Food Irradiation Principles 004

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Radiation Inactivationof Microorganisms

JAMES S. DICKSON

Department of Microbiology, Iowa State University, Ames, Iowa

2 . 1 . INTRODUCTION

The ability of radiation to inactivate microorganisms has been the main rationale

for the use of food irradiation. Radiation has been demonstrated to be an effective

means of destroying both pathogenic and nonpathogenic bacteria, as well as para-

sites and, to a lesser degree, viruses. In this context, radiation can be seen as

analogous to various other food processes used to inactivate microorganisms, such

as the various forms of heating.

2 .2 . MECHANISMS OF INACTIVATION

Radiation, whether ionizing or nonionizing (i.e., a photon of energy or an electron),inactivates microorganisms by damaging a critical element in the cell, most often

the genetic material. This damage prevents multiplication and also randomly ter-

minates most cell functions. Damage to the genetic material occurs as a result of a

direct collision between the radiation energy and the genetic material, or as a result

of the radiation ionizing an adjacent molecule, which in turn reacts with the genetic

material. In most cells, the adjacent molecule is usually water (Grecz et al. 1983).

In the first instance, the effects are straightforward. A photon of energy or an

electron randomly strikes the genetic material of the cell and causes a lesion in theDNA. The lesion can be a break in a single strand of the DNA or, if the orientation

of the DNA is appropriate, the energy or electron can break both strands on the

DNA. Single-strand lesions may not be lethal in and of themselves, and may in fact

result in mutations. However, large numbers of single-strand lesions may exceed

the bacterium's repair capability, which ultimately results in the death of the cell.

Food Irradiation: Principles and Applications, Edited by R. A. Molins

ISBN 0-471-35634-4 © 2001 John Wiley & Sons, Inc.

CHAPTER 2



A doub le-strand lesion occurs w hen the photon or electron strikes adjacent areas

on both strands of the DN A. This in effect severs the DNA into two pieces. D ouble

strand lesions are almost invariably lethal, as the mechanism necessary to repair a

double-strand lesion is beyond the ability of virtually all biological systems. How-

ever, because of the necessary orientation of the DNA in relation to the irradiationsource, double-strand lesions occur much less frequently than do single-strand

lesions.

The interactions of radiation with molecules adjacent to the genetic material are

more complex. The chemistry of the irradiation of water is well known. Radiation

causes water molecules to lose an electron, producing H 2 O+ and e~. These pro-

ducts react with other water molecules to produce a number of compounds, includ-

ing hydrogen and hydroxyl radicals, molecular hydrogen and oxygen, as well as

hydrogen peroxide (Arena 1971). The reactive components of these equations,

which are generally believed to be most significant, are the hydroxyl radicals

(OH~) and hydrogen peroxide (H 2O 2). These m olecules react with the nucleic acids

and the chemical bonds that bind one nucleic acid to another in a single strand, as

well as with the bonds that link the adjacent base pair in the opposite strand. Since

the location of the ionization of the water molecules is random, the subsequent

reactions with the nucleic acids are random. As with the direct interaction of

radiation with DN A, the indirect action can result in both single- and double-strand

lesions, with the same overall effects.

In add ition to effects on the genetic m aterial, radiation has a variety of effects on

the other components of the cell. Applying radiation to a cell results in the direct

and indirect interaction with cell components such as membranes, enzymes, and

plasmids. These interactions m ay h ave the potential to be lethal to the cell, in and of

themselves but in most cases would not be so unless there were also damage to the

genetic material. These interactions may have a role in the survival of sublethally

injured bacteria, in that a cell that has not sustained lethal genetic damage may bedamaged in other ways that complicate or impede survival of the injured cell.

The radiation sensitivity of various organic compounds is proportional to their

mo lecular w eight. On the basis of this assumption, it has been e stimated that a dose

of 0.1kGy would damage 0.005% of the amino acids, 0.14% of the enzymes, and

2.8% of the DNA within a given cell (Pollard 1966). It is difficult to separate the

effects of genetic damage from the nongenetic damage of irradiation, and the

differentiation may not be of any practical value. However, one important aspect

of this point is that the damage is random and not related to a specific genetic locusor cell component. This is a significant factor in the elucidation of radiation resis-

tance of bacteria, especially in relation to the ability of microorganisms to develop

or acquire radiation resistance.

