Opportunities to Improve Food Safety From Farm to Fork

What interventions effectively reduce risk of meat and poultry contamination?

Issue Brief
Projects: Safe Food
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Opportunities to Improve Food Safety From Farm to Fork
The Pew Charitable Trusts

Overview

Contaminated meat and poultry products are responsible for an estimated 2 million bacterial illnesses in the United States each year.1 One analysis conducted jointly by the Centers for Disease Control and Prevention, Food and Drug Administration, and Department of Agriculture indicates that up to 38 percent of E. coli O157:H7 infections are attributable to beef, 35 percent of Campylobacter cases are linked to chicken and turkey, and 36 percent of Salmonella illnesses are associated with chicken, turkey, beef, and pork.2 Reducing meat and poultry contamination presents a significant opportunity to prevent serious—and sometimes fatal—disease caused by these major foodborne pathogens.

A comprehensive approach to meat and poultry safety must begin at the farm level, because harmful bacteria often originate there and then enter the slaughterhouse with food animals. Although certain interventions and handling practices during and after slaughter can reduce contamination risks, these measures are much more effective when farms and feedlots minimize contamination in their herds and flocks.

In a 2017 report, “Food Safety From Farm to Fork: Interventions on Farms and Feedlots Can Improve U.S. Meat and Poultry Safety,” The Pew Charitable Trusts examined existing food safety control measures aimed at reducing Salmonella, Campylobacter, and E. coli O157:H7 contamination of cattle, chicken, and swine before slaughter. This issue brief outlines the interventions that were found to be effective on farms, many of which can be implemented with products already available to U.S. livestock businesses. It’s time to seize these opportunities to decrease foodborne illnesses linked to meat and poultry.

Good animal husbandry is a prerequisite for on-farm food safety

Implementation of exposure-reduction strategies such as storing animal feed under hygienic conditions and controlling vermin provides a vital foundation for all food safety efforts on farms. Such practices, often called biosecurity measures, are also important for livestock businesses because they help prevent the spread of foreign animal illnesses such as avian influenza, African swine fever, and foot-and-mouth disease. The effectiveness of such programs in controlling food safety hazards has been well-demonstrated in other countries. However, scientific research quantifying the efficacy of individual exposure-reduction interventions is limited. For these reasons, this issue brief assumes that these programs are a prerequisite for livestock production and focuses on approaches and products that have been shown to be effective against specific foodborne pathogens on farms.

Countries Find Success With Farm-Focused Strategies

Several countries have achieved major improvements in the safety of meat and poultry products from prevention-based systems that combine exposure-reduction strategies with other types of interventions. Sweden, Finland, Norway, and Denmark have implemented successful food safety control programs to reduce Salmonella contamination on poultry and swine.3 These countries require strict, on-farm biosecurity measures including cleaning and disinfecting animal housing, extensive testing and monitoring for Salmonella in the animals and feed, culling of infected breeding animals, and separate handling of Salmonella-positive flocks or herds at slaughter. The results have been impressive. No Salmonella was detected in a sample of 4,033 Swedish poultry carcasses in 2017; less than 1 percent of Norwegian and Finnish poultry flocks were contaminated with the pathogen in 2016; and up to 600,000 human infections from the bacterium were avoided in Denmark from 1994 to 2005.4 By contrast, among USDA-regulated raw poultry products, Salmonella contaminates about 5 percent of whole chicken carcasses, 15 percent of chicken parts such as legs, breasts and wings, and 40 percent of ground chicken.5 Data from European pathogen surveillance programs also demonstrate that effective biosecurity measures for swine operations are associated with a lower probability of the herds testing positive for Salmonella.6

How the interventions were selected

The availability and type of research on pre-harvest interventions vary broadly. Certain species, products, and practices have been studied more often than others. For instance, with cattle, more research is available for interventions targeting E. coli than Salmonella. No single pre-harvest intervention completely eliminates contamination risks; however, reductions in contamination can have substantial public health benefits even if residual bacteria remain.7 Successful pre-harvest programs are typically based on a combination of interventions. For example, exposure-reduction strategies and pathogen surveillance are used in conjunction with vaccines and probiotics.

