Practical Preventive Considerations for Reducing the Public Health Burden of Poultry-Related Salmonellosis
Abstract
:1. Introduction
2. Identification of Salmonella Serovars
3. Colonization of Salmonella Serovars in Poultry Flocks
4. Salmonella in the Poultry Production System at the Preharvest Level
4.1. Feed
4.2. Parent Stock and Hatchery
4.3. Litter
4.4. Feed Withdrawal
5. Contribution of Poultry as a Reservoir of Antimicrobial Resistance
6. Control and Prevention of Salmonella
6.1. Feeding-Based Strategies
6.1.1. Prebiotics
6.1.2. Probiotics
6.1.3. Phytobiotics
6.1.4. Essential Oils
6.2. Non-Feeding Strategies
6.2.1. Bacteriophages
6.2.2. Vaccines
6.2.3. In Ovo Strategies
6.3. Omics Tool for Identifying Antibiotic-Resistance Genes
6.4. Treatment of Salmonella in Poultry-Processing Facilities (Post-Harvest)
6.5. Biosecurity at the Poultry Farm
7. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Asefaw, S.; Aras, S.; Kabir, M.N.; Wadood, S.; Chowdhury, S.; Fouladkhah, A.C. Public Health Importance of Preventive Measures for Salmonella Tennessee and Salmonella Typhimurium Strain LT2 Biofilms. Microbiol. Res. 2023, 14, 714–726. [Google Scholar]
- Kumar, A.; Allison, A.; Henry, M.; Scales, A.; Fouladkhah, A.C. Development of salmonellosis as affected by bioactive food compounds. Microorganisms 2019, 7, 364. [Google Scholar] [PubMed]
- Abd El-Ghany, W.A. Salmonellosis: A food borne zoonotic and public health disease in Egypt. J. Infect. Dev. Ctries 2020, 14, 674–678. [Google Scholar] [PubMed]
- Scallan, E.; Hoekstra, R.M.; Angulo, F.J.; Tauxe, R.V.; Widdowson, M.A.; Roy, S.L.; Jones, J.L.; Griffin, P.M. Foodborne illness acquired in the United States—Major pathogens. Emerg. Infect. Dis. 2011, 17, 7. [Google Scholar]
- Crump, J.A.; Luby, S.P.; Mintz, E.D. The global burden of typhoid fever. Bull. World Health Organ. 2004, 82, 346–353. [Google Scholar] [PubMed]
- Fouladkhah, A.; Geornaras, I.; Sofos, J.N. Biofilm formation of O157 and Non-O157 Shiga toxin-producing Escherichia coli and multidrug-resistant and susceptible Salmonella Typhimurium and Newport and their inactivation by sanitizers. J. Food Sci. 2013, 78, M880–M886. [Google Scholar]
- Allison, A.; Fouladkhah, A.C. Sensitivity of planktonic cells and biofilm of wild-type and pressure-stressed Cronobacter sakazakii and Salmonella enterica serovars to sodium hypochlorite. Food Prot. Trends 2021, 41, 195–203. [Google Scholar]
- Chowdhury, A.; Aras, S.; Kabir, N.; Wadood, S.; Allison, A.; Chowdhury, S.; Fouladkhah, A.C. Susceptibility of pathogenic nontyphoidal Salmonella serovars and avirulent Salmonella LT2 to elevated hydrostatic pressure and citricidalTM. J. Tenn. Acad. Sci. 2021, 96, 49–54. [Google Scholar]
- Fouladkhah, A.C.; Thompson, B.; Camp, J.S. Safety of food and water supplies in the landscape of changing climate. Microorganisms 2019, 7, 469. [Google Scholar]
- Fouladkhah, A.C.; Thompson, B.; Camp, J.S. The threat of antibiotic resistance in changing climate. Microorganisms 2020, 8, 748. [Google Scholar]
- Mottet, A.; Tempio, G. Global poultry production: Current state and future outlook and challenges. World’s Poult. Sci. J. 2017, 73, 245–256. [Google Scholar]
- Magdelaine, P.; Spiess, M.P.; Valceschini, E. Poultry meat consumption trends in Europe. Worlds Poult. Sci. J. 2008, 64, 53–64. [Google Scholar]
- Alexandratos, N.; Bruinsma, J. World Agriculture towards 2030/2050: The 2012 Revision. 2012. Available online: https://www.fao.org/3/ap106e/ap106e.pdf (accessed on 2 October 2022).
- Organisation for Economic Co-Operation and Development. Meat Consumption. 2022. Available online: https://data.oecd.org/agroutput/meat-consumption.htm (accessed on 8 November 2022).
