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Scientific Opinion on an estimation of the public health impact of setting a new target for the reduction of Salmonella in turkeys

EFSA Journal 2012;10(4):2616 [89 pp.]. doi:10.2903/j.efsa.2012.2616
  EFSA Panel on Biological Hazards (BIOHAZ) Panel Members Olivier Andreoletti, Herbert Budka, Sava Buncic, John D Collins, John Griffin, Arie Havelaar, James Hope, Günter Klein, Kostas Koutsoumanis, James McLauchlin, Christine Müller-Graf, Christophe Nguyen-The, Birgit Noerrung, Luisa Peixe, Miguel Prieto Maradona, Antonia Ricci, John Sofos, John Threlfall, Ivar Vågsholm, Emmanuel Vanopdenbosch. Acknowledgment The Panel wishes to thank the members of the Working Group on an estimation of the public health impact of new target for the reduction of Salmonella in turkeys: Birgitte Borck Høg, Marianne Chemaly, Robert Davies, Hafez M. Hafez, Arie Havelaar, Antonia Ricci and John Sofos for the preparatory work on this scientific opinion and the hearing expert: Tine Hald, and EFSA staff: Winy Messens (BIOHAZ) and Giusi Amore (BIOMO) for the support provided to this scientific opinion. Possible conflict of interest One member of the Panel did not participate in the discussion on the subject referred to above because of potential conflicts of interest identified in accordance with the EFSA policy on declarations of interests. Contact biohaz@efsa.europa.eu
Type: Opinion of the Scientific Committee/Scientific Panel On request from: European Commission Question number: EFSA-Q-2010-00899 Adopted: 08 March 2012 Published: 13 April 2012 Affiliation: European Food Safety Authority (EFSA), Parma, Italy
Abstract

The quantitative contribution of turkeys and other major animal-food sources to the burden of human salmonellosis in the European Union was estimated. A ‘Turkey Target Salmonella Attribution Model’ (TT-SAM) based on the microbial-subtyping approach was used. TT-SAM includes data from 25 EU Member States, four animal-food sources of Salmonella and 23 Salmonella serovars. The model employs 2010 EU statutory monitoring data on Salmonella in animal populations (EU baseline survey data for pigs), data on reported cases of human salmonellosis and food availability data. It estimates that 2.6 %, 10.6 %, 17.0 % and 56.8 % of the human salmonellosis cases are attributable to turkeys, broilers, laying hens (eggs) and pigs, respectively. The top-6 serovars of fattening turkeys that contribute most to human cases are S. Enteritidis, S. Kentucky, S. Typhimurium, S. Newport, S. Virchow and S. Saintpaul. Comparing the prevalence of Salmonella in turkey flocks reported in 2010 with a theoretical combined prevalence for S. Enteritidis and S. Typhimurium of 1 % (i.e. the transitional target), a reduction of 0.4 % in the percentage of turkey-associated human salmonellosis cases would be achieved. However, when adjusting the combined prevalence of all serovars to 1 %, an 83.2 % reduction in the percentage of turkey-associated human salmonellosis cases, equivalent to 2.2 % of all human salmonellosis cases, is expected. Uncertainty and data limitations are discussed, including recommendations on how these could be overcome. Vertical transmission of Salmonella as well as hatchery acquired Salmonella contamination originating from breeding stock are very important sources for Salmonella infection in turkeys, and therefore controlling Salmonella in breeding flocks as well as in rearing and fattening flocks is necessary to minimise Salmonella in turkeys at slaughter.

© European Food Safety Authority, 2012

Summary

Following a request from the European Commission, the Scientific Panel on Biological Hazards (BIOHAZ) was asked to deliver a Scientific Opinion on an estimate of the public health impact of setting a new target for the reduction of Salmonella in turkeys. Specifically, EFSA was asked to indicate and rank the Salmonella serovars with public health significance, to assess the impact of a reduction of the prevalence of Salmonella in breeding flocks of turkeys on the prevalence of Salmonella in flocks of fattening turkeys and to assess the relative public health impact if a new target for reduction of Salmonella is set in turkeys being 1 % or less of flocks remaining positive for all Salmonella serovars with public health significance, compared to (1) the theoretical prevalence at the end of the transitional period (1 % or less flocks remaining positive for Salmonella Enteritidis and/or Salmonella Typhimurium), and (2) the real prevalence in 2010 reported by the Member States (MSs).

In order to assess the impact of a reduction of Salmonella prevalence in breeding flocks of turkeys on the prevalence in flocks of fattening turkeys, information available in the literature and monitoring results about the presence of Salmonella serovars in turkey flocks at different level, were taken into account. From these data, it is clear that in some cases there is a coincidence between the serovars isolated in breeding flocks and the ones isolated in fattening flocks, but some of the serovars isolated in fattening flocks are not detected in breeding flocks, thus suggesting the relevance of other sources of infection, such as contaminated feed or turkey houses and breaches in biosecurity, not related to the concurrent presence of Salmonella in the parent stocks. The Panel therefore concluded that vertical transmission and hatchery acquired infection appear as most important sources for Salmonella infection in fattening turkeys. Controlling the infection in breeders is necessary, but not sufficient to control Salmonella in fattening flocks.

