17 Irradiation D. A. E. Ehlermann, Federal Research Centre for Nutrition, Germany 17.1 Introduction ‘Genetically modified food’ has become the object of a heated debate by con- sumer activists and replaced irradiation’s leading role as a target. In this debate the term irradiation is frequently confused with radioactive contamination, espe- cially after the Chernobyl accident. The allegation is made that the nuclear indus- try needs food irradiation badly in order to find some use for the waste from nuclear power stations. In addition, the historical involvement of the US Army in research on food irradiation is used as proof of its link to nuclear weapons and military purposes. However, this chapter on the radiation processing of food by ionising energy, i.e. on food irradiation, highlights the history of the subject which extends over a hundred years. It elaborates the peaceful background, emphasises that radiation processing is a non-nuclear technology and elucidates the physical principles of the interaction between ionising radiation and matter. This basic information is then used to elaborate the beneficial effects of ionising radiation by describing its chemical, biological and microbiological action in the food environment. These two sections will lead to the radiological and toxicological safety of food processed by ionising radiation. The aim of the Nutrition Handbook for Food Processors is covered in a section on nutritional adequacy and is followed by a section summarising the evaluation of overall safety by national and inter- national expert groups. Radiation processing has already found its area of commercial application, governments have approved the process, the food industry is using it and where the irradiated product is available on the market consumers respond favourably. Under the WTO-agreement with the associated Codex Alimentarius standards (1984) and recommended by the WHO*, it is a tool that helps resolve several recent problems of food production, manufacturing and marketing. It can greatly support food safety and environment conservation and therefore serve the con- sumer. In conclusion, there is a list of sources of further information; for detailed literature the reader is referred to the monographs referenced. Several concerns have been voiced, for instance about nutritional quality, radiolytic products, toxicology, microbiology, occupational safety, environmen- tal side-effects, deception of consumers, consumer acceptance, substitution for good manufacturing practice, negligent hygienic practice, misuse and increased prices. These are the main arguments of certain consumer organisations against the legal clearance of this technology. They still influence the officials and politi- cians who are responsible for the regulation of food technologies. However, with the information available in this chapter readers should be able to make their own informed decisions. References given are restricted to textbooks, monographs and survey or review articles only, but interested readers will use them to lead to more detailed information. 17.2 The history of food irradiation As early as in 1885 and 1886 ionising radiation was discovered and in sub- sequent years its bactericidal effects were described. The purpose of the first patent on food irradiation (Appleby and Banks, 1905) was to bring about an improvement in food and its general keeping quality. It was followed by an invention of an ‘Apparatus for preserving organic materials by the use of X-rays’ (Gillett, 1918). However, radiation sources strong enough for industrial exploita- tion were not available before the 1950s. The following five decades were devoted to the development of this technology to a state where it could be applied both commercially and industrially as well as to an investigation into the health aspects of food treated by ionising radiation. This was done in a world-wide, concerted effort; the US Army and the US Atomic Energy Commission were involved and stimulated by Eisenhower’s initiative ‘Atoms for Peace’. The academia were led by the Massachusetts Insti- tute of Technology and followed by university and government research estab- lishments in many countries. Details are given by Diehl (1995). Radiation sources, such as radioactive isotopes and machines, became available and were strong enough for treating food at commercial throughput. A radiation process- ing industry developed so that everyday goods could be produced by using ion- ising radiation. Floor-heating pipes, automobile tyres, car parts, electrical wires and cables, shrinkable food packaging, medical disposables (syringes, implants, compresses, bandaging material, blood transfusion equipment) – all are manu- factured using ionising radiation. Even astronauts prefer irradiated food in their diets. 372 The nutrition handbook for food processors * The WHO Golden Rules for Safe Food Preparation list under ‘Rule 1 “Chose foods processed for safety”:...if you have the choice, select fresh or frozen poulty treated with ionizing radiation... The world-wide first food irradiation facility became operational in Germany in 1957 for spices, but had to be dismantled in 1959 when Germany banned food irradiation. In 1974 in Japan the Shapiro Potato Irradiator was commissioned and is the oldest food irradiation facility still in operation today. When in 1980 the JECFI made a landmark decision and declared irradiated foods as safe and whole- some for human consumption, it led many governments to permit the radiation processing of food. This did not result in commercial application of the process in all countries. Nevertheless, the total amount of food treated by ionising radi- ation is increasing, about 200 000 tonne per annum at the time of writing, but is still a very small volume compared to the total amount consumed. However, food irradiation is a niche application, supplementing traditional methods of food processing and serving specific purposes. Two important classes of application, sanitary and phytosanitary, are increas- ingly recognised. As recently as 1993, children died tragically after eating undercooked (‘rare’) hamburgers. This was caused by Escherichia coli type O157:H7 (EHEC), an emerging pathogen microorganism which is now considered to be ubiquitous. There is always the threat of such emerging hazards in modern, industrial food production. Such risks can only be fought by further improvement of good man- ufacturing practices and the application of ‘Hazard Analysis and Critical Control Point (HACCP)’. Adherence to such procedures and improvement of hygienic concepts can only reduce or limit the hazard but never eliminate it. For this reason, supplementary methods, in addition to good practices, help suppress such residual risks to a tolerable, acceptable level. Ionising radiation is such a tool, now legal in the USA and helping to make hamburgers, fresh or deep-frozen, far safer for the consumer. Many other pathogen microorganisms are a threat to society, causing death and illness, damages and economic losses. Other ex- amples are Campylobacter and Salmonella in poultry, Salmonella in eggs, Listeria in cheese and sprouts. Governments increasingly recognise the value of radiation processing of food in fighting such threats to health and hygiene. The threat to plant production (i.e. phytosanitary aspects) is less widely feared but many areas that are very productive in fruit and vegetables have suppressed several of the original pests. Such areas have strict quarantine controls on imports that might carry insects or pests capable of proliferation. The USA is the leading country in exploitation of ionising radiation for insect elimination: an X-ray facility for treating fruit on Hawaii is now operational and allows for the direct transport of fruit to mainland areas such as California. Also, other countries have strict quarantine regulations; they include Australia, Japan and South Africa where ionising radiation can play a valuable role. Certification systems presently under development will help facilitate international trade. 