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The reliability of the examination of foods, processed for safety, for enteric pathogens and Enterobacteriaceae: a mathematical and ecological study

Published online by Cambridge University Press:  15 May 2009

E. F. Drion
Affiliation:
Institute for Mathematics and Statistics, Central Organization TNO, The Hague, The Netherlands
D. A. A. Mossel
Affiliation:
Chair of Food Microbiology, University of Utrecht, The Netherlands
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Because of the paucity of quantitative data on numbers of other enteric pathogens in food, the reliability of the examination of processed foods for Enterobacteriaceae was estimated taking Salmonella as a model. For this purpose an assessment was carried out of the risk of accepting Salmonella contaminated consignments of foods, despite a negative outcome of (i) examination of 1·5 kg samples for Salmonella; (ii) examination of one or two 1 g samples for Enterobacteriaceae; (iii) simultaneous application of both tests. The computations were based on the results of the examination of 6830 samples of dried foods, processed for safety, out of a total of 18170 samples.

Only 69 samples permitted the exact calculation of the factor, defined as c.f.u./g of Enterobacteriaceae/c.f.u./g of Salmonella; 4642 were positive for the former group but ‘free’ from Salmonella, and the rest were negative in both tests. Numbers of c.f.u./g for both groups, and hence the factors, varied widely between commodities and also between different consignments of the same food product. The average for amounted to 5·8 × 103, far from the base-line value of 0·75 × 103 assessed earlier. In only 0·1% of samples did the Enterobacteriaceae test fail to achieve the required consumer protection.

This investigation therefore substantiates that testing foods processed for safety by examining accurately chosen quantities for ecologically well selected and taxonomically thoroughly defined index organisms is a most effective procedure in terms both of consumer protection and simplicity of examination without compelling the food industry to achieve hardly attainable microbiological quality standards.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1977