For the second task (to assess the relative public health impact of a new target for reduction of Salmonella in turkey flocks), the Panel was supported by the work of a contractor that developed a source attribution model providing estimates for the quantitative contribution of turkeys and other major animal-food sources to the estimated true burden of human salmonellosis in the EU. The model was based on the so-called microbial-subtyping approach, where the serovar distributions observed in different animal-food sources is compared with the serovar distribution found in humans. The Technical Report submitted to EFSA by the contractor provides detailed information on the modelling approach and results.

The model considered the following data: (i) the results from the harmonised EU monitoring in turkeys, broiler and laying hen flocks in 2010, (ii) the EU-wide Salmonella baseline survey on slaughter pigs, (iii) the reported cases of human salmonellosis in EU in 2010 by MSs as provided by the European Centre for Disease Prevention and Control (ECDC), and (iv) the amount of each food source available for consumption by MS as estimated from EUROSTAT data on production, import and export. The model included data from 25 MSs, four animal-food Salmonella sources (turkeys, broilers, laying hens and pigs) and 23 individual serovars. To take account for differences in underreporting of human salmonellosis cases between MSs, MS-specific underreporting factors were calculated and applied in the model. Some sources of Salmonella (e.g. cattle/beef) were not included in the model due to lack of data. The possible influence of this is discussed.

Initially, a model applying prevalence data from the harmonised EU monitoring conducted in turkey flocks in 2010 was developed. This model is referred to as the ‘Turkey Target Salmonella Attribution Model’ or TT-SAM model throughout the Opinion. In order to answer the Terms of Reference, seven different scenarios where Salmonella prevalences in turkey flocks were changed were developed and the results compared to the results of the TT-SAM model.

The Panel concluded that, based on the results of the TT-SAM model, in 2010, there were approximately 5.4 (95 % CI: 3.0-9.5) million true cases of human salmonellosis (i.e. estimated true number of cases when accounting for underreporting) in the EU, a 13 % decrease compared to 2009. 2.6 % (95 % CI: 1.2-5.2) of these human salmonellosis cases were attributed to turkeys. The top-6 serovars of fattening turkeys that contribute most to human cases are S. Enteritidis, S. Kentucky, S. Typhimurium, S. Newport, S. Virchow and S. Saintpaul.

For the other Salmonella sources considered, the model estimated that around 17.0 % (95 % CI: 11.3-24.0), 56.8 % (95 % CI: 48.2-65.8) and 10.6 % (95 % CI: 5.1-18.3) of the estimated number of human salmonellosis cases could be attributed to reservoirs relating to laying hens (eggs), pigs and broilers, respectively. However, when considering the risk between turkey meat and the other three sources weighted by the tonne of food available for consumption, the risk of infection is highest when consuming table eggs closely followed by the consumption of pig meat, whereas the risks associated with broiler and turkey meat were similar and approximately two-fold lower.

The Panel concluded that (1) considering that the current transitional target of the EU control programme of Salmonella in fattening turkey flocks would be met (i.e. the combined prevalence of S. Enteritidis and S. Typhimurium being 1 % or less), and keeping the prevalence for the other 21 serovars as per the 2010 harmonised monitoring in turkey flocks, an estimated reduction in the number of turkey-associated human salmonellosis cases of 0.4 % compared to the situation in 2010 is expected (in 2010 all MSs except one had already met the transitional target); (2) considering that an EU-wide target of maximum of 1 % of flocks remaining positive for the all the Salmonella serovars considered in the model would be met, an estimated reduction in the number of turkey-associated human salmonellosis cases of 83.2 % compared to the situation in 2010 is expected, corresponding to a 2.2 % reduction of all human salmonellosis cases. The Panel emphasised that the individual MS contributions to the estimated reductions vary greatly. 

The Panel finally concluded that the main factors contributing to the uncertainty of the model results, apart from statistical uncertainties, are the lack of harmonised monitoring of human salmonellosis in the EU as well as the different levels of serovar detail reported in both the human and animal food source data. These uncertainties could not be statistically quantified with the model employed to support this Scientific Opinion.

The Panel makes a series of recommendations related to the establishment of active surveillance of human salmonellosis in all MSs including harmonised typing of human Salmonella isolates and efforts to quantify the level of under-ascertainment and underreporting. It is recommended to investigate the effectiveness of different sampling options at primary production, in order to ensure comparability of results, and to implement reliable tests, epidemiological studies and accurate reporting in order to identify emerging strains and antimicrobial use, and to apply targeted control measures. Comparable data on Salmonella in cattle would be necessary to obtain better estimates on the public health impact of different animal reservoirs.

Keywords

Salmonella, poultry, turkeys, source attribution, microbial subtyping, targets