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Journal of Food Protection, Vol. 58, No.5, Pages 560-563 Copyrighl©, International Association of Milk, Food and Environmental Sanitarians

Acaricidal Activity of Some Essential Oils and Their Constituents against Tyrophagus longior, a Mite of Stored Food

STEF ANIA PERRUCCI*

Dipartimento di Patologia Animale Profilassied Igiene degli Alimenti, Viale delle Piagge 2, Pisa, Italy 56/24 Downloaded from http://meridian.allenpress.com/jfp/article-pdf/58/5/560/1665363/0362-028x-58_5_560.pdf by guest on 24 September 2021

(MS# 94-226: Received 23 September 1994/Accepted 5 January 1995)

ABSTRACT In addition, the presence of a large number of these pests in stored food can cause gastroenteric problems in Essential oils of four plants (two species of lavender, pepper- animals and humans ingesting them. Some authors report mint, and a ) and some of their principal constituents, that biscuits and meal infested by Tyrophagus putrescentiae i.e., linalool, linalyl acetate, fenchone, menthone, , and have caused diarrhea in dogs (6); moreover, other , were tested in vitro for their acaricidal activity against Tyrophagus longior, a mite species that is a pest in stored food. Tyrophagus species have caused gastrointestinal disorders Two different procedures were carried out to test the activity of in consumers of stored cheeses (5, 24). Storage mites are these compounds by direct contact and by inhalation. In the direct also frequently reported as being the etiological agents of contact assays five different quantities of each undiluted substance several allergic diseases in subjects coming into contact (6, 2, I, 0.5, and 0.25 J.ll) were spread on the internal surface of with them. Czernecki and Kraus (2) speak about an out- 6-cm petri dishes, each containing 10 mites. The activity by break of allergic dermatitis in a butcher's family caused by inhalation was tested using two petri dishes of different sizes: the Tyrophagus dimidatus, while T. longior was recorded by smaller one (6 cm), containing 10 mites, was covered with a filter- Rimbaud (21) as the cause of a severe canine dermatitis paper disk and enclosed in a bigger dish (9 cm) containing 6 oz with pruritus and alopecia. Allergic rhinitis and asthma 2 J.ll of each undiluted substance. At the highest doses, the essential oils of the two lavender species and of peppermint killed caused by storage mites are frequently reported worldwide 100% of the mites, both by direct contact and by inhalation. in farming communities and among cheese workers and Eucalyptus oil was the least active. Among the essential oil children (4,9,10,11,20,29). constituents, menthol showed the highest activity, killing 100% of These are some of the reasons why we need a means the mites at the lowest dose (0.25 J.ll) by direct contact and at 6 to control mites infestation of stored food. In addition, the J.ll by inhalation. However, Iinalool, fenchone, and menthone also development of drug resistance reported by some authors showed good acaricidal activity. Eucalyptol, like the essential oil (27,31) for T. longior and other Tyrophagus species justi- of which it is the principal constituent, had the lowest activity. fies the search for new effective acaricidal compounds. This study, part of more extensive research on the Key words: Essential oils, , Tyrophagus longior, acaricidal activity employment of new natural compounds to control arthropods, evaluates the acaricidal activity on T. longior of The high frequency of drug resistance of arthropods to the essential oils of two species of lavender ( pesticides and the problems of environmental safety due to angustifolia Miller and Lavandula stoechas L.), peppermint the persistence of these drugs and to their widespread use ( x piperita L.), and a eucalyptus (Eucaliptus globulus in the agricultural and zootechnical fields (12,21,22,25) Labill.), and of some terpenes (linalool, linalyl acetate, illustrate why alternative means to fight dangerous acari menthone, menthol, and eucalyptol), which are their princi- and insects are needed. pal constituents (19). The killing activity of essential oils In this preliminary study we evaluated in vitro the acari- and their constituents on several arthropod species has cidal activity of some natural compounds against T. longior previously been reported; among them spearmint oil, (Gervais, 1844), an acarid species commonly found on menthone, and linalool were found to kill Dermatophagoides stored food (7,23). pteronyssinus, Dermatophagoides farinae, and T. putre- Among the mites that infest stored food, there are scentiae, mites closely related to T. longior (13). Hink and several species belonging to the genus Tyrophagus. These Duffy (8) found that linalool is an against ticks mites normally live on the external surface of seasoned and fleas. In some previous studies we have demonstrated hams, sausages, and cheeses, but sometimes they get into the acaricidal activity of the essential oil of L. angustifolia these products, causing the commercial exclusion of stored and of linalool against Psoroptes cuniculi, both by direct products (3,24,30). contact (17) and by inhalation (18).

