The nature of ionizing radiation
Ionizing radiation results in the breaking of chemical bonds due to electromagnetic radiance or high-energy particles. The ionizing portion of the electromagnetic spectrum includes visible light and shorter wavelengths, although visible light ionizes only certain chemicals, such as chlorophyll that is ionized to initiate photosynthesis. Ultraviolet light (10 to 400 nm with photon energies of 3 to 124 eV) is ionizing and has been researched as a phytosanitary treatment for surface pests (Heather and Hallman 2008). It is not commercially used and will not be covered in this review. Gamma rays from the isotopes cobalt-60 (1.17 and 1.33 MeV) and cesium-137 (0.66 MeV) may be legally used for food irradiation according to the U.S. Food and Drug Administration and the Codex Alimentarius Commission (CAC 2003). Cobalt-60 is bred from standard nonradioactive cobalt (atomic weight 58.9) via neutron irradiation. It has a half-life of 5.27 y and decays to standard nickel. Cesium-137 is a fission product of uranium and plutonium and is recovered when processing spent nuclear fuel. It has a half-life of 30.07 y and decays to barium-137 m. Although cesium-137 could be used in food irradiation, it is not done so on a commercial scale; and because it is soluble in water, its availability has been strictly regulated, and it will probably not be used in food irradiation in the near future.
Machine sources of radiation produce electrons and X-rays. Electrons are high-energy particles that can be used for food irradiation at energy levels up to 10 MeV. An electron beam (e-beam) directed at a heavy metal, such as tantalum or gold, will give off X-rays, and energies up to 7.5 MeV are allowed for food irradiation. At best, about 14% of the energy from an e-beam is converted to X-rays with the rest given off as heat. The energy levels emitted by all of these sources are below those that could lead to radioactivity in food.
Irradiation, whether by isotopes or machine sources (e-beam or X-ray), has the same mode of action: the gamma rays, X-rays, or electrons knock electrons out of their orbits thus creating ions. The free electrons further collide with other electrons creating an electron shower. Radicals are formed and cause further damage to large organic molecules such as DNA therefore stopping further development of irradiated organisms.
Efficacy of phytosanitary irradiation
Phytosanitary irradiation (PI) differs from all other commercial treatments in one important technical consideration: the end point of the treatment is not acute mortality but prevention of further biological development and reproduction (Table 1). Irradiated arthropods will eventually die, but Hallman (2000) has shown that some may live as long as or even longer than nonirradiated ones at the doses required to prevent reproduction.
Inspection of commodities treated for phytosanitation is an independent form of verifying that the treatment is efficacious and has been done correctly. If live quarantine pests are found upon inspection for all other treatments except irradiation, it is concluded that the treatment was not done, done subefficaciously, or the commodity was reinfested after treatment, and the consignment is rejected. Further research may need to be conducted to determine if the treatment protocol must be changed. For example, after live Mediterranean fruit fly, Ceratitis capitata (Wiedemann), larvae were found in the United States in mandarin oranges from Spain that had supposedly been properly cold-treated in 2001, 3 cold treatment schedules were lengthened by 13% to 17% and 2 were withdrawn altogether in an attempt to prevent future incidents (Heather and Hallman 2008).
The measures of efficacy used for PI are, broadly speaking, prevention of completion of development for those pests not found as pupae or adults on the exported commodity or prevention of reproduction for those pests that can be present as pupae or adults. For example, the measure of efficacy for fruit flies of the family Tephritidae (that only occur as eggs or larvae on fruit) is prevention of the emergence of adults (IPPC 2009a). The measure of efficacy for the plum curculio, Conotrachelus nenuphar (Herbst), is prevention of reproduction when adults are irradiated (IPPC 2010).
Because insects do not quickly die after irradiation, there is no independent verification of treatment efficacy for PI. That places a greater burden compared with all other treatments on the research, implementation, and regulation of PI to ensure that the treatment is efficacious. That challenge has been met by researchers and plant protection agencies in various countries as well as the International Plant Protection Convention that issued an International Standard for Phytosanitary Measures on PI in 2003 (IPPC 2003).
History of phytosanitary irradiation
Shortly after ionizing radiation was discovered in the late 19th century, it was noted that biological organisms could be reproductively sterilized with relatively low doses that showed no other obvious gross effects (Hunter 1912). Early attempts to use radiation to prevent arthropod reproduction found little effect because doses used were too low (Hunter 1912; Morgan and Runner 1913). Soon researchers began using doses high enough to stop development and reproduction. Runner (1916) found that Lasioderma serricorne (cigarette beetle) egg age was positively related to the dose required to prevent egg hatch and that larvae hatching from irradiated eggs may not develop further. Although irradiated larvae remained alive some time after treatment, they became steadily less active and did not pupate. The larvae remained alive longer than the normal time required for the larval stage. Irradiation of pupae reduced adult emergence and prevented oviposition by the adults that did emerge. Irradiation of adults did not affect activity, mating, oviposition, or length of life, although no eggs laid hatched. Observations that insects would mate normally after irradiation but not reproduce led to the successful use of irradiation in the sterile insect technique, which uses massive numbers of factory-reared insects reproductively sterilized with radiation and released in the field to sexually outcompete and reduce population levels of wild pests, sometimes to extinction (Dyck and others 2005).
