Effects of simultaneous UV-C radiation and ultrasonic energy postharvest treatment on bioactive compounds and antioxidant activity of tomatoes during storage

Food Chemistry 270 (2019) 113–122

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Effects of simultaneous UV-C radiation and ultrasonic energy postharvest treatment on bioactive compounds and antioxidant activity of tomatoes during storage

T

⁎

Okon Johnson Esuaa,c, Nyuk Ling China, , Yus Aniza Yusofa, Rashidah Sukorb a

Department of Process and Food Engineering, Universiti Putra Malaysia, Serdang, Selangor 43400, Malaysia Department of Food Science, Universiti Putra Malaysia, Serdang, Selangor 43400, Malaysia c Department of Agricultural and Food Engineering, University of Uyo, Uyo, Akwa Ibom 520101, Nigeria b

A R T I C LE I N FO

A B S T R A C T

Chemical compounds studied in this article: Iron (III) chloride (PubChem CID: 24380) Sodium carbonate (PubChem CID: 10340) Ascorbic acid (PubChem CID: 54670067) 2, 6 dichlorophenolindophenol (PubChem CID: 13726) Acetic acid (PubChem CID: 176) Trolox (PubChem CID: 40634) 2, 2-diphenyl-1-picrylhydrazyl (PubChem CID: 74358) Metaphosphoric acid (PubChem CID: 3084658) 2, 4, 6-tris (2-pyridyl)-s-triazine (PubChem CID: 77258) Hydrochloric acid (PubChem CID: 313) Gallic acid (PubChem CID: 370) Sodium acetate trihydrate (PubChem CID: 23665404) Chloroform (PubChem CID: 6212) Methanol (PubChem CID: 887)

The effects of a novel technology utilizing a simultaneous combination of Ultraviolet-C radiation and ultrasound energy postharvest treatment on tomato bioactive compounds during 28 days’ storage period was investigated by varying Ultraviolet-C radiation intensities of 639.37 or 897.16 µW/cm2 at a constant ultrasound intensity of 13.87 W/L from a 40 kHz–1 kW transducer. A minimal treatment time of 240 s at Ultraviolet-C dosage of 2.15 kJ/m2 was observed to provoke a considerable increase in bioactive compounds content, proportionated to treatment time. Although treatment led to temperature increase in the system reaching 39.33 °C due to heat generation by ultrasonic cavitation, the extractability and biosynthesis of phytochemicals were enhanced resulting in 90%, 30%, 60%, 20%, and 36% increases in lycopene, total phenols, vitamin C, hydrophilic and lipophilic antioxidant activities respectively. Results present the potential use of the combined non-thermal technologies as post-harvest treatment to improve bioactive compounds and antioxidant activity during storage.

Keywords: Phytochemicals Biosynthesis Cavitation Dosage Permeability Membrane Hydrophilic Lipophilic

1. Introduction Recent trends in epidemiological research have associated tomato consumption with a variety of health benefits such as reduced risk of chronic cardiovascular diseases, prostrate and lung cancer, and antioxidant activity (Wang, Jacobs, Newton, & McCullough, 2016; Del

Giudice et al., 2017). Antioxidant activity is the foundation of a variety of biological functions such as anti-carcinogenicity, anti-mutagenicity, anti-aging and anti-inflammatory (Zou, Xi, Hu, Nie & Zhou, 2016). These benefits are ascribed mostly to the presence of lipophilic (fatty acids, tocopherols, carotenoids) and hydrophilic (sugars, ascorbic acid, phenols, folates) compounds (Rigano et al., 2014), trace elements like

⁎

Corresponding author. E-mail addresses: [email protected] (O.J. Esua), [email protected] (N.L. Chin), [email protected] (Y.A. Yusof), [email protected] (R. Sukor). https://doi.org/10.1016/j.foodchem.2018.07.031 Received 19 March 2018; Received in revised form 28 June 2018; Accepted 3 July 2018 Available online 04 July 2018 0308-8146/ © 2018 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/BY-NC-ND/4.0/).

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tomatoes by harnessing the advantages and minimizing the limitations associated with individual application of both technologies.

