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Pathogens in Cheese and Foodborne Illnesses

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Fundamentals of Cheese Science

Summary

This chapter summarises foodborne illness due to cheese. Since 1980, there have been 53 outbreaks of food poisoning due to the consumption of cheese during which time almost 250,000,000 tonnes of cheese were produced. The most common organisms involved were Listeria monocytogenes, enteropathogenic Escherichia coli, particularly 0157:H7, Salmonella and Staphylococcus aureus. Of these, listeriosis is the most serious since many outbreaks have resulted in fatalities. The factors controlling the growth of pathogens are the same as those controlling the growth of starters and non-starter lactic acid bacteria in cheese (see Chap. 6). Generally, soft cheeses are more likely to be involved in cheese-associated outbreaks of foodborne illness than hard and semi-hard cheese. Generally, no details of the compositional data of the cheese involved in an outbreak are given, e.g., pH, salt and moisture; such information could be important in understanding how outbreaks occurred. Each of the four groups of bacteria involved is considered in some detail regarding their origin, the symptoms of the illness and the experimental evidence for their growth in cheese. Many cheeses are made from raw milk and confounding factors other than the use of raw milk were involved in these outbreaks.

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References

  • Allerberger F, Kreidl P, Dierich MP et al (2000) Salmonella enterica serotype Oranienburg infections associated with consumption of locally produced Tyrolean cheese. Euro Surveill 5(11):123–126

    Google Scholar 

  • Anon (1995) Brucellosis associated with unpasteurised milk products abroad. Commun Dis Rep No 5(32):151

    Google Scholar 

  • Anon (1997a) Salmonella gold-coast and Cheddar cheese: update. Commun Dis Rep No 7(11): 93, 96

    Google Scholar 

  • Anon (1997b). Vero cytotoxin producing Escherichia coli O157. Commun Dis Rep No 7(46):409, 412

    Google Scholar 

  • Anon (2004) Bacteriological safety of cheeses made from raw or thermised milk. In: 2nd Trimester National Microbiological Survey. Food Safety Authority of Ireland, Dublin

    Google Scholar 

  • Aureli P, Franciosa G, Pourshaban M (1996) Foodborne botulism in Italy. Lancet 348:1594 (1 page)

    Article  CAS  Google Scholar 

  • Austin C, Saathoff-Huber L, Bordson M et al (2008) Outbreak of multidrug-resistant Salmonella enterica serotype Newport infections associated with consumption of unpasteurized Mexican-style aged cheese--Illinois, March 2006-April 2007. MMWR 57(16):432–435

    Google Scholar 

  • Azadian BS, Finnerty GT, Pearson AD (1989) Cheese borne meningitis in immunocompetent patient. Lancet 333:322–323

    Article  Google Scholar 

  • Bachmann HP, Spahr U (1995) The fate of potentially pathogenic bacteria in Swiss hard and semi-hard cheeses made from raw milk. J Dairy Sci 78:476–483

    Article  CAS  Google Scholar 

  • Bautista L, Kroll RG (1988) Survival of some non-starter bacteria in naturally ripened and enzyme-accelerated Cheddar cheese. J Dairy Res 55:597–602

    Article  CAS  Google Scholar 

  • Bell C, Kyriakides A (1998) E. coli. A practical approach to the organism and its control in foods. Blackie Academic and Professional, London

    Google Scholar 

  • Bell C, Kyriakides A (2002) Salmonella. A practical approach to the organism and its control in foods. Blackie Academic and Professional, London

    Google Scholar 

  • Bille J (1990) Epidemiology of human listeriosis in Europe with special reference to the Swiss outbreak. In: Miller AJ, Smith JL, Somkuti GA (eds) Foodborne listerosis. Elsevier, Amsterdam, pp 71–74

    Google Scholar 

  • Bille J, Blanc DS, Schmid H et al (2006) Outbreak of human listeriosis assocoaited with Tomme cheese in Northwest Switzerland, 2005. Euro Surveill 11(6):91–93

