By Abhinav Upadhyay, DVM, PhD, postdoctoral associate and Dan J. Donoghue, PhD, professor University of Arkansas.

Contaminated poultry has been associated with at least 14 multi-state outbreaks, resulting in over 1 million cases of foodborne illnesses in people over the past decade. [1] Salmonella and campylobacter are the two bacterial pathogens responsible for most cases. An estimated 10 percent to 29 percent of salmonella infections and 43 percent of illness due to campylobacter are associated with contaminated poultry. [2]

The most commonly detected Salmonella serovars in poultry are Salmonella enteritidis, Salmonella typhimurium and Salmonella heidelberg [3] — all pathogens that can lead to food poisoning in people. Most cases of foodborne illness involving campylobacter are due to C. jejuni. [4]

Some progress has been made. The prevalence of Salmonella in US poultry products is the lowest it’s been since 2002.5 Nevertheless, poultry companies are under increased pressure to further improve food safety, especially since USDA tightened its standards for the maximum acceptable limits of salmonella and campylobacter found at processing.

It’s becoming apparent that an important first step toward producing a microbiologically safe product has to start preharvest, during live production, instead of depending on the processing plant to minimise the prevalence of foodborne pathogens.

A receptive host

Salmonella and campylobacter are difficult to manage because chickens are a reservoir host. Both pathogens have genes enabling them to evade the chicken’s immune system, survive the gut environment and utilise host resources for energy production - all factors that help them colonise the gut in high numbers.

Several factors can predispose birds to colonisation by salmonella and campylobacter. These include the gut’s microbial composition and the presence of immunosuppressive disease. It’s possible that older birds may have a higher prevalence of salmonella and campylobacter and that certain lines of chickens are more or less resistant to them - both possibilities under investigation.

Management considerations

Farm management factors contributing to the prevalence of salmonella and campylobacter during live production include stress due to overcrowding, insufficient biosecurity and contaminated litter or feed.

Reducing bird density is the obvious way to prevent overcrowding and poultry companies are generally well-versed about biosecurity. Strategies to reduce contamination in litter include composting and the addition of chemicals such as alum, lime and heat treatment. [6] Similarly, for preventing feed contamination, good environmental hygiene and regular testing for pathogens is critical. [7]

Breeder vaccination

Salmonella vaccines for broiler breeders aimed at providing protective immunity to their offspring are in high demand and have shown significant efficacy. [8,9] Broilers from breeders vaccinated against salmonella have less of the pathogen at processing, [10] and a dramatic reduction in human salmonella cases in the United Kingdom has been attributed in large part to vaccination of breeders against Salmonella. [11]

Vaccination of breeders must be administered at the right time to convey material antibodies to their progeny. Studies indicate this can be accomplished with vaccination between 11 to 18 weeks of age. [12,13] It’s important to make sure the vaccine used is effective against multiple serotypes of Salmonella and that it provides cross-protection. [14]

Broiler vaccination

Vaccination of broilers is challenging due to the cost of vaccinating huge numbers of birds that are often raised to only five or six weeks of age. In addition, vaccination during the first week of life may have limited efficacy due to an immature immune system. There is evidence, however, that broilers can be successfully vaccinated with a modified live Salmonella vaccine.[15]

With rising concern that antibiotic use in food animals may contribute to antibiotic resistance, vaccination of broilers against Salmonella is likely to become more prevalent, but the poultry industry needs improved vaccination strategies that are economical and easy to administer.

Developing an effective vaccine against campylobacter for chickens is another matter. It’s problematic due to the extensive diversity in the pathogen’s genome and surface-expressed proteins. [16] Several vaccination strategies, including killed and flagella-based vaccines, have been tested, but provide only moderate protection, [17,18] indicating more research is needed.

Prebiotics and probiotics

Another approach aimed at reducing the colonisation of salmonella and campylobacter in the gut is the use of prebiotic and probiotics in feed or water.

Prebiotics are ingredients that nourish good gut microorganisms and may promote resistance to colonisation of harmful pathogens. They aren’t digested by the body and have been described as food for probiotics.

Popular prebiotics are fructans and galactans. Numerous studies indicate they can enrich beneficial gut bacteria such as lactobacillus and/or bifidobacterium spp. These beneficial microbes in turn reduce colonisation by salmonella [19] and campylobacter. [20] Some prebiotics such as mannan oligosaccharide can bind and remove pathogens from the intestinal tract and stimulate the immune system. [21]

With advances in microbiome research, our understanding of gut microbiota composition and substances that modify the microbiota has improved. This has expanded the prebiotic concept to include new compounds such as yeast-based products and dietary fibres.

