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Journal of Tropical Medicine logoLink to Journal of Tropical Medicine
. 2016 Nov 7;2016:8540830. doi: 10.1155/2016/8540830

Preparation of Ecofriendly Formulations Containing Biologically Active Monoterpenes with Their Fumigant and Residual Toxicities against Adults of Culex pipiens

Mohamed E I Badawy 1,*, Nehad E M Taktak 2, Osama M Awad 2, Souraya A Elfiki 2, Nadia E Abou El-Ela 2
PMCID: PMC5116529  PMID: 27891154

Abstract

Different mixtures of monoterpenes (ketone, alcohol, and alkene) were loaded on paper discs and wax and their knockdown activities were evaluated against Culex pipiens adults. Some individual monoterpenes were also evaluated by residual toxicity technique. Citronella oil as a reference was also loaded separately or in combination with monoterpenes on paper discs and wax. The ketone monoterpenes mixture (camphor, menthone, carvone, and fenchone) on paper discs was the most active (KT50 = 17.20 min) followed by ketone monoterpenes with citronella oil (KT50 = 20.79 min) and citronella oil alone (KT50 = 28.72 min). Wax formulations proved that the ketone and alcohol (geraniol, thymol, and menthol) monoterpenes gave the most activity as knockdown (KT50 = 31.79 and 43.39 min, resp.). Alcohol monoterpenes formulation recorded KT50 = 43.39 min. Residual activity of tested individual monoterpenes reported that the menthol was more toxic than camphor and camphene. Generally, this study suggests that the monoterpenes have the properties, which make them used as eco-friendly compounds in the control programs of Cx. pipiens adult. The use of paper discs is more applicable than wax in the adulticidal formulations.

1. Introduction

Man has suffered from the activities of mosquitoes since time immemorial and it is ranked as man's most important insect pest. The genera of mosquito have been incriminated as the main vectors: Culex, Aedes, and Anopheles, which transmit several infectious diseases to human; for example, filariasis, Japanese encephalitis, dengue and yellow fever viruses, and malaria [1, 2] are major threat to over two billion people in the tropics. Mosquito bites may also cause allergic responses including local skin reactions and systemic reactions such as urticaria and angioedema [3].

In Egypt, the widespread house mosquito Cx. pipiens molestus (Forsk) has been recorded in all governorates without any exception [4] causing a health problem and nuisance to humans [5]. It is the major vector of bancroftian filariasis, which caused the problems of about 120 million infected and disabled persons annually [6], Rift valley fever, and diseases caused by other viruses [7, 8].

Mosquito control represents an important strategy for prevention of diseases transmission and epidemic outbreaks. Synthetic pesticides have been commonly used for adult mosquito control such as organophosphates (Malathion and Naled) and synthetic pyrethroids (Permethrin, Resmethrin, Sumithrin, Prallethrin, and Etofenprox). Adulticides were applied as ultra-low volume (ULV) sprays either by aircraft or on the ground employing truck-mounted sprayers. ULV sprayers dispense very fine aerosol droplets that stay aloft and kill flying mosquitoes on contact. ULV applications involve small quantities of pesticide active ingredient in relation to the size of the area treated, which minimizes exposure and risks to people and the environment [9, 10]. However, continued use of adulticides for generations develops the phenomenon of resistance accompanied by harmful effects on human health and the environment [1, 1113]. The search for ecofriendly alternative mosquitocides that have minimal risk to human health and the environment is considered the goal of many researchers. Therefore, botanical insecticides have become more popular as alternatives to synthetic chemical mosquitocides, substantiated by many studies confirming the mosquitocidal properties of numerous plant-derived compounds from various sources [1418]. Monoterpenes are the main component in the plurality of plant essential oils and give plants their unique odoriferous properties because of their low boiling points. The natural pesticidal properties of some monoterpenes make them good alternative pest control agents as well as good lead compounds for the development of ecofriendly and fully biodegradable pesticides. Some studies have been conducted on the insecticidal properties of monoterpenes against various mosquitoes. For example, Radwan and others studied fourteen major monoterpenoids and reported their toxic effect against Cx. pipiens [19]. The larvicidal and antioviposition effects of pulegone, thymol, and eugenol against Ae. aegypti were also described [20]. Zahran and Abdelgaleil evaluated twelve monoterpenes for larvicidal and adulticidal activities towards Cx. pipiens [5]. Knockdown and larvicidal activity of six monoterpenes were studied against Ae. aegypti and their structure-activity relationships were investigated [21]. Michaelakis et al. tested twenty acyclic monoterpenes with different functional groups as repellent and larvicidal agents against Cx. pipiens [22].

