Irradiation of Fruits and Vegetables

Irradiation of Fruits and Vegetables

C H A P T E R 17 Irradiation of Fruits and Vegetables Anuradha Prakash*, Jose de Jesu´s Ornelas-Paz† * Schmid College of Science and Technology, Ch...

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C H A P T E R

17 Irradiation of Fruits and Vegetables Anuradha Prakash*, Jose de Jesu´s Ornelas-Paz† *

Schmid College of Science and Technology, Chapman University, One University Drive, Orange, CA, United States †Research Center for Food and Development, Cd. Cuauhtemoc, Chihuahua, Mexico

17.1 INTRODUCTION Radiation is any energy traveling through the space in form of waves or particles. It can be classified as ionizing and nonionizing, depending on its energy. Ionizing energy has shorter wavelengths yet higher frequency and energy as compared to nonionizing energy (Fig. 17.1). The visible light spectrum, radio waves, microwaves, and infrared waves contain sufficient energy for molecular vibrations and excitations, but not ionization. In contrast, far UV rays, X-rays, and γ-rays contain higher energy, which can eject electrons from atoms, thus causing the ionization of molecules. Ionizing radiation can also break chemical bonds in molecules, causing alterations in the normal functioning of cells. The term “food irradiation” refers to the deliberate exposure of food to ionizing radiation. Ionizing radiation, specifically X-rays, was discovered in 1895 by Wilhelm Conrad R€ ontgen. Radioactivity was recognized 1 year later, when Henri Becquerel discovered that uranium salts emitted energy that could penetrate opaque matter. Further studies demonstrated that these rays contained α, β, and γ radiation, which were composed of fast-moving atomic nuclei of helium, energetic electrons, and photons, respectively. The effects of irradiation on foods were rapidly studied, although the early studies were merely at laboratory scale, with the absence of powerful sources of ionizing energy being the most relevant limitation to do a deep exploration of irradiation effects in foods. These early studies demonstrated the bactericidal and nematicidal effects of ionizing radiation and were mainly performed using X-rays. The military developments generated during the Second World War and the Cold War in the field of irradiation were incorporated to other sectors, including the food sector. The increased availability of radioactive materials/sources (i.e., 137Cs, 60Co, and X-ray generators) and powerful accelerators made easier the research of food irradiation.

Postharvest Technology of Perishable Horticultural Commodities https://doi.org/10.1016/B978-0-12-813276-0.00017-1

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# 2019 Elsevier Inc. All rights reserved.

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FIG. 17.1

17. IRRADIATION OF FRUITS AND VEGETABLES

The types of electromagnetic radiation composing the electromagnetic spectrum.

Among the early applications of irradiation in plant foods highlights the British Patent 1909 that proposed the using of irradiation to keep the quality of cereals. The use of irradiation to avoid tuber and bulb sprouting was proposed in 1936. In 1958 an electron accelerator was established in Stuttgart (Germany) to irradiate spices at commercial scale, but a year later food irradiation was banned in that country. Irradiation with phytosanitary purposes was firstly used at commercial level at the end of the 1980s to ship mangoes and papayas to the continental United States from Puerto Rico and Hawaii. In the 1990s an irradiation facility was constructed in Florida to treat grapefruits. During this time the exportation of fruits, mainly papayas, from Hawaii to the continental United States increased significantly due to the use of phytosanitary irradiation. Many countries presently use irradiation for insect control and other purposes. Several justified and nonjustified concerns about food irradiation have maintained the use of this technology at commercial scale without significant changes for a long time; however, there is currently an increasing interest in and need of this technology in the food sector.

17.2 TYPES OF IONIZING ENERGY AVAILABLE FOR IRRADIATION OF PLANT FOODS The γ-rays, electron beams, and X-rays are the types of ionizing energy currently used to treat plant foods. The γ-rays consist of high energy (0.662–1.33 MeV) photons released by radioactive elements 60Co and 137Cs. 60Co is currently the common source of γ-rays. It is produced by bombarding 59Co pellets with neutrons for 1.5–2 years. The resultant 60Co is radioactive and decays to nonradioactive 60Ni with a half-life of 5.27 years. 60Co is not water soluble, and it is enclosed in thin stainless steel pencils that reduce heat buildup. The most important advantages of γ-rays are that they penetrate deeply into food materials and that almost all of the emitted energy becomes available for use. 60Co pencils are generally stored under water when not in use. When required for treatment the pencils are lifted out of the water tank to expose foods, contained in totes, to γ-rays. Alternatively, some systems submerge the food enclosed in water-tight carriers into the water tank for exposure to γ-rays. Treatment chambers are composed of 1.5 m thick concrete walls, which avoid the dispersion

17.2 TYPES OF IONIZING ENERGY AVAILABLE FOR IRRADIATION OF PLANT FOODS

FIG. 17.2

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60

Co irradiation plant. (A) general view of product containers entrance to the irradiation chamber (upper conveyor); (B) hydraulic table for product pallets to load containers; (C) control console; (D) inside view of irradiation chamber; (E) 60Co source inside the storage pool; and (F) 60Co with lighting. Courtesy of the “Instituto Nacional de Investigaciones Nucleares” (Mexico).

of energy outside the treatment area (Fig. 17.2). 137Cs sources are rarely used because Cs salts are highly soluble in water and the risk of leaks is high. 137Cs also has a longer half-life of 30 years. Electron beams and X-rays are generated by machines. High-speed electrons generated by a linear accelerator (Fig. 17.3) are directed toward the food using a scanning horn. The main disadvantage of electron beam irradiation is the low penetrability of the electrons into matter. X-rays are produced by the same apparatus that generate electron beams; the difference is

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FIG. 17.3

17. IRRADIATION OF FRUITS AND VEGETABLES

Electron emitter and linear accelerator. Courtesy of MEVEX (US).

that the high-velocity electrons generated in the accelerator are targeted toward an anode consisting of a plate of tungsten or tantalum. The collision with the metal target releases X-rays in the process. These rays are composed by photons varying in energy, depending on the energy of the electrons striking the converter plate. For food irradiation the energy of the striking electrons should be 5 MeV or lower, generating X-rays with a penetrability similar to that of irradiation with 60Co. Electron beam and X-ray machines must also be operated in shielded facilities, but they can be switched on and off in contrast to γ-irradiation sources, which are continuously emitting energy. Only about 7% of the energy of the electrons is converted to X-rays. This inefficiency makes X-rays expensive, limiting the use of this kind of energy to treat foods, although newer more efficient X-ray systems are becoming more popular, especially given that 60Co is becoming more expensive and transport is highly regulated and restricted. There are two main units to measure irradiation. The rad is a unit of the absorbed radiation that was defined in 1953 as the dose causing 100 ergs of energy to be absorbed by 1 g of matter. The rad, a unit of the centimetre-gram-second system of units, was used for long time but replaced by the Gray (Gy), which was named by Louis Harold Gray and adopted by the International System of Units in 1975. One rad is equivalent to 0.01 Gy. These units (Gy and rad) are indistinctly used to express exposition and absorption of irradiation. The Gy is currently the most used unit to measure radiation. In general, irradiation facilities are composed of the radiation source, shielding to protect personnel from radiation exposure and a product-transporting conveyor, which must be synchronized with the exposure of the product to the radiation source. Typically, the shielding includes thick walls of concrete and a pool of water (6 m deep) where the radiation source is kept while it is not used (see Fig. 17.2). The irradiation room and water pool have this kind of thick walls. The shielding provides safety for workers. All irradiation facilities require an efficient air evacuation system to remove the ozone formed by the reaction of oxygen with free radicals generated during the food irradiation process.

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17.3 COMMERCIAL IMPORTANCE OF IRRADIATION OF PLANT FOODS

17.3 COMMERCIAL IMPORTANCE OF IRRADIATION OF PLANT FOODS Food irradiation technology is approved in approximately 60 countries, but its use is limited to a handful mostly in Asia and North America. The interest in this technology and the number of irradiation facilities is increasing, mainly as a consequence of the increase in the international trade of foods. China irradiates 70% of all irradiated food in Asia, primarily garlic, spices, fruit, and dehydrated vegetables. The main spices irradiated in India are turmeric, coriander, mangoes, and chili pepper. In Indonesia, cocoa, spices, and dehydrated vegetables represent more than 85% of irradiated food. Potatoes are the only food irradiated in Japan. Some European countries (Belgium, Czech, Germany, Spain, Estonia, France, Netherlands, Hungary, and Poland) allow irradiated foods, but irradiated plant foods (spices, herbs, and vegetables) in these countries do not represent more than 20% of total irradiated food. In the United States, spices are the most treated plant food with radiation. Other important foods of plant origin irradiated in this country are papayas and sweet potatoes. The United States imports many irradiated fruits, including mangoes, longans, mangosteens, lychees, rambutans, dragon fruit, guavas, sweet limes, grapefruits, and manzano peppers from countries like India, Thailand, Vietnam, and Mexico. Mexico is mainly irradiating guavas and manzano chili for exportation; however, small quantities of other fruits (starfruits, citrus, pomegranate, figs, mango, pitayas, and pitahaya) are also treated in this country. Estimated quantities of irradiated foods by country are shown in Table 17.1. TABLE 17.1

