C.L. Little

Prepared salads and public health

In recent years the importance of prepared salads as potential vehicles of gastrointestinal infection has been highlighted by several large outbreaks both nationally and across international boundaries. Between 1992 and 2006, 2274 foodborne general outbreaks of infectious intestinal disease were reported in England and Wales, of which 4% were associated with the consumption of prepared salads. In total, 3434 people were affected, with 66 hospitalizations and one death reported. The attribution of prepared salad types and pathogens among prepared salad associated outbreaks are presented and discussed. Findings from UK studies on salad vegetables, fruit and mixed salads from 1995 to 2007 (21 247 samples) indicate that most bacteria of concern with regard to human health are relatively rare in these products (98·6% of satisfactory quality); however, outbreaks of salmonellosis were uncovered associated with bagged salad leaves and fresh herbs during two such studies. Although it is known that fresh salad vegetables, herbs or fruit may become contaminated from environmental sources, only in recent years has the association of foods of nonanimal origin, such as salad vegetables, with foodborne illness become evident and recurrent, demonstrating that major health problems can arise from consumption of contaminated prepared salads if hygiene practices breakdown.

Microbiological quality of retail cheeses made from raw, thermized or pasteurized milk in the UK.

Two studies of retail fresh, ripened and semi-hard cheeses made from raw, thermized or pasteurized milk were undertaken in the UK during 2004 and 2005 to determine the microbiological quality of these products. Using microbiological criteria in European Commission Recommendations 2004/24/EC and 2005/175/EC, 2% of both raw, thermized (37/1819 samples) and pasteurized (51/2618 samples) milk cheeses were of unsatisfactory quality. Raw or thermized milk cheeses were of unsatisfactory quality due to levels of Staphylococcus aureus at 10(4)cfu g(-1), Escherichia coli at 10(5)cfu g(-1), and/or Listeria monocytogenes at 10(2)cfu g(-1), whereas pasteurized milk cheeses were of unsatisfactory quality due to S. aureus at 10(3)cfu g(-1) and/or E. coli at 10(3)cfu g(-1). Salmonella was not detected in any samples. Cheeses were of unsatisfactory quality more frequently when sampled from premises rated as having little or no confidence in management and control systems, and stored/displayed at above 8 degrees C. Raw or thermized milk cheeses were also more likely to be of unsatisfactory quality when they were unripened types, and pasteurized milk cheeses when they were: semi-hard types; from specialist cheese shops or delicatessens; cut to order. These results emphasize the need for applying and maintaining good hygiene practices throughout the food chain to prevent contamination and/or bacterial growth. Labelling of cheeses with clear information on whether the cheese was prepared from raw milk also requires improvement.

Campylobacter and Salmonella in raw red meats in the United Kingdom : Prevalence, characterization and antimicrobial resistance pattern, 2003-2005

The prevalence of Campylobacter and Salmonella was assessed in 3959 raw red meats in the UK during 2003-2005. Meats were more frequently contaminated with Campylobacter (7.2%) than with Salmonella (2.4%). Lamb and other meats (e.g. mutton, rabbit) exhibited the highest contamination from Campylobacter (12.6% and 19.8%, respectively), compared with pork (6.3%) and beef (4.9%). Pork however had the highest contamination from Salmonella (3.9%), followed by lamb (2.0%), other meats (2.0%) and beef (1.3%). Offal samples (36.6%) were more frequently contaminated with Campylobacter or Salmonella than muscle tissue (7.0%). C. jejuni predominated in all meat types. C. coli isolates were more likely to exhibit antimicrobial drug resistance, including quinolones, than C. jejuni. Salmonella typhimurium was the most frequent Salmonella serotype isolated from meats; S. typhimurium DT104/104b isolates exhibited higher rates of multiple drug resistance than other serotypes. The findings reinforce the importance of adequate cooking of meat and good hygiene to avoid cross-contamination.

Changing Pattern of Human Listeriosis, England and Wales, 2001–2004

Disease has reemerged, mainly in patients ≥60 years of age with bacteremia.