Therefore, the main goal of this study was to determine the efficiency of mixtures of some monoterpenes that have already toxic potential effect against mosquitoes. The study was conducted by two methods including residual and fumigant activity assays. The compounds were formulated in two types including impregnating them into paper discs and wax. The toxicity assessment was investigated as knockdown with calculation of the KT50 values and was discussed in detail.

2. Materials and Methods

2.1. Chemicals, Monoterpenes, and Essential Oil

Monoterpenes include (R)-camphor (98%), (L)-menthone (97%), (S)-fenchone (98%), (R)-carvone (98%), geraniol (98%), thymol (98%), (1R, 2S, 5R)-menthol (98%), (S)-limonene (96%), and camphene (95%) which were purchased from Sigma-Aldrich (St. Louis, MO, USA). Citronella oil was supplied from El Gomhoria Co. (Alexandria, Egypt). Chemical structures of these monoterpenes and citronella oil are shown in Figures 1 and 2, respectively. All other commercially available solvents and reagents were used without further purification.

Figure 1.

Figure 1

Chemical structures of pure tested monoterpenes.

Figure 2.

Figure 2

Constituents of citronella oil (R-(+)-citronellal as a main component and geraniol, citronellol, and geranyl acetate as minor ones).

2.2. Test Insect and Rearing

Third instar larvae of Cx. pipiens were obtained from Research Institute of Medical Entomology, Ministry of Health, Dokki, Giza, Egypt, and reared under laboratory conditions. About 400–600 larvae were transferred to white enameled and shallow trays about 30 cm in diameter containing 2-3 L of dechlorinated water. These trays were always covered with mesh screen to prevent oviposition by escaping adult mosquitoes and were maintained at a room temperature (26 ± 2°C) and RH (70 ± 5%) with a 14 : 10 (L : D) photo-period and water was replaced every two days. Larvae were daily fed on biscuits and yeast powder (3 : 1 ratio) until pupation. The pupae were transferred from the trays to plastic cups containing dechlorinated water into cages with netting cover wood frames (30 × 30 × 30 cm) until adults emerged. Adults were provided with 30% sucrose solution and females were fed on pigeon blood for four times a week [23]. The egg-rafts were placed in the white trays containing dechlorinated water for larval hatch.

2.3. Preparation of Ecofriendly Formulations

2.3.1. Formulation of Biologically Active Monoterpenes Impregnated in Paper Discs

The method used was according to Kawada and his coauthors [24, 25] with some modifications as follows: multilayer paper discs were prepared by sticking of six layers of filter paper (Whatman filter paper number 1) by glue material to form discs (2 × 2 cm, 1.08 mm average in thickness), and total surface area of the paper discs was 4 cm2. A weight of 100 mg of each monoterpene was dissolved in 10 mL acetone to obtain 10000 mg/L of each compound in final mixture solution. The paper discs (15 discs per replicate per each mixture) were dipped for one minute in this blend solution, then removed, and left to vaporize the acetone under ambient conditions. The discs were sealed in plastic bag (Figure 3). Seven formulations were prepared manually with average of 15 replicates for each formulation and then we calculated the loaded monoterpenes of each formulation according to the weight before each average of the discs. The formulated paper discs were used in bioassay to calculate the times required to knock down 50% of the female adults exposed (KT50). According to the class of monoterpenes, the paper discs divided into seven groups as PD1–PD7 (PD: paper discs) as follows:

  • immobilization of blend of ketone monoterpenes (camphor, menthone, carvone, and fenchone) on paper discs.

  • immobilization of blend of alcohol monoterpenes (geraniol, thymol, and menthol) on paper discs.

  • immobilization of blend of alkene monoterpenes (limonene and camphene) on paper discs.

  • PD1 + citronella oil on paper discs.

  • PD2 + citronella oil on paper discs.

  • PD3 + citronella oil on paper discs.

  • immobilization of citronella oil on paper discs.

Figure 3.

Figure 3

Schematic illustration of the preparation paper mosquito repellent incense.

2.3.2. Formulation of Biologically Active Monoterpenes Incorporated on Wax

The sustained release of biologically active monoterpenes from wax was evaluated. The method of preparation was as follows: raw wax (50 g) was weighted and melted at 120°C. Blend of different tested monoterpenes dissolved in acetone was mixed with the melted wax to obtain 1000 ppm of each compound in final formulation. The solution was then poured into alumina cups with fuse (Figure 4). According to the class of monoterpenes, these products divided into seven groups W1–W7 mentioned previously (W: wax):

  • immobilization of blend of ketone monoterpenes (camphor, menthone, carvone, and fenchone) on paper discs.

