Abstract
Salmonella spp. are bacteria that cause salmonellosis, a common form of foodborne illness with major impact on human health and huge financial losses in poultry industry. The incidence of notified cases of salmonellosis has declined from a peak of 24 per 100,000 in 2009 to 20.4 reported cases per 100,000 population in 2013, with S. enteritidis and S. typhimurium being the most commonly reported serovar in EU. Salmonella spp. has been detected in a range of foods, and outbreaks have predominantly been associated with animal products such as eggs, poultry and dairy products, but also with plant origin food such as salad dressing, fruit juice and sesame. At the time of slaughter, Salmonella-infected poultry may have high numbers of organisms in their intestines as well as on the outside of the bird and are therefore an important source of contamination. Nowadays, food safety has become an important concern for the European society and governments; therefore, more strict and harmonized regulations are being implemented throughout the poultry production chain with the aim to guarantee and increase the consumer confidence in foodstuffs of animal origin. Furthermore, increasing antimicrobial resistance in non-typhoid Salmonella species has been a serious problem for public health worldwide.
Keywords
- salmonellosis
- foodborne
- prevalence
- poultry
- antibiotic resistance
1. Introduction
2. Salmonella species classification
The bacteria of the genus
A few serotypes are host specific; i.e.
3. Transmission routes, public health and economic cost associated with Salmonella infection
The gastrointestinal tracts of humans and animals are the primary sources of
Transovarian (vertical transmission) or trans-shell (horizontal transmission) occurs in poultry. In the first case, a contamination of the vitelline membrane, albumen and possibly the yolk of eggs occurs. Following this route,
Plant origin material can be contaminated through direct deposition of
Person-to-person transmission of
Non-typhoidal
In the latest EFSA’s report, a total of 82,694 confirmed salmonellosis cases were reported by 27 European Union (EU) member states in 2013, resulting in an EU notification rate of 20.4 cases per 100,000 population [11].
A decrease of 7.9% in the EU notification rate compared with 2012 was shown in the above report, which supports the declining trend of salmonellosis in the EU/European Economic Area (EEA) in the 5-year period of 2009–2013 (Figure 1). However, the above was not statistically significant when analysed by month. Nine out of 14 EU member states reported a total of 59 fatal cases, which gave an EU case-fatality rate of 0.14% among the 40,976 confirmed cases. Some researchers claim that human salmonellosis represents a considerable economic impact and the estimated costing can be as €3 billion/year [34]. As in previous years,
In a recent report published by USDA in 2015 [35], a comparison of the economic burden showed that
According to Decision No. 2119/98/EC and 2000/96/EC, surveillance of foodborne salmonellosis in humans is mandatory in the EU member states as well as setting up a network for the epidemiological surveillance and control of communicable diseases in the Community [36, 37]. Data on humans, animals and food are compiled and analysed jointly by the European Food Safety Agency (EFSA) and the European Centre for Disease Prevention and Control (ECDC) and presented annually in the EU Summary Report on trends and sources of zoonoses, zoonotic agents and foodborne outbreaks [37].
4. Salmonella spp. in poultry and poultry products
In the primary production, there are numerous activities that influence the introduction, growth or elimination of
The Panel on Biological Hazards [42] recommended that the application of hazard analysis critical control point (HACCP) principles, including good manufacturing practices and general hygiene procedures are recognized as important measures for
Nowadays, the trend seems to be towards production becoming more integrated, and many small farms will be replaced in the future by fewer, bigger farms, which will allow a greater integration and consequently to a better control of
Sewage and farm effluents, which can contaminate pasture, soil and water with
5. Primary and secondary poultry processing and retail
The most important control measure at primary production, apart from those focusing in the elimination of
To reduce carcass contamination, decontamination measures can be applied. Many countries after the adoption of the ‘Code of hygienic practice recommended for poultry processing’ by the Codex Alimentarius in 1994, adopted their own code of practices for poultry processing. The requirements for cleaning of de-feathering equipment and recommended list of used disinfectants and practices of physical separation of de-feathering from later primary processing steps, requirements for processors to define acceptable levels of visible faecal contamination following evisceration and monitoring requirements for faecal contamination and practices of spaying or rinsing/dipping are included in this code. As far as these decontamination measures is concerned, one should take into consideration that, there are some regional differences, since chemical treatment is not accepted in the EU at the moment, but is widely used in other parts of the world, e.g. in the USA and New Zealand.
