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Oxygen introduction during extraction and the improvement of antioxidant activity of essential oils of basil, lemon and lemongrass/Introducao de oxigenio durante a extracao e aumento da atividade antioxidante de oleos essenciais de manjericao, limao e capim-limao.


The demand of consumers for natural products as substitutes for synthetic additives has increased given that synthetic substances can result in adverse effects to human health. In this way, several natural compounds have been studied as food additives, including essential oils, which are a promising alternative for food industries that is being recognized by regulatory bodies (e.g.. Food and Drug Administration FDA, USA) as safe substances (ALFONZO et al., 2017). Essential oils are secondary metabolites with a strong odoriferous impact obtained through different parts of several aromatic plants including leaves, flowers, roots, seeds, fruits and peels. These oils are composed of a complex mixture of volatile compounds, mainly monoterpenes and sesquiterpenes, which can be classified as hydrocarbons or oxygenated ones (DJOUAHRI, BOUDARENE, & MEKLATI, 2013). Oxygenated compounds play an important role in essential oils, and they are often responsible for the main biological properties. However, their amount is closely related to the extraction method used (AMORATI et al., 2013). Antioxidant and antimicrobial activity of essential oils are often reported, and they have been used for the improvement of the quality and shelf-life of food such as fish, meat, cheese and minimally processed fruits and vegetables (AMORATI et al., 2013; PATEL, 2015). In addition, essentials oils can be used in active food packaging to reduce the oxidation process and extend the shelf-life of perishable products (MAISANAB A et al., 2017).

Extraction of essential oils is a critical step because, depending on the conditions used for extraction (e.g., heating, amount of plant material, atmosphere composition, time for extraction), the composition of essential oils could change with impact on their antioxidant and antimicrobial activities (DJOUAHRI et al., 2013). Hydro distillation (HD) is one of the most used methods for essential oil extraction, and it is recommended in official compendia of quality control of aromatic plants (Brazilian Pharmacopeia, 2010; I AL, 2004). This method is based on the heating of plant material with water, and the essential oil is carried out together with the water vapor and further condensed (and separated from water) into a Clevenger-type apparatus (ORIO et al., 2012).

In this way, HD could be considered to be a simple process for essential oil extraction, and the main modifications for the improvement of extraction (e.g., reduction in extraction time) have focused on the use of microwaves for heating (CHEMAT & CRAVOTTO, 2013). Despite the good results obtained regarding the reduction in extraction time and energy consumption, the use of microwaves requires dedicated instruments, which generally have a high cost of acquisition and limited widespread application in laboratories. In this research, a simple modification was made to conventional HD extraction in order to obtain essential oil from different plants with higher antioxidant activity by the introduction of oxygen gas during extraction. In this way, essential oils from lemon peel and leaves of basil and lemongrass were extracted with and without addition of oxygen. Chemical composition of essential oils was then evaluated by gas chromatography (GC) and antioxidant activity results were obtained by using the oxygen radical absorbance capacity (ORAC) method.


Plants, chemicals, materials and instrumentation

The lemon (Persian lime) peels and basil (Ocimum basilicum) and lemongrass (Cymbopogon citratus) leaves were obtained in May 2016 from local plants and stored at -18[degrees]C for a week until the end of the extraction experiments. Samples of basil and lemongrass were ground in a knife mill at 5,400rpm for 3s and lemon peels at 13,500rpm for 5s in order to avoid the rupture of structures that retain essential oils in the plants (TISCHER et al., 2017). Anhydrous sodium sulfate RA. (99%, Impex, Brazil) was used to dry the essential oil after extraction. Deionized water for distillation and hexane for the dilution of essential oils for GC analysis were used. Chromatographic grade helium, hydrogen, nitrogen and oxygen (White Martins, Brazil) were used in the GC-FID and GC-MS determination, and oxygen was also used in HD. All reagents for the evaluation of the antioxidant activity of ORAC were of analytical grade (Sigma-Aldrich USA).

A Clevenger apparatus equipped with a 1L glass flask was used for the extraction of essential oils by HD, with an adaptation for oxygen introduction (Figure 1). Samples were ground using a knife mill (model MA 630/1, Marconi, Brazil). Compounds presented in essential oils were determined using a gas chromatograph (Varian Star 3400CX, USA) equipped with a flame ionization detector and a fused silica capillary column RTX-5MS (30m x 0.25mm i.d. x 0.25|im film thickness, Restek Corporation, USA). A mass spectrometry chromatograph Shimadzu Q-2010 Plus (GC-MS, Shimadzu Corporation, Japan) equipped with a fused silica capillary column ZB-5MS (30m x 0.25mm i.d. x 0.25 [micro]m film thickness, Phenomenex, USA) was used for identification of substances. Antioxidant activity was measured by fluorimetrie assay for ORAC and carried out using SpectraMax M5 (Molecular Devices, USA).

