 2500 ppm. Twenty larvae were collected with a Pasteur pipette and placed on a 50 mL graduated cylinder. The volume was completed to 20 mL with natural mineral water and transferred to disposable cups containing variable concentrations of the standard solution. For each test, negative control was conducted using the same number of larvae in Tween-80 (0.1 mL), dimethyl sulfoxide (0.3 mL), and mineral water (19.6 mL) or only Tween-80 (0.1 mL) and mineral water (19.9 mL). Three replicates were used for each concentration and the control. The organophosphorate Temephos (O,O0 -(thio-di-4,1-phenylene)bis(O,Odimethylphpsphorothiotate)), a commonly used insecticide for larvae control, was used as positive control. The mortality was recorded after 24 h exposure to different concentration of testing solutions. Larvae were considered dead when they did not respond to stimulus.
2.4. Isolation of rotundifolone from the essential oil of M. x villosa
2.7. Statistical analysis
Rotundifolone was isolated of MVEO using a procedure previously described by Almeida et al. (1996). The essential oil was submitted to preparative thin layer chromatography (PTLC). The plates were developed three times using hexanes as eluent. When the plates were exposed to UV light (254 nm), rotundifolone was visualized as the major component of the essential oil. Rotundifolone was removed from chromatographic plates and later recovered by extraction with dichloromethane followed by filtration and evaporation to obtain a yellowish oil. The structural identification was made by infrared, 1H and 13C Nuclear Magnetic Resonance
The larvicidal assays mortality data were subjected to Probit analysis (Finney, 1971) to estimate the lethal concentration for 50% mortality (LC50) and 95% confidence intervals (CI) values for the respective oil and compounds (Table 1). In all cases where deaths had occurred in the control experiment between 5% and 20%, correction was performed by applying the Abbott’s formula (1925):
M. x villosa leaves were collected in the Medicinal Plants’ Garden of the Pharmaceutical Technology Laboratory of the Federal University of Paraíba/Brazil in July 2008 (7°080 2900 S, 34°500 4800 W). A voucher specimen has been deposited at the Herbarium Prisco Bezerra of the Federal University of Ceará/Brazil, with the number 14996. 2.2. Extraction of the essential oil Fresh leaves of M. x villosa (10 kg) were subjected to a steam distillation for 8 h and an oil of yellowish coloration and characteristic odor was obtained. Subsequently, the oil was dried over anhydrous sodium sulfate, filtered, and stored at 4 °C. The yield was calculated from weight of fresh material (Matos et al., 1999). 2.3. Analysis by GC/MS
(NMR) analysis and comparison with the literature data (Almeida et al., 1996). 2.5. Rotundifolone analogues
% Deaths ¼
% test mortality % control mortality 100 100 % mortality
Please cite this article in press as: Lima, T.C., et al. Larvicidal activity of Mentha x villosa Hudson essential oil, rotundifolone and derivatives. Chemosphere (2013), http://dx.doi.org/10.1016/j.chemosphere.2013.10.035
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O
O O
O
Rotundifolone, 1
(+)-Pulegone, 2
O
O
Pulegone epoxide, 3
(-)-Carvone, 4
O
O
O
O
O
(-)-Carvone epoxide, 6
(+)-Carvone epoxide, 5
H
(-)-Limonene, 7
O
H
O
(+)-Limonene epoxide, 8
O O
O
(-)-Limonene epoxide, 9
(-)-Perillaldehyde, 10
O
Perillaldehyde epoxide, 11
O
O
O
OH Transdihydrocarvone, 13
Trans-isopulegone, 12
O
OH
Hydroxycarvone, 14 Hydroxydihydrocarvone, 15
O
Acetoxycarvotanacetone, 16 Fig. 1. Structures of evaluated compounds.
