bacterial challenges in food · bacterial challenges infood to workin terms oftheld50-thedosethat...

Postgraduate Medical Journal (October 1974) 50, 636-643.

Bacterial challenges in food

J. G. COLLEEM.D., M.R.C.Path.

University Medical School, Teviot Place, Edinburgh

SummaryQualitative and quantitative aspects of bacterialchallenges that might be encountered in food are dis-cussed with reference to recognized and relatively un-recognized hazards. Mechanisms of pathogenicity arereviewed and the populations at risk are noted. Thebacterial content of food as it is served at table meritsmore study. The challenge of prevention by educationis discussed. Indirect bacterial challenges in our foodare considered. The real challenge of diagnosis dependsupon an awareness of a complex range of conditions;the importance of effective communication with effi-cient laboratory and epidemiological services isstressed. There is an increasing need for care in thepreparation and distribution of food.

Components of pathogenicityThe various components involved in the expression

of bacterial pathogenicity were summarized byStanier, Doudoroff and Adelberg (1958) as follows.The source of the infectious agent may be a case ofthe disease or a carrier; a human or an animal sourceis usually incriminated. There is then a stage oftransmission of the infectious challenge when anopportunity allows transfer to a new host, followed

by a process during which the infectivity of the agentmay be established. Thereafter, the organism ex-presses its virulence and damages the host by essen-tially invasive or toxic mechanisms or a combinationof these (Fig. 1).The above concepts are changing, but they can be

applied in various degrees to the food-borne diseasescaused by bacteria. The outcome of such an attackon a new host depends upon many variables thatmay influence the host-parasite association and theseinclude the nature and size of the challenge dose. Itis useful to consider qualitative and quantitativeaspects of the bacterial challenges that may bedelivered in our food, and it is convenient to includemilk and water in this consideration.

Measurement of challenge dosesIn experimental work, infective hazards are con-

sidered in relation to the size of the challenge dosethat may produce some demonstrable effect. Asimple example, at least in theory, is the minimumlethal dose (MLD) for a specified test animal. Inpractice, as animal and human responses to infectiveor toxic challenges vary so much among individuals,the MLD is not a reliable measurement. It is better

SOURCE TRANSMISSION INFECTION

Microbial factors

Viability *

Resistance** *Effective dose * \* *Avenue of infection \ *Vehicle of infection*

INVASIVENESS TOXIGENICITY

VIRULENCEFIG. 1. The 'components' of microbial pathogenicity.

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Bacterial challenges in food

to work in terms of the LD50-the dose that is lethalfor 500% of a test group of similar animals. If thestandard indicating effect is not death but someother result, we work in terms of the effective dose(ED) and the ED50. The ID50 is similarly used ifinfectivity is measured. There is no need to berestricted to 50% in these measurements; the ED75or the ED35 might be of interest. However, it is wellknown that dose-response curves tend to be linear intheir mid-section and are far from linear at theextremes where individual variation is so obvious.In experimental work, therefore, we are seldom con-cerned with the ED1-the effective dose for 1% ofthe test group; and we are even less concerned withthe dose that might affect 0.01 % of the test group.On the other hand, those who are responsible for

the production and distribution of our processedfoods realize that they have in Britain a potentialtest group of 50 million individuals. An ED1challenge in a widely distributed food under thesecircumstances would be catastrophic. Moreover, ahuman population is in no way composed of similarindividuals. Susceptibility to various bacterial chal-lenges in such a group varies enormously, and thereare innumerable permutations of circumstances thatmight influence the challenges and those challenged.It is therefore clear that a food manufacturer musttake into account and make some allowances for:(1) unfavourable situations that may adversely affecthis product; and (2) unduly susceptible members ofthe public, for example those at extremes of age orconvalescent patients, who may be more severelychallenged by the bacterial content of his products.