    CAS  Google Scholar 

  • Bone FJ, Bogie D, Morgan-Jones SC (1989) Staphylococcal food poisoning from sheep milk cheese. Epidemiol Infect 103:449–458

    Article  CAS  Google Scholar 

  • Cody SH, Abbott SL, Marfin AA et al (1999) Two outbreaks of multidrug-resistant Salmonella serotype typhimurium DT104 infections linked to raw-milk cheese in Northern California. JAMA 281:1805–1810

    Article  CAS  Google Scholar 

  • D’Amico DJ, Donnelly CW (2011) Characterization of Staphylococcus aureus strains isolated from raw milk utilized in small-scale artisan cheese production. J Food Prot 74:1353–1358

    Article  Google Scholar 

  • Dalmasso M, Jordan K (2014) Absence of growth of Listeria monocytogenes in naturally contaminated Cheddar cheese. J Dairy Res 81:46–53

    Article  CAS  Google Scholar 

  • Deschenes G, Casenave C, Grimont F et al (1996) Cluster of cases of haemolyticuraemic syndrome due to unpasteurised cheese. Pediatr Nephrol 10:203–205

    Article  CAS  Google Scholar 

  • Desenclos JC, Bouvet P, Benz-Lemoine E et al (1996) Large outbreak of Salmonella enterica serotype paratyphi B infection caused by a goats’ milk cheese, France, 1993: a case finding and epidemiological study. BMJ 312:91–94

    Article  CAS  Google Scholar 

  • Donaghy JA, Totton NL, Rowe MT (2004) Persistence of Mycobacterium paratuberculosis during manufacture and ripening of Cheddar cheese. Appl Environ Microbiol 70:4899–4905

    Article  CAS  Google Scholar 

  • deValk H, Delarocque-Astagneau E, Colomb G et al (2000) A community wide outbreak of Salmonella enterica serotype Typhimurium infection associated with eating a raw milk soft cheese in France. Epidemiol Infect 124:1–7

    Article  CAS  Google Scholar 

  • Dominguez M, Jourdan-Da Silva N, Vaillant V et al (2009) Outbreak of Salmonella enterica serotype Montevideo infections in France linked to consumption of cheese made from raw milk. Foodborne Pathog Dis 6:121–128

    Article  CAS  Google Scholar 

  • Durch J, Ringhan T, Manner K et al (2000) Outbreak of Escherichia coli O157:H7 infection associated with eating fresh cheese curds--Wisconsin, June 1998. MMWR 49:911–913

    Google Scholar 

  • Ellis A, Preston M, Borczyk A et al (1998) A community outbreak of Salmonella berta associated with a soft cheese product. Epidemiol Infect 120:29–35

    Article  CAS  Google Scholar 

  • Espié E, Vaillant V, Mariani-Kurkdjian P et al (2006) Escherichia coli O157 outbreak associated with fresh unpasteurized goats’ cheese. Epidemiol Infect 134:143–146

    Article  Google Scholar 

  • Espinosa F H, Ryan W M, Vigil P L et al (1983) Group C streptococcal infections associated with eating homemade cheese – New Mexico MMWR 32: 510, 515–516

    Google Scholar 

  • Even S, Charlier C, Nouaille S et al (2009) Staphylococcus aureus virulence expression is impaired by Lactococcus lactis in mixed cultures. Appl Environ Microbiol 75:4459–4472

    Article  CAS  Google Scholar 

  • Even S, Leroy S, Charlier C et al (2010) Low occurrence of safety hazards in coagulase negative staphylococci isolated from fermented foodstuffs. Int J Food Microbiol 139:87–95

    Article  CAS  Google Scholar 

  • Fontaine RE, Cohen ML, Martin WT, Vernon TM (1980) Epidemic salmonellosis from Cheddar cheese: surveillance and prevention. Am J Epidemiol 111:247–253

    CAS  Google Scholar 

  • Frank JF, Marth EH, Olson NF (1977) Survival of enteropathogenic and non-pathogenic Escherichia coli during the manufacture of Camembert cheese. J Food Prot 40:835–842

