Comparison of different drying methods on Chinese ginger (Zingiber officinale Roscoe): Changes in volatiles, chemical profile, antioxidant properties, and microstructure.

Food Chemistry xxx (2015) xxx–xxx

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Comparison of different drying methods on Chinese ginger (Zingiber officinale Roscoe): Changes in volatiles, chemical profile, antioxidant properties, and microstructure Kejing An a, Dandan Zhao b,c, Zhengfu Wang b,c, Jijun Wu a, Yujuan Xu a, Gengsheng Xiao a,⇑ a Sericulture and Agri-Food Research Institute Guangdong Academy of Agricultural Sciences/Key Laboratory of Functional Foods, Ministry of Agriculture/Guangdong Key Laboratory of Agricultural Products Processing, Guangzhou 510610, PR China b College of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100083, PR China c National Engineering and Technology Research Center for Fruits and Vegetable Processing, PR China

a r t i c l e

i n f o

Article history: Received 18 May 2015 Received in revised form 4 November 2015 Accepted 6 November 2015 Available online xxxx Chemical compounds studied in this article: 6-Gingerol (PubChem CID: 442793) 8-Gingerol (PubChem CID: 168114) 10-Gingerol (PubChem CID: 168115) 6-Shogaol (PubChem CID: 5281794) Zingerone (PubChem CID: 31211) b-Phellandrene (PubChem CID: 11142) b-Bisabolene (PubChem CID: 10104370) a-Curcumene (PubChem CID: 3083834) 2,2-Diphenyl-1-picrylhydrazyl (PubChem CID: 74358) 2,20 -Azinobis (3-ethylbenzo thiazoline-6sulfonic acid) diammonium salt (ABTS) (PubChem CID: 9570474)

a b s t r a c t Nowadays, food industry is facing challenges in preserving better quality of fruit and vegetable products after processing. Recently, many attentions have been drawn to ginger rhizome processing due to its numerous health promoting properties. In our study, ginger rhizome slices were subjected to airdrying (AD), freeze drying (FD), infrared drying (IR), microwave drying (MD) and intermittent microwave & convective drying (IM&CD). Quality attributes of the dried samples were compared in terms of volatile compounds, 6, 8, 10-gingerols, 6-shogaol, antioxidant activities and microstructure. Results showed that AD and IR were good drying methods to preserve volatiles. FD, IR and IM&CD led to higher retention of gingerols, TPC, TFC and better antioxidant activities. However, FD and IR had relative high energy consumption and drying time. Therefore, considering about the quality retention and energy consumption, IM&CD would be very promising for thermo sensitive material. Ó 2015 Elsevier Ltd. All rights reserved.

Keywords: Intermittent microwave & convective drying Volatiles Antioxidant activity Microstructure Ginger

1. Introduction Ginger, one of the most ancient spices in the world, has been widely used as a spice or a common condiment for a variety of compound food and beverages (Larsen, Ibrahim, Khaw, & Saw, 1999). It is also an important medicine for treating cold, stomach upset, diarrhea, and nausea. Phytochemical studies show that gin⇑ Corresponding author at: Sericulture and Agri-Food Research Institute, Dong Guanzhuang Yiheng RD., Tianhe District, Guangzhou 510610, PR China. E-mail address: [email protected] (G. Xiao).

ger has antioxidant and anti-inflammatory activities, and some of them exhibit potential cancer preventive activity (Shukla & Singh, 2007; Stoilova, Krastanov, Stoyanova, Denev, & Gargova, 2007; Thomson et al., 2002). The characteristic components of ginger include essential oil and oleoresin, which are responsible for its fragrant and pungent behavior, respectively. Essential oil mainly consists of monoterpenoid and sesquiterpene hydrocarbons, whereas oleoresin is composed of non-volatile phenolics known as gingerols, shogaols and zingerone (Huang, Wang, Chu, & Qin, 2012). The gingerols are identified as the major active components in fresh ginger. Shogaol series of compounds do not intrinsically

http://dx.doi.org/10.1016/j.foodchem.2015.11.033 0308-8146/Ó 2015 Elsevier Ltd. All rights reserved.

Please cite this article in press as: An, K., et al. Comparison of different drying methods on Chinese ginger (Zingiber officinale Roscoe): Changes in volatiles, chemical profile, antioxidant properties, and microstructure. Food Chemistry (2015), http://dx.doi.org/10.1016/j.foodchem.2015.11.033

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K. An et al. / Food Chemistry xxx (2015) xxx–xxx

