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Bergamot Essential Oil Attenuates Anxiety-Like Behaviour in Rats

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Bergamot Essential Oil Attenuates Anxiety-Like Behaviour in Rats molecules Article Bergamot Essential Oil Attenuates Anxiety-Like Behaviour in Rats Laura Rombolà 1, Laura Tridico 1, Damiana Scuteri 1, Tsukasa Sakurada 2, Shinobu Sakurada 3, Hirokazu Mizoguchi 3, Pinarosa Avato 4, Maria Tiziana Corasaniti 5, Giacinto Bagetta 1 and Luigi Antonio Morrone 1,* 1 Department of Pharmacy, Health and Nutritional Sciences, Section of Preclinical and Translational Pharmacology, University of Calabria, 87036 Rende, Italy; [email protected] (L.R.); [email protected] (L.T.); [email protected] (D.S.); [email protected] (G.B.) 2 First Department of Pharmacology, Daiichi College of Pharmaceutical Sciences, 815-8511 Fukuoka, Japan; [email protected] 3 Department of Physiology and Anatomy, Tohoku Pharmaceutical University, 981-8558 Sendai, Japan; [email protected] (S.S.); [email protected] (H.M.) 4 Department of Pharmacy-Drug Sciences, University of Bari Aldo Moro, IT-70125 Bari, Italy; [email protected] 5 Department of Health Sciences, University “Magna Graecia” of Catanzaro, 88100 Catanzaro, Italy; [email protected] * Correspondence: [email protected]; Tel.: +39-0984-493-054; Fax: +39-0984-493-107 Academic Editor: Olga Tzakou Received: 15 March 2017; Accepted: 9 April 2017; Published: 11 April 2017 Abstract: Preclinical studies have recently highlighted that bergamot essential oil (BEO) is endowed with remarkable neurobiolological effects. BEO can affect synaptic transmission, modulate electroencephalographic activity and it showed neuroprotective and analgesic properties. The phytocomplex, along with other essential oils, is also widely used in aromatherapy to minimize symptoms of stress-induced anxiety and mild mood disorders. However, only limited preclinical evidences are actually available. This study examined the anxiolytic/sedative-like effects of BEO using an open field task (OFT), an elevated plus-maze task (EPM), and a forced swimming task (FST) in rats. This study further compared behavioural effects of BEO to those of the benzodiazepine diazepam. Analysis of data suggests that BEO induces anxiolytic-like/relaxant effects in animal behavioural tasks not superimposable to those of the DZP. The present observations provide further insight to the pharmacological profile of BEO and support its rational use in aromatherapy. Keywords: bergamot essential oil; diazepam; behavioural tests; rat 1. Introduction Bergamot essential oil (BEO) is obtained by cold pressing of the epicarp and part of the mesocarp of Citrus bergamia Risso and Poiteau, belonging to the Rutaceae family, genus Citrus. Bergamot is defined as a hybrid of bitter orange (Citrus aurantium L.) and lemon (Citrus limon L.) by some authors, or of Citrus aurantium L. and Citrus aurantifolia Swing by others [1]. BEO consists of several substances among which terpens and oxygenated molecules in the volatile fraction (93%–96% of total), coumarines and psoralens in the non-volatile fraction (4%–7% of total) of the essence [2,3]. Particularly, the volatile fraction includes monoterpene and sesquiterpene hydrocarbons (e.g., d-limonene, β-bisabolene, γ-terpinene, α- and β-pinene, sabinene, β-myrcene, terpinolene, and geranyl acetate) and oxygenated derivatives (e.g., linalool, linalyl acetate, neral, geranial, neryl acetate, and geranyl acetate). The most abundant compounds are the monoterpene hydrocarbons d-limonene (25.62%–53.19% of the whole Molecules 2017, 22, 614; doi:10.3390/molecules22040614 www.mdpi.com/journal/molecules Molecules 2017, 22, 614 2 of 11 Moleculesessential 2017 oil),, 22 the, 614monoterpene ester, linalyl acetate (15.61%–40.37%), and the monoterpene alcohol,2 of 11 linalool (1.75%–20.26%) (Figure1)[ 4]. Bergamot essential oil is widely used in the cosmetic industry 20.26%)as perfume (Figure fixative 1) [4]. and Bergamot as an aromaessential in oil the is foodwidel tradey used and in the pharmaceutical cosmetic industry industry. as perfume As reported fixative andby the as an European aroma in Medicines the food trade Agency and pharmaceutic (EMA) monographal industry. in the As Herbalreported Medicinal by the European Products Medicines section, Agencytraditional (EMA) and monograph folk medicine in the use Herbal of BEO Medicinal has long Products been known section, of, buttraditional only in and the folk last tenmedicine years usehave of preclinical BEO has long studies been provided known severalof, but dataonly toin supportthe last potentialten years therapeutichave preclinical use of studies the essential provided oil. severalBEO is useddata to facilitatesupport potential wound healing therapeutic as antiseptic use of the and essential antihelminthic, oil. BEO effects is used that to arefacilitate