  • immobilization of blend of alcohol monoterpenes (geraniol, thymol, and menthol) on paper discs.

  • immobilization of blend of alkene monoterpenes (limonene and camphene) on paper discs.

  • PD1 + citronella oil on paper discs.

  • PD2 + citronella oil on paper discs.

  • PD3 + citronella oil on paper discs.

  • immobilization of citronella oil on paper discs.

After solidification, the formulated products were used in bioassay to calculate KT50 against adult mosquitoes.

Figure 4.

Figure 4

Schematic illustration of the preparation of monoterpenes incorporated into wax for mosquito control.

2.4. Adulticidal Bioassay Techniques

Susceptibility of Cx. pipiens female adult to different monoterpenes was assayed in two different formulations

2.4.1. Fumigant Assay of Monoterpenes Loaded on Paper Discs against Female Adults

The vapor action released from paper discs impregnated with biologically active monoterpenes was observed against adults of Cx. pipiens (Figure 5(a)). The paper disc was held on heater in the centre of the test chamber (70 × 40 × 38 cm). The paper discs were adapted to heat in the presence of 30 susceptible female adults. The number of knocked-down adults was counted at 5 min intervals along 60 minutes [25, 26]. Experiments were run in three replicates and the KT50 values were calculated according to the probit analysis [27].

Figure 5.

Figure 5

Fumigant assay of paper discs against mosquito adults (a) and knockdown assay of monoterpenes incorporated on wax (b).

2.4.2. Fumigant Bioassay of Monoterpenes Incorporated on Wax

Evaluation of the vapor action of monoterpenes loaded into wax was tested against female adults of Cx. pipiens as shown in Figure 5(b). In test chamber (70 × 40 × 38 cm), the monoterpene candle was placed in the centre of the chamber and illuminated it in the presence of 30 female adults. The number of knocked-down mosquitoes was counted at 5 min intervals for 60 minutes. Experiments were run in three replicates and the KT50 values were calculated according to the probit analysis [27].

2.4.3. Residual Activity of Monoterpenes against Female Adult of Cx. pipiens

The monoterpenes (camphor, menthol, and camphene) were selected from each tested group previously. Four concentrations (5, 10, 20, and 40 mg/cm2) of monoterpenes were prepared in acetone. Glass bottles 30 mL were coated with selected monoterpenes to form residual layer according to the Centre for Disease Control and Prevention (CDC) protocol [28]. The monoterpene left a sufficient period for the completion of drought. Twenty female adults were introduced into three glass bottles of 30 mL each, coated with monoterpenes. One control bottle of 30 mL was coated with acetone only. Deltamethrin at different concentrations (0.05, 0.1, 0.5, and 5 mg/cm2) was tested as a reference. The number of knocked-down mosquitoes was counted at 5 min intervals for 60 minutes. Experiments were run in three replicates. KT50 values were calculated by the probit method [27].

3. Results and Discussion

3.1. Formulation of Biologically Active Monoterpenes Impregnated in Paper Discs

In this study we prepared seven formulations of paper discs impregnated in different mixtures of monoterpenes and citronella oil. We divided the compounds according to their chemical groups to ketone, alcohol, and alkene monoterpenes groups avoiding any chemical reaction that may occur between them after loading into formulation. In addition, citronella oil was used as a reference because it is currently on the U.S. Environmental Protection Agency (EPA) list of minimum risk pesticides. Besides, it is considered one of the most essential oils extensively used in the markets as a repellent of mosquitoes. The properties of these paper discs are shown in Table 1. The concentration of the active ingredient (8.86%) in PD4 (camphor, menthone, carvone, fenchone, and citronella oil) formulation was the highest followed by PD5 (geraniol, thymol, menthol, and citronella oil) (8.51%). On the contrary, the concentration of the active ingredient in PD7 (citronella oil alone) formulation was the least (5.4%).

Table 1.

Properties of paper discs impregnated in mixtures of monoterpenes.

