80M. Adams, R. Mitchell / International Journal of Food Microbiology 79 (2002) 75–83Table 2Pasteurisation <strong>and</strong> its association with outbreaks of foodborne illness caused by cheese (data from IFST 1998)Year Location Pathogen Food Unpasteurisedmilk used1992 Engl<strong>and</strong> Salmonella Livingstone cheese no1992/1993 France VTEC fromage frais yes1993 France Salmonella Paratyphi B goats’ milk cheese yes1994 Scotl<strong>and</strong> VTEC (O157) local farm cheese yes1995 France Listeria monocytogenes Brie de Meaux yes1995 Malta Brucella melitensis soft cheese yes1995 Switzerl<strong>and</strong> <strong>and</strong> France Salmonella Dublin cheese from Doubs region yes1996 Engl<strong>and</strong> <strong>and</strong> Scotl<strong>and</strong> Salmonella Gold Coast cheddar cheese pasteurisation failure1996 Italy Clostridium botulinum Marscapone cheese noClearly, while the value of pasteurisation cannot beignored, it is possible to produce safe products withoutit. To do so, however, places even greater emphasison other aspects of the process such as carefulattention to hygiene <strong>and</strong> temperature <strong>control</strong> duringproduction to avoid contamination <strong>and</strong> minimise bacterialgrowth.It is not sufficient to have an estimate of the levelof a hazard in a food <strong>and</strong> the variation in that level.Exposure will also depend on the pattern of consumption—theamount of food consumed by individuals,the average serving size, the frequency of consumption<strong>and</strong> the distribution of that consumption withinthe population. There may be a whole range of socioeconomic,seasonal, regional, ethnic or demographicfactors affecting consumption. For example, UK statisticsindicate that in the year 2000 total cheeseconsumption was equivalent to 110 g per person perweek, but also revealed consumption to be highest inhigher income households, lower in households wherethere were more children, lowest in the Yorkshire <strong>and</strong>Humberside area <strong>and</strong> highest in the Southeast ofEngl<strong>and</strong> (National Food Survey, 2000). Official statisticsmay have rather a broad brush <strong>approach</strong> in thisregard <strong>and</strong> commercial data owned by manufacturers<strong>and</strong> retailers can play a critical role in assembling acomplete picture of the consumption pattern for aparticular product.5. Hazard characterisationIn contrast to exposure <strong>assessment</strong>, which focusesmainly on the food, hazard characterisation is concernedwith what the effect of a hazard will be onpeople. It provides a description of the frequency,nature, severity <strong>and</strong> duration of illness caused by thepresence of the hazard in the food. This can be eitherqualitative or quantitative. Central to this activity isestablishing the relationship between exposure (doseingested) <strong>and</strong> the response (harm caused). This is notan easy task as several interacting factors such as theproperties of the <strong>pathogen</strong>, the food vehicle <strong>and</strong> itsconsumption pattern, the dynamics of infection <strong>and</strong>the individual consumer can all contribute to determiningwhether illness occurs. There is an inherentvariability in each of these <strong>and</strong> this is further compoundedby uncertainty in the data available.For most <strong>pathogen</strong>s a set of characteristic symptomscan be described which are generally associatedwith the illness they cause. However, these symptomscan occur with a widely varying degree of severity <strong>and</strong>complications or long-term sequelae such as reactivearthritis from salmonellosis or Guillain–Barré syndromefrom campylobacteriosis can also sometimesarise (Mossel et al., 1995; Nachamkin et al., 2000).There is considerable variability between strains of thesame organism in their capacity to cause illness, <strong>and</strong>the previous history of a strain can also affect itsvirulence. Human susceptibility to infection can differmarkedly between subpopulations such as younghealthy adults, the very young, the very old, the sick,pregnant women <strong>and</strong> the immuno-compromised aswell as between individuals within subpopulations.This might lead to diffuse outbreaks which are difficultto recognise. The food vehicle can play a significantrole in facilitating infection by protecting the <strong>pathogen</strong>from the effects of the stomach’s acidity. In someoutbreaks associated with fermented foods such ascheese <strong>and</strong> salami, the level of <strong>pathogen</strong> present in