17.3 The principles of irradiation Processing by ionising radiation is a particular kind of energy transfer: the portion of energy transferred per transaction is high enough to cause ionisation. This kind Irradiation 373 of radiation was discovered because the emitting radioactive material caused ion- isation in the surrounding air. From the multitude of atomic particles known, only gamma rays from nuclear disintegration and accelerated electrons are useful for food processing (Table 17.1). Electrons may be converted into X-rays by stop- ping them in a converter or target (Fig. 17.1). Other particles such as neutrons 374 The nutrition handbook for food processors Table 17.1 Types of particle Particle Description electron An elementary corpuscle carrying one unit of positive or negative electrical charge. The positively charged electron is called a positron. alpha A charged particle, identical to the nucleus of a helium atom, composed of two neutrons and two protons. It carries two positive elementary units of charge. beta A charged particle, identical to an electron or a positron but emitted from a radioactive nucleus. gamma A particle or photon emitted from a radioactive nucleus. X Fast-moving charged particles in an electric or magnetic field, usually generated by high-energy electrons impinging on a high-atomic-number absorber (e.g. tungsten); also called R?ntgen-rays. They are generated by braking radiation (bremsstrahlung). Wavelength [cm] 10 4 10 2 10 –2 10 –4 10 –6 10 –8 10 –10 10 –12 10 –14 10 –16 10 0 10 0 10 2 10 4 10 6 10 8 10 10 Radio waves Infrared Visible light Ultraviolet ionising radiation Photon energy [eV] X-radiation Gamma radiation Cosmic radiation Fig. 17.1 Range of energies (electromagnetic spectrum): ionising radiation is charac- terised by the ability to split molecular bonds and to transfer electrons; this energy limit is indicated by the vertical, dashed line beginning in the range of ultraviolet light. are unsuitable because induced radioactivity is produced. The same may occur at elevated energy levels with electrons and X-rays; for this reason the electron energy is limited to a maximum of 10 MeV and the nominal energy of X-rays is limited to 5 MeV. Gamma rays of cobalt-60 have photon energies of 1.17 MeV and 1.33 MeV and cannot induce radioactivity; caesium-137 is not available in commercial quantities but gamma rays of 0.66 MeV are emitted from it. This means that gamma rays from available isotope sources are incapable of inducing radioactivity. Whether in the form of particles or as electromagnetic waves, the primary high energy is broken into smaller portions and converted into a ‘shower’ of secondary electrons (Fig. 17.2). These electrons finally interact with other atoms and mol- ecules knocking out electrons from their orbits or transferring them to other positions (Fig. 17.3). This means that an elementary negative charge is removed and a positively charged atom or molecule, i.e. an ion, is left behind. If an elec- tron has been transferred then orbital electrons are no longer paired and free radicals are created. Both ions and free radicals are very reactive, in particular in an aqueous medium such as in food, leading finally to chemical reaction prod- ucts that are stable. The effects caused by corpuscular or electromagnetic radia- tion are essentially equal; the difference is in the dose distribution along the penetration line into matter. Corpuscles have a definite physical range in matter, they are slowed down by several processes of collision and finally stopped. They have no energy beyond their range. Electromagnetic waves are attenuated expo- nentially and do not have a defined physical range. A schematic diagramme of irradiation facilities (Fig. 17.4) helps to understand the simplicity of the irradiation process: the goods are brought by a transport system into the irradiation cell which essentially is a concrete bunker shielding Irradiation 375 Electrons Photons 5 1 4 3 1 4 3 2 Fig. 17.2 Interaction with matter (photon versus electron): 1) primary incident radiation, 2) Compton electrons caused by photon interaction, 3) secondary electrons and final energy transfer, 4) irradiated medium, 5) finite depth of penetration for electrons. 376 The nutrition handbook for food processors Incident Scattered Ionisation Secondary electron Orbital electrons Fig. 17.3 Principal diagram of ‘ionisation’: whether photon or electron, the incident par- ticles interact with the orbital electrons and are scattered, an orbital electron is removed gaining kinetic energy as a secondary electron; in this way an ionised atom/molecule is left behind and a cascade of secondary electrons causes further ionisation or formation of free radicals. Beam handling system (10 MeV electrons) Radioactive source (Co 60) Irradiated food product 1 6 12 11 10 7 8 9 2 3 Fig. 17.4 Schematic diagram of irradiation facilities: the product to be irradiated has to pass through the irradiation zone; the design details largely depend on the physical prop- erties of the type of radiation used and may be adapted to the packaging and handling requirements of the goods. the environment and the workers from the radiation. A tunnel system allows free access for the goods but prevents radiation leakage; fences and detectors prevent unintentional access of anything or anyone when the radiation is ‘on’. Machine sources (accelerators) emit the radiation uni-directionally, gamma sources (radioactive isotopes) emit it in all directions. This means that for electron and X-ray processing the goods pass just before the beam exit window and for gamma processing the goods are piled and moved around the source to absorb as much as possible of the emitted energy. When it is not needed a machine source is simply switched off; for radioactive isotopes the frame with the source must be moved to a safe position which is usually a deep water pool. The design of irra- diation facilities is widely standardised; the safety-features are offically approved and authoritative control is well established. 