2.3. MECHANISMS OF MICROBIAL SURVIVAL AND REPAIR

Since the primary means of inactivation of microorganisms by radiation is damageto DNA, the mechanisms of survival and repair center on the repair of DNA. The



sensitivity of a microorganism to irradiation is often based on the efficiency of its

repair m echanisms for DN A, and organisms that have a mo re efficient DNA repair

mechanism are more resistant to irradiation. An extreme example of this is the

bacterium Deinococcus radiodurans, which was first identified as Micrococcus

radiodurans in foods that were thought to be sterilized by radiation (Brooks andMurray 1981). This bacterium is exceptionally resistant to radiation, as it has been

isolated from foods exposed to doses in the 35-4OkGy range. The enzymatic DNA

repair system within D. radiodurans is very efficient (Moseley 1976), while other

radiation resistant bacteria possess efficient excision mechanisms (Lavin et al.

1976), to remove damaged portions of the DNA.

In addition to the efficiency of DNA repair, another mechanism of survival for

microorganisms relates to the number of copies of a given gene within the DNA.

2 .4. RAD IATION SENSITIVITY OF SPECIFIC MICROO RGA NISMS

Bacterial populations increase in numbers by doubling; that is, one bacterium

reproduces by growing and dividing, forming two bacteria. On a population basis,

this becomes

b = (l x 2") (2.1)

where b is the bacterial population after n generations, beginning with a single cell.

In most cases, the growth from a single cell is limited to laboratory experimenta-

tion. Therefore

b = (B x 2") (2.2)

where b is the bacterial population after n generations, beginning with an initial

population of B cells. When the numbers of bacterial cells are converted to Iogi 0

values and plotted during the active phase of the growth curve (logarithmic growth),

the results form a straight line.

Bacterial populations also decline in a similar fashion after being subjected to

an environmental stress, such as heat or radiation. The kinetics of bacterial death

follows a first-order reaction, with the same proportion "or percentage killed over

time. To allow com parisons between different microorganism s and the same micro-organism under different conditions, a decimal reduction value is calculated.

This value is the amount of radiation required to reduce the population of a

specific bacterium by 90% (Ilog 1 0 cycle) under the stated conditions. The

calculation is

1Og10TV0-IOg10M



where D i0 = decimal reduction value

d — radiation dose applied

1Og1 Q^VO = bacterial population prior to irradiation

1Og10Wi = bacterial pop ulation after irradiation

The D 1 0 value may also be determined by graphing bacterial populations after a

series of increasing radiation doses has been applied (e.g., 0.5, 1.0, 2.0, 4.OkGy).

The negative inverse of the slope is equivalent to the D 1 0 value

Ao =-1(V-) (2'4)

\ s l o p e /

Although most microbial death curves are linear, two notable features occur with

some frequency with irradiation. The first is the appearance of a "sh ou lde r" on the

curve at initial doses (Fig. 2.1). This shoulder is more pronounced with highly

radiation resistant genera, such as Deinococcus (Sweet and Moseley 1976).

Although the explanation of this shoulder varies, a reasonable explanation is that

the bacterium's genetic repair mechanism is capable of addressing the damage

caused by low doses of radiation. The Z)10 value is commonly calculated over

the linear part of the death curve, but the presence of a shoulder may result in

underestimation of the actual dose required unless two-parameter models are used

to account for this phenomenon.

Another feature that occurs with some frequency on microbial death curves is a

"t a il " or survival portion of the curve (Fig. 2.1). This portion of the curve represen ts

Dose (kGy)

FIGURE 2.1. Typical bacte rial survival curve following irradiation.

Tail

Shoulder

Baea p

ao (o 1



bacteria that survive radiation doses at a higher-than-expected level. Although this

survival phenomenon is less well understood than the shoulder, it has been well

documented with radiation and with other environmental stresses. Although the

explanations for this phenomenon are mostly unsatisfactory, it is clear that this is

a subset of the population that exhibits this characteristic in response to environ-mental stress. This characteristic is not heritable, in that subcultures from the

survival tail do not exhibit higher radiation resistance than the homologous parent

population, which suggests that this is a response to environmental stress.

2.4 .1 . Bacteria of Public Health Significance

The application of any nonchemical antimicrobial process to foods can be regardedin terms of the number of logio reductions (D 1 0 values) required to achieve a

predetermined level of safety. A common target level of reduction in the United

States has been 5 Iog10 cycles (5Z)). Although there are limitations to the use of the

D 1 0 value (shoulder and tail effects) as described previously, it still provides a

standard point of reference for process evaluation and control. In addition to these

limitations, the effect of irradiation on the death of microorganisms can also be

significantly affected by environmental conditions and the nature of the food ma-

trix. This is discussed in more detail in Section 2.5. Tables 2.1 and 2.2 present D 1 0

values for selected bacteria of public health significance.

