Abstract
The effect of lemon oil (Citrus limon) on Sarcoptes scabiei var. cuniculi was evaluated in vitro and in vivo. The mite samples were collected from naturally infected rabbits. The lemon oil was prepared in six concentrations by dilution with distilled water (2.5, 5, 10, 20, 50, and 100 %). In vitro application was done in five replicates for each concentration in petri dishes in the laboratory. The treated mites were observed at 1, 12, and 24 h post application (PA) for lemon oil effect. In addition, oxidative stress profile was evaluated for the treated mite. Dependent on in vitro results, 20 % lemon oil was used in vivo trial. Twenty-four naturally infected rabbits were divided into three groups of eight: 20 % lemon oil, deltamethrin, and untreated control. The infected parts of rabbits were treated topically once a week for four successive weeks. In vitro application results showed that lemon oil 10 and 20 % diluted in water caused mortality to 100 % of mites after 24 h PA. The oxidative stress profile revealed that mites treated with 20 % lemon oil had significantly (P < 0.05) higher hydrogen peroxide and malondialdehyde when compared with mites treated with deltamethrin or distilled water. In vivo application of 20 % lemon oil on naturally infected rabbits showed complete recovery from clinical signs, absence of mite in microscopic examination from the second week of treatment. In addition, productive performance was significantly better than infected untreated group. Also, the treated tissue showed stoppage of scale formation and hair growth faster than deltamethrin-treated rabbits. Consequently, lemon oil has remarkable miticidal activity in vitro and in vivo applications.
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Abdel-Kafy EM, Ali WAH, Hoda AS, Azoz AA (2008) Effects of short heat exposure, balanced feed restriction and acetic acid supplement at post weaning on growth and thermoregulation in growing rabbits during hot season. Nutr. Dig. Physiolo. 9th world rabbit congress-June 10-(13), Verona - Italy, p 507–512
Ademola IO, Ibironke AA, Aghanu NV, Chris CO (2014) Evaluation of acaricidal activity of different seed oils on Psoroptes cuniculi (Delafond, 1859) (Cheyletidae) in rabbits. J Pharm Bio Sci 9(4):94–97
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126
Ahmed L, Khan A, Khan MZ, Hussain I, Mahmood F, Sleemi MK, Lodhi LA, Abdullah I (2012) Toxico -pathological effects of Cypermethrin upon male reproductive system in rabbits. Pestic Biochem Physiol 103:194–201
Amer A, Mehlhorn H (2006) Larvicidal effects of various essential oils against Aedes, Anopheles, and Culex larvae (Diptera, Culicidae). Parasitol Res 99:466–472
Armstrong JS (2006) Mitocondrial membrane permeabilization: the sine qua non for cell death. BioEssays 2:253–260
Ayoola GA, Johnson OO, Adelowoton T, Aibinu IE, Adenipekun E, Adepoju-Bello AA, Coker HAB, Odugbemi TO (2008) Evaluation of the chemical constituents and antimicrobial activity of the volatile oil of Citrus reticulate (Tangerine fruit peel) from South West Nigeria. Afr J Biotechnol 7:2227–2231
Baker SA (1999) Mites and ticks of domestic animals. An identification guide and information source. Department of Entomology, the Natural History Museum, London
Bancroft JD, Stevan A, Turner DR (1990) Theory and practice of histological techniques, 3rd edn. Churchill Livingstone, New York, p 258
Białon M, Krzyśko-Łupicka T, Koszałkowska M, Wieczorek PP (2014) The influence of chemical composition of commercial lemon essential oils on the growth of candida strains. Mycopathologia 177:29–39
Cristian M, Mihai C, Horea B, Eronim S (2010) Acaricidal effect of eleven essential oils against the poultry red mite Dermanyssus gallinae (Acari: Dermanyssidae). Sci Parasitol 11(2):71–75
Dagleish MP, Ali Q, Powell RK, Butz D, Woodford MH (2007) Fetal Sarcoptes scabiei infection of blue sheep (Pseudoisnayaur) in Pakistan. J Wildl Dis 43:512–517
