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Repelling properties of some plant materials on the tick Ixodes ricinus L.

Abstract

The repellent effects on nymphal stages of Ixodes ricinus L. of some plant materials have been studied in the laboratory. The plant material consisted of an ethanolic extract from Achillea millefolium L., and volatile oils of birch and/or pine tar, citronella, cloves, eucalyptus, geranium, lavender, lily of the valley and peppermint. The most pronounced effects were observed for the oils of citronella, cloves and lily of the valley. They possessed repelling activities of the same magnitude as the reference repellent DEET (N,N-diethyl-m-toluamide). Some major constituents of these oils, e.g. citronellol and geraniol (oil of citronella and lily of the valley) and eugenol (oil of cloves) showed pronounced repelling effects. This was also the case for phenethyl alcohol, a minor component in the oil from lily of the valley.

[c] 2005 Elsevier GmbH. All rights reserved.

Keywords: Achillea millefolium; Citronella; Clove; Eucalyptus; Geranium; Lavender; Lily of the valley; Peppermint; Ixodes ricinus; Tick repellents

Introduction

Worldwide, about 800 species of ticks are known and some can carry disease-causing agents, e.g. bacteria, vira or other organisms giving rise to health problems. Control of ticks is thus of importance. In an integrated tick control programme covering different methods repellents may be of value. Most tick repellents are intended for application on skin and/or clothing. However, some are supposed to give protection even after oral use, e.g. garlic (Stjernberg and Berglund, 2000).

There are only a few reports published covering plant materials with repelling effects on the tick Ixodes ricinus, i.e. powdered rhizomes of Acorus calamus (Mironov, 1943); a mixture of garlic and lemon peel (Catar, 1954), kyuzol (mainly consisting of 1-acetyl-1,2,3,4-tetrahydroquinoline) (Zolotarev, 1959); volatiles from Clausena anisata, Viola and jasmine (Novak, 1973); and (-)-myrtenal, a weaker repellent than DEET (Dautel et al., 1999). Due to the limited number of reports of the repelling effect of plant materials on the disease transferring tick, Ixodes ricinus, the following study was performed. The intention was, if possible, to find single repelling components that are also harmless to the user. The plant materials chosen have already been studied for the repelling effect on several Aedes species (Thorsell et al., 1998).

Experimental

Plant material

Yarrow (Achillea millefolium)--an ethanolic extract was prepared as described earlier (Tunon et al., 1994) and a 10 per cent ethanolic solution (w/w) was used in the tick tests.

The following volatile oils were also used as 10 per cent (w/w) ethanolic solutions/suspensions in the biological tests: birch/pine tar oil (Apoteket AB, Arjeplog), citronella oil (BPC), clove, eucalyptus, geranium, lavender, lily of the valley and peppermint oils (Stockholms Aether & Essence fabrik). Available components of the oils were of highest purity and used as 10 per cent (w/w) solutions/suspensions in ethanol in the tests.

Ten per cent (w/w) ethanolic solution of N,N-diethyl-m-toluamide (DEET) (Merck Co, 98 per cent) served as reference compound.

Tick tests

Nymphal stages of the tick Ixodes ricinus were collected in the archipelago of Stockholm. They were kept in small net cages supported with wet filter papers and grass at a temperature of about +22[degrees]C.

The test procedure was the following: Petri dishes with an inner diameter of 9.5 cm were provided with 3 pieces of filter paper (Munktell No. 3, 9 cm). The test solutions, 0.5 ml, were applied along the periphery of the papers. After air-drying, 6 nymphs were placed in the centre of the papers and their behaviour with regard to avoiding the treated area was observed. After the test, which usually lasted for about 5 min, the nymphs were replaced in the net cages. The petri dishes were uncovered and exposed to open air. The procedure with the nymphs was repeated after 0, 4, 6 and 8 h. At each occasion the number of nymphs avoiding the treated area was estimated. The repellency was expressed as number of avoiding nymphs in relation to the total number of nymphs at each occasion. Thus 6 nymphs avoiding out of a total number of 6 is recorded as 100 per cent repellency. The tests were performed mainly in duplicate. Controls with only ethanol were always used. The range was about [+ or -]17 per cent.

Chemical analysis

The plant material was analyzed by thin layer chromatography (TLC) and gas chromatography combined with mass spectrometry (GC/MS) as described earlier (Thorsell et al., 1998).

Results

All the tested plant materials, except Achillea millefolium, showed some repellency initially. However, for some of the essential oils the duration was short and the effect was lost within 4 h. Table 1 shows the results during the course of 8 h as well as some toxicity data as described in the literature (Lewis, 1996). The table shows that the most long-lasting repellent effect was exerted by citronella, clove and lily of the valley oils. However, some of these oils have to some extent shown toxic properties for humans and other animals. Similar unfavourable effects have also been found for the reference compound DEET.

According to the literature citronella, clove and lily of the valley oils contain a great amount of constituents. Data of the repellent activity and some toxicity data can be found in the literature (Thorsell et al., 1998, Lewis, 1996).