exist in fresh sample, as they are derived from the corresponding gingerols during thermal processing or long-term storage. Generally, the degradation of gingerol to shogaol takes place either because of the acidic environment or as a result of the increase in temperature (Kubra & Rao, 2012). Studies also have proven that shogaols are more pungent, and exhibit higher antioxidant activity than gingerols (Guo, Wu, Du, Zhang, & Yang, 2014). Fresh gingers usually contain 85–95% of water and are susceptible to microbial spoilage and chemical deterioration (Mishra, Gauta, & Sharma, 2004). Dehydration of ginger is the most practiced processing procedure to inhibit microbial growth and delay deteriorative biochemical reactions. It is also a fundamental processing method to obtain new products. Dried ginger can be utilized for manufacturing ginger spices, medicine and cosmetics as well as food with ginger flavor such as soft drinks and candies. However, drying process may cause thermal damage and severe changes in physical, chemical and organoleptic properties of aromatic plant. Therefore, the selection of drying method is very important. According to Mujumdar and Law (2010), drying technologies have attracted significant research and development efforts because of the growing demand for better product quality and lower operating cost, as well as lessened environmental impact. The most conventional drying method is hot air drying (AD), however, its high temperature and long drying cycle usually result in the degradation of important flavor, color and nutritional compounds. Freeze drying (FD) can yield high quality products, but it also leads to high energy consumption, high capital cost and long drying time. Microwave drying (MD) and infrared radiation (IR) have their own place in drying technology, due to the same transfer direction of temperature and moisture, they can offer many advantages such as great energy efficiency and high heat transfer rate. IR has more advantages in uniform heating and high quality of final products (Sellami et al., 2013). Although MW heating can readily deliver energy to generate heat within foods, one of its major drawbacks is the inherent non-uniformity of the electromagnetic field (Zhang, Tang, Mujumdar, & Wang, 2006). Since its local temperature can easily rise to a level that causes scorching, microwave drying usually has been combined with other techniques including convective hot-air, vacuum, and intermittent power application to achieve more uniform, high quality and effective drying (Gunasekaran, 1999; Kaensup, Chutima, & Wongwises, 2002; Soysal, Ayhan, Esßtürk, & Arıkan, 2009). Microwave-convection drying includes two kinds of form, one is microwave and air convection drying conducted in stages, the other being these two dryings carried out simultaneously. In our study, the second form was adopted. In microwave combined convection drying, microwave energy removes the inner moisture of material to the surface and convective air helps removing the surface moisture out of drying chamber, which not only increases the energy efficiency but also reduces the surface temperature of material. Intermittent application of microwave energy has proven itself a good method to avoid uneven heating, improve product quality and increase energy utilization by allowing redistribution of temperature and moisture profiles within the product during off times (Gunasekaran, 1999). Many authors have studied the variations of volatiles, nonvolatiles or antioxidant capacity of ginger induced by drying process. Huang et al. (2012) studied the effects of oven drying, microwaving drying, and silica gel drying methods on the volatile components of ginger and found that microwave and silica gel can be used in drying of ginger to maintain the taste and appearance of fresh ginger. Bartley and Jacobs (2000) reported that the major effects of drying process on ginger are the reduction in gingerol content, increase in terpene hydrocarbons and conversion of some monoterpene alcohols to their corresponding acetates. Gümüsßay,

Borazan, Ercal, and Demirkol (2015) studied thermal dryings and freeze drying (FD) for ginger in terms of total phenolic content (TPC), ascorbic acid (AA) and antioxidant capacity. He found freeze dried gingers have better antioxidant properties than samples treated by thermal dryings. Yet so far there is no systematic investigation regarding the effects of drying methods on energy consumption, volatile and non-volatile components, antioxidant capacity, and microstructure of ginger at the same time. The objective of this work was to explore the possibility of using intermittent microwave combined convection drying (IM&CD) for processing of ginger product. Therefore, an investigation was build on the comparison of different drying methods, namely, AD, IR, FD, MD and IM&CD on the energy consumption and quality conservation of ginger. 2. Materials and methods 2.1. Reagent and chemicals Acetonitrile and methanol (HPLC grade) were purchased from Honeywell (Morris, NJ, USA). Authentic standards of 6-, 8-, 10gingerol and 6-shogaol were purchased from Chromadex Inc. (Irvine, CA, USA). Analytical grade chemicals: Folin–Ciocalteu reagent; gallic acid; ascorbic acid; 2,2-diphenyl-1-picrylhydrazyl (DPPH); 2,20 -azinobis (3-ethylbenzo thiazoline-6-sulfonic acid) diammonium salt (ABTS); 2,4,6-tripyridyl-s-triazine (TPTZ) were procured from Sigma–Aldrich (St. Louis, MO, USA). Metaphosphoric acid, sodium carbonate, potassium persulfate and glacial acetic acid were from National Pharmaceutical Corporation (Beijing, China). 2.2. Samples The fresh matured gingers (Shandong Laiwu variety) were purchased from China Agricultural University regional market, in March, 2013. Voucher specimens were preserved at 4 °C before drying. Raw ginger rhizomes were washed to detach the dirt and sand adhering to them and blotted up with filter paper to remove the excess water. Then gingers were cut into cylinder slices with thickness of 4 ± 0.2 mm and diameter of 34 ± 2.0 mm. The initial moisture was determined by using a vacuum oven at 70 °C with 13.3 kPa, until the weight of samples was constant. Gingers used for experiment were from the same batch. 2.3. Drying of the ginger rhizomes 150 g ginger slices were spread out evenly and subject to five different drying methods, and drying was last until the ginger moisture content reached to 0.12 ± 0.02 g H2O/g d.w. 2.3.1. Hot-air drying (AD) Ginger slices were dried in an electric thermo static drying oven (DHA-9070A; Shanghai Jinghong Experiment Instrument Co., Shanghai, China) at 60 °C. 2.3.2. Infrared drying (IR) Ginger slices were put into an infrared radiation chamber (Senttech Infrared Technology Co., Ltd. Taizhou, China) with three red glass lamps (225 W each). 2.3.3. Freeze drying (FD) Ginger slices were first frozen at 40 °C for 12 h, and then were quickly placed into a freeze dryer (LGJ-25C; Beijing Si Huan Scientific Instrument Factory Co., Beijing, China) and dried under 20 Pa