Zn, Mn and Cu, antioxidant enzyme cofactors which gives protection against damaged cells, and the interactions occurring between them at various developmental stages. Coupled with the tendency of consumers towards health consciousness, this trend has promoted and warrants profound studies towards the evaluation, preservation and improvement of these phytochemicals during postharvest handling and processing (Liu, Cai, Lu, Han, & Ying, 2012). As Guerreiro et al. (2016) mentioned that majority of natural antioxidants are multifunctional, the need for proper consideration to the various antioxidant mechanisms of action through diverse assays for reliable evaluation is therefore important. Conventional thermal processing and sanitizer applications typically remains the most extensively utilized approach for postharvest handling of fruits and vegetables (Chipurura & Muchuweti, 2010; Ribeiro, Canada, & Alvarenga, 2012). However, nutrient loss associated with the conventional processing (Aadil, Zeng, Han, & Sun, 2013), health concerns associated with sanitizer applications (Ribeiro et al., 2012) and increasing demands for minimally processed food products with preserved fresh-like characteristics have encouraged alternatives to be sought for, especially in the form of novel and non-thermal technologies. Alternatives such as Ultraviolet-C (UV-C) radiation and ultrasound energy can function as abiotic stress elicitors towards the accumulation and biosynthesis of bioactive components of plants, with minimal effects on taste and quality (Freitas et al., 2015; Gomes et al., 2017; Jacobo-Velazquez et al., 2017). Researchers have linked individual postharvest applications of UV-C radiation or ultrasound energy with induced secondary metabolites synthesis and accumulation of tomato phytochemicals. For UV-C radiation, Bravo and co-workers (2012, 2013) reported an increased lycopene, z-lycopene, cis-isomers, total phenolic content and antioxidant activity in vine-ripe and breaker tomatoes exposed to 3.0 kJ/m2 UV-C radiation. Similar results were also reported by Liu et al. (2012) and Maharaj, Arul, and Nadeau (2014) in matured green tomatoes fruits exposed to 4 kJ/m2 and 3.7 kJ/m2 UV-C radiation respectively during 28 days’ storage although Maharaj et al. (2014) also observed a reduction in ascorbic acid, alpha-tocopherol and glutathione content during the period. Pinheiro, Alegria, Abreu, Goncalves, and Silva (2015a) reported that UV-C treated and untreated tomato fruits reached similar values at the end of storage period when exposed to 0.32 kJ/m2. For ultrasound treatment, Pinheiro, Alegria, Abreu, Goncalves, and Silva (2015b) reported higher contents of phenolic compounds with ultrasound treatment at 40–100% power level for 4 min during 15 days storage period. Ding et al. (2015) reported that ultrasound alone at 240 W for 10 min and in combination with slightly acidified electrolytic water (SAEW) had no significant effect on vitamin C content of tomato. As the UV-C radiation is limited by low penetration capability especially into solid materials (Tremarin, Brandao, & Silva, 2017) while the ultrasonic energy consumes high energy coupled with long treatment time, synergistic effect of UV-C radiation or ultrasound energy with other thermal and non-thermal approaches have been recognised in recent times as promising for the postharvest handling and processing of fruits and vegetables and their products (Evelyn, Kim, & Silva, 2016; Gomes et al., 2017). However, there is no information available on the effect of an integrated technology utilizing both UV-C radiation and ultrasound energy in combination and used simultaneously. An integrated technology that combines UV-C radiation and ultrasonic energy is potential towards ensuring overall safety and wholesomeness of fruits and vegetables. The influence of the application of the posited novel integrated technology on bioactive compounds content becomes a significant feature for the process appraisal, since the submission of a novel sanitizing technique to delay microbial growth on fresh produce will be of no good if it impacts negatively on functional and nutraceutical properties. Based on these submissions, this study seeks to evaluate the influence of the simultaneous combination of UV-C radiation and ultrasound energy on the bioactive compounds and antioxidant activity of

2. Material and methods 2.1. Sampling and sampling preparation Tomato fruits (Solanum lycopersicum cv. Baby TM1536) of uniform sizes and shapes at the turning stage, i.e. between 10 and 30% of surface aggregate exhibiting a definite change in colour from green to tannish–yellow, pink, red or a combination of both were selected from heaps that were manually harvested in a commercial farm, Twin Diamond Plantation in the Cameron Highland District of Malaysia. A total of 675 fruits with weight ranging from 97.361 to 140. 019 g were used for the study. Fruits were placed in cold storage of 12 ± 2 °C at relative humidity of 76 ± 2% until treatment. 2.2. Chemicals and reagents All chemicals and reagents used were handled with minimal exposure to light. Standards of Iron (III) chloride (FeCl3·6H2O), 99% purity sodium carbonate (Na2CO3), L-ascorbic acid, 2, 6 Dichlorophenolindophenol (DCIP) sodium salt (C12H6Cl2NNaO2·2H2O), Folin and Ciocalteu’s phenol reagent and acetic acid (CH3COOH) were obtained from R and M Chemicals, Essex, UK. Sigma-Aldrich Chemie, Steinheim, Germany supplied trolox (C14H18O4), 95% purity grade 2, 2diphenyl-1-picrylhydrazyl, (DPPH), metaphosphoric acid (HPO3) and 2, 4, 6-Tris (2-pyridyl)-s-triazine (TPTZ). Analytical grade (37%) hydrochloric acid (HCl) was purchased from Quality Reagent Chemical Product (QREC), Selangor, Malaysia. Gallic acid was procured from Acros Organics, New Jersey, USA, while SYSTERM chemicals provided sodium acetate trihydrate (C2H3NaO2·3H2O), 100% reagent grade chloroform and methanol. 2.3. Combined UV-C radiation and ultrasonic energy equipment set-up The combined UV-C radiation and ultrasonic energy equipment is a bath system utilizing the indirect ultrasonic agitation method integrated with low pressure mercury UV-C lamps having principal emission at 253.7 nm. The stainless steel tank of capacity 67.12 L measures 406 mm (L) × 406 mm (W) × 610 mm (H), with a tank cover to protect UV-C radiation exposure and a fill and drain inlet/outlet, each located at the bottom and by the side of the tank for ease of filling and draining. The equipment simultaneously emits ultrasonic cavitation from an immersible integral mounting flange type piezoelectric transducer (1 kW, 40 kHz, Branson Ultrasonic, Shanghai, China) enclosure bonded at the bottom of the tank and UV-C radiation from four singleended pins high power series lamps (ZW18D15W-Z356, CnLight Co. Ltd, Guangdong, China), uprightly held in place on each of the interior of the four-walled tank just directly above the transducer surface. The lamps irradiate towards the centre of the tank and are specially treated on electrode and quartz tubes for longer lifetime and improved output. The lamps, 15 mm diameter, rated 18 W and intensity of 48–54 µW/cm2 (1 m distance) are encased in quartz glass sleeves for protection in water. A perforated stainless steel produce basket held in place by a mechanical system, positioned equidistant from the walls of the tank, and within the lamp base face length so as to ensure full surface exposure of the produce to UV-C radiation holds produce for contamination in place. 2.4. Treatment and experimental design The power dissipated by ultrasonic cavitation was estimated from Eq. (1) (Kek, Chin, & Yusof, 2013) where temperature was logged as a function of time during heat production as a result of both ultrasonic cavitation and UV-C radiation. The effective acoustic energy density 114

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humidity for 28 days. Fresh tomatoes were sampled for its initial properties, while treated and control samples were taken for analysis immediately after treatment and at periodic interval of 7 days. For a proper comparison of the temperature of the system following two and four lamps use, the temperature rise in the medium during treatments was recorded every 30 s for treatment durations of 80–240 s and every 180 s for durations of 360–1680 s as shown in Table 1, using a logging thermometer (CENTER 309, CENTER Technology Corp., New Taipei, Taiwan) with a K type thermocouple attached.