When the control experiment mortality was over 20% the test were discarded and repeated. Compounds activity was considered significantly different if the 95% confidence limits did not overlap. 3. Results and discussion The MVEO was obtained by steam distillation with 0.1% yield. Table 1 shows the identified chemical constituents, their retention indices, and percentage composition, listed in order of elution in the OV-5 column. A total of 15 compounds, representing 91.92% of the essential oil, were characterized using GC/MS analyses. Among these 84.70% were monoterpenes and 7.22% sesquiterpenes. The major component was identified as the oxygenated monoterpene rotundifolone, also known as piperitenone oxide, found in high percentage (70.96%). All the other constituents were present in low amount ( 500 mg/L) against the larvae of Ae. aegypti than borneol (alcohol) (LC50 = 183.1 mg/L). In view of the importance of chirality in the biological activity, the pairs of enantiomers (+)-carvone epoxide (5) and ()-carvone epoxide (6), as well as, (+)-limonene epoxide (8) and ()-limonene epoxide (9) were compared to investigate the role of enantioselectivity in the larvicidal activity against mosquitoes. (+)- and ()carvone epoxide showed different larvicides activities, LC50 values of 254.6 ppm and 217.5 ppm, respectively. These data indicate that the enantioselectivity may play an important role in the larvicidal activity. However, there is no difference in the larvicidal potency when comparing compounds 8 and 9, exhibiting LC50 values of
Please cite this article in press as: Lima, T.C., et al. Larvicidal activity of Mentha x villosa Hudson essential oil, rotundifolone and derivatives. Chemosphere (2013), http://dx.doi.org/10.1016/j.chemosphere.2013.10.035
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525.0 ppm and 522.5 ppm, respectively. Michaelakis et al. (2009) evaluated the larvicidal activity and selectivity of four enantiomeric pinenes against the mosquito Cx. pipiens. The authors reported that the enantiomers (1R)-(+)-a-pinene and (1S)-()-apinene showed similar activity, while the enantiomers (1R)-(+)b-pinene and (1S)-()-b-pinene exhibit different larvicidal effects. Additionally, the ()-b enantiomer was the most toxic among pinenes, with LC50 value of 36.53 mg/L. Michaelakis et al. (2011) revealed that menthone was more toxic against the larvae of Cx. pipiens than its enantiomer isomenthone, indicating that the enantioselectivity seems to play an important action for the toxicity of essential oils. Some of the LC50 values expressed in this report are different from published data in the literature (Cheng et al., 2009; Waliwitiya et al., 2009) which may be the result of different analysis and methodologies (Santos et al., 2011). Moreover, larvae of different species or populations and that occupy different ecological niches may have different susceptibility level to specific compounds (Waliwitiya et al., 2009). 4. Conclusion This paper presented a study about the larvicidal activity of the MVEO, and its main constituent, the monoterpene rotundifolone, against larvae of Ae. aegypti. Additionally, we have attempted to learn the SAR involving a set of 15 analogues of rotundifolone. The MVEO showed strong toxic effect against Ae. aegypti larvae, suggesting a potential use to control the dengue vector. The results of comparing rotundifolone and its analogues confirmed that the different functional groups and their positions in the p-menthane skeleton influence the larvicidal activity, suggesting that appropriate structural modifications in the monoterpenes may be possible to develop new larvicides agents. Acknowledgements The authors are thankful to the CAPES, CNPq, FAPITEC, and Federal University of Sergipe for financial support. References Abbott, W.S., 1925. A method for computing the effectiveness of insecticides. J. Econ. Entomol. 