Infections associated with a low challenge doseA few organisms have specific infective potential

at relatively low challenge doses and these are per-haps passively carried on hands or in food or drinkto produce new cases. Such infective hazards includetyphoid fever and Escherichia coli gastro-enteritis.We are still uncertain regarding the infective dosesof the respective pathogens and it is possible that rela-tively small numbers can cause disease in certaincircumstances. For example, the transmissibility oftyphoid fever depends upon the ingestion of aneffective dose by a new host. Barrier nursing pro-cedures may protect the immediate contacts of anacute case, but the infection is classically transmittedby the inadvertent contamination of a water supplyor food with excreted bacilli from a carrier oftyphoid. The circumstances usually suggest that alow challenge dose is involved and the sporadic wayin which new cases arise, unless a real epidemicgets going, indicates that an extension of the ED1concept may be valid. However, it is not fundamen-tally clear why typhoid differs so markedly in itsepidemiology from bacillary dysentery.

Bacillary dysentery is a convincing example of aninfection in which a hand-to-mouth transmissionappears to operate. Our present evidence suggeststhat relatively direct spread is involved in this case,perhaps involving 'mediate contact', and that foodor drink is not typically involved.Some forms of infantile gastro-enteritis caused by

enteropathogenic strains of E. coli share features incommon with bacillary dysentery and acute typhoidinfections; food and eating utensils and feedingbottles may well be involved here. At the presentstage of our ignorance, these diseases can begrouped together on the basis of their hand-to-mouthinfectivity or their 'passive transfer' in food or drink,though a clinical bacteriologist, a clinician and anepidemiologist would all argue that these diseasesare poles apart. The term 'passive transfer' is coinedhere to denote transfer without multiplication in thevehicle, but a multiplication stage in food cancertainly occur and the challenge could then be evenmore severe.

Gastro-intestinal infections that can be trans-mitted by small challenge doses are characteristicallydifficult to control and are associated with a tendencyto spread with the production of secondary cases,despite modern toilet systems (Thomas and Tillett,1973a, b; Leading Article, 1973). Our lack of care inthis context is deplorable, and the design and use ofthe 'modern' toilet system in general take inadequatenote of hygienic principles. This is also true of ourcatering.

Infections associated with larger challenge dosesInfections that seem to be associated with moder-

ately large challenge doses under certain circum-stances include brucellosis, cholera, and Vibrioparahaemolyticus food poisoning, with milk, waterand fish as the respective vehicles involved. It mightbe helpful to consider that these diseases, possiblyinvolving quantitatively significant challenges, are'actively transferred' in their vehicles. The diseasesoccur when circumstances allow a relatively largechallenge to be delivered, but control can be achievedby relatively simple hygienic practices such aspasteurization, sewage engineering, and cold storage.

Infections associated with very large challenge dosesSalmonella food poisoning and Clostridium welchii

food poisoning operate in entirely different ways.The types offood involved also differ, but in each casea prior booster stage is involved when the infectingorganism multiplies in food. Although Cl. welchiiultimately presents a toxic challenge in vivo, theinitial development of the disease depends uponingestion of large numbers of viable organisms.The mechanism of pathogenicity involved inSalmonella food poisoning is not understood, but

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J. G. Cotlee

again the ingestion of large numbers of viable organ-isms is characteristically required. In both of theseforms of food poisoning, the important point is thata possibly harmless degree of contamination is trans-formed into an effective challenge at some point infood-handling. The effective dose is generally con-sidered to be some thousands or tens of thousandsof organisms of food-poisoning species of Salmon-ella (Taylor and McCoy, 1969), and some millionsof Cl. welchii (Hobbs, 1969). These conditions illus-trate the dangers of the booster effect that occurswhen circumstances of time and temperature allowbacterial multiplication in food at some stage in itspreparation. It should be borne in mind that somestrains of food-poisoning Salmonella serotypes havespread among hospital patients in a manner thatsuggests that low challenge doses of these organismsmay sometimes be effective.