HD, GC analysis and antioxidant activity determination

Ground leaves and peels (50g) were mixed with 500mL of water in the glass flask, with further heating for 3h in a Clevenger-type apparatus. A polytetrafluoroethylene (PTFE) tube (3mm of internal diameter) was adapted through one of the necks of the flask using silicon rubber for oxygen introduction (Figure 1). Oxygen flow rate was maintained constant at 0.7L min1 during all extractions, but a purge step was used previously, using 2L min1 oxygen for 5min. The essential oil was separated by density and was collected and dried using anhydrous sodium sulfate to eliminate traces of moisture. The extracted essential oils were kept at 4[degrees]C until further analysis.

Composition of essential oil was determined by GC-FID using 1 [micro]L of diluted sample in hexane (1:100). Equipment was operated in split mode (1:20) at 250[degrees]C for both injection and detection. For evaluation of the basil essential oil, the temperature program was started at 35[degrees]C for 5min, increasing to 90[degrees]C at 4[degrees]C [min.sup.-1] and to 150[degrees]C at 31[degrees]C [min.sup.-1], and finally to 220[degrees]C at 20[degrees]C [min.sup.-1]; it was then held for 1min at this temperature. For the lemongrass and lemon peel essential oils, the column temperature started at 35[degrees]C for 5min, increasing to 100[degrees]C at 2[degrees]C [min.sup.-1] and thereafter to 220[degrees]C at 20[degrees]C [min.sup.-1], held for 5min. Hydrogen was used as carrier gas and flow rate and pressure values were 2.5mL [min.sup.-1] and 15psi, respectively. Quantification of compounds was performed based on the normalization of the peak areas. Identification was performed by GC-MS using the same conditions as GC-FID, but using helium instead of hydrogen. Temperature of GC-MS interface and ionization source was fixed at 250[degrees]C using the electron ionization mode (+70eV) and monitoring ions between 35 to 350m [z.sup.-1]. In order to calculate the Kovats Index (KI) of volatile compounds, a homologous series of alkanes ([C.sub.6]-[C.sub.24]) was analyzed using the same chromatographic conditions. In addition, the identification of compounds was confirmed by a comparison with mass spectra available in the National Institute of Standards and Technology library (NIST 02, Gaithersburg, MD, USA) and also with the calculated KI reported in the literature.

Antioxidant activity determination by using the ORAC method was performed based on the method of OU et al. (2001). This method is based on the scavenging activity of essential oils against peroxyl radicals generated from the AAPH radical inductor. For this purpose, 25 [micro]L of diluted essential oil or Trolox reference solutions was added into potassium phosphate buffer (75mmol L1, pH 7.4) and incubated at 37[degrees]C for lOmin in microplates; 150[micro]L of fluorescein solution (81mnol [L.sup.-1]) was used as an indicator and 25 [micro]L of AAPH (152mmol [L.sup.-1]) was added as peroxyl radical generator. Using wavelengths of 485mn for excitation, fluorescence was measured in 528mn at 37[degrees]C for 120min. Antioxidant activity was determined considering the area under curve (AUC) values and Trolox curve (0-96[micro]mol [L.sup.-1]).

All extractions as well as chromatographic and antioxidant activity analysis were carried out in triplicate and the results were statistically evaluated using the Student's t-test at 5% confidence level with the software Statistica v. 7.0 (Statsoft Tulsa, USA, 2004).


Oxygen introduction during extraction process presented little influence on yield of the essential oils evaluated. For lemongrass, no differences were observed for extractions with and without oxygen, and an essential oil yield of 1.49% was obtained. For the basil and lemon essential oils, a slight reduction in yield was observed, from 2.75% and 5.25% (without oxygen) to 2.58% and 4.69% (with oxygen) for basil and lemon, respectively. In relation to the chemical composition, essential oils extracted with and without oxygen introduction presented the same number of volatile substances, but with changes in the amount of some compounds, as can be seen in table 1.

A total of 16 monoterpenes were reported in the essential oil from basil, and in general oxygen addition resulted in a decrease in hydrocarbon monoterpenes, reaching an amount of 8.87% in conventional HD and 2.33% in HD with oxygen introduction. In this case, a significant reduction in [beta]-pinene, [alpha]-pinene and limonene was observed. In relation to oxygenated monoterpenes in basil, a higher amount was obtained using oxygen introduction during extraction (78.32%) in comparison to conventional HD (without oxygen, 72.98%). Changes were observed mainly for linalool and eugenol, but it was also important for camphor and [alpha]-terpineol. For the sesquiterpenes of basil, effect of oxygen introduction was lower in relation to monoterpenes, but it presented a slight decrease in hydrocarbons (from 14.04% to 13.28%) and also an increase in oxygenated ones (from 4.02% to 6.07%).