As can be seen from a review of the information in Tables 2.1 and 2.2, there is

wide variation in microbial sensitivity to irradiation. However, the greatest resis-

tance to radiation is seen with spore forming bacteria. Bacterial spores are more

resistant to radiation than vegetative cells, in part because of their extremely low

moisture content. A "typical" vegetative cell may be composed of as much as 70%

water, while the moisture content of a "typical" spore is less than 10%. Thereduced levels of moisture in spores minimize the secondary effects of irradiation,

with a net result of an increase in resistance to radiation.

2.4.2. Viruses

Although not as extensively researched as bacteria, there are data available on the

sensitivity of pathogenic viruses to radiation. Because of the biology of viruses,most notably the small size of their genetic material and a very low moisture

content, human viruses are even more resistant to radiation than bacterial spores.

Table 2.3 presents D 1 0 values for some viruses of public health significance. Food-

borne viruses account for a significant portion of foodborne disease in the United

States (Mead et al. 1999), but typically enter the food chain during preparation. A

typical viral outbreak would occur if a food preparation employee, ill with the

virus, were to subsequently contaminate food that was served to many people.

Irradiated foods would be equally susceptible to contamination at this point inthe food chain, with irradiation offering neither an advantage or disadvantage to



Conditions

Spore Formers

20-25

0

C;aerobic

-780C, aerobic; spores

-780C

50C

-8O0C; type A

-8O0C; type B

20-250C; type E

20-250

C

Non-Spore Formers

2-40C

120C

12 0C

O0C

O0C

-78

0

CpH7

20-250C

1O0C

Medium

Distilled water

Mozzarella cheese

Yogurt

Buffer

Buffer

Buffer

Beef stew

Water

Chicken

Chicken

Gound beef

Trypticase soy broth

Phospahte buffer

Ice creamPhosphate buffer

Physiological saline

Poultry

Meat

Bacterium

Bacillus cereus

Clostridium botulinum

Clostridium perfringens

Listeria monocytogenes

Staphylococcus aureus

TABLE 2.1. D IQ Values for Selected Gram -Positive B acteria of Public Health Sign



Conditions

20C

-150C

0-50C

0-5

0

C; vacuum-17

0C

2-50C

30C; S. typhimurium

30C; S. typhimurium

2O0C; S. typhimurium

-4O0C; vacuum; S. typhimurium

-4O0C; air; S. typhimurium

-4O

0

C; air; S. enteritidis-4O

0C; air; S. newport

-4O0C; air; S. anatum

Frozen; S. seftenberg

Frozen; S. gallinarum

S. dysenteriae

S. dysenteriae

S. flexneri

S. flexneri

S. sonnei

S. sonnei

Frozen; V. cholerae

Frozen; V parahaemolyticus

250C

-3O0C

Medium

Ground fish

Ground fish

BHI broth

Ground turkey

Ground beef

Ground beef

Gravy

Roast beef

Ground beef

Deboned chicken

Deboned chicken

Deboned chickenDeboned chicken

Deboned chicken

Liquid whole egg

Liquid whole egg

Oysters

Crabmeat

Oysters

Crabmeat

Oysters

Crabmeat

Prawns

Shrimp

Ground beef

Ground beef

Minced meat

Bacterium

Aeromonas hydrophila

Campylobacter jejuni

Escherichia coli 0157 : H7

Salmonella

Shigella

Vibrio

Yersinia enterocolitica

TABLE 2.2. D10 Values for Selected Gram-Negative Bacteria of Public Health Sig



D10Conditions

-90-160C

O0C

Medium

Raw and cooked beef

Fish

MEM medium

Oysters

Oysters

Virus

Coxsackie

Polio

Echovirus

Hepatitis A

Rotavirus S A I l

TABLE 2.3. D I O Values for Selected Viruses of Public Health Significance



contamination. The resistance of viruses to radiation would only be a factor in

processing shellfish that would be consumed raw.