17.4 The effects of irradiation on food There is a vast literature on the effects of ionising radiation on food and food components; for the nutritional aspects of the subject a very few references are sufficient (Diehl, 1995; Molins, 2001). Early textbooks even today are still rele- vant (Elias and Cohen, 1977, Josephson and Peterson, 1983) and in later years there has been an updating of details (WHO, 1994). The interaction of ionising radiation with matter takes place by means of a cascade of secondary electrons carrying enough kinetic energy to cause ionisa- tion of atoms and molecules and the formation of free radicals. Besides these direct effects and primary chemical reactions chain reactions of secondary and indirect transitions take place. In systems as complex as food and for biological systems usually high in water content most primary reactive species are formed by the radiolysis of water and the pathways of further reactions largely depend on composition, temperature, dose rate and relative reactivities. Only for a few very simple single-component models have the full pathways of reactions been identified; for highly complex systems a complete picture has not yet been achieved. Nevertheless, some aspects of the picture are beginning to emerge, especially with regard to the main components, i.e. carbohydrates, lipids and proteins. The effects of radiation on micronutrients, in particular on vitamins, are complex and are also dependent on overall composition; some macronutrients may protect micronutrients from radiolysis. Minerals and trace elements are not studied because they cannot be affected by radiation processing of food. However, the toxicological and nutritional consequences are discussed in further sections of this chapter. Biological effects include the beneficial use of irradiation for sprout inhibi- tion, ripening delay and insect disinfestation. Microbiological effects include the use of irradiation for the suppression of pathogen microorganisms and the reduc- tion of other, spoilage-causing microorganisms. For both procedures, the princi- pal reaction is irreversible radiation damage to the DNA disabling essential functions of the cell. Such DNA changes are irrelevant with regard to food and Irradiation 377 nutrition. There was previous concern as to whether irradiation and recycling these irradiated microorganisms could cause mutations that were capable of sur- vival and were more toxic or vigorous as their precursors. It has been shown that this is not the case and that ‘no special microbiological problems’ are introduced (World Health Organization, 1981). The storage of irradiated food is important in order to avoid growth of microorganisms or recontamination. 17.5 The safety of irradiated food Irradiated food does not become radioactive and this is now accepted even by opponents of the procedure. The limitation of allowable isotope sources to cobalt- 60 and caesium-137 and the limitation of the maximum energy of electrons to 10 MeV and of the maximum nominal energy for X-rays (bremsstrahlung or braking radiation) to 5 MeV provides adequate safeguards. Even if the nominal energy for X-rays is increased to 10 MeV the theoretically induced radioactivity would be much less than the natural activity there already is in food due mainly to the presence of potassium-40. Furthermore, it would be very difficult to measure such sparse induced activity in the presence of the natural radioactivity. It can be generally stated that the safety record of the radiation processing indus- try is slightly higher than that of other branches. There have been only a few acci- dents related to radiation exposure or radioactive contamination and the reason for all of them was a conscious violation of safety rules or non-adherence to pre- scribed procedures that included bridging safety circuits. From the beginning of systematic studies in the late 1940s it was recognised that irradiated food needed careful toxicological study before the technology could be applied to food manufacturing and processing. It is useless to question why the word ‘radiation’ carries such a negative image and causes considerable suspicion, not only among lay persons, but also among many scientists. In such a situation, governments and food control authorities were well advised to restrict the application of the new technology. However, further results have become available and the final judgement has been stated by the World Health Organi- zation (1981) as: ‘Irradiation of any commodity...presents no toxicological hazard’. This means that governments and authorities are responsible for the con- sequences and recognise the radiation processing of food as safe and as simply one among several other technologies. There have been thorough chemical studies, leading to the principle of ‘chemiclearance’ and classes of food that are chemically similar have been compared. It was also standard procedure to feed the food under consideration to animals and to look for possible effects on factors such as longevity, reproductive capacity, tumour formation, growth, unusual behaviour, haematological and biochemical indices, chromosomal abnormalities and genetic defects. These studies are very numerous and difficult for the non- specialist to follow; expert reviews are available elsewhere (Diehl, 1995). There have been also several publications reporting negative effects; however, a thor- ough follow-up always revealed deficiencies in the experimental organisation or 378 The nutrition handbook for food processors in the final evaluation and validation of the results. This is not the place to discuss such findings as increased polyploidy in malnourished children and the reasons why those experiments have been dismissed by expert bodies; full details and arguments can be found elsewhere (Diehl, 1995). It is sufficient to state that the validation of competent expert bodies (World Health Organization, 1981, 1994) always resulted in the ‘green light’ for food irradiation, and finally for any food at any dose (World Health Organization, 1999). 17.6 The nutritional adequacy of irradiated food Most food preservation and decontamination procedures, including irradiation, cause some loss in the nutritional value of foods. Further losses generally occur during storage and during preparation for consumption (e.g. in cooking). The spe- cific chemical changes brought about in foods by irradiation include some that alter the nutritional value, but the magnitudes of the changes are small when com- pared with those that result from other procedures currently in use. This has led most expert groups to conclude that reduction in the nutritional quality of foods resulting from the widespread use of irradiation is an insignificant part of the total diet as a whole (Elias and Cohln 1977; Advisory Committee on Irradiated and Novel Foods, 1986). One expert group concluded that ‘irradiation of food... introduces no special nutritional problems’ (World Health Organization, 1981). This conclusion emphasises the word ‘special’, recognising that there might be particular problems with some individual food products. Most expert groups also recommend that the nutrient content of irradiated foods should continue to be monitored while such foods are being introduced. A problem with many of the literature reports on the effects of irradiation on food constituents is that the studies have used laboratory ‘model’ experiments, often with pure or relatively pure target substances and irradiated in such media as water or buffers. Whilst these studies are ideal for investigating the chemistry of the radiation-induced changes, it is very difficult to extrapolate from them to the situation