With these factors in mind, Pew selected the interventions discussed in this brief for two reasons. First, the intervention is available to livestock producers in the U.S. and can be used in an animal agriculture setting. Secondly, strong scientific evidence (based on experimental studies, field trials, or systematic reviews) demonstrates that use of these interventions results in consistent reductions in the target pathogen.

What works

Probiotics

Probiotics are composed of live beneficial microorganisms that can colonize an animal’s lower intestinal tract and thereby prevent growth of pathogenic bacteria such as E. coli and Salmonella. Certain probiotics may be referred to by other terms, such as direct-fed microbials (DFMs) or competitive exclusion products. DFMs are probiotics that are added to feed and enhance an animal’s gut health, provide nutrients, and prevent or reduce the growth of pathogens. Competitive exclusion products may be delivered through feed or sprayed on animals. These are typically given at birth or hatching to help prevent pathogens from colonizing the gastrointestinal tract.8 Despite their wide use, the current regulatory system can make it difficult for certain probiotics to obtain approval.

Effects on E. coli O157:H7 in cattle

A 2011 Animal and Plant Health Inspection Service feedlot survey found that 28.5 percent of large feedlots (more than 1,000 cattle) in the U.S. use probiotics.9 DFMs have been shown to significantly reduce fecal shedding of E. coli in cattle.10 A meta-analysis that assessed the efficacy of DFMs fed to cattle found that the odds of fecal E. coli O157:H7 shedding were reduced by approximately 54 percent compared with placebo or no treatment.11

Probiotics are used commercially by the cattle industry to increase growth rate and milk production.12 These benefits can help offset the costs of adding probiotics to animal feed, improving the economic feasibility of this practice as a food safety intervention.13 However, microbes in probiotics can transmit genes that confer resistance to a variety of antibiotics, so the absence of antibiotic resistance genes in the formulations must be ensured.14

Effects on Salmonella in chicken

Probiotics can be administered to poultry to reduce the prevalence of Salmonella. Defined probiotics may consist of Lactobacillus species, heat-stable Bacillus species that can be given in heat-treated pelleted feed, or other microorganisms. A systematic review of commercial products found that defined direct-fed probiotics products are effective at reducing Salmonella. As in cattle, the economic benefits of the use of probiotics in poultry may offset the cost, thus making probiotics a practical pre-harvest intervention in broiler chickens.

Vaccines

Vaccines are widely used to prevent viral and bacterial infections in animals and are an effective approach for pre-harvest food safety.17 Vaccination prevents infection by stimulating the animal’s immune system using an agent that resembles the disease-causing pathogen.

Effects on E. coli O157:H7 in cattle

Commercial E. coli O157:H7 vaccines have been demonstrated to significantly reduce fecal shedding in cattle.18 One commercially available cattle vaccine was found to reduce the concentration of E. coli O157:H7 in fecal samples by 98 percent in large field trials with more than 2,500 cattle.19 Additionally, a mathematical model estimated that giving all cattle a vaccine that reduces fecal shedding by 50 percent could prevent up to 83 percent of human foodborne infections.20

Although studies demonstrate the efficacy of vaccination as a pre-harvest intervention, there are economic barriers to their use. The 2011 feedlot survey indicated that only 2.4 percent of U.S. feedlots with more than 1,000 head of cattle administered an E. coli O157:H7 vaccine.21 One study estimated a vaccination cost of $8 to $15 per animal.22 Vaccination may also negatively affect how quickly the cattle grow; however, this was a novel finding of one feedlot study, and further research is warranted.23 Additionally, the operations bearing the cost of vaccines are not able to realize any benefits from vaccination that occur further down the supply chain.24

