Risk Assessment of Human Listeriosis from Semisoft Cheeses Made from Raw Sheep's Milk in Lazio and Tuscany (Italy)

Semisoft cheese made from raw sheep's milk is traditionally and economically important in southern Europe. However, raw milk cheese is also a known vehicle of human listeriosis and contamination of sheep cheese with Listeria monocytogenes has been reported. In the present study, we have developed and applied a quantitative risk assessment model, based on available evidence and challenge testing, to estimate risk of invasive listeriosis due to consumption of an artisanal sheep cheese made with raw milk collected from a single flock in central Italy. In the model, contamination of milk may originate from the farm environment or from mastitic animals, with potential growth of the pathogen in bulk milk and during cheese ripening. Based on the 48-day challenge test of a local semisoft raw sheep's milk cheese we found limited growth only during the initial phase of ripening (24 hours) and no growth or limited decline during the following ripening period. In our simulation, in the baseline scenario, 2.2% of cheese servings are estimated to have at least 1 colony forming unit (CFU) per gram. Of these, 15.1% would be above the current E.U. limit of 100 CFU/g (5.2% would exceed 1,000 CFU/g). Risk of invasive listeriosis per random serving is estimated in the 10-12 range (mean) for healthy adults, and in the 10-10 range (mean) for vulnerable populations. When small flocks (10-36 animals) are combined with the presence of a sheep with undetected subclinical mastitis, risk of listeriosis increases and such flocks may represent a public health risk.

[1]  S. Casu,et al.  Estimating lactation curves and seasonal effects for milk, fat and protein in Sarda dairy sheep with a test day model , 1995 .

[2]  L. Tessier,et al.  Control of Listeria monocytogenes in raw-milk cheeses. , 2006, International journal of food microbiology.

[3]  C. Leclercq,et al.  The Italian National Food Consumption Survey INRAN-SCAI 2005–06: main results in terms of food consumption , 2009, Public Health Nutrition.

[4]  F. Morgan,et al.  Survival of Listeria monocytogenes during manufacture, ripening and storage of soft lactic cheese made from raw goat milk. , 2001, International journal of food microbiology.

[5]  R. Comunian,et al.  Sheep's and goat's dairy products in Italy: Technological, chemical, microbiological, and sensory aspects , 2011 .

[6]  L. Guillier,et al.  Growth rate and growth probability of Listeria monocytogenes in dairy, meat and seafood products in suboptimal conditions , 2005, Journal of applied microbiology.

[7]  Liu Jun-hui Improvement of the Animal Feeding Stuffs—Determination of Trypsin Inhibitor Activity of Soybean Products(ISO 14902:2001) , 2009 .

[8]  J. Karns,et al.  Quantitative risk assessment of listeriosis due to consumption of raw milk. , 2011, Journal of food protection.

[9]  M. Wagner,et al.  Important vectors for Listeria monocytogenes transmission at farm dairies manufacturing fresh sheep and goat cheese from raw milk. , 2011, Journal of food protection.

[10]  E. H. Marth,et al.  Behavior of Listeria monocytogenes during manufacture and ripening of brick cheese. , 1989, Journal of Dairy Science.

[11]  D. Mercanti,et al.  Studies on a fast method for determining the yield in the production of Argentinean sheep cheeses , 2008 .

[12]  E. H. Marth,et al.  Fate of Listeria monocytogenes during the Manufacture, Ripening and Storage of Feta Cheese. , 1989, Journal of food protection.

[13]  M. Medina,et al.  Incidence of Listeria monocytogenes and other Listeria spp. in Ewes' Raw Milk. , 1994, Journal of food protection.

[14]  R T Mitchell,et al.  Listeria monocytogenes and listeriosis: a review of hazard characterisation for use in microbiological risk assessment of foods. , 2004, International journal of food microbiology.

[15]  R. C. Whiting,et al.  When is simple good enough: a comparison of the Gompertz, Baranyi, and three-phase linear models for fitting bacterial growth curves , 1997 .