2.4.3. Parasites

Parasites of public health significance are far more sensitive to radiation than

are either bacteria or viruses. The parasite Trichinella spiralis has been the most

extensively studied in regard to radiation, with a report from 1921 demonstrating

the ability to control this parasite with radiation (Schwartz 1921). Further studies

have shown that a dose of 0.3 kGy is sufficient to eliminate the public health

concern regarding this parasite in pork (Brake et al. 1985). Other parasites, such

as Taeniarhynchus sag inatus (known as Cysticercus bovis in cattle), exhibit a

relatively high resistance to radiation [3 kGy, (Van Kooy and Robjins 1968)], but

are rendered noninfective at lower doses [0.4 kGy, (Tolgay et al. 1972)].

2.5. ENVIRONMENTAL FACTORS AFFECTING

RADIATION SENSITIVITY

The lethal effect of radiation on biological hazards is in part affected by theenvironmental conditions under which the organism is irradiated. The most sig-

nificant environmental factor is the temperature at which irradiation occurs. The

effect of temperature on the lethality of a given radiation dose is seen clearly during

irradiation at freezing and above-freezing temperatures. As an example, the D i 0

value for Clostridium botulinum type A is almost 1 kGy greater when the bacterium

is irradiated at freezing temperatures in comparison to refrigeration temperatures

[Table 2.1 (Anellis et al. (1977)]. Perhaps one of the best illustrations of this effect

has been reported with Escherichia coli O157: H7, where the reported D i 0 valuealmost doubled between + 5 0 C (0.2SkGy) and - 5 0 C [0.44 kGy (Thayer and Boyd

1993)]. This research clearly shows the biphasic response of the bacterium to

temperature, as the D 1 0 values were relatively constant at temperatures above

O0C, and were likewise relatively constant at irradiation temperatures below O0C.

The cause of this change in sensitivity to radiation is due to the change of state of

the water molecules in the cell. When the water is no longer in a liquid form, the

radiation chemistry of the water is changed, so that the secondary or indirect effects

of irradiation are minimized.Other environmental factors may also affect the sensitivity of microorganisms to

radiation. The composition of the medium in which the microorganism is sus-

pended may have a profound effect on radiation sensitivity. In one study, the

reported D i 0 value for Listeria monocytogenes in nutrient broth was 0.35 kGy,

but the D I O value in ground chicken was 0.77 kGy (Huhtanen et al. 1989). Another

study reported that the D 1 0 values for Sa lmonella senftenberg were 0.13 kGy (buf-

fer) and 0.56 kGy [bone meal (Ley et al. 1963)]. Many of these effects attributable

to media may, at a very basic level, also be attributable to the availability of waterin the medium.



2.6. OTHER ISSUES

Two concerns that have been raised regarding the irradiation of microorganisms are

the effect of the reduction in the natural microflora on surviving pathogens and the

potential for the development of radiation resistant mutants. Radiation processing

dramatically reduces the populations of indigenous microflora in foods. The con-

cern that has been expressed is that these "clean" foods would allow a more rapid

outgrowth of bacteria of public health concern, since the lower populations of

indigenous microflora would have less of an antagonistic effect on the pathogenic

bacteria (Jay 1995). If correct, this hypothesis would also support the theory that

irradiated foods would be more amenable to the growth of foodborne pathogens if

the food were contaminated after irradiation. This hypothesis has apparently been

refuted, at least in regard to radiation processing, in both chicken (Szczawiska et al.

1991) and ground beef (Dickson and Olson 1999). In both cases, the growth rates

of either salmonellae (chicken and beef) or Escherichia coll O157:H7 (beef)

were the same in both nonirradiated and irradiated meats. This suggests that the

indigenous microflora in these products does not normally influence the growth

parameters of these bacteria.

The concern with radiation mutations is significant, because ionizing radiation

has been known for many years to induce mutations (Muller 1928). However,

irradiation has not been shown to induce pathogenicity in a nonpathogenic bacte-

rium, but has been shown to reduce the virulence of pathogenic bacteria (Ingram

and Farkas 1977). Most bacteria that undergo radiation-induced mutations are more

susceptible to environmental stresses, so that a radiation-resistant mutant would be

more sensitive to heating than would its nonradiation-resistant parent strain.

2 .7 . CONCLUSIONS

Radiation processing of foods has been demonstrated to be a safe and effective

means of reducing or eliminating biological hazards in foods (WHO 1994). The

process has been shown to be able to pasteurize or sterilize foods, based on the

amount of energy applied to the food. The consensus of the available scientific

information suggests that irradiation processing would effectively control many

biological hazards associated with foods, without resulting in any adverse effects.

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Food Irradiation Principles 004