Effects on Salmonella in chicken

Studies have demonstrated the efficacy of vaccinating broiler-breeders (the parents of chickens destined for slaughter) to reduce Salmonella prevalence and concentration in their progeny.25 One study found that poultry companies in the United States with vaccination programs for breeders saw a significant reduction in the prevalence of Salmonella on birds entering the slaughterhouse.26 Other researchers found that the amount of Salmonella sampled from the housing environment and after slaughter was 50 percent lower for broiler chickens from vaccinated breeders.27 Vaccinating breeders may be more economical than targeting the intervention at their offspring, because an average breeder will lay up to 180 broiler eggs per year.28

Like cattle vaccines, poultry vaccination can yield substantial public health benefits. The World Health Organization found that reducing the prevalence of Salmonella-contaminated chicken by half would reduce the risk of illness from eating a serving of chicken by as much as 50 percent.29 A significant decline in human Salmonella enteritidis infections in the United Kingdom and other European countries has been attributed to vaccination of egg-laying hens.30

A limitation of Salmonella vaccines is a lack of coverage for multiple strains. Autogenous vaccines that are made from killed pathogens and are tailored to the disease risks on a given operation target specific pathogens but provide no or very limited cross-protection for other strains. Live vaccines offer more cross-protection but are available for only a few Salmonella serotypes.31

Other promising approaches on the horizon

Some pre-harvest practices are effective but are not used in the U.S. or need further research trials in farms and feedlots. For example, sodium chlorate has been found to reduce Salmonella in chickens, E. coli in cattle, and Salmonella and E. coli in swine when administered through water and feed.32 However, more studies are needed on commercial farms, and sodium chlorate has not been approved for use in the United States.

Similarly, the amount of scientific evidence supporting Salmonella vaccines for swine is relatively small compared with that available for the intervention in other food animals. The literature nonetheless indicates that vaccination of pigs can improve the safety of pork products. Vaccines that target the types of Salmonella that cause disease in swine and are a food safety risk to humans are commercially available.33 However, more well-designed controlled trials are needed.

Campylobacter has proved more challenging to control with discrete pre-harvest interventions and might be reduced only through on-farm biosecurity measures.34 Sweden has had success with Campylobacter reduction in poultry flocks using hygiene measures on the farm. Campylobacter-positive flocks decreased from 50 percent to 10 percent from 1991 to 2006 as a result of strategies that included rodent and bird barriers as well as employee protocols that kept contamination from entering facilities on shoes and clothes.35 Although studies have established some relationship between Campylobacter infection and the bacterium’s presence in ponds, puddles, and other water sources on farms, more research is needed to fully understand these and other potential sources of contamination and routes of transmission to animals.36

Conclusion

Strong scientific evidence supports the effectiveness of probiotics and vaccines in reducing foodborne pathogens, and commercial products are already available. Use of these interventions can make a significant public health impact if adopted across all farms or feedlots.

Pre-harvest measures are the first step to effectively controlling food safety hazards and improving public health, and they should begin as far up the supply chain as possible—ideally with breeding flocks or herds from which the food-producing animals are derived. Salmonella infections in broiler-breeder chicken flocks and breeder pig herds can be transmitted to chicks and piglets, underscoring the need for efficient control measures earlier in the production chain.37 Ultimately, successful pre-harvest programs target specific food animal species and their production systems; combine multiple interventions such as probiotics and vaccines; and include biosecurity and farm management practices, feed and water safety, and pathogen surveillance. These are fundamental parts of a comprehensive farm-to-fork approach that can significantly reduce the public health risk associated with meat and poultry consumption.