- Farrell, D. The role of poultry in human nutrition. In Poultry Development Review; Food and Agriculture Organization: Rome, Italy, 2013; pp. 2–9. [Google Scholar]
- Gomes, B.C.; Franco, B.D.G.D.M.; De Martinis, E.C.P. Microbiological food safety issues in Brazil: Bacterial pathogens. Foodborne Pathog. Dis. 2013, 10, 197–205. [Google Scholar]
- Abebe, E.; Gugsa, G.; Ahmed, M. Review on major food-borne zoonotic bacterial pathogens. J. Trop. Med. 2020, 2020, 4674235. [Google Scholar]
- Ravel, A.; Greig, J.; Tinga, C.; Todd, E.; Campbell, G.; Cassidy, M.; Marshall, B.; Pollari, F. Exploring historical Canadian foodborne outbreak data sets for human illness attribution. J. Food Prot. 2009, 72, 1963–1976. [Google Scholar]
- Guo, C.; Hoekstra, R.M.; Schroeder, C.M.; Pires, S.M.; Ong, K.L.; Hartnett, E.; Naugle, A.; Harman, J.; Bennett, P.; Cieslak, P.; et al. Application of Bayesian techniques to model the burden of human salmonellosis attributable to U.S. food commodities at the point of processing: Adaptation of a Danish model. Foodborne Pathog. Dis. 2011, 8, 509–516. [Google Scholar]
- Antunes, P.; Mourão, J.; Campos, J.; Peixe, L. Salmonellosis: The role of poultry meat. Clin. Microbiol. Infect. 2016, 22, 110–121. [Google Scholar]
- Williams, M.S.; Ebel, E.D.; Golden, N.J.; Schlosser, W.D. Temporal patterns in the occurrence of Salmonella in raw meat and poultry products and their relationship to human illnesses in the United States. Food Control. 2014, 35, 267–273. [Google Scholar]
- Lee, M.D.; Newell, D.G. Campylobacter in poultry: Filling an ecological niche. Avian Dis. 2006, 50, 1–9. [Google Scholar]
- Cox, N.A.; Berrang, M.E.; Cason, J.A. Salmonella penetration of egg shells and proliferation in broiler hatching eggs—A review. Poult. Sci. 2000, 79, 1571–1574. [Google Scholar]
- Lahellec, C.; Colin, P. Relationship between serotypes of Salmonellae from hatcheries and rearing farms and those from processed poultry carcases. Br. Poult. Sci. 1985, 26, 179–186. [Google Scholar] [CrossRef]
- Opitz, H.M.; El-Begearmi, M.; Flegg, P.; Beane, D. Effectiveness of five feed additives in chicks infected with Salmonella enteritidis phage type 13a. J. Appl. Poult. Res. 1993, 2, 147–153. [Google Scholar] [CrossRef]
- Ramirez, G.A.; Sarlin, L.L.; Caldwell, D.J.; Yezak Jr, C.R.; Hume, M.E.; Corrier, D.E.; Deloach, J.R.; Hargis, B.M. Effect of feed withdrawal on the incidence of Salmonella in the crops and ceca of market age broiler chickens. Poult. Sci. 1997, 76, 654–656. [Google Scholar] [CrossRef]
- Dunkley, K.D.; McReynolds, J.L.; Hume, M.E.; Dunkley, C.S.; Callaway, T.R.; Kubena, L.F.; Nisbet, D.J.; Ricke, S.C. Molting in Salmonella Enteritidis-challenged laying hens fed alfalfa crumbles: II. Fermentation and microbial ecology response. Poult. Sci. 2007, 86, 2101–2109. [Google Scholar] [PubMed]
- Ruvalcaba-Gómez, J.M.; Villagrán, Z.; Valdez-Alarcón, J.J.; Martínez-Núñez, M.; Gomez-Godínez, L.J.; Ruesga-Gutiérrez, E.; Anaya-Esparza, L.M.; Arteaga-Garibay, R.I.; Villarruel-López, A. Non-Antibiotics Strategies to Control Salmonella Infection in Poultry. J. Anim. 2022, 12, 102. [Google Scholar] [CrossRef]
- Bhunia, A.K. Salmonella Enterica. In Foodborne Microbial Pathogens; Springer: New York, NY, USA, 2008; pp. 201–216. [Google Scholar]
- Pui, C.F.; Wong, W.C.; Chai, L.C.; Tunung, R.; Jeyaletchumi, P.; Hidayah, N.; Ubong, A.; Farinazleen, M.G.; Cheah, Y.K.; Son, R. Salmonella: A foodborne pathogen. Int. Food Res. J. 2011, 18, 465–473. [Google Scholar]
- Mouttotou, N.; Ahmad, S.; Kamran, Z.; Koutoulis, K.C. Prevalence, Risks and Antibiotic Resistance of Salmonella in Poultry Production Chain. In Current Topics in Salmonella and Salmonellosis; Mares, M., Ed.; InTechOpen: London, UK, 2017; p. 67438. [Google Scholar]
- World Health Organization. Salmonella (Non-Typhoidal). Available online: https://www.who.int/news-room/fact-sheets/detail/salmonella-(non-typhoidal) (accessed on 20 August 2023).
- Flint, J.A.; Van Duynhoven, Y.T.; Angulo, F.J.; DeLong, S.M.; Braun, P.; Kirk, M.; Scallan, E.; Fitzgerald, M.; Adak, G.K.; Sockett, P.; et al. Estimating the burden of acute gastroenteritis, foodborne disease, and pathogens commonly transmitted by food: An international review. Clin. Infect. Dis. 2005, 41, 698–704. [Google Scholar] [CrossRef]
- FDA. Human Health Impact of Fluoroquinolone Resistant Campylobacter Associated with the Consumption of Chicken. 2000. Available online: https://www.fda.gov/media/76429/download (accessed on 20 August 2023).