in real foods. In real foods, many of the other components present, usually in large quantities, interact, quench and otherwise interfere with the reactions of the radiolysis-derived products. Consequently, the magnitude of the changes that occur in specific components in a food matrix is generally much lower than the magnitude of those observed in simpler laboratory studies (Josephson et al, 1979). In general, the nutritional values of the macronutrients in foods (e.g. the car- bohydrate, lipid and protein components) are very little affected by ionising radi- ation. Some of the micronutrients, including some vitamins and polyunsaturated fatty acids, are more sensitive but their sensitivity is very dependent on the nature of the food. At the 1 kGy dose level, which is in excess of insect disinfestants applications, virtually no nutrient depletion is usually measurable although there have been reports of rise and fall in ascorbic acid (vitamin C) levels made in con- flicting publications. At the 10 kGy level, the vitamins ascorbic acid, thiamine Irradiation 379 (vitamin B 1 ) and pyridoxine (vitamin B 6 ) are generally the most sensitive to change but the extent varies considerably and depends on the specific food. Certain minerals and trace elements are essential for health but their irradia- tion at the energies employed in food processing does not result in any change (Harris and von Loeseke, 1969). 17.7 Vitamins Some vitamins are well known for their sensitivity to the effects of ionising radi- ation. Their inactivation (i.e. loss of biological activity) results predominantly from reactions with free radicals and other reactive species generated by the radi- olysis of water in foods. Since these reactive molecules interact with a wide variety of food components, the exact effect of irradiation on a particular vitamin depends not only on the chemical nature of the particular vitamin, but also varies greatly with the nature of the food itself. In vitro studies, in which dilute solu- tions of vitamins have been irradiated, may indicate sensitivities that are never seen in foods, where substantial ‘quenching’ by competitor molecules usually occurs (Goldblith, 1955). Reactivity of individual vitamins varies according to their chemical nature (World Health Organization, 1994). The most important with respect to food irra- diation, include the water soluble vitamins: ascorbic acid (vitamin C); thiamine (vitamin B 1 ); riboflavin (vitamin B 2 ); niacin (vitamin B 5 ); biotin (vitamin B 10 ); folic acid (pteroylglutamic acid); pyridoxine (vitamin B 6 ); pantothenic acid; cyanocobalamin (vitamin B 12 ); and the fat soluble vitamins: retinol and some of its derivatives (vitamin A); calciferol and some of its derivatives (vitamin D); tocopherols (vitamin E); naphthaquinone derivatives (vitamin K). Among the fat-soluble vitamins the ranking by decreasing sensitivity to radi- ation is: E >> A >> D >> K Carotenoids have a similar sensitivity to vitamin A. However, this is no strict order as sensitivity is largely affected by the protective properties of the other main components of a particular food. For this reason, conflicting findings from the published literature are easily explained by the experimental conditions, sometimes using low concentrations of a single vitamin in a solvent which does not resemble a real food. Such findings always need expert interpretation. Among the water-soluble vitamins B 1 (thiamine) is the most sensitive. However, it is notable that radiation-sterilised pork and beef still retains more thiamine than a heat-sterilised equivalent. The most contradictory results have been obtained with vitamin C. One main explanation is whether only ascorbic acid or ascorbic and dehydroascorbic acid was determined, or whether the results are reported as ‘total vitamin C’. Vitamin C is also very sensitive to storage conditions and natural variability might even mask irradiation effects. The following sections discuss particular vitamins. 380 The nutrition handbook for food processors 17.7.1 Vitamin A (retinol) Dry retinol and dietary precursors, such as b-carotene, are relatively radiation- tolerant, with little inactivation brought about by doses up to about 20 kGy (Lukton and MacKinney, 1956). Even doses as high as 200kGy only reduced b- carotene levels in tomatoes by about 10 to 20% (Lukton and MacKinney, 1956), depending on whether or not oxygen was present. Irradiation of carrot purée at 20 kGy caused no more than a 5% loss. Changes in vitamin A activity in fruits given low doses for disinfestation or to delay ripening were well below this level of loss, e.g. mangoes (Thomas and Janave, 1975), papayas and strawberries (Beyers et al, 1979). 17.7.2 Vitamin B This section discusses the following vitamins: B 1 (thiamine), B 2 (riboflavin), B 5 (niacin), B 6 (pyridoxine), B 10 (biotin) and B 12 (cyanocobalamin). Irradiation of thiamine causes deamination and destruction of the pyrimidine ring (Groninger and Tappel, 1957) with loss of biological activity (Ziporin et al, 1957). Thiamine is relatively radiation sensitive in some foods. Low disinfestation doses of 0.25–0.35 kGy, delivered to cereal grains resulted in losses of thiamine of 20–40% (Diehl, 1975). In cooked pork chops, irradiated at 0.3 and 1.0 kGy (the dose range proposed for Trichina control), losses were 5.6 and 17.6% (Fox et al, 1989). It is calculated that loss of thiamine in the American diet, due to irradiation of pork chops and roasts, would be 1.5% at 1kGy. When radiation doses as high as 25 kGy were used, raw fish retained nearly 40% of total thiamine (Brooke et al, 1966), and treatment of clams, at 45 kGy, led to no detectable loss of thiamine (Brooke et al, 1964). Following a major US study of the potential nutritional and toxicological effects of radiation sterilisa- tion on chicken breasts, Black et al (1983) concluded that g-irradiation, at doses of 45–68 kGy, reduced thiamine levels to a similar level as that produced by heat sterilisation. As a consequence of its relative chemical inertness, riboflavin is the vitamin most resistant to irradiation in the majority of foodstuffs. Sometimes levels of riboflavin in foods have been found to rise following irradiation, most probably due to release from binding to proteins, e.g. in pork meat (Fox et al, 1989) and onions (Le Clerk, 1963). Although slightly less stable to irradiation than is riboflavin in simple aqueous solution, niacin has substantial radiation tolerance in foods. As has been observed with riboflavin, niacin levels in some foods rise on radiation, e.g. in pork and chicken (Fox et al, 1989) and in bread made from irradiated flour (Diehl, 1980). In general, radiation-induced losses of pyridoxine in foods have been found to be small, similar to or slightly greater than losses of thiamine. Losses induced by radiation sterilisation of poultry and liver, at doses up to 55 kGy, were less than those induced by sterilisation by heat (Richardson et al, 1961). The converse Irradiation 381 was true for cabbage. Most studies have found little pyridoxine loss in foods irradiated at realistic doses and little further loss on subsequent storage. Biotin is very radiation resistant in foods. Sterilising doses of gamma and elec- tron beam irradiation did not significantly reduce levels in poultry (Black et al, 1983), or in eggs, at doses up to 50 kGy (Kennedy, 1965). Its relative stability to irradiation is reduced in the presence of oxygen more so than that of the other vitamins (Watanabe et al, 1976). Most studies have indicated that little or no loss of vitamin B 12 occurs during food irradiation, e.g. in various seafoods at doses up to about 4.5 kGy (Brooke et al, 1964); in pork irradiated at doses up to about 7 kGy (Fox et al, 1989); and in poultry, in a study comparing the nutritional effects of preservation by freezing with sterilisation by heat and with sterilisation by irradiation (Thayer et al, 1987). 