absolute pressure. The temperature of the heating plate and the cold trap were at 25 and 58 °C. 2.3.4. Microwave drying (MD) Ginger slices were dried in a microwave oven (NJ07-3; Nanjing Jiequan Microwave Apparatus Co. Ltd., Nanjing, China) with an initial energy density of 5 w/g until moisture content reached to 50% w.b. (1.0 g H2O/g d.w.), then dried samples with 1 w/g to the terminal point. 2.3.5. Intermittent microwave-convection drying (IM&CD) Ginger slices were dried in laboratory-setup microwave oven with an output of 700 W and hot air drying of 60 °C, including a control unit for microwave pulse ratio (PR) regulation. Fresh samples were first dried at initial PR = 2 (5 s on–5 s off) to 50% w.b., then adjusted PR = 6 (5 s on–25 s off) to the end of drying. The whole drying process was assisted with hot air. After each drying, the samples were ground into powder form sieved with 60 mesh wire screen and kept in dark and dry place for further analysis. 2.4. Preparation of extract for determination of volatile composition The volatile components of ginger were extracted by solidphase micro-extraction (SPME) method. The SPME manual device (Supelco Co., Bellefonte, PA) was equipped with a fused silica fiber coated with polydimethylsiloxane (PDMS). 1.0 g ginger powder was placed in a 15-mL vial and sealed. The fiber was inserted into the headspace for 30 min at 40 °C water bath, then it desorbed at 250 °C for 3 min in the injection port of an Agilent GC–MS (7890A-5975C). 2.5. Determination of volatile flavor composition Analysis of volatiles was according to the procedure described by Ding et al. (2012) with modifications. The aroma compounds were identified using an Agilent J&W DB-5 column (30 m 0.25 mm 0.25 lm). The oven temperature programme was as follows: 50 °C (held for 3 min), then raised to 120 °C at a rate of 4 °C/min (held for 8 min), then heated to 200 °C at 4 °C/ min (held for 3 min) and finally increased to 250 °C at 10 °C/min (held for 3 min). Helium was used as the carrier gas at a flow rate of 1.0 mL/min. The split ratio was 1:60. The MS fragmentation was performed by electronic impact (EI) at 70 eV, a source temperature of 230 °C, scanning rate of 1 scan s1 and mass acquisition range of 35–550 Da. The compounds were identified using the Wiley and NIST libraries (Washington, DC), and also by matching against the published data (Bartley & Jacobs, 2000; Ding et al., 2012; Nirmala Menon et al., 2007). Compounds whose similarity is more than 78 were reported here. The relative amounts present were calculated on the basis of peak-area ratios. 2.6. Preparation of extract for the determination of HPLC analysis and antioxidant activity Extracts were prepared according to the procedure described by Chan et al. (2008). The ginger powder 5 g was accurately weighed and placed into a beaker, then 30 mL of 80% aqueous methanol was added. Ginger was ultrasonically extracted three times for 30 min each time and filtered. Methanol was removed by drying at 40 °C in a rotary evaporator. After concentration, the extract was transferred to a 50 mL volumetric flask and made up to the volume using 80% methanol. The solution was filtered through 0.45 lm organic membrane filter to an auto sampler vial for HPLC analysis. Similarly, 10 g of each fresh ginger sample was homogenized with

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30 mL 80% methanol using a breaking pulper (JYL-CO51 type, Joyoung Company, Beijing, China). The extraction procedure was repeated. 2.7. Determination of 6, 8, 10-gingerol and 6-shagaol by HPLC method HPLC analysis was performed on an Agilent 1100 liquid chromatography system, chromatographic separation was carried out according to the method of Cheng, Liu, Peng, Qi, and Li (2011). The chromatographic separation was carried out using the RF10AXL HPLC system (Shimadzu Co., Japan). The column used was a reverse phase column (SunfireTM C18, 4.6 250 mm i.d., 5 lm). The mobile phase was prepared from water (A) and acetonitrile (B). The gradient program for the HPLC was as follows: 0–5 min, 0–20% B; 5–45 min, 20–90% B; and 45–55 min, 100% B. The flow rate was 1 mL min1, the injection volume was 20 lL, and the column temperature was maintained at 30 °C. The detection wavelength was set at 280 nm. 2.8. Determination of total phenolic content (TPC) TPC of ginger was determined using the Folin–Ciocalteu assay according to Singleton, Orthofer, and Lamuela-Raventos (1999). Samples (400 lL) were introduced into test tubes followed by 2.0 mL of Folin–Ciocalteu phenol reagents (10 times dilution with deionized water). After 5 min, 3.0 mL of sodium carbonate (7.5% w/v) solution was added to the mixture. The absorbance was measured at 765 nm using a spectrophotometer (UV-726, Shimadzu, Shanghai, China) after 2 h reaction in darkness. 400 lL 80% methanol was added instead of sample taken as blank. The amount of total phenolics was expressed as gallic acid equivalents (GAE, mg/g of dry sample). 2.9. Determination of total flavonoid contents (TFC) The TFC was measured according to the method of Dewanto, Wu, Adom, and Liu (2002) with small modifications. Diluted solutions of extracts of dried ginger 2 mL were put in a 10 mL volumetric flask. Initially, 5% NaNO2 0.3 mL was added to the volumetric flask, after 6 min, 10% AlCl36H2O 0.3 mL was added, after 6 min, 4% NaOH 2 mL was added. Water (5.4 mL) was added to the reaction flask after 15 min and mixed well. Absorbance of the reaction mixture was read at 510 nm. 400 lL 80% methanol was added instead of sample taken as blank. TFC were determined as rutin equivalents (mg/g of dry weight). 2.10. Determination of DPPH radical scavenging assay This assay is based on the measurement of the scavenging ability of antioxidants towards the stable radical DPPH. It was conducted according to Lim and Murtijaya (2007) with modifications. Different dilutions of extract 0.4 mL were added to 3.5 mL of 0.14 m mol/LDPPH solution in methanol and shaken vigorously. The mixture was allowed to stand for 30 min before measuring the absorbance at 517 nm. Results were also expressed as IC50 and ascorbic acid equivalent antioxidant capacity (AEAC). IC50 of the extract was determined from the graph of antioxidant activity (%) against amount of extract (mg). Antioxidant activity was expressed using the equation:

AA% ¼

Abscontrol Abssample =Abscontrol 100

where control: 3.5 mL 0.14 mM DPPH + 0.4 mL 80% methanol; sample: 3.5 mL 0.14 Mm DPPH + 0.4 mL extract. AEAC in mg ascorbic acid/100 g of fresh material with following equation:


4


AEAC ðmg ascorbic acid=100gÞ ¼ The IC50

ascorbic acid

IC50 ðascorbic acidÞ 105 IC50 ðsampleÞ

used was determined to be 0.00387 mg/mL.

2.11. Determination of ferric-reducing antioxidant power (FRAP) The FRAP assay was performed according to the method reported by Kubra and Rao (2012). The stock solution included 300 Mm acetate buffer (5.1 g C2H3NaO23H2O and 20 mL C2H4O2) at pH 3.6, 10 mM TPTZ (2,4,6-tripyridyl-s-triazine) solution in 40 mM HCl, and 20 Mm FeCl36H2O solution in distilled water. Then acetate buffer 25 mL and TPTZ 2.5 mL were mixed together with FeCl36H2O 2.5 mL. The temperature of the solution was raised to 37 °C before it was used. Ginger extracts 100 lL were allowed to react with the FRAP solution 4.0 mL for 10 min under 37 °C. The ferric reducing ability was measured by monitoring the absorbance at 593 nm and the FRAP solution was used as blank. Results of the FRAP assay were expressed as mg ascorbic acid/g. 2.12. Determination of ABTS antioxidant activity The ABTS antioxidant activity was carried out using the ABTS+ radical cation decolorization assay followed the method of Sogi, Siddiq, Greiby, and Dolan (2013) with some modifications. ABTS stock solution was dissolved in sodium acetate–acetic acid buffer (20 Mm pH = 4.5) to make a 7 mM ABTS stock solution. 7 mM ABTS solution and 2.45 mM potassium persulfate were mixed in 1:1 ratio and allowed to stand in the dark for 12–16 h to produce ABTS+ working solution. This solution was further diluted with 80% methanol to reach the absorbance of 0.70 ± 0.02 at 734 nm. The ABTS+ working solution 3.6 and 0.4 mL of extracts were mixed and the absorbance was measured at 734 nm after 30 min in the dark. The blank was run with 80% methanol. A standard curve was prepared using Trolox solution (30–90 lg/mL). 2.13. Microstructure of dried ginger Microstructure changes of ginger during different drying process were analyzed using a scanning electron microscope (Phenom-World BV, Eindhoven, The Netherlands). To obtain the SEM images, 5 5 5 mm3 small pieces were taken from both the inner parts and surface of dried ginger slices, then glued on the metal stub, each specimen was coated with a very thin layer of gold under high vacuum. 2.14. Statistical analysis Experiment data were analyzed using Origin 8.0 (Microcal Software, Inc., Northampton, USA) and Spss18.0 (Chicago, IL, USA). Significant differences between samples were analyzed using analysis of variance (ANOVA) and Duncan’s multiple-range test (P < 0.05). Principal composition analysis (PCA) and cluster analysis were conducted using Spss18.0 (Chicago, IL, USA). All experiments were run in triplicate, and data were reported as the mean ± standard deviation (SD). 3. Results and discussion 3.1. Comparison of drying time, energy consumption and extraction yield of different dried gingers The drying time, energy consumption and extraction yield were different in the selected drying techniques. As shown in Table 1, FD had the longest drying time and highest energy consumption, with drying time of 44.5 ± 2.0 h and energy consumption of