- U.S. Department of Agriculture, Food Safety and Inspection Service. Modernization of Poultry Slaughter Inspection. Available online: https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/modernization-poultry-slaughter (accessed on 20 August 2023).
- Braden, C.R. Salmonella enterica serotype Enteritidis and eggs: A national epidemic in the United States. Clin. Infect. Dis. 2006, 43, 512–517. [Google Scholar] [CrossRef]
- Painter, J.A.; Hoekstra, R.M.; Ayers, T.; Tauxe, R.V.; Braden, C.R.; Angulo, F.J.; Griffin, P.M. Attribution of foodborne illnesses, hospitalizations, and deaths to food commodities by using outbreak data, United States, 1998–2008. Emerg. Infect. Dis. 2013, 19, 407. [Google Scholar] [CrossRef] [PubMed]
- Gast, R.K. Serotype-specific and serotype-independent strategies for preharvest control of food-borne Salmonella in poultry. Avian Dis. 2007, 51, 817–828. [Google Scholar] [CrossRef]
- Ferrari, R.G.; Rosario, D.K.; Cunha-Neto, A.; Mano, S.B.; Figueiredo, E.E.; Conte-Junior, C.A. Worldwide epidemiology of Salmonella serovars in animal-based foods: A meta-analysis. Appl. Environ. Microbiol. 2019, 85, e00591-19. [Google Scholar] [CrossRef] [PubMed]
- Popa, G.L.; Papa, M.I. Salmonella spp. Infection—A continuous threat worldwide. Germs 2021, 11, 88. [Google Scholar] [CrossRef] [PubMed]
- Threlfall, E.J.; Frost, J.A.; Ward, L.R.; Rowe, B. Increasing spectrum of resistance in multiresistant Salmonella typhimurium. Lancet 1996, 347, 1053–1054. [Google Scholar] [CrossRef]
- Le Hello, S.; Harrois, D.; Bouchrif, B.; Sontag, L.; Elhani, D.; Guibert, V.; Zerouli, K.; Weill, F.X. Highly drug-resistant Salmonella enterica serotype Kentucky ST198-X1: A microbiological study. Lancet Infect. Dis. 2013, 13, 672–679. [Google Scholar] [CrossRef]
- Swartz, M.N. Human diseases caused by foodborne pathogens of animal origin. Clin. Infect. Dis. 2002, 34, S111–S122. [Google Scholar] [CrossRef] [PubMed]
- Haque, M.H.; Sarker, S.; Islam, M.S.; Islam, M.A.; Karim, M.R.; Kayesh, M.E.H.; Shiddiky, M.J.A.; Answer, M.S. Sustainable Antibiotic-Free Broiler Meat Production: Current Trends, Challenges, and Possibilities in a Developing Country Perspective. Biology 2020, 9, 411. [Google Scholar] [CrossRef]
- Issenhuth-Jeanjean, S.; Roggentin, P.; Mikoleit, M.; Guibourdenche, M.; De Pinna, E.; Nair, S.; Fields, P.I.; Weill, F.X. Supplement 2008–2010 (no. 48) to the white–Kauffmann–Le minor scheme. Res. Microbiol. 2014, 165, 526–530. [Google Scholar] [CrossRef]
- Alikhan, N.F.; Zhou, Z.; Sergeant, M.J.; Achtman, M. A genomic overview of the population structure of Salmonella. PLoS Genet. 2018, 14, e1007261. [Google Scholar] [CrossRef]
- Mkangara, M.; Mwakapuja, R.; Chilongola, J.; Ndakidemi, P.; Mbega, E.; Chacha, M. Mechanisms for Salmonella infection and potential management options in chicken. J. Anim. Plant Sci. 2020, 30, 259–279. [Google Scholar]
- Forsythe, S.J. The Microbiology of Safe Food; Wiley-Blackwell: Hoboken, NJ, USA, 2020. [Google Scholar]
- Kurtz, J.R.; Goggins, J.A.; McLachlan, J.B. Salmonella infection: Interplay between the bacteria and host immune system. Immunol. Lett. 2017, 190, 42–50. [Google Scholar] [CrossRef] [PubMed]
- The U.S. Food and Drug Administration. Bad Bug Book: Handbook of Foodborne Pathogenic Microorganisms and Natural Toxins; CreateSpace Independent Publishing Platform: Scotts Valley, CA, USA, 2017. Available online: https://www.fda.gov/food/foodborne-pathogens/bad-bug-book-second-edition (accessed on 20 August 2023).
- ISO 6579-1:2017; Microbiology of Food and Feeding Stuffs—Horizontal Method for the Detection of Salmonella spp. in the Food Production Chain. ISO: Geneve, Switzerland, 2017.