Estimated Quantity (ton) of Irradiated Plant Foods Year

Country/Food

2005

2006

2007

2008

2009

2010

2011

2012

2013

2014

2015

19

129

201

346

585

1095

620

918

1018

866

1480

2

10

20

57

110

15

132

76

29

34

12

1

AUSTRALIA Mangoes Lychees Papayas

22

Peppers

58

28

Tomatoes

413

430

Plums

2

Table grapes

28

MEXICO Guavas

5345

5027

6611

7743

8302

9709

Chilies

97

315

523

595

898

982

Mangoes

213

1002

771

774

781

42

102

4

5

Sweet limes

265

3564

21

Continued

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TABLE 17.1 Estimated Quantity (ton) of Irradiated Plant Foods—cont’d Year Country/Food

2005

2006

2007

2008

2009

2010

2011

2012

2013

2014

2015

Pomegranates

49

135

Starfruits

3

27

Pitahayas

66

Grapefruits

19

Mandarins

10

Figs

1000

SOUTH AFRICA Fresh plant foods

1000

1050

1500

1800

1200

1200

1900

1850

1750

1300

1300

Dried plant foods

200

600

400

220

600

800

750

800

850

1200

1300

Dried vegetables

91.75

951.17

46.2

111.3

Dried fruits

137.45

144.16

122.4

199.65

2.1

237

TURKEY

VIETNAM Lychees Dragon fruits

2000

Rambutan

200

INDIA Spices, dried fruits, fruits Mangoes

1600

2100 157

275

130

100

95

15,000

79,000

295

400

79,000

79,000

UNITED STATES Fruit and vegetables Spices

79,000 79,000

17.4 EFFECTS OF IRRADIATION ON FRESH FRUIT AND VEGETABLES Irradiation has little impact on dried foods, such as spices and seasonings. Fresh fruit and vegetables are metabolically active; therefore irradiation can impact ripening as well as quality attributes. All food components can be split or ionized directly by the atomic nuclei, energetic electrons, or photons of ionizing energy. However, the effects of irradiation on living cells are mainly driven by the action of radiolytic products of water because it is the most abundant component of living cells. Several highly reactive ions and free radicals are formed

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from water by irradiation, especially hydrogen and hydroxyl radicals. These radicals can react with organic molecules, converting them to new free radicals, which collectively can damage macromolecules that are required for life (e.g., enzymes, proteins, lipids, carbohydrates, and nuclei acids). These macromolecules experience changes in their structure, affecting their normal functioning and compromising life. The main changes induced by irradiation in proteins/enzymes include the reduction of the molecular weight, cross-linking, and alterations in their secondary, tertiary, and quaternary structure. Irradiated proteins/ enzymes are more susceptible to the further attack by other compounds due to structural affectation caused by irradiation. All these irradiation-mediated alterations of proteins highly compromise the normal activity of enzymes, with these alterations having positive or negative effects in foods. In the case of nuclei acids, irradiation can cause the breaking of DNA strains and alter the units composing DNA. Pyrimidines are more sensible to irradiation than the purines, with thymine being the most sensible. Sufficient single or double strand breaks of the DNA can overcome repair mechanisms and prevent cell reproduction or reparation or induce cell death. The damage of cell membranes, especially lipids, by radiolytic products also contributes to cell death. The chain reaction of oxidation of membrane lipids highly depends on the concentration of free radicals in the cellular environment. Polysaccharides of fruits and vegetables are also altered by irradiation, especially pectin, which is depolymerized, thus showing alterations in the degree of methyl esterification. Polysaccharides, however, are more resistant to irradiation than other macromolecules. The free radicals formed by irradiation also consume the cellular content of antiradical compounds, weakening the protective systems of cell and compromising the normal functioning of cell. The maximum irradiation dose allowed for foods is 10 kGy; however, fresh fruits typically tolerate doses below 1 kGy. The response of foods to irradiation has been tested at a wide range of doses, including doses above 10 kGy.

17.4.1 Retardation of Ripening Ripening is a complex process characterized by rapid changes in the physical and chemical attributes of fruits and vegetables. These changes are mainly triggered by the autocatalytic production of ethylene. Early studies demonstrated that irradiation generally causes an increase in the respiration rate and production of ethylene, although depending on the irradiation dose and commodity the respiration rate may increase while ethylene biosynthesis decreases. These effects are usually temporary in nature. The impact on ethylene production is greater in partially ripe fruit than in fully ripe fruit, although the opposite can also occur. The treatment of immature fruit may lead to disruption of the ripening process. Irradiation is able to alter the production of substrates and enzymes involved in ethylene biosynthesis (i.e., 1-aminocyclopropane-1-carboxylic acid, 1-(malonylamino)cyclopropane-1-carboxylic acid, 1-aminocyclopropane-1-carboxylate synthase, 1-aminocyclopropane-1-carboxylate oxidase, etc.). This alteration occurs at the transcriptional level almost immediately following irradiation application. However, the alteration of ethylene production by irradiation is often not correlated with the ripening of the irradiated fruit, which suggests that irradiation directly affects the activity or biosynthesis of enzymes involved in the characteristic changes induced by the ripening process. For example, the ethylene biosynthetic pathway in papaya fruit is

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altered by irradiation, but fruit ripening is not closely related to these changes of ethylene biosynthesis. However, it is well known that low irradiation doses delay the postharvest ripening of many fruits, including plantains (0.15–0.3 kGy), bananas (0.2–0.4 kGy), papayas (0.5 kGy), strawberries (0.3 kGy), apples (<0.9 kGy), pears (<0.9 kGy), mangoes (0.2 kGy), peaches (0.1 kGy), etc. This ripening delay typically varies from a few days to 2 weeks. The delay of ripening can be valuable because it makes possible the trade of fruits and vegetables to distant markets. Higher irradiation doses inhibit fruit ripening and may cause physiological damage to the fruit.

17.4.2 Postharvest Weight Loss The effect of irradiation on the postharvest weight loss of fresh fruits and vegetables depends on food type, irradiation doses, and postharvest storage conditions. At doses that can be tolerated by fruits (<1 kGy), irradiation causes a small weight loss, which typically does not exceed 10%. The use of refrigeration after irradiation application can reduce or even inhibit the irradiation-mediated postharvest weight loss in fruits and vegetables. At higher doses (˃1 kGy), irradiation can significantly modify the microstructure of vegetable tissues and consequently their barrier properties and susceptibility to postharvest dehydration. These changes can favor or reduce postharvest weight loss. The most common effect is the exacerbation of the postharvest dehydration, which can be of two or more times that of the nontreated fruit. This is particularly true for citrus and other fruits having cracked peels that favor dehydration. For example the postharvest weight loss in navel oranges increases with the irradiation dose. Similar results have been reported for grapefruit and other citrus fruits; however, this effect of irradiation has not been seen in pummelos, which have a very thick peel. This confirms that the physical properties of the peels are closely related to the modification of the barrier properties of peels by irradiation. Interestingly, in some fruits some irradiation doses can prevent the postharvest dehydration, presumably due to the modification of the peel structure. For example, doses of 1 to 1.3 kGy in steps of 0.1 kGy are able to prevent the dehydration of peaches. The protective effect of some irradiation doses against postharvest dehydration has also been observed in blueberries and pears. The antifungal properties of irradiation also contributes to the preservation of weight. In general, postharvest weight loss induced by irradiation is far less than weight loss experienced during storage.

17.4.3 Firmness Firmness is an important quality attribute of fruits and vegetables that influences consumer acceptance and determines the capacity of the fruit to tolerate handling. Firmness is among the most irradiation-sensitive quality attributes. A decrease in firmness is manifested immediately after an irradiation application, and it can be observed at low irradiation doses (<1 kGy) in raspberries, kiwis, blueberries, some apple varieties, some pear varieties, papaya, oranges, lettuce, and tamarillos, among others. At low irradiation doses, the firmness loss does not exceed 10% of the initial firmness. Differences in firmness between irradiated and nonirradiated fruits also depend on storage conditions. Cold storage reduces the loss of firmness, but it is typically insufficient to inhibit completely the effect of irradiation.

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571

The firmness loss in fruits and vegetables has been explained in terms of the irradiationmediated biosynthesis of ethylene, which can induce the de novo synthesis of enzymes involved in the modification of structural polysaccharides. This hypothesis has been demonstrated in several fruits, including apples, pears, peaches, mangoes, carrots, and others. However, the direct alteration of the structure of cell wall polysaccharides (e.g., pectic substances) is likely the major cause of softening immediately following irradiation and has been observed in many fruits including tomatoes, apples, citrus, and berries. It must be noted that in some cases, low irradiation doses prevent postharvest softening, as has been observed in clemenules, mushrooms, and some pear and lychee varieties. This effect might be related to the inactivation of enzymes involved in ethylene biosynthesis and polysaccharide modification.

17.4.4 Color of Irradiated Foods Color of fruits and vegetables, as visually evaluated, is generally not altered significantly by irradiation. However, the values of tristimulus color change after fruit irradiation. The external color of irradiated plant foods typically becomes darker and more intense than that of nonirradiated fruits, according to their L* values of tristimulus color. These changes are a consequence of the direct alteration of pigments by irradiation, although the modulation of enzyme activity/biosynthesis and ethylene production might also be involved in such changes. However, in most cases the irradiation-mediated changes in pigments is not manifested in tristimulus color values. For example, irradiation of raspberries at 1 kGy causes a higher decrease in the anthocyanin content as compared with doses of 0–0.4 kGy; however, this trend is not observed for tristimulus color values. In mandarins the content of free and esterified carotenoids changes significantly after irradiation application (0–1 kGy) but color changes are minimal. Similar results have been observed for other fruits and vegetables. Even at high irradiation doses the color changes are small, as reported for example, in cherry tomatoes treated at doses of 1.3–5.7 kGy, where the changes of L* and C* were less than 10% in comparison to those of nonirradiated tomatoes.