References

REFERENCES

Alichanidis, E. S. & Tsanetakis, N. M. (1974). Characterisation of bacteria isolated from colonies atypical of the coliform group on desoxycholate lactose agar. Milchwissenschaft 29, 344–5.Google Scholar
Brent, P. & Vosti, K. L. (1973). Micromethod for serogrouping Escherichia coli. Applied Microbiology 25, 208–11.Google Scholar
Brown, C. & Seidler, R. J. (1973). Potential pathogens in the environment: Klebsiella pneumoniae, a taxonomic and ecological enigma. Applied Microbiology 25, 900904.Google Scholar
Busse, M. (1968). Der Enterobakterien-Nachweis bei der Überwachung von Trinkmilch. Milchwissenschaft 23, 414–18.Google Scholar
Canale-Parola, E. & Ordal, Z. J. (1957). A survey of the bacteriological quality of frozen poultry pies. Food Technology 11, 578–82.Google Scholar
Cragg, J. & Andrews, A. V. (1973). Observations on the microbiological flora of canned Parma ham. Journal of Hygiene 71, 417–22.Google Scholar
Dienstag, J. L., Flinstone, S. M., Kapikian, A. Z. & Purcell, R. H. (1975). Immune electron microscopy and hepatitis A. Lancet i, 102.Google Scholar
Drion, E. F. & Mossel, D. A. A. (1972). Mathematical–ecological aspects of the examination for Enterobacteriaceae of foods processed for safety. Journal of Applied Bacteriology 35, 233–9.CrossRefGoogle ScholarPubMed
Edel, W. & Kampelmacher, E. H. (1973). Comparative studies on the isolation of ‘sub-lethally injured’ salmonellae in nine European laboratories. Bulletin of the World Health Organization 48, 167–74.Google Scholar
Emmenegger, T. (1959). Zum Nachweis von Salmonellen in Eiprodukten und anderen Lebensmitteln. Mitteilungen aus dem Gebiet der Lebensmittel-untersuchung und Hygiene 50, 145–58.Google Scholar
Fishbein, M. & Wentz, B. (1973). Vibrio parahaemolyticus methodology for isolation from seafoods and epidemic specimens. Journal of Milk and Food Technology 36, 118–23.Google Scholar
Foster, E. M. (1971). The control of salmonellae in processed foods: a classification system and sampling plan. Journal of the Association of Official Analytical Chemists 54, 259–66.Google ScholarPubMed
Harrewijn, G. A., Mossel, D. A. A. & deGroote, J. Groote, J. (1972). Assessment of the bacteriological safety of lactose. Netherlands Milk and Dairy Journal 26, 141–8.Google Scholar
Hechelmann, H., Rossmanith, E., Peric, M. & Leistner, L. (1973). Untersuchung zur Emittlung der Enterobacteriaceae – Zahl bei Schlachtgeflügel. Fleischwirtschaft 53, 107–13.Google Scholar
Henriksen, S. D. (1955). A study of the causes of discordant results of the presumptive and completed coliform tests on Norwegian waters. Acta Pathologica Microbiologica Scandinavica 36, 8795.Google Scholar
Hobbs, B. C. (1955). The laboratory investigation of non-sterile canned hams. Annales de l'institut Pasteur, Lille 7, 190200.Google Scholar
Hobbs, B. C. & Gilbert, R. J. (1975). The significance of numbers of micro-organisms in food. Zentralblatt für Bakteriologie und Parasitenkunde (Abt. I, Ref.) 242, 165–6.Google Scholar
Holmes, A. W., Deinhardt, F., Wolfe, L., Froesner, G., Paterson, D., Castro, B. & Conrad, M. E. (1973). Specific neutralization of human hepatitis type A in marmoset monkeys. Nature, London 243, 419–20.CrossRefGoogle ScholarPubMed
Hunyady, G., Leistner, L. & Luike, H. (1973). Erfassung von enteropathogenen Escherichia coli – Stammen bei Gefrier-hähnchen mit Kristallviolett-Neutralrot-Galle-Glucose-Agar. Fleischwirtschaft 53, 998–9.Google Scholar
Jacobs, J., Guinée, P. A. M., Kampelmacher, E. H. & Keulen, A. Van (1963). Studies on the incidence of Salmonella in imported fish meal. Zentralblatt für Veterinärmedizin 10, 542–50.Google Scholar
Kallings, L. O., Laurel, A. B. & Zetterberg, B. (1959). An outbreak due to Salmonella typhimurium in veal with special reference to phage and fermentation typing. Acta Pathologica Microbiologica Scandinavica 45, 347–56.CrossRefGoogle ScholarPubMed
Koburger, J. A. (1964). Isolation of Mima polymorpha from dairy products. Journal of Dairy Science 47, 646.CrossRefGoogle Scholar
Koch, R. (1890). Ueber bakteriologische Forschung. Zentralblatt für Bakteriologie und Parasitenkunde 8, 563–73.Google Scholar
Mehlman, I. J., Simon, N. T., Sanders, A. C., Fishbein, M., Olson, J. C. & Read, R. M. (1975). Methodology for enteropathogenic Escherichia coli. Journal of the Association of Official Analytical Chemists 58, 283–92.Google ScholarPubMed