In lemongrass essential oil, only monoterpenes were identified and the use of oxygen resulted in a strong reduction in hydrocarbon monoterpenes in comparison to conventional HD without oxygen (from 14.70% in HD to 7.05% for HD plus oxygen). In relation to the oxygenated compounds of the lemongrass essential oil, it is important to note the higher amount of citral for extraction with oxygen, which is considered to be the most important substance for lemongrass essential oil. This compound is represented by the isomers neral and geranial, which are mainly responsible for the odor and biological properties of oil. In addition, it has been considered to be a building block for fine chemicals (GANJEWALA et al., 2012). Thus, oxygen introduction increased the geranial and neral amount from 34.41% and 49.82% to 36.58% and 55.10%, respectively. Therefore, the use of oxygen during extraction allowed the production of more valuable compounds in the lemongrass essential oil.

For the lemon peel essential oil, the amount of hydrocarbon monoterpenes decreased (from 91.43% to 86.36%) by the introduction of oxygen, mainly due to the reduction in limonene, [beta]-pinene and [alpha]-pinene. These results are in agreement with NGUYEN et al. (2009) that demonstrated the high susceptibility of these compounds to oxidation under an oxygen atmosphere. Lemon essential oil is represented by a small amount of oxygenated compounds, but the oxygen addition almost doubled the amount of these compounds (from 6.59% to 11.43%). In this case, a significant increase in [alpha]-terpineol, neral and geranial (citral) was obtained with the oxygen. This is an important feature because citral was described as one of the major contributors to the aroma of lemon oil (NGUYEN et al., 2009).

According to the results obtained, the introduction of oxygen during extraction increased the concentration of oxygenated compounds in the essential oils. Studies have demonstrated that the antioxidant and antimicrobial capacity of essential oils are directly related to oxygenated terpenes. For this reason these compounds could be considered to be more valuable (AMORATI et al., 2013) and the antioxidant activity evaluation of oils was performed (Figure 2) by using the ORAC method (BENTAYEB et al., 2014). As shown in figure 2, extraction process in an oxygenated atmosphere resulted in the highest antioxidant activity for all analyzed essential oils. The antioxidant activity of the basil essential oil increased from 618 to 906 [micro]mol Trolox [g.sup.-1] oil, which could be explained by chemical modifications of the essential oil promoted by oxygen addition. Oil extracted with oxygen presented higher amounts of linalool and eugenol, which are compounds reported in the literature as highly antioxidant (GULCIN, 2011; DUARTE et al., 2016). For lemongrass, an increase in antioxidant activity with oxygen addition was also observed, with values of 355 and 613 [micro]mol Trolox [g.sup.-1] oil for conventional HD without and with oxygen, respectively. For lemon essential oil, antioxidant activity improved to a high extent, considering that generally this essential oil presented low antioxidant potential. Oxygen introduction in this case improved antioxidant activity four times, from 72 to 262 [micro]mol Trolox [g.sup.-1] oil with oxygen addition probably by the higher concentration of citral. Therefore, the antioxidant activity evaluation confirmed that changes observed in the chemical composition of oils extracted with oxygen improved the quality of essential oils obtained from the three plant materials evaluated.


The introduction of oxygeninthe extraction of essential oils of basil, lemongrass and lemon peel lead to a higher amount of oxygenated compounds in the oil, mainly a rise in linalool, camphor, [alpha]-terpineol, neral, geranial, eugenol and [alpha]-muurolol. Antioxidant activity showed that the use of oxygen during extraction provided essential oils with more activity, explained by the increase in oxygenated terpenes. Taking into account these features, it was possible to conclude that the simple modification proposed in this study could be considered to be a suitable alternative to obtain compounds in the essential oil with higher antioxidant activity. 10.1590/0103-8478cr20170045

Received 01.22.17

Approved 05.24.17

Returned by the author 06.17.17



The authors are grateful to Coordenacao de Aperfeicoamento de Pessoal de Nivel Superior (CAPES), Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq) and Fundacao de Amparo a Pesquisa do Estado do Rio Grande do Sul (FAPERGS) for supporting this study.