33.7 ± 0.53 kW h/g H2O. Air-dried samples went through the second longer drying time of 12.0 ± 0.5 h, but its energy consumption was relatively low, 3.30 ± 0.08 kW h/g H2O. The second large energy consumption was IR process with the drying time of 6.0 ± 0.7 h. MD and IM&CD had both lower drying time and energy consumption compared with other drying methods, while IM&CD had lower drying time but higher energy consumption than MD. In terms of extraction of yield, FD samples had the highest yield, followed by IM&CD, MD, AD and IR samples. According to Asami, Hong, Barret, and Mitchell (2003), freeze drying has higher extraction efficiency due to the rupture of cell structure caused by ice crystals formed within plant matrix. In general, IM&CD had lower drying time, lower energy consumption and higher extraction of yield. 3.2. Effect of drying process on volatile components composition In the analysis of fresh ginger, 48 compounds were extracted and identified (Supplementary Table 1). The main compounds of the fresh ginger were zingiberene (22.76%), b-phellandrene (12.40%), b-sesquiphellandrene (7.01%), geranial (14.50%), a-curcumene (2.78%) and b-bisabolene (3.25%) (Supplementary Table 2). The relatively high content of zingiberene and b-phellandrene are account for the odor of the fresh ginger, which was consistent with the result of Huang et al. (2012). However, Bartley and Jacobs (2000) have reported that main flavor fractions of Australian-grow ginger were geranial, zingiberene, zingerone and (E,E)-a-farnesene. Nishimura (1995) adopted n-hexane to extract the characteristic odorants in fresh ginger and found that linalool, geraniol, geranial, neral and isoborneol presented high value in flavor factors. The differences in the main volatile composition may be attributed to the different origins of ginger, methods of extraction and kinds of solvents used (Ding et al., 2012). Different drying methods resulted in different changes of the volatile compounds, but there was a same trend after drying that the relative percentage of sesquiterpenes compounds (zingiberene, b-sesquiphellandrene, a-farnesene, and a-curcumene) showed considerable increase while monoterpenes (b-phellandrene, camphene) decreased significantly. This could be attributed to the synthesization of short-chain alkenes and isomerization of similar compounds. In the hot-air drying of 60 °C, 49 compounds were found. It was worth noting that the concentrations of zingiberene, a-curcumene, b-bisabolene, b-sesquiphellandrene and a-farnesene were lower compared with other dried samples (Supplementary Table 2). This was possibly owing to long exposure to high temperature air resulting in the degradation of sesquiterpenes to monoterpenes. We also found many esters such as Propanoic acid, 2-methyl-, 3,7-dimethyl-2,6-octadienyl ester and bornyl acetate were only formed in hot air drying. This was attributed to long time exposure to oxygen promoting the esterification of alcohols to corresponding esters, which was also proved by Ding et al. (2012). In the IR drying, 47 compounds were extracted and identified. We found appearance of many new volatile compounds and disappearance of original compounds (Supplementary Table 1). According to Sellami et al. (2011), IR drying of Laurus nobilis leaves at 65 °C may cause oxidation process and chemical rearrangements, which may also explain the phenomenon we found in ginger. We also found that IR drying preserved the levels of sesquiterpenes (zingiberene, b-sesquiphellandrene, b-bisabolene and a-curcumene), which was proved by Yoshikawa et al. (1993). In microwave, the concentrations of major sesquiterpenes were well retained, even marginally increased as well as the concentrations of monoterpenes (b-phellandrene, camphene, 1s-a-pinene). This indicated that higher temperature inside the products would accelerate the release of volatile compounds owing to cell damage, which was consistent with the report of Kubra and Rao (2012).


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K. An et al. / Food Chemistry xxx (2015) xxx–xxx Table 1 Drying time, energy consumption and extraction yield of different dried gingers. Drying methods Drying time (h) Energy consumption (kW h/g H2O) Extraction yield (v/w%)

AD

IR b

12.0 ± 0.5 3.30 ± 0.08c 2.69 ± 0.32cd

FD c

MD a

6.0 ± 0.7 12.23 ± 0.24b 2.58 ± 0.19d

IM&CD d

44.5 ± 2.0 33.7 ± 0.53a 3.55 ± 0.22a

1.5 ± 0.2e 3.21 ± 0.1d 3.35 ± 0.55b

1.8 ± 0.3 2.7 ± 0.12e 2.97 ± 0.65c

AD: hot air drying; IR: infrared drying; FD: freeze drying; MD: microwave drying; IM&CD: intermittent microwave-convection drying. Values are means ± SD (n = 3). For each column, values followed by the same small or capital superscript letter did not share significant differences at P < 0.05 (Duncan’s test).

There were 41 and 43 compounds detected in FD and IM& CD dried gingers, indicating the two processes decreased the varieties of total volatiles significantly. Though former research reported freeze drying was an optimal technique for volatile retention (Liapis & Bruttini, 1995), we found the long vacuum treatment of FD changed the categories and quantities of ginger volatiles significantly. In the IM&CD process, volatile compounds were also greatly affected. According to Sellami et al. (2011), many volatiles have more affinity to the water fraction contained in plant samples and were lost accompanied with evaporating water during drying process. Thereby, in the IM&CD process, microwave accelerates the release of volatile compounds and hot air speeds up the evaporation of surface moisture, which increase the loss of volatile compounds. Cluster analysis was carried out to characterize the correlation between different drying methods (Fig. 1). The longer euclidean distance, the lower similarities of the samples are. As shown in Fig. 1, AD had shortest euclidean distance with fresh samples, followed by IR, MD, FD and IM&CD. The dendrogram indicated that drying methods could be regrouped into three clusters. The first cluster included AD and IR, with shorter euclidean distance of 26.13 (Supplementary Table 3). The second cluster was composed of FD, IM&CD and MD, with the most similar profiles of FD and IM &CD. The third cluster consisted of MD, AD and IM &CD. Therefore, AD is the most preferable method, followed by IR and MD, while FD and IM &CD were not advisable drying methods for volatile preservation of ginger. In general, the mild heating process led to less impact on the volatile components, despite its long treatment time, whereas the intense drying method exerted significant effect on volatiles. In addition, the vacuum treatment also had substantial influence