Poultry secondary processing includes portioning and processing of carcasses or portions into value-added products. During secondary processing,
In a New Zealand consumer survey, the times and temperatures of purchased poultry products during transportation by consumers were examined [58]. It showed that thawing poultry at room temperature for up to 12 hours was a common practice and that any
The detection of
Furthermore, interventions at the processing stages are assessed using growth models. These take into consideration several factors such as the levels of contamination when carcasses leave the processing plant, storage time in retail stores, transport time, storage times in homes and the temperatures carcasses were exposed to during each of these periods. It should be mentioned that the presence and level of
6. Food of animal and plant origin as a source of Salmonella serovars for humans
Both plant and animal product-based animal feed ingredients may be contaminated with
In the European Union (EU), contaminated foodstuffs serving as a source of
A long list of foods that have been contaminated by
In foods from vegetable origin, detection of
In 2002, tomatoes, grown and packed in Virginia state (USA), contaminated with
Unpasteurized orange juice was responsible for foodborne salmonellosis in 152 people in six states in the USA between May and July 2005 [77]. From 1995 to 2005, some researchers reviewed fruit juice-associated outbreaks of illness reported to Centres for Disease Control and Prevention (CDC), in Atlanta, USA [78]. Twenty-one juice-associated outbreaks were reported to CDC; 10 implicated apple juice or cider, eight were linked to orange juice and three implicated other types of fruit juice. These outbreaks caused 1366 illnesses, with an average of 21 cases per outbreak (range, 2–398 cases). Five out of 13 outbreaks of known aetiology, were caused by
Human salmonellosis due to
7. Antibiotic resistance in Salmonella serovars: a serious problem in public health
Since 2003, according to the U.S. Food and Drug Administration, antimicrobial resistance in
Individual organisms may transfer mutations that render antibiotics ineffective, passing on a survival advantage to the mutated strain, resulting in a normal genetic variation in bacterial populations. Advantageous mutations can also be conveyed via plasmid exchange within the bacterial colony, in the presence of antibiotics, resulting in proliferation of the resistance trait in the bacterial populations. Natural selection leads to an inherent consequence of exposure to antibiotic compounds and then antibiotic resistance arises.
On the other hand, the spread of particularly resistant clones and the occurrence of resistance genes within these clones can be exacerbated by the use of antimicrobials in human and animal populations and its selective pressure [81]. Many factors may also influence the spread of resistant clones, such as foreign travel by humans, international food trade, animal movements, farming systems, animal husbandry and the pyramidal structure of some types of animal primary production. During the late 1990s and early 2000s, several clones of multi-drug-resistant (MDR)
2013/652/EU Commission Decision sets an enhanced monitoring of antibiotic resistance (AMR) in bacteria from food and food-producing animals, which has been successfully implemented in all reporting and non-reporting member states. In accordance with the above legislation, the AMR monitoring started in 2014 and collected data referred on food and food-producing animals specifically targeted in different poultry populations and meat derived thereof. Two agents are responsible in performing the analyses of the data: EFSA and ECDC. The results are published in the first EU Summary Report on AMR [81] derived from 28 member states which reported data on AMR in zoonotic bacteria to the EFSA and 21 member states which submitted data to the ECDC. In the above report, the results showed that high proportions of human
In another study [85], it was reported that over 80% of strains from both human and animal sources that were tested for their antimicrobial resistance, showed that resistance patterns were similar among strains from humans and animals: the commonest phenotype comprised resistance to ampicillin, sulphonamides, streptomycin, chloramphenicol, and tetracycline and was found in 76% of human and 73% of animal strains. Between 1972 and 1974, almost 50,000
Overall, antimicrobial resistance varies among different serotypes of non-typhoidal
References
- 1.
Coburn B, Grassl GA, Finlay BB. Salmonella, the host and disease: a brief review. Immunol Cell Biol. 2007; 85: 112–118. DOI: 10.1038/sj.icb.7100007 - 2.
Majowicz S, Musto J, Scallan E, Angulo F, Kirk M, O'Brien S, Jones T, Fazil A, Hoekstra R. The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis. 2010;50: 882–889. - 3.