Formulation code Weight of disc before loading (mg) ± SD Weight of disc after loading (mg) ± SD Weight of pure loaded monoterpenes (mg) ± SD % of monoterpenes loaded on paper discs formulations ± SD
PD1 200.41a ± 7.60 214.27a ± 11.24 13.86a ± 5.61 6.380bc ± 2.320
PD2 143.33c ± 7.46 153.00d ± 07.19 09.66b ± 2.38 6.322bc ± 1.571
PD3 152.47c ± 5.36 161.20c ± 09.61 08.72c ± 5.66 5.264c ± 3.096
PD4 145.93c ± 7.71 160.33cd ± 09.20 14.39a ± 2.97 8.940a ± 1.540
PD5 146.40c ± 8.44 158.86cd ± 09.13 12.46ab ± 1.41 7.840ab ± 0.743
PD6 166.53b ± 21.42 178.33b ± 23.94 11.79ab ± 3.05 6.549bc ± 1.052
PD7 170.33b ± 17.73 179.53b ± 18.45 09.19b ± 1.15 5.132c ± 0.496

Values are average of 15 replicates.

Weight of pure loaded monoterpenes (mg) = weight after loading (mg) − weight before loading (mg).

%  of  monoterpenes  loaded  on  paper  discs  formulations = (Weight  of  pure  loaded  monoterpenes  (mg)/Weight  of  disc  after  loaded  (mg)) × 100.

PD1: immobilization of blend of ketone monoterpenes (camphor, menthone, carvone, and fenchone) on paper discs.

PD2: immobilization of blend of alcohol monoterpenes (geraniol, thymol, and menthol) on paper discs.

PD3: immobilization of blend of alkene monoterpenes (limonene and camphene) on paper discs.

PD4: PD1 + citronella oil on paper discs.

PD5: PD2 + citronella oil on paper discs.

PD6: PD3 + citronella oil on paper discs.

PD7: immobilization of citronella oil on paper discs.

3.2. Fumigant Assay of Monoterpenes Loaded on Paper Discs against Female Adults

Knockdown activity of a mixture of monoterpenes impregnated paper discs against the female adult of Cx. pipiens is shown in Table 2. The results showed that after 1 hr exposure period at paper discs impregnated with different monoterpenes, the mixture of ketone monoterpenes (PD1) recorded the highest median time (KT50) which was calculated as 17.2 min followed by mixture of ketone monoterpenes and citronella oil (PD4) which was calculated as 20.8 min. The mixture of alkene monoterpenes (PD3) recorded knockdown median time at 27.4 min, followed by the paper disc impregnated with citronella oil alone (PD7) at 28.7 min and the mixture of alkene monoterpenes with citronella oil together (PD6) at 33.2 min. The lowest median time recorded with paper discs impregnated with alcohol monoterpenes (PD2) was calculated as 35.9 min, followed by mixture of alcohol monoterpenes and citronella oil together (PD5) at 37.3 min. From these results the mixture of ketone monoterpenes showed the highest larvicidal effect, followed by alkene monoterpenes and then alcohol monoterpenes. The result showed that the knockdown time decreased with increased concentration in citronella oil. Mixing the citronella oil with any previous group decreased its adulticidal activity. The citronella oil alone showed medium effect. This result is in agreement with results obtained previously by Ramar and Paulraj who studied mosquito knockdown and adulticidal activities of essential oils by vaporizer, impregnated filter paper, and aerosol methods [29]. They proved that the citronella oil has adulticidal effect against Cx. quinquefasciatus and recorded KT50 of 11.4 min as determined by filter paper assay. In addition, Kawada et al. (2004) evaluated multilayer paper strip impregnated with metofluthrin against mosquitoes. They found that the use of metofluthrin reduced mosquito collection by > 80% during the 1st 4 weeks [24]. Fumigant bioassay of carvacrol, thymol, and l-perillaldehyde was conducted against Cx. pipiens [30]. They reported that carvacrol exhibited the highest fumigant activity followed by thymol and l-perillaldehyde, with LC50 values of 0.26, 0.28, and 0.34 mg/L air, respectively. In addition, Choi et al. determined the repellent activities of five monoterpenes to Cx. pipiens. They reported that terpinene had a potent repellent activity with a protection rate of 97% at a concentration of 0.05% topical treatment. Additionally, carvacrol and thymol showed an equivalent level of repellency. A spray-type solution containing 2% a-terpinene was tested for its repellent activity against Cx. pipiens. This solution showed stronger repellent activity than the currently used repellent, N,N-diethyl-z-methyl benzamide [31].

Table 2.

Knockdown time (KT50) of different monoterpenes loaded on paper discs against female adult Cx. pipiens.