Direct toxic challengesSome bacterial food-poisoning conditions result

from ingestion of a toxin that has been preformed inthe food. Although the bacteria that produced thetoxin are usually ingested along with the toxin, thepathogenesis does not necessarily involve an infec-tive step in vivo. The elaboration of an effective doseof toxin depends upon contamination of the foodwith the toxigenic bacteria; subsequent mishandlingof the food allows bacterial multiplication and toxinproduction.The classical example is botulism caused by Cl.

botulinum, especially types A, B and E in the caseof man. Some of these organisms can grow andproduce toxin at temperatures as low as 1-5°C.

Staphylococcal food poisoning is also a directintoxication. The staphylococcal enterotoxin (aneurotoxin) is produced when enterotoxigenicstrains of Staphylococcus aureus grow in certainfoods such as salt-cooked meats and dairy products.As the hands are so often involved in contaminatingfoods with staphylococci and with other potentialpathogens, it is perhaps time to discard the termfoodhandler as a professional label and to reserve itas a term of abuse in the kitchen when certain foodsthat should be untouched are handled.

Bacillus cereus, an organism that abounds as anaerobic spore-former in nature, sometimes contami-nates foods such as left-over cooked rice and may thengrow and produce a toxin. This is associated with aform of Chinese restaurant food poisoning.

Mechanisms of pathogenicity in the intestineThe following patterns of attack have been con-

sidered and there is much interest in the mechanismsof pathogenicity that may be involved. Savage(1972) and Craig (1972) have summarized and dis-

cussed some of these (see also Hornick et al., 1970;Formal, Dupont and Hornick, 1973).

(1) Local infection, usually non-invasive, with nosingle toxin recognized: Salmonella food poisoning;E. coli gastro-enteritis.

(2) Local infection with local invasion but norecognized toxin: Shigella dysentery (but see vanHeyningen, 1971); E. coli gastro-enteritis.-(3) Local invasion with generalized invasion; no

single toxin incriminated: Typhoid fever andbrucellosis.

(4) Local infection with no invasion; enterotoxinproduced in vivo: Cl. welchii food poisoning; cholera;V. parahaemolyticus food poisoning; E. coli gastro-enteritis.

(5) Direct intoxication with a preformed toxin;infection not primarily involved: Botulism; staphylo-coccal food poisoning; B. cereus food poisoning.

These concepts summarized in Table 1 will requiremodification as our knowledge advances. Entero-pathogenic strains of E. coli presently appear tomerit classification in various categories and it ispossible that the pathogenesis of infantile gastro-enteritis differs significantly from that of variousforms of E. coli diarrhoea that may afflict adults.The potential pathogenicity and transmissibility ofsome strains of this species, especially among veryyoung children in hospital, are frightening remindersof our lack of understanding of the challenges in-volved. Parallel studies of diarrhoeal disease inanimals (e.g. by Smith and Linggood, 1971) indicatethat special antigens may be of importance in allow-ing a coliform pathogen to colonize and attack asusceptible area of the small gut. The preferentialattachment of certain bacterial pathogens to mucosalsurfaces has been discussed by Savage (1972). The'invasiveness' of certain pathogens at the host cellsurface may depend upon a phagocytic reaction ofthe host cell that is triggered by the pathogen.

The population at riskAlthough distributors of bulk-produced in-

gredients and processed foods pay attention to thebacterial content of their products, remarkablylittle attention has been paid to the bacterial contentof foods served at table. As it is presented at table,or in hospital, or in the nursery, our food is regularlycontaminated with many different organisms (Mc-Killop, 1959; Riemann, 1969; Anderson andGatherer, 1970; Ayliffe, Collins and Pettit, 1970;Cooke et al., 1970; Shooter et al., 1970, 1971).Some of these organisms are generally regarded asindices of faecal contamination and the implicationsare disturbing.