Probiotics are live, beneficial gut microorganisms. Competitive exclusion is a popular, on-farm, method that employs one or more probiotic bacteria to establish in the chicken gut and exert colonisation resistance to incoming pathogens.

Laboratory testing of candidate probiotics against Salmonella and campylobacter often yields promising results, however, when tested in the field, their efficacy varies. Hopefully this outcome will change with recent advancements in next generation sequencing technologies that make it possible to study the interactions between probiotics, target pathogens and other gut microbiota.

Promising compounds

Significant research conducted by our group and others in the last two decades has identified a plethora of compounds with significant antimicrobial efficacy. These compounds could be used in feed or water and include fatty acids, polyphenols, flavonoids, lectins and tannins.

Addition compounds with promise for controlling Salmonella and Campylobacter are caprylic acid obtained from coconut oil, trans-cinnamaldehyde from cinnamon bark, carvacrol from oregano oil and eugenol from clove oil. [22,23,24]

Future possibilities

Besides vaccination as well as the use of compounds with antimicrobial activity, future research might lead to the development of new chicken lines with improved resistance traits against salmonella and campylobacter.

Although concern about the possible development of resistance has led to the elimination or reduced use of antibiotics in food animals, research might eventually lead to ways antibiotics can be used to improve food safety without the development of resistance.

Recent findings from human research, for example, suggests that short courses of antibiotic therapy might be better than longer term administration and might actually reduce the development of resistance. [25,26] At Ohio State University, researchers have found that supplementation of bacitracin in feed didn’t affect Salmonella levels, but did lead to a reduction in the abundance of Clostridium perfringens, another pathogen that can make humans ill. [27]

Summing up

It’s clear the development of strategies for reducing the prevalence of Salmonella and Campylobacter during live production of poultry is sorely needed. We predict that new technologies and fresh ideas are paving the way for development of novel approaches that ultimately should enable the poultry industry to produce nutritious and microbiologically safe poultry products.

References

1. Scallan, E., Griffin, P. M., Angulo, F. J., Tauxe, R. V., & Hoekstra, R. M. (2011). Foodborne illness acquired in the United States—unspecified agents. Emerging infectious diseases, 17(1), 16.

2. Painter JA, Hoekstra RM, Ayers T, Tauxe RV, Braden CR, Angulo FJ, Griffin PM. 2013. Attribution of foodborne illnesses, hospitalizations, and deaths to food commodities by using outbreak data, United States, 1998- 2008.

3. Foley, S. L., Nayak, R., Hanning, I. B., Johnson, T. J., Han, J., & Ricke, S. C. (2011). Population dynamics of Salmonella enterica serotypes in commercial egg and poultry production. Applied and Environmental Microbiology, 77(13), 4273-4279.

4. Medic8. Campylobacter jejuni. medica8.com http://www.medic8.com/healthguide/food-poisoning/campylobacter-jejuni.html. Accessed July 19, 2018.
5. FDA NARMS Retail Meat Interim Report for Shows Encouraging Trends Continue; Includes Whole Genome Sequencing Data for the First Time http://www.fda.gov/AnimalVeter... Accessed July 14, 2016.
6. Chen, Z et al. 2014. Microbiological safety of chicken litter or chicken litter-based organic fertilizers: a review. Agriculture, 4(1), pp.1-29.

7. Davies, R.H. and Wales, A.D., 2010. Investigations into Salmonella contamination in poultry feedmills in the United Kingdom. Journal of applied microbiology, 109(4), pp.1430-1440.

8. Berghaus, R.D., Thayer, S.G., Maurer, J.J. and Hofacre, C.L., 2011. 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(5), pp.727-734.

9. Dórea, F.C., Cole, D.J., Hofacre, C., Zamperini, K., Mathis, D., Doyle, M.P., Lee, M.D. and Maurer, J.J., 2010. Effect of Salmonella vaccination of breeder chickens on contamination of broiler chicken carcasses in integrated poultry operations. Applied and environmental microbiology, 76(23), pp.7820-7825.

10. Ibid.

11. Poultry Vaccinations Credited for UK’s Big Drop in Salmonella. Food Safety News. January 23, 2013. http://www.foodsafetynews.com/... Accessed September 28, 2016

12. Berghaus, R.D., Thayer, S.G., Maurer, J.J. and Hofacre, C.L., 2011. 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(5), pp.727-734.