Endnotes

  1. John A. Painter et al., “Attribution of Foodborne Illnesses, Hospitalizations, and Deaths to Food Commodities by Using Outbreak Data, United States, 1998-2008,” Emerging Infectious Diseases 19, no. 3 (2013), http://wwwnc.cdc.gov/eid/article/19/3/11-1866-t4.
  2. Interagency Food Safety Analytics Collaboration, “Foodborne Illness Source Attribution Estimates for 2013 for Salmonella, Escherichia coli O157, Listeria monocytogenes, and CampylobacterUsing Multi-Year Outbreak Surveillance Data, United States,” https://www.cdc.gov/foodsafety/pdfs/IFSAC-2013FoodborneillnessSourceEstimates-508.pdf.
  3. Johan Lindblad, “Lessons From Sweden’s Control of Salmonella and Campylobacter in Broilers,” Agricultural Outlook Forum (2007), https://econpapers.repec.org/scripts/redir.pf?u=http%3A%2F%2Fageconsearch.umn.edu%2Frecord%2F8109%2Ffiles%2Ffo07li01.pdf;h=repec:ags:usaose:8109; Berit Tafjord Heier, researcher for veterinary public health, Norwegian Veterinary Institute, email message to The Pew Charitable Trusts, Aug. 22, 2013; Riitta Maijala and Jukka Peltola, “Finnish Salmonella Control Program—Efficiency and Viability in Food Safety Promotion” (presentation prepared for the 10th European Association of Agricultural Economists Congress in Zaragoza, Spain, 2002), http://ageconsearch.umn.edu/bitstream/24793/1/cp02ma17.pdf; Henrik C. Wegener, “Danish Initiatives to Improve the Safety of Meat Products,” Meat Science 84, no. 2 (2010), https://doi.org/10.1016/j.meatsci.2009.06.025.
  4. Tove Christensen and Lill Andersen, “Case Study #3-12: Salmonella Control in Denmark and the EU” (2007), https://ecommons.cornell.edu/handle/1813/55684; Riitta Maijala et al., “A Quantitative Risk Assessment of the Public Health Impact of the Finnish Salmonella Control Program for Broilers,” International Journal of Food Microbiology 102, no. 1 (2005), https://doi.org/10.1016/j.ijfoodmicro.2004.11.012; Lindblad, “Lessons From Sweden’s Control”; Martin Wierup et al., “Control of Salmonella enteritidis in Sweden,” International Journal of Food Microbiology 25, no. 3 (1995), https://doi.org/10.1016/0168-1605(94)00090-S; National Veterinary Institute, Department of Disease Control and Epidemiology, “Surveillance of Infectious Diseases in Animals and Humans in Sweden 2017” (2017), https://www.sva.se/globalassets/redesign2011/pdf/om_sva/publikationer/surveillance-2017-w.pdf; Finnish Food Safety Authority Evira, “Animal Diseases in Finland 2016” (2017), http://aineisto.ruokavirasto.fi/evira20181231/www/globalassets/tietoa-evirasta/julkaisut/julkaisusarjat/elaimet/evira_publications_4_2017.pdf; Berit Tafjord Heier et al., “The Surveillance Programmes for Salmonella in Live Animals, Eggs and Meat in Norway 2016,” Norwegian Veterinary Institute (2017), https://www.vetinst.no/overvaking/salmonella/_/attachment/download/7612d270-0214-4381-ae7a-9af336f54f04:7e3b44f0852a4c33bb10546cefbacbd0227f1b4e/2017_OK_Salmonella_Report%202016.pdf.
  5. U.S. Department of Agriculture, Food Safety Inspection Service, “Sampling Results for FSIS Regulated Products: Calculations” (2018), https://www.fsis.usda.gov/wps/wcm/connect/68f5f6f2-9863-41a5-a5c4-25cc6470c09f/Sampling-Project-Results-Data.pdf?MOD=AJPERES.
  6. Filipa M. Baptista et al., “Use of Herd Information for Predicting Salmonella Status in Pig Herds,” Zoonoses and Public Health 57, supplement 1 (2010), https://www.ncbi.nlm.nih.gov/pubmed/21083818.