Irradiation as a commercial insect control technique was applied for the first time in the early 1910s to tobacco products, although it seems to have been ineffective because of the low doses used (Morgan and Runner 1913). Adequate dosimetry did not exist then (Imai and others 2006). In 1929, a more effective X-ray source with a conveyor was installed to irradiate cigars but the system was eventually replaced by fumigation (Diehl 1995) that was cheaper, more reliable, and easier to use than the X-ray equipment available then.
The first commercial irradiation of food was to disinfect spices in the Federal Republic of Germany in 1957 (Diehl 1995). Although food irradiation was legislatively prohibited in that country a couple of years later until 2000, spice disinfection is the chief use of food irradiation worldwide today with over 185600 tons irradiated each year (Kume and others 2009). The first use of food irradiation for a fresh commodity was on potatoes in Canada in 1965 to inhibit sprouting (Diehl 1995). Cobalt-60 was the source, and the factory could treat 15000 tons per month. However, the facility closed after one season due to financial problems. Today, irradiation is used to prevent sprouting of 88200 tons of potatoes and onions in China, Japan, and India (Kume and others 2009). In the world today, over 400000 tons of food are irradiated every year among spices, meat, and fresh fruits and vegetables.
Until the late 1920s, phytosanitary treatments were based on fumigation or nonsynthetic pesticide applications. The chemicals used then were largely not safe enough to be used on food but were used on nursery stock and other nonfood items that could carry invasive species. In 1929, nonchemical treatments (heated air and cold) were used as phytosanitary treatments against the Mediterranean fruit fly, Ceratitis capitata, infesting citrus fruit in Florida. At about the same time, Koidsumi (1930) first mentioned using radiation as a phytosanitary treatment to rid fruit of fruit flies in Taiwan. He suggested that acute mortality was not necessary to provide quarantine security and that prevention of adult emergence was a reasonable objective for fruit flies. This is the end point used for fruit flies today.
Research into PI accelerated in the 1960s. In 1972, Hawaii filed a petition to the U.S. Food and Drug Administration (FDA) to use PI on papayas (Moy and Wong 2002) and 14 years later the FDA (1986) approved the use of irradiation up to 1 kGy to disinfest foods of arthropods at doses up to 1 kGy. The food must be labeled with the radura logo (Figure 1) and the statement “treated with radiation” or “treated by irradiation.” That same year the first commercial use of PI occurred when one load of irradiated mangoes was shipped from Puerto Rico to Florida (Heather and Hallman 2008). This shipment was part of a search for alternatives to the fumigant ethylene dibromide used as a phytosanitary treatment for fruit that was then being banned as a health risk. Another alternative treatment, hot water immersion, was used for mangoes, and further irradiation treatments were not done.
Figure 1–. Radura, the international green-colored symbol to indicate that a food has been irradiated. A variation by the U.S. Food and Drug Administration uses empty green outlines of the 2 leaf-like parts (FDA 1986). The plant-like structure represents agricultural products in a closed package (the circle) broken in the upper half by penetrating ionizing rays or particles (Ulmann 1972).
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A single pilot shipment of Hawaiian papayas irradiated at a small research facility was sent to California in 1987, and in 1989 APHIS approved an irradiation treatment of 150 Gy for papayas from Hawaii (APHIS 1989). However, that treatment was never used by the fruit industry because of perceived problems with consumer acceptance, the large capital investment required, and logistics in moving all quarantine fruit through one facility (Moy and Wong 2002). Funding from the U.S. Department of Energy that was mandated by the U.S. Congress for a food irradiation facility in Hawaii ran out after 2 X-ray sources were funded in Iowa and Florida. Alternative heat treatments were developed for papayas.
In 1992, a cobalt-60 facility was completed in Mulberry, Florida, to irradiate grapefruits as a phytosanitary treatment against Caribbean fruit fly, Anastrepha suspensa, to replace ethylene dibromide making it the first irradiation facility in the world built expressly for PI. However, other phytosanitary measures were used and commercial irradiation of grapefruit was not done; the cobalt-60 facility was used for other types of food irradiation. In 1999, the facility began to be used for PI when guavas were irradiated and shipped to Texas and California; a few other fruits (carambola and grape) have been commercially irradiated. In 2000, the facility began irradiating white-fleshed sweet potato for shipment to California (Hallman 2001). This was the first use of PI expressly for a quarantine pest that may occur in the adult stage (sweet potato weevil, Cylas formicarius elegantulus) on shipped commodities and represents a major step in acceptance of PI because plant protection organizations are more concerned about having live, albeit reproductively sterile, adults on imported commodities than live immature stages, as is the case with fruit flies.