    Google Scholar 

  • Fretz R, Sagel U, Ruppitsch W et al (2010a) Listeriosis outbreak caused by acid curd cheese Quargel, Austria and Germany 2009. Euro Surveill 15(5):pii=19477

    Google Scholar 

  • Fretz R, Pichler J, Sagel U et al (2010b) Update: multinational listeriosis outbreak due to ‘Quargel’, a sour milk curd cheese, caused by two different L. monocytogenes serotype 1/2a strains, 2009–2010. Euro Surveill 15(16):pii=9543

    Google Scholar 

  • Gaulin C, Ramsay D, Bekal S (2012) Widespread listeriosis outbreak attributable to pasteurized cheese, which led to extensive cross-contamination affecting cheese retailers, Quebec, Canada, 2008. J Food Prot 75:1–78

    Google Scholar 

  • Gianfranceschi M, D’Ottavio MC, Gattuso A et al (2006) Listeriosis associated with Gorgonzola (Italian blue-veined cheese). Foodborne Pathog Dis 3:190–195

    Article  CAS  Google Scholar 

  • Gilot P, Hermans C, Yde M et al (1997) Sporadic case of listeriosis associated with the consumption of a Listeria monocytogenes-contaminated ‘Camembert’ cheese. J Infect 35:195–197

    Article  CAS  Google Scholar 

  • Gori K, Mortensen C, Jespersen L (2010) A comparative study of the anti-listerial activity of smear bacteria. Int Dairy J 20:555–559

    Article  Google Scholar 

  • Goulet V, Jacquet C, Vaillent V et al (1995) Listeriosis from consumption of raw-milk cheese. Lancet 345:1581–1582

    Article  CAS  Google Scholar 

  • Guillier L, Stahl V, Hezard B et al (2008) Modelling the compeditive growth between Listeria monocytogenes and biofilm microflora of smear cheese wooden shelves. Int J Food Microbiol 128:51–57

    Google Scholar 

  • Haeghebaert S, Sulem P, Deroudille L et al (2003) Two outbreaks of Salmonella enteritidis phage type 8 linked to the consumption of Cantal cheese made with raw milk, France, 2001. Euro Surveill 8(7):151–156

    CAS  Google Scholar 

  • Hargrove RE, McDonough FE, Mattingly WA (1969) Factors affecting survival of Salmonella in Cheddar and Colby Cheese. J Milk Food Technol 32:480–484

    CAS  Google Scholar 

  • Hedberg CW, Korlath JA, D’Aoust JY et al (1992) A multistate outbreak of Salmonella javiana and Salmonella oranienberg infections due to contaminated cheese. JAMA 268:3203–3207

    Article  CAS  Google Scholar 

  • Hicks SJ, Lund BM (1991) The survival of listeria in cottage cheese. J Appl Microbiol 70:308–314

    CAS  Google Scholar 

  • Honish L, Predy G, Hislop N et al (2005) An outbreak of E. coli O157:H7 hemorrhagic colitis associated with unpasteurized Gouda cheese. Can J Public Health 96:182–184

    Google Scholar 

  • Hunt DC, Banez Ocfemia MC, Neises D et al (2009) Campylobacter jejuni infection associated with unpasteurised milk and cheese- Kansas 2007. MMWR 57:1377–1379

    Google Scholar 

  • Hunt K, Drummond N, Murphy M et al (2012) A case of bovine raw milk contamination with Listeria monocytogenes. Irish Vet J 65:13–17

    Google Scholar 

  • Ingham SC, Su YC, Spangenberg DS (2000) Survival of Salmonella typhimurium and Escherichia coli O157:H7 in cheese brines. Int J Food Microbiol 61:73–79

    Article  CAS  Google Scholar 

  • Izquierdo E, Marchioni E, Aoude-Werner D et al (2009) Smearing of soft cheese with Enterococcus faecium WHE 81, a a multi-bacteriocin producer, against Listeria monocytogenes Food Microbiol 26:16–20