JOURNAL OF FOOD PROTECT/ON, VOL 58, MAY 1995 MATERIALS AND METIIODS Acaricidal activity by inhalation Mites (lO/plate) were placed in 6-cm petri dishes covered Essential oils with filter paper disks that allowed gas exchange; each plate so Flowering tops of Mentha x piperita (peppermint) plant prepared was inserted in a 9-cm petri dish containing the tested materials, harvested from a cultivated area located at substance and closed with the usual cover. After 24 h all immobile Sansepolcro (Ditta Aboca, Arezzo, Italy), were dried and mites were transferred to a sterile 6-cm petri dish. Each pure processed by hydrodistillation, using an apparatus (a Clevenger-like substance was used at 6 and 2 Ill; only menthol was dissolved device) according to Italian and European pharmacopoeia methods (20%) in vaseline oil. (Farmacopea Ufticiale, 1985), in order to extract its essential oil. The temperature, relative humidity, controls, and evaluation The essential oils of the two lavender species ( of the acaricidal activity were the same as above. Each test was Miller and Lavandula stoechas L.) and of the eucalyptus (Eucaliptus repeated six times. The results are reported as the mean percent- globulus Labill.) were commercial samples (Ditta Primavera, Pisa). age of the mortality plus or minus the standard deviation of the six All the essential oils were analyzed using a Perkin-Elmer replicates. 8420 gas chromatograph equipped with a DB-Wax capillary column (30 m by 0.25 mm). The oven temperature was RESULTS AND DISCUSSION programmed as follows: first isotherm 60°C for 10 min, then

up to 220°C at 5°C/min, and finally isotherm 220°C for 10 Table I shows the chemical composition of the oils Downloaded from http://meridian.allenpress.com/jfp/article-pdf/58/5/560/1665363/0362-028x-58_5_560.pdf by guest on 24 September 2021 min. The temperatures of the injector and detector were tested, analyzed by gas chromatography. 250°C. The carrier gas was nitrogen at 2 ml/min flow. The On the basis of the length of the body, the morphology detector was a flame ionization detector. The essential oil was of the fourth tarsus, and the male genital opening, the mites dissolved (I %) in diethyl ether (Et,O) and I III of this isolated from the ham were identified as belonging to the solution was injected using the split -technique (26). Peaks species Tyrophagus longior (Gervais, 1844). This acarid were identified by comparing the ,retention times to those of authentic samples, by means of their relative retention times species has been frequently isolated from ham, numerous with respect to two internal standards (cellosolve acetate and kinds of cheeses, and other foodstuffs (7, 23). butyl cellosolve), and by means of the reliability factors Table 2 shows the acaricidal activity by direct contact method (16). and by inhalation found for each essential oil and each constituent. The percentage of mortality of the control Constituents of essential oils mites was always very low in all the tests (6.7 to 10%). The main constituents of the essential oils tested were L angustifolia, L stoechas, and Mentha x piperita essential respectively linalool and linalyl acetate for the L. angustifolia oils, tested for their activity by direct contact, were able to oil, fenchone for the L. stoechas oil, menthone and menthol for the Mentha x piperita oil, and I, 8-cineole (eucalyptol) for E. globulus oil. They were all purchased from Aldrich (Sigma- TABLE I. Chemical composition of the essential oils (%). Aldrich Szl via Gallarate 154,20151 Milano, Italy). Principal Lavandula Mentha Lavandula Eucalyptus Mites components angustifolia piperita stoechas globulus Mites isolated from samples of seasoned Parma ham were microscopically identified using the keys and descrip- a- 0.14 0.44 3.68 6.60 tions of Robertson (23). At least 20 pairs of adult male and Camphene 0.10 0.91 female mites were confined in individual 9-cm petri dishes ~-Pinene 0.11 0.61 0.11 0.30 containing two slices (2 by 2 by 2 cm) of uninfested Parma ham. All 0.64 tr 0.25 0.33 plates were placed in a controlled chamber (A. Gallenkarnp & Co., 0.20 0.60 2.35 5.73 Ltd., London) at 25°C and 70% relative humidity. In this way it was Eucalyptol 1.06 4.00 3.58 76.00 possible to obtain an in vitro culture (27). y-Terpinene tt' 0.15 0.78 The adult stages of the mites could be recognized and p-Cymene 9.05 0.51 1.02 selected from the culture by the presence of four pairs of legs, Fenchone 47.23 a stronger color, and a greater length. Menthone Menthofuran Acaricidal activity by direct contact Isomenthone Each substance was placed in a 6-cm petri dish and uni- formly dispensed over the plate surface using a flow of com- Linalool 0.18 pressed air (14, 15, 31). Then 10 mites were placed inside the Linalyl acetate dish. All plates were placed in a controlled chamber at 25°C and Terpinen-4-o1 70% relative humidity. All the motionless mites observed by Lavandulyl acetate stereoscopic microscope after a period of 24 h were transferred Bornil acetato into fresh petri dishes and observed 24 hours later. If still immo- ~-cariophylene 0.42 bilized, mites were stimulated with a needle; lack of any reaction Menthol and the persistence of immobility was taken to indicate death (28). For each pure substance the acaricidal activity of scalar doses (6, Lavandulol 2, I, 0.5, and 0.25 Ill) measured with a Gilson P2 microtiter Borneol 1.05 pipette was investigated. Only menthol, being solid, was dissolved a-Terpineol 3.05 (20%) in vaseline oil. Mites placed in plates containing vaseline Neryl acetate oil (2 ml/plate) and mites placed in empty plates were used as Geranyl acetate controls. At the same time, six replications of each dose were made for each compound. 'tr = traces « 0.1%).