18, 265–267. Abdelgaleil, S.A.M., Mohamed, M.I.E., Badawy, M.E.I., El-Arami, S.A.A., 2009. Fumigant and contact toxicities of monoterpenes to Sitophilus oryzae (L.) and Tribolium castaneum (Herbst) and their inhibitory effects on acetylcholinesterase activity. J. Chem. Ecol. 35, 518–525. Adams, R.P., 2001. Identification of Essential Oil Components by Gas Chromatography/mass Spectroscopy. Allured Publishing Corporation, Carol Stream, Illinois (USA), p. 456. Andrade, L.N., Batista, J.S., De Sousa, D.P., 2011. Spasmolytic activity of p-menthane esters. J. Med. Plant Res. 5, 6995–6999. Alencastro, F.M.M.R., Scatone, Z., Prisco, J.T., Laboriau, L.F.G., 1965. Contribuição para uma bibliografia do gênero Mentha L. Associação Brasileira de Pesquisa de Plantas Aromáticas. Óleos Essenciais, Campinas, SP, Brazil, p. 354. Almeida, R.N., Hiruma, C.A., Barbosa-Filho, J.M., 1996. Analgesic effect of rotundifolone in rodents. Fitoterapia 67, 334–338. Ansari, M.A., Vasudevan, P., Tandon, M., Razdan, R.K., 2000. Larvicidal and mosquito repellent action of peppermint (Mentha piperita) oil. Bioresour. Technol. 71, 267–271. Arruda, T.A., Antunes, R.M.P., Catão, R.M.R., Lima, E.O., Sousa, D.P., Nunes, X.P., Pereira, M.S.V., Barbosa-Filho, J.M., Da Cunha, E.V.L., 2006. Preliminary study of the antimicrobial activity of Mentha x villosa Hudson essential oil, rotundifolone and its analogues. Rev. Bras. Farmacog. 16 (3), 307–311. Büchi, G., Wuest, H.J., 1979. New synthesis of b-agarofuran and of dihydroagarofuran. J. Org. Chem. 44, 546–549. Cheng, S.S., Chang, H.T., Lin, C.Y., Chen, P.S., Huang, C.G., Chen, W.J., Chang, S.T., 2009. Insecticidal activities of leaf and twig essential oils from Clausena excavata against Aedes aegypti and Aedes albopictus larvae. Pest Manage. Sci. 65, 339–343. Coelho, A.A.M., De Paula, J.E., Espíndola, L.S., 2009. Atividade larvicida de extratos vegetais sobre Aedes aegypti (L.) (Diptera: Culicidae), em condições de laboratório. Bioassay 4, 1–6.
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Please cite this article in press as: Lima, T.C., et al. Larvicidal activity of Mentha x villosa Hudson essential oil, rotundifolone and derivatives. Chemosphere (2013), http://dx.doi.org/10.1016/j.chemosphere.2013.10.035
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Larvicidal activity of Mentha x villosa Hudson essential oil, rotundifolone and derivatives Tamires Cardoso Lima a, Tayane Kayne Mariano da Silva a, Fabiana Lima Silva b, José Maria Barbosa-Filho b, Márcia Ortiz Mayo Marques c, Roseli La Corte Santos d, Sócrates Cabral de Holanda Cavalcanti a, Damião Pergentino de Sousa b,⇑ a
Department of Pharmacy, Federal University of Sergipe, CEP 49100-000 São Cristóvão, Sergipe, Brazil Department of Pharmaceutical Sciences, Federal University of Paraíba, CEP 58051-970 João Pessoa, Paraíba, Brazil Center of Genetics, Molecular Biology and Phytochemistry, Agronomic Institute, CEP 13001-970 Campinas, São Paulo, Brazil d Department of Morphology, Federal University of Sergipe, CEP 49100-000 São Cristóvão, Sergipe, Brazil b c
h i g h l i g h t s The Mentha x villosa Hudson essential oil exhibited toxic effects against Aedes aegypti mosquitoes larvae. Rotundifolone, the major constituent of the Mentha x villosa Hudson essential oil, exhibited larvicidal activity. The study showed the structural characteristics which may contribute to the larvicidal activity of rotundifolone and its analogues.
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Article history: Received 3 July 2013 Received in revised form 6 October 2013 Accepted 8 October 2013 Available online xxxx Keywords: Larvicidal activity Essential oil Aedes aegypti Terpene Dengue
a b s t r a c t The aim of this study was to evaluate the larvicidal activity of Mentha x villosa essential oil (MVEO) and its major constituent, rotundifolone, against larvae of Aedes aegypti. Additionally, a set of 15 analogues of the rotundifolone were evaluated to identify the molecular characteristics which contribute to the larvicidal effect. The results from the present study showed that the MVEO exhibited outstanding toxic effects against Ae. aegypti larvae (LC50 = 45.0 ppm). Rotundifolone exhibited reasonable larvicidal activity (LC50 = 62.5 ppm). With respect to comparative study of rotundifolone and its analogues, all tested compounds were less potent than rotundifolone, except ()-limonene. In general, replacement of C–C double bonds by epoxides groups decreases the larvicidal potency. The presence of a,b-unsaturated carbonyls contributes to the larvicidal toxicity. The addition of hydroxyl groups in the chemical structure resulted in less potent compounds. Furthermore, the enantioselectivity seems to play an important role for the larvicidal toxicity. Ó 2013 Published by Elsevier Ltd.