Ideally, hygienic precautions should be taken tominimize the degree of initial contamination, and asubsequent bactericidal heat-treatment should re-

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Bacterial challenges in food 639

TABLE 1. A provisional guide to some features of the causative organisms of various food-borne diseases

Infectivechallenge dose Known toxic

Disease Transmission involved Invasiveness challenge*

Bacillary dysentery Hand-to-mouth + LocalTyphoid fever 'Passive' in water, + General -t

milk or foodEscherichia coli ? Passive in ? +, + + or + + + Local or nil§ - or + (in vivo)

gastro-enteritis s water, milk {Brucellosis or food +k GeneralCholera J ++ - + (in vivo)Vibro parahaemolyticus 'Active' in food + + - + (in vivo)food poisoning

Salmonella Booster stage in + + + Local$ -tfood poisoning food or milk

Clostridium welchii Booster stage + + + - + (in vivo)food poisoning in food

Staphylococcal Booster stage in - - + + (EXO) (N)food poisoning food or milk

Bacillus cereus Booster stage - - + + (EXO)food poisoning in food

Botulism Booster stage - - + + + (EXO) (N)in food

* 'In vivo' here indicates that toxin is elaborated within the gut; 'EXO' indicates that a known exotoxin isrecognized; 'N' indicates neurotoxic activity.

t The endotoxins of various pathogenic Gram-negative bacteria are toxic, but the pathogenicity of theseorganisms is not solely attributable to their production of endotoxin.

4 Some of the food-poisoning salmonellae, notably S. typhimurium, are occasionally invasive.§ E. coli may be fiercely invasive in the neonate or young child.-= nil or not recognized;+, + +, + + + = increasing numbers of viable organisms (challenge dose) or increasing severity of toxicchallenge.

duce any challenge still further. The pasteurizationof milk is a good example, but our record with creamis not good (Leading Article, 1970a). Circumstancesthat lead to certain food-poisoning hazards are nowclearly defined and we should at least be able toexclude gross bacterial contamination of our foodduring its preparation. That this is not achieved isclearly shown by the statistics for Cl. welchii foodpoisoning, for example. The occurrence of this formof food poisoning is a direct indictment of the cater-ing practices involved, yet we continue to have manyoutbreaks.

Table 2 summarizes results of studies on carriagerates for so-called typical food-poisoning strains ofCl. welchii. Although it is now known that otherstrains of Cl. welchii can cause food poisoning, thesedata are still of interest. Sutton (1966a, b) was ableto correlate high carrier rates of typical food-poisoning strains with communal feeding and withpoor hygiene. It is disturbing that relatively highcarriage rates were generally reported among hospi-tal patients and personnel by various workers. Thisprobably unfairly singles out hospitals for criticismbecause medical research workers tend to turn theirattention to hospitals for their material. It is quitelikely that institutional meals in general, and possibly

many bulk-cooked meals, fall short of acceptablebacteriological standards. A recent leading article(British Medical Journal, 1972b) entitled 'Bad FoodGuide' draws attention to some current trends incatering that give cause for concern, and anotherleading article (British Medical Journal, 1970b) indi-cates hazards to man that may result when animalsare fed with infected feeding-stuffs. It is also clearthat standards of care in the home are not goodenough. For example, the survey of the hygiene ofinfant-feeding utensils by Anderson and Gatherer(1970) demonstrated that there is much room forimprovement and indicates why E. coli gastro-enteritis still has many opportunities to demonstrateits lethal potential in infants.

It appears that different age-groups and differentsections of the community are particularly likely toencounter or to be affected by certain challenges.The recognized hazards include infantile gastro-enteritis in the first 2 years, and bacillary dysenteryat nursery school and primary day school. At allages, a variety of challenges ranges from Salmonellainfections, which are widespread, to Cl. welchii foodpoisoning particularly associated with bulk-cookedmeat foods at school, hospital or canteen. Otherforms of food poisoning or food-borne infection may



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640 J. G. Collee

TABLE 2. Reported faecal carrier rates for heat-resistant strains of Clostridium welchii