17.7.3 Vitamin C (ascorbic acid) Ionising radiation initially induces oxidation of ascorbic acid to dehydroascorbic acid (Barr and King, 1956). This reaction (in which the biological activity of the vitamin is retained) has been found to occur in many studies of irradiated fruits and vegetables. Further irradiation eventually leads to losses of activity as biologically non-functional products are formed. Low doses of g-radiation, used to delay sprouting of potatoes, reduced ascor- bic but not dehydroascorbic acid levels. However, during subsequent storage, ascorbate levels rose, so that the differences between irradiated and non-irradi- ated potatoes disappeared (Schrieber and Highlands, 1958). Similarly, losses of ascorbic acid in orange and lemon juices, irradiated at 16 kGy, were accompa- nied by neat stoichiometric increases in dehydroascorbic acid (Romani et al, 1963). Losses of about 16% ascorbic acid occurred in 3 kGy irradiated freeze dried apples. Tomatoes lost between about 8 and 20% according to the state of ripeness of the fruit (Maxie and Sommer, 1968). In other studies, virtually no losses of vitamin C (nor of the B vitamins riboflavin, niacin or thiamine) were detected in mangoes, papayas, lychees or strawberries, irradiated at 2 kGy (Beyers et al, 1979). No vitamin C losses were detected in grapefruits irradiated at up to about 1 kGy (Moshonas and Shaw, 1984). Overall, the most likely changes occurring in low dose irradiated fruit and veg- etables seem to be the conversion of a proportion of ascorbate to dehydroascor- bate, and, sometimes, a small reduction in total vitamin C level. This reduction may then be reversed in intact fruits and vegetables as metabolism continues. 17.7.4 Vitamin D (calciferol) Although the presence of water increases sensitivity, the D vitamins are relatively stable to ionising radiation in their normal lipid-rich food environments. At doses of up to 15 kGy, cholecalciferol is more radiation resistant than is vitamin A or 382 The nutrition handbook for food processors vitamin E. Irradiation resistance of vitamin D in fish oils was even greater than in solvents, such as iso-octane, presumably due to the presence of tocopherols and other naturally occurring antioxidants (Knapp and Tappel, 1961). 17.7.5 Vitamin E (tocopherols) Vitamin E is the most radiation-sensitive of the fat-soluble vitamins. A sterilis- ing dose for beef (30 kGy) reduced beta-tocopherol levels by about 60% in air, but not significantly in nitrogen. Alpha- and gamma-tocopherols decreased sim- ilarly in irradiated chicken breast (Lakritz and Thayer, 1992). Oats irradiated at a dose of 1 kGy had lost only 5% tocopherol after 8 months storage in nitrogen, but nearly 60% when stored in air (Diehl, 1979). Diehl (1980) reported a near 20% loss following 1 kGy irradiation of hazelnuts. 17.8 Carbohydrates Apart from water, the major constituents of most foods are carbohydrates, pro- teins and lipids. Irradiation of low molecular weight food carbohydrates, such as glucose, mannose, ribose and lactose results in the formation of low levels of radiolytic products mostly derived from reaction of hydroxyl radicals (OH°), generated from water, with the sugar. A predominant reaction is the oxidation of hydroxyl groups, often with loss of a neighbouring hydroxyl group. Products such as 2-deoxy-gluconolactone and gluconic acid are formed, and the pH value of simple sugar solutions falls (von Sonntag, 1980). Carbohydrates irradiated in the solid state are generally more resistant than those irradiated in solution. Irradiation of high molecular weight carbohydrates (starch, pectin, cellulose, carrageenans, etc.) sometimes causes major changes in the physical properties of the foods that contain them. Properties such as viscosity, mechanical strength, swelling and solubility are likely to change in such a way as to reduce their func- tionality in a food, but sometimes change to improve their effectiveness for a particular function. Irradiation of lignocelluloses, in woody materials, has been shown to increase their subsequent biodegradability by microorganisms such as Flavobacterium species (Bhatt et al, 1992). The limited breakdown that occurs increases their susceptibility to the microorganism’s hydrolytic exoenzymes. The properties of gums, such as Karaya gum (Le Cerf et al, 1991) change greatly on irradiation with, for example, very large increases in solubility, falls in viscosity and loss of water-swelling properties. 17.9 Lipids The irradiation of unsaturated fatty acids in foods predominantly results in the formation of alpha and beta unsaturated carbon compounds (Nawar, 1983). Irradiation 383 Further reaction, and the addition of oxygen, leads to the formation of a hydroper- oxyl radical. Then formation of a hydroperoxide: The hydroperoxides are generally unstable in foods and breakdown to form mainly carbonyl compounds, many of which have low odour thresholds, and con- tribute to the rancid notes often detected when fat-rich (and particularly unsatu- rated fat-rich) foods are irradiated (Hammer and Wills, 1979; Wills, 1981). For example, irradiation of whole egg and egg yolk powder resulted in the genera- tion of lipid hydroperoxides (Katusin-Razem et al, 1992). In the absence of air, their formation was limited by available oxygen. Interestingly, destruction of carotenoids was strongly correlated with hydroperoxide formation. Irradiation in the presence of oxygen leads to accelerated autoxidation (Diehl, 1995), but the end products are similar to those found following long storage of unirradiated lipids (Urbain, 1986). 17.10 Proteins Many studies of the nutritional effects of irradiation on proteins have been made with generally only small or insignificant changes found. For example, irradia- tion of fish and meat meal, eggs, wheat and wheat gluten (Kennedy and Ley, 1971) showed little change in nutritive value in feeding studies after irradiation at doses up to 10 kGy. The biggest changes were in wheat gluten (7%). At 50 kGy larger losses occurred, but were largely reversed by supplementation of the diets with methionine. 