1. Introduction Dengue is an infectious disease caused by an arbovirus transmitted to humans by the bite of female mosquitoes of the genus Aedes. Among many vectors, Aedes aegypti L. (Diptera: Culicidae) is the one of utmost epidemiological importance (Ligon, 2005; Coelho et al., 2009). Over the past 60 years the incidence, distribution, and clinical severity of dengue have increased dramatically; resulting in the most important viral disease transmitted by arthropod vectors in terms of mortality and morbidity (Rigau-Pérez et al., 1998; Rosen, 1999). In the absence of effective and safe vaccines for dengue prevention, the epidemics control is accomplished by monitoring ⇑ Corresponding author. Tel.: +55 7988329710. E-mail address: [email protected] (D.P. de Sousa).
mosquitoes breeding sites and by the use of synthetic chemical insecticides to control the spreading of adult or larval forms of Ae. aegypti (Tauil, 2001; Porto et al., 2008). Although the chemical products are effective, the continuous use in large scale has contributed to the emergence of many negative consequences, such as, the appearance of insecticide resistance in dengue vectors leading to decreased efficacy and adverse effects on non-target species, including humans (Zahran and Abdelgaleil, 2011). These problems have persuaded numerous researches in order to develop alternative strategies using natural products to control Ae. aegypti proliferation. In this direction, the plant essential oils and their major constituents have received much attention as potential bioactive agents against mosquito vector (Cheng et al., 2009; Waliwitiya et al., 2009; Zahran and Abdelgaleil, 2011). The genus Mentha is represented by about 19 species and 13 natural hybrids and it is an important member of the family
0045-6535/$ - see front matter Ó 2013 Published by Elsevier Ltd. http://dx.doi.org/10.1016/j.chemosphere.2013.10.035
Please cite this article in press as: Lima, T.C., et al. Larvicidal activity of Mentha x villosa Hudson essential oil, rotundifolone and derivatives. Chemosphere (2013), http://dx.doi.org/10.1016/j.chemosphere.2013.10.035
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Lamiaceae (Kumar et al., 2011a). Various essential oils of Mentha have been described in the literature for its insecticidal properties, such as the essential oil of Mentha pulegium (Franzios et al., 1997), Mentha piperita (Ansari et al., 2000), Mentha spicata, Mentha longifolia, and Mentha suaveolens (Koliopoulos et al., 2010). The specie Mentha x villosa Hudson popularly known as ‘‘hortelã-da-folhamiúda’’ or Cuban mint is an herb largely cultivated in northeastern Brazil (Alencastro et al., 1965). The essential oil from M. x villosa Hudson possess several biological properties (Arruda et al., 2006; De Sousa et al., 2007, 2008), however, there are no studies about its insecticidal activity against Ae. aegypti. Therefore, the present study aims to evaluate the larvicidal activity of M. x villosa Hudson (MVEO) leaves essential oil and its main constituent, the monoterpene rotundifolone, against thirdinstar larvae of Ae. aegypti. Additionally, the Structure-Activity Relationships (SAR) involving a set of 15 analogues compounds of rotundifolone was investigated.
The compounds pulegone epoxide (Katsuhara, 1967), (+)- and ()-carvone epoxide (Santos et al., 1997), (+)- and ()-limonene epoxide (Thomas and Bessière, 1989), ()-perillaldehyde (Furniss et al., 1998), perillaldehyde epoxide (Kido et al., 1992), transisopulegone (Moreira and Corrêa, 2003), hydroxycarvone, hydroxydihydrocarvone (Büchi and Wuest, 1979), trans-dihydrocarvone (Faria et al., 2000) and acetoxycarvotanacetone (Andrade et al., 2011) were prepared in our laboratory according to the literature and analyzed by infrared, 1H and 13C NMR. (+)-Pulegone, ()-carvone, ()-limonene and Temephos was purchased from Sigma– Aldrich Co. (St. Louis, MO, USA). Chemical structures of the evaluated compounds are shown in Fig. 1.