Discussion

This study shows that amongst the tested plant materials the strongest repelling effect against nymphs of Ixodes ricinus was exerted by the oils of citronella, cloves and lily of the valley. Their efficacy was of the same magnitude as the pure reference compound DEET. Some of the main constituents of these essential oils were active up to 8 h. This was the case for some compounds of the citronella oil, e.g. citronellol and geraniol. Also eugenol, but not [beta]-caryophyllene, the main components of clove oil, gave a lasting effect, as was the case for the mentioned citronellol, one of the main constituents of essential oil from lily of the valley. Additional minor components of this oil like phenethyl alcohol and geraniol might have contributed to its total tick repelling activity. It is also possible that several components of the oils act synergistically. Hydroxycitronellal, the most abundant compound in the oil of lily of the valley (49.5 per cent), showed only a weak activity and just for a short duration.

Problems with essential oils and their components intended for application on humans and larger animals are their toxic properties. According to toxicity data from the literature the essential oils from citronella and cloves seem to be unacceptable for cutaneous application (Lewis, 1996). This might also be the case for the essential oil from lily of the valley since it also contains compounds, e.g. citronellol, claimed to be toxic to the skin (Lewis, 1996). Synergistic toxic effects may also be considered.

One possibility to avoid synergistic, additional or antagonistic effects of repellents is to use monopreparations containing a single component with well-known repelling and toxic properties. An example of this was geraniol. However, geraniol is mentioned in connection with both cytotoxic (Nachev et al., 1968) and teratogenic effects (Abramovici and Rachmuth-Roizman, 1983). Maybe geraniol as well as citronellol, eugenol and phenethyl alcohol might be of interest as lead compounds in the future search for effective tick repellents harmless for the users. Many other aspects on tick repellents are of importance, e.g. distance and long-lasting effect, if possible against many arthropods, and not causing adaptation or resistance. It should also be almost without smell or colour and having a good consistency and not affecting clothes or other materials.

Acknowledgements

Thanks are due to Prof. Tommy Radesater, docent Goran Malmberg, Dr. Marianne Malmberg, Mrs. Hillevi Isaksson and Mrs. Ingrid Malander, University of Stockholm, for their support making the studies possible.

References

Abramovici, A., Rachmuth-Roizman, P., 1983. Molecular structure-teratogenicity relationships of some fragrance additives. Toxicology 29, 143-156.

Catar, G., 1954. Effect of plant extract on Ixodes ricinus. Bratislava Lekarske Listy.

Dautel, H., Kahl, O., Siems, K., Oppenrieder, M., Muller-Kuhrt, L., Hilker, M., 1999. A novel test system for detection of tick repellents. Entomol. Exp. Appl. 91, 431-441.

Lewis Sr., R.J., 1996. Sax's Dangerous Properties of Industrial Materials, 9th ed. van Nostrand Reinhold, New York.

Mironov, V.S., 1943. Acorus calamus used as an insecticidal and repellent preparation. Rev. Appl. Entomol. 31B, 127-128.

Nachev, C., Zolotovichm, G., Silyanovska, K., Stoichev, S., 1968. Cytotoxic effect of some essential oils and some of their components. Parfuemerie Kosmetik 49, 104-108.

Novak, D., 1973. Preliminary laboratory tests with tick repellents. Proc. Int. Congr. Acarol. 3rd, 685-686.

Stjernberg, L., Berglund, J., 2000. Garlic as an insect repellent. J. Am. Med. Assoc. 284, 831.

Thorsell, W., Mikiver, A., Malander, I., Tunon, H., 1998. Efficacy of plant extracts and oils as mosquito repellents. Phytomedicine 5, 311-323.

Tunon, H., Thorsell, W., Bohlin, L., 1994. Mosquito repelling activity of compounds occurring in Achillea millefolium (L.). (Asteraceae). Econ. Bot. 48, 111-120.

Zolotarev, E.Kh., 1959. Individual protection from the attack of vermin and ticks. Invest. Sibir. Otdel. Akad. Nauk. S.S.S.R. (9), 92-97.

W. Thorsell (a), A. Mikiver (a), H. Tunon (b,*)

(a) University of Stockholm, Department of Zoology, Stockholm, Sweden

(b) Swedish Biodiversity Centre, Uppsala, Sweden

Received 27 November 2003; accepted 22 April 2004

*Corresponding author. Tel.: + 46 18 672591; fax: + 46 18 673537.

E-mail address: hakan.tunon@cbm.slu.se (H. Tunon).
Table 1. Tick repelling activity of some natural products compared with
the insect repellent DEET

 Tick repellency
 (per cent) after Toxicity according to the
Product 4 h 6 h 8 h literature (Lewis, 1996)

Achillea 0 -- --
millefolium
Oil of birch and/or 67 17 -- Moderate irritant for eyes and
pine tar mucous membranes, allergen,
 skin irritant
Oil of citronella 89 90 83 Mutation data reported, eye
 irritant
Oil of cloves 68 82 78 Mildly toxic by skin contact,
 mutation data reported
Oil of eucalyptus 0 -- -- Skin irritant
Oil of geranium 0 -- -- Skin irritant
Oil of lavender 0 -- -- Skin irritant
Oil of lily of the 67 67 67 --
valley
Oil of peppermint 50 10 -- Allergen, mutation data
 reported
DEET 76 71 71 Skin and eye irritating,
 mutation data reported,
 reproduction disturbances in
 experiments, can cause
 CNS-disturbances
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Title Annotation:SHORT COMMUNICATION
Author:Thorsell, W.; Mikiver, A.; Tunon, H.
Publication:Phytomedicine: International Journal of Phytotherapy & Phytopharmacology
Geographic Code:4EUSW
Date:Jan 1, 2006
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