Elsevier

Food Research International

Volume 55, January 2014, Pages 311-323
Food Research International

Meta-analysis of the incidence of foodborne pathogens in Portuguese meats and their products

https://doi.org/10.1016/j.foodres.2013.11.024Get rights and content

Highlights

  • The first meta-analysis on incidence of pathogens in Portuguese meats was conducted.

  • Campylobacter (40%) and Salmonella (4.0%) in poultry are within current EU ranges.

  • The high incidence of Salmonella in pork (12.6%) calls for on-farm control measures.

  • Non-compliance of traditional meat products to microbiological criteria is high.

  • S. aureus is the pathogen of greatest concern (22.6%) in traditional meat products.

Abstract

Meat and meat products are the main vehicles of foodborne diseases in humans caused by pathogens such as Salmonella spp., Campylobacter spp., Listeria monocytogenes, Yersinia enterocolitica, verotoxigenic Escherichia coli (VTEC) and Staphylococcus aureus. In order to prioritise research on those microbial hazards, a meta-analysis study was conducted to summarise available information on the presence of such pathogens in meats produced in Portugal. By using a logit-transformed proportion as effect size parameterisation, a number of multilevel random-effect meta-analysis models were fitted to estimate mean occurrence rates of pathogens, and to compare them among meat categories (i.e., bovine meat, broiler meat, pork, minced beef and minced pork), and among meat product categories (i.e., intended to be eaten cooked, to be eaten raw and cured meats). The mean occurrence rate of Campylobacter in Portuguese broiler meat (40%; 95% CI: 22.0–61.4%) was about ten times higher than that of Salmonella (4.0%; 95% CI: 1.4–10.8%); although these levels were comparable to current EU ranges. Nevertheless, in the other meat categories, the meta-analysed incidences of Salmonella were slightly to moderately higher than EU averages. A semi-quantitative risk ranking of pathogens in Portuguese-produced pork pointed Salmonella spp. as critical (with a mean occurrence of 12.6%; 95% CI: 8.0–19.3%), and Y. enterocolitica as high (6.8%; 95% CI: 2.2–19.3%). In the case of the Portuguese meat products, the non-compliance to EU microbiological criteria for L. monocytogenes (8.8%; 95% CI: 6.5–11.8%) and Salmonella spp. (9.7%; 95% CI: 7.0–13.4%) at sample units level, in the categories ‘intended to be eaten cooked’ and ‘to be eaten raw’, were considerably higher than EU levels for ready-to-eat products in comparable categories. S. aureus was the pathogen of greatest concern given its high occurrence (22.6%; 95% CI: 15.4–31.8%) in meat products. These results emphasised the necessity of Portuguese food safety agencies to take monitoring, and training actions for the maintenance of good hygiene practices during the production of the great variety of traditional meat products. This meta-analysis study also highlighted important gaps of knowledge, and may assist food safety authorities in the prioritisation of microbiological hazards, and the implementation of essential food safety assurance systems at primary production.

Introduction

Raw meat provides an ideal growth medium for a wide range of pathogens, and, if there is any malpractice in the handling, post-processing, storage or cooking of the product, illness can be a real possibility. Contamination of meat with foodborne pathogens is a major public health issue. In fact, in 2011, campylobacteriosis was the most commonly reported gastrointestinal bacterial pathogen in humans in the EU, followed by salmonellosis, with 220,209 and 95,548 confirmed cases, respectively While campylobacteriosis has increased significantly over the past four reported years (2008–2011), salmonellosis continues its decreasing trend since 2007 although it is the most reported cause of outbreaks (EFSA, 2013). In particular, the human cases caused by the two most common serovars, Salmonella Enteritidis (44%) and Salmonella Typhimurium (25%), diminished significantly since 2008. In foodstuffs, the highest proportion of Campylobacter positive samples was once again reported for fresh poultry (31.3% of positive samples), while Salmonella serovars were most often detected in fresh broiler (6.7%) and pig meat (0.7%). Furthermore, non-compliance with the EU Salmonella criteria has been most often observed in foods of meat origin, being higher for minced poultry (6.8% based on sample units) and minced meat from other species (1.1%) intended to be eaten cooked and minced meat and meat preparations intended to be eaten raw (1.6%) (EFSA, 2013).

In the case of the verotoxigenic Escherichia coli (VTEC) infections (9485 cases), a 2.6-fold increase was observed in comparison to 2010, while the confirmed EU cases of human listeriosis (1476) was slightly lower than previous years, yet with a high fatality rate of 12% (EFSA, 2013). Contaminated bovine meat (1.4% of contaminated sample units in 2011) continues to be considered the major source of VTEC infections in humans (EFSA, 2012, EFSA, 2013), while non-compliance with the EU Listeria monocytogenes criteria is mostly observed in ready-to-eat (RTE) fishery products (6.7%) and of meat origin (2.4%). In 2011, although following a decreasing five-year trend, yersiniosis was the fourth most frequently reported zoonosis (7017 confirmed cases) in the EU. Pigs are considered to be a major reservoir while pork and poultry products are considered to be the most important source of pathogenic Yersinia enterocolitica infection in humans (Simonová, Vazlerová & Steinhauserová, 2007). In fact, in pig meat samples taken from four European countries, the overall incidence of Y. enterocolitica was 2.4% (EFSA, 2013).