    Google Scholar 

  • Jackson KA, Biggerstaff M, Tobin-D’Angelo M et al (2011) Multistate outbreak of Listeria monocytogenes associated with Mexican-style cheese made from pasteurized milk among pregnant Hispanic women. J Food Prot 74:949–953

    Article  CAS  Google Scholar 

  • Jelastopulu E, Venieri D, Komninou G et al (2006) Outbreak of acute gastroenteritis in an air force base in Western Greece. BMC Public Health 6:254

    Article  Google Scholar 

  • Johnson EA, Nelson JH, Johnson M (1990a) Microbiological safety of cheese made from heat-treated milk.1.Executive Summary, Introduction and History. J Milk Food Technol 53:441–452

    Google Scholar 

  • Johnson EA, Nelson JH, Johnson M (1990b) Microbiological safety of cheese made from heat-treated milk. 2. Microbiology. J Milk Food Technol 53:519–540

    Google Scholar 

  • Johnson EA, Nelson JH, Johnson M (1990c) Microbiological safety of cheese made from heat-treated milk. 3. Technology, discussions, recommendations, bibliography. J Milk Food Technol 53:610–623

    Google Scholar 

  • Kagkli DM, Vancanneyt M, Vandamme P et al (2007) Contamination of milk by enterococci and coliforms from bovine faeces. J Appl Microbiol 103:1393–1405

    Google Scholar 

  • Lind L, Reeser J, Stayman K et al (2007) Salmonella typhimurium infection associated with raw milk and cheese consumption--Pennsylvania, 2007. MMWR 56:1161–1164

    Google Scholar 

  • Linnan MJ, Mascola M, Lou XO et al (1988) Epidemic listeriosis associated with Mexican-style cheese. N Engl J Med 319:823–828

    Article  CAS  Google Scholar 

  • Little CL, Rhoades JR, Sagoo SK et al (2008) Microbiological quality of retail cheeses made from raw, thermized or pasteurized milk in the UK. Food Microbiol 25:304–312

    Article  CAS  Google Scholar 

  • Loessner M, Guenther S, Steffan S et al (2003) A pediocin-producing Lactobacillus plantarum strain inhibits Listeria monocytogenes in a multispecies cheese surface microbial ripening consortium. Appl Environ Microbiol 69:1854–1857

    Google Scholar 

  • MacDonald KL, Eidson M, Strohmeyer C et al (1985) A multistate outbreak of gastrointestinal illness caused by enterotoxigenic Escherichia coli in imported semisoft cheese. J Infect Dis 151:716–720

    Article  CAS  Google Scholar 

  • MacDonald PD, Whitwam RE, Boggs JD et al (2005) Outbreak of listeriosis among Mexican immigrants as a result of consumption of illicitly produced Mexican-style cheese. Clin Infect Dis 40:677–682

    Article  Google Scholar 

  • Maguire HCF, Boyle M, Lewis MJ et al (1992) An outbreak of Salmonella dublin infection in England and Wales associated with a soft, unpasteurised cow’s milk cheese. Epidemiol Infect 109:389–396

    Article  CAS  Google Scholar 

  • Maher MM, Jordan KN, Upton ME et al (2001) Growth and survival of E. coli O157:H7 during the manufacture and ripening of a smear-ripened cheese produced from raw milk. J Appl Microbiol 90:201–207

    Google Scholar 

  • Makino SI, Kawamoto K, Takeshi K et al (2005) An outbreak of food-borne listeriosis due to cheese in Japan, during 2001. Int J Food Microbiol 104:189–196

    Article  Google Scholar 

  • Marier R, Wells JG, Swanson RC et al (1973) An outbreak of enteropathogenic Escherichia coli foodborne disease traced to imported French cheese. Lancet 2:1376–1378

    Google Scholar 

  • McCollum JT, Williams NJ, Beam SW et al (2012) Multistate outbreak of Escherichia coli O157:H7 infections associated with in-store sampling of an aged raw-milk Gouda cheese, 2010. J Food Prot 75:759–765

    Article  Google Scholar 

  • Modi R, Hirvi Y, Hill A et al (2001) Effect of phage on survival of Salmonella enteritidis during manufacture and storage of Cheddar cheese made from raw and pasteurized milk. J Food Prot 64:927–933

