Christine L. Little

An outbreak due to peanuts in their shell caused by Salmonella enterica serotypes Stanley and Newport: sharing molecular information to solve international outbreaks

Salmonellosis is a global problem caused by the international movement of foods and high incidence in exporting countries. In September 2001, in an outbreak investigation Australia isolated Salmonella Stanley from imported peanuts, which resulted in a wider investigation in Canada, England & Wales and Scotland. Patients infected with Salmonella serotypes known to be isolated from peanuts and reported to surveillance systems were interviewed to determine exposure histories. Tagged image file format (TIFF) images of pulsed-field gel electrophoresis (PFGE) patterns of Salmonella isolates were shared electronically amongst laboratories. Laboratories tested packets of Brand X peanuts from various lots and product lines. In total, 97 cases of S. Stanley and 12 cases of S. Newport infection were found. Seventy-three per cent (71/97) of S. Stanley cases were in persons of Asian ethnicity. Twenty-eight per cent of cases recalled eating Brand X peanuts and a further 13% had peanuts in their house in the previous month or had eaten Asian-style peanuts. Laboratories isolated S. Stanley, S. Newport, S. Kottbus, S. Lexington and S. Unnamed from Brand X peanuts. Isolates of S. Stanley from peanuts and human patients were indistinguishable by PFGE. This international outbreak resulted from a product originating from one country affecting several others. Rapid sharing of electronic DNA images was a crucial factor in delineating the outbreak; multinational investigations would benefit from a harmonized approach.

Packed with Salmonella--investigation of an international outbreak of Salmonella Senftenberg infection linked to contamination of prepacked basil in 2007.

Salmonella Senftenberg is uncommon in the United Kingdom. In January-June 2007, the Health Protection Agency reported on 55 primary human cases of Salmonella Senftenberg in England and Wales. In May 2007, fresh basil sold in the United Kingdom was found to be contaminated with Salmonella Senftenberg. We launched an investigation to elucidate the cause of this outbreak. Isolates were examined using plasmid profiling and pulsed-field gel electrophoresis, and the outbreak strain (SSFTXB.0014) was identified. We enquired via Enter-net whether other countries had isolated the outbreak strain, analyzed samples of fresh herbs from U.K. retailers, and interviewed patients on food history. Thirty-two patient-cases were referred to this outbreak in England and Wales. Onsets of illness occurred between 5 March and 6 June 2007. Fifty-six percent of patient-cases were females and 90% adults (>20 years old); three were admitted to hospital as a result of Salmonella infection. Scotland, Denmark, the Netherlands, and the United States reported on 19 cases of Salmonella Senftenberg infection presenting with the outbreak strain since January 2007. Eight samples of prepacked fresh basil imported from Israel tested positive with the same strain. A minority of patients could recall the consumption of basil before illness, and some reported consumption of products where basil was a likely ingredient. Environmental investigations in Israel did not identify the contamination source. Microbiological evidence suggested an association between contamination of fresh basil and the cases of Salmonella Senftenberg infection, leading to withdrawal of basil from all potentially affected batches from the U.K. market.

Host Association of Campylobacter Genotypes Transcends Geographic Variation

ABSTRACT Genetic attribution of bacterial genotypes has become a major tool in the investigation of the epidemiology of campylobacteriosis and has implicated retail chicken meat as the major source of human infection in several countries. To investigate the robustness of this approach to the provenance of the reference data sets used, a collection of 742 Campylobacter jejuni and 261 Campylobacter coli isolates obtained from United Kingdom-sourced chicken meat was established and typed by multilocus sequence typing. Comparative analyses of the data with those from other isolates sourced from a variety of host animals and countries were undertaken by genetic attribution, genealogical, and population genetic approaches. The genotypes from the United Kingdom data set were highly diverse, yet structured into sequence types, clonal complexes, and genealogical groups very similar to those seen in chicken isolates from the Netherlands, the United States, and Senegal, but more distinct from isolates obtained from ruminant, swine, and wild bird sources. Assignment analyses consistently grouped isolates from different host animal sources regardless of geographical source; these associations were more robust than geographic associations across isolates from three continents. We conclude that, notwithstanding the high diversity of these pathogens, there is a strong signal of association of multilocus genotypes with particular hosts, which is greater than the geographic signal. These findings are consistent with local and international transmission of host-associated lineages among food animal species and provide a foundation for further improvements in genetic attribution.

A recipe for disaster: outbreaks of campylobacteriosis associated with poultry liver pâté in England and Wales.