JOURNAL OF FOOD PROTECTION, VOL. 58, MAY 1995 562 PERRUCCI

TABLE 2. Acaricidal activity (percentage lethality) by direct contact and by inhalation of the tested substances at several doses against Tyrophagus longior; mean (± SD) of six replicates.

Tested Substances Direct Contact Inhalation

6.00J.ll 2.00 I.d 1.00 J.lI 0.501·d 0.25 J.lI 6.00 I.d 2.00 J.lI

Essential oils Lavandula stoechas 100.0 (0.0) 100.0 (0.0) 100.0 (0.0) 98.3 (4.1) 85.0 (36.7) 100.0 (0.0) 33.3 (27.3) Lavandula angustifolia 100.0 (0.0) 100.0 (0.0) 100.0 (0.0) 93.3 (10.3) 88.3 (24.0) 86.7 (10.3) 56.7 (48.0) Eucalyptus globulus 91.7 (13.3) 90.0 (11.0) 85.0 (25.1) 80.0 (24.5) 53.3 (17.5) 76.7 (25.8) 33.3 (10.3) Mentha x piperita 100.0 (0.0) 100.0 (0.0) 100.0 (0.0) 93.3 (5.2) 78.3 (26.4) 100.0 (0.0) 96.7 (8.2)

Constituents Linalool 100.0 (0,0) 100.0 (0.0) 98.3 (4.1) 98.3 (4.1) 88.3 (24.0) 100.0 (0.0) 67.6 (33.2) Linalyl acetate 100.0 (0.0) 96.7 (5.2) 93.3 (12.1) 91.7 (16.0) 50.0 (54.8) 6.7 (10.3) Fenchone 100.0 (0.0) 100.0 (0.0) 100.0 (0.0) 89.2 (17.4) 60.0 (31.0) 100.0 (0.0) 60.0 (17"9) Menthone 100.0 (0.0) 100.0 (0.0) 100.0 (0.0) 100.0 (0.0) 63.3 (42.7) 90.0 (16.7) 60.0 (45.6) Downloaded from http://meridian.allenpress.com/jfp/article-pdf/58/5/560/1665363/0362-028x-58_5_560.pdf by guest on 24 September 2021 Eucalyptol 81.7 (24.8) 71.7 (17.2) 46.7 (41.8) 28.3 (37. 10) 10.0 (11.0) 50.0 (54.8) Menthol" 100.0 (0.0) 100.0 (0.0) 100.0 (0.0) 100.0 (0.0) 100.0 (0.0) 100.0 (0.0) 66.7 (37.2)