(AED) of the tank medium was subsequently estimated at 13.87 W/L by dividing the ultrasonic power dissipated in the tank with the volume of the medium in the tank used as expressed in equation (2).

dT Pdiss = mCp ⎛ ⎞ ⎝ dt ⎠

AED =

(1)

Pdiss Vm

(2)

where Pdiss is the ultrasonic power dissipated in the tank (W), m is mass of the medium which is tap water, Cp is the specific heat capacity of water (4187 J/kg K), dT/dt is the slope of the temperature versus time curve (K/s). The initial temperature of the medium was 34.5 °C. AED is the acoustic energy density (W/L) and Vm is the volume of medium (L). The mass of 1 L of water is approximately 1 kg, therefore volume of water in the treatment tank was 67.12 L from mass of water of 67.12 kg. Two different UV-C intensities, the lower intensity with two lamps use (CT) and the higher intensity with four lamps utilization (CF) were tested. The effective irradiances for the two and four lamps utilization were measured by radiometer (UVX radiometer, UVP, CA, USA) readings at the edge of the tank adjacent to the lamps and after necessary corrections for use in water medium (Bolton & Linden, 2003), arrived at 639.37 µW/cm2 and 897.16 µW/cm2 respectively for two (CT) and four (CF) lamps use. UV-C dosage was calculated using equation (3) as a product of intensity and treatment duration to achieve similar dosage levels ranging from 0.72 to 10.77 kJ/m2.

2.5. Quantitative determination of bioactive compounds 2.5.1. Preparation of tomato hydrophilic and lipophilic Extracts Extracts from treated and untreated tomato samples were obtained using the method of Rigano et al. (2014) with modifications. 3 g of carefully blended homogenate tomato tissue was extracted using 10 mL analytical grade methanol in an ultrasound bath (Model 5200, Branson Ultrasonic Corp., Danbury, CT, USA) at 30 °C for 60 min and subsequent centrifugation at 3500×g (Hettich, Universal 320, Andreas Hettich GmbH. Tuttlingen, Germany) for 10 min at 4 °C. Hydrophilic extract obtained was stored at −5 °C in glass bottle covered with foil for total phenolic compounds and hydrophilic antioxidant activity assay. Pellet obtained was extracted with 10 mL chloroform using a mortar and pestle and subsequently centrifuged at 3500×g for 5 min at 4 °C to obtain lipophilic extract stored at −5 °C in glass bottles covered with foil for lycopene content and lipophilic antioxidant activity estimation.

(3)

D = I ∗t 2

2

where D is UV-C dosage (kJ/m ), I is intensity (µW/cm ) and t is treatment time (s) The CT experimental runs had a longer treatment duration of 112, 280, 337, 674, 1010, 1348 and 1683 s grouped as CT1, CT2, CT3, CT4, CT5, CT6 and CT7 while the CF treatment durations were slightly shorter, i.e. 80, 200, 240, 480, 720, 960 and 1200 s represented as CF1, CF2, CF3, CF4, CF5, CF6 and CF7, as summarised in Table 1. This produced a total of 15 experimental runs including a control. In each run or combined UV-C radiation and ultrasound energy treatment, 18 tomatoes samples (3 tomatoes × 5 periodic intervals plus 3 spares) were selected randomly and treated in 3 batches at the capacity of 6 fruits per basket during treatment. The completely randomized block design was used for the total of 15 runs × 3 batches. Each treated sample was allowed to dry and transferred into separate autoclavable disposable bags and labelled. Treated samples and untreated samples (control) were kept in cold storage at 12 ± 2 °C and 76 ± 2% relative

2.5.2. Lycopene content measurement Absorbance of lipophilic extract was measured in a quartz cuvette (1 cm optical path) at 503 nm on a UV/Visible Spectrophotometer (Ultrospec 3100 Pro. Biochrom Ltd Cambridge, UK) blanked against distilled water. Lycopene concentration was expressed as milligrams per kg of fresh weight, estimated using a modified Beer-Lambert equation (Eqs. (4)–(6)

Absorbance at 503 nm (A503 ) = ε (L∗ mol−1∗ cm−1) ∗l (cm) ∗c (g∗mol−1) (4) where ε is molar extinction coefficient for lycopene in chloroform (152,989 L/mol cm), l is path length (cm), c is concentration of lycopene (mol/L)

c=

Table 1 UV-C Radiation Dosage Levels and Temperature in Medium for the Two and Four Lamps Treatment. Dosage (kJ/m2)

0 0.72 1.79 2.15 4.31 6.46 8.61 10.76

Sample Code

Control CT1 or CF1 CT2 or CF2 CT3 or CF3 CT4 or CF4 CT5 or CF5 CT6 or CF6 CT7 or CF7

Two Lamps (CT) at 639.37 µW/cm2

Four Lamps (CF) at 897.16 µW/ cm2

Treatment Time (s)

Treatment Temp (°C)

Treatment Time (s)

Treatment Temp (°C)

0 112

34.57 ± 0.06 35.07 ± 0.35

0 80

34.57 ± 0.12 35.17 ± 0.25

280

35.47 ± 0.25

200

35.50 ± 0.10

337

35.90 ± 0.10

240

35.87 ± 0.06

674

36.53 ± 0.12

480

36.47 ± 0.06

1010

37.75 ± 0.10

720

36.97 ± 0.10

1348

38.87 ± 0.06

960

37.63 ± 0.12

1683

39.33 ± 0.12

1200

38.13 ± 0.32

vol of Chloroform (ml) 536.9 g A503 mol cm 1L ∗ ∗ ∗ 3 152, 989L∗1 cm weight of sample (g ) mol 10 ml ∗