2. Material and methods
2.6. Larvicidal assay
2.1. Plant material
The steam-distilled oil was analyzed by gas chromatographymass spectrometry (GC/MS) using a Hewlett Packard equipment, chromatograph model 5890 equipped with a mass spectrometer model 5988A and an OV-5 capillary column (30 m 0.25 mm 0.25 lm) using the following analytical conditions: electron impact, 70 eV; carrier gas, Helium; flow rate, 1.0 mL/min; oven temperature programmed from 60 to 240 °C at 3 °C/min; injector temperature, 240 °C; detector temperature, 230 °C; split ratio 1/20. The injected volume was 1.0 ll of a solution containing ca. 0.1 ll of oil in 1.0 mL of ethyl acetate. The identification of each component was performed by comparing their mass spectra with the database of the GC/MS (Nist 62 lib.) and Kovats retention indices (Adams, 2001).
Larval mortality bioassays were performed according to the methodology recommended by WHO and adapted by Santos et al. (2011). The larvicidal properties of the MVEO, rotundifolone and its analogues were evaluated on third-instar larvae and in all the experiments was used only the Rockefeller lineage. Eggs of Ae. aegypti were obtained from the insectary of the Federal University of Sergipe attached to paper stips. Paper strips (1000 eggs L1) were placed in a rectangular polyethylene container containing natural mineral water and cat food (whiskas) to allow regular development of the larvae. The container was kept in the insectary for hatching and monitoring of larvae development for 3–4 days. The concentration ranges were determined by a preliminary curve concentration–response with 20 larvae. Standard solutions (20,000 ppm) of the tested oil and compounds were prepared using MVEO (20 mg), Tween-80 (10% v/v) and natural mineral water (90% v/v) or each compound (20 mg), Tween-80 (10% v/v), dimethyl sulfoxide (30% v/v) and natural mineral water (60% v/v). From the standard solution, a series of dilutions was prepared ranging from 10 to 2500 ppm. Twenty larvae were collected with a Pasteur pipette and placed on a 50 mL graduated cylinder. The volume was completed to 20 mL with natural mineral water and transferred to disposable cups containing variable concentrations of the standard solution. For each test, negative control was conducted using the same number of larvae in Tween-80 (0.1 mL), dimethyl sulfoxide (0.3 mL), and mineral water (19.6 mL) or only Tween-80 (0.1 mL) and mineral water (19.9 mL). Three replicates were used for each concentration and the control. The organophosphorate Temephos (O,O0 -(thio-di-4,1-phenylene)bis(O,Odimethylphpsphorothiotate)), a commonly used insecticide for larvae control, was used as positive control. The mortality was recorded after 24 h exposure to different concentration of testing solutions. Larvae were considered dead when they did not respond to stimulus.