Compound KT50 a (min)  95% confidence limits (min) Slopeb ±  SE Interceptc  ± SE (χ 2)d
Lower Upper
PD1 17.200 14.800 19.400 5.786 ± 0.334 −7.152 ± 0.447 46.12
PD2 35.900 34.300 37.400 7.635 ± 0.421 −11.871 ± 0.667 15.281
PD3 27.445 25.919 28.913 8.419 ± 0.470 −12.111 ± 0.694 20.666
PD4 20.799 19.224 22.287 7.35 ± 0.433 −9.688 ± 0.595 24.426
PD5 37.329 36.035 38.639 6.286 ± 0.356 −9.882 ± 0.566 7.304
PD6 33.205 31.399 34.991 6.054 ± 0.329 −9.210 ± 0.514 16.426
PD7 28.726 26.764 30.651 4.897 ± 0.260 −7.141 ± 0.396 17.673

aKnockdown times required to kill 50% of the population exposed.

bSlope of the regression line ± standard error (SE).

cIntercept of the regression line ± SE.

dChi square value.

PD: paper discs.

PD1: immobilization of blend of ketone monoterpenes (camphor, menthone, carvone, and fenchone) on paper discs.

PD2: immobilization of blend of alcohol monoterpenes (geraniol, thymol, and menthol) on paper discs.

PD3: immobilization of blend of alkene monoterpenes (limonene and camphene) on paper discs.

PD4: PD1 + citronella oil on paper discs.

PD5: PD2 + citronella oil on paper discs.

PD6: PD3 + citronella oil on paper discs.

PD7: immobilization of citronella oil on paper discs.

3.3. Fumigant Bioassay of Monoterpenes Incorporated on Wax

The results of the fumigant bioassay revealed that W1 showed the high knockdown effect (KT50 = 31.79) followed, in the descending order, by W2 (KT50 = 43.39) and then W7 (KT50 = 85.45). However, formulations of W3, W4, W5, and W6 showed neglected knockdown effect (KT50 > 120 min) (Table 3). These results proved that the ketone monoterpenes incorporated into wax gave the highest activity against mosquitoes. It can be noted that citronella oil decreased the activity of monoterpenes. This is due to the high density (d = 1.45 g/cm3) and less vapor pressure (VP) (VP = 0.15 mm Hg at 25°C) compared to the tested compounds (camphor, d = 0.992 g/cm3; VP = 4 mm, camphene, d = 0.842 g/cm3; VP = 2.4 mm, carvone, d = 0.96 g/cm3; VP = 0.4, fenchone, d = 0.948 g/cm3; VP = 0.16, menthone d = 0.895; VP = 0.5, geraniol, d = 0.889; VP = 0.2, limonene, d = 0.8411; VP = 5, menthol, d = 0.890; VP = 0.8, and thymol, d = 0.96; VP = 0.04).

Table 3.

Knockdown time (KT50) of different monoterpenes incorporated in wax against female adult Cx. pipiens.

Compound KT50 a(min)   95% confidence limits (min) Slopeb ± SE Interceptc ± SE (χ 2)d
Lower Upper
W1 31.79 28.225 36.099 1.421 ± 0.129 −2.134 ± 0.191 4.741
W2 43.391 40.135 47.429 2.481 ± 0.183 −4.063 ± 0.282 10.148
W3 >120
W4 >120
W5 >120
W6 >120
W7 85.446 71.269 111.004 1.863 ± 0.197 −3.599 ± 0.306 5.256

aKnockdown times required to kill 50% of the population exposed.

bSlope of the regression line ± standard error (SE).

cIntercept of the regression line ± SE.

dChi square value.

W: wax.

Revay and his coauthors evaluated the tabletop mosquito repellent with another six commercially spatial repellents or mosquito traps under field conditions. They proved that, under minimal air-movement, three spatial repellent based products (ThermaCELL® Patio Lantern, OFF® PowerPad lamp, and Terminix® AllClear tabletop mosquito repellent) significantly reduced the biting-pressure (t-test, P < 0.01) when positioned at short distances from a volunteer (3, 7.5, and 10 ft.) [32].