17.11 The wholesomeness of irradiated food The definition of ‘wholesomeness’ (in the sense of being sound, healthy, clean and otherwise fit for human consumption) requires some elaboration as it does not occur in food laws and regulations. It was originally introduced in the 1950s in the US, expanded by the FDA and others and developed in food and inspec- tion acts. At the same time the studies on the safety of irradiated food for con- sumption were begun on a large scale and in international cooperation. During RCHCHCHR 1 OOH RCHCHCHR 1 OO 384 The nutrition handbook for food processors the procedure the terminology of wholesomeness was unanimously accepted to mean ‘safety for consumption’ under any relevant aspect and comprises the fol- lowing features: radiological safety, toxicological safety, microbiological safety, and nutritional adequacy. The main contribution to the judgement of wholesomeness was made by the FAO/IAEA/WHO Joint Expert Committee on Food Irradiation (World Health Organization, 1965, 1970, 1977, 1981). At the time of the Committee’s founda- tion in 1961 it was concluded that ‘general authorization of the commercial use of radiation for the treatment of food is premature’. Based on the work of the International Project in the Field of Food Irradiation (IFIP, founded in 1970 and concluded in 1981) and on the international work coordinated through IFIP the World Health Organization concluded finally (1981) that: . . . the irradiation of any food commodity up to an overall average dose of 10 kGy presents no toxicological hazard; hence, toxicological testing of foods so treated is no longer required. and . . . the irradiation of food up to an overall average dose of 10 kGy introduces no special nutritional or microbiological problems. Several national advisory groups have endorsed those findings and many national governments that had previously banned food irradiation introduced per- mission legislation for irradiated food. In addition, the European Commission asked their Scientific Committee on Food for advice, the JECFI conclusions were expressedly endorsed and a list of foods for clearance was proposed. However, at the time of writing no resolution of this issue has been achieved. 17.12 Current and potential applications Some of the benefits of food irradiation are listed in Table 17.2. Food safety will present great challenges for all involved, including governments and industry (Loaharanu, 2001; Osterholm and Potter, 1997). Globalisation brings food from previously unavailable sources to markets that were previously unreachable. Pro- duction conditions are not always acceptable and the rules and regulations that are already in place do not always accord with targets and measurements. This means that attempts at harmonisation are indispensable (Mortarjemi et al, 2001). New hazards are emerging which means that appropriate and coordinated action must be taken. Food security is still the main issue in developing areas, but in industrialised countries the problem of food safety is paramount and the main aspects are hygienic quality and, in particular, microbial contamination (Doyle, 2000). Processing of food by ionising radiation is a perfect tool (Molins et al, 2001), supplementing traditional methods and in some applications is the only Irradiation 385 procedure available. Irradiation will not be at all effective if it displaces good practices and is most effective if used as the final critical control point in an overall HACCP-concept. Under the SPS-agreement (Sanitary and Phytosanitary) food safety is the first aspect and quarantine for plant products is the second. Here again, radiation pro- cessing is a perfect tool to achieve quarantine and at the same time conserve the environment, thus avoiding the use of ozone-layer depleting chemicals. It con- tributes to occupational safety by avoiding the use of toxic fumigants. Both uses are spreading, the volume of treated goods is increasing; governments and com- petent international bodies are developing harmonised protocols. The potential of such applications in the future is high despite the fact that at present world-wide only about 250 000 tonne per annum are irradiated (Loaharanu, 2001). 17.13 Consumer attitudes and government regulations It is widely said that consumers reject food irradiation and any irradiated product on the market will be turned down. Table 17.3 lists common objections to irra- diation. In most countries, however, irradiated food products are not on the market and the consumer has no decision left to buy or to abstain and so it appears that there is no consumer demand. On the other hand, the food industry is reluctant to bring irradiated products on the market or to be identified with food irradia- tion. There have even been advertising campaigns of consumer activists pub- lishing names of companies who guarantee that their products are not treated by ionising radiation. This is a vicious circle which can only be broken by strong arguments which has occurred in the US where a number of people, in particular children, died because they ate undercooked, ‘raw’ hamburgers. The reason is a nearly unavoid- able infection of raw, minced meat by Escherichia coli, including type O157:H7 (also called EHEC). E. coli microorganisms are deadly and can spread despite tight hygienic measures; an effective safety measure is radiation processing to 386 The nutrition handbook for food processors Table 17.2 Some of the benefits of food irradiation Benefit ? improves microbiological safety ? reduces chemical treatment ? facilitates international trade regarding food safety and quarantine security ? improves availability and quality of tropical products previously unavailable ? fresh food remains fresh, raw food remains raw ? can be applied to solid foods for pasteurisation ? can be applied in the frozen state; there is no need for warming-up ? leaves no residue ? can be applied to pre-packed food fight any residual risk. ‘Red meat’ irradiation has been legal in USA since 1999 and has been applied on a commercial scale since the middle of the year 2000. An increasing number of food suppliers now rely on hamburger patties for domes- tic use and for institutional catering which should be stamped with the words: ‘irradiated for your safety – serve with confidence’. The consumer appreciates the availability of such products and the choice between irradiated products and those which are not irradiated. The indications are that the well-informed consumer will respond favourably to the irradiated product once it becomes available to the market as well as being open-minded and ready for pertinent, trustworthy information. Scientific and sociological studies back these observations. Activists against food irradiation play guardians for an ‘under-age population’. There have been other studies on the market place, for instance on the sale of irradiated fruit from the Hawaiian islands in mainland USA where strict quaran- tine regulations against Mediterranean fruit fly are in place. Consumers responded favourably to such tests and now the product is on the commercial market; in Hawaii a facility dedicated to fruit irradiation has been established. From this it can be inferred that alleged consumer resistance to irradiated food either does not exist or that it can be overcome (anon, 1998). Such resistance is created by certain opponents and is taken over by a timid food industry. In the history of food irradiation there have been many ill-founded claims, misunder- standings, half-truths, and intentional distortions. Much controversial information has been published and the discussions contain more emotion than fact. However, the professional view is that the benefits by far outweigh any potential, still unidentified, risk. From this position of alleged