Moy and Wong (2002) discuss the first years of continuing commercial use of PI in Hawaii starting in 1995. Although this was not the first commercial use of PI for tropical fruits in the world (that honor goes to the 1-time shipment of Puerto Rican mangoes 9 y earlier) because the FDA (1986) did not approve the process for fruits until 1986, it is paramount because PI has been used increasingly every year since then. Personnel from the Univ. of Hawaii and Hawaii Dept. of Agriculture decided in 1994 to forge ahead with PI and obtained a limited use permit by APHIS in early 1995 to allow papayas to be air-freighted to a cobalt-60 facility in Morton Grove, Illinois, to be irradiated with 250 Gy. That dose was established after Hallman (1994) noted that research done in Hawaii did not support doses lower than that for the quarantine fruit flies there. The first shipment was on April 5th, and the papayas were distributed to supermarkets in Illinois and Ohio where market and consumer acceptance were “excellent” (Moy and Wong 2002). Over the next 5 y, an increasing amount and variety of irradiated Hawaiian fruits were shipped to more markets (Table 2). Fruits were irradiated at 2 facilities near Chicago and 1 at Whippany, New Jersey, and distributed to grocery stores in California, Florida, Illinois, Indiana, Iowa, Massachusetts, Minnesota, Michigan, New Jersey, New York, Ohio, Oregon, Pennsylvania, Texas, Washington State, and Washington, DC.
Table 2–. Commercial shipments of Hawaiian fruits to the U.S. mainland between 1995 and 2000 for irradiation at 250 Gy (Moy and Wong 2002). Beginning in August 2000, commodities were irradiated in a newly built X-ray facility in Hawaii, and amount shipped (mostly sweetpotato) reached 4000 tons/year.
|Fruit||Total quantity shipped (tons)|
In 1998, a company proposed to install a cobalt-60 facility in Hilo, Hawaii, where most of the commercial papaya production is located. Opposition arose to the presence of radioactive isotopes, but a ballot initiative to ban radioactive materials in a commercial irradiator there was narrowly defeated. The company decided not to proceed anyway and 2 local entrepreneurs entered into a partnership with a company to build an X-ray facility in Keaau using a $6.75 million loan through the USDA Rural Development Business and Industry Guaranteed Loan Program. The facility began operating in August, 2000.
The lessons Moy and Wong (2002) list from this experience are (1) that markets are not adverse to irradiated produce if the quality and price are good; (2) consumers are increasingly accepting irradiated food in the United States; (3) regulatory agencies in the United States are taking the initiative to move the technology forward; and (4) growers and the business community will step forward to support food irradiation.
Current applications of phytosanitary irradiation
Between 500 to 750 tons of guava continue to be irradiated each year in Florida at a dose of 250 to 550 Gy. The minimum required dose is 70 Gy for the pest of concern (Caribbean fruit fly) but that low dose is difficult to measure with the dosimetry system currently used, and the guavas tolerate the treatment well. Sweet potatoes are not currently being irradiated.
The opening of the X-ray facility in Hawaii in 2000 allowed for a greater diversity and quantity of produce to be irradiated at a more economical cost. Capacity of the facility is >13000 tons/year when operated at 0.4 kGy; about a third of that is realized. At first, papayas were about two-thirds of the volume treated with rambutan and lychee making up most of the rest. Today 75% of the volume irradiated is purple-fleshed sweet potato, at 150 Gy for 3 pests, and no papayas are irradiated. After sweet potato, rambutan and longan are the most irradiated, with smaller quantities of apple-banana (Musa acuminata), curry leaf, dragon fruit (Hylocereus spp.), and mangosteen irradiated at 400 Gy for a variety of pests. All of the products irradiated in Hawaii are sent to the U.S. mainland.
The first international use of PI was in December, 2004, when Australia sent one-half ton of irradiated mangoes to New Zealand. Exports have steadily increased (Figure 2) and now Australia sends irradiated lychee as well. Papaya was irradiated before, but cannot compete in price (cost of irradiation is U.S. $106/ton) with heat-treated papaya, currently.
Figure 2–. Tons of irradiated mangoes exported from Australia to New Zealand by year ending the season. Amount in 2004 was 0.5 ton.
