48 Brunt, L,M., Porlnoy, D.A. and Unanue. E.R. (1990)/./mmunol. 145, 52 Niederhauser, C., HOfelein, C., Lethy, J., Kaufmann, U., B~ihler, H.P. 3540-3546 and Candrian, U. (1993) Res. Mictobiol. 144, 47-54

49 Ruhland, G.L., Hellwig, M., Wanner, G. and Fiedler, F. (1993) I. Gen. 53 Kerr, K.G., Rotowa, N.A,, Hawkey, P.M. and/acey, R.W, (1990( AppL Microbiol. 139, 609-616 F.nviron. Microbiol. 56, 657-660

SO Gentschev, I,, Sokolovic, Z., KOh[er, S., Krohne, G.F., Hof, H., Wagner, $4 Bubert, A., KOhler, A. and Goebe], W. (1992) AppL Environ. Microbiol. I. and Goebel, W. (1992) Infect. Immun. 60, 5091-5098 58, 2625-2632

St Wernats, K., Heuvelmann, C.J., Chakraborly, T. and Notermans, $S Rocourl, J., £atimel, B., Jacquel, Ch., Brosch, R. and Buchrieser, C. S.H.W. (1991) J. Appl, Bactenol. 70,121-126 (1992) Meal. Mal. Infect. 22, 35-40

A role for irradiation

in the control of foodborne parasites

Paisan Loaharanu and Darwin Murrell

Various foodborne parasites cause human illnesses, resulting

in medical costs and productivity losses totaling bill ions of

dollars annually. Many of these zoonoses can be effectively

controlled by management and inspection strategies,

although the practicality and cost effectiveness of these

methods for some countries is problematical. Food irradiation offers an alternative control method for the major foodbome

parasites, and this review discusses its technical feasibility and potential uses.

The incidence of foodbome diseases continues to adversely affect the health and productivity of popu- lations in most countries, particularly those in developing countries. The report of a Joint FAO / IAEA (Food and Agriculture Organization / International Atomic Energy Agency) Expert Committee on Food Safety concluded that 'illness due to contaminated food is perhaps the most widespread health problem in the contemporary world and an important cause of reduced economic pro- ductivity". Parasitic and bacterial diseases combined represented the most frequent cause of death (35%)

Pai~n [oaharanu is at the Food Preservation Section, Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture, Vienna, Austria. Darwin Murrell is at Bel~sville Agricultural Research Center, USDA-ARS, Bellsville, MD. USA.

Review

worldwide in 1990, the majority of which occurred in developing countries'-. These diseases include diarrheas, malaria, tuberculosis and pertussis. Diarrheal diseases cause ~25% of deaths in developing ceuntries, and it is estimated that in up to 70% of cases, food is the vehicle for transmission of causative agents.

The contamination of foods, especially those of ani- mal origin, with pathogens such as non-spore-forming bacteria, parasitic helminths and protozoa, is a signifi- cant health problem and an important cause of human suffering globally ~.4. The econotnic impact of lost pro- ductivity and the cost of medical treatment is consider- able (Table 1). For example, economic loss from trichinellosis, toxoplasmosis, salmonellosis, campylo- bacteriosis and taeniasis in the USA in 1985 was esti- mated to be over US$1.5 × 109 (Ref. 7). The cost of condemnation of pork infected with the larval Taenia solium in Mexico in 1982 was estimated to be as high as US$43 × 106 (Ref. 8). Economic losses resulting from a number of foodborne parasitic zoonoses were reported by MurrelP; the estimated loss due to animal cysticerco- sis in Latin America was US$428 × 106 and in Africa US$I.8 x 109. The economic losses of human illness because of congenital toxoplasmosis in the USA are US$4.0-8.8 x 109 annually, a wide range reflecting the uncertainly over the number of infected babies s. lllnesses stemming from foodborne congenital toxo- plasmosis (excluding sub-clinical cases) in the UK were estimated to cost US$1.2-12.0 × 106 (Ref. 5). World- wide, the rates of congenital toxoplasmosis infec- tion are estimated at 0 .1-0 .8% of live births or 140920-1 127360 infected babies born each year t°. Toxoplasmic encephalitis has become the most com- monly recognized cause of central nervous system opportunistic infection in AIDS patients ~L