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Daniele de Freitas Ferreira (1) Flavia Michelon Dalla Nora (1) Bruna Nichelle Lucas (1) Cristiano Ragagnin de Menezes (1) Alexandre Jose Cichoski (1) Sandro Rogerio Giacomelli (2) Roger Wagner (1) Juliano Smanioto Barin (1) *

(1) Departamento de Tecnologia e Ciencia dos Alimentos, Universidade Federal de Santa Maria (UFSM), 97105-900, Santa Maria, RS, Brasil.

E-mail: * Corresponding author.

(2) Departamento de Ciencias Exatas e da Terra, Universidade Regional Integrada do Alto Uruguai e Missoes (URI), Frederico Westphalen, RS, Brasil.

Caption: Figure 1--Apparatus used for the essential oil extraction with oxygen introduction.

Caption: Figure 2-Antioxidant activity profile of basil (A), lemongrass (B) and lemon (C) essential oils extracted under conventional hydrodistillation without oxygen (HD) and with oxygen (HD + [O.sub.2]) using ORAC assay.
Table 1--Volatile compounds of basil, lemongrass and lemon essential
oil (%) obtained by GC-FID after extraction using conventional
hydrodistillation without oxygen (HD) and with oxygen (HD +

Volatile compounds               [RI.sup.1]   [RI.sup.2]

                        Hydrocarbon monoterpenes

[alpha]-thujene                     926          925
[alpha]-pinene                      935          936
Campitene                           954          954
[beta]-pinene                       978          978
Myrcene                             992          992
[beta]-cymene                       1026         1026
Limonelle                           1029         1029
(Z)-[beta]-ocimene                  1044         1041
(E)-P[beta]ocimene                  1056         1055
[gamma]-terpinene                   1064         1063
[alpha]-terpinolene                 1090         1089

                        Oxygenated monoterpenes

1,8-cineol                          1036         1035
Linalool                            1102         1103
[beta]-citronellol                  1143         1228
Camphor                             1176         1177
4-terpineol                         1190         1184
[alpha]-terpineol                   1229         1203
Nerol                               1230         1228
Neral                               1240         1240
Geranial                            1268         1270
Bomyl acetate                       1287         1286
Neryl acetate                       1361         1365
Geranyl acetate                     1366         1368
Eugenol                             1386         1378

                        Hydrocarbon sesquiterpenes

[alpha]-copaene                     1374         1374
[beta]-bourbonene                   1382         1382
[beta]-caryophyllene                1416         1418
[alpha]-bergamotene                 1435         1436
D-Gennacrene                        1479         1479
[beta]-bisabolene                   1510         1500
[gamma]-cadinene                    1511         1512
[delta]-cadinene                    1522         1525

                        Oxygenated sesquiterpenes

[alpha]-muurolol                    1641         1645
[alpha]-cadinol                     1653         1653
Total oxygenated compounds
Total non oxygenated compounds

Volatile compounds

                                   HD      HD+[O.sub.2]

                        Hydrocarbon monoterpenes

[alpha]-thujene                    --           --
[alpha]-pinene                   1.47 *       0.05 *
Campitene                        1.08 *       0.13 *
[beta]-pinene                    2.23 *       0.41 *
Myrcene                          1.15 *       0.37 *
[beta]-cymene                      --           --
Limonelle                        1.89 *       0.79 *
(Z)-[beta]-ocimene               0.23 *       0.12 *
(E)-P[beta]ocimene                 --           --
[gamma]-terpinene                0.26 *       0.13 *
[alpha]-terpinolene              0.56 *       0.33 *
Total                             8.87         2.33

                        Oxygenated monoterpenes

1,8-cineol                       22.21 *      9.06 *
Linalool                         22.45 *     29.41 *
[beta]-citronellol                 --           --
Camphor                          13.70 *     16.00 *
4-terpineol                       0.56         0.62
[alpha]-terpineol                2.53 *       3.49 *
Nerol                            0.02 *       0.04 *
Neral                              --           --
Geranial                           --           --
Bomyl acetate                    0.11 *       0.16 *
Neryl acetate                      --           --
Geranyl acetate                    --           --
Eugenol                          11.39 *     19.54 *
Total                             72.98       78.32

                        Hydrocarbon sesquiterpenes

[alpha]-copaene                   0.28         0.27
[beta]-bourbonene                 0.24         0.26
[beta]-caryophyllene              1.71         1.71
[alpha]-bergamotene               3.20         3.23
D-Gennacrene                     6.98 *       6.02 *
[beta]-bisabolene                  --           --
[gamma]-cadinene                 1.52 *       1.49 *
[delta]-cadinene                 0.21 *       0.30 *
Total                             14.04       13.28