3.4. Residual Activity of Monoterpenes against Female Adult of Cx. pipiens

Three single monoterpenes from different groups (camphor, menthol, and camphene) were evaluated against the adults of Cx. pipiens as determined by residual assay at different concentrations (5, 10, 20, and 40 mg/cm2) for 1 h exposure period. The results proved that, at 5 mg/cm2, all tested monoterpenes showed knockdown effect after more than one hour (Table 4). Among the three monoterpenes, menthol was the highest compound which gave KT50 of 11.66, 3.73, and 2.57 min at 10, 20, and 40 mg/cm2, respectively. However, camphor and camphene showed significant knockdown effect at the highest concentration (40 mg/cm2) with KT50 of 25.49 and 49.84 min, respectively. Deltamethrin was tested as a reference mosquitocide (Table 4). It showed 19.48, 12.02, 5.54, and 1.94 min at tested concentrations of 0.05, 0.1, 0.5, and 5 mg/cm2, respectively. These results are in agreement with the results obtained previously by Zahran and Abdelgaleil [5] who studied insecticidal and developmental inhibitory properties of monoterpenes on Cx. pipiens. They reported that menthol has more adulticidal activity than camphor and camphene with mortality percentages of 63.3, 53.3, and 10%, respectively, at 24 h after exposure time. The evaluation demonstrated that the efficacy of the monoterpenes (5, 10, 20, and 40 mg/cm2) was comparable with that of deltamethrin (0.05, 0.1, 0.5, and 5 mg/cm2). It can be noted that deltamethrin is still the most active against adult compared to the tested monoterpenes. However, this product (synthetic pyrethroid) does not meet the environment requirement and safety. Although a hundred times higher dosage than deltamethrin is required for monoterpenes to achieve the same effect as deltamethrin, the results give an insight into the potential use of monoterpenes compounds as safe and effective household insecticides for mosquito control, for the insecticides derived from plant sources have a much lower level of risk to the environment than synthetic pesticides [33]. However, further study for selecting more effective monoterpenes and optimizing the formulations should be conducted to enhance the efficacy and extend the effective duration. These results are in agreement with [30] who reported that the efficacy of the binary mixture of carvacrol and thymol (300 mg/mat) was comparable with that of d-allethrin (30 mg/mat).

Table 4.

Knockdown time (KT50) of single monoterpenes at different concentrations (mg/cm2) against the female adult Cx. pipiens as determined by residual assay.

Compound Concentration (mg/cm2) KT50  95% confidence limits (min) Slop ± SE Intercept ± SE (χ 2)
Lower Upper
Camphor 5 >60
10 >60
20 >60
40 25.49 22.65 28.43 3.54 ± 0.198 −4.97 ± 0.296 28.67

Menthol 5 >60
10 11.66 8.59 14.55 4.05 ± 0.22 −4.32 ± 0.27 87.40
20 3.73 2.01 5.29 2.41 ± 0.23 −1.38 ± 0.25 23.43
40 2.57 1.38 3.46 3.37 ± 0.66 −1.38 ± 0.55 1.79

Camphene 5 >60
10 >60
20 >60
40 49.84 46.42 54.24 3.09 ± 0.23 −5.25 ± 0.37 9.76

Deltamethrin 0.05 19.48 16.86 21.87 4.42 ± 0.23 −5.70 ± 0.33 36.89
0.1 12.02 10.11 13.81 3.78 ± 0.20 −4.08 ± 0.26 30.58
0.5 5.54 5.01 6.03 5.53 ± 0.59 −4.11 ± 0.50 1.74
5 1.94 0.59 2.98 3.08 ± 0.78 −0.89 ± 0.64 1.98

4. Conclusion

The current study proved that the use of paper discs was better than the wax to formulate the monoterpene and produce ecofriendly formulations in the controlling of Cx. pipiens. Single or mixed monoterpenes showed high activity against Cx. pipiens adult. Activity of monoterpenes differed depending on the method of application. The selection of natural products reduces the environmental harmful impacts of pesticides and the phenomenon of resistance in adult mosquitoes. Finally such products can be used as ecofriendly alternative to chemical insecticides in vector-borne diseases control program.

Competing Interests

The authors declare no competing interests.