  7. Ben A. Smith et al., “A Risk Assessment Model for Escherichia coli O157:H7 in Ground Beef and Beef Cuts in Canada: Evaluating the Effects of Interventions,” Food Control 29, no. 2 (2013): 364-381, https://doi.org/10.1016/j.foodcont.2012.03.003; Beef Industry Food Safety Council Subcommittee on Pre-harvest, “Production Best Practices (PBP) to Aid in the Control of Foodborne Pathogens in Groups of Cattle” (2015), https://www.bifsco.org/CMDocs/BIFSCO2/Best%20Practices%20New/Production%20Best%20Practices-2015.pdf.
  8. Yadav S. Bajagai et al., “Probiotics in Animal Nutrition—Production, Impact and Regulation,” Food and Agriculture Organization of the United Nations Animal Production and Health Paper no. 179 (2016), http://www.fao.org/3/a-i5933e.pdf; S.M. Lutful Kabir, “The Role of Probiotics in the Poultry Industry,” International Journal of Molecular Sciences 10, no. 8 (2009), https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2812824/.
  9. The survey included 12 states. Large feedlots in these states accounted for 96.2 percent of cattle in large feedlots and 86.1 percent of large feedlots in the U.S. The survey results are representative of all large feedlots in the U.S. U.S. Department of Agriculture, Animal and Plant Health Inspection Service, Centers for Epidemiology and Animal Health, “Preharvest Food Safety Practices in U.S. Feedlots, 2011” (2013), https://www.aphis.usda.gov/animal_health/nahms/feedlot/downloads/feedlot2011/Feed11_is_Preharvest.pdf; U.S. Department of Agriculture, Animal and Plant Health Inspection Service, Veterinary Services, National Animal Health Monitoring System, “Feedlot 2011, Part 1: Management Practices on U.S. Feedlots with a Capacity of 1,000 or More Head” (2013), https://www.aphis.usda.gov/animal_health/nahms/feedlot/downloads/feedlot2011/Feed11_dr_PartI.pdf.
  10. Jeff T. LeJeune and Amy N. Wetzel, “Preharvest Control of Escherichia coli O157 in Cattle,” Journal of Animal Science 85, no. 13 (2007),
    https://academic.oup.com/jas/article/85/suppl_13/E73/4775325; Lee V. Wisener et al., “The Use of Direct-Fed Microbials to Reduce Shedding of Escherichia coli O157 in Beef Cattle: A Systematic Review and Meta-Analysis,” Zoonoses and Public Health 62, no. 2 (2015), https://doi.org/10.1111/zph.12112.
  11. Wisener et al., “The Use of Direct-Fed Microbials.”
  12. Stephen P. Oliver et al., “ASAS Centennial Paper: Developments and Future Outlook for Preharvest Food Safety,” Journal of Animal Science 87, no. 1 (2009), https://www.ncbi.nlm.nih.gov/pubmed/18708597.
  13. Ibid.
  14. Bajagai et al., “Probiotics in Animal Nutrition.”
  15. Defined probiotics consist of a known mixture of microorganisms, whereas undefined probiotics consist of an unknown mixture of microorganisms and tend to be more effective than defined probiotics. However, use of undefined probiotics raises concerns because of the lack of characterization. Ar’Quette Grant, Cyril G. Gay, and Hyun S. Lillehoj, “Bacillus spp. as Direct Fed Microbial Antibiotic Alternatives to Enhance Growth, Immunity, and Gut Health in Poultry,” Avian Pathology 47, no. 4 (2018): 339-351, https://doi.org/10.1080/03079457.2018.1464117.
  16. Ashley K. Kerr et al., “A Systematic Review-Meta-Analysis and Meta-Regression on the Effect of Selected Competitive Exclusion Products on Salmonella spp. Prevalence and Concentration in Broiler Chickens,” Preventive Veterinary Medicine 111, no. 1-2 (2013), https://www.ncbi.nlm.nih.gov/pubmed/23731553.