103 mg 103 g ∗ 1 g 1 kg

Lycopene concentration (mg kg ∗3.5094

(5) -1

FW) =

vol of chloroform ∗A503 weight of sample

(6)

2.5.3. Total phenolic content assay Total phenolic content (TPC) of samples was determined using the Folin-Ciocalteu method as modified by Del Giudice et al. (2015). 62.5 µL of supernatant from hydrophilic extraction was mixed with 62.5 µL of Folin-Ciocalteu’s phenol reagent and 250 µL of sterile distilled water and vortex. 625 µL of 7% sodium bicarbonate (Na2CO3) was subsequently added after 6 min followed by dilution with 500 µL of sterile distilled water and vortex. The absorbance of the mixture was read at 760 nm (Ultrospec 3100 Pro. Biochrom Ltd Cambridge, UK) in a plastic cuvette (1 cm optical path) against a blank of distilled water after incubation at room temperature in a dark room for 90 min. Samples were analysed in triplicates, and total phenolic contents of samples was expressed as milligram Gallic acid equivalents (GAE) 100 g−1 fresh weight using standard Gallic acid curve (0.042 mg/mL to 0.492 mg/mL; y = 3.7089x −0.0063; r 2 = 0.9965). 115

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vortexed in 5 mL Eppendorf tube and kept at room temperature in a dark room for 30 min. Spectrophotometric absorbance of the mixture was read at 515 nm (Ultrospec 3100 Pro. Biochrom Ltd Cambridge, UK) in a plastic cuvette (1 cm optical path) blanked against distilled water. Results were expressed as milligram ascorbic acid equivalent (AAE) 100 g−1 of fresh weight from a standard L-ascorbic acid curve (0.024 µg/mL to 25 µg/mL; y = −0.0094x + 0.4396; r 2 = 0.924 ).

2.5.4. Vitamin C content determination Vitamin C content of samples was assayed using the indophenol titrimetric method as reported by Kek et al. (2013) with modifications. 3 g of sample was ground with 10 mL metaphosphoric-acetic acid (HPO3-CH3COOH) solution using a porcelain mortar and pestle. The extract was emptied into 50 mL Eppendorf tube, while the pulp residue was ground again with 10 mL HPO3-CH3COOH solution. The extract obtained from both process was mixed and the filtrate obtained was stored at −5 °C in an airtight dark corner until further analysis, usually within 24 hrs. On the day of analysis, 7 mL of the filtrate was titrated with 2, 6-dichlorophenolindophenol (DCIP) solution, until a light blue distinct rose-pink colour persisted for 5–10 s in an Erlenmeyer flask. Vitamin C content measurement was based on the average values of triplicate determinations including the blanks, where 7 mL of HPO3CH3COOH solution was titrated. 2 mL of standard ascorbic acid solution having a concentration of 1 mg/mL was added to 5 mL of HPO3CH3COOH solution and titrated against DCIP solution until a light blue distinct rose-pink colour persisted for 5–10 s, for the purpose of dye standardisation. The titre, F was calculated using Eq. (7) from data obtained for dye standardisation. Titre, F =

2.6. Statistical analysis Statistical analysis and the influence of treatment, storage period and their interactive effect on studied properties were assessed by twoway analysis of variance (ANOVA) using SigmaPlot, version 12.0 data analysing and graphing software (Systat software Inc., CA, USA). The differences among treatment means were separated using a post-hoc Tukey test at 95% confidence interval (α = 0.05) for all pairwise multiple comparison. Mann-Whitney rank sum test (two sample t-test) was also performed to test significant difference between the low and high UV-C intensity use. 3. Results and discussions

mg of ascorbic acid in vol of standard solution titrated [average ml for standard titration−average ml for blank titration]

3.1. Temperature of system during combined UV-C and ultrasound treatment

(7) Vitamin C content in mg 100 g−1 sample was calculated following Equation (8)

mg vitamin c F V = (X −B ) ∗ ∗ ∗100 100 g sample E Y

Table 1 presents the increase of temperature of about 4–5 °C in medium of the UV-C and ultrasound system for both lamp configurations due to heat generation by UV-C radiation lamps and energy released during ultrasonic cavitation caused by the formation and collapse of micro-size bubbles in the form of waves and friction (Cao, Cai, Wang, & Zheng, 2018). The water flow circulation system of the tank however keeps the system from overheating. The final temperature of the four lamps system after the maximum exposure time of 1200 s at 38.13 °C was not considerably different from that with the two lamps configuration at 38.30 °C obtained at 1348 s, which is the closest exposure time for the two lamps system to 1200 s. This indicates that the primary source of heat generation in the system is through ultrasonic cavitation, since the difference in the number of lamps used did not significantly affected the temperature of the system. The final temperature of 39.33 °C, at the longest treatment duration of 1683 s was within the optimum temperature of 40 °C as suggested for low mercury lamp operation by Koutchma, Forney, and Morau (2009). Although high temperatures and molecular oxygen exposure during cavitation could result in unwanted loss of quality such as bioactive compounds degradation as observed by Cao et al. (2018), increased temperatures have been reported to improve the extraction capability of targeted bioactive compounds for bayberry juice (Cao et al., 2018) due to synergistic effect of temperature and novel treatments on enzyme inactivation. Chemat et al. (2017) observed that such increase in temperature could improve the efficiency of compounds extraction.