- Dunkley, K.D.; Callaway, T.R.; Chalova, V.I.; McReynolds, J.L.; Hume, M.E.; Dunkley, C.S.; Kubena, L.F.; Nisbet, D.J.; Ricke, S.C. Foodborne Salmonella ecology in the avian gastrointestinal tract. Anaerobe 2009, 15, 26–35. [Google Scholar] [CrossRef] [PubMed]
- Tanner, J.R.; Kingsley, R.A. Evolution of Salmonella within Hosts. Trends Microbiol. 2018, 26, 986–998. [Google Scholar] [CrossRef]
- Mebrhatu, M.T.; Cenens, W.; Aertsen, A. An overview of the domestication and impact of the Salmonella mobilome. Crit. Rev. Microbiol. 2014, 40, 63–75. [Google Scholar] [CrossRef]
- Staes, I.; Passaris, I.; Cambré, A.; Aertsen, A. Population heterogeneity tactics as driving force in Salmonella virulence and survival. Food Res. Int. 2019, 125, 108560. [Google Scholar] [CrossRef] [PubMed]
- Cheng, R.A.; Eade, C.R.; Wiedmann, M. Embracing Diversity: Differences in Virulence Mechanisms, Disease Severity, and Host Adaptations Contribute to the Success of Nontyphoidal Salmonella as a Foodborne Pathogen. Front. Microbiol. 2019, 10, 1368. [Google Scholar] [CrossRef]
- Marcus, S.L.; Brumell, J.H.; Pfeifer, C.G.; Finlay, B.B. Salmonella pathogenicity islands: Big virulence in small packages. Microbes Infect. 2000, 2, 145–156. [Google Scholar] [CrossRef]
- Shivaprasad, H.L.; Barrow, P.A. Pullorum disease and fowl typhoid. In Diseases of Poultry, 12th ed.; Blackwell Publishing Professional: Ames, IA, USA, 2008; pp. 620–634. [Google Scholar]
- Oakley, B.B.; Lillehoj, H.S.; Kogut, M.H.; Kim, W.K.; Maurer, J.J.; Pedroso, A.; Lee, M.D.; Collett, S.R.; Johnson, T.J.; Cox, N.A. The chicken gastrointestinal microbiome. FEMS Microbiol. Lett. 2014, 360, 100–112. [Google Scholar] [CrossRef]
- Tavechio, A.T.; Fernandes, S.A.; Neves, B.C.; Dias, A.M.G.; Irino, K. Changing patterns of Salmonella serovars: Increase of Salmonella enteritidis in São Paulo, Brazil. Rev. Inst. Med. Trop. 1996, 38, 315–322. [Google Scholar] [CrossRef] [PubMed]
- Bäumler, A.J.; Hargis, B.M.; Tsolis, R.M. Tracing the origins of Salmonella outbreaks. Science 2000, 287, 50–52. [Google Scholar] [CrossRef]
- Silva, E.N.D.; Duarte, A. Salmonella Enteritidis em aves: Retrospectiva no Brasil. Braz. J. Poult. Sci. 2002, 4, 85–100. [Google Scholar] [CrossRef]
- Foley, S.L.; Lynne, A.M.; Nayak, R. Salmonella challenges: Prevalence in swine and poultry and potential pathogenicity of such isolates. J. Anim. Sci. 2008, 86, E149–E162. [Google Scholar] [CrossRef] [PubMed]
- Voss-Rech, D.; Vaz, C.S.; Alves, L.; Coldebella, A.; Leao, J.A.; Rodrigues, D.P.; Back, A. A temporal study of Salmonella enterica serotypes from broiler farms in Brazil. Poult. Sci. 2015, 94, 433–441. [Google Scholar] [CrossRef]
- Wernicki, A.; Nowaczek, A.; Urban-Chmiel, R. Bacteriophage therapy to combat bacterial infections in poultry. Virology J. 2017, 14, 179. [Google Scholar] [CrossRef]
- Jones, F.T. A review of practical Salmonella control measures in animal feed. J. Appl. Poult. Res. 2011, 20, 102–113. [Google Scholar] [CrossRef]
- Jones, F.T.; Axtell, R.C.; Rives, D.V.; Scheideler, S.E.; Tarver, F.R., Jr.; Walker, R.L.; Wineland, M.J. A survey of Salmonella contamination in modern broiler production. J. Food Prot. 1991, 54, 502–507. [Google Scholar] [CrossRef]
- Dórea, F.C.; Cole, D.J.; Hofacre, C.; Zamperini, K.; Mathis, D.; Doyle, M.P.; Lee, M.D.; Maurer, J.J. Effect of Salmonella vaccination of breeder chickens on contamination of broiler chicken carcasses in integrated poultry operations. Appl. Environ. Microbiol. 2010, 76, 7820–7825. [Google Scholar] [CrossRef]
- Timoney, J.F. Egg transmission after infection of hens with Salmonella enteritidis phage type 4. Vet. Rec. 1989, 125, 600–601. [Google Scholar] [PubMed]
- Shivaprasad, H.L.; Timoney, J.F.; Morales, S.; Lucio, B.; Baker, R.C. Pathogenesis of Salmonella enteritidis infection in laying chickens. I. Studies on egg transmission, clinical signs, fecal shedding, and serologic responses. Avian Dis. 1990, 34, 548–557. [Google Scholar] [CrossRef] [PubMed]
- Rizk, S.S.; Ayres, J.C.; Kraft, A.A. Effect of holding condition on the development of salmonellae in artificially inoculated hens’ eggs. Poult. Sci. 1966, 45, 825–829. [Google Scholar] [CrossRef]
- Heyndrickx, M.; Vandekerchove, D.; Herman, L.; Rollier, I.; Grijspeerdt, K.; De Zutter, L. Routes for Salmonella contamination of poultry meat: Epidemiological study from hatchery to slaughterhouse. Epidemiol. Infect. 2022, 129, 253–265. [Google Scholar] [CrossRef]