Ebigwai JK, Ilondu EM, Markson AA, Ekeleme E (2012) In vitro evaluation of the essential oil extract of six plant species and Ivermectin on the Microfilaria Larva of Simulium yahense. Res J Med Plant 6(6):461–465
EL-Zemity SR, Rezk HA, Zaitoon AA (2006) Acaricidal activity of some essential oils and their monoterpenoidal constituents against the parasitic Bee mites Varroa destructor (Acari: Varroidae). J Appl Sci Res 2(11):1032–1036
Fichi G, Flamini G, Zaralli L, Perrucci S (2007) Efficacy of an essential oil of Cinnamomum Zeylanicum against Psoroptes cunicul. Phytomedicine 14:227–231
Fisher K, Phillips C (2008) Potential antimicrobial uses of essential oils in food: is citrus the answer? Trends Food Sci Technol 19:156–164
Gassner B, Wuthrich A, Lis J, Scholtysik G, Solioz M (1997) Topical application of synthetic pyrethroids to cattle as a source of persistent environmental contamination. J Environ Sci Health B 32:729–739
Giatropoulos A, Papachristos DP, Kimbaris A, Koliopoulos G, Polissiou MG, Emmanouel N, Michaelakis A (2012) Evaluation of bioefficacy of three Citrus essential oils against the dengue vector Aedes albopictus (Diptera: Culicidae) in correlation to their components enantiomeric distribution. Parasitol Res 111(6):2253–2263
Gurgose SY, Sahin T, Sevigili M, Ozkutlu Z, Ozan ST (2003) The effects of ivermectin or doramectin treatment on some antioxidant enzymes and the level of lipid perioxidationin sheep with natural sarcoptic scabs. J Fac Vet Med 14:30–34
Hanafi ME, Maghraby AN, Ramadan MM, Mahmoud AM, EL-Allawy MH (2010) Aromatherapy of Cinnamomum zeylanicum Bark oil for treatment of scabies in rabbits with emphases on the productive performance. Am Eurasian J Agric Environ Sci 7(6):719–727
Harkness JE, Wagner JE (1995) Specific diseases and conditions, The Biology and medicine of rabbits and rodents. Williams & Wilkins, Baltimore, p 172
Isman MB (1999) Pesticides based on plant esential oils. Pestic Outlook 10:68–72
Isman MB (2001) Pesticides based on plant essential oils for management of plant pests and disease. International symposium on development of natural pesticides from forest resources. Korea forest Research Institute, Seoul Korea, p 1–9
Isman MB, Machial CM (2006) Pesticides based on plant essential oils: from traditional practice to commercialization. In: Rai M, Carpinella MC (eds) Naturally Occurring Bioactive Compounds. Elsevier, Amsterdam, pp 29–44
Jana PS, Guha C, Saha SB, Biswas SU, Datta S, Baksi S (2004) Clinico-pathological and therapeutic studies on natural psoroptic acariosis in rabbits. Bangl J Vet Med 2(2):155–158
Jones TC, Hunt RD, King NW (1997) Veterinary pathology, 6th edn. Williams and Wilkins, Baltimore Philadelphia
Kim SI, Yi JH, Tak JH, Ahn YJ (2004) Acaricidal activity of plant essential oils against Dermanyssus gallinae (Acari: Dermanyssidae). Vet Parasitol 120:297–304
Kurade NP, Bhat TK, Jithendran KP (1996) Effect of ivermectin against ear mange mite (Psoroptes cuniculi) in naturally infested rabbits. World Rabbit Sci 4(1):25–27
Lee HS (2006) Mosquito larvicidal activity of aromatic medicinal plant oils against Ae. aegypti and Cx. pipiens pallens. J Am Mosq Control Assoc 22:292–295
Lim PC, Liu XY, Chan SY (2009) A review on terpenes as skin penetration enhancers in transdermal drug delivery. J Essent Oil Res 21:423–428
Macchioni F, Perrucci S, Cecchi F, Cioni PL, Morelli I, Pampiglione S (2004) Matricaria chamomilla, against the mite Psoroptes cuniculi. Med Vet Entomol 18:205–207
Melliou E, Michaelakis A, Koliopoulos G, Skaltsounis AL, Magiatis P (2009) High quality bergamot oil from Greece: chemical analysis using enantiomeric GC-MS and larvicidal activity against the West Nile virus vector. Molecules 14:839–849
Merck R (2005) The Merck Veterinary manual, 9th edn. Merck & Co., Whitehouse station
Michaelakis A, Papachristos D, Kimbaris A, Koliopoulos G, Giatropoulos A, Polissiou MG (2009) Citrus essential oils and four enantiomeric pinenes against Cx. pipiens (Diptera: Culicidae). Parasitol Res 105(3):769–773
Moharram SA (1996) Experimental pathological studies on pesticides and parasitic infection in rabbits. MVSc Thesis Path Fac Vet Med Zagazig University