References

  • 1.Barbosa S., Black W. C., IV, Hastings I. Challenges in estimating insecticide selection pressures from mosquito field data. PLoS Neglected Tropical Diseases. 2011;5(11) doi: 10.1371/journal.pntd.0001387.e1387 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Jang Y.-S., Kim M.-K., Ahn Y.-J., Lee H.-S. Larvicidal activity of Brazilian plants against Aedes aegypti and Culex pipiens pallens (Diptera: Culicidae) Agricultural Chemistry and Biotechnology. 2002;45(3):131–134. [Google Scholar]
  • 3.Peng Z., Beckett A. N., Engler R. J., Hoffman D. R., Ott N. L., Simons F. E. R. Immune responses to mosquito saliva in 14 individuals with acute systemic allergic reactions to mosquito bites. Journal of Allergy and Clinical Immunology. 2004;114(5):1189–1194. doi: 10.1016/j.jaci.2004.08.014. [DOI] [PubMed] [Google Scholar]
  • 4.Kady G. A. E. L., Kamel N. H., Mosleh Y. Y., Bahght I. M. Comparative toxicity of two bio-insecticides (Spinotoram and Vertemic) compared with methomyl against Culex pipiens and Anopheles multicolor . World Journal of Agricultural Sciences. 2008;4(2):198–205. [Google Scholar]
  • 5.Zahran H. E.-D. M., Abdelgaleil S. A. M. Insecticidal and developmental inhibitory properties of monoterpenes on Culex pipiens L. (Diptera: Culicidae) Journal of Asia-Pacific Entomology. 2011;14(1):46–51. doi: 10.1016/j.aspen.2010.11.013. [DOI] [Google Scholar]
  • 6.Yadav S. Dose optimization of thermal fogging trials for household insecticide formulation (EC) against Aedes aegypti (L.) Current Biotica. 2012;6(1):71–79. [Google Scholar]
  • 7.Hoogstraal H., Meegan J. M., Khalil G. M., Adham F. K. The Rift Valley fever epizootic in Egypt 1977–1978 2. Ecological and entomological studies. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1979;73(6):624–629. doi: 10.1016/0035-9203(79)90005-1. [DOI] [PubMed] [Google Scholar]
  • 8.Harb M., Faris R., Gad A. M., Hafez O. N., Ramzy R., Buck A. A. The resurgence of lymphatic filariasis in the Nile delta. Bulletin of the World Health Organization. 1993;71(1):49–54. [PMC free article] [PubMed] [Google Scholar]
  • 9.Chavasse D. C., Yap H. H. Chemical Methods for the Control of Vectors and Pests of Public Health Importance. Geneva, Switzerland: World Health Organization; 1997. [Google Scholar]
  • 10.Rozendaal J. A. Vector Control: Methods for Use by Individuals and Communities. Geneva‎, Switzerland: World Health Organization; 1997. [Google Scholar]
  • 11.Joseph C. C., Ndoile M. M., Malima R. C., Nkunya M. H. H. Larvicidal and mosquitocidal extracts, a coumarin, isoflavonoids and pterocarpans from Neorautanenia mitis. Transactions of the Royal Society of Tropical Medicine and Hygiene. 2004;98(8):451–455. doi: 10.1016/j.trstmh.2003.10.008. [DOI] [PubMed] [Google Scholar]
  • 12.Yang P., Ma Y., Zheng S. Adulticidal activity of five essential oils against Culex pipiens quinquefasciatus . Journal of Pesticide Science. 2005;30(2):84–89. doi: 10.1584/jpestics.30.84. [DOI] [Google Scholar]
  • 13.Abdel-Hamid Y. M., Soliman M. I., Allam K. M. Spatial distribution and abundance of culicine mosquitoes in relation to the risk of filariasis transmission in El Sharqiya Governorate, Egypt. Egyptian Academic Journal of Biological Sciences. 2009;1:39–48. [Google Scholar]
  • 14.Mayeku W. P., Omollo N. I., Odalo O. J., Hassanali A. Chemical composition and mosquito repellency of essential oil of Conyza newii propagated in different geographical locations of Kenya. Medical and Veterinary Entomology. 2014;28(3):253–256. doi: 10.1111/mve.12039. [DOI] [PubMed] [Google Scholar]
  • 15.Runyoro D. K. B., Ngassapa O., Kachali L., Obare V., Lyamuya E. F. Biological activities of essential oils from plants growing in Tanzania. East and Central African Journal of Pharmaceutical Sciences. 2014;13(3):85–91. [Google Scholar]
  • 16.Ali A., Tabanca N., Demirci B., et al. Chemical composition and biological activity of four salvia essential oils and individual compounds against two species of mosquitoes. Journal of Agricultural and Food Chemistry. 2015;63(2):447–456. doi: 10.1021/jf504976f. [DOI] [PubMed] [Google Scholar]
  • 17.Pavela R. Essential oils for the development of eco-friendly mosquito larvicides: a review. Industrial Crops and Products. 2015;76:174–187. doi: 10.1016/j.indcrop.2015.06.050. [DOI] [Google Scholar]