Despite the frequency of Campylobacter as the principal cause of bacterial gastroenteritis in the UK, outbreaks attributed to this pathogen are rare. One hundred and fourteen general foodborne outbreaks of campylobacteriosis were reported to the Health Protection Agency from 1992 to 2009 with most occurring in food service establishments (64%, 73/114). Poultry meat (38%, 43/114) was the most commonly reported vehicle of infection, of which poultry liver pâté, and undercooking, were strongly associated with this pathogen. Notably, the number of outbreaks of campylobacteriosis linked to consumption of poultry liver pâté in England and Wales increased significantly from 2007 (74% as opposed to 12%, P<0·00001) with a preponderance of these occurring in December. These outbreaks highlight the hazards associated with inappropriate culinary practices leading to undercooking of poultry liver pâté and suggest that improving catering practice is an important last line of defence in reducing exposure to Campylobacter-contaminated products.

Prevalence, characterisation and antimicrobial resistance of Campylobacter and Salmonella in raw poultrymeat in the UK, 2003–2005

This study was conducted to determine the prevalence and antimicrobial resistance of Campylobacter and Salmonella isolates from retail poultrymeat in the UK during 2003–2005. Poultrymeat (n = 2104) were more frequently contaminated with Campylobacter (57.3%) than with Salmonella (6.6%). Chicken exhibited the highest contamination from Campylobacter (60.9%), followed by duck (50.7%), turkey (33.7%) and other poultrymeat (34.2%). Duck had the highest contamination from Salmonella (29.9%), compared with chicken (5.6%), turkey (5.6%), and other poultrymeat (8.6%). C. jejuni predominated in raw chicken, whereas C. coli predominated in turkey and duck. C. coli isolates were more likely to exhibit antimicrobial drug resistance, including quinolones, than C. jejuni. Salmonella Enteritidis was the most frequent Salmonella serotype isolated. Salmonella isolates from turkey exhibited higher rates of multiple drug resistance (55.6%) than isolates from chicken (20.9%) and duck (13.6%). The findings reinforce the importance of thorough cooking of poultrymeat and good hygiene to avoid cross-contamination.

Attribution of human Listeria monocytogenes infections in England and Wales to ready-to-eat food sources placed on the market: adaptation of the Hald Salmonella source attribution model.

Human listeriosis is a rare but serious foodborne disease, with high morbidity and mortality in vulnerable populations (e.g., pregnant women, the elderly, and the immunocompromised). The disease is predominantly caused by the consumption of contaminated ready-to-eat foods. Since 2001, an increase in the number of listeriosis cases has been observed in several European Union countries, including England and Wales, predominantly in the over-60s population. The cause of this selective increased incidence is unknown. The Hald Salmonella Bayesian source attribution model was adapted to determine the potential of this approach to quantify the contribution of different food sources to the burden of human listeriosis in England and Wales from 2004 to 2007. The most important food sources for the overall population were multicomponent foods (sandwiches and prepacked mixed salad vegetables) (23.1%), finfish (16.8%), and beef (15.3%). Attribution of major sources of infection was similar for the elderly population (>or=60 years old, multicomponent foods [22.0%], finfish [14.7%], and beef [13.6%]). For pregnancy-associated cases, beef (12.3%), milk and milk products (11.8%), and finfish (11.2%) were more important sources of infection. The adapted model also showed that the serotype 4b was associated with relatively more human infections than that of other serotypes; further, the subtype 4b amplified fragment-length polymorphism V was associated with more pregnancy-associated cases than other subtypes of 4b. This approach of quantifying the contribution of various food sources to human listeriosis provides a useful tool in food safety risk analysis, and underlines the need for further emphasis to be given to the reduction of Listeria monocytogenes in high-risk foods, such as multicomponent foods, which are consumed without any further treatment. The need for targeted dietary advice for the elderly population is also highlighted.