17.4.5 Sugars Irradiation can increase or reduce the content of sugars in fruits, depending on the fruit, ripening stage, and irradiation dose. Unfortunately the content of sugars in irradiated fruit has been mainly estimated as the content of total soluble solids (TSS), which does not provide a clear effect in this regard because irradiation-mediated changes in sugars are typically small and compounds other than sugars contribute to TSS values. At low irradiation doses (<1 kGy), only small increases or decreases in TSS have been observed. Irradiation-mediated changes in individual sugars are also small. Very low irradiation doses (0.075 and 0.3 kGy) do not alter the content of glucose, fructose, and sucrose in lemons, cucumbers, nectarines, pawpaws, persimmons, zucchinis, Ellendale mandarins; however, such doses cause slight but significant increases in the glucose content in Custard apples and decreases in glucose and sucrose in mangoes and Imperial mandarins. Slightly higher doses (1 kGy) do not alter the content of individual sugars in pummelos. Slight decreases of sucrose and increases of glucose and fructose have been observed in irradiated mandarins

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(0.15, 0.4, and 1 kGy). In some mushrooms varieties the levels of sugars are significantly altered (up to 86%) by high irradiation doses (2–10 kGy), with mushrooms being one of the most affected commodities in this regard. The changes in individual sugars have been attributed to the irradiation-mediated activation or biosynthesis of enzymes (invertases, sucrose synthases, and sucrose phosphate synthases) involved in the metabolism of these compounds. It has also been demonstrated that irradiation promotes the expression of genes codifying these enzymes. Of course, starch hydrolysis and increased respiration rates promoted by irradiation could also influence changes in sugar concentrations.

17.4.6 Organic Acids Low-dose irradiation typically has little effect on titratable acidity and individual organic acids. Low irradiation doses (0.075 and 0.3 kGy) cause a slight increase in the titratable acidity of zucchini and small alterations of the levels of citric and malic acid in red peppers, lemons, some mandarin varieties, mangoes, pawpaws, and persimmons. Higher irradiation doses also typically cause small changes in organic acids and titratable acidity, with some exceptions like raspberries (1 kGy), jujubes (5 kGy), Custard apples (1–1.75 kGy), and cherry tomatoes (5.7 kGy), where the changes in titratable acidity can be from 10% to 76%. Irradiation in the range from 0 to 5 kGy cause a dose-dependent decrease in many organic acids of jujubes, with fruit treated at 5 kGy showing changes of up to 42% in acids as compared with nonirradiated fruit. These changes undoubtedly reveal irradiation-mediated alterations of the normal function of the tricarboxylic acid cycle. Some studies have demonstrated that irradiation shifts the glycolytic pathway to the pentose phosphate pathway, causing a reduction in the production of energy and altering the levels of acids by an increased usage of proteins to enhance the gluconeogenic flux. The increase of organic acids and reducing sugars by irradiation and the probable involvement of amino acids has also been hypothesized in vegetables. Undoubtedly the irradiation-mediated respiration rate of fruits might be involved in the changes observed in organic acids and sugars.

17.4.7 Vitamins Irradiation can alter the content of some vitamins (A, B1, C, and E are the most sensitive) in foods, mostly as a consequence of the free radicals generated by irradiation, as suggested by the immediate reduction of vitamin content in foods by irradiation. Free radical reactions result in the partial conversion of ascorbic acid into dehydroascorbic acid, both of which contribute to total vitamin C activity. Irradiation typically diminishes vitamin C content in plant foods, although increases in this compound have also been induced by irradiation in some fruits. The decrease in vitamin C is typically small (<10%) at low irradiation doses (<1 kGy) and can be seen immediately after irradiation application. The decrease is also influenced by temperature and exposure to oxygen. In plant foods with low vitamin C content, low irradiation doses can cause the total loss of vitamin C, as observed in cucumbers, certain apple varieties, and nectarines treated at 0.075 and 0.3 kGy. But for most fresh fruits and vegetables, vitamin C content is not altered at 1 kGy and lower, as reported for lychees, certain mandarin varieties, pawpaws, certain mango varieties, persimmons, and

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573

certain minimally processed vegetables. The losses of vitamin C increase as the irradiation dose is increased. At irradiation doses between 1 and 6 kGy, fruits like jujube and chestnuts can lose 18%–47% of their vitamin C content. The impact of irradiation in vitamin E has received little attention, probably due to the very low amount of this vitamin in the majority of fruits and vegetables. The existing evidence is conflicting, making it difficult to do a general statement in this regard. However, it is known that vitamin E is sensitive to ionizing energy and that such sensitivity depends on temperature, oxygen, radiation dose, and produce type. Irradiation doses lower than 1 kGy either do not affect the α-tocopherol content or cause slight increases, with some exceptions like tomatoes, which can lose up to 40% in their tocopherol content at doses of 1 kGy. Another exception are mandarins, which lose small amounts of α-tocopherol immediately after irradiation application (0.15, 0.4, and 1 kGy). Spinaches lose 10% of their tocopherol content at doses of 2 kGy. The irradiation-mediated decrease of tocopherol has been explained in terms of the reaction between tocopherol and radiation-induced radicals. The storage conditions and time usually reverse the initial negative effect of irradiation on α-tocopherol content. Thiamin is highly sensitive to irradiation, according to numerous studies conducted in meats. However, there is scarce information about the impact of irradiation in the content of this and other vitamins in fruits and vegetables. Treatment of grains (chickpeas, beans, and lentils) with low irradiation doses (0.25–1 kGy) increases the content of thiamine and riboflavin, especially that of riboflavin. The increase of riboflavin content by low irradiation doses (0.75 kGy) has also been reported in papayas. However, high irradiation doses (5 and 10 kGy) can cause significant changes in thiamin and riboflavin in beans. In jujube, irradiation at 0.5–5 kGy causes significant decreases in a dose-dependent fashion in the contents of pantothenic acid (6%–11%), pyridoxine (2.5%–27%), thiamine (21%–63%), and folic acid (6%–28%) while biotin and riboflavin shows minor decreases (10%). In the leaves of jujube (Zizipus mauritiania), however, niacin, thiamine. and riboflavin are not altered by irradiation doses of 2.5–12.5 kGy, suggesting that the type of plant food impacts the sensitivity of vitamins to irradiation.

17.4.8 Phenolic Compounds Irradiation can either increase or reduce the levels of phenolic compounds in fresh plant foods. The increases are typically observed at low irradiation doses (<1–1.5 kGy) and it is clearly observed for specific phenols, as reported for strawberries, citrus, papayas, avocados, and mangoes. In spinach the content of 14 phenolic acids increases with irradiation dose (0.25–1.5 kGy). High irradiation doses (2–10 kGy) cause the loss of phenols of up to 40%–70% or even higher in rice and mushrooms. The alteration of phenolic content in plant foods by irradiation can occur via several mechanisms. The increase in phenolic content by irradiation has been attributed to the stimulation of gene expression involved in the coding of enzymes of the phenol biosynthetic pathway. Irradiation-induced increases in phenolic compounds have been associated with higher antioxidant capacities in several fruits and vegetables. The stimulation of phenylalanine ammonia lyase activity by irradiation and the subsequent production of polyphenolic compounds have also been demonstrated in some

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plant foods. In some cases the decrease of specific phenols has been attributed to the irradiation-induced transformation of these compounds. In strawberries, for example, the content of certain phenols increases while the content of other phenols decreases as the irradiation dose increases from 2 to 10 kGy. In general the concentration of phenolic compounds appears to be influenced more by variety, season, time of harvest, and origin than by irradiation at doses tolerated by fruits and vegetables.

17.4.9 Carotenoids Irradiation can alter the carotenoid composition in plant foods. Very low doses (<0.12 kGy) of irradiation can increase the content of carotenoids in plant tissues; however, it is unclear if this increase is a consequence of the stimulation of the carotenoid biosynthesis, the accumulation of specific carotenoids, or both. Slightly higher irradiation doses (0.15–1 kGy) can cause the reduction of the content of these compounds, as seen in several fruits and vegetables, with some exceptions like spinach leaves, where irradiation doses up to 1.5 kGy gradually increase (up to 247%) the content of total and individual carotenoids (violaxanthin, antheraxanthin, lutein, zeaxanthin, α-, and β-carotene). The negative effect of irradiation on carotenoid content depends on storage time and conditions, which have a higher impact on carotenoid content than irradiation. In some cases, this negative effect of irradiation is reversed during storage. For example, irradiation of papayas at 0.8 kGy cause an immediate reduction in lycopene, provitamin A carotenoids, and total carotenoids but these decreases are reversed during storage, with irradiated fruit showing higher carotenoid content than nonirradiated papayas at the end of the storage. Similar effects have been observed in other fruits. It should be noted that the change in carotenoid content varies with carotenoid speciation. Thus the content of the majority of carotenoids can decrease but that of few carotenoids can increase, suggesting that irradiation alters the biosynthetic pathway of carotenoids. High irradiation doses (typically above 1 kGy) can cause a total loss of carotenoids. In unripe tomatoes a dose of 3 kGy causes the total loss of the main carotenoids (phytoene, phytofluene, ζ-carotene, lycopene, β-zeacarotene, γ-carotene, and β-carotene). Interestingly the negative effects of irradiation in carotenoid content have been reported for dried plant foods like paprika, where doses of 2.5–10 kGy reduce the majority of carotenoids, except for capsanthin and capsorubin. Due to the low enzymatic activity in dried tissues, the detrimental effect of irradiation on carotenoid content might be attributed to the irradiation-mediated breakdown of carotenoid molecules. However, the generation of hydroxyl radicals from the splitting of water molecules (even at low moisture contents) and the subsequent generation of other highly reactive free radicals (i.e., peroxyl and alkoxyl radicals) might also be involved in carotenoid depletion because these radicals show a strong reactivity with carotenoids.