Carrier rateYear Authors Population Country (0)

1953 Hobbs et al. General England 2-21957 Dische and Elek Hospital and England 20

hospital-associated1961 Leeming, Price and Meynell ) Hospital (recently 14-5-22

Iadmitted patients)r Hospital (established England 30-32-5J inpatients) J

1961 Turner and Wong Hospital and Hong Kong 63hospital-associated

J General England 91961 Collee et al. Students Scotland 6-81966b Sutton | General 1-5-6-0

l Subjects associated with Australia 151-25(communal feedingJ and/or poor hygiene

be respectively associated with such special hazardsas meat sandwiches bulk-produced at home, or aChinese restaurant meal prepared under unhygieniccircumstances, or contaminated sea-food eaten raw.

Prevention by educationSome of our raw food is quite seriously contami-

nated at source; for example Cl. welchii is ubiquitous,and salmonellae are often associated with intensivelyreared chickens, calves and pigs. The handling ofraw foods and ready-cooked processed foods in thesame kitchen, on the same work surfaces and some-times with the same utensils, therefore merits specialconsideration in relation to the hazard of cross-contamination. However, conditions such as sal-monella food poisoning and Cl. welchii food poison-ing are not likely to be produced unless the primarycontamination is gross or the challenge dose isboosted in a suitable food that allows growth of thecausative organism. With much of our processedfood nowadays, particularly in restaurants, canteensand institutions, the importance of time and tem-perature in relation to bacterial growth and toxi-genesis is not adequately stressed.The significance of the thermometer scale illus-

trated in Fig. 2 should be clear to every caterer. Thebooster effect normally illustrated as a logarithmicplot (the bacterial growth curve) is not readily com-prehensible in arithmetical terms to catering staff oflimited academic background. Perhaps the 'bio-logical clock' shown in Fig. 3 has a greater impact.The counts given in the clock diagram are based ona mean generation time of20 min, a generally acceptedvalue for mesophilic bacteria multiplying in the ex-ponential phase under good conditions. Actual dataobtained with Cl. welchii (Collee, Knowlden andHobbs, 1961) show that even greater rates of division

can be achieved at temperatures up to 45°C with thisorganism growing in a medium resembling a cookedmeat food.

Processed meats and meat foods are frequentlyincriminated in food-poisoning outbreaks. Oursociety is now geared to the large-scale consumptionof processed meats and to bulk catering, and ourcatering areas and domestic kitchens are usuallycentrally heated. We have been slow to install ade-quate chilling plant and refrigeration facilities toprotect our foods during preparation or holdingperiods under these circumstances. The message ofFig. 4 might litetally bring the point home, but itmust also be conveyed to firms and boards ofmanagement that modern catering demands modernequipment.

Indirect challengesThis is an intriguing area for discussion. Our con-

sumption of sugar and sweets encourages bacterialproduction of dextrans in the mouth and this is re-lated to dental plaque formation and to dental caries.It can therefore be argued that some of our modernfoods have unsafe effects on our commensal floraand this thesis can be extended.The ability of commensal Cl. welchii and Bacter-

oides species in the gut to alter steroid-like moleculesand to transform them into potentially carcinogenicagents (Hill et al., 1971) is of interest to the clinicianconcerned with diet in relation to bowel stasis andslow transit times.

Coliform organisms ingested in food may carryresistance transfer factors (RTF). If a patient harbour-ing such organisms is given an oral broad-spectrumantibiotic (A), there is a possibility that resistantorganisms, including those with the RTF, will beselectively favoured and will become much more



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2120F 10000O 1

Death to- vegetative

bacteria145°F 62800C

120OF - 490C

104°F = 400C IIncubation-danger

zone'98 4°F- 370C

500F 000

45°F - 70C -Relativelysafe

320F 000c j storage

FIG. 2. Holding temperatures in relation to the hazardof growth of mesophilic bacteria in food.

numerous (Anderson, Gillespie and Richmond,1973). When the RTF-bearing organisms are rela-tively numerous, the chances of spread of the RTFto other organisms in the gut are increased and thismay involve a pathogen. Under these circumstances,for example, an antibiotic-sensitive strain of a dysen-tery bacillus would promptly become resistant toantibiotic (A) and to several other antimicrobial sub-stances for which the RTF carried the necessarygenetic information. Antibiotic therapy is notrecommended in most cases of dysentery, but, forexample, the principle has worrying parallels inrelation to typhoid fever.

