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