17.4.10 Chlorophyll There is little research regarding the effects of irradiation in chlorophyll content in fruits and vegetables. Irradiation doses above 2.5 kGy completely destroy chlorophyll in solution. However, chlorophyll in plant tissues is very resistant to irradiation. Early studies with spinach leaves revealed that irradiation doses of 0.25–1.5 kGy cause insignificant decreases in the

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575

content of total chlorophyll and chlorophylls a and b. Similar results have been observed in peas treated at doses of 1.8 and 4.5 kGy. This small but immediate effect of irradiation is typically reversed by storage, with irradiated and nonirradiated commodities showing similar chlorophyll content at the end of storage. This high radio tolerance of chlorophyll seems to be similar in magnitude for chlorophylls a and b, and is independent of the moisture content in the food. Chlorophylls are located in chloroplasts together with fat-soluble materials such as lipids and carotenoids, which confer protection to chlorophylls. Interestingly, very low irradiation doses (2–70 Gy) have been shown to significantly stimulate the biosynthesis of chlorophylls in vegetables like lettuce.

17.4.11 Volatile Compounds Irradiation, even at low doses, can cause important alterations in the aroma of fresh fruits and vegetables. The volatile compounds are mainly altered in quantity rather than in type. In cabbage the content of trans-hex-2-enal increase (41%–78%) immediately after irradiation application, depending on the variety. This increase has been attributed to the irradiationmediated oxidation of linolenic acid via the lipoxygenase pathway. Low irradiation doses (<1 kGy) do not modify the type of volatile compounds in apples; however, their concentration is significantly altered by irradiation, especially the content of alcohols and aldehydes. These irradiation doses cause a 12%–13% increase in volatile compounds of apples, as compare with nonirradiated fruit. Irradiation doses of 0.15 and 0.4 kGy cause increases of the volatile content in mandarins, while irradiation at 1 kGy causes a decrease in the concentration of some of these compounds, especially of aldehydes, ketones, and terpene alcohols. These same irradiation doses cause only minor changes in the volatile content of pummelos. The modification of aroma of plant foods by irradiation has been attributed to the structural alteration of volatile compounds already existing in the food; however, the generation of new compounds has been explained in terms of the radiolytic degradation of amino acids, which can occur at the side chains, and amino- and carboxyl-groups of the α-carbon. The oxidative decomposition of lipids also contributes to the alteration of the profile of volatile compounds in foods.

17.4.12 Disorders Caused by Irradiation Low irradiation doses (<1–1.5 kGy) cause minimal changes in fresh fruits and vegetables, as described above. At higher doses, however, irradiation can cause disorders, including tissue softening, increased fungal/bacterial infections, electrolyte leakage, off-odors, offflavors, increased sensitivity to chilling injury, stem pitting (i.e., artichoke and citrus fruits), oleocellosis in citrus fruits, internal darkening in avocados and other fruits, kernel denting in corn, yellowing of green vegetables and fruits, and skin depressions in many fruits, among others. The negative effects of irradiation highly depend on the irradiation dose and are typically exacerbated at nonrefrigerated conditions. For example, irradiation at 0.4 and 1 kGy increase the susceptibility of mandarins to fungal infections and skin darkening during storage at room temperature, while irradiation at 0.15 kGy confers some protection against these

576

17. IRRADIATION OF FRUITS AND VEGETABLES

disorders. In whole green onions, irradiation at 2.0 kGy achieves the best combination of microbial reduction and maintenance of visual quality. However, at lower doses, microbial reduction is lower, and at higher dose levels browning and shriveling of the green onion leaves with subsequent microbial colonization is typically observed. Besides irradiation dose and storage temperature the cultivar type is also an irradiation factor, as some cultivars of the same produce are more radio tolerant. For example, at the 2–3 kGy doses required to delay mold growth in strawberries, certain varieties can experience significant softening, but irradiated Confitura and Dukat strawberries, for example, maintain quality and delay mold growth with significant shelf life extensions. In general the negative effects of irradiation in fresh fruits and vegetables are typically observed at doses above of 1 kGy.

17.5 SENSORY ATTRIBUTES OF IRRADIATED PLANT FOODS Low-moisture foods such as dried herbs, spices, seasonings, and seeds are generally not affected in sensory quality even at relatively high irradiation dose levels. The irradiation, as with other nonthermal treatments, prevents the loss of aroma, flavor, and pigments that are important quality characteristics of such products. Fresh commodities, on the other hand, can generally tolerate lower doses only. The free radicals generated by irradiation can influence the components that are responsible for texture, taste, and appearance. However, each product responds to irradiation differently and while some of these changes may be measureable by instrumental means, consumers may or may not be able to perceive changes in the texture, production of off-flavor, loss of aroma compounds, and changes in appearance. For example a trained sensory panel found that peaches irradiated at 0.69 and 0.9 kGy had a firmer skin texture and were juicier, darker in flesh color, and less firm. These changes were corroborated with instrumental tests. However, untrained consumers were only able to perceive the changes in texture and juiciness and rated the irradiated peaches higher than untreated fruits. Similarly, irradiation at 0.6 and 0.8 kGy caused the softening of Crimson Seedless grapes as measured using a texture analyzer. However, there was no difference in liking between irradiated (0.6 or 0.8 kGy) and control samples of Crimson Seedless. It seems that small differences caused by low doses on sweetness, color, flavor, and aroma are often not perceived by consumers. More obvious changes in appearance, such as browning, pitting, and softening, are more perceptible and may cause negative impacts on sensory quality.

17.6 CONSUMER ACCEPTANCE OF IRRADIATED FOOD The connotation of the term “radiation” is not a positive one, particularly as it relates to food irradiation; thus consumer acceptance of irradiated foods has always been a challenge. The acceptance by the consumers is further hindered due to a lack of understanding of how irradiation works and its effects on food. This lack of knowledge generates confusion in the minds of the consumers and ultimately leads to a rejection of irradiated foods. Lack of consumer acceptance is exacerbated by the fact that irradiated foods have to be labeled with radura symbol (Fig. 17.4) or clearly indicated at the point of purchase, which consumers

17.6 CONSUMER ACCEPTANCE OF IRRADIATED FOOD

577

FIG. 17.4 The radura symbol.

may perceive as a warning rather than a point of information. Other processing technologies do not have to be indicated on the label nor do chemical treatments, even though some of which may leave a residue in the food or otherwise harm agricultural workers or the environment. Still, some companies have taken to explaining their use of irradiation to improve the safety of the product. For example, Schwan’s and Omaha Steaks highlight the advantages of irradiation for ground beef patties. In New Zealand for example, irradiated mangoes are advertised as “better for the environment,” alluding to reduced chemical use to achieve the phytosanitary treatment. Interestingly a study in Santiago (Chile) revealed that although 95.8% of the surveyed consumers were unfamiliar with the radura symbol, 55.8% of consumers once educated would purchase food that had the symbol, citing their sense of confidence of the safety of such products. Several studies have shown that when you ask a consumer a direct question about their perception of irradiation, a majority will respond with a negative view. However, when they are informed about the benefits the technology offers, they are far more accepting of the technology, although a small percentage of consumers will not change their minds. Positive shifts in the attitudes of consumers toward irradiation are achieved when they are presented with information regarding the nature and benefits of irradiation. Conjoint analysis have shown that appearance is the most important factor for Brazilian consumers in their decision to purchase papayas. They do not respond negatively to irradiation labels, even though the consumers have little understanding of the technology. When the product is available for sale, consumers respond to the availability of the product and are most interested in quality attributes of appearance and flavor. In the last few years, irradiated fresh fruit such as mangoes, dragonfruit, rambutan, guavas, and lychees have

578

17. IRRADIATION OF FRUITS AND VEGETABLES

become available in nonspecialty US supermarkets. Consumer response has been positive even when fruit may be priced relatively high. It may be that the small lettering on the pricetag is difficult to read, but it is more likely that consumers are now more interested in the product and less concerned about the technology. The challenge about consumer perception seems to be more of an issue with distributors and retailers who are unwilling to take a risk of the irradiated food not selling, or worse, inviting negative consumer reviews. While there is much value in educating consumers about the benefits of radiation, educating retailers and distributors would also be highly beneficial.