(8)

where X is average mL for test sample titration (volume of titrant), B is average mL for test blank titration, F is titre in mg/mL (mg ascorbic acid equivalent to 1.0 mL indophenol standard solution), E is weight of the sample (g), V is volume of initial assay solution (liquid extract), Y is volume test solution or filtrate (7 mL). 2.5.5. Hydrophilic antioxidant activity assay The hydrophilic antioxidant activity (HAAT) was evaluated by the FRAP assay which directly measures the ability of antioxidants to reduce ferric tripyridyltriazine complex (Fe+3-TPTZ) to ferrous complex (Fe+2-TPTZ) at low pH. The method of Liu et al. (2012) was used with slight modification. Supernatant (150 µL) from hydrophilic extraction was mixed with 3 mL of FRAP reagent, vortex and incubated for 30 min at room temperature in the dark. The absorbance of the mixture was read at 593 nm (Ultrospec 3100 Pro. Biochrom Ltd Cambridge, UK) in a plastic cuvette (1 cm optical path) against a blank of distilled water. FRAP reagent used for the assay was freshly prepared for each day of analysis according to the method of Peng (2009). 0.3 M acetate buffer having a pH of 3.6 was prepared from 16 mL acetic acid and 3.1 g C2H3NaO2·3H2O in 1000 mL sterile distilled water. 10 mM 2, 4, 6-tris (1-pyridyl)-5-triazine (TPTZ) was prepared by dissolving 0.0468 g TPTZ in 15 mL of 40 mM HCl at 50 °C in a water bath. 20 mM ferric solution (FeCl3·6H2O) was prepared by dissolving 0.0811 g in 15 mL sterile distilled water. Final working volume of FRAP was obtained by freshly mixing acetate buffer, TPTZ and ferric solution in a ratio of 10:1:1. 18 mL of sterile distilled water was added and maintained in a water bath at 37 °C for use. Results were expressed as mM Trolox Equivalent (TE) 100 g−1 of fresh weight from a standard Trolox curve ( y = 0.0017x + 0.1395; r 2 = 0.9993) linear between 20 µM and 960 µM Trolox.

3.2. Fresh tomato properties The tomatoes used in this study were at the turning stage and have an average lycopene content of 2.31 mg kg−1 FW, which is slightly above recorded values of 1.6 mg/100 g and 212.06 µg/100 g (Liu, Cai, Han, & Ying, 2011; Jagadeesh et al., 2011) and below 2.32, 6.94 and 17.79 mg/kg (Bravo et al., 2012, 2013; Choi, Park, Choi, Kim, & Chun, 2015). Total phenolic content averaged 13.38 mg GAE 100 g−1 FW was comparable to 14.58 mg GAE 100 g−1 FW recorded by Bravo et al. (2013), but lower than values in the range of 25.4–77.88 mg GAE 100 g−1 FW documented by Jagadeesh et al. (2011); Pinheiro, Alegria, Abreu, Goncalves, and Silva (2013) and Bravo et al. (2012). Vitamin C content was observed as 5.06 mg 100 g−1 FW, comparable to values reported in literature at 2.72 mg 100 g−1 (Liu et al., 2011) and 4.32 mg 100 g−1 (Maharaj et al., 2014). Tomato samples had an initial

2.5.6. Lipophilic antioxidant activity assay Lipophilic antioxidant activity (LAAT) was assayed by the evaluation of tomato scavenging effect on the 2,2–diphenyl-1-picrylhydrazyl (DPPH) radical based on the method of Liu et al. (2012). Homogenate mixture of 2.8 mL of freshly prepared 60 µmol L−1 DPPH reagent and 0.2 mL of supernatant obtained from lipophilic extraction and was 116

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Fig. 1. Effect of Combined UV-C Radiation and Ultrasonic Energy Treatment on Lycopene Content of Tomato (mg kg−1 FW). (a) Two (CT); (b) Four (CF) Lamps Configuration. Results are mean ± standard error from three measurements.

hydrophilic antioxidant activity of 70.31 mMTE 100 g−1 FW, similar to values reported in other studies at 0.75 mmol Trolox kg−1 FW (Bravo et al., 2012), 78.72 µM TEAC 100 g−1 FW (Jagadeesh et al., 2011), 599.40 µM Trolox 100 g−1 (Pinheiro, Alegria, Abreu, Goncalves, and Silva, 2016), 187.43 µmol TE 100 g−1 FW (Del Giudice et al., 2015). Data show high initial levels of lipophilic antioxidant activity of 23.83 µg AAE g−1 FW, which corroborates the report by Bravo et al. (2012), possibly due to high chlorophyll concentration. Chlorophylls are usually seen as probable contributors to vegetables’ antioxidant properties, even though they are not generally regarded as dietary antioxidants (Bravo et al., 2012). Variations in the values of initial quality parameters from this study and values recorded in other studies could be attributed to the different maturity stage of samples used.

apparent that the combined UV-C radiation and ultrasonic energy treatment has enhanced it significantly over the course of the 28 days’ storage period. The lycopene synthesis may not require light for induction (Liu et al., 2009; Bravo et al., 2012) and is known to be temperature dependent where it occurs at a predominantly higher rate between 12 and 30 °C and is totally inhibited from 32 °C (Choi et al., 2015). While the lycopene synthesis occurs in the chloroplast during off-vine ripening process as a result of increased biological activity, the combined UV-C radiation and ultrasound energy actions have possibly disrupted some chemical bonds and macromolecules structure holding nutraceuticals thereby facilitating its extraction (Jacobo-Velazquez et al., 2017). Nowacka and Wedzik (2016) ascribed the increase in extractability bioactive compound contents immediately after such novel treatment to the disruption of cell membrane and JacoboVelazquez et al. (2017) related it to the late response of tomato fruit to abiotic stress from combined UV-C and ultrasound energy actions. While the ultrasonic cavitation can lead to a series of rapid expansions of plant tissue, the UV-C radiation provokes hormetic responses which brings about various oxidative and biological stresses and biochemical reactions in plants (Nowacka & Wedzik, 2016). The late response, which is usually a consequence of the immediate response is responsible for secondary metabolites and enzyme production necessary for horticultural produce adjustment to such abiotic stress from the combined actions of UV-C radiation and ultrasonic energy. Other studies which have used UV-C radiation alone to disinfect fruits and vegetables recorded differing results. Pristijono et al. (2017) observed significantly higher lycopene content in UV-C radiation treated fruits and Bravo et al. (2012) reported 8-fold increase in lycopene and significant reduction in β-carotene content of tomatoes exposed to 1.0 and 3.0 kJ/m2 during 8 days’ storage period at room temperature. Choi et al. (2015) observed higher lycopene contents relative to control samples after UV-C radiation exposure. Pataro, Sinik, Capitoli, Donsi, and Ferrari (2015) mentioned that UV-C radiation was less effective in stimulating carotenoid synthesis compared to pulsed light treatment even though total carotenoid increased significantly as storage progressed leading to 1.4-fold significant increase. Similarly, Liu et al. (2009) and Liu et al. (2011) obtained 1.8-fold and 40-fold