- Alali, W.Q.; Hofacre, C.L. Preharvest Food Safety in Broiler Chicken Production. Microbiol. Spectr. 2016, 4, 69–86. [Google Scholar] [CrossRef]
- David, B.; Mejdell, C.; Michel, V.; Lund, V.; Moe, R.O. Air Quality in Alternative Housing Systems may have an Impact on Laying Hen Welfare: Part II—Ammonia. J. Anim. 2015, 5, 886–896. [Google Scholar] [CrossRef] [PubMed]
- Pal, A.; Bailey, M.A.; Talorico, A.A.; Krehling, J.T.; Macklin, K.S.; Price, S.B.; Buhr, R.J.; Bourassa, D.V. Impact of poultry litter Salmonella levels and moisture on transfer of Salmonella through associated in vitro generated dust. Poult. Sci. 2021, 100, 101236. [Google Scholar] [CrossRef]
- Bhatia, T.R.S.; McNabb, G.D. Dissemination of Salmonella in broiler-chicken operations. Avian Dis. 1980, 24, 616–624. [Google Scholar] [CrossRef] [PubMed]
- Corrier, D.E.; Byrd, J.A.; Hargis, B.M.; Hume, M.E.; Bailey, R.H.; Stanker, L.H. Survival of Salmonella in the crop contents of market-age broilers during feed withdrawal. Avian Dis. 1999, 43, 453–460. [Google Scholar] [CrossRef]
- European Centre for Disease Prevention and Control; European Food Safety Authority. European Medicines Agency and European Commission’s Scientific Committee on Emerging and Newly Identified Health Risks 2009. EFSA J. 2009, 7, 1372. [Google Scholar]
- Threlfall, E.J. Antimicrobial drug resistance in Salmonella: Problems and perspectives in food- and water-borne infections. FEMS Microbiol. Rev. 2002, 26, 141–148. [Google Scholar] [CrossRef] [PubMed]
- Parry, C.M.; Threlfall, E.J. Antimicrobial resistance in typhoidal and nontyphoidal salmonellae. Curr. Opin. Infect. Dis. 2008, 21, 531–538. [Google Scholar] [CrossRef]
- Chen, H.M.; Wang, Y.; Su, L.H.; Chiu, C.H. Nontyphoid Salmonella infection: Microbiology, clinical features, and antimicrobial therapy. Pediatr. Neonato. 2013, 54, 147–152. [Google Scholar] [CrossRef]
- Aarestrup, F.M. The livestock reservoir for antimicrobial resistance: A personal view on changing patterns of risks, effects of interventions and the way forward. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2015, 370, 20140085. [Google Scholar] [CrossRef]
- O’Neill, J. Antimicrobials in Agriculture and the Environment: Reducing Unnecessary Use and Waste. 2015. Available online: https://amr-review.org/Publications.html (accessed on 20 August 2023).
- Roberts, M.C. Antibiotics and Resistance in the Environment. In Antimicrobial Resistance in the 21st Century; Springer: Cham, Switzerlands, 2018; pp. 383–407. [Google Scholar]
- Antunes, P.; Machado, J.; Peixe, L. Illegal use of nitrofurans in food animals: Contribution to human salmonellosis? Clin. Microbiol. Infect. 2006, 12, 1047–1049. [Google Scholar] [CrossRef] [PubMed]
- Dutil, L.; Irwin, R.; Finley, R.; Ng, L.K.; Avery, B.; Boerlin, P.; Bourgault, A.M.; Cole, L.; Daignault, D.; Desruisseau, A.; et al. Ceftiofur resistance in Salmonella enterica serovar Heidelberg from chicken meat and humans, Canada. Emerg. Infect. Dis. 2010, 16, 48. [Google Scholar] [CrossRef]
- Moulana, Z.; Asgharpour, F. Prevalence and Antimicrobial Resistance of Salmonella enterica Serovar Infantis Isolates from Poultry: A review. Poult. Sci. J. 2022, 10, 13–26. [Google Scholar]
- Nandi, S.; Maurer, J.J.; Hofacre, C.; Summers, A.O. Gram-positive bacteria are a major reservoir of Class 1 antibiotic resistance integrons in poultry litter. Proc. Natl. Acad. Sci. USA 2004, 101, 7118–7122. [Google Scholar] [CrossRef]
- Yang, Y.; Ashworth, A.J.; Willett, C.; Cook, K.; Upadhyay, A.; Owens, P.R.; Ricke, S.C.; DeBruyn, J.M.; Moore Jr, P.A. Review of antibiotic resistance, ecology, dissemination, and mitigation in US broiler poultry systems. Front. Microbiol. 2019, 10, 2639. [Google Scholar] [CrossRef] [PubMed]
- Didelot, X.; Fraser, C.; Gardy, J.; Colijn, C. Genomic Infectious Disease Epidemiology in Partially Sampled and Ongoing Outbreaks. Mol. Biol. Evol. 2017, 34, 997–1007. [Google Scholar] [CrossRef]
- Butel, M.J.; Waligora-Dupriet, A.J.; Wydau-Dematteis, S. The developing gut microbiota and its consequences for health. Dev. Orig. Health Dis. 2018, 9, 590–597. [Google Scholar] [CrossRef]
- Xu, Z.R.; Hu, C.H.; Xia, M.S.; Zhan, X.A.; Wang, M.Q. Effects of dietary fructooligosaccharide on digestive enzyme activities, intestinal microflora and morphology of male broilers. Poult. Sci. 2003, 82, 1030–1036. [Google Scholar] [CrossRef]