2.4. Isolation of rotundifolone from the essential oil of M. x villosa
2.7. Statistical analysis
Rotundifolone was isolated of MVEO using a procedure previously described by Almeida et al. (1996). The essential oil was submitted to preparative thin layer chromatography (PTLC). The plates were developed three times using hexanes as eluent. When the plates were exposed to UV light (254 nm), rotundifolone was visualized as the major component of the essential oil. Rotundifolone was removed from chromatographic plates and later recovered by extraction with dichloromethane followed by filtration and evaporation to obtain a yellowish oil. The structural identification was made by infrared, 1H and 13C Nuclear Magnetic Resonance
The larvicidal assays mortality data were subjected to Probit analysis (Finney, 1971) to estimate the lethal concentration for 50% mortality (LC50) and 95% confidence intervals (CI) values for the respective oil and compounds (Table 1). In all cases where deaths had occurred in the control experiment between 5% and 20%, correction was performed by applying the Abbott’s formula (1925):
M. x villosa leaves were collected in the Medicinal Plants’ Garden of the Pharmaceutical Technology Laboratory of the Federal University of Paraíba/Brazil in July 2008 (7°080 2900 S, 34°500 4800 W). A voucher specimen has been deposited at the Herbarium Prisco Bezerra of the Federal University of Ceará/Brazil, with the number 14996. 2.2. Extraction of the essential oil Fresh leaves of M. x villosa (10 kg) were subjected to a steam distillation for 8 h and an oil of yellowish coloration and characteristic odor was obtained. Subsequently, the oil was dried over anhydrous sodium sulfate, filtered, and stored at 4 °C. The yield was calculated from weight of fresh material (Matos et al., 1999). 2.3. Analysis by GC/MS
(NMR) analysis and comparison with the literature data (Almeida et al., 1996). 2.5. Rotundifolone analogues
% Deaths ¼
% test mortality % control mortality 100 100 % mortality
Please cite this article in press as: Lima, T.C., et al. Larvicidal activity of Mentha x villosa Hudson essential oil, rotundifolone and derivatives. Chemosphere (2013), http://dx.doi.org/10.1016/j.chemosphere.2013.10.035
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O
O O
O
Rotundifolone, 1
(+)-Pulegone, 2
O
O
Pulegone epoxide, 3
(-)-Carvone, 4
O
O
O
O
O
(-)-Carvone epoxide, 6
(+)-Carvone epoxide, 5
H
(-)-Limonene, 7
O
H
O
(+)-Limonene epoxide, 8
O O
O
(-)-Limonene epoxide, 9
(-)-Perillaldehyde, 10
O
Perillaldehyde epoxide, 11
O
O
O
OH Transdihydrocarvone, 13
Trans-isopulegone, 12
O
OH
Hydroxycarvone, 14 Hydroxydihydrocarvone, 15
O
Acetoxycarvotanacetone, 16 Fig. 1. Structures of evaluated compounds.
When the control experiment mortality was over 20% the test were discarded and repeated. Compounds activity was considered significantly different if the 95% confidence limits did not overlap. 3. Results and discussion The MVEO was obtained by steam distillation with 0.1% yield. Table 1 shows the identified chemical constituents, their retention indices, and percentage composition, listed in order of elution in the OV-5 column. A total of 15 compounds, representing 91.92% of the essential oil, were characterized using GC/MS analyses. Among these 84.70% were monoterpenes and 7.22% sesquiterpenes. The major component was identified as the oxygenated monoterpene rotundifolone, also known as piperitenone oxide, found in high percentage (70.96%). All the other constituents were present in low amount ( 500 mg/L) against the larvae of Ae. aegypti than borneol (alcohol) (LC50 = 183.1 mg/L). In view of the importance of chirality in the biological activity, the pairs of enantiomers (+)-carvone epoxide (5) and ()-carvone epoxide (6), as well as, (+)-limonene epoxide (8) and ()-limonene epoxide (9) were compared to investigate the role of enantioselectivity in the larvicidal activity against mosquitoes. (+)- and ()carvone epoxide showed different larvicides activities, LC50 values of 254.6 ppm and 217.5 ppm, respectively. These data indicate that the enantioselectivity may play an important role in the larvicidal activity. However, there is no difference in the larvicidal potency when comparing compounds 8 and 9, exhibiting LC50 values of
Please cite this article in press as: Lima, T.C., et al. Larvicidal activity of Mentha x villosa Hudson essential oil, rotundifolone and derivatives. Chemosphere (2013), http://dx.doi.org/10.1016/j.chemosphere.2013.10.035