EFSA. Report of the Task Force on Zoonoses Data Collection on the analysis of the baseline survey on the prevalence of Salmonella in turkey flocks, in the EU, 2006–2007. Part A:Salmonella prevalence estimates. EFSA J. 2008;134: 1–91. - 4.
Vargas-Galindo Á. Probabilistic inversion in priority setting of food borne pathogens [MSc thesis]. Delft University of Technology: Department of Applied Mathematics and Risk Analysis; 2007 - 5.
Popoff MY, Le Minor L. Antigenic formulas of the Salmonella serovars, 8th ed. WHO Collaborating Centre for Reference and Research on Salmonella, Institute Pasteur, Paris, France; 2001 - 6.
Porwollik S, Boyd EF, Choy C, Cheng P, Florea L, Proctor E, McClelland M. Characterization of Salmonella enterica subspecies I genovars by use of microarrays. J Bacteriol. 2004; 186: 5883–5898. - 7.
Brenner F, Villar R, Angulo F, Tauxe R, Swaminathan B. Salmonella nomenclature. J Clin Microbiol. 2000;38: 2465–2467. - 8.
Jay LS, Davos D, Dundas M, Frankish E, Lightfoot D. Salmonella. In: Hocking AD (ed). Foodborne microorganisms of public health significance. 6th ed, Australian Institute of Food Science and Technology (NSW Branch), Sydney; 2003; pp. 207–266. - 9.
Gast RK. Salmonella infections. In: Swayne DE, Glisson JR, McDougald LR, Nolan LK, Suarez DL, Nair VL (eds). Diseases of Poultry. 13th ed, Ames, IA: John Wiley and Sons Inc.; 2013; pp. 677–736. ISBN: 978-0-470-95899-5. - 10.
Allison MJ, Dalton HP, Escobar MR, Martin CJ. Salmonella choleraesuis infections in man: a report of 19 cases and a critical literature review. South Med J. 1969;62: 593–596. - 11.
EFSA. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2013 Scientific Report of EFSA and ECDC. EFSA J. 2015; 13(1): 3991. - 12.
Castagna SMF, Schwartz P, Canal CW, Cardoso M. Presence of Salmonella sp. in the intestinal tract and tonsils/mandibular lymph nodes in pigs at slaughter. Arq Brasil Med Veter Zoo. 2004; 56(3): 300–306 DOI: 10.1590/S0102-09352004000300003 - 13.
Shimoni Z, Pitlik's K, Leibovici L. Nontyphoidal salmonella bacteremia: age-related differences in clinical presentation, bacteriology, and outcome. Clin Infect Dis. 1999; 28: 822–7. - 14.
De Jong B, Ekdahl K. Human salmonellosis in travellers is highly correlated to the prevalence of Salmonella in laying hen flocks. Eurosurveillance. 2006; 11: E060706.1. - 15.
Bell C, Kyriakides A. Salmonella : a practical approach to the organism and its control in foods. Oxford: Blackwell Science; 2002. - 16.
FAO/WHO. Risk assessments of Salmonella in eggs and broiler chickens (Microbiological Risk Assessment Series 2). Food and Agriculture Organization of the United Nations/World Health Organization. 2002. Available from: http://www.who.int/foodsafety/publications/micro/en/salmonella.pdf - 17.
CCFH. Food safety risk profile for Salmonella species in broiler (young) chickens. Codex Committee on Food Hygiene Working Group on guidelines for control ofCampylobacter andSalmonella species in broiler (young bird) chicken meat. 2007. Available from: http://www.foodsafety.govt.nz/elibrary/industry/Food_Safety_Risk-Compiled_Ccfh.pdf. - 18.
Poppe C. Salmonella infections in the domestic fowl. In: Wray C, Wray A (eds).Salmonella in domestic animals. Oxon, United Kingdom: CABI Publishing; 2000;107–132. - 19.
Gast RK, Guraya R, Jones DR, Anderson KE. Persistence of fecal shedding of Salmonella enteritidis by experimentally infected laying hens housed in conventional or enriched cages. Poult Sci. 2015;94: 1650–1656. http://dx.doi.org/10.3382/ps/pev113 - 20.
Davies RH, Wray C. Persistence of Salmonella enteritidis in poultry units and poultry food. Br Poult Sci. 1996;37(3): 589–96. - 21.