- Donalson, L.M.; McReynolds, J.L.; Kim, W.K.; Chalova, V.I.; Woodward, C.L.; Kubena, L.F.; Nisbet, D.J.; Ricke, S.C. The influence of a fructooligosaccharide prebiotic combined with alfalfa molt diets on the gastrointestinal tract fermentation, Salmonella enteritidis infection, and intestinal shedding in laying hens. Poult. Sci. 2008, 87, 1253–1262. [Google Scholar] [CrossRef] [PubMed]
- Charalampopoulos, D.; Rastall, R.A. (Eds.) Prebiotics and Probiotics Science and Technology; Springer Science & Business Media LLC: Berlin/Heidelberg, Germany, 2009. [Google Scholar]
- Durant, J.A.; Corrier, D.E.; Ricke, S.C. Short-chain volatile fatty acids modulate the expression of the hilA and invF genes of Salmonella typhimurium. J. Food Prot. 2000, 63, 573–578. [Google Scholar] [CrossRef]
- El-Shall, N.A.; Awad, A.M.; El-Hack, M.E.A.; Naiel, M.A.; Othman, S.I.; Allam, A.A.; Sedeik, M.E. The simultaneous administration of a probiotic or prebiotic with live Salmonella vaccine improves growth performance and reduces fecal shedding of the bacterium in Salmonella-challenged broilers. J. Anim. 2019, 10, 70. [Google Scholar] [CrossRef] [PubMed]
- Borchers, A.T.; Selmi, C.; Meyers, F.J.; Keen, C.L.; Gershwin, M.E. Probiotics and immunity. J. Gastroenterol. 2009, 44, 26–46. [Google Scholar] [CrossRef]
- Tellez, G.; Pixley, C.; Wolfenden, R.E.; Layton, S.L.; Hargis, B.M. Probiotics/direct fed microbials for Salmonella control in poultry. Food Res. Int. 2012, 45, 628–633. [Google Scholar] [CrossRef]
- Higgins, J.P.; Andreatti Filho, R.L.; Higgins, S.E.; Wolfenden, A.D.; Téllez, G.; Hargis, B.M. Evaluation of Salmonella-lytic properties of bacteriophages isolated from commercial broiler houses. Avian Dis. 2008, 52, 139–142. [Google Scholar] [CrossRef] [PubMed]
- Gheisar, M.M.; Hosseindoust, A.; Kim, I.H. Evaluating the effect of microencapsulated blends of organic acids and essential oils in broiler chickens diet. J. Appl. Poult. Res. 2015, 24, 511–519. [Google Scholar] [CrossRef]
- Amad, A.A.; Männer, K.; Wendler, K.R.; Neumann, K.; Zentek, J. Effects of a phytogenic feed additive on growth performance and ileal nutrient digestibility in broiler chickens. Poult. Sci. 2011, 90, 2811–2816. [Google Scholar] [CrossRef]
- Orndorff, B.W.; Novak, C.L.; Pierson, F.W.; Caldwell, D.J.; McElroy, A.P. Comparison of prophylactic or therapeutic dietary administration of capsaicin for reduction of Salmonella in broiler chickens. Avian Dis. 2005, 49, 527–533. [Google Scholar] [CrossRef]
- Solarte, A.L.; Astorga, R.J.; Aguiar, F.; Galán-Relaño, Á.; Maldonado, A.; Huerta, B. Combination of antimicrobials and essential oils as an alternative for the control of Salmonella enterica multiresistant strains related to foodborne disease. Foodborne Pathog. Dis. 2017, 14, 558–563. [Google Scholar] [CrossRef]
- Ebani, V.V.; Nardoni, S.; Bertelloni, F.; Tosi, G.; Massi, P.; Pistelli, L.; Mancianti, F. In vitro antimicrobial activity of essential oils against Salmonella enterica serotypes Enteritidis and Typhimurium strains isolated from poultry. Molecules 2019, 24, 900. [Google Scholar] [CrossRef]
- Rochín-Medina, J.J.; Mendoza-López, I.A.; Castro-del Campo, N.; Bastidas-Bastidas, P.J.; Ramírez, K. Activity of plant essential oils against clinically and environmentally isolated Salmonella enterica serotypes: In vitro assays and molecular docking. Lett. Appl. Microbiol. 2023, 76, ovad045. [Google Scholar] [CrossRef] [PubMed]
- Abedon, S.T.; Loc-Carrillo, C. Pros and cons of phage therapy. Bacteriophage 2011, 1, 111–114. [Google Scholar]
- Żbikowska, K.; Michalczuk, M.; Dolka, B. The use of bacteriophages in the poultry industry. Animals 2023, 10, 872. [Google Scholar] [CrossRef] [PubMed]
- Nilsson, A.S. Phage therapy—Constraints and possibilities. Ups. J. Med. Sci. 2014, 119, 192–198. [Google Scholar] [CrossRef] [PubMed]
- Wong, C.L.; Sieo, C.C.; Tan, W.S.; Abdullah, N.; Hair-Bejo, M.; Abu, J.; Ho, Y.W. Evaluation of a lytic bacteriophage, Φ st1, for biocontrol of Salmonella enterica serovar Typhimurium in chickens. Int. J. Food Microbiol. 2014, 172, 92–101. [Google Scholar] [CrossRef]
- Centre for Disease Control and Prevention. Whole Genome Sequencing. 2016. Available online: https://www.cdc.gov/pulsenet/pathogens/wgs.html (accessed on 5 November 2022).