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525.0 ppm and 522.5 ppm, respectively. Michaelakis et al. (2009) evaluated the larvicidal activity and selectivity of four enantiomeric pinenes against the mosquito Cx. pipiens. The authors reported that the enantiomers (1R)-(+)-a-pinene and (1S)-()-apinene showed similar activity, while the enantiomers (1R)-(+)b-pinene and (1S)-()-b-pinene exhibit different larvicidal effects. Additionally, the ()-b enantiomer was the most toxic among pinenes, with LC50 value of 36.53 mg/L. Michaelakis et al. (2011) revealed that menthone was more toxic against the larvae of Cx. pipiens than its enantiomer isomenthone, indicating that the enantioselectivity seems to play an important action for the toxicity of essential oils. Some of the LC50 values expressed in this report are different from published data in the literature (Cheng et al., 2009; Waliwitiya et al., 2009) which may be the result of different analysis and methodologies (Santos et al., 2011). Moreover, larvae of different species or populations and that occupy different ecological niches may have different susceptibility level to specific compounds (Waliwitiya et al., 2009). 4. Conclusion This paper presented a study about the larvicidal activity of the MVEO, and its main constituent, the monoterpene rotundifolone, against larvae of Ae. aegypti. Additionally, we have attempted to learn the SAR involving a set of 15 analogues of rotundifolone. The MVEO showed strong toxic effect against Ae. aegypti larvae, suggesting a potential use to control the dengue vector. The results of comparing rotundifolone and its analogues confirmed that the different functional groups and their positions in the p-menthane skeleton influence the larvicidal activity, suggesting that appropriate structural modifications in the monoterpenes may be possible to develop new larvicides agents. Acknowledgements The authors are thankful to the CAPES, CNPq, FAPITEC, and Federal University of Sergipe for financial support. References Abbott, W.S., 1925. A method for computing the effectiveness of insecticides. J. Econ. Entomol. 18, 265–267. Abdelgaleil, S.A.M., Mohamed, M.I.E., Badawy, M.E.I., El-Arami, S.A.A., 2009. Fumigant and contact toxicities of monoterpenes to Sitophilus oryzae (L.) and Tribolium castaneum (Herbst) and their inhibitory effects on acetylcholinesterase activity. J. Chem. Ecol. 35, 518–525. Adams, R.P., 2001. Identification of Essential Oil Components by Gas Chromatography/mass Spectroscopy. Allured Publishing Corporation, Carol Stream, Illinois (USA), p. 456. Andrade, L.N., Batista, J.S., De Sousa, D.P., 2011. Spasmolytic activity of p-menthane esters. J. Med. Plant Res. 5, 6995–6999. Alencastro, F.M.M.R., Scatone, Z., Prisco, J.T., Laboriau, L.F.G., 1965. Contribuição para uma bibliografia do gênero Mentha L. Associação Brasileira de Pesquisa de Plantas Aromáticas. Óleos Essenciais, Campinas, SP, Brazil, p. 354. Almeida, R.N., Hiruma, C.A., Barbosa-Filho, J.M., 1996. Analgesic effect of rotundifolone in rodents. Fitoterapia 67, 334–338. Ansari, M.A., Vasudevan, P., Tandon, M., Razdan, R.K., 2000. Larvicidal and mosquito repellent action of peppermint (Mentha piperita) oil. Bioresour. Technol. 71, 267–271. Arruda, T.A., Antunes, R.M.P., Catão, R.M.R., Lima, E.O., Sousa, D.P., Nunes, X.P., Pereira, M.S.V., Barbosa-Filho, J.M., Da Cunha, E.V.L., 2006. Preliminary study of the antimicrobial activity of Mentha x villosa Hudson essential oil, rotundifolone and its analogues. Rev. Bras. Farmacog. 16 (3), 307–311. Büchi, G., Wuest, H.J., 1979. New synthesis of b-agarofuran and of dihydroagarofuran. J. Org. Chem. 44, 546–549. Cheng, S.S., Chang, H.T., Lin, C.Y., Chen, P.S., Huang, C.G., Chen, W.J., Chang, S.T., 2009. Insecticidal activities of leaf and twig essential oils from Clausena excavata against Aedes aegypti and Aedes albopictus larvae. Pest Manage. Sci. 65, 339–343. Coelho, A.A.M., De Paula, J.E., Espíndola, L.S., 2009. Atividade larvicida de extratos vegetais sobre Aedes aegypti (L.) (Diptera: Culicidae), em condições de laboratório. Bioassay 4, 1–6.
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Please cite this article in press as: Lima, T.C., et al. Larvicidal activity of Mentha x villosa Hudson essential oil, rotundifolone and derivatives. Chemosphere (2013), http://dx.doi.org/10.1016/j.chemosphere.2013.10.035