    Google Scholar 

  • O’Sullivan L, O’Connor EB, Ross RP et al (2006) Evaluation of live culture producing Lacticin 3147 as a treatment for the control of Listeria monocytogenes on the surface of smear-ripened cheese. J Appl Microbiol 100:135–143

    Google Scholar 

  • Panico MG, Primiano F, Nappi F et al (1999) An outbreak of Salmonella enteritidis food poisoning from a commercially produced cheese. Euro Surveill 4(4):47–48

    Google Scholar 

  • Pastore R, Schmid H, Altpeter E et al (2008) Outbreak of Salmonella serovar Stanley infections in Switzerland linked to locally produced soft cheese, September 2006 - February 2008. Euro Surveill 13(37):Pii=18979

    Google Scholar 

  • Peng S, Hoffmann W, Bockelmann W et al (2013) Fate of Shiga toxin producing and generic Escherichia coli during production and ripening of semi-hard raw milk cheese. J Dairy Sci 96:815–823

    Article  CAS  Google Scholar 

  • Ratnam S, Stratton F, O’Keefe C et al (1999) Salmonella enteritidis outbreak due to contaminated cheese--Newfoundland. Can Commun Dis Rep 25:17–19

    CAS  Google Scholar 

  • Reitsma CJ, Henning DR (1996) Survival of enterohemorragic Escherichia coli 0157:H7 during the manufacture and curing of Cheddar cheese. J Food Prot 59:460–464

    Google Scholar 

  • Rutzinski JL, Marth EH, Olson NF (1979) Behavior of Enterobacter aerogenes and Hafnia species during the manufacture and ripening of Camembert cheese. J Food Prot 42:790–793

    Google Scholar 

  • Ryser ET, Marth EH (1987) Behavior of Listeria monocytogenes during the manufacture and ripening of Cheddar cheese. J Food Prot 50:7–13

    Google Scholar 

  • Sadik C (1986). An epidemiological investigation following an infection by Salmonella typhimurium due to the ingestion of cheese made from raw milk. In: Proceedings of 2nd World Congr. Foodborne Infect Intoxications 1, 280–282

    Google Scholar 

  • Sharpe JCM (1987) Infections associated with milk and dairy products in Europe and North American, 1980–85. Bull World Health Organ 65:397–406

    Google Scholar 

  • Spahr U, Schafroth K (2001) Fate of Mycobacterium avium subsp. paratuberculosis in Swiss hard and semihard cheese manufactured from raw milk. Appl Environ Microbiol 67:4199–4205

    Article  CAS  Google Scholar 

  • Stephan R, Schumacher S, Tasara T et al (2007) Prevalence of Mycobacterium avium susp. paratuberculosis in Swiss raw milk cheeses collected at retail level. J Dairy Sci 80:3590–3595

    Google Scholar 

  • Tindall BJ, Grimont PAD, Garrity GM et al (2005) Nomenclature and taxonomy of the genus Salmonella. Int J Syst Evol Microbiol 55:521–524

    Article  CAS  Google Scholar 

  • Todd ECD, Szabo R, Gardiner MA et al (1981) Staphylococcal intoxication from cheese curds. Quebec. Can Dis Weekly Rep 7:171–172

    Google Scholar 

  • Tuckey SL, Stiles ME, Ordal ZJ et al (1964) Relation of cheesemaking operations to survival and growth of Staphylococcus aureus in different varieties of cheese. J Dairy Sci 47:604–611

    Google Scholar 

  • Vaillant V, Haeghebaert S, Desenclos JC (1996) Outbreak of Salmonella dublin infection in France, November-December 1995. Euro Surveill 1(2):9–10

    Google Scholar 

  • van Cauteren D, Jourdan-da Silva N, Weill FX et al (2009) Outbreak of Salmonella enterica serotype Muenster infections associated with goat’s cheese, France, March 2008. Euro Surveill 14(31):Pii=19290