Santos RL, Zhang S, Tsolis RM, Baumler AJ, Adams LG. Morphologic and molecular characterization of Salmonella typhimurium infection in neonatal calves. Vet Pathol. 2002; 39: 200–215. - 22.
Jones BD. Salmonella invasion gene regulation: a story of environmental awareness. J Microbiol. 2005; 43: 110–117. - 23.
Solari CA, Mandarino JR, Panizzutti MHM, Farias RHG. A new serovar and a new serological variant belonging to Salmonella enterica subspecies diarizonae. Mem Inst Oswaldo Cruz. 2003; 98(4) . http://dx.doi.org/10.1590/S0074-02762003000400013 - 24.
Hidalgo-Vila J, Díaz-Paniagua C, de Frutos-Escobar C, Jiménez-Martínez C, Pérez-Santigosa N. Salmonella in free living terrestrial and aquatic turtles. Vet Microbiol. 2007; 119: 311–315. - 25.
Foster JW, Spector MP. How Salmonella survive against the odds. Annu Rev Microbiol. 1995; 49: 145–74. - 26.
Turpin PE, Maycroft KA, Rowlands CL, Wellington EMH. Viable but non-culturable Salmonellas in soil. J Appl Bacteriol. 1993; 74: 421–427. - 27.
Mannion C, Lynch PB, Egan J, Leonard FC. Seasonal effects on the survival characteristics of Salmonella Typhimurium and Salmonella Derby in pig slurry during storage. J Appl Microbiol. 2007; 103(5): 1386–1392. - 28.
Heaton JC, Jones K. Microbial contamination of fruit and vegetables and the behaviour of enteropathogens in the phyllosphere: a review. J Appl Microbiol. 2008; 104(3): 613–626. - 29.
Loewenstein M. An outbreak of salmonellosis propogated by person-to-person transmission on an Indian reservation. Am J Epidemiol. 1974; 102: 257–262. - 30.
Pether J, Scott R. Salmonella carriers: are they dangerous? A study to identify finger contamination withSalmonella by convalescent carriers. J Infect. 1982;5: 81–88. - 31.
Dryden MS. Asymptomatic foodhandlers as the source of nosocomial salmonellosis. J Hosp Infect. 1994; 28: 195–208. - 32.
Stein-Zamir C, Tallen-Gozani E, Abramson N, Shoob H, Yishai R, Agmon V, Reisfeld A, Valinsky L, Marva E. Salmonella enterica outbreak in a banqueting hall in Jerusalem: the unseen hand of the epidemiological triangle? Israel Med Assoc J. 2009;11: 94–97. - 33.
Kendall ME, Crim S, Fullerton K, Han PV, Cronquist AB, Shiferaw B. Travel-associated enteric infections diagnosed after return to the United States, Foodborne Diseases Active Surveillance Network (FoodNet), 2004–2009. Clin Infect Dis. 2012; 54(Suppl 5): S480–S487. - 34.
Havelaar AH, Ivarsson S, Löfdahl M, Nauta MJ. Estimating the true incidence of campylobacteriosis and salmonellosis in the European Union, 2009. Epidemiol Infect. 2013; 141(2): 293–302. - 35.
Hoffmann S, Maculloch B, Batz M. Economic burden of major foodborne illnesses acquired in the United States. In: Economic Research Service Economic Information Bulletin; Number 140, May 2015; pp.33; United States Department of Agriculture (USDA ). Available from: https://www.ers.usda.gov/webdocs/publications/eib140/52806_eib140_summary.pdf - 36.
Commission Decision No. 2119/98/EC of the European Parliament and of the Council of 24 September 1998 setting up a network for the epidemiological surveillance and control of communicable diseases in the community. O J L. 1998;268:1–6. - 37.
Commission Decision No. 2000/96/EC of 22 December 1999 on the communicable diseases to be progressively covered by the community network under Decision No. 2119/98/EC of the European Parliament and of the Council. O J L. 2000;28:50–53. - 38.
Rose N, Beaudeau F, Drouin P, Toux J, Rose V, Colin P. Risk factors for Salmonella enterica subsp.enterica contamination in French broiler-chicken flocks at the end of the rearing period. Prevent Vet Med. 1999;39: 265–277. - 39.
Marin C, Balasch S, Vega S, Lainez M. Sources of Salmonella contamination during broiler production in Eastern Spain. Prevent Vet Med. 2011; 98: 39–45. - 40.