  • 18.Tabanca N., Demirci B., Ali A., Ali Z., Blythe E. K., Khan I. A. Essential oils of green and red Perilla frutescens as potential sources of compounds for mosquito management. Industrial Crops and Products. 2015;65:36–44. doi: 10.1016/j.indcrop.2014.11.043. [DOI] [Google Scholar]
  • 19.Radwan M. A., El-Zemity S. R., Mohamed S. A., Sherby S. M. Larvicidal activity of some essential oils, monoterpenoids and their corresponding N-methyl carbamate derivatives against Culex pipiens (Diptera: Culicidae) International Journal of Tropical Insect Science. 2008;28(2):61–68. doi: 10.1017/s1742758408962366. [DOI] [Google Scholar]
  • 20.Waliwitiya R., Kennedy C. J., Lowenberger C. A. Larvicidal and oviposition-altering activity of monoterpenoids, trans-anethole and rosemary oil to the yellow fever mosquito Aedes aegypti (Diptera: Culicidae) Pest Management Science. 2009;65(3):241–248. doi: 10.1002/ps.1675. [DOI] [PubMed] [Google Scholar]
  • 21.Lucia A., Zerba E., Masuh H. Knockdown and larvicidal activity of six monoterpenes against Aedes aegypti (Diptera: Culicidae) and their structure-activity relationships. Parasitology Research. 2013;112(12):4267–4272. doi: 10.1007/s00436-013-3618-6. [DOI] [PubMed] [Google Scholar]
  • 22.Michaelakis A., Vidali V. P., Papachristos D. P., et al. Bioefficacy of acyclic monoterpenes and their saturated derivatives against the West Nile vector Culex pipiens . Chemosphere. 2014;96:74–80. doi: 10.1016/j.chemosphere.2013.07.032. [DOI] [PubMed] [Google Scholar]
  • 23.El-Bokl M. M., Moawad H. M. Evaluation of some plant extracts as mosquito larvicides. Ain Shams Science Bulletin. 1996;34:351–362. [Google Scholar]
  • 24.Kawada H., Maekawa Y., Takagi M. Laboratory and field evaluation of spatial repellency with metofluthrin impregnated paper strip against mosquitoes in Lombok Island, Indonesia. Journal of the American Mosquito Control Association. 2004;20(3):292–298. [PubMed] [Google Scholar]
  • 25.Ujihara K., Mori T., Iwasaki T., Sugano M., Shono Y., Matsuo N. Metofluthrin: a potent new synthetic pyrethroid with high vapor activity against mosquitoes. Bioscience, Biotechnology and Biochemistry. 2004;68(1):170–174. doi: 10.1271/bbb.68.170. [DOI] [PubMed] [Google Scholar]
  • 26.Yamaguchi T., Shinjo G., Tsuda S., Yoshida K., Inaba E., Okuno Y. Insecticidal activity of a new synthetic pyrethroid. Japanese Journal of Sanitary Zoology. 1981;32:59–66. [Google Scholar]
  • 27.Finney D. J. Probit Analysis. 3rd. Cambridge University Press; 1971. [Google Scholar]
  • 28.Brogdon W., Chan A. Guidelines for evaluating insecticide resistance in vectors using the CDC bottle bioassay/methods in Anopheles research. CDC Atlanta USA: CDC Technical Report. 2010
  • 29.Ramar M., Paulraj S. I. M. G. Mosquito knock-down and adulticidal activities of essential oils by vaporizer, impregnated filter paper and aerosol methods. International Journal of Mosquito Research. 2014;3(1):26–32. [Google Scholar]
  • 30.Ma W.-B., Feng J.-T., Jiang Z.-L., Wu H., Ma Z.-Q., Zhang X. Fumigant activity of eleven essential oil compounds and their selected binary mixtures against Culex pipiens pallens (Diptera: Culicidae) Parasitology Research. 2014;113(10):3631–3637. doi: 10.1007/s00436-014-4028-0. [DOI] [PubMed] [Google Scholar]
  • 31.Choi W.-S., Park B.-S., Ku S.-K., Lee S.-E. Repellent activities of essential oils and monoterpenes against Culex pipiens pallens. Journal of the American Mosquito Control Association. 2002;18(4):348–351. [PubMed] [Google Scholar]
  • 32.Revay E. E., Kline D. L., Xue R.-D., et al. Reduction of mosquito biting-pressure: spatial repellents or mosquito traps? A field comparison of seven commercially available products in Israel. Acta Tropica. 2013;127(1):63–68. doi: 10.1016/j.actatropica.2013.03.011. [DOI] [PubMed] [Google Scholar]
  • 33.Govindarajan M., Sivakumar R., Rajeswary M., Veerakumar K. Mosquito larvicidal activity of thymol from essential oil of Coleus aromaticus Benth. against Culex tritaeniorhynchus, Aedes albopictus, and Anopheles subpictus (Diptera: Culicidae) Parasitology Research. 2013;112(11):3713–3721. doi: 10.1007/s00436-013-3557-2. [DOI] [PubMed] [Google Scholar]

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