3.3. Effect of treatment and storage on lycopene content Fig. 1 shows that combined UV-C radiation and ultrasonic energy treatment has led to lycopene content increase in tomato with respective treatment time represented by the dosage levels consistently for both lamp configuration and progressively with storage period of 28 days. Lycopene content was enhanced immediately after treatment, at Day 0 of storage. The increase of lycopene was 48%, at 3.41 mg kg−1 FW from an initial value of 2.31 mg kg−1 FW for maximum treatment time of 1683 s (CT7) for the two lamps configuration and 1200 s (CF7) for the four lamps. There was no significant difference in lycopene content at the higher end of dosage levels, between treatment times of 1348 s (CT6) and 1683 s (CT7) for two lamps use and 720 s (CF5), 960 s (CF6) and 1200 s (CF7) for four lamps use. The two sample statistical ttest also confirms the absence of any significant difference between two and four lamps usage referring to no differences between the low and high UV-C radiation intensity used. At the end of storage period, the highest lycopene content of 24.33 mg kg−1 FW from CF7 and 23.34 mg kg−1 FW from CT7 recorded about 90% increase compared to untreated sample (control) which lycopene has also increased to 12.81 mg kg−1 FW. Synthesis of lycopene during storage was expected due to selected tomato samples at the turning stage (Liu, Zabaras, Bennett, Aguas, & Woonton, 2009), it is 117

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Fig. 2. Effect of Combined UV-C Radiation and Ultrasonic Energy Treatment on Total Phenolic Content of Tomato (mg GAE 100 g−1 FW) (a) Two (CT), (b) Four (CF) Lamps Configuration. Results are mean ± standard error from three measurements.

increase during storage after exposure to 13.7 kJ/m2 UV-C and 80 kJ/ m2 UV-B radiation respectively. Jagadeesh et al. (2011) reported a reduction in lycopene content of fruits exposed to 3.7 kJ/m2 UV-C radiation. The inconsistent outcomes suggest that this nature of study is limited to and dependent on many factors including harvesting period, cultivar, physiological stage, ripening stage, storage conditions, dosage and mode of delivery, and equipment characteristics (Jagadeesh et al., 2011) which needed to been taken into consideration during postharvest treatment.

conditions of pressure and temperature arising from ultrasonic cavitation implosion ruptures cell envelopes of tomatoes may also explain the facilitation of UV-C radiation access to enhance release of phenolic contents and activation of bound enzymes. There is possibility that combined DNA-damaging effect of UV-C radiation and strong mechanical cavitation effect of ultrasonic energy induces accumulation of UV-C light absorbing phenolic compounds to activate phenolic biosynthesis pathway, thereby enhancing total phenols of tomatoes remains. The increase in total phenolic content during ripening have been documented in literature (Pinheiro et al., 2013). Maharaj et al. (2014) observed that phenolic acids and flavonoids are the main phenolic compounds of tomatoes and attributed total phenol increase during storage to decrease of hydroxycinnamic acid levels in tomato flesh and increase in naringenin in the exocarp as a result of ripening. In general, the total phenols in this research increased with storage for both control and treated fruits with small exception of a slight decrease noticed for CT4 (14 days), CF2 (14 days), CF4 (14 and 28 days) and CF5 (14 days). At the end of storage period, highest phenolic content of 28.95 mg GAE 100 g−1 FW and 29.77 mg GAE 100 g−1 FW was induced by the longer treatment time of 1348 s (CT6) and 1200 s (CF7) respectively which recorded about 30% increase relative to control value of 22.88 mg GAE 100 g−1 FW. For the two lamps use, there was no significant difference between 1348 s (CT6) and 1683 s (CT7). Most other researchers also found significant increases and higher phenolic content in mature green tomatoes when given UV-C radiation treatment at dosage range of 1–8 kJ/m2 (Jagadeesh et al., 2011; Liu et al., 2012; Bravo et al., 2012, 2013; Maharaj et al., 2014; Pristijono et al., 2017), UV-B radiation at 20 kJ/m2 (Liu et al., 2011), 80% power level of ultrasound treatment (Pinheiro et al., 2015b), and gamma radiation applications (Guerreiro et al., 2016). Contrarily, Pinheiro et al. (2015a) reported that total phenol content of tomato treated with 0.32–4.83 kJ/m2 UV-C radiation was not significantly different to control fruits at the end of storage.

3.4. Effect of treatment and storage on total phenolic content Fig. 2 shows that the overall concentration of total phenols was higher in treated tomatoes relative to control where longer treatment duration provoked higher levels of total phenols for both lamp configurations. For longer treatment time of 1200 s (CF7), an increase of 50% at 20.12 mg GAE 100 g−1 FW from an initial value of 13.38 mg GAE 100 g−1 FW was significant and evident immediately after treatment (Day 0) although the lower treatment duration of 120–240 s (CT1–CT2) and 80–200 s (CF1–CF2) were less significant. The instantaneous increase in total phenol content immediately after treatment and comparative increase during storage in this study can be attributed to the release of bound phenolic contents and the activation of phenylalanine ammonialyase (PAL) enzymes, responsible for the synthesis of some phenolic compounds such as flavonoids, chlorogenic acids, coumarins and phenylpropanoids as noted by Maharaj et al. (2014). Jagadeesh et al. (2011) attributed total phenol content increase of UV-C treated tomato to synthesis of flavanols mostly found on tomato skin. Since UV-C has limited penetrability to surfaces, UV-C radiation is known to change permeability of cell membranes and activate the biosynthetic pathways of membrane bound enzymes resulting in toxic intermediates accumulation and generation of physiological stress in the cells of plants which leads to increase in the levels of hydroxycinnamoyl quinate transferase (HQT) and phenylalanine ammonialyase (PAL) enzymes (Toor & Savage, 2006; Maharaj et al., 2014). As Fu, Zhang, Cheng, Jia, and Zhang (2014) observed that ultrasonic cavitation simplifies plant cell wall breakage due to alterations in surface structure from their scanning electron microscopy, the extreme