- Acevedo-Villanueva, K.Y.; Akerele, G.O.; Al Hakeem, W.G.; Renu, S.; Shanmugasundaram, R.; Selvaraj, R.K. A Novel Approach against Salmonella: A Review of Polymeric Nanoparticle Vaccines for Broilers and Layers. Vaccines 2021, 9, 1041. [Google Scholar] [CrossRef]
- Renu, S.; Han, Y.; Dhakal, S.; Lakshmanappa, Y.S.; Ghimire, S.; Feliciano-Ruiz, N.; Senapati, S.; Narasimhan, B.; Selvaraj, R.; Renukaradhya, G.J. Chitosan-adjuvanted Salmonella subunit nanoparticle vaccine for poultry delivered through drinking water and feed. Carbohydr. Polym. 2020, 243, 116434. [Google Scholar] [CrossRef] [PubMed]
- Rabie, N.S.; Amin Girh, Z.M.S. Bacterial vaccines in poultry. Bull. Natl. Res. Cent. 2020, 44, 15. [Google Scholar] [CrossRef]
- Jia, S.; McWhorter, A.R.; Andrews, D.M.; Underwood, G.J.; Chousalkar, K.K. Challenges in Vaccinating Layer Hens against Salmonella Typhimurium. Vaccines 2020, 8, 696. [Google Scholar] [CrossRef]
- Shehata, A.M.; Paswan, V.K.; Attia, Y.A.; Abdel-Moneim, A.M.E.; Abougabal, M.S.; Sharaf, M.; Elmazoudy, R.; Alghafari, W.T.; Osman, M.A.; Farag, M.R.; et al. Managing gut microbiota through in ovo nutrition influences early-life programming in broiler chickens. J. Anim. 2021, 11, 3491. [Google Scholar] [CrossRef]
- Alagawany, M.; Elnesr, S.S.; Farag, M.R.; Abd El-Hack, M.E.; Barkat, R.A.; Gabr, A.A.; Foda, M.A.; Noreldin, A.E.; Khafaga, A.F.; El-Sabrout, K.; et al. Potential role of important nutraceuticals in poultry performance and health—A comprehensive review. Res. Vet. Sci. 2021, 137, 9–29. [Google Scholar] [CrossRef]
- Vaezirad, M.M.; Koene, M.G.; Wagenaar, J.A.; Van Putten, J.P.M. Chicken immune response following in ovo delivery of bacterial flagellin. Vaccine 2018, 36, 2139–2146. [Google Scholar] [CrossRef]
- Cox, C.M.; Dalloul, R.A. Immunomodulatory role of probiotics in poultry and potential in ovo application. Benef. Microbes 2015, 6, 45–52. [Google Scholar] [CrossRef]
- Li, S.; He, Y.; Mann, D.A.; Deng, X. Global spread of Salmonella Enteritidis via centralized sourcing and international trade of poultry breeding stocks. Nat. Commun. 2021, 12, 5109. [Google Scholar] [CrossRef]
- Calenge, F.; Lecerf, F.; Demars, J.; Feve, K.; Vignoles, F.; Pitel, F.; Vignal, A.; Velge, P.; Sellier, N.; Beaumont, C. QTL for resistance to Salmonella carrier state confirmed in both experimental and commercial chicken lines. Anim. Genet. 2009, 40, 590–597. [Google Scholar] [CrossRef]
- Patsias, A.; Chouliara, I.; Badeka, A.; Savvaidis, I.N.; Kontominas, M.G. Shelf-life of a chilled precooked chicken product stored in air and under modified atmospheres: Microbiological, chemical, sensory attributes. Food Microbiol. 2006, 23, 423–429. [Google Scholar] [CrossRef]
- Geornaras, I.; de Jesus, A.E.; von Holy, A. Bacterial populations associated with the dirty area of a South African poultry abattoir. J. Food Prot. 1998, 61, 700–703. [Google Scholar] [CrossRef] [PubMed]
- Russell, S.M. Salmonella reduction calls for multi-hurdle approach. WATT Poult. USA. 2010, 15487544. [Google Scholar]
- Scott, B.R.; Yang, X.; Geornaras, I.; Delmore, R.J.; Woerner, D.R.; Reagan, J.O.; Morgan, J.B.; Belk, K.E. Antimicrobial Efficacy of a Sulfuric Acid and Sodium Sulfate Blend, Peroxyacetic Acid, and Cetylpyridinium chloride against Salmonella on Inoculated Chicken Wings. J. Food Prot. 2015, 78, 1967–1972. [Google Scholar] [CrossRef]
- Smith, J.; Corkran, S.; McKee, S.R.; Bilgili, S.F.; Singh, M. Evaluation of post-chill applications of antimicrobials against Campylobacter jejuni on poultry carcasses. J. Appl. Poult. Res. 2015, 24, 451–456. [Google Scholar] [CrossRef]