Messer, J. W., Lovett, J., Murthy, G. K., Wehby, A. J., Schafer, M. L. & Read, R. B. (1971). An assessment of some Public Health problems resulting from feeding poultry litter to animals. Microbiological and chemical parameters. Poultry Science 50, 874–81.CrossRefGoogle ScholarPubMed
Meijs, C. C. J.van der, M (1970). Resultaten van een bacteriologisch en chemisch onderzoek van gemalen vlees. Tijdschrift voor Diergeneeskunde 95, 1180–4.Google Scholar
Mossel, D. A. A. (1957). The presumptive enumeration of lactose negative as well as lactose positive Enterobacteriaceae in foods. Applied Microbiology 5, 379–81.Google Scholar
Mossel, D. A. A. (1958). Die Verhütung der Verbreitung von Salmonellosen und sonstigen Enterobacteriosen durch Lebensmittel. Zentralblatt für Bakteriologie und Parasitenkunde (Abt. I, Ref.) 166, 421–32.Google Scholar
Mossel, D. A. A. (1962). Significance of micro-organisms in foods. In Chemical and Biological Hazards in Food (ed. Ayres, J. C. et al. ), pp. 157201. Ames; Iowa State University Press.Google Scholar
Mossel, D. A. A. (1967). Ecological principles and methodological aspects of the examination of foods and feeds for indicator micro-organisms. Journal of the Association of Official Analytical Chemists 50, 91104.Google Scholar
Mossel, D. A. A. (1970). The role of microbiology and hygiene in the manufacture of margarine. In Margarine Today (ed. Coenen, J. W. E., Feron, R. and Mossel, D. A. A.), pp. 104–24. Leiden: Brill.Google Scholar
Mossel, D. A. A. (1974). Bacteriological safety of foods. Lancet i, 173.Google Scholar
Mossel, D. A. A. (1975). Occurrence, prevention and monitoring of microbial quality loss of foods and dairy products. Critical Reviews of Environmental Control 5, 1139.Google Scholar
Mossel, D. A. A. & Drion, E. F. (1958). Sampling of canned foods for bacteriological analysis. Food 27, 333–7.Google Scholar
Mossel, D. A. A., Eelderink, I. & Sutherland, J. P. (1977). Development of and experience with single ‘polytropic’ tubes for the tentative taxonomic grouping of bacteria isolated from foods and water. Zentralblatt für Bakteriologie (Abt. 1, Orig. A). 238, 6679.Google Scholar
Mossel, D. A. A., Harrewijn, G. A. & Nesselrooy-van Zadelhoff, C. F. M. (1974). Standardisation of the selective inhibitory effect of surface active compounds used in media for the detection of Enterobacteriaceae in foods and water. Health Laboratory Science 11, 260–67.Google Scholar
Mossel, D. A. A., Harrewijn, G. A. & Sprang, F. J. Van (1973). Microbiological quality-assurance for weaning formulae. In The Microbiological Safety of Food (ed. Hobbs, B. C. and Christian, J. H. B.), pp. 7788. London: Academic Press.Google Scholar
Mossel, D. A. A. & Krugers Dagneaux, E. L. (1959). Bacteriological requirements for and bacteriological analysis of precooked (‘instant’) cereals and similar foods. Antonie van Leeuwenhoek 25, 230–36.CrossRefGoogle ScholarPubMed
Mossel, D. A. A. & Krugers Dagneaux, E. L. (1963). Die hygienisch-bakteriologische Beurteilung von Trocken-Kochsuppen. Archiv für Lebensmittel Hygiene 14, 108–11.Google Scholar
Mossel, D. A. A., Mengerink, W. H. J. & Scholts, H. H. (1962). Use of a modified MacConkey agar medium for the selective growth and enumeration of Enterobacteriaceae. Journal of Bacteriology 84, 381.Google Scholar
Mossel, D. A. A. & Ratto, M. A. (1970). Rapid detection of sublethally impaired cells of Enterobacteriaceae in dried foods. Applied Microbiology 20, 273–5.Google Scholar
Mossel, D. A. A. & Ratto, M. A. (1973). Wholesomeness of some types of semi-preserved foods. Journal of Food Technology 8, 97103.Google Scholar
Mossel, D. A. A. & Shennan, J. L. (1976). Micro-organisms in dried foods: their significance, limitation and enumeration. Journal of Food Technology 11, 205–19.CrossRefGoogle Scholar
Mossel, D. A. A., Shennan, J. L. & Vega, C. (1973). The bacteriological condition of animal feeds: a survey to aid in determining product standards for proteinaceous food ingredients. Journal of the Science of Food and Agriculture 24, 499508.Google Scholar
Mossel, D. A. A. & Vincentie, H. (1968). The differential Enterobacteriogramme. Laboratory Practice 17, 1344–6.Google ScholarPubMed
Mossel, D. A. A., Visser, M. & Cornelissen, A. M. R. (1963). The examination of foods for Enterobacteriaceae using a test of the type generally adopted for the detection of Salmonellae. Journal of Applied Bacteriology 26, 444–52.Google Scholar
Nouws, J. F. & Heymans, P. G. (1975). A microbiological classification system for minced meat. Archiv für Lebensmittel Hygiene 26, 175–80.Google Scholar