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On March 2, 2006, the U.S. president and the Indian prime minister signed an agreement as part of a broad set of bilateral initiatives that their respective countries would work together to facilitate entry of Indian mangoes to the United States after 17 years of being prohibited for phytosanitary reasons. Irradiation was chosen as a phytosanitary measure that could solve the issues involved. Five wk before this agreement was signed, the United States approved a generic dose of 400 Gy for all insects except pupae and adults of Lepidoptera (APHIS 2006b). This dose would cover all of the insects that are quarantine pests on Indian mangoes bound for the United States. On April 27, 2007, the first irradiated Indian mangoes reached the United States by air freight, and by the end of the season 157 tons had been shipped. In 2008, the total rose to 275 tons. In 2009, 1 14.5-ton shipment was successfully done by boat using low oxygen atmosphere and cold to prolong shelf life. Shipment by boat would reduce costs of the mangoes but it takes 3 wk, which is close to the limit that mangoes tolerate in cold storage. During 2009 and 2010, the amount of irradiated mangoes exported to the United States dropped to 130 and 95 tons, respectively, and no more shipments were made by boat. The lower volume of export during the last 2 y is attributed to mango crop failures in the region in 2009 and problems in air freight due to volcanic ash over Europe in 2010. Irradiated Indian mangoes cost about 4 times the hot water treated Mexican mangoes, but the quality of the cultivars shipped is claimed to be better, and there seems to be a small market for these high-priced but good-quality mangoes in the United States. Some of these mango cultivars do not tolerate hot water immersion well. There have been reports of irradiated mangoes arriving in poor quality, although that may be due more to the shipping conditions than the radiation.
The first irradiated Thai fruit (longan and mango) arrived at the Los Angeles, California, airport on November 1, 2007. Since then, over 70% of the fruit is shipped by boat because of the lower cost compared to air transport, and most of the fruit shipped are longan because they can tolerate the 3-wk boat trip. Mangosteen and rambutan have also been shipped by air. Thailand has permission to irradiate and ship lychee and pineapple to the United States, but has only done test shipments of lychee. Over 4080 tons of Thai fruit have been irradiated and shipped to the United States since late 2007.
In the autumn of 2008, both Vietnam and Mexico started shipping irradiated fruit to the United States. Vietnam has only been given permission by APHIS to ship dragon fruit, although they are hoping to eventually gain permission for other fruits, such as longan, lychee, and rambutan. The dragon fruit goes by boat, and about 500 tons have been shipped to date. Chile will become the third country to receive irradiated fruit when Vietnam begins sending irradiated dragon fruit by the end of 2010.
On 21st November, 2008, the first shipments of irradiated Mexican guavas began crossing the border into the United States and by the end of the year 257 tons had been exported (Table 3). The next year exports jumped to 3623 tons of mostly guava, with some grapefruit and mango. In 2010, Mexico exported over 10000 tons of 5 types of irradiated fruits to the United States, making it the world's largest user in volume of PI. The country also has permission to ship irradiated orange and tangerine to the United States, which it may start doing in 2011. Mexico enjoys the advantage of low cost, rapid land transport for its irradiated fruits to the United States.
Table 3–. Mexico is currently the world's largest user of phytosanitary irradiation with the following exports to the United States.
|Fruit||Tons of irradiated fruit exported per year|
|Sweet lime|| 0||0||600|
|Manzano pepper|| 0||0||257|
Effect of phytosanitary irradiation on fruits and vegetables
For a phytosanitary treatment to be commercially viable, the treated commodities must tolerate it. At the doses used for PI (150 to 400 Gy), more fresh fruits and vegetables tolerate radiation than any other commercially available treatment (Heather and Hallman 2008). The most economical form of applying radiation involves treatment in bulk, such as in finished pallet loads, and this will result in a greater dose being absorbed by much of the load to ensure that the minimum required dose is absorbed by the entire load, which means the dose absorbed by the edges of a pallet could be at least twice that received in the center, as in the case of guavas irradiated in Florida. Some commercial arrangements, especially those using X-rays (which travel in more parallel lines instead of diverging outward in the case of gamma rays) combined with loads narrower than the dimensions of a standard pallet can achieve a dose uniformity ratio (the maximum absorbed dose divided by the minimum) as low as about 1.3. Knowing what maximum dose would be absorbed commercially when a minimum is sought gives the maximum dose that a commodity must tolerate if PI is to be used on it.
Because radiation inhibits development, fruit that is not eating-ripe when harvested, such as bananas, papayas, mangoes, and many other tropical fruits, may be more inclined to not ripen normally than fruit that is ready-to-eat when irradiated. The ideal physiological stage of harvest may need to be delayed when using PI; delayed harvest in itself should lead to a better-quality product compared with fruit picked for traditional marketing. The fact that papaya, mango, banana, and guava have been irradiated commercially from different countries for several years while in the hard green stage testifies to the ability of fruit to tolerate PI and still ripen adequately.