Arsenault J, Letellier A, Quessy S, Normand V, Boulianne M. Prevalence and risk factors for Salmonella spp. and Campylobacter spp. caecal colonization in broiler chicken and turkey flocks slaughtered in Quebec, Canada. Prevent Vet Med. 2007; 81: 250–264. - 41.
Denagamage T, Jayarao B, Patterson P, Wallner-Pendleton E, Kariyawasam S. Risk factors associated with Salmonella in laying hen farms: systematic review of observational studies. Avian Dis. 2015; 59(2): 291–302. DOI: 10.1637/10997-120214-Reg - 42.
EFSA. Scientific opinion on microbiological risk assessment in feeding stuffs for food-producing animals. Scientific opinion of the panel on biological hazards. EFSA J. 2008; 720: 1–84. - 43.
Directive 2003/99/EC of the European Parliament and of the Council of 17 November 2003 on the monitoring of zoonoses and zoonotic agents, amending Council Decision 90/424/EEC and repealing Council Directive 92/117/EEC. O J L. 2003;325:31–40. - 44.
Fernanda DC, Cole DJ, Hofacre C, Zamperini K, Mathis D, Doyle MP, Lee MD, Maurer JJ. Effect of Salmonella vaccination of breeder chickens on contamination of broiler chicken carcasses in integrated poultry operations. Appl Environ Microbiol. 2010;76(23): 7820–7825. DOI:10.1128/AEM.01320-10 DOI:10.1128%2FAEM.01320-10#pmc_ext - 45.
Papatsiros VG, Katsoulos PD, Koutoulis KC, Karatzia M, Dedousi A, Christodoulopoulos G. Alternatives to antibiotics for farm animals. CAB Rev. 2013; 8: 32 - 46.
Roth N. The use of acidifiers in controlling Salmonella. Poultry World. 2012; Dec 31. Available from: http://www.poultryworld.net/Health/Articles/2012/12/The-use-of-acidifiers-in-controlling-Salmonella-1136075W/ - 47.
Young I, Rajic A, Wilhelm BJ, Waddell L, Parker S, McEwen SA. Comparison of the prevalence of bacterial enteropathogens, potentially zoonotic bacteria and bacterial resistance to antimicrobials in organic and conventional poultry, swine and beef production: a systematic review and meta-analysis. Epidemiol Infect. 2009; 137: 1217–1232. - 48.
Mulder RWAW. Impact of transport and related stresses on the incidence and extent of human pathogens in pigmeat and poultry. J Food Safety. 1995; 15(3): 239–246. - 49.
Corry JEL, Allen VM, Hudson WR, Breslin MF, Davies RH. Sources of Salmonella on broiler carcasses during transportation and processing: modes of contamination and methods of control. J Appl Microbiol. 2002;92(3): 424–432. - 50.
Marin C, Lainez M. Salmonella detection in feces during broiler rearing and after live transport to the slaughterhouse. Poult Sci. 2009;88(9): 1999–2005. - 51.
Lillard H. The impact of commercial processing procedures on the bacterial contamination and cross-contamination of broiler carcasses. J Food Protect. 1990; 53(3): 202–204. - 52.
Lake R, Hudson A, Cressey P, Bayne G, Turner N. Quantitative risk model: Salmonella spp. in the poultry food chain. In: ESR Client Report FW0546. ESR, Christchurch; 2005. - 53.
EFSA. Scientific opinion on the public health risks related to the maintenance of the cold chain during storage and transport of meat. Part 2 (minced meat from all species). EFSA Panel on Biological Hazards (BIOHAZ). EFSA J . 2014; 12(7): 3783. - 54.
ICMSF. Microorganisms in Foods 6: Microbial Ecology of Food Commodities. 2nd edition. International Commission on Microbiological Specifications for Foods (ICMSF). New York: Kluwer Academic & Plenum Publishers; 2005; pp108. ISBN: 0-306-48675-X. - 55.
Abu Ruwaida AS, Sawaya WN, Baroon ZH, Murad M, Terry WR. Shelf life and microbiological quality of eviscerated broiler carcasses in the State of Kuwait. Arab Gulf J Sci Res. 1996; 14: 363–381. - 56.
King N, Wong T. Feasibility study: trace back of fresh poultry portions sold at retail. In: ESR Client Report FW10056. Christchurch: ESR; 2010. - 57.