17.7 CURRENT AND POTENTIAL USES OF THE IRRADIATION OF PLANT FOODS 17.7.1 Control of Food-Borne Pathogens The presence of food-borne pathogens in fruits and vegetables presents a major risk for consumers that could restrict the international trade of these foods. Irradiation doses below 1 kGy allow the reduction of several enteropathogenic bacteria (L. monocytogenes, S. aureus, C. jejuni, E. coli O157:H7, S. typhimurium, S. dysenteriae, etc.). Many parasites are very sensitive to irradiation, and doses of 0.15–0.6 kGy are typically sufficient to inactive them. However, given the low tolerance of fresh fruits and vegetables to irradiation, ionizing energy is not useful to inactivate pathogenic viruses because high irradiation doses (above of 3 kGy) are required to inactivate them. The benefits of irradiation on the improvement of the microbiological quality/safety of fresh fruits and vegetables have been highlighted recently, stating that the use of irradiation for disinfection remains underutilized. For fresh produce, irradiation is particularly suitable for improving safety, especially as the nonthermal treatment does not impact the fresh character of intact and fresh-cut fruits and vegetables. The volumetric treatment provided by these ionizing waves penetrates through the food and destroys organisms that would otherwise be inaccessible and difficult to eliminate using surface treatments, such as sanitizers. The other advantage is that the product can be processed in the final packaging, thus reducing the chances of contamination after handling in the packing house and during storage and distribution. Many factors influence the efficacy of microbial inactivation. Other than irradiation doses the type of organism and food matrix, as well as use of complementary control technologies can help achieve the required sanitization effect. 17.7.1.1 Influence of Organism Type Irradiation inactivates microorganisms by disrupting their genetic material and affecting proteins and membrane lipids. In the genome of microbial cells, sufficient single or double strand breaks of the DNA can overcome repair mechanisms and prevent cell reproduction. Damage to cell membranes by radiolytic products also contributes to cell death. The larger the size of the nucleus and DNA targets, the higher the susceptibility of the organism to irradiation. Prokaryotic bacterial cells that are smaller genomic targets are thus more resistant to irradiation than eukaryotic cells, such as yeasts and molds. Microbial inactivation using radiation is expressed in D10 values, which refer to the dose that can achieve a 1 log or 90% reduction of the target organism. The D10 values for the common vegetative bacterial

17.7 CURRENT AND POTENTIAL USES OF THE IRRADIATION OF PLANT FOODS

579

pathogens found on fresh produce range from 0.15 to 0.5 kGy, with Salmonella spp. among the more resistant of nonspore bacterial pathogens. Vegetative bacteria such as Aeromonas hydrophila, C. jejuni, E. coli, and L. monocytogenes are more sensitive to irradiation than spore formers, such as B. cereus and C. perfringens. D10 values are affected by the medium of radiation, water activity of the food matrix, and temperature. Table 17.2 shows the D10 values for various bacterial pathogen in fresh produce. The US Food and Drug Administration’s (FDA) regulatory limit of 1 kGy for fresh produce would thus achieve a 1.5–5 log reduction in bacterial pathogen counts. Following a major outbreak of E. coli O157:H7 in fresh spinach, the TABLE 17.2 D10 Values of Different Bacteria in Different Produce Items Genus

Species

Produce Item

D10 (kGy)

E. coli

O157:H7

Spinach

0.1

O157:H7

Iceberg lettuce

0.136

O157:H7

Red lettuce

0.35

O157:H7

Green lettuce

0.37

Listeria

Salmonella

Shigella

O157:H7

Boston lettuce

0.45

wild O157:H7

Bitter gourd Roma tomatoes

0.23 0.39

monocytogenes

Spinach

0.20–1.0

monocytogenes

Iceberg lettuce

0.20

monocytogenes

Red lettuce

0.19

monocytogenes

Green Lettuce

0.19

monocytogenes

Boston lettuce

0.19

monocytogenes

Roma tomatoes

0.66

enterica

Spinach

0.19–1.2



Green onions

0.26–0.32

paratyphae A

Bitter gourd

0.28

typhimurium

Pineapple

0.242



Iceberg lettuce

0.25



Red lettuce

0.23



Green Lettuce

0.31



Boston lettuce

0.24

typhimurium LT2 enterica

Roma tomato

0.17–0.56

flexneri

Spinach

0.96

flexneri

Roma tomato

0.98

580

17. IRRADIATION OF FRUITS AND VEGETABLES

FDA raised the limit to 4 kGy to ensure a 5 log reduction; however, produce companies have been unwilling to use irradiation to enhance produce safety. Other than China and Vietnam, no other country uses irradiation to enhance the safety of produce; however, fresh fruits and vegetables typically tolerate irradiation doses below 1 kGy. Irradiation is also highly effective against parasites and helminths. However, there is little research on the irradiation of parasites found in fresh plant foods. Cyclospora (a coccidian parasite) has been implicated in various outbreaks related to raspberries, lettuce, basil, and snow peas. It has been suggested that a dose of 0.5 kGy is effective in killing coccidian parasites’ oocysts in fruits and vegetables. However, studies using Eimeria acervulina in raspberries, as a model system to treat Cyclospora, have revealed that a dose of 0.5 kGy is not completely effective in controlling the oocysts but at a 1 kGy dose or higher the oocysts population is reduced to below detectable limit. Viruses such as hepatitis A, rotavirus, norovirus, and poliovirus have much higher D10 values than bacteria. For example the D10 values (i.e., dose required to reduce virus titers by 90%) of rotavirus in spinach is 1.29 kGy. Poliovirus has an even higher D10 value of 2.35 kGy in spinach. Norovirus is shown to have a D10 value of 4 kGy in cabbage and close to 6 kGy in strawberries, highlighting the high resistance of viruses due to their highly stable viral capsid, their small sizes, and the protective effect of the food matrix. 17.7.1.2 Effect of the Food Matrix The type of food matrix is involved in the infectiveness of irradiation on control of food borne pathogens. D10 values of pathogens can vary significantly on different food matrices and even between varieties of the same product. Moisture content or water activity is probably the most important compositional factor that affects D10 value. For example, the D10 values for E. coli O157:H7 and Salmonella spp. on dry alfalfa sprout seeds are higher (0.6 and 0.97 kGy, respectively) than those on moist vegetables such as lettuce (0.2–0.4 kGy). Thus, dry spices and seasonings are treated at doses above 10 kGy to achieve a sufficient reduction in microbial counts, but fresh produce would need to be treated at much lower dose levels. Smaller compositional differences in food matrices can also affect D10 values. For example the D10 value for E. coli O157:H7, Salmonella and L. monocytogenes vary significantly among lettuce varieties, indicating that D10 values cannot be generalized and should be measured for each specific product. In sprouts, D10 values for E. coli O157:H7 on three types of sprouts vary between 0.26 and 0.34 kGy. The D10 values of Salmonella in two green onion varieties, Banner and Baja Verde, vary between 0.26 and 0.32 kGy. Table 17.3 shows the differences in D10 values for bacteria in various types of food. For some products where the pathogen can be internalized through the stem end, lenticels, calyx, or stomata, irradiation provides a benefit given the volumetric nature of the treatment. However, D10 values can be higher than for the same organism found on the surface. For example the D10 values for E. coli O157:H7 on lettuce with internalized cells vary from 0.3 to 0.45 kGy, which is significantly higher than D10 values for surface inoculated cells. 17.7.1.3 Effect of the Combination of Technologies The use of complementary technologies is also involved in the effectiveness of irradiation on the control of food-borne pathogens. Combining irradiation with other treatments (e.g., the use of sanitizers or cold treatments) can reduce the dose required, especially in cases

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17.7 CURRENT AND POTENTIAL USES OF THE IRRADIATION OF PLANT FOODS

TABLE 17.3 Produce Item Arugula

Inactivation/Log Reduction Irradiation Doses (kGy) of Pathogens Present in Various Foods Whole or Minimally Processed Minimally processed

Bitter gourd Whole

Burdock

Seasoned

Irradiation Source

Storage Irradiation Conditions Dose (kGy)

Log Reduction Achieved

Salmonella

60

4°C

1

5

Listeria monocytogenes

60

2

5

Salmonella

Electron beam

1.4

5

E. coli

Electron beam

1.4

5

Salmonella typhimurium

60

2

BDL

E. coli

60

1

BDL

Staphylococcus aureus

60

2

4

Listeria ivanovii

60

1

BDL

Pathogen

Co Co

Co

5°C

10°C

Co Co Co

Cantaloupe

Sliced

Salmonella

Electron beam

5°C

1

3

Carrot

Peeled and coated with essential oil

Salmonella typhimurium

60

4°C

1

5

Shredded carrot paste

Mix microbes L. monocytogenes E. coli

60

2°C

0.5 0.5 0.26

1

Fresh cut

E. coli

60

5°C

1

BDL

Aerobic pathogenic bacteria

60

1

4

Listeria spp.

γ-Irradiation

1

BDL

Yersinia spp. Salmonella spp.