3.5. Effect of treatment and storage on vitamin C content Fig. 3 presents the increase of vitamin C content of tomatoes 118

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Fig. 3. Change in Vitamin C Content of Tomato (mg 100 g−1 FW) Subjected to Combined UV-C radiation and Ultrasonic Treatment. (a) Two (CT), (b) Four (CF) Lamps Configuration. Results are mean ± standard error from three measurements.

tomato (18% and 2.8-fold lower than untreated fruit respectively). Ding et al. (2015) found no significant effect on vitamin C content of cherry tomatoes subjected to combined ultrasound and slightly acidified electrolytic water (SAEW) treatment. The increased levels of vitamin C in tomatoes during storage have been reported with advancement in senescence and ripening (Jagadeesh et al., 2011; Liu et al., 2011; Maharaj et al., 2014). The stability of ascorbic acid in fruits is usually influenced by high titratable acidity (Toor & Savage, 2006). Tomato being a highly acidic fruit, showed relatively stable ascorbic acid content during storage.

subjected to combined UV-C radiation and ultrasonic energy treatment from its initial value of 5.06 mg 100 g−1 FW to 8.43 mg 100 g−1 FW immediately after treatment (Day 0) and 20.10 mg 100 g−1 FW after 28 days’ storage. There was considerable increase in vitamin C content after 7 days of storage until the 14th day, reaching 10.20 for the control, 16.73 mg 100 g−1 for CT6 and 14.61 mg 100 g−1 for CF7. The slight decrease of vitamin C content on day 21 which preceded before a further increase to its maximum at the end of the 28 days’ storage may be considered as fluctuation in an overall increasing trend of vitamin content. The impact of treatment was evident and at the end of storage, vitamin C content of treated fruit between was between14.35 and 20.10 mg 100 g−1 amounting to 20–60% increase relative to control value of 12.29 mg 100 g−1. For the two lamps, statistical analysis suggested that further treatment beyond 337 s (CT3-17.42 mg 100 g−1) did not give significant increase of its vitamin C value (1348 s-CT619.66 mg 100 g−1). In the same vein, for the four lamps, 20.10 mg 100 g−1 was observed for treatment duration of 1200 s (CF6) to be the highest for four lamps use, just as there was no significant increase after 240 s (CF3) of treatment time. The positive outcome of combined UV-C radiation and ultrasonic energy treatment may be related to the elimination of dissolved oxygen necessary for the degradation of vitamin C by cavitation and a probable reduction in the activity of ascorbate oxidase by combined treatment (Ali, Russly, Jamilah, Azizah, & Mandana, 2011; Jagadeesh et al., 2011). The phenolic substances are known to have protective influence on ascorbic acid, hence flavonoids and phenolic presence in tomato cells may also play some role (Toor and Savage, 2006). Jagadeesh et al. (2011) has presented evidences claiming higher levels of ascorbic acid with UV-C radiation treated fruit. Ali et al., 2011 reported higher values of vitamin C retained in thermosonically treated seedless guava. Freitas et al. (2015) on the other hand attributed higher levels of L-ascorbic acid in UV-C treated pineapple rind to the impact of UV-C radiation on ascorbate-glutathione cycle, while Reddy, Khan, Patnaik, Mohanty, and Kumar (1986) observed a positive correlation between decreased ascorbic acid levels and increased activity of ascorbate oxidase enzyme. Despite positive outcome of combined UV-C radiation and ultrasonic energy treatment, Liu et al. (2011) and Maharaj et al. (2014) reported a negative effect of UV-B and UV-C radiation on ascorbic acid content of

3.6. Effect of treatment and storage on antioxidant activity The antioxidant activity of tomato was evaluated from the hydrophilic and lipophilic extract using the FRAP assay and DPPH scavenging ability, respectively. Fig. 4 shows that the antioxidant activity of tomatoes treated with combined UV-C and ultrasonic energy increased with storage period significantly for all treatment duration. Fig. 4a and 4b show that the increase in hydrophilic antioxidant activity to 95.67 and 89.65 mMTE 100 g−1 FW for CT6 and CF6, respectively was evident immediately after treatment (Day 0). The increase as a result of treatment was also maintained throughout storage period with the exception of slight reduction in value on Day 21 for treatment durations of 337 (CT3), 1348 (CT6), 1683 s (CT7) and 200 (CF2), 240 (CF3), and 1200 s (CF7). With successive increases in exposure time, hydrophilic antioxidant activity values of tomatoes tended towards peak values, reaching the highest values of 161.88 and 168.51 mMTE 100 g−1 FW respectively, following 1348 (CT6) and 960 s (CF6) treatment duration at the end of the storage period. Generally, treatment did not evoke further significant accumulation in hydrophilic antioxidant activity after treatment duration of 1348 (CT6) and 960 s (CF6). Bravo et al. (2012), Liu et al. (2012) and Pinheiro et al. (2016) have indicated positive effect of UV-C treatment on hydrophilic antioxidant activity of tomatoes. These reports are in contrast with reports by Jagadeesh et al. (2011) and Liu et al. (2011) who found that hormetic UV-C and UV-B radiation dose had no significant effect on tomato hydrophilic fraction antioxidant activity after storage. This is probably attributed to resultant effect of treatment on delayed singlet oxygen production 119