on volatile compounds. Based on above findings, more work is required to improve the effect of IM&CD on ginger volatiles. 3.3. Effect of drying methods on the quantities of 6-, 8-, 10-gingerol and 6-shogaol of ginger extract The major pharmacologically active and pungent components of ginger are 6-gingerol, 8-gingerol, 10-gingerol and 6-shagaol (Yu, Huang, Yang, Liu, & Duan, 2007). Molecular structure of gingerol consisted of b-hydroxyl keto functional group which is thermally labile (Puengphian & Sirichote, 2008). According to Huang, Chung, Wang, Law, and Chen (2011), the higher drying temperature would promote the decomposition of 6-gingerol or the transformation of 6-gingerol to 6-shogaol. As shown in Fig. 2, the quantity of 6-gingerol was 5.91 mg/g in fresh ginger, after drying, the 6-gingerol was decreased significantly, especially in microwave drying, only 2.12 mg/g. FD samples had a higher content of 3.54 mg/g, followed by IR, IM&CD and AD samples of 3.44, 3.21 and 2.50 mg/g respectively. It can be inferred that the high temperature and long drying time would promote the degradation and conversion of 6-gingerol. The quantity of 8-gingerol and 10gingerol also showed decreasing trend after drying process except for FD process. As shown in Fig. 2, 8-gingerol and 10-gingerol were 2.52 and 2.62 mg/g in fresh ginger, 2.52 and 2.74 mg/g in FD samples, and there was no significant differences between fresh and FD samples. IR, IM&CD, AD and MD samples were with average content of 8-gingerol and 10-gingerol of 2.48 and 2.52 mg/g, 2.43 and 2.5 mg/g, 2.15 and 2.33 mg/g, and 1.35 and 1.05 mg/g. It indicated that 8-, 10-gingerol were much more stable than 6-gingerol during drying, except in the intense heating process of MD, whose higher temperature accelerated the decomposition

6-gingerol 8-gingerol 10-gingerol 6-shogoal

a

6

Content (mg/g d.w.)

5 4

bc

b

a

c c

3

b

a

bb

e

2

d

d

1

a

b

0 Fresh

AD

IR

FD

MD

IM&CD

Drying methods

Fig. 1. Ward connection spectrum of the similarity of total volatile components between different drying methods.

Fig. 2. The changes of 6-, 8-, 10-gingerol, and 6-shogaol content of ginger extract during AD, IR, FD, CM and IM&CD drying process. AD: hot air drying; IR: infrared drying; FD: freeze drying; MD: microwave drying; IM&CD: intermittent microwave-convection drying. For each column, values followed by the same letter (a–c) are not statistically different at P < 0.05 as measured by Duncan’s test.


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the conclusion that drying process results in high or low levels of TPC depending on the type of plant material and the location phenolic compounds present in the cell. In terms of TFC, it had a different trend with TPC. TFC of fresh ginger was 13.49 ± 0.36 mg Rutin/g, after drying, IM&CD led to highest TFC of 15.42 ± 0.87 mg Rutin/g, followed by IR samples with 14.52 ± 0.23 mg Rutin/g (Table 2). It worth noting that freeze dried samples had lower TFC than IM&CD and IR samples, and there was no significant differences between FD and fresh samples. MD caused a loss of TFC of 6.97%, while AD caused the highest loss of 10.45%, which confirmed that the loss of such macromolecules might be caused by the combination of the duration and temperature (Schieber, Keller, & Carle, 2001). According to Toor and Savage (2006), IM&CD has the penetrability of microwave radiation, which would cause the breakdown of cellular constituents, making flavonoids more accessible during the extraction. Besides, the shorter duration and less intense heating of IM&CD make it more advantageous in preserving flavonoids. According to Niwa, Kanoh, Kasama, and Neigishi (1988), far infrared may have the capability to break down covalent bonds and liberate antioxidants such as flavonoids, polyphenols carotene, tannin, ascorbate or flavoprotein from repeating polymers, which would increase TFC in IR dried samples.

and transformation of 8-gingerol and 10-gingerol significantly. As shown in Fig. 2, the content of 6-shogaol was 0.09 mg/g in fresh ginger, then increased to 0.214, 0.209, 0.221, 0.384 and 0.243 mg/g after AD, IR, FD, MD and IM&CD process. This phenomenon proved that 6-shogaol was normally not present in fresh ginger but dehydrated from gingerols during thermal drying or storage (Bhattarai, Tran, & Duke, 2001). We can see microwave drying resulted in the largest increase of 6-shogaol, followed by IM&CD, indicating that higher temperature would be advantageous for conversion of gingerol to shogaol, which was agreed with the reported of Huang et al. (2011) and Cheng et al. (2011). We have measured the temperature changes of ginger in the entire MD and IM&CD process, and found that temperature in IM&CD process was much lower and more stable than that in MD process, especially at the end of drying (data were shown in Supplementary Fig. 2), which can well explain that why IM&CD had better retention of chemical profiles than MD process.