Ray, B., Jezeski, J. J. & Busta, F. F. (1971 a). Isolation of Salmonellae from naturally contaminated dried milk products. 1. Influence of sampling procedure on the isolation of Salmonellae. Journal of Milk and Food Technology 34, 389–93.Google Scholar
Ray, B., Jezeski, J. J. & Busta, F. F. (1971 b). Repair of injury in freeze-dried Salmonella anatum. Applied Microbiology 22, 401–7.Google Scholar
Reusse, U., Hafke, A. & Meyer, A. (1975). Erfahrungen bei der Isolierung von Salmonellen und Enterobacteriaceae. Archiv für Lebensmittel Hygiene 26, 137–43.Google Scholar
Rishbeth, J. (1947). The bacteriology of dehydrated vegetables. Journal of Hygiene 45, 3345.Google Scholar
Rosen, A. & Levin, R. E. (1970). Vibrios from fish pen slime which mimic Escherichia coli on violet red bile agar. Applied Microbiology 20, 107–12.Google Scholar
Schardinger, F. (1892). Ueber das Vorkommen Gahrung erregender Spaltpilze im Trink-wasser und ihre Bedeutung für die hygienische Beurtheilung desselben. Wiener Klinische Wochenschrift 5, 403–5; 421–3.Google Scholar
Schothorst, M.van Mossel, D. A. A., Kampelmacher, E. H. & Drion, E. F. (1966). The estimation of the hygienic quality of feed components using an Enterobacteriaceae enrichment test. Zentralblatt für Veterinärmedizin 13, 273–85.CrossRefGoogle ScholarPubMed
Schothorst, M. van & Leusden, F. M. van (1975). Further studies on the isolation of injured Salmonellae from foods. Zentralblatt für Bakteriologie und Parasitenkunde (Abt I, Orig. A) 230, 186–91.Google ScholarPubMed
Seeliger, H. (1952). Die Keimzahlbestimmung und Differenzierung coliformer Bakterien in Milch und Speiseeis. Milchwissenschaft 7, 389–94.Google Scholar
Semple, A. B., Graham, A. J. & Dutton, E. M. (1961). A review of the sampling of imported desiccated coconut. Medical Officer 105, 5960.Google Scholar
Sheneman, J. M. (1973). Survey of aerobic mesophilic bacteria in dehydrated onion products. Journal of Food Science 38, 206–9.CrossRefGoogle Scholar
Silliker, J. H. & Gabis, D. A. (1973). ICMSF methods studies. I. Comparison of analytical schemes for detection of Salmonella in dried foods. Canadian Journal of Microbiology 19, 475–9.CrossRefGoogle ScholarPubMed
Silverstolpe, L., Plasikowski, U., Kjellander, J. & Vahlne, G. (1961). An epidemic among infants caused by Salmonella muenchen. Journal of Applied Bacteriology 24, 134–42.Google Scholar
Smith, T. (1895). Notes on Bacillus coli communis and related forms, together with some suggestions concerning the bacteriological examination of drinking-water. American Journal of Medical Science, N.S. 110, 283302.CrossRefGoogle Scholar
Spicher, G. (1971). Untersuchungen über das Auftreten coliformer Bakterien und fäkaler Streptokokken in Weizen- und Roggenmehlen. Deutsche Lebensmittel Rundschau 67, 14.Google Scholar
Spicher, G. (1972). Die Mikroflora des Durumweizens und seiner Verarbeitungsprodukte im Blickpunckt der Lebensmittelhygiene. Getreide, Mehl und Brot 26, 246–50.Google Scholar
Splittstoesser, D. F. & Wettergreen, W. P. (1964). The significance of coliforms in frozen vegetables. Food Technology 18, 392–4.Google Scholar
Sutton, R. R. & McFarlane, V. H. (1947). Microbiology of spray-dried whole egg. III. Escherichia coli. Food Research 12, 474–83.Google Scholar
Taylor, W. I. & Schelhart, D. (1971). Isolation of Shigellae. VIII. Comparison of xylose lysine deoxycholate agar, Hektoen enteric agar, Salmonella–Shigella agar and eosin methylene blue agar with stool specimens. Applied Microbiology 21, 32–7.Google Scholar
Turner, R. J. & Campbell, N. E. R. (1962). A bacteriological survey of certain processed meats. Part I. Population studies at packer and retail levels. Canadian Journal of Public Health 53, 382–6.Google Scholar
Willems, R. & Thomas, J. (1959). Contrôle bactériologique des farines animales. Bulletin de l'office International des Epizooties 52, 212–22.Google Scholar
Wundt, W. & Voss, J. (1963). Zur Frage der Verhütung von Infektionen durch Speiseeis. Archiv für Hygiene und Bakteriologie 147, 358–68.Google Scholar
Zipplies, G. (1964). Salmonellenfunde bei der tierärztlichen Lebensmittelüberwachung. Monatshefte für Veterinärmedizin 19, 588–91.Google Scholar
Korowkin, P. P. (1966). Ungleichungen. Berlin: Veb. Deutscher Verlag der Wissenschafter.Google Scholar
Uspensky, J. V. (1937). Introduction to Mathematical Probability. New York: McGraw Hill.Google Scholar