γ-Irradiation 60 Co

8–10°C 5°C 22°C

1 1 1

BDL 5.6 4.4

Salmonella typhimurium

60

10°C

2

4

E. coli

60

2

4

Staphylococcus aureus

60

2

4

Listeria ivanovii

60

2

BDL

Celery

Coriander (cilantro)

Whole

Cucumber

Whole

Co Co

Co Co

Co Co Co Co

Green onions

Whole

Salmonella

Electron beam

4°C

1.6–2.56

5

Lettuce

Whole

L. monocytogenes

137

4°C

0.19

1

Salmonella

137

0.23–0.31

1

E. coli O157:H7

137

1

4

Cs Cs Cs

4°C

Continued

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17. IRRADIATION OF FRUITS AND VEGETABLES

TABLE 17.3 Inactivation/Log Reduction Irradiation Doses (kGy) of Pathogens Present in Various Foods— cont’d Produce Item

Whole or Minimally Processed

Irradiation Source

Storage Conditions

Irradiation Dose (kGy)

Log Reduction Achieved

Pathogen

Mint

Whole

E. coli O157:H7

60

Co

4°C

1

BDL

Salmonella Total aerobic count

60

Co Co

1 1

BDL BDL

Mushrooms Sliced

Psychrotrophs, spores, and aerobic counts

Electron beam

10°C

1

BDL

Pineapple

Salmonella typhimurium Aerobic plate count

4–10°C

2

5

1

2.8

2

BDL

Spinach

Sliced and freeze dried Blanched and seasoned

Whole

60

60

Co

Salmonella typhimurium

60

Co

E. coli

60

Co

1

3

Staphylococcus aureus

60

Co

2

4

Listeria ivanovii

60

Co

2

4

Lactic acid bacteria

Electron beam

4°C

0.7, 1.4

2, 2.5

E. coli O157:H7

X-ray

4°C

1

3.5

L. monocytogenes

X-ray

1

5.4

S. enterica

X-ray

1

3.4

Shigella flexneri Aerobic plate counts

X-ray E-beam

1 0.7

5.2 2.6

0.5

4+

1.5

4.2 2.3 3.7 3.6

Grape tomato

Whole

E. coli O157:H7

137

Roma tomato

Whole

E. coli O157:H7 L monocytogenes S. enetrica S. flexneri

X-ray

Cs + UV

10°C

5°C

where higher doses might affect quality attributes. Low-dose irradiation can be used as a contributing factor in a hurdle approach along with modified atmosphere packaging, warm water dips, temperature control, surface sanitizers, calcium dips, and essential oils/ antimicrobials. It should be noted, however, that combination treatments may lead to enhanced radiation resistance. For example, Roma tomatoes stored at 10°C (for 0, 24, and 48 h) in modified atmosphere packaging conditions followed by irradiation yield higher D10 values than the samples packaged in normal air conditions. This suggests that the efficacy of irradiation may be affected if Roma tomatoes are being stored then shipped to an offsite

17.7 CURRENT AND POTENTIAL USES OF THE IRRADIATION OF PLANT FOODS

583

irradiation plant under a reduced oxygen atmosphere. Similarly a significant increase in the radiation resistance of L. monocytogenes can be observed in cut Gala apples treated with 3.5% and 7.0% calcium ascorbate (CaA) to maintain firmness. The reason for this resistance is due to the antioxidant effect of CaA that may scavenge free radicals generated from the radiolysis of water. A 3.5% CaA treatment along with a 1.6 kGy irradiation treatment to achieve a 5 log L. monocytogenes reduction maintain firmness and reduce browning of Gala apple slices. In summary, irradiation has the capacity for reducing pathogens significantly without impacting quality. However, the reductions at the doses allowed will not achieve the reductions necessary to eliminate all pathogens unless the initial load is low and/or irradiation is combined with other treatments. Rather than comparing irradiation to thermal pasteurization or sterilization, irradiation should be viewed as a single but important hurdle in a comprehensive food safety program, which will help reduce disease burden.

17.7.2 Control of Fungal Infections in Fruits The effects of the irradiation on spoilage microorganisms depend on many factors, including the fungi species, moisture content, the initial number of spores or microbial cells in the food, the atmosphere surrounding the commodity, distribution and handling conditions, and the application of other antimicrobial technologies. Yeast and mold are generally more sensitive to irradiation than bacteria; however, fungi vary in their response to irradiation. Fungi belonging to Rhizopus and Mucor, common spoilage organisms in fruit, are fairly resistant while Botrytis cinerea and Penicillium expansum can be eliminated at a dose of 1 kGy. In general, multi- and bicellular spores are more resistant to irradiation than unicellular spores of fungi. Irradiation can impact all stages of the life cycle of fungi (i.e., spore formation, germination, and growth of hyphae and mycelium). In addition to the inherent resistance of the fungus, the density of the cells in the host material is a very important factor. Ionizing radiation exerts fungal control by altering molecules in fungal cells as well as the normal physiology of fruit cells. Like other stressing technologies, irradiation can stimulate the biosynthesis of phytoalexins and phytoanticipins, thus increasing the resistance of fresh plant foods to fungal infections. For example, X-ray treatment at 0.51 kGy can induce the scoparone and scopoletin accumulation in clemenules; these compounds are able to inhibit the growth of P. digitatum. Other antifungal compounds induced by irradiation (1–3 kGy) in fruits are scopolin, isonitroso, scetophenone, and rishitin. The radiation can also increase the activity of enzymes (i.e., chitinase, β-1,3-glucanase, phenylalanine ammonia lyase, etc.) and genes (i.e., CCR-1 allele, CAT, CHI2, PPO, and PLA6) involved in defense against fungal infections. However, irradiation at 1 kGy or lower seems to be insufficient to reach to adequately control fungal growth in fresh produce. Additionally, low irradiation doses can induce the formation of fungi strains with either reduced or increased resistance to further irradiation. Several studies have demonstrated that ionizing radiation can reduce or inhibit the growth of several fungi with relevance in postharvest, including several species of the genus Trichothecium, Trichoderma, Stemphylium, Rhizopus, Alternaria, Botrytis, Penicillium, Ceratocystis, etc. The doses used in these studies ranged from 1 to 10 kGy, and the extent of reduction ranged from modest to complete growth inhibition. However, these doses clearly exceed those tolerated by fresh fruits and vegetables, causing damage to tissues and increasing their susceptibility to postharvest fungal infections. However, ionizing radiation can

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17. IRRADIATION OF FRUITS AND VEGETABLES

reduce postharvest fungal infections when combined with other control methods, especially chemicals. The combination of chemicals and irradiation allows the reduction of irradiation doses, as this combination of treatments exerts a synergistic effect. For example the application of sodium dichloro-s-triazinetrione and γ-irradiation (0.4 kGy) effectively control the severity and incidence of postharvest infections of P. digitatum in satsuma mandarins. The combination of this chemical is also useful for the postharvest control of B. cinerea in fresh paprika at irradiation doses that do not compromise the quality of this fruit. The combination of thiabendazole and low doses of γ-irradiation allows the control of postharvest infections in grapefruits. Other chemicals generating a synergistic effect with irradiation in the control of postharvest diseases in grapes, citrus fruits, apples, and tomatoes are aureofungin, captan, benomyl, diphenyl, and calcium chloride. Treatments with hot water (above 50°C) and irradiation represent another combination of technologies exerting a synergistic effect on fungi growth, as hot water immersion confers susceptibility of fungi to irradiation. This kind of combination has shown benefits for the postharvest control of several fungi, such as Hendersonia creberrima, B. cinerea, P. digitatum, R. stolonifer, M. fructicola, and A. alternata, in citrus, peaches, mangoes, papayas, and strawberries, although in many cases the applied irradiation was above of 1 kGy. There is little research in this regard at doses below 1 kGy. Papayas exhibit peel damage at doses close to 1 kGy; however, a combination of lower radiation dose (0.75 kGy) and a hot water dip (50°C for 10 min) is more effective than using radiation or hot water treatment alone. The combination of low-irradiation doses (0.8 kGy) and immersion in hot water (50°C for 10 min) confers additional resistance for papayas against postharvest infections caused by Colletotrichum gleosporioides, Botryodiplodia theobromae, and R. stolonifer. Mild hot treatments (above of 52°C for less than 5 min) and low irradiation doses (below 1 kGy) can be effectively used to control the postharvest decay of citrus fruits, peaches, and mangoes. Undoubtedly the combination of irradiation and hot treatments is expensive, which might limit its commercial application. Modified/controlled atmospheres are technologies highly used for the trade of fruits and vegetables. Currently, there is little information regarding the effect of the combination of these technologies with irradiation on postharvest infections. Some studies allow inferring a synergistic effect of both technologies, thus reducing the irradiation doses; however, this technology combination might be very expensive if used commercially. The combination of modified/controlled atmospheres based in nitrogen and irradiation is useful to preserve berries. The combination of γ-irradiation (0.5 kGy) and the application of commercially available coatings (i.e., Sta-Fresh 2505) have shown to reduce weight loss and improve the appearance and firmness of golden-yellow tamarillos as compared to the untreated control, which is fruit that has been only coated or only irradiated.