                        Oxygenated sesquiterpenes

[alpha]-muurolol                 3.80 *       5.64 *
[alpha]-cadinol                  0.22 *       0.43 *
Total                             4.02         6.07
Total oxygenated compounds        76.99       84.39
Total non oxygenated compounds    23.01       15.61

Volatile compounds

                                   HD      HD+[O.sub.2]

                        Hydrocarbon monoterpenes

[alpha]-thujene                    --           --
[alpha]-pinene                     --           --
Campitene                          --           --
[beta]-pinene                      --           --
Myrcene                          14.10 *      6.60 *
[beta]-cymene                     0.02         0.06
Limonelle                         0.02         0.02
(Z)-[beta]-ocimene               0.34 *       0.22 *
(E)-P[beta]ocimene               0.22 *       0.15 *
[gamma]-terpinene                  --           --
[alpha]-terpinolene                --           --
Total                             14.70        7.05

                        Oxygenated monoterpenes

1,8-cineol                         --           --
Linalool                         0.68 *       0.76 *
[beta]-citronellol               0.39 *       0.51 *
Camphor                            --           --
4-terpineol                        --           --
[alpha]-terpineol                  --           --
Nerol                              --           --
Neral                            34.41 *     36.58 *
Geranial                         49.82 *     55.10 *
Bomyl acetate                      --           --
Neryl acetate                      --           --
Geranyl acetate                    --           --
Eugenol                            --           --
Total                             85.30       92.95

                        Hydrocarbon sesquiterpenes

[alpha]-copaene                    --           --
[beta]-bourbonene                  --           --
[beta]-caryophyllene               --           --
[alpha]-bergamotene                --           --
D-Gennacrene                       --           --
[beta]-bisabolene                  --           --
[gamma]-cadinene                   --           --
[delta]-cadinene                   --           --
Total                              --           --

                        Oxygenated sesquiterpenes

[alpha]-muurolol                   --           --
[alpha]-cadinol                    --           --
Total                              --           --
Total oxygenated compounds        85.30       92.95
Total non oxygenated compounds    14.70        7.05

Volatile compounds

                                    HD      HD+[O.sub.2]

                        Hydrocarbon monoterpenes

[alpha]-thujene                   0.64 *       0.28 *
[alpha]-pinene                    2.37 *       1.03 *
Campitene                           --           --
[beta]-pinene                    12.46 *       7.87 *
Myrcene                           1.51 *       1.31 *
[beta]-cymene                       --           --
Limonelle                         58.00        58.64
(Z)-[beta]-ocimene                  --           --
(E)-P[beta]ocimene                  --           --
[gamma]-terpinene                15.7 (a)      16.36
[alpha]-terpinolene               0.73 *       0.87 *
Total                             91.43        86.36

                        Oxygenated monoterpenes

1,8-cineol                          --           --
Linalool                            --           --
[beta]-citronellol                  --           --
Camphor                             --
4-terpineol                       0.29 *       0.62 *
[alpha]-terpineol                 0.48 *       0.98 *
Nerol                               --           --
Neral                             1.77 *       3.01 *
Geranial                          2.45 *       4.20 *
Bomyl acetate                       --           --
Neryl acetate                     1.15 *       1.92 *
Geranyl acetate                   0.45 *       0.70 *
Eugenol                             --           --
Total                              6.59        11.43

                        Hydrocarbon sesquiterpenes

[alpha]-copaene                     --           --
[beta]-bourbonene                   --           --
[beta]-caryophyllene               0.36         0.39
[alpha]-bergamotene               0.56 *       0.63 *
D-Gennacrene                        --           --
[beta]-bisabolene                  1.07         1.19
[gamma]-cadinene                    --           --
[delta]-cadinene                    --           --
Total                              1.99         2.21

                        Oxygenated sesquiterpenes

[alpha]-muurolol                    --           --
[alpha]-cadinol                     --           --
Total                               --           --
Total oxygenated compounds         6.59        11.43
Total non oxygenated compounds    93.41        88.57

Results reported as mean of determinations (n=3); Means followed by
are statistically different (Student's f-test; P>0.05).

(1) Kovats' retention index obtained by GC-MS in this study using a
RTX-5MS and a ZB-5MS column.

(2) Kovats' retention index values for all constituents obtained from
literature (Adams, NIST, 2005).
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Title Annotation:FOOD TECHNOLOGY
Author:de Freitas Ferreira, Daniele; Nora, Flavia Michelon Dalla; Lucas, Bruna Nichelle; de Menezes, Cristi
Publication:Ciencia Rural
Article Type:Ensayo
Date:Aug 1, 2017
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