Foodbome trematodes also have an important effect on the health and economic productivity of human popu- lations in Southeast Asia, China and Korea, where the habit of consuming raw fish and meat is prevalent 3. Approximately one third of the people living in the northeastern region of Thailand (i.e. 6 -7 million) are infected by the liver fluke Opisthorchis viverrini ~2. The estimated wage losses and medical treatment costs for this population were ~US$85× 106 annually. Large

190 ©tee~. Eisevset Sc,ence Lid 0924 -2244p)4/$07 O0 Trends in Food Science & Technology June 1994 IVoL 51

numbers of people in China and South Korea are in- fected by the related Clonorchis sinensis, although econ- omic losses have not been adequately estimated.

Measures to control foodborne parasitic infect ion Food-processing and preparation methods such as

cooking and freezing are effective for the control of foodbome parasites. Although typical cooking methods are effective in killing parasites, this practice is not always adhered to and in many countries the preference for raw or lightly cooked food still prevails. Freezing at temperatures below -20°C for a specific period also ren- ders parasites noninfective. However, the freezing of food is often not feasible in developing countries. The Task Force on the Use of Irradiation to Ensure Hygienic Quality of Food, convened by the FAO / IAEA / WHO (Food and Agriculture Organization / International Atomic Energy Agency / World Health Organization) International Consultative Group on Food Irradiation concluded that "at present, and in the foreseeable future, there are no techniques which would guarantee the absence of pathogenic microorganisms and parasites in the production of raw food of animal origin, except at an exceptionally high cost' s3.

For many situations, the irradiation of food may offer a solution for such deficiencies. Although the concept and the technologies for the irradiation of food have developed slowly, this strategy is gaining wide. accept- ance, especially in the USA 4. For instance, in 1993, the American Medical Association's Council on Scientific Affairs endorsed food irradiation as a safe and effective tool to increase food safety and reduce the incidence of foodborne illness, a view expressed earlier by the US Department of Agriculture. The purpose of this brief review is to summarize for a broad audience the data on the effectiveness of irradiation in killing or blocking the pathogenicity of major foodborne parasites. Much of the literature on these studies is scattered or printed in non- traditional sources, hence this review is intended to make the data on irradiation of foodborne parasites more accessible to the general reader. We also discuss the prospects for the adoption of this technology in the global effort to ensure food safety.

What is food irradiation? h'radiation offers a unique method for the control o f

foodborne parasites acquired through the consumption of raw or semi-processed foods. Food irradiation is the treatment of food by ionizing radiation to achieve certain desired effects. The process involves exposing the food, either prepackaged or in bulk, to a predetermined level of ionizing radiation. In this way, it is similar to freez- ing, heating or microwave processing of food. The types of radiation applicable to the treatment of food are:

• gamma-rays from radionuclides 6°Co or 137Cs;

• electrons generated from machine source, operated at or below an energy level of 10 MeV"

• X-rays generated from machine sources operated at or below 5 MeV.

Table 1. Examples of foodborne parasitic diseases'

Disease Total cost (million US$) USA

Congenital toxoplasmosis 5256

Toxoplasmic encephalitis in AIDS patients 23-I 06

Cysticercosis h 9.0

Trichinellosis 0.8

Taeniasis (tapeworm! 0.3

[ Giardiasis 36.0

UK

, Congenital toxoplasmosis 1.2-I 2.0

', Mexico

Neurocysticercosis 195.0

Brazil

I Neurocysticercosis 85.0 i I Thailand

[ Opislhorchiasis (fishbornel 99.9

F [ "Data taken from Reis 5 and 6 i b Omits value for 66 lives lost annually

These types of radiation have too low an energy to induce radioactivity in any materials, and eannot therefore add radioactivity to food regardless of the length of time it is exposed or the amount of energy or 'dose' absorbed.