17.7.3 Insect Control The international trade of plant foods implies the risk of introducing pests into protected areas if adequate phytosanitary treatments are not applied before shipment. Currently, there are different methods for the disinfestation of insects, including fumigation (methyl bromide, sulfuryl fluoride, and phosphine), cold treatments, hot treatments, irradiation, and controlled atmospheres. Irradiation represents an alternative method to insect control and possesses

17.7 CURRENT AND POTENTIAL USES OF THE IRRADIATION OF PLANT FOODS

585

advantages over the other methods, especially in terms of human safety, fruit quality, time, and environmental impacts. Ionizing radiation causes direct and indirect alterations in DNA and vital components in the cell, compromising the proper communication to repair damage in the cell or replicate, resulting in sterilization or death of the insect. The success and advantages of generic phytosanitary irradiation doses for the postharvest control of pests in fruits and vegetables have clearly been demonstrated. Currently, two generic irradiation doses (0.15 and 0.4 kGy) are approved by the Animal and Plant Health Inspection Services (APHIS) for fruits to be exported to the continental United States, and the maximum irradiation dose allowed in foods by the FDA is 1 kGy. The dose of 0.15 kGy was approved in 1989. These doses have been adopted by many countries. The generic doses of 0.15 and 0.4 kGy allow the control of the most important quarantine pests of fruits and vegetables. On the other hand the World Health Organization/Food and Agriculture Organization of the United Nations (WHO/FAO) allows a maximum irradiation dose of 10 kGy. The generic doses of 0.25 and 0.3 kGy are approved to import lychees and mangoes into New Zealand and to export mangoes from New Zealand to Malaysia, respectively. The success of irradiation as a phytosanitary treatment depends not only on its capacity to kill or neutralize target insects, but also on the tolerance of plant foods to ionizing energy. Depending on the fruit type, irradiation may accelerate ripening and/or induce disorders, which compromise fruit quality. For this reason, each commodity must be evaluated for its tolerance to irradiation. Table 17.4 shows specific doses of γ-irradiation for several insects of relevance in the international trade of fruits and vegetables. As seen in Table 17.4 the generic doses of 0.15 and 0.4 kGy are enough to control most pests. These doses are currently being used to treat several fruits, including carambola, several citrus fruits, guavas, peppers, mangoes, pitahayas, persimmons, pomegranates, and dragon fruit. The term “control” implies the death and sterilization of the insects. The sterilization of insects used to be enough for exportation/importation of fresh plant foods. The sufficiency of insect sterilization as quarantine treatment was noted since 1930, but the acceptance took much time because it was difficult to know whether or not irradiated insects were sterile. At this time, insect sterilization by irradiation is a legal and accepted phytosanitary treatment.

17.7.4 Shelf Life Extension The postharvest shelf life of fruits and vegetables is limited by microbial spoilage, enzymatic reactions, and the onset of senescence. Irradiation can influence all of these factors that limit shelf life, thus reducing or delaying certain reactions and in other cases accelerating them, as described in previous sections of this chapter. Other than sanitizers, few nonthermal treatments can extend the microbial shelf life of raw fruits and vegetables without impacting quality. The extension of shelf life by irradiation has been demonstrated in many intact fruits and vegetables, including onions, citrus fruits, strawberries, plantains, etc. However, irradiation is particularly suited for fresh-cut produce (e.g., peeled, diced, or shredded), which are more susceptible to enhanced decay and have a shorter shelf life as compared to the intact fruit or vegetable. Studies of shredded carrots, pico de gallo, lettuce, cilantro, and sliced apples, among others, have shown significant reductions in aerobic plate counts, lactic acid bacteria, and Enterobacteriacae at dose levels up to 2 kGy with minimal quality effects.

586

17. IRRADIATION OF FRUITS AND VEGETABLES

TABLE 17.4 Minimum Doses of γ-Irradiation Approved for the Control of Pests of Relevance in the International Trade of Fruits and Vegetables Pest

Dose (Gray)

Apple maggot (Rhagoletis pomonella)

60

Mexican fruit fly (Anastrepha ludens)

70

West Indian fruit fly (Anastrepha obliqua)

70

Caribbean fruit fly (Anastrepha suspensa)

70

Plum curculio (Conotrachelus nenuphar)

92

Sapote fruit fly (Anastrepha serpentina)

100

Javis fruit fly (Bactrocera jarvis)

100

Queensland fruit fly (Bactrocera tryoni)

100

Other fruit flies of the Tephritidae family

150

Sweetpotato vine borer (Omphisa anastomosalis)

150

Sweet potato weevil (Cylas formicarius elegantulus)

150

West Indian sweet potato weevil (Euscepes postfasciatus)

150

Codling moth (Cydia pomonella)

200

Oriental fruit moth (Grapholita molesta)

200

Koa seedworm (Cryptophlebia illepida)

250

Litchi fruit moth (Croptphlebia ombrodelta)

250

False red spider mite (Brevipalpus chilensis)

300

Mango seed weevil (Sternochetus mangiferae (Fabricus))

300

Pests of insecta class (excludes pupae/adults of Lepidoptera order)

400

In sliced mushrooms irradiated at and above 0.5 kGy a reduction of microbial counts is accompanied by a concomitant decrease in microbial-mediated enzymatic reactions and a shelf life extension for up to 3 weeks. Sliced mushrooms are predisposed to spoilage by gramnegative psychrotrophic bacteria, particularly Pseudomonas. These bacteria can cause the softening of mushrooms and enhance browning by activating polyphenolic oxidase. Pseudomonas are very susceptible to irradiation, thus low-dose irradiation can effectively reduce microbial counts and preserve the texture and color of mushrooms. The extension of shelf life by irradiation has also been demonstrated for many minimally processed fruits and vegetables.

17.7.5 Other Applications Commercially, irradiation has been used for sprout inhibition of potatoes in 25 countries for the past 70 years. Irradiation is also used to avoid the sprouting of garlic and onions in many countries, particularly in India and China. This is the most popular use of irradiation

17.9 CONCLUSIONS

587

at commercial conditions. Radiation can prevent sprouting in these products at very low doses (i.e., in the range of 0.05–0.2 kGy) primarily by impacting DNA. Potato sprouting and quality depend on storage temperature and relative humidity as well as the time between harvest and irradiation. In general, low irradiation doses and quick irradiation after harvest promote potato quality. Furthermore the storage of the treated potatoes at the optimum temperature could prevent the loss of vitamin C and formation of reducing sugars. For onions, less than 0.1 kGy can prevent sprouting. Similar to potatoes, sprouting is best inhibited when the onions are treated soon after harvest while still in their dormant state. However, internal browning has been observed in irradiated onions stored for an extended period of time. For garlic cloves, 0.060 kGy is used in India to inhibit sprouting, although a slightly higher dose of 0.08–0.09 kGy can also reduce rotting and weight loss for up to 11 months. Irradiation can be used to reduce the postharvest growth of asparagus and mushrooms. Doses of 0.05–0.15 kGy are enough to limit the postharvest growth of asparagus and resultant curvature. Similar doses (0.06–0.5 kGy) are used to avoid cap opening and stalk growing in mushrooms.

17.8 REGULATIONS In 1980 the Joint Expert Committee on Food Irradiation formed by the WHO, the International Atomic Energy Agency (IAEA), and FAO established that foods treated up to an overall average dose of 10 kGy for any purpose were safe and wholesome. The dose for specific foods varies among countries. The Codex General Standard for the Labeling of Prepackaged Foods (ftp://ftp.fao.org/codex/Publications/Booklets/Labelling/Labelling_2007_EN.pdf) states that “the label of a food which has been treated with ionizing radiation shall carry a written statement indicating that treatment in close proximity to the name of the food.” The Codex standard allows for the optional use of the radura symbol (Fig. 17.4). Countries vary in the specific doses and many require that irradiated foods be labeled. The FDA requires that irradiated fresh produce be labeled with a radura symbol and a statement saying “treated by radiation” or “treated with radiation.” The FDA permits a maximum of 1 kGy for the irradiation of fresh fruits and vegetables to inhibit the growth of decay organisms and to delay the maturation and ripening of fresh foods or for the disinfestation of arthropod pests.

17.9 CONCLUSIONS Low-dose irradiation is useful to improving and maintaining the safety and quality of fresh fruits and vegetables. Higher doses can induce negative effects on quality. Irradiation presents advantages over other existing technologies, especially because it does not affect the raw character of the fresh product. It can also be applied to the final package and has a lower impact on the environment compared to other technologies. Despite these advantages, lowdose irradiation is underutilized as a postharvest technology mainly due to the labeling requirements and lack of understanding about how ionizing energy works. In the last decade, there has been a tremendous growth in its use as phytosanitary treatment. The impact of low

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17. IRRADIATION OF FRUITS AND VEGETABLES

irradiation doses on fresh plant foods is highly variable and depends of many factors, including variety, maturity, and packaging, as well as the conditions of storage and distribution. To ensure optimal quality, research must be conducted to understand the mechanisms by which irradiation alters the physicochemical attributes of plant foods at allowed doses.

Acknowledgment J.J. Ornelas-Paz thanks CONACYT (Mexico) for the support provided for his sabbatical leave at Chapman University.