  17. Oliver et al., “ASAS Centennial Paper.”
  18. Kate G. Snedeker, Mollie Campbell, and Jan M. Sargeant, “A Systematic Review of Vaccinations to Reduce the Shedding of Escherichia coli O157 in the Faeces of Domestic Ruminants,” Zoonoses and Public Health 59, no. 2 (2012), https://doi.org/10.1111/j.1863-2378.2011.01426.x; Norma P. Varela, Paul Dick, and Jeff Wilson, “Assessing the Existing Information on the Efficacy of Bovine Vaccination Against Escherichia coli O157:H7: A Systematic Review and Meta-Analysis,” Zoonoses and Public Health 60, no. 4 (2013): 253–68, https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1863-2378.2012.01523.x; Amanda R. Vogstad et al., “Assessment of Heterogeneity of Efficacy of a Three-Dose Regimen of a Type III Secreted Protein Vaccine for Reducing STEC O157 in Feces of Feedlot Cattle,” Foodborne Pathogens and Disease 10, no. 8 (2013), https://doi.org/10.1089/fpd.2012.1374.
  19. Daniel U. Thomson et al., “Use of a Siderophore Receptor and Porin Proteins-Based Vaccine to Control the Burden of Escherichia coli O157:H7 in Feedlot Cattle,” Foodborne Pathogens and Disease 6, no. 7 (2009): 871-877, https://doi.org/10.1089/fpd.2009.0290.
  20. Louise Matthews et al., “Predicting the Public Health Benefit of Vaccinating Cattle Against Escherichia coli O157,” Proceedings of the National Academy of Sciences 110, no. 40 (2013), https://doi.org/10.1073/pnas.1304978110.
  21. U.S. Department of Agriculture, “Preharvest Food Safety Practices.”
  22. Glynn T. Tonsor and Ted C. Schroeder, “Market Impacts of E. coli Vaccination in U.S. Feedlot Cattle,” Agricultural and Food Economics 3 (2015), https://doi.org/10.1186/s40100-014-0021-2.
  23. Charley A. Cull et al., “Efficacy of a Vaccine and a Direct-Fed Microbial Against Fecal Shedding of Escherichia coli O157:H7 in a Randomized Pen-Level Field Trial of Commercial Feedlot Cattle,” Vaccine 30, no. 43 (2012), https://doi.org/10.1016/j.vaccine.2012.05.080.
  24. The Pew Charitable Trusts, “Food Safety From Farm to Fork.”
  25. Roy D. Berghaus et al., “Effect of Vaccinating Breeder Chickens With a Killed Salmonella Vaccine on Salmonella Prevalences and Loads in Breeder and Broiler Chicken Flocks,” Journal of Food Protection 74, no. 5 (2011), https://doi.org/10.4315/0362-028X.JFP-10-542; Fernanda C. Dórea et al., “Effect of Salmonella Vaccination of Breeder Chickens on Contamination of Broiler Chicken Carcasses in Integrated Poultry Operations,” Applied and Environmental Microbiology 76, no. 23 (2010), https://aem.asm.org/content/76/23/7820.
  26. Dórea et al., “Effect of Salmonella Vaccination.”
  27. Berghaus et al., “Effect of Vaccinating Breeder Chickens.”
  28. Chris McDaniel, “The Only Good Broiler Breeder Egg Is a Fertilized Egg,” Mississippi State University Extension (2010), http://extension.msstate.edu/sites/default/files/publications//IS1610_web.pdf; Phillip Clauer, “Modern Meat Chicken Industry,” Penn State University Extension, https://extension.psu.edu/modern-meat-chicken-industry; The Pew Charitable Trusts, “Food Safety From Farm to Fork”; U.S. Department of Agriculture, Animal and Plant Health Inspection Service, Veterinary Services, National Animal Health Monitoring System, “Poultry 2010: Structure of the U.S. Poultry Industry, 2010” (2011), https://www.aphis.usda.gov/animal_health/nahms/poultry/ downloads/poultry10/Poultry10_dr_Structure.pdf.