A 17-year review of foodborne outbreaks: describing the continuing decline in England and Wales (1992–2008)

Systematic national surveillance of foodborne disease outbreaks effectively serves the development of public health policy on food safety. The Health Protection Agency has maintained a collaborative surveillance system for foodborne outbreaks in England and Wales since 1992. Up to 2008, 2429 foodborne outbreaks were identified, described and analysed for changes over time. Salmonella spp. accounted for half of the outbreaks, although the proportion of these decreased over the surveillance period. Similarly, the proportion of outbreaks caused by Clostridium perfringens decreased, while those attributed to Campylobacter spp. and Vero cytotoxin-producing Escherichia coli O157 increased. Although poultry meat was the most frequently implicated food vehicle in outbreaks followed by miscellaneous foods and red meats, the proportion of outbreaks attributed to meats in fact decreased over time but those linked to miscellaneous foods did not. Over the surveillance period, the proportion of outbreaks linked to eggs and S. Enteritidis non-phage-type 4, particularly in food service establishments, increased, highlighting the importance of this organism/setting/vehicle association. Contributory factors in most outbreaks were cross-contamination, inadequate heat treatment, and inappropriate food storage. This study describes the overall decline in foodborne outbreaks, providing evidence that the introduction and adherence to effective control measures provide the best means of minimizing the risk of foodborne infection.

Microbiological study of fresh herbs from retail premises uncovers an international outbreak of salmonellosis

This Local Authorities Co-ordinators of Regulatory Services/Health Protection Agency study was prompted by the increasing concern regarding the microbiological safety of ready-to-eat salad vegetable products, particularly fresh herbs. During May to October 2007, 3760 ready-to-eat fresh herbs, of different varieties, were sampled across the UK to assess their microbiological safety in relation to salmonella contamination and levels of Escherichia coli. Sixty (1.6%) herb samples were found to be of unsatisfactory quality according to Regulation (EC) No. 2073/2005 on the microbiological criteria of foodstuffs, i.e. contaminated with Salmonella spp. and/or containing E. coli at >10(3) cfu/g. When criteria in the PHLS Microbiological Guidelines for some ready-to-eat foods (2000) were used, 117 (3.9%) of herb samples were of unsatisfactory quality due to the presence of salmonella and/or E. coli at > or = 10(2) cfu/g. Eighteen (0.5%) samples of six different herb types were contaminated with Salmonella spp.: identified as serotypes Senftenberg (8), Agona (2), Anatum (1), Durban (1), Javiana (1), Mgulani (1), Montevideo (1), Unnamed (I 16:g, t: z42) (1), Virchow (1) and mixed Newport & Virchow (1). In each case the retailer and the UK Food Standards Agency were immediately informed and remedial action taken. Samples contaminated with S. Senftenberg were specifically associated with basil grown in Israel. Thirty-two human cases of S. Senftenberg infection were subsequently identified throughout England and Wales and a further 19 in Scotland, Denmark, The Netherlands and the USA. The strain of S. Senftenberg identified from the basil and that from cases had an indistinguishable molecular profile, suggesting a likely connection between consumption of basil and human infection. The presence of Salmonella spp. is unacceptable in ready-to-foods such as fresh herbs. This study highlights the necessity of applying good agricultural and hygiene practices pre-, during and post-harvest, at processing, retail and use. These practices help to prevent cross-contamination and/or bacterial growth occurring in these products. Best practice is to store and display such products at, or below, 8 degrees C as this inhibits bacterial growth.

Prevalence and Level of Listeria monocytogenes and Other Listeria Species in Selected Retail Ready-to-Eat Foods in the United Kingdom

Although listeriosis is a rare cause of human disease in the United Kingdom, an increase in the number of cases has been observed since 2001, almost exclusively in persons older than 60 years. This increase prompted this study on the microbiological safety of ready-to-eat (RTE) foods, which included those types potentially linked to cases of listeriosis. Between May 2006 and April 2007, 6,984 RTE foods were sampled (2,168 sliced meats, 1,242 hard cheese, 1,088 sandwiches, 878 butter, 725 spreadable cheese, 515 confectionery products containing cream, and 368 probiotic drinks). The food types with the highest prevalence of Listeria monocytogenes were sandwiches (7.0%) and sliced meats (3.7% within shelf life, 4.2% end of shelf life). L. monocytogenes at > 100 CFU/g (exceeding the European Commissions food safety criteria limit) only occurred in sandwiches (0.4%) and sliced meats (0.7% within shelf life, 1.0% end of shelf life). Contamination with L. monocytogenes at >100 CFU/g was more frequent in meats that were prepacked and/or of pack size > or = 300 g and in sandwiches that were supplied prepacked that contained salad vegetables as an ingredient. Satisfactory microbiological quality was associated with premises on which the management was trained in food hygiene and those that complied with hazard analysis and critical control point principles. This study provides important information about the microbiological safety of RTE foods and demonstrates that the control of L. monocytogenes in such foods, and in particular sandwiches and sliced meats, is essential in order to minimize the risk of this bacterium being present at levels hazardous to health at the point of consumption.