Ionizing radiations act through changes induced in the DNA structure of the irradiated cells, which result in prevention of replication or function. The energy level used for food irradiation to achieve any technological purpose is normally extremely low. At the maximum energy level or dose of ionizing radiation recommended by the Codex Alimentarius Commission ~'~ for treating food (10kGy), the absorbed energy is equivalent to the heat energy needed to increase the temperature of water by 2.4°C [calculated on the basis that 10 kGy of ionizing energy is equivalent to a heat energy of 10Jig and the heat capacity of water is -4.2 J/g/°C: I0 Jig + 4.2 J/g/°C = 2.4°C]. Quite often, irradiation of food requires much lower doses, e.g.O. 1 or 1.0 kGy, which would be equivalent to the heat energy of 0.024°C or 0.24°C. Thus, irradiated food remains at nearly the original natural state after treatment.

Effectiveness of irradiation to control infectivity of foodborne parasites

Numerous studies have been carried out to determine the minimum effective dose (MED) of radiation to con- trol foodborne parasites. Because this emerging tech- nology has significant relevance to food safety, we have summarized the results of this research below (see Table 2).

Trends in Food Science & Technology lune 1994 [Vol. 51 191

Table 2. l:f+ect of irradiation on foodbome parasites

Parasite Minimum effective

dose (kGy)

Prci~io°i/asma gondii 0,3

0.09

05

0.7

0.45-0.6

Trematodes

Fasciola hepatica 0.03

Clonorchis sinensis 0.2

0.15

Opisthorchis viverrini O.l

Paragonimus westermani 03

Cestodes

Taenia saginata >3,0

Taenia solium

Echinococcus granulosus

Nematodes

Trichinella spiralis

Angiostrongylus cantonensis

Gnathostoma spinigirum

Anisakis sp.

0.4

0.3

0.2-0.6

0.7

0.5

0.3

0.3

0.15

0.11

0.1-0.6

2.0

4.0

7.0

6.0

Effect of Bioassay References irradiation model

Parasite killed Mice 15

Elimination of infeclivity Mice 15

Elimination of infectivity Mice, cats 16

Elimination of infectivity Mice, pigs 17

Elimination of infeclivity Mice, cats 18

Inhibits maluration Mice 19

Inhibits maturation Guinea pigs 20

Inhibits maturation Guinea pigs, rats 21, 22

Inhibits maturation Hamsters 23

Inhibits maturation Cats 24

Complete inactivation in vitro 25, 26 of larvae excystment

Prevents development Human volunteers 27 in humans

Elimination of infectivity Human volunteers 28-30

Elimination of infectivity Hamsters 28, 31

Elimination of infectivity Hamsters 32

Elimination of infectivity Mice 33

Elimination of infectivity Mice 34, 35

Elimination of infectivity Rats 36

Elimination of infectivity Mice, rats 37

Sterilization of females Rats 38

Elimination of infectivity Mice 39

Decreased infeclivity Mice 40-42

Decreased infectivity Mice 40, 41

Reduced larval penetration Rals Setasuban, P., pers. commun.

Reduced larval penetration in vitro: agar plate 43

Protozoa Radiation at an appropriate level will inhibit cell div-

ision of living cells including protozoa. The sensitivity of protozoa to radiation varies according to species, stage of development and irradiation conditions. Schneider ~ found that a minimum dose of 251 Gy

killed the cyst stage of Entamoeba histolytica. Baldelli et al. I~ reported that a dose of 90 Gy was sufficient to eliminate the infectivity of Toxoplasma gondii tachy- zoites for mice, while a dose of 300 Gy was required 1o kill the parasite outright. Studies conducted between 1987-1991 under the aegis of the Coordinated Research

192 Trends in Food Science & Technology June 1994 [Vol. 5l

Programme on Use of Irradiation to Control Infectivity It appears that much larger doses of radiation are ot Foodborne Parasites (sponsored by the Joint FAO / needed to inhibit the tissue migration of many larval IAEA Division) re-examined the radio-sensitivity of nematode species than are needed to block maturation T. gondii, particularly the influence of parasite strain and reproduction of nematodes, such as T..~piralis. and host species. Dubey et al. ~6 demonstrated that Simimrly, the in vitro motility of larval Taenia appears 0.5 kGy was sufficient to prevent infection of cats and more resistant to radiation than is its ability lo establish pigs with several isolates of T. gondii. Wikerhouser et and develop in the host intestine. alJ 7 and Song et alJ 8, using several different strains of 1". gondii, reported that the MED for mice, rats, cats and Status of acceptance and application of food irradiation pigs was 0.45 - 0.7 kGy. for the control of foodborne parasites