  29. Food and Agriculture Organization of the United Nations and the World Health Organization, “Risk Assessments of Salmonella in Eggs and Broiler Chickens,” accessed Dec. 14, 2018, http://www.fao.org/docrep/005/y4392e/y4392e00.htm.
  30. Sarah J. O’Brien, “The ‘Decline and Fall’ of Nontyphoidal Salmonella in the United Kingdom,” Clinical Infectious Diseases 56, no. 5 (2013), https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3563394/; Richard K. Gast, “Serotype-Specific and Serotype-Independent Strategies for Preharvest Control of Food-Borne Salmonella in Poultry,” Avian Diseases 51, no. 4 (2007), https://doi.org/10.1637/8090-081807.1; Anna Catharina Berge and Zöe Kay, “The Salmonella Puzzle: What Can We Learn From Europe?” Poultry World, https://www.poultryworld.net/Special-Focus/Salmonella-special/The-Salmonella-puzzle—what-can-we-learn-from-Europe/.
  31. The Pew Charitable Trusts, “Food Safety From Farm to Fork.”
  32. Jan M. Sargeant et al., “Pre-Harvest Interventions to Reduce the Shedding of E. coli O157 in the Faeces of Weaned Domestic Ruminants: A Systematic Review,” Zoonoses and Public Health54, no. 6-7 (2007): 260-77, https://www.ncbi.nlm.nih.gov/pubmed/17803515; Todd R. Callaway, Thomas S. Edrington, and David J. Nisbet, “Meat Science and Muscle Biology Symposium: Ecological and Dietary Impactors of Foodborne Pathogens and Methods to Reduce Fecal Shedding in Cattle,” Journal of Animal Science 92, no. 4 (2014), https://doi.org/10.2527/jas.2013-7308; Sarah C. Totton et al., “The Effectiveness of Selected Feed and Water Additives for Reducing Salmonella spp. of Public Health Importance in Broiler Chickens: A Systematic Review, Meta-Analysis, and Meta-Regression Approach,” Preventive Veterinary Medicine 106 (2012): 197–213, https://doi.org/10.1016/j.prevetmed.2012.07.007.
  33. Richard. P. Smith et al., “Maternal Vaccination as a Salmonella Typhimurium Reduction Strategy on Pig Farms,” Journal of Applied Microbiology 124, no. 1 (2018), https://doi.org/10.1111/jam.13609; Thomas N. Denagamage et al., “Efficacy of Vaccination to Reduce Salmonella Prevalence in Live and Slaughtered Swine: A Systematic Review of Literature From 1979 to 2007,” Foodborne Pathogens and Disease 4, no. 4 (2007), https://doi.org/10.1089/fpd.2007.0013.
  34. European Food Safety Authority, Panel on Biological Hazards, “Scientific Opinion on Campylobacter in Broiler Meat Production: Control Options and Performance Objectives and/or Targets at Different Stages of the Food Chain,” EFSA Journal 9, no. 4 (2011): http://www.efsa.europa.eu/en/efsajournal/pub/2105.
  35. Lindblad, “Lessons From Sweden’s Control.”
  36. D.G. Newell et al., “Biosecurity-Based Interventions and Strategies to Reduce Campylobacter spp. on Poultry Farms,” Applied and Environmental Microbiology 77, no. 24, (2011): 8605-8614, https://dx.doi.org/10.1128%2FAEM.01090-10.
  37. European Food Safety Authority, “Scientific Opinion on a Quantitative Microbiological Risk Assessment of Salmonella in Slaughter and Breeder Pigs,” EFSA Journal 8, no. 4 (2010): 1547, http://onlinelibrary.wiley.com/doi/10.2903/j.efsa.2010.1547/epdf; Jean Guard-Petter, “The Chicken, the Egg and Salmonella enteritidis,” Environmental Microbiology 3, no. 7 (2001): 421-430, https://doi.org/10.1046/j.14622920.2001.00213.x.