3.4. Effect of drying methods on the total phenolic, flavonoids content of ginger extract Different drying treatments were shown variable effects on total phenolic (TPC) and total flavonoids content (TFC) of ginger samples. As shown in Table 2, the content of TPC in fresh ginger was 11.97 ± 0.33 mg GAE/g d.w., which is similar to the report of Gümüsßay et al. (2015), who found the TPC of ginger from Turkey was 13.51 ± 0.62 mg GAE/g d.w. There were many researchers who got different results (Hinneburg, Damien, & Hiltunen, 2006; Puengphian & Sirichote, 2008). These differences were possibly due to different genetics, varieties and regions of ginger. In our study, the TPC of freeze dried gingers was increased significantly compared with fresh ones, while other thermal drying caused a significant decrease in TPC (P < 0.05). According to Asami et al. (2003), the increased extraction efficiency would promote the extraction of active ingredients in dried samples, which would increase the content of total phenols detected in FD samples. In the thermal drying, IR, IM&CD and AD process resulted in losses of TPC of 5.17%, 5.76% and 19.05%, respectively, and MD caused a highest loss of 29.74%. According to Lim and Murtijaya (2007), heat generated from microwave drying was intense and rapid, which could cause severe thermal degradation of phenolic compounds. Besides, activation of oxidative enzymes (polyphenoloxidase and peroxidase) during drying process may lead to the loss of phenolic complexes. According to Toor and Savage (2006), changes in chemical structure of phenols, such as bingings of phenols to proteins could also result in a loss of phenolic content. However, Kubra and Rao (2012) observed an increase in TPC of MW-dried gingers with MW power levels (385–800 W) increased. He explained that this was ascribed to MW energy causing breakdown of cellular constituents, resulting in higher release of polyphenols from the matrices. Many researchers have found that TPC in various plant spices have irregular change under different drying process (Chan et al., 2008; Dewanto et al., 2002). Therefore, we can get

3.5. Effect of drying methods on the antioxidant activity of ginger extract In the present study, antioxidant activity of ginger extracts was evaluated using DPPH, FRAP and ABTS assay. The DPPH free radical is a stable free radical, which has been widely accepted as a tool for estimating the free radical-scavenging activity of antioxidants. In the DPPH test, the highest AEAC value (lowest IC50) was observed in freeze dried samples, followed by IM&CD (3.58 ± 0.11 mg AA/ g d.w., IC50 1.08 ± 0.03 mg/mL extract), IR (3.55 ± 0.14 AA mg/g d. w., IC50 1.09 ± 0.02 mg/mL extract) and MD (3.42 ± 0.19 AA mg/ g d.w., IC50 1.13 ± 0.06 mg/mL extract) samples, whereas AD method gave the lowest free radical scavenging ability (Table 2). The DPPH scavenging ability had higher correlation with TPC (R2 = 0.866), and less correlation with TFC (R2 = 0.594). Many researchers have found the high correlations between TPC, TFC and antioxidant activity (Velioglu, Mazza, Gao, & Oomah, 1998), whereas others found there was no relationship (Kähkönen et al., 1999). As shown in Table 2, the highest FRAP value (22.14 ± 0.27 g Vc/ g d.w.) was observed in IR dried samples, followed by IM&CD (21.91 ± 0.54 Vc g/g d.w.), FD (20.88 ± 1.19 Vc g/g d.w.), and AD (17.41 ± 1.78 Vc g/g d.w.) samples, whereas the microwave drying was found to exert the most negative effect. FRAP value had high correlation with TPC (R2 = 0.741) and TFC (R2 = 0.850). The values of ABTS obtained in terms of Trolox equivalent were lower than those obtained by the FRAP assay but the overall trend was similar (Table 2). The highest antioxidant capacity was found in IM&CD samples, followed by FD, IR, and AD samples, whereas the microwave drying also exerted lowest antioxidant capacity.

Table 2 Changes of total phenolic, flavonoids content, and antioxidant activity of ginger during AD, IR, FD, CM and IM&CD.

TPC (mg GAE/g d.w.) TFC (mg Rutin/g d.w.) IC50 (mg/mL extract) AEAC (mg AA/g d.w.) FRAP (g Vc/g d.w.) ABTS (mg Trolox/g d.w.)

Fresh

AD

IR

FD

MD

IM&CD

11.97 ± 0.33b 13.49 ± 0.36c 1.11 ± 0.05c 3.49 ± 0.27c 19.37 ± 0.81d 64.45 ± 5.15d

9.69 ± 0.54d 12.08 ± 1.17d 1.15 ± 0.09a 3.37 ± 0.23d 17.41 ± 1.78e 62.22 ± 3.21e

11.35 ± 0.66c 14.52 ± 0.23b 1.09 ± 0.02d 3.55 ± 0.14b 22.14 ± 0.27a 66.79 ± 4.40c

13.83 ± 0.31a 13.32 ± 0.52c 1.05 ± 0.11e 3.69 ± 0.21a 20.88 ± 1.19c 68.65 ± 11.55b

8.41 ± 0.35e 12.55 ± 0.74d 1.13 ± 0.06b 3.42 ± 0.19d 15.66 ± 1.21f 60.06 ± 14.43f

11.28 ± 0.40c 15.42 ± 0.87a 1.08 ± 0.03d 3.58 ± 0.11b 21.91 ± 0.54b 71.68 ± 6.11a

AD: hot air drying; IR: infrared drying; FD: freeze drying; MD: microwave drying; IM&CD: intermittent microwave-convection drying. Values are means ± SD (n = 3). For each column, values followed by the same small or capital superscript letter did not share significant differences at P < 0.05 (Duncan’s test).