[16]  N Bemrah,et al.  Quantitative risk assessment of human listeriosis from consumption of soft cheese made from raw milk. , 1998, Preventive veterinary medicine.

[17]  A. Margolles,et al.  Behavior of Listeria monocytogenes during the Manufacture, Ripening, and Cold Storage of Afuega'l Pitu Cheese. , 1997, Journal of food protection.

[18]  J Olley,et al.  Relationship between temperature and growth rate of bacterial cultures , 1982, Journal of bacteriology.

[19]  Moez Sanaa,et al.  Risk Assessment of Listeriosis Linked to the Consumption of Two Soft Cheeses Made from Raw Milk: Camembert of Normandy and Brie of Meaux , 2004, Risk analysis : an official publication of the Society for Risk Analysis.

[20]  M. Griffiths,et al.  Survivial of Bioluminescent Listeria monocytogenes and Escherichia coli 0157:H7 in Soft Cheeses , 1998 .

[21]  S. Hulin,et al.  Behaviour of Listeria monocytogenes in raw milk Cantal type cheeses during cheese making, ripening and storage in different packaging conditions , 2015 .

[22]  Rhona K. M. Smith Regulation (EC) No 883/2004 of the European Parliament and of the Council of 29 April 2004 , 2015 .

[23]  A. De Cesare,et al.  Survival kinetics of Listeria monocytogenes on raw sheep milk cured cheese under different storage temperatures. , 2014, International journal of food microbiology.

[24]  M. Sanaa,et al.  Modelling the fate of Listeria monocytogenes during manufacture and ripening of smeared cheese made with pasteurised or raw milk. , 2011, International journal of food microbiology.

[25]  S. Virdis,et al.  Listeria monocytogenes growth potential in Ricotta salata cheese , 2012 .

[26]  M. Wiedmann,et al.  Ecology and Transmission of Listeria monocytogenes Infecting Ruminants and in the Farm Environment , 2004, Applied and Environmental Microbiology.

[27]  T. Farver,et al.  Growth and Survival of Listeria monocytogenes in Market Cheeses Stored at 4 to 30°C. , 1991, Journal of food protection.

[28]  Janne Lundén,et al.  Human Listeriosis Outbreaks Linked to Dairy Products in Europe , 2004 .

[29]  Panagiotis N. Skandamis,et al.  Prevalence and sources of cheese contamination with pathogens at farm and processing levels , 2010 .

[30]  Patrick F. Fox,et al.  Comparison of the microbiological, compositional, biochemical, volatile profile and sensory characteristics of three Italian PDO ewes’ milk cheeses , 2003 .

[31]  M. Wagner,et al.  A case of sporadic ovine mastitis caused by Listeria monocytogenes and its effect on contamination of raw milk and raw-milk cheeses produced in the on-farm dairy , 2003, Journal of Dairy Research.

[32]  R. G. Kroll,et al.  Growth of Listeria monocytogenes in Camembert and other soft cheeses at refrigeration temperatures , 1993, Journal of Dairy Research.

[33]  G. Fthenakis,et al.  Naturally occurring subclinical ovine mastitis associated with Listeria monocytogenes , 1998 .

[34]  S. Ferreira-Dias,et al.  Evolution of Listeria monocytogenes populations during the ripening of naturally contaminated raw ewe’s milk cheese , 2007 .

[35]  S. Omar,et al.  A study of the occurrence of Listeria species in raw sheep milk , 2008 .

[36]  M. Wagner,et al.  Clinical and histopathological aspects of naturally occurring mastitis caused by Listeria monocytogenes in cattle and ewes. , 2004, Journal of veterinary medicine. B, Infectious diseases and veterinary public health.

[37]  J. McLauchlin,et al.  Association between a case study of asymptomatic ovine listerial mastitis and the contamination of soft cheese and cheese processing environment with Listeria monocytogenes in Portugal. , 2009, Foodborne pathogens and disease.

[38]  K. Thong,et al.  Prevalence, characterisation, and antimicrobial resistance of Listeria species and Listeria monocytogenes isolates from raw milk in farm bulk tanks , 2013 .