Zero Salmonella tolerance on poultry: Worthy goal or trade protectionism?

Can an importing country justify on purely scientific grounds a zero-tolerance policy for Salmonella on raw poultry? The term ‚Äúzero tolerance‚ÄĚ for specific pathogens such as Salmonella in raw food products is interpreted differently in different countries and therefore has been confusing, misleading and misapplied. Using terms such as ‚Äúzero tolerance‚ÄĚ or ‚Äúabsence of a bacterium‚ÄĚ in relation to raw poultry should be avoided unless these terms are specifically defined and explained by international agreement.

The poultry industry has a vested interest in mitigating Salmonella contamination.
The poultry industry has a vested interest in mitigating Salmonella contamination.

The global trade of poultry meat is often hampered by non-tariff barriers, which are often thinly disguised mechanisms to limit the import of poultry for the benefit of the domestic industries in the importing countries. Probably one of the most widely used ‚Äď and abused ‚Äď of these non-tariff barriers is a zero tolerance for Salmonella on raw poultry. In some cases, any finding of Salmonella on raw product can lead to the rejection of an entire shipment, or the de-listing of the plant of origin of the suspect product.

This raises the question that has long been asked by countries that export poultry: Can an importing country justify, on purely scientific grounds, a zero-tolerance policy for Salmonella on raw poultry?

Salmonella ‚Äď widely occurring and elusive  

We know that Salmonella occurs commonly in livestock and poultry, and can be frequently isolated from wild animals, including rodents, reptiles and birds. When poultry flocks become infected, most Salmonella are carried within the gut of the birds and subsequently contaminate the environment, including the birds’ feathers, feet and skin. During post-slaughter processing, Salmonella may also be transferred among carcasses by fecal or ingesta contamination, or may be spread by cross-contamination of carcasses in the rinse or chill cycles, or on equipment surfaces.

The industry, regulators and consumers all have a vested interest in interventions to mitigate Salmonella contamination of poultry throughout the food chain, and it is an important goal for all stakeholders to ensure that the final cooked product is safe for consumption.

Although raw poultry meat is a frequent vehicle of foodborne Salmonella infections in humans, it is difficult to quantify the true proportion of all salmonellosis cases that are associated with poultry consumption.

Food source attribution under scrutiny  

Because of the trade ambiguities and regulatory confusion resulting from different Salmonella sampling and testing methodologies, an international group of 26 scientific experts from 16 countries convened in 2009 to discuss the scientific and technical issues that affect the setting of a microbiological criterion for Salmonella contamination of raw poultry.

The result of these deliberations was the peer-reviewed publication of ‚ÄúScientific and Technical Factors Affecting the Setting of Salmonella Criteria for Raw Poultry: A Global Perspective,‚ÄĚ published in the Journal of Food Protection, 73(8):1566-1590, 2010.

Although Salmonella on raw poultry products is an important cause of human salmonellosis, it is difficult to determine the extent to which it is responsible for foodborne human illness, whether directly or indirectly via cross-contamination. It is precisely this type of information, however, that is needed to understand the true risk to public health and to determine the effectiveness of intervention strategies. Ultimately, the efficacy of regulatory activities should be assessed on the basis of risk outcomes.

Zero tolerance often misunderstood  

The use of HACCP in primary processing of poultry is widely advocated and is mandatory in the United States and the European Union. In the U.S., the processing operation is the main focus for regulatory oversight and industry management of Salmonella, whereas in the EU processing is only one stage in the supply chain at which monitoring measures are required.

Both approaches include a microbiological criterion for Salmonella, and both require regular testing of post-chill carcasses as part of the verification of the food safety management system. The U.S. system also includes a zero-tolerance policy for visible fecal contamination on carcasses before they enter the chiller, as well as the requirement in the HACCP plan of a critical control point to help ensure fecal contamination is avoided. Otherwise, individual companies determine critical control points and they may differ among establishments.

Quantitative risk assessment needed  

Applying quantitative risk-assessment practices in microbiological food safety exposes the reality that zero risk is unattainable for all raw foods. Zero tolerance, which implies the complete absence of a hazard, may be regarded as the expression of a regulatory preference for the precautionary principle, but has little to do with food safety and human health. The term ‚Äúzero tolerance‚ÄĚ itself is commonly used but generally poorly defined or understood. This is troublesome because it has different meanings for different audiences.

To some people, zero tolerance implies zero risk associated with the food, or zero prevalence of a pathogen in the food. But without any way of consistently eliminating the pathogen from a raw product, the ‚Äúzero‚ÄĚ concept is misleading to consumers with unrealistic expectations of the effectiveness of regulation, who may interpret such regulations as implying no risk. If a hazard exists, there is some probability it will cause an adverse effect, no matter how small.