Further Reading Abad, J., Valencia-Chamorro, S., Castro, A., Vasco, C., 2017. Studying the effect of combining two nonconventional treatments, gamma irradiation and the application of an edible coating, on the postharvest quality of tamarillo (Solanum betaceum Cav.) fruits. Food Control 72, 319–323. Banerjee, A., Variyar, P.S., Chatterjee, S., Sharma, A., 2014. Effect of post harvest radiation processing and storage on the volatile oil composition and glucosinolate profile of cabbage. Food Chem. 151 (Suppl. C), 22–30. Bhumiratana, N., Belden, L.K., Bruhn, C.M., 2007. Effect of an educational program on attitudes of California consumers toward food irradiation. Food Prot. Trends 27 (10), 744–748. de Figueiredo, S.G., Silva-Sena, G.G., de Santana, E.N., dos Santos, R.G., Oiano Neto, J., de Oliveira, C.A., 2014. Effect of gamma irradiation on carotenoids and vitamin C contents of papaya fruit (Carica papaya L.) Cv. Golden. Food Process. Technol. 5 (6), 1–5. Deliza, R., Rosenthal, A., Hedderley, D., Jaeger, S.R., 2010. Consumer perception of irradiated fruit: a case study using choice-based conjoint analysis. J. Sens. Stud. 25 (2), 184–200. D’Innocenzo, M., Lajolo, F.M., 2001. Effect of gamma irradiation on softening changes and enzyme activities during ripening of papaya fruit. J. Food Biochem. 25 (5), 425–438. Eustice, R.F., Bruhn, C.M., 2012. Consumer acceptance and marketing of irradiated foods. In: Fan, X., Sommers, C.H. (Eds.), Food Irradiation Research and Technology. John Wiley & Sons, Inc, pp. 173–195. Golding, J.B., Blades, B.L., Satyan, S., Jessup, A.J., Spohr, L.J., Harris, A.M., Banos, C., Davies, J.B., 2014. Low dose gamma irradiation does not affect the quality, proximate or nutritional profile of ‘Brigitta’ blueberry and ‘Maravilla’ raspberry fruit. Postharvest Biol. Technol. 96 (Suppl. C), 49–52. Gunes, G., Watkins, C.B., Hotchkiss, J.H., 2000. Effects of irradiation on respiration and ethylene production of apple slices. J. Sci. Food Agric. 80 (8), 1169–1175. Hallman, G.J., 2012. Generic phytosanitary irradiation treatments. Radiat. Phys. Chem. 81 (7), 861–866. Hussain, P., Meena, R., Dar, M., Wani, A., Mir, M., Shafi, F., 2007. Effect of gamma-irradiation and refrigerated storage on mold growth and keeping quality of strawberry (Fragaria sp) cv ‘Confitura’. J. Food Sci. Technol. 44 (5), 513–516. Hussain, P.R., Wani, A.M., Meena, R.S., Dar, M.A., 2010. Gamma irradiation induced enhancement of phenylalanine ammonia-lyase (PAL) and antioxidant activity in peach (Prunus persica Bausch, Cv. Elberta). Radiat. Phys. Chem. 79 (9), 982–989. Iglesias, I., Fraga, R., 2000. Preservation of garlic by irradiation. I. Main results during the last 10 years. Alimentaria 37 (311), 55–56. Jain, A., Ornelas-Paz, J.J., Obenland, D., Rodriguez, K., Prakash, A., 2017. Effect of phytosanitary irradiation on the quality of two varieties of pummelos (Citrus maxima (Burm.) Merr). Sci. Hortic. 217, 36–47. Jin, P., Wang, H., Zhang, Y., Huang, Y., Wang, L., Zheng, Y., 2017. UV-C enhances resistance against gray mold decay caused by Botrytis cinerea in strawberry fruit. Sci. Hortic. 225, 106–111. Junqueira-Gonc¸alves, M.P., Galotto, M.J., Valenzuela, X., Dinten, C.M., Aguirre, P., Miltz, J., 2011. Perception and view of consumers on food irradiation and the Radura symbol. Radiat. Phys. Chem. 80 (1), 119–122. Kim, G.C., Rakovski, C., Caporaso, F., Prakash, A., 2014. Low-dose irradiation can be used as a phytosanitary treatment for fresh table grapes. J. Food Sci. 79 (1), S81–S91. Kim, H.J., Feng, H., Toshkov, S.A., Fan, X., 2005. Effect of sequential treatment of warm water dip and low-dose gamma irradiation on the quality of fresh-cut green onions. J. Food Sci. 70 (3), M179–M185.

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Kume, T., Todoriki, S., 2013. Food irradiation in Asia, the European Union, and the United States: a status update. Radioisotopes 62 (5), 291–299. McDonald, H., Arpaia, M.L., Caporaso, F., Obenland, D., Were, L., Rakovski, C., Prakash, A., 2013. Effect of gamma irradiation treatment at phytosanitary dose levels on the quality of ‘Lane Late’ navel oranges. Postharvest Biol. Technol. 86 (Suppl. C), 91–99. McDonald, H., McCulloch, M., Caporaso, F., Winborne, I., Oubichon, M., Rakovski, C., Prakash, A., 2012. Commercial scale irradiation for insect disinfestation preserves peach quality. Radiat. Phys. Chem. 81 (6), 697–704. Moreira, R.G., Puerta-Gomez, A.F., Kim, J., Castell-Perez, M.E., 2012. Factors affecting radiation D-values (D10) of an Escherichia coli cocktail and Salmonella typhimurium LT2 inoculated in fresh produce. J. Food Sci. 77 (4), E104–E111. Murugesan, L., Williams-Hill, D., Prakash, A., 2011. Effect of irradiation on salmonella survival and quality of 2 varieties of whole green onions. J. Food Sci. 76 (6), M439–M444. Naresh, K., Varakumar, S., Variyar, P.S., Sharma, A., Reddy, O.V.S., 2015. Effect of γ-irradiation on physico-chemical and microbiological properties of mango (Mangifera indica L.) juice from eight Indian cultivars. Food Biosci. 12 (Suppl. C), 1–9. Ndoti-Nembe, A., Vu, K.D., Han, J., Doucet, N., Lacroix, M., 2015. Antimicrobial effects of nisin, essential oil, and γ-irradiation treatments against high load of Salmonella typhimurium on mini-carrots. J. Food Sci. 80 (7), M1544–M1548. Niemira, B.A., 2003. Radiation sensitivity and recoverability of Listeria monocytogenes and Salmonella on 4 lettuce types. J. Food Sci. 68 (9), 2784–2787. Niemira, B.A., 2008. Irradiation compared with chlorination for elimination of Escherichia coli O157:H7 internalized in lettuce leaves: influence of lettuce variety. J. Food Sci. 73 (5), M208–M213. Ornelas-Paz, J.J., Meza, M.B., Obenland, D., Rodrı´guez, K., Jain, A., Thornton, S., Prakash, A., 2017. Effect of phytosanitary irradiation on the postharvest quality of seedless Kishu mandarins (Citrus kinokuni mukakukishu). Food Chem. 230, 712–720. Prakash, A., 2016. Particular applications of food irradiation fresh produce. Radiat. Phys. Chem. 129 (Suppl. C), 50–52. Prakash, A., Foley, D., 2004. Improving safety and extending shelf life of fresh-cut fruits and vegetables using irradiation. In: Komolprasert, V., Morehouse, K.M. (Eds.), Irradiation of Food and Packaging. American Chemical Society, pp. 90–106. Prakash, A., Guner, A.R., Caporaso, F., Foley, D.M., 2000. Effects of low-dose gamma irradiation on the shelf life and quality characteristics of cut Romaine lettuce packaged under modified atmosphere. J. Food Sci. 65 (3), 549–553. Rashid, M.H.A., Grout, B.W.W., Continella, A., Mahmud, T.M.M., 2015. Low-dose gamma irradiation following hot water immersion of papaya (Carica papaya Linn.) fruits provides additional control of postharvest fungal infection to extend shelf life. Radiat. Phys. Chem. 110, 77–81. Roberts, P.B., Henon, Y.M., 2015. Consumer response to irradiated food: purchase versus perception. Stewart Postharvest Rev. 11 (3), 1–6. Rojas-Argudo, C., Palou, L., Bermejo, A., Cano, A., del Rı´o, M.A., Carmen Gonza´lez-Mas, M., 2012. Effect of X-ray irradiation on nutritional and antifungal bioactive compounds of ‘Clemenules’ clementine mandarins. Postharvest Biol. Technol. 68 (Suppl. C), 47–53. Shi, H., Chen, K., Wei, Y., He, C., 2016. Fundamental issues of melatonin-mediated stress signaling in plants. Front. Plant Sci. 7, 1–6. Surendranathan, K., Nair, P., 1980. Carbohydrate metabolism in ripening banana and its alteration on gamma irradiation in relation to delay in ripening. J. Ind. Inst. Sci. 62 (8), 63–80. Topuz, A., Ozdemir, F., 2003. Influences of γ-irradiation and storage on the carotenoids of sun-dried and dehydrated paprika. J. Agric. Food Chem. 51 (17), 4972–4977. Villegas, C.N., Chichester, C.O., Raymundo, L.C., Simpson, K.L., 1972. Effect of γ-irradiation on the biosynthesis of carotenoids in the tomato fruit. Plant Physiol. 50 (6), 694–697. Yoon, M., Jung, K., Lee, K.-Y., Jeong, J.-Y., Lee, J.-W., Park, H.-J., 2014. Synergistic effect of the combined treatment with gamma irradiation and sodium dichloroisocyanurate to control gray mold (Botrytis cinerea) on paprika. Radiat. Phys. Chem. 98, 103–108. Zaman, A., Ihsanullah, I., Shah, A.A., Khattak, T.N., Gul, S., Muhammadzai, I.U., 2013. Combined effect of gamma irradiation and hot water dipping on the selected nutrients and shelf life of peach. J. Radioanal. Nucl. Chem. 298 (3), 1665–1672.