13. Dórea, F.C., Cole, D.J., Hofacre, C., Zamperini, K., Mathis, D., Doyle, M.P., Lee, M.D. and Maurer, J.J., 2010. Effect of Salmonella vaccination of breeder chickens on contamination of broiler chicken carcasses in integrated poultry operations. Applied and environmental microbiology, 76(23), pp.7820-7825.

14. Hofacre, C. Vaccination as key Salmonella control strategy in poultry meat production. Salmonella 360 Bulletin. Issue 8. Global Technical Services. Elanco.

15. Muni, E, et al. Evaluation of the effectiveness and safety of a genetically modified live vaccine in broilers challenged with Salmonella Heidelberg. Journal of Avian Pathology, Volume 46, 2017. Issue 6.
16. Duong and Konkel, 2009

17. Kobierecka, P.A., Wyszy?ska, A.K., Gubernator, J., Kuczkowski, M., Wi?niewski, O., Maruszewska, M., Wojtania, A., Derlatka, K.E., Adamska, I., Godlewska, R. and Jagusztyn-Krynicka, E.K., 2016. Chicken anti-Campylobacter vaccine–comparison of various carriers and routes of immunization. Frontiers in microbiology, 7.

18. Logan, S.M., Kelly, J.F., Thibault, P., Ewing, C.P. and Guerry, P., 2002. Structural heterogeneity of carbohydrate modifications affects serospecificity of Campylobacter flagellins. Molecular microbiology, 46(2), pp.587-597.

19. Pascual, M., Hugas, M., Badiola, J.I., Monfort, J.M. and Garriga, M., 1999. Lactobacillus salivarius CTC2197 prevents Salmonella enteritidis colonization in chickens. Applied and environmental microbiology, 65(11), pp.4981-4986.

20. Ghareeb, K., Awad, W.A., Mohnl, M., Porta, R., Biarnes, M., Böhm, J. and Schatzmayr, G., 2012. Evaluating the efficacy of an avian-specific probiotic to reduce the colonization of Campylobacter jejuni in broiler chickens. Poultry Science, 91(8), pp.1825-1832.

21. Spring, P., Wenk, C., Dawson, K.A. and Newman, K.E., 2000. The effects of dietary mannaoligosaccharides on cecal parameters and the concentrations of enteric bacteria in the ceca of salmonella-challenged broiler chicks. Poultry science, 79(2), pp.205-211.

22. Upadhyaya, I., Upadhyay, A., Yin, H.B., Nair, M.S., Bhattaram, V.K., Karumathil, D., Kollanoor-Johny, A., Khan, M.I., Darre, M.J., Curtis, P.A. and Venkitanarayanan, K., 2015. Reducing colonization and eggborne transmission of Salmonella enteritidis in layer chickens by in-feed supplementation of caprylic acid. Foodborne pathogens and disease, 12(7), pp.591-597.

23. Upadhyaya, I., Upadhyay, A., Kollanoor-Johny, A., Mooyottu, S., Baskaran, S.A., Yin, H.B., Schreiber, D.T., Khan, M.I., Darre, M.J., Curtis, P.A. and Venkitanarayanan, K., 2015. In-feed supplementation of trans-cinnamaldehyde reduces layer-chicken egg-borne transmission of Salmonella enterica serovar enteritidis. Applied and environmental microbiology, 81(9), pp.2985-2994.

24. Wagle, B.R., Upadhyay, A., Arsi, K., Shrestha, S., Venkitanarayanan, K., Donoghue, A.M. and Donoghue, D.J., 2017. Application of β-Resorcylic Acid as Potential Antimicrobial Feed Additive to Reduce Campylobacter Colonization in Broiler Chickens. Frontiers in microbiology, 8.
25. Spellberg, B., 2016. The New Antibiotic Mantra—“Shorter Is Better”. JAMA internal medicine, 176(9), pp.1254-1255.

26. Llewelyn, M.J., Fitzpatrick, J.M., Darwin, E., Gorton, C., Paul, J., Peto, T.E., Yardley, L., Hopkins, S. and Walker, A.S., 2017. The antibiotic course has had its day. Bmj, 358, p.j3418.

27. Wei, S., Gutek, A., Lilburn, M. and Yu, Z., 2013. Abundance of pathogens in the gut and litter of broiler chickens as affected by bacitracin and litter management. Veterinary microbiology, 166(3-4), pp.595-601.