Dominguez SA, Schaffner DW. Survival of Salmonella in processed chicken products during frozen storage. J Food Protect. 2009;72: 2088–2092. - 58.
Gilbert S, Bayne G, Wong T, Lake R, Whyte R. Domestic food practices in New Zealand. 2005–2006 project report. In: ESR Client Report FW0640. Christchurch: ESR; 2006. - 59.
Gilbert S, Whyte R, Bayne G, Paulin S, Lake R, van der Logt P. Survey of domestic food handling practices in New Zealand. Int J Food Microbiol. 2007; 117: 306–311. - 60.
McIntyre L, Bayne G, Gilbert S, Lake R. Domestic food practices in New Zealand. Freezer survey. In: ESR Client Report FW0735. Christchurch: ESR; 2007. Available from: http://foodsafety.govt.nz/elibrary/industry/Domestic_Food_Practices-Baseline_Information.pdf - 61.
CAC. Report of the forty-second session of the Codex Committee on Food Hygiene, Kampala, Uganda, 29 November–3 December 2010. Codex Alimentarius Commission. Available from: https://ec.europa.eu/food/sites/food/files/safety/docs/codex_ccfh_42_agenda-item_04.pdf - 62.
Anonymous. Outbreak of Salmonella Enteritidis 9a, Auckland, April-May 2005 (an internal report provided by Public Health Services). - 63.
Hess IM, Neville LM, McCarthy R, Shadbolt CT, McAnulty JM. A Salmonella Typhimurium 197 outbreak linked to the consumption of lambs' liver in Sydney, NSW. Epidemiol Infect. 2008; 136(4): 461–467. - 64.
Jansen A, Frank C, Stark K. Pork and pork products as a source for human salmonellosis in Germany. Berliner und Münchener tierärztliche Wochenschrift. 2007; 120(7-8): 340–346. - 65.
Luzzi I, Galetta P, Massari M, Rizzo C, Dionisi AM, Filetici E, Cawthorne A, Tozzi A, Argentieri M, Bilei S, Busani L, Gnesivo C, Pendenza A, Piccoli A, Napoli P, Loffredo L, Trinito MO, Santarelli E, Ciofi degli Atti ML. An Easter outbreak of Salmonella Typhimurium DT 104A associated with traditional pork salami in Italy. Euro Surveill. 2007; 12(4): 11–12. - 66.
Haeghebaert S, Duché L, Gilles C, Masini B, Dubreuil M, Minet JC, Bouvet P, Grimont F, Delarocque Astagneau E, Vaillant V. Minced beef and human salmonellosis: review of the investigation of three outbreaks in France. Euro Surveill. 2001; 6(2): 21–26 - 67.
Little CL, Richardson JF, Owen RJ, de Pinna E, Threlfall EJ. Campylobacter and Salmonella in raw red meats in the United Kingdom: prevalence, characterization and antimicrobial resistance pattern, 2003–2005. Food Microbiol. 2008; 25(3): 538–543. - 68.
EFSA. Panels on Biological Hazards (BIOHAZ), on Contaminants in the Food Chain (CONTAM) and on Animal Health and Welfare (AHAW), 2012. Scientific Opinion on the public health hazards to be covered by inspection of meat (poultry). EFSA J. 2012; 10(6): 2741 (179 pp.). DOI:10.2903/j.efsa.2012.2741 - 69.
EFSA (European Food Safety Authority) and ECDC (European Centre for Disease Prevention and Control). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2012. EFSA J. 2014; 12(2): 3547 (312 pp.). DOI:10.2903/j.efsa.2013.3129 - 70.
EFSA. Panel on Biological Hazards (BIOHAZ). Scientific opinion on an estimation of the public health impact of setting a new target for the reduction of Salmonella in turkeys. EFSA J. 2012; 10(4): 2616 (89 pp). DOI: 10.2903/j.efsa.2012.2616 - 71.
Scanga JA, Grona AD, Belk KE, Sofos JN, Bellinger GR, Smith GC. Microbiological contamination of raw beef trimmings and ground beef. Meat Sci. 2000; 56: 145–152. - 72.
James C, James S. Quantification of the controls that should be placed on meat prior to mincing. FSA (Food Standards Agency) Project: M01054. 2012