ABTS value also presented high correlation with TPC (R2 = 0.710) and TFC (R2 = 0.848). 3.6. Morphology of fresh and dried Zingiber officinale Roscoe Structures of fresh ginger were observed by light microscopy (LM). As shown in Fig. 3A, an oil cell appeared in ginger tissue structure. According to Azian, Mustafa Kamal, and Azlina (2004), for a fresh ginger tissue of 220 220 lm there appeared an oil cell with the size of 25 25 lm. As shown in Fig. 3B, abundant starch grains were present within the fresh ginger tissue. Both micrographs of (A) and (B) showed distinct wall of the parenchyma indicating no cell fracture of the fresh tissue. Structural changes of dried gingers were observed by scanning electron microscope (SEM) shown in Fig. 3a–e. In general, dehydration caused fractures of parenchyma cell wall, the oil cell was absent and the starch grains were scattered all over the tissue after drying. As shown in Fig. 3a, air-dried ginger showed more dense structures, the cell parenchyma structure was severely damaged and the starch grains were not well preserved. In the freeze drying, as shown in Fig. 3c, the skeleton structure of ginger was well retained because the removal of water occurs by sublimation from frozen substances with the simultaneous effect of the vacuum. Therefore, the freeze dried samples had less-dense texture and relative complete cell structure, which was agreed with the observation of Huang et al. (2011). In the microwave drying, due to the rapid conversion of microwave radiation, the inner moisture was difficult to evaporate outside. Therefore, the accumulated inner moisture caused cellular structures crosslinked together and starch grains showed a higher degree of gelatinization (Fig. 3d). In the IR

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and IM&CD samples (Fig. 3b and e), the cellular structures were well retained and much similar to that of freeze dried samples. Starch grains were preserved intact and showed little degree of gelatinization. This was because of the less intense heating and shorter duration of IR and IM&CD.

3.7. Principal component analysis Principal component analysis (PCA) was applied to observe any possible clusters within these five drying methods. The clustering variety was considered caused by the entire physico-chemical and antioxidant properties. As shown in Fig. 4, the cumulative contribution of the first and the second principal components attained 97.99%. PC1 was highly contributed by 6-gingerol (0.818), 8-gingerol (0.718), 10-gingerol (0.610), 6-shogaol (0.466), TPC (0.797), TFC (0.975), AEAC (0.712), FRAP (0.942) and ABTS (0.907). PC2 was mainly correlated to drying time (0.996), energy consumption (0.964), extraction yield (0.551). The PC1 and PC2 scores of FD were found to be much higher than other drying methods as it had higher content of 6, 8, 10-gingerol, 6-shogaol, TPC, TFC, higher antioxidant activities and higher extraction yield at the cost of higher drying time and energy consumption. MD was highly negatively correlated with both PC1 and PC2, as it had negative effects on active component content and antioxidant activity with less drying time and energy consumption. It was worth noting that IM&CD and IR could be clustered into one group as they had highly positive correlations with PC1, indicating they had very good impact on physicochemical and antioxidant properties.

Fig. 3. Light microscopy image of fresh ginger: (A) (250); B (400); scanning electron micrographs of dried gingers: (a) AD (1000); (b) IR (1000); (c) FD (500); (d) MD (200); (e) IM&CD (1000). AD: hot air drying; IR: infrared drying; FD: freeze drying; MD: microwave drying; IM&CD: intermittent microwave-convection drying.


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Fig. 4. Principal component analysis plot of data from different physic-chemical and antioxidant properties of ginger from five drying methods.

4. Conclusions Based on the results of present investigation, we conclude that drying methods and conditions have profound effect on the quality and energy consumption of the dehydrated product. Compared with AD and MD process, FD, IR and IM&CD had higher retention of chemical profiles, antioxidant activity and cellular structures, which was attributed to their less intense heating. However, FD and IR had relatively higher energy consumption and drying time, especially freeze drying. Therefore, IM&CD is a very promising technology for high sensitive products like fruits and vegetables due to its higher efficiency, good quality retention and lower cost, which had a broad market prospect for commercial-scale application. Acknowledgments Special thanks were given to Prof. Wang Zhengfu for his technical support of the intermittent microwave & convective drying equipment and helpful recommendations for the experiment. We also thank the financial support of Province Natural Science Fund of Guangdong (2014A030310208) and Province Science and Technology Plan Projects of Guangdong (2013B020203001) for this research. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.foodchem.2015. 11.033. References Asami, D. K., Hong, Y. J., Barret, D. M., & Mitchell, A. E. (2003). Comparison of the total phenolic and ascorbic content of freeze-dried and air dried marionberry, strawberry, and corn grown using conventional, organic and sustainable agricultural practices. Journal of Agricultural and Food Chemistry, 51, 1237–1241. Azian, M. N., Mustafa Kamal, A. A., & Azlina, M. N. (2004). Changes of cell structure in ginger during processing. Journal of Food Engineering, 62, 359–364.

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