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Fig. 4. Changes in Hydrophilic Antioxidant Activity (mMTE 100 g−1 FW) (a) Two (CT), (b) Four (CF) Lamps Configuration and Lipophilic Antioxidant Activity (µg AAE g−1 FW) (c) Two (CT), (d) Four (CF) Lamps Configuration of Tomato Subjected to Combined UV-C Radiation and Ultrasonic Energy Treatment. Results are mean ± standard error from three measurements.

antioxidant activity showed high values immediately after treatment (Day 0), especially for higher treatment durations, attaining values of 37.44 and 38.83 µg AAE g−1 FW for 1348 s (CT6) and 960 s (CF6) treatment times respectively. There was no further significant increase from 29.49 and 34.44 µg AAE g−1 FW after 1010 s (CT5) and 480 s (CF4) exposure durations. In general, a decrease in lipophilic antioxidant activity was observed for all sample on storage Day 21, after an initial increase during the first 14 days of storage. Pataro et al. (2015) reported similar trend of increase in DPPH scavenging ability during the first 14 days and subsequent decrease on the last day of storage (day 21) for some pulsed light and UV-C irradiated tomato fruits. Liu et al. (2011) claimed a slight decrease for 7 days followed by an increase till day 37, from an initial increasing trend during the first 21 days on

(Rivera-Pastrana, Gardea, Yahia, Martinez-Tellez, & Gonzalez-Aguilar, 2014) and increase in hydrophilic components of phenols and ascorbic acids (Guerreiro et al., 2016) evident in the treated fruits, since a positive correlation was established between hydrophilic antioxidant activity and total phenol (r = 0.78, 0.81) and hydrophilic antioxidant activity and vitamin C (r = 0.83, 0.82) for two and four lamps configurations respectively. The lipophilic antioxidant activity appraised from the DPPH scavenging activity similarly showed significant improvement after combined UV-C radiation and ultrasonic energy treatment (Fig. 4c and d). Increase in values was proportional to increased treatment time for all storage days, except for decrease in value observed with 480 (CF4), 674 (CT4), 1200 (CF7) and 1683 s (CT7) exposure time. Lipophilic 120

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Table 2 p Values of Two-Way ANOVA for Bioactive Compounds and Antioxidant Activities of Tomatoes Subjected to Combined UV-C Radiation and Ultrasonic Energy Treatment. Factors

Treatment (T) Storage (S) TxS

DF

7 4 28

Lycopene

TPC

Vitamin C

HAAT

LAAT

CT

CF

CT

CF

CT

CF

CT

CF

CT

CF

< 0.001 < 0.001 < 0.001

< 0.001 < 0.001 < 0.001

< 0.001 < 0.001 < 0.001

< 0.001 < 0.001 < 0.001

< 0.001 < 0.001 0.769

< 0.001 < 0.001 0.928

< 0.001 < 0.001 < 0.001

< 0.001 < 0.001 0.031

< 0.001 < 0.001 0.128

< 0.001 < 0.001 0.362

DF: Degrees of Freedom, TPC: Total Phenolic Contents, HAAT: Hydrophilic Antioxidant Activity Assay, LAAT: Lypophilic Antioxidant Activity Assay.

Conflict of interest

tomato fruit subjected to UV-B irradiation. At the end of storage, an ample increase succeeded the decrease noticed on Day 21 for all sample with control having the lowest lipophilic antioxidant activity at 41.75 µg AAE g−1 FW. No further significant increase was evident from 52.02 and 55.16 µg AAE g−1 FW after 1010 s (CT5) and 720 s (CF5). Fairly strong correlation, r = 0.65 (CT) and 0.66 (CF) between lipophilic antioxidant activity and lycopene was also evident, indicating that lipophilic antioxidant activity in tomatoes is predominantly determined by lycopene content. Literatures on effect of such treatment on lipophilic antioxidant activity are not consistent. Liu et al. (2011 and 2012) and Pataro et al. (2015) reported enhanced DPPH scavenging ability of tomato (11.2%, 15% and 40% respectively) subjected to UV-C and UV-B irradiation. Bravo et al. (2012) also indicated a provoked increase in lipophilic antioxidant activity by 1.0 kJ/m2 UV-C exposure. Pristijono et al. (2017) reported no significant difference in DPPH scavenging activity of tomato after treatment with UV-C irradiation and 1-MCP, even though similar treatment led to 11% increase in lycopene content. The overall statistical analysis presented in Table 2 shows that both factors, treatment duration and storage period have significant effects (p < 0.001) on all the bioactive compounds and antioxidant activity of treated tomato for both lamp configurations. The paired comparison ttest results between data from low and high UV-C radiation intensity use was not significant, even though high UV-C radiation intensity (four lamps) may give slightly higher bioactive compound values at the end of storage.

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4. Conclusions The combined effects of UV-C irradiation with ultrasonic cavitation stimulated the accumulation of tomato phytochemicals enhancing lycopene, total phenols, ascorbic acid and antioxidant capacity after a short exposure time of 240 s despite an increase in the temperature reaching 39.33 °C in the system due to heat generation. The enhancement was significant for both the treatment time and storage period, whilst the low and high UV-C intensity utilization has no significant difference. This combination of UV-C radiation and ultrasonic energy may be used as a new approach of postharvest treatment for tomatoes and other fruits as it has shown significant improvements of bioactive compounds and antioxidant activities during storage. This novel process warrants further investigations with other fruits and vegetables, acoustic energy density variations, scanning electron microscopy analysis to understand the relationship of treatment with cell structure and HPLC analysis to check the stability of lycopene isomers as a result of treatment.

Acknowledgements This study was supported by Universiti Putra Malaysia, Malaysia (GP-I/2014/9439000) and first author was sponsored by the Niger Delta Development Commission (NDDC/DEHSS/2014PGFS/AKS/014), Nigeria. 121

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