In Portugal, there is considerably less information on zoonoses, and incidence of pathogens in meats. Because of the current compulsory national surveillance, and control programmes of Salmonella in foods, more information is available for this pathogen. According to the last EFSA report (EFSA, 2013), the notification rates of salmonellosis in 2011 (1.6 confirmed cases per 100,000) appeared lower than the EU average (20.7 per 100,000), and, peculiarly, well below other Western European countries such as Spain (32.8 per 100,000), France (13.4 per 100,000) and Denmark (21.0 per 100,000). However, as Portugal has one of the highest hospitalisation rates (84% as pointed out in the same report), this may indicate that, apart from a likely large number of citizens not seeking medical advice, there is also under-reporting by the surveillance systems which capture primarily the most severe cases. With regard to the foodstuff contaminated with Salmonella spp. in Portugal, pig meat has been identified as the most important likely source of infection, with a mean incidence of 5.0%, in comparison with the EU average of 0.6% (EFSA, 2013). Nevertheless, information with regard to other foodborne diseases is scarce (i.e., no Portuguese surveillance systems in place for campylobacteriosis, listeriosis, yersiniosis and VTEC infections), which leads to an inaccurate evaluation of the relative importance of each foodborne disease. Due to the limited zoonosis information, it is difficult to establish an evolution trend of the incidence of foodborne diseases as well as the occurrence of the main microbial contaminants in Portuguese foods in the last years (Veiga et al., 2012). Nonetheless, given (i) the strong association of foodborne diseases in humans with the consumption of contaminated meat and meat products, and (ii) the high consumption of meats (93 kg per Portuguese habitant in 2012 above the average 80 kg per EU citizen) and meat products (672 tonnes production in 2009 in Portugal), it is imperative to gather as much information as possible on the levels of foodborne pathogens in Portuguese meats and meat products in order to understand the current epidemiological situation, prioritise microbial hazards for risk analysis, and identify knowledge gaps to provide direction for further research.

Meta-analysis is a body of summarising statistical techniques whose objective is to synthesise, integrate and contrast the results from a large amount of primary studies investigating the same research question (Gonzales-Barron, Cadavez, Sheridan, & Butler, 2013). The primary objective of meta-analysis is to produce a more precise estimate of the effect size of a particular treatment, with increased statistical power, than is possible using only a single study (Sutton, Abrams, & Jones, 2001). Yet, with meta-analysis, it is also possible to explain differences in the study outcomes by coding study characteristics, such as: research design features, data collection procedures, type of samples or even year (Hox & De Leeuw, 2003). In the past few years, meta-analysis has increasingly been applied in food safety (Den Besten and Zwietering, 2012, Gonzales Barron et al., 2008, Gonzales-Barron and Butler, 2011, Gonzales-Barron et al., 2013, Grieg et al., 2012, McQuestin et al., 2009, Sánchez et al., 2007). In food safety research, meta-analysis may be conducted to address a broad range of research questions such as disease incidence, prevalence of microorganisms in foods, effect of interventions pre- and post-harvest, risk ranking of pathogens and consumer practices, among others. Thus, the objectives of this research are: (i) to compile all publicly accessible information on the occurrence of Salmonella spp., Campylobacter, L. monocytogenes, VTEC, Y. enterocolitica and Staphylococcus aureus in Portuguese meats, and meat products grouped by categories; (ii) to quantitatively summarise, and compare the occurrence of pathogens according to available information by conducting separate meta-analysis models for meat and meat products; (iii) to appraise likely publication bias, a common artefact in meta-analysis studies (Viechtbauer, 2010); (iv) to conduct a semi-quantitative risk ranking of pathogens in pork using the characterisation of severity of hazards proposed in EFSA (2011a); and (iv) to identify knowledge gaps on the occurrence of pathogens in certain meat categories.

Section snippets

Methodology

The problem statement in this study was the estimation of the overall incidence or occurrence of foodborne pathogens in Portuguese meats. The population was specified as meat and meat products produced in Portugal while the measured outcome is the detection of pathogens in meats sampled either at processing plants or at retail. Following the systematic review protocol presented by Sargeant, Amezcua, Rajic, and Waddell (2005), electronic searches were carried out to identify official reports

Results and discussion

Although there is a perception that a high incidence of foodborne diseases may have various causes such as inadequate manipulation, preparation and distribution of foods along the food chain, it is also true that quantitative risk assessment leading to efficient prevention demands data availability. Overall, in Portugal, data on microbial contaminants in meats and epidemiology is relatively scarce. For instance, at the level of national compulsory surveillance of infectious diseases,

Conclusion

The systematic review conducted in this research allowed to recognise the sparseness of knowledge on the incidence of pathogens in meats and meat products produced in Portugal. This meta-analysis study provided the first pooled incidence estimates for pathogens in specific meat categories, which are more robust and reliable than single study estimates. For the meta-analyses conducted on Portuguese meats categorised by origin, a greater number of incidence observations from primary studies were

Acknowledgments

Dr. Gonzales-Barron wishes to acknowledge the financial support provided by the Portuguese Foundation for Science and Technology (FCT) through the award of a five-year Investigator Fellowship (IF) in the mode of Development Grants (IF/00570).

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