    Google Scholar 

  • Villar RG, Macek MD, Simons S et al (1999) Investigation of multidrug-resistant Salmonella serotype typhimurium DT104 infections linked to raw-milk cheese in Washington State. JAMA 281:1811–1816

    Article  CAS  Google Scholar 

  • Weinmaier T, Riesing M, Ratttei, T et al (2013) Complete genome sequence of Listeria monocytogenes LL195, a serotype 4b strain from the 1983–1987 listeriosis outbreak in Switzerland. Genome Announc 1:e00152-12

    Google Scholar 

  • Wood DS, Collins-Thompson DL, Irvine DM et al (1984) Source and persistence of Salmonella muenster in naturally contaminated Cheddar cheese. J Food Prot 47:20–22

    Google Scholar 

Suggested Reading

  • Balaban N, Rasooly A (2000) Review Stapylococcus enterotoxins. Int J Food Microbiol 61:1–10

    Article  CAS  Google Scholar 

  • Brooks JC, Martinez B, Stratton J et al (2012) Survey of raw milk cheeses for microbiological quality and prevalence of foodborne pathogens. Food Microbiol 31:154–158

    Article  CAS  Google Scholar 

  • De Buyser ML, Dufour B, Maire M et al (2001) Implication of milk and milk products in food-borne diseases in France and in different industrialised countries. Int J Food Microbiol 67:1–17

    Google Scholar 

  • Delhalle L, Ellouze M, Yde M et al (2012) Retrospective analysis of a Listeria monocytogenes contamination episode in raw milk goat cheese using quantitative microbial risk assessment tools. J Food Prot 75:2122–2135

    Article  CAS  Google Scholar 

  • Donnelly CW (2001) Factors associated with hygienic control and quality of cheeses prepared from raw milk. Bull 369, International Dairy Federation, Brussels, pp 16–27

    Google Scholar 

  • Farrokh C, Jordan K, Auvray F et al (2013) Review of Shiga-toxin-producing Escherichia coli (STEC) and their significance in dairy production. Int J Food Microbiol 162:190–212

    Article  CAS  Google Scholar 

  • Gandhi M, Chikindas ML (2007) Listeria: a foodborne pathogen that knows how to survive. Int J Food Microbiol 113:1–15

    Article  Google Scholar 

  • Goerges S, Koslowski M, Velagic S et al (2011) Anti-listerial potential of food-borne yeasts in red smear cheese. Int Dairy J 21:3–89

    Article  Google Scholar 

  • Guenther S, Loessner MJ (2011) Bacteriophage biocontrol of Listeria monocytogenes on soft ripened white mold and red-smear cheeses. Bacteriophage 1:94–100

    Article  Google Scholar 

  • Peng S, Tasara T, Hummerjohann J et al (2011) An overview of molecular stress response mechanism in Escherichia coli contributing to survival of shiga toxin-producing Escherichia coli during raw milk cheese production. J Food Prot 74:849–864

    Google Scholar 

  • Roth E, Schwenninger SM, Eugster-Meier E et al (2011) Facultative anaerobic halophilic and alkaliphilic bacteria isolated from a natural smear ecosystem inhibit Listeria growth in early ripening stages. Int J Food Microbiol 147:26–32

    Google Scholar 

  • Schlesser JE, Gerdes R, Ravishankar S et al (2006) Survival of a five-strain cocktail of Escherichia coli O157:H7 during the 60-day aging period of Cheddar cheese made from unpasteurized milk. J Food Prot 69:990–998

    CAS  Google Scholar 

  • van Duynhoven YTHP, Isken LD, Borgen K et al (2009) A prolonged outbreak of Salmonella typhimurium infection related to an uncommon vehicle: hard cheese made from raw milk. Epidemiol Infect 137:1548–1557

    Google Scholar 

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Fox, P.F., Guinee, T.P., Cogan, T.M., McSweeney, P.L.H. (2017). Pathogens in Cheese and Foodborne Illnesses. In: Fundamentals of Cheese Science. Springer, Boston, MA. https://doi.org/10.1007/978-1-4899-7681-9_19

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