Mugnaini L, Nardoni S, Pinto L, Pistelli L, Leonardi M, Pisseri F, Mancianti F (2012) In vitro and in vivo antifungal activity of some essential oils against feline isolates of Microsporum canis. J Mycol Med 22(2):179–184
Nong X, Fang CL, Wang JH, Gu XB, Yang DY, Liu TF, Fu Y, Zhang RH, Zheng WP, Peng XR, Wang SX, Yang GY (2012) Acaricidal activity of extract from Eupatorium adenophorum against the Psoroptes cuniculi and Sarcoptes scabiei in vitro. Vet Parasitol 187:345–349
Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95(2):351–358
Oshaghi MA, Ghalandari R, Vatandoost H, Shayeghi M, Kamali-nejad M, Tourabi-Khaledi H, Abolhassani M, Hashemzadeh M (2003) Repellent effect of extracts and essential oils of Citrus lemon (Rutaceae) and Melissa officinalis (Labiatae) against main Malaria Vector, An. stephensi (Diptera: Culicidae). Iran J Public Health 32(4):47–52
Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158–168
Patel JS, Patel RR, Panchasara HH, Brahmaxtri KG (2003) Epizootiology of sarcoptic mange in buffalo calves. Indian Vet J 80:972–974
Raal A, Orav A, Arak E (2007) Composition of the essential oil of Salvia Officinalis L. from various European countries. Nat Prod Res 21:406–411
Regnault-Roger C, Vincent C, Arnason JT (2012) Essential oils in insect control: low-risk products in a high-stakes world. Annu Rev Entomol 57:405–424
Sammataro D, Pia U, Guerrero F, Finley J (2005) The resistance of varroa mites (Acari: Varroidae) to acaricides and the presence of esterase. Int J Acarol 31(1):67–74
Sapra B, Jain S, Tiwary AK (2008) Percutaneous permeation enhancement by terpenes: mechanistic view. AAPS J 10:120–132
Schmahl G, Al-Rasheid KA, Abdel-Ghaffar F, Klimpel S, Melhorn H (2010) The efficacy of neem seed extracts (Tre-San, MiteStop) on a broad spectrum of pets and parasites. Parasitol Res 107(2):261–269
Seddiek SA, Khater HF, El-Shorbagy MM, Ali MA (2013) The acaricidal efficacy of aqueous neem extract and ivermectin against Sarcoptes scabiei var. cuniculi in experimentally infested rabbits. Parasitol Res 112:2319–2330
Sook RI, Cha-Ho J (2006) Acaricidal effects of herb essential oils against Dermatophagoides farinae and D.pteronyssinus (Acari: Pyroglyphidae) and qualitative analysis of a herb Mentha pulegium (pennyroyal). Korean J Parasitol 44(2):133–138
Sun B, Jing Y, Chen K, Song L, Chen F, Zhang L (2007) Protective effect of nitric oxide on iron deficiency-induced oxidative stress in maize (Zea mays). Plant Physiol 164:536–543
Uni Z, Gal-Garber O, Geyra A, Sklan D, Yahav S (2001) Changes in growth and function of chick small intestine epithelium due to neonatal thermal conditioning. Poult Sci 80:438–445
Valgimigli L, Gabbanini S, Berlini E, Lucchi E, Beltramini C, Bertarelli YL (2012) Lemon (Citrus limon, Burm.f.) essential oil enhances the trans-epidermal release of lipid- (A, E) and water- (B6, C) soluble vitamins from topical emulsions in reconstructed human epidermis. Int J Cosmet Sci 34:347–356
Villafañe E, Tolosa D, Bardón A, Neske A (2011) Toxic effects of Citrus aurantium and C. lemon essential oils on Spodoptera frugiperda (Lepidoptera: Noctuidae). Nat Prod Commun 6(9):1389–1392
Zenner L, Callait MP, Granier C, Chauve C (2011) In vitro effect of essential oils from Cinnamomum aromaticum, Citrus lemon and Allium sativum on two intestinal flagellates of poultry, Tetratrichomonas gallinarum and Histomonas meleagridis. Parasite 10(2):153–157
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The authors introduce most greetings for Dr. Waleed M. Arafa and Dr. Ibrahim M. Yousef for helping in this work.
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Aboelhadid, S.M., Mahrous, L.N., Hashem, S.A. et al. In vitro and in vivo effect of Citrus limon essential oil against sarcoptic mange in rabbits. Parasitol Res 115, 3013–3020 (2016). https://doi.org/10.1007/s00436-016-5056-8
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DOI: https://doi.org/10.1007/s00436-016-5056-8