M. Adams, R. Mitchell / International Journal of Food Microbiology 79 (2002) 75–83 81the implicated food has been very low <strong>and</strong> this may bedue to the protective effects of fat (D’Aoust et al.,1985; Getty et al., 2000). Foods that are often consumedon an empty stomach, e.g. at breakfast, couldpose a greater threat due to their more rapid transitthrough the stomach.In the past, the concept of a minimum infectivedose has often been used. The idea that there is acertain threshold below which an organism cannotcause illness may apply to toxigenic <strong>pathogen</strong>s wherea certain population may be necessary to producesufficient toxin to cause illness. In such cases, the<strong>risk</strong> <strong>assessment</strong> procedures will resemble those usedto assess <strong>risk</strong> posed by chemicals. With infectious<strong>pathogen</strong>s which multiply in the body, a single organismcould in principle initiate an infection. Althoughthe chances of infection from a single organism maybe very low, they cannot be neglected entirely, particularlyin view of the low doses implicated in someoutbreaks associated with fermented foods (Getty etal., 2000). Data on the relationship between dose <strong>and</strong><strong>risk</strong> of infection can be obtained from volunteerfeeding trials. These have their own inherent flawssuch as the employment of healthy volunteers <strong>and</strong> thefrequent use of nonfood matrices to deliver the<strong>pathogen</strong> (Kothary <strong>and</strong> Babu, 2001). They are alsonot possible with <strong>pathogen</strong>s such as L. monocytogenes<strong>and</strong> E. coli O157 for ethical reasons <strong>and</strong> in these casesoutbreak data have to be relied on. Dose–responsemodelling is currently an active area of research. Useof a number of models has been explored <strong>and</strong> problemsassociated with availability of data, treatment ofsub-populations <strong>and</strong> extrapolation to low doses havebeen identified (see, for example, Coleman <strong>and</strong>Marks, 1998; Teunis et al., 1999; Teunis <strong>and</strong> Havelaar,2000). There is still some way to go in this area.For example, in one study comparing six differentmodels, the estimate of the infectious dose required toaffect 1% of the population ranged over nine orders ofmagnitude (Holcomb et al., 1999).6. Risk characterisationThe final step in the <strong>risk</strong> <strong>assessment</strong> process is asynthesis of the information assembled in the earlierstages of the process to produce an estimate of theprobability of illness <strong>and</strong> its severity in a givenpopulation. To be of greatest use informing <strong>risk</strong>management strategies, it would ideally be quantitative,but can be qualitative, <strong>and</strong> must also specify thedegree of uncertainty attending that estimate.Given their huge diversity, quantitative <strong>risk</strong> <strong>assessment</strong>cannot be applied in any meaningful sense tofermented foods as a whole. A more tightly definedstatement of purpose does facilitate this <strong>and</strong> a quantitative<strong>risk</strong> <strong>assessment</strong> has been described covering the<strong>risk</strong> of human listeriosis from consumption of rawmilk soft cheeses (Bemrah et al., 1998). Overall, theepidemiological information indicates that fermentedfoods have a good safety record, particularly in viewof the large quantities consumed worldwide. Oneestimate has suggested that fermented foods of varioustypes can comprise 30% of our food supply(Knorr, 1998). The available data have, however, alsohighlighted some notable exceptions where fermentedfoods have been associated with outbreaks of foodborneillness <strong>and</strong> these have prompted concern in theindustry <strong>and</strong> regulatory intervention in some cases.Further development of <strong>risk</strong> <strong>assessment</strong>s in this areaoffers a powerful <strong>and</strong> valuable tool in successfullymanaging food safety hazards, allowing these interesting<strong>and</strong> appealing foods to be consumed withconfidence.ReferencesAdams, M.R., 1986. Fermented flesh foods. Prog. Ind. Microbiol.23, 159–198.Adams, M.R., 2001. Why fermented foods can be safe. In: Adams,M.R., Nout, M.J.R. (Eds.), <strong>Fermentation</strong> <strong>and</strong> Food Safety. AspenPublishers, Gaithersburg, pp. 39–52.Anon., 1995a. Escherichia coli O157:H7 outbreak linked to commerciallydistributed dry-cured salami—Washington <strong>and</strong> California,1994. Morb. Mortal. Wkly. Rep. 44, 157–160.Anon., 1995b. Community outbreak of haemolytic uremic syndromeattributable to Escherichia coli O111:NM—South Australia,1995. Morb. Mortal. Wkly. Rep. 44, 550–558.Arocha, M.M., Mc Vey, M., Loder, S.D., Rupnow, J.H., Bullerman,L., 1992. Behaviour of enterohaemorrhagic E. coli O157:H7 duringmanufacture of cottage cheese. J. Food Prot. 55, 379–381.Bemrah, N., Sanaa, M., Cassin, M.H., Griffiths, M.W., Cerf, O.,1998. Quantitative <strong>risk</strong> <strong>assessment</strong> of human listeriosis fromconsumption of soft cheeses made from raw milk. Prev. Vet.Med. 37, 129–145.Benford, D., 2001. Principles of Risk Assessment of Food <strong>and</strong>Drinking Water Related to Human Health ILSI Europe, Brussels34 pp.