The microbiological safety of ready-to-eat specialty meats from markets and specialty food shops: a UK wide study with a focus on Salmonella and Listeria monocytogenes.

From 2359 specialty meats (continental sausages, cured/fermented, dried meats) sampled from markets and specialty food shops, 98.9% of samples were of satisfactory or acceptable microbiological quality. However, 16 (0.7%) were unsatisfactory as a result of Escherichia coli, Staphylococcus aureus or Listeria spp. contamination (>or=10(2) CFU/g), and nine (0.4%) were unacceptable due to presence of Salmonella spp. or Listeria monocytogenes (>10(2) CFU/g). Meats with unacceptable levels of L. monocytogenes were within shelf life (range: 8-143 days remaining). Nine different subtypes of L. monocytogenes were detected with sero/AFLP type 1/2c VII predominating (37%), although this subtype was not overrepresented in any particular meat type (P > 0.05). Ninety-six percent of continental sausages and cured/fermented products were stored at <8 degrees C at premises, including seven of the nine unacceptable samples. These nine meats were all pre-packed prior to supply to retail premises (OR = 0.1 P = 0.003) indicating that contamination with bacterial pathogens occurred earlier in the production chain. Most samples (72.7%, 8/11) with unsatisfactory levels of E. coli were sliced on request, suggesting cross-contamination at point of sale. This study highlights the importance of ensuring that products do not become contaminated before final packaging, that storage conditions are controlled, and that durability dates are an accurate indication of the shelf life of the product so as to minimise the potential for L. monocytogenes to be present at levels hazardous to health at the point of sale.

Assessment of the microbiological safety of edible roasted nut kernels on retail sale in England, with a focus on Salmonella.

There is little published information on the prevalence of Salmonella in edible nut kernels. A study in early 2008 of edible roasted nut kernels on retail sale in England was undertaken to assess the microbiological safety of this product. A total of 727 nut kernel samples of different varieties were examined. Overall, Salmonella and Escherichia coli were detected from 0.2 and 0.4% of edible roasted nut kernels. Of the nut varieties examined, Salmonella Havana was detected from 1 (4.0%) sample of pistachio nuts, indicating a risk to health. The United Kingdom Food Standards Agency was immediately informed, and full investigations were undertaken. Further examination established the contamination to be associated with the pistachio kernels and not the partly opened shells. Salmonella was not detected in other varieties tested (almonds, Brazils, cashews, hazelnuts, macadamia, peanuts, pecans, pine nuts, and walnuts). E. coli was found at low levels (range of 3.6 to 4/g) in walnuts (1.4%), almonds (1.2%), and Brazils (0.5%). The presence of Salmonella is unacceptable in edible nut kernels. Prevention of microbial contamination in these products lies in the application of good agricultural, manufacturing, and storage practices together with a hazard analysis and critical control points system that encompass all stages of production, processing, and distribution.

Survey of Salmonella contamination of edible nut kernels on retail sale in the UK

Consumption of nut kernels has shown an upward trend due to peoples increasing tendency to eat healthy snacks. The purpose of this survey was to establish the microbiological safety of retail edible nut kernel samples of different varieties. Overall Salmonella spp. and Escherichia coli were detected from 0.1% and 0.8% of 2886 edible nut kernels, respectively. S. Senftenberg and S. Tennessee were detected from two pre-packed samples of Brazil nuts (0.4%) and S. Anatum from a pre-packed mixed nuts sample (0.9%; mix: almonds, Brazils, cashews, peanuts, walnuts) indicating a risk to health. The levels of Salmonella ranged from <0.01 to 0.23/g. E. coli at unsatisfactory levels (150/g) was present in another pre-packed Brazils nuts sample (0.2%). E. coli was additionally found at lower levels (range: 3.6-43/g) in Brazils (1.9%), macadamia (1.5%), pistachios (1.1%), walnuts (0.7%), peanuts (0.7%), hazels (0.5%), cashews (0.4%), and almonds (0.3%). Levels of E. coli did not correlate with the presence of Salmonella. The batches contaminated with Salmonella were recalled and Food Standards Agency food alerts were issued to advise against the consumption of the affected products. The presence of Salmonella is unacceptable in ready-to-eat foods and follows that the need for applying good agricultural and hygiene practices and effective decontamination procedures during the production of edible kernels cannot be overemphasized.