supported wound by healingantimicrobial as antiseptic [5] and and antifungal antihelminthic, [6] activities effects as th wellat are as supported the capacity by ofantimicrobial the phytocomplex [5] and toantifungal increase [6]oxidative activities metabolism as well as inthe human capacity polymorphonuclear of the phytocomplex leukocytes to increase [7]. oxidative Furthermore, metabolism data accumulated in human polymorphonuclearin the literature so far leukocytes indicate that[7]. bergamotFurthermore, oil isda endowedta accumulated with notable in the neurobiolologicalliterature so far indicate effects (seethat bergamot [8,9]) originating, oil is endowed at least with in part, notable by an neurobiolological interference with effects basic (see mechanisms [8,9]) originating, finely tuning at least synaptic in part, byplasticity an interference under physiological with basic mechanisms [10,11] as wellfinely as tuning pathological synaptic conditions, plasticity under i.e., brain physiological ischemia [10,11] [12] and as wellpain as [13 pathological–18], induced conditions, under controlled i.e., brain and ischemia broadly [12] validated and pain experimental [13–18], induced settings. under Interestingly, controlled andBEO broadly also showed validated neuroprotective experimental effectssettings. in Interest humaningly, neuroblastoma BEO also showed cell line neuroprotective [19–22]. Moreover, effects this in humanphytocomplex, neuroblastoma as with cell other line essential [19–22]. oilsMoreover, [23,24], this is widely phytocom usedplex, in aromatherapyas with other essential (a branch oils of [23,24], herbal ismedicine) widely used to relieve in aromatherapy symptoms of(a branch stress-induced of herbal anxiety medicine) [25], to although relieve symptoms limited preclinical of stress-induced data are anxietyactually [25], available although [26, 27limited]. In thispreclinical regard, data to further are actually characterize available the [26,27]. neurobiological In this regard, profile to further of the characterizephytocomplex the and,neurobiological consequently, profile to contributeof the phytocom to a rationalplex and, use consequently, of BEO in aromatherapy, to contribute to this a rational study useinvestigated of BEO in the aromatherapy, effects of the this essential study oilinvestigated in behavioural the effects tests usuallyof the essential performed oil in to behavioural study anxiolytic, tests usuallystimulant performed or sedative to study and antidepressive anxiolytic, stimulant effects ofor compoundssedative and asantidepressive the open field effects (OFT) of [28 compounds], elevated asplus-maze the open (EPM)field (OFT) [29], [28], and forcedelevated swimming plus-maze (FST) (EPM) [30 [29],,31] tasks.and forced The resultsswimming obtained (FST) with [30,31] BEO tasks. are Thecompared results with obtained the benzodiazepine with BEO are compared diazepam with (DZP). the benzodiazepine diazepam (DZP). Figure 1. MainMain compounds compounds present in volatile frac fractiontion of bergamot essential oil (BEO). 2. Results 2.1. Effects of BEO on Open Field Test (OFT) Analysis of data indicates that systemic administration of bergamot essential oil (250 or 500500 µμL/kg)L/kg) induces significant significant differences differences in the in frequencies the frequencies of crossing of crossing (F treatment, (F treatment, Ftr(3, 140) Ftr(3,= 11.98, 140) p <= 0.0001, 11.98, Fp <time, 0.0001 Ft(3,, 140) F time, = 68.78, Ft(3, p < 140)0.0001, = Ftxtr(9, 68.78, 140)p < = 0.0001 1.004,, p Ftxtr(9, < 0.4395), 140) rearing = 1.004, (Ftr(3, 140)p < =0.4395), 6.348, p = rearing 0.0005, (Ft(3,Ftr(3, 140) 140) = 5.249, = 6.348 p <, 0.0018,p = 0.0005 Ftxtr(9,, Ft(3, 140) 140) = 1.610, = 5.249, p = 0.1179)p < 0.0018, and wallrearing Ftxtr(9, 140) (Ftr(3, = 1.610,140) = 11.24,p = 0.1179) p < 0.0001, and wallrearingFt(3, 140) = 32.80, (Ftr(3, p 140) < 0.0001, = 11.24 Ftxtr(9,, p < 0.0001, 140) Ft(3,= 2.42, 140) p = = 0.0138) 32.80, p (Figure< 0.0001, 2) Ftxtr(9,versus 140)jojoba = 2.42,oil (vehicle)p = 0.0138 or) (FigureDZP (1.22) mg/kg) versus group. jojoba oilParticularly, (vehicle) orthe DZP rats treated (1.2 mg/kg) with the group. higher Particularly, dose of BEO the (500 rats μ treatedL/kg) show with a decreasethe higher of dosecrossing, of BEO rearing, (500 µandL/kg) wallrearing show a decreasethat reach of statistical crossing, significance rearing, and at wallrearing the first two that intervals reach ofstatistical testing (5 significance and 10 min) at versus the first jojoba two oil intervals treated of rats testing (Figure (5 and2). Interestingly, 10 min) versus a statistically jojoba oil treated significant rats (Figuredifference2). is Interestingly, also observed a statisticallyat 5 min between significant BEO (500 difference μL/kg) isand also DZP observed groups
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