Zero tolerance also implies that both minor and major deviations from a policy will be treated with the same severity. This is obviously not a sensible approach to identifying and resolving the source of contamination problems.

Dealing with deviations  

Internationally, there is no consistency in interpreting the concept and how to deal with deviations. The purpose of a Salmonella monitoring policy for raw poultry should be to provide an alert that prompts a review of policies and procedures. It should also permit the finished product with minor deviation to be distributed into the marketplace, and should take into account cost and other practical considerations of withholding the product from sale.

Several other challenges exist to applying a zero-tolerance policy for Salmonella on raw poultry meat: defining the accuracy, sampling intensity, sampling material, and sensitivity of the testing method. At which point is the assessment to be made, pre-harvest or post-harvest? Who bears the repercussions for enforcement? And, who has and what is the enforcement capacity? How does one quantify cross-contamination of other foods or account for other transmission routes, such as person-to-person? The evidence suggests that currently there are no intervention treatments that can be applied in all countries to ensure the complete elimination of Salmonella from raw poultry products.

Measuring levels instead of prevalence  

Salmonella contamination is usually expressed in terms of prevalence, but evidence from microbiological risk assessment indicates that the levels (number of cells) of contamination can be even more important to public health, and efforts at any stage of production or processing that reduce the Salmonella cell numbers on the raw product will reduce risk.

With the development of more sensitive methods for counting Salmonella and methods that are internationally acceptable, we should pay much greater attention to this aspect in the future, enabling more heavily contaminated items to be identified and suitable interventions developed.

How far to take management programs?  

Over the years, Sweden has developed and implemented a stringent and successful Salmonella management program for poultry. The present degree of Salmonella prevalence on raw poultry took several decades to achieve at considerable expense. For all countries, however, such measures are unlikely to be economically or technically feasible. Some lessons can be learned from the Swedes, especially about the need for Salmonella-free breeding stock and feed, as well as improved biosecurity.

Salmonella infection of broiler flocks and the contamination of processed carcasses differ widely among countries, largely reflecting the stringency of measures undertaken to eliminate Salmonella in poultry production and processing. Conditions in production and processing also differ widely, as do the strategies and methods used for sampling and testing for Salmonella. These sampling methods must be standardized, especially for raw product testing, in the interests of consumer safety and trade.

Four recommendations  

  • Given the nature of the poultry industry, current interventions won‚Äôt guarantee the absence of Salmonella from raw poultry products. Approaches differ among countries in the emphasis placed on pre-harvest and post-harvest regulatory monitoring. However, the most effective strategy for Salmonella management would be one that covers all stages of the food chain. Therefore, this strategy should be followed wherever possible.
  • To establish international standards and achieve global compliance, governments and industries must be willing to work toward developing and adopting harmonized approaches for data collection and analysis.
  • The term ‚Äúzero tolerance‚ÄĚ for specific pathogens such as Salmonella in raw food products is interpreted differently in different countries and therefore has been confusing, misleading and misapplied. Using terms such as ‚Äúzero tolerance‚ÄĚ or ‚Äúabsence of a bacterium‚ÄĚ in relation to raw poultry should be avoided unless these terms are specifically defined and explained by international agreement.
  • New metrics, such as ‚Äúperformance objectives‚ÄĚ that are linked to human health outcomes based on risk assessment, should be used throughout the food chain and will better define the resultant public health risk.


The following groups and organizations contributed to the authors‚Äô project: International Expert Committee of Salmonella on Raw Poultry; United Soybean Board; Illinois Soybean Program Operating Board; International Poultry Council; UBABEF ‚Äď Associa√ß√£o Brasileira dos Produtores e Exportadores de Frangos (Brazilian Chicken Producers and Exporters Association); Asociaci√≥n de Productores Av√≠colas (Chilean Poultry Producers Association); Federaci√≥n de Av√≠cultores de Honduras (Federation of Honduran Poultry Producers); U.S. Department of Agriculture/Foreign Agricultural Service; USA Poultry & Egg Export Council; and U.S. Poultry & Egg Association.


N. A. Cox1, M. P. Doyle2, A. M. Lammerding3, L. J. Richardson4, R. J. Buhr1, Y. V. Thaxton5, and J. A. Cason1
1 USDA, ARS, Russell Research Center, Athens, Ga.
2 Center for Food Safety, University of Georgia, Griffin, Ga.
3 Public Health Agency of Canada, Guelph
4 Coca Cola Company, Atlanta, Ga.
5 Center for Food Animal Well Being, University of Arkansas, Fayetteville, Ark.

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