Widespread acquisition of antimicrobial resistance among Campylobacter isolates from UK retail poultry and evidence for clonal expansion of resistant lineages

BackgroundAntimicrobial resistance is increasing among clinical Campylobacter cases and is common among isolates from other sources, specifically retail poultry - a major source of human infection. In this study the antimicrobial susceptibility of isolates from a UK-wide survey of Campylobacter in retail poultry in 2001 and 2004–5 was investigated. The occurrence of phenotypes resistant to tetracycline, quinolones (ciprofloxacin and naladixic acid), erythromycin, chloramphenicol and aminoglycosides was quantified. This was compared with a phylogeny for these isolates based upon Multi Locus Sequence Typing (MLST) to investigate the pattern of antimicrobial resistance acquisition.ResultsAntimicrobial resistance was present in all lineage clusters, but statistical testing showed a non-random distribution. Erythromycin resistance was associated with Campylobacter coli. For all antimicrobials tested, resistant isolates were distributed among relatively distant lineages indicative of widespread acquisition. There was also evidence of clustering of resistance phenotypes within lineages; indicative of local expansion of resistant strains.ConclusionsThese results are consistent with the widespread acquisition of antimicrobial resistance among chicken associated Campylobacter isolates, either through mutation or horizontal gene transfer, and the expansion of these lineages as a proportion of the population. As Campylobacter are not known to multiply outside of the host and long-term carriage in humans is extremely infrequent in industrialized countries, the most likely location for the proliferation of resistant lineages is in farmed chickens.

Assessment of the microbiological safety of edible dried seeds from retail premises in the United Kingdom with a focus on Salmonella spp.

Sesame seed products have recently been associated with a number of Salmonella outbreaks in the UK and elsewhere. Aside from sesame seeds, there is little published information on the prevalence of Salmonella spp. in edible seeds. A study of 3735 samples of retail edible dried seeds in the UK was therefore carried out between October 2007 and March 2008 to assess their microbiological safety in relation to Salmonella contamination and levels of Escherichia coli, an indicator of faecal contamination. Overall, Salmonella was detected in 23 samples (0.6%), of which over half (57%) were sesame seeds. Other seeds contaminated with Salmonella were linseed (1 sample), sunflower (1 sample), alfalfa (1 sample), melon (4 samples) and mixed seeds (3 samples). E. coli was detected in 9% of samples, with 1.5% containing unsatisfactory levels (> or = 10(2)/g). These included melon, pumpkin, sesame, hemp, poppy, linseed, sunflower and mixed seeds. The UK retailers affected by the detection of Salmonella in their products recalled the contaminated batches, and Food Standards Agency food alerts were issued to advise against the consumption of affected seed products. This study highlights the importance of good hygiene practices and effective decontamination procedures during the production of these products.

Listeria monocytogenes infection in the over-60s in England between 2005 and 2008: a retrospective case-control study utilizing market research panel data.

A retrospective case-control study of listeriosis in patients in England aged over 60 years is described. The incidence of listeriosis in patients aged ≥60 years in England has doubled since 2001; hence, the investigation of risk factors for infection in this group is important to inform on prevention and control. Standardized epidemiological information has been sought on cases since 2005, but the value of the data accrued is limited without some perception of exposure prevalence in the population at risk of listeriosis. The exposures of listeriosis cases aged ≥60 years reported in England from 2005 to 2008 were compared to those of market research panel members representing the same population (i.e., residents of England aged ≥60 years) and time period. Exposures were grouped to facilitate comparison. Odds ratios and 95% confidence intervals were calculated. Cases were more likely than panel members to report the consumption of cooked meats (beef and ham/pork, but not poultry), cooked fish (specifically smoked salmon) and shellfish (prawns), dairy products (most noticeably milk but also certain cheeses), and mixed salads. They were less likely to report the consumption of other forms of seafood, dairy spread, other forms of dairy, sandwiches, and fresh vegetables. The diversity of high-risk food exposures reflects the ubiquity of the microorganism in the environment and/or the susceptibility of those at risk, and suggests that a wider variety of foods can give rise to listeriosis. Food safety advice on avoiding listeriosis should be adapted accordingly. While not inexpensive, the application of market research data to infectious disease epidemiology can add value to routine surveillance data.

Salmonella enterica serovar Agona European outbreak associated with a food company.

We investigated an international outbreak of Salmonella Agona with a distinct PFGE pattern associated with an Irish Food company (company X) producing pre-cooked meat products sold in various food outlet chains in Europe. The outbreak was first detected in Ireland. We undertook national and international case-finding, food traceback and microbiological investigation of human, food and environmental samples. We undertook a matched case-control study on Irish cases. In total, 163 cases in seven European countries were laboratory-confirmed. Consumption of food from food outlet chains supplied by company X was significantly associated with being a confirmed case (mOR 18·3, 95% CI 2·2-149·2) in the case-control study. The outbreak strain was isolated from the companys pre-cooked meat products and production premises. Sufficient evidence was gathered to infer the vehicles of infection and sources of the outbreak and to justify the control measures taken, which were plant closure and food recall.