The challenge of diagnosisIt has been necessary to limit this discussion to

certain bacterial diseases, and to exclude other con-ditions such as abdominal tuberculosis, streptococcal

ixio3x108

2 xl

262,1432,764096

51264

32-.-16/I26 128/

2048 102416,384 8192

131,072 ~-------65,5361,048,576 -____---54x288

8x1066-4x107 3-2x10

5-2x108 26x I8

FIG. 3. A 'bacteriological clock' based on a generationtime of 20 min. The Arabic numerals spiralling from thecentre indicate the increase in numbers of organisms at20-min intervals. The Roman numerals indicate time inhours.

disease and Q fever that can be food-borne. More-over, the medical practitioner must also be aware ofviral, protozoal, fungal, algal and chemical causesof disease that may present with gastro-intestinalsigns and symptoms. The differential diagnosis iscomplex. Clinical appearances suggestive of acerebrovascular attack or of coronary thrombosismay be produced by staphylococcal food-poisoningor botulism; and the syndrome of staphylococcalfood poisoning can be produced by the virus ofwinter vomiting disease (Leading Article, 1965,1972a). Prompt diagnosis can be of vital importance,and an efficient epidemiological service ensuringcommunication between practitioners, clinicians,public health officers and laboratory workers isessential.

The need for careThose of us concerned about food-borne infection

and intoxication are often challenged with the oldadage that 'a peck of dirt never hurt anybody'. Thisdownright lie has hindered the work of hygienists foryears and, as our feeding habits and food productionmethods have evolved during this century, it hasbecome alarmingly evident that the access of a peckof dirt to certain stages of our food processing canhurt many people.Our food is not invariably safe and we manipulate

it in potentially dangerous ways. Our principles and



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642 J. G. Collee

A FRI GE

FIG. 4. A suggested statement of priorities for a societythat consumes many processed foods.

our technology to make food safely and to keep itsafe have been developed and are observed by thelarge commercial undertakings who recognize thehealth risks and the financial risks involved. Thisrequires control of the standard of ingredients andraw materials and subsequent control at all stages ofprocessing, holding and distribution. Then the batonof responsibility for care is often passed to the re-tailer, the caterer or the householder. Present evi-dence suggests that it is not infrequently dropped atthat stage and that we may unwisely challenge ourbabies, our patients and the general public. Theseare not 'natural' challenges, any more than feedingbottles or processed foods are 'natural'. The risksinvolved have been contrived by man whose chang-ing practices and procedures allow special bacterialchallenges to evolve and to be delivered. The presentsymposium is therefore timely.

It is not possible to given an unqualified assuranceregarding the safety of our food. Although it mustbe conceded that less harm seems to arise than analarmed bacteriologist might predict, very disturbing

examples of carelessness are frequently reported andmany people are annually affected with food-bornedisease. It seems clear that more care is needed.

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infant-feeding utensils. Practices and standards in thehome. British Medical Journal, 1, 20.

ANDERSON, J.A.D., GILLESPIE, W.A. & RICHMOND, M.H.(1973) Chemotherapy and antibiotic-resistance transferbetween enterobacteria in the human gastro-intestinaltract. Journal of Medical Microbiology, 6, 461.

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COOKE, E.M., SHOOTER, R.A., KUMAR, P.J., RoUSSEAU, S.A.& FOULKES, A.L. (1970) Hospital food as a possible sourceof Esch. coli in patients. Lancet, i, 436.

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