" Diluted (20%) in vaseline oil. kill 100% of the mites at I to 6 IJI/plate. At the lowest dose having both acaricidal and flavoring properties could be (0.25 IJI) the essence of L. angustifolia still showed good added to the sausages to control mite infestation without activity (88.3% mortality). altering the organoleptic character of these products. By inhalation, L. stoechas and Mentha x piperita es- More studies are needed to confirm the miticidal activ- sential oils killed all the mites at a dose of 6 IJI; the latter ity of these natural compounds directly on food products, essence was very efficacious also at 2 IJI. E. globulus but their present use to control dust mites, ticks, and fleas essential oil was the least active both by direct contact and (1,8,13) give us good expectations of applying these sub- by inhalation. stances with favorable results. Among the essential oil constituents tested in the assay by direct contact, linalool, linalyl acetate, fenchone, ACKNOWLEDGMENTS menthone, and menthol had great effectiveness down to a dose of 0.5 fJI; menthol killed 100% of the mites also at I am grateful to Professor Cioni PierLuigi and to Flamini Guido of the Dipartimento di Chimica Biorganica, University of Pisa, for 0.251JI, making it the most active miticidal compound. By their help in analyzing the essential oils; to FBM s.r.I. (Pisa) and direct contact I, 8-cineole had the lowest effectiveness. At Salumificio Ripafratta s.r.I. (Pisa) for providing the specimens of the dose of 6 fJI, linalool, menthol, and fenchone, tested by infested ham: and to Professor Macchioni Guido for the identification inhalation, showed values of mite mortality similar to those of the acarids. of the essential oils of the two lavender species and Mentha x piperita. In this test linalyl acetate did not show any REFERENCES activity; in fact at the. dose of 6 fJI it caused a percentage I. Boehm, S. 1990. DEET"based insect repellents, especially useful of mortality for the mites similar to that of the controls (6.7 against ticks, comprising olive and especially useful lavender oils. to 10%). Ger. Offen. 3:205"206. Considering both the assays, by direct contact and by 2. Czemecki, N., and H. Kraus. 1978. Mite dermatitis from Tyrophagus dimidatus. Z. Hautkrankheiten 53:414-416. inhalation, linalool, fenchone, and menthol were found to 3. Del Monte, P., U. Magnani, and M. Monari. 1990. Industria dei be the essential oil constituents presenting the best acaricidal salumi. Edagricole, Bologna, Italy. activity. The results obtained show that these compounds 4. Di Bernardino, L., A. Agrisano, L. Gori, and M. Cattaneo. 1987. really possess an acaricidal activity; in fact also at low Allergy to house dust and storage mites in children: epidemiologic observations. Ann. Allergy 59: 104-106. doses (0.25 IJI) L. stoechas, L. angustifolia, and Mentha x 5. Domenichini, G. 1978. La contaminazione biotica nei formaggi piperita essential oils, linalool, and menthol were able to pecorini in stagionatura. Sci. Teen. Lattiero Casearia 29: 182-193. kill most of the mites by direct contact. On the other hand, 6. Fox, M. T., T. 1. Sykes, and D. E. Jacobs. 1986. Forage mite for a possible use of these natural compounds, their activity infestation in the dog. Vet. Rec. 118:459--460. 7. Griffiths, D. A. 1960. Some field habitats of mites of stored food by inhalation must also be emphasized; for example, they products. Ann. AppI. Bioi. 48: 134-144. could easily be used to disinfest the rooms where food 8. Hink, W. F., and T. E. Duffy. 1986. Linalool as insecticide and products will be stored; or they could easily be used to kill acaricide. Belgium Pat. 902977AI860127. Jan 27. mites living on stored products, just by treating the rooms 9. Ingram, C. G., I. G. Jeffrey, I. S. Symington, and O. D. Cuthbert. 1979. Lancet ii, 1330-1332. where they are stored. 10. Iversen, M., J. Korsgard, T. Hallas, and R. Dahl. 1990. Mite allergy The absence of residues dangerous for human health and exposure to storage mites and dust mites in farmers. Clin. Exp. and the absence of modification of the color, flavor, odor, Allergy 20:211-219. and texture of stored food could permit a direct use of these II. Iversen, M., and B. Pedersen. 1990. The prevalence of allergy in Danish farmers. Allergy (Copenhagen) 65:344"353. natural pesticides on food products. Moreover, natural es- 12. Jacobson, M. 1988. Botanical pesticides past, present, and future. In sential oils and terpenes as well as synthetic terpenes J. T. Amason, B. 1. R. Philgime, and P. Morand (ed.). of

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JOURNAL OF FOOD PROTECTION, VOL. 58, MAY 1995