- Bolton, D.J.; Meredith, H.; Walsh, D.; McDowell, D.A. The effect of chemical treatments in laboratory and broiler plant studies on the microbial status and shelf-life of poultry. Food Control. 2014, 36, 230–237. [Google Scholar] [CrossRef]
- Hinton, A.; Northcutt, J.K., Jr.; Smith, D.P.; Musgrove, M.T.; Ingram, K.D. Spoilage microflora of broiler carcasses washed with electrolyzed oxidizing or chlorinated water using an inside-outside bird washer. Poult. Sci. 2007, 86, 123–127. [Google Scholar] [CrossRef]
- Wideman, N.; Bailey, M.; Bilgili, S.F.; Thippareddi, H.; Wang, L.; Bratcher, C.; Sanchez-Plata, M.; Singh, M. Evaluating best practices for Campylobacter and Salmonella reduction in poultry processing plants. Poult. Sci. 2016, 95, 306–315. [Google Scholar] [CrossRef] [PubMed]
- Kim, Y.Y.; Kil, D.Y.; Oh, H.K.; Han, I.K. Acidifier as an alternative material to antibiotics in animal feed. Asian-Australas. J. Anim. Sci. 2005, 18, 1048–1060. [Google Scholar] [CrossRef]
- Dittoe, D.K.; Ricke, S.C.; Kiess, A.S. Organic acids and potential for modifying the avian gastrointestinal tract and reducing pathogens and disease. Front. Vet. Sci. 2018, 5, 216. [Google Scholar] [CrossRef]
- Ryan, D.; Ojha, U.K.; Jaiswal, S.; Padhi, C.; Suar, M. The small RNA DsrA influences the acid tolerance response and virulence of Salmonella enterica serovar Typhimurium. Front. Microbiol. 2016, 7, 599. [Google Scholar] [CrossRef]
- Madushanka, D.N.N.; Jayaweera, T.S.P.; Jayasinghe, J.M.C.S.; Yasawathie, D.G.; Ruwandeepika, H.A.D. Decontaminating effect of organic acids and natural compounds on broiler chicken meat contaminated with Salmonella typhimurium. Asian Food Sci. J. 2018, 3, 1–9. [Google Scholar] [CrossRef]
- Eltholth, M.M.; Mohamed, R.A.; Elgohary, F.A.; Abo Elfadl, E.A. Assessment of biosecurity practices in broiler chicken farms in Gharbia Governorate, Egypt. Alex. J. Vet. Sci. 2016, 49, 68. [Google Scholar] [CrossRef]
- Aiyedun, J.O.; Oludairo, O.O.; Olorunsola, I.D.; Daodu, O.B.; Furo, N.A. Effectiveness of biosecurity measures in some selected farms in Kwara state, Nigeria. J. Res. For. Wildl. Environ. 2018, 10, 17–23. [Google Scholar]
- Conan, A.; Goutard, F.L.; Sorn, S.; Vong, S. Biosecurity measures for backyard poultry in developing countries: A systematic review. BMC Vet. Res. 2012, 8, 240. [Google Scholar] [CrossRef]
- Kouam, M.K.; Jacouba, M.; Nsangou, I.N.; Teguia, A. Assessment of biosecurity level in small-scale broiler farms in the Western highlands of Cameroon (Central Africa). Trop. Anim. Health Prod. 2018, 50, 1529–1538. [Google Scholar] [CrossRef]
- Wijesinghe, W.M.J.B.; De Silva, P.G.J.C.; Gunaratne, S.P. Evaluation of biosecurity status in commercial broiler farms in Sri Lanka. Int. J. Sci. Res. Publ. 2017, 7, 114–119. [Google Scholar]
- Fouladkhah, A. The Need for evidence-based outreach in the current food safety regulatory landscape. J. Ext. 2017, 55, 20. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Raut, R.; Maharjan, P.; Fouladkhah, A.C. Practical Preventive Considerations for Reducing the Public Health Burden of Poultry-Related Salmonellosis. Int. J. Environ. Res. Public Health 2023, 20, 6654. https://doi.org/10.3390/ijerph20176654
Raut R, Maharjan P, Fouladkhah AC. Practical Preventive Considerations for Reducing the Public Health Burden of Poultry-Related Salmonellosis. International Journal of Environmental Research and Public Health. 2023; 20(17):6654. https://doi.org/10.3390/ijerph20176654
Chicago/Turabian StyleRaut, Rabin, Pramir Maharjan, and Aliyar Cyrus Fouladkhah. 2023. "Practical Preventive Considerations for Reducing the Public Health Burden of Poultry-Related Salmonellosis" International Journal of Environmental Research and Public Health 20, no. 17: 6654. https://doi.org/10.3390/ijerph20176654