consumer resistance, reinforced by the loud voices of consumer activists, politicians and governments are very cautious when it comes to regulating food irradiation. The Codex Alimentarius (1984) in its stan- dard on food irradiation does not restrict by individual food, nor by groups or Irradiation 387 Table 17.3 Some arguments against food irradiation Argument ? allows lax food hygiene ? does not remove toxins ? spores are not killed ? causes loss of nutrients ? freshness is apparent rather than real ? spoilage may flourish without warning signs ? impairs sensory quality ? increases costs ? harms the environment ? endangers personnel ? needs restructuring of the total logistics classes, most countries have preferred to regulate by this approach (Table 17.4). A very few have adopted Codex Alimentarius completely (namely Brazil, which has removed any upper dose limit, Ghana, Mexico, Pakistan, Turkey and ASEAN member states). On the other hand, the USA prefers ‘permit as petitioned’ and requires documentation in addition to Codex Alimentarius and WHO evidence (the US regulatory system is explained in much detail elsewhere (Looney at al, 2001)). At present, some 53 countries have regulations on food irradiation; this varies widely and conflicts with international trade. The International Consultative Group on Food Irradiation (ICGFI) holds an inventory of regulations by country and by item (http://www.iaea.org/icgfi) and provides other useful information. In some cases, the minimum or the maximum dose or both are regulated; in other cases an ‘average’ is regulated. Under the aspects of food irradiation technology only the upper and the lower dose limits are of interest because they are related to the effectiveness of the treatment. An average dose is of interest under rather rare circumstances: a liquid being stirred after irradiation. The idea of ‘overall average dose’ originated from toxicological considera- tions (World Health Organization, 1981), a concept which is totally unsuitable for regulatory purposes. Regulating the average requires the food inspector to execute a certain integration over a prescribed extent of the sample. This problem has been resolved by more recent regulations in the Netherlands and in the United Kingdom: the regulated reference value is the average of the ‘batch’ and the minimum and the maximum dose values are strictly bound to this set value. However, the common regulation for all EU-members falls back to crude average 388 The nutrition handbook for food processors Table 17.4 Legislation concerning food irradiation European Union clearances only for ‘dried aromatic herbs, spices and vegetable seasonings’: Austria, Denmark, Finland, Germany, Greece, Ireland, Luxembourg, Portugal, Spain, Sweden ‘dried aromatic herbs, spices and vegetable seasonings’ and other specified items: Belgium, France, Italy, Netherlands, United Kingdom Non-EU countries in Europe Clearance: Croatia, Czech Republic, Hungary, Norway, Poland, Russian Federation, Switzerland, Turkey, Ukraine, Former Yugoslavia Other countries with clearances Asia/Pacific: Australia, Bangladesh, China, China, Republic of (Taiwan), Indonesia, India, Iran, Japan, Korea, Pakistan, Republic of, Philippines, Thailand, Vietnam Africa (including Middle East): Egypt, Ghana, Israel, South Africa, Syrian Arab Republic Latin America (Middle and South): Argentina, Brazil, Chile, Costa Rica, Cuba, Mexico, Uruguay North America: Canada, United States of America limits. As such details vary widely and are sometimes contradictory, international trade is severely hampered. For this reason regional harmonisation efforts have been undertaken (1993/1999 Asia/Pacific; 1996 Africa; 1997 Latin America and Caribbean; 1998 near east) and are now being implemented by ASEAN-members. Imports and exports are permitted in most regulations; the mutual conditions, however, are not coordinated. In particular, the European Union requires that the irradiation facility in the exporting country must be registered with and inspected by the EU authorities. 17.14 World Trade Organization, Codex Alimentarius and international trade The World Trade Organization (WTO) agreement has replaced the former GATT and the standards of Codex Alimentarius have become the indisputable reference for trade in food. Most countries have adopted the rules of WTO and disputes between signatories must be settled in a WTO conciliation procedure. Such dis- putes have already arisen in the European Union because of its regulations on ‘hormone beef’ and on ‘dollar bananas’. Irradiated food might become the next case. The specifications in the Codex Alimentarius Standard on Irradiated Food and its associated Code of Practice (1984) are not restricted to any class or group of food. Such specifications are presently under revision, and the upper dose limit will be removed in order to follow the latest development (World Health Organization, 1999). The Joint FAO/WHO Codex Alimentarius Commission (CAC) was created in 1962 with the intention to facilitate international trade in food by world-wide har- monisation and the Codex Alimentarius has become a collection of accepted and internationally recognised standards. With the emergence of WTO these standards have become the only technical reference; there are particular references under the agreements on Technical Barriers to Trade (TBT) and on Sanitary and Phy- tosanitary (SPS) measures which are an integral part of WTO. In this situation, even the existence of any regulation that does not cover all food but restricts per- mission to a particular list may be considered as a TBT and a violation of the WTO rules. The SPS agreement explicitly refers to processing by ionising radia- tion as one of the generally acceptable tools for achieving sanitary and phy- tosanitary purposes. Only a few countries have initiated the legal procedures to convert to the new framework (as described for Brazil in section 17.13). The European Union in particular has issued directives on food irradiation that are at variance with the rules of WTO underwritten by all EU-Member States. For instance, Germany is bound by a parliamentary vote to object to and block any clearance of food irradiation beyond spices: ‘We strictly object to any expansion of the (EU) “positive list” [which presently only contains spices] because we deem irradiation of any further products as unnecessary.’ As can be seen from the possible applications and from reports from many countries on their food safety and food security needs it is obvious that there is Irradiation 389 a technological need for processing food by ionising radiation. Negating such needs lacks arguments founded on sound science which is a prerequisite for reg- ulations under WTO. Or as WHO worded it, the countries which need the new technology most would also suffer most from the resistance of developed coun- tries. There are provisions in national regulations for imports from third coun- tries. However, when using such rules administrative obstacles must still be overcome. The US is preparing to accept imports of irradiated fruits from its southern partners; ASEAN member states are harmonising their national regula- tions; many countries are joining forces to develop the standards of the Codex Alimentarius to the present state of the art. The parties to the Montreal Protocol of 1997 agreed to a phase out (2005 and 2015 for advanced and developing coun- tries, respectively) of several fumigants, with radiation processing being the tech- nology that will take its place. Other fumigants such as ethylene oxide are already banned in several areas because of their toxicological properties and radiation processing has been demonstrated as an effective replacement for such fumigants. The International Plant Protection Organization (IPPO) has decided that radia- tion processing is the broad spectrum quarantine treatment that has no specific requirements regarding insect species or host commodities. Regional organisa- tions such as the North American Plant Protection Organization (NAPPO), the European and Mediterranean Plant Protection Organization (EPPO) and the Asian and the Pacific Plant Protection Commission (APPPC) have endorsed this alter- native technology. Furthermore, under such competent bodies certification systems have been developed to facilitate international trade in commodities carrying a phytosanitary risk. Similar efforts have not yet been undertaken for sanitary purposes. 17.15 Future trends Industrialised countries increasingly face the problem of providing their popula- tions with safe food. As the tip of the iceberg, Escherichia coli type O157:H7 (EHEC) has become a major threat to the US food industry. The arrival of ‘elec- tronically pasteurised hamburgers’ on the US market, i.e. treated with high-energy electrons as ionising radiation and their acceptance by the consumer mark a new era; the change in the public opinion occurred when consumers realised the deadly risk of foodborne pathogen microorganisms. It would be too simple an argument to state that only the diversion of the US food industry from natural production to industrial mass production is the cause of this new challenge. The increase in world population and the concentration of population in centres of economic activity and wealth is unavoidable, and there is no way to return to the days of our ancestors. Even under strict hygienic control and at the best level of Good Manufacturing Practices there always remains a residual hazard. Radiation processing of food can help ease this problem, to improve hygienic quality of the food available, to save human lives, to save costs to the society and its social system and to contribute to the wellbeing of everyone. Ionising radiation is one 390 The nutrition handbook for food processors tool among many; it has specific limitations and advantages but is superior to tra- ditional means in its hygienic applications. Less industrialised and developing countries in particular face the problem to secure the food supply; the growing population can ‘eat up’ any increase in food production and 20 to 40 % (estimation by FAO) of the harvest can be lost during distribution and storage. Ionising radiation is a tool here but must be combined with substantial improvement of the logistics of the food production and distrib- ution system. The usual improvement of Good Agricultural Practices and Good Manufacturing Practices alone cannot alleviate the problem. Furthermore, the application of ionising radiation can replace traditional chemical treatments that are becoming more and more suspect. Fumigants which were an upholder of agricultural production are likely to become unavailable in the near future; several developed countries have banned their use because of the toxicity to workers of some and of the ozone-depleting properties of others (as detailed in the Montreal Agreement). Most advanced countries have even banned the imports of raw materials produced using such chemicals and their long-term availability is questionable because production is already dramatically reduced. Because developing countries achieve a considerable part of their gross net income from exports of food and agricultural raw materials this development is a threat to their economies. Insect infestation is a major cause of such loss of food exports, followed by spoilage through moulds, yeasts and other bacteria. Once the harvest is stored in insect-tight silos and transported in insect-tight sacks, re-infestation can be avoided and the contents are preserved for human consumption, the insects can be prevented from proliferation by irradiation. When the storage of grain, cocoa and coffee beans is under controlled humidity condi- tions, the outgrowth of pathogen bacteria is retarded and the formation of myco- toxins excluded. Consequently, food irradiation is a tool that supplements traditional methods of food preservation; it has already found its niche application. The total volume of goods treated is still small, estimated at about 200 000 tonne per annum, one half of which is spices and dry seasonings. Official statistics are unavailable for other methods such as canning, cooling and freezing. As the development in the US clearly demonstrates, the industrial implementation of radiation processing and its acceptance by the consumer come at the time when awareness for such needs has been established and the product is clearly labelled. This means that a slow but steady growth of the amount of irradiated food is to be expected. 17.16 Sources of further information and advice At present, 45 governments are members of the International Consultative Group on Food Irradiation (ICGFI) with a secretariat at Vienna, Austria (c/o IAEA, P.O. box 100, A-1400 Vienna, Austria; http://www.iaea.org/icgfi). ICGFI has devel- oped technical guidelines and Codes of Practice for radiation processing of food. It is an international group of experts designated by Governments to evaluate and Irradiation 391 advise on global activities of food irradiation. A few very general and introduc- tory publications are available (Satin, 1996; Murano, 1995; World Health Orga- nization, 1991); renowned and competent organisation have published ‘position papers’ (Olson, 1998; anon, 2000; anon 1999); full details of the technology are covered in multipage compendia (Josephson and Peterson, 1983; Elias and Cohen, 1977; Elias and Cohen, 1983). The crucial question of the safety of irradiated food is covered in full detail by Diehl (1995) and WHO has published the results of expert evaluations (World Health Organization, 1981, 1994 and 1999). The actual status of the technology can be determined from the proceedings of recent con- ferences (Loaharanu and Thomas, 1999) and from textbooks (Molins, 2001). Nor must it be forgotten that in many countries national, competent bodies have pub- lished positive judgements of the technology. Through national and international consumer organisations more information is available to the general public and it completes the picture by analysing the technology from different aspects. 17.17 References Advisory Committee on Irradiated and Novel Foods (1986), The Safety and Wholesome- ness of Irradiated Foods, ACINF, London, HMSA anon (1998), ‘A round table on food irradiation: identifying, addressing and overcoming consumer concerns’, World Food Regulation Review 7 (12), 23–30 anon (1999), ‘IFST position statement: The use of irradiation for food quality and safety’, Food Sci. 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