Trematodes Data from the same Coordinated Research Pro-

gramme showed that the MED required to eliminate the infectivity of trematodes is well below 1.0 kGy. In studies in China and South Korea (employing the rat bioassay) the MED for C. sinensis larvae in fish was 0.15 kGy, and for isolated larvae, 0.05 kGy (Refs 21 and 22). Differences in the MED of different geographi- cal strains of this parasite were not detected. Sornmani et al. 23 reported that O. viverrini had a MED of O. I kGy (using a hamster bioassay), regardless of whether the larvae were free or in fish tissue. No significant changes in odor or taste of the irradiated fish were observed. The infectivity of Paragonimus westermani metacercaria (irradiated in sit,t in their crab host) for cats was elim- inated by 0,10 kGy of gamma irradiation -'4.

Cestodes Verster et al. ~'8 used a hamster bioassay for determin-

ing the infectivity of irradiated T. solium and Taenia

saginata, and reported that a dose of 0.2-0.6 kGy could render infected meat fit for human consumption. Geerts et al. '9 reported that in an in vitro study, no differ- ences in evagination and motility between irradiated (0.2-0.6 kGy) and non-irradiated T. saginam meta- cestodes were apparent. However, a trial with three human volunteers indicated that the MED for T. saginata was 0.3 kGy. Infectivity trials with metacestodes of T. solium in hamsters were also carded out by de Aluja et al.3~-: the results suggest that a dose of 0.7 kGy can suppress infectivity, although a dose of 6.5 kGy was required to cause outright in vitro death of the metacestodes.

Nematodes Brake et al? 7 demonstrated that pork infected with

Trichinella spiralis can be rendered safe by irradiation to 0.15 kGy. This low radiation dose prevented larval development in the intestine, but was insufficient to kill the first-stage larvae outright. For the purposes of control of this disease, this dose is sufficient 37. These data were instrumental in obtaining Food and Drug Administration (FDA) approval in the USA for pork irradiation 4~. A preliminary study on Gnathostoma spinigirum showed that a dose of 7 kGy significantly reduced worm recovery in rats although the MED for isolated larvae and for those in fish or other hosts were not determined (Setasuban. P., pers. commun.). Out et al. 40"41 reported that the MED for Angiostrongylus cantonensis is ~2.0 kGy.

Currently. 37 countries have approved the use of ir- radiation for processing or preserving over 40 food items or groups of food, either on an unconditional or on a restricted basis 4. Commercial applications nf food irradiation, while still limited, are presently carried out in 25 countries. The most common irradiated food prod- ucts for commercial use are spices and dry vegetable seasonings: some 20000 tonnes are estimated to have been irradiated in 1991 (Ref, 46). The recent ban on the use of ethylene oxide for food, already in effect in the European Union (EU), could increase the quantity of spices and vegetable seasonings processed by irradiation in the near future.

While thermal pasteurization of liquid food is a we!l- established and satisfactory means of terminal decon- tamination/disinfection of such commodities, this process is not suitable for solid foods and dry ingredients. Irradiation is instead a more effective method for "pasteur- izing' solid foods such as meat, poultry, spices, in order to avoid changes in the physicochemical and sensory quality of the product, in addition to treatment of spices and vegetable seasonings, irradiation has recently been used on a commercial scale to ensure the hygienic quality of poultry meat in France and fermented pork sausages in Thailand. In the case of the poultry meat. an electron accelerator was installed in 1987 in a poultry processing plant in Normandy, France, to "pasteurize" frozen blocks of mechanically deboned poultry meat. Thousands of tonnes of such products have been processed by irradiation each year since without prob- lems 47. In Thailand fermented pork sausages are almost always consumed raw after fermentation because of cul- tural food preferences. The product has a high incidence of contamination by Salmonella and occasionally by T. spiralis. According to Khamboonruang 4s, there were 118 outbreaks of trichinellosis in Thailand in the period 1962-1990, which affected -5400 patients, 95 of whom died. Thus. irradiation offers a unique treatment to ensure the hygienic quality of this "raw" product. Approxi- mately 50 tonnes of such product have been irradiated for commercial use each year in Thailand and the quantity is increasing (Ungsunantwiwat, A., unpublished).

A milestone in the commercial application of food irradiation occurred in early 1992 when the first commer- cial food irradiator in the USA went into operation near Tampa, Florida. Irradiated strawberries, citrus fruits, mushrooms, onions, etc. were subsequently successfully sold at retail levels in Florida and lllinois 4~'5°. This fa- cility has recently commenced the commercial irradiation of poultry products to inactivate Sabnonella and related

Trends in Food Science & Technology June 1994 IVol. 51 l q3

microorganismsSL It appears thai contrary to public per- ception, irradiated foods (e.g. mangoes, papayas, po- tatoes, onions, garlic, strawberries, cheeses, sausages) have little or no marketing difficulties at retail levels. There is no evidence to indicate that well-informed con- sumers will not accept irradiated food when they can exercise their freedom of choice 46.

Will irradiation be used? Low-dose irradiation (below 1 kGy) offers a unique

opportunity for controlling the infectivity of a number of foodborne parasites without changing the character of the food. Among the groups of foodborne parasites, trematodes appear to be the most sensitive to irradiation, followed by cestodes and protozoa. While some species of nematodes such as T. spiralis appear to be very sensi- tive, other species, which cause disease through larval migration (e.g. Anisakis spp., Gnathostoma spp. and Angiastrnngyh~s spp.), may require much higher doges of radiation to abolish their infectivity. Although the effect of irradiation on the transmission of a number of foodborne parasites (e .g.T. spiralis, T. gondii, C. sinensis and O. viverrini) has been conclusive, further research is needed to confirm the MED for parasites such as T. solium, Anisakis simplex, A. cantonensis and G. spinigimm. The most serious constraint to perform- ing the needed research is the lack of good alternative experimental hosts. This technical 'bottleneck' must be solved before accurate MEDs can be determined for these parasites.

The application and cost effectiveness of irradiation as a method to control foodborne parasites will depend on consumer attitudes, regulatory actions and the econ- omics and logistics associated with different situ- ations 4. The importance of these factors cannot ~-!ways be judged a priori. The acceptance and cost/benefits of this technology may only become apparent when it is implemented on a trial basis, as occurred in Florida with fruits and vegetables 49. Pilot studies to demonstrate the effectiveness of irradiation as a method to control T. solhm~ cysticercosis in Latin America are being planned in a research project on "Use of Irradiation as a Public Health Intervention Measure to Control Foodborne Diseases', jointly sponsored by the Pan American Health Organization, and the Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture. The outcome of that demonstration and research project will make an important contribution to the debate on the value of this technology to the effort to enhance food safety.

In many circumstances, it will not be cost effective to irradiate food for a specific parasite zoonosis. More likely, such control win result when irradiation of a product is employed to ensure safety from a variety of foodborne pathogens, especially Sahnonella, Campylo- bacter and Listeria, and to prolong shelf life quality.

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T r e n d s i n M i c r o b i o l o g y 2 ( 6 ) , 2 0 6 - 2 0 8

F o o d - b o r n e t r e m a t o d e s : i g n o r e d o r e m e r g i n g ? ,

b y H -J . R i m , H . F . F a r a g , S. S o r n m a n i a n d J . H . C r o s s ,

P a r a s i t o l o g y T o d a y 1 0 ( 6 ) , 2 0 7 - 2 0 9

S p e c i a l i s s u e : P r o t e i n E n g i n e e r i n g ,

T r e n d s i n B i o t e c h n o l o g y 1 2 ( 5 ) , 1 4 5 - 2 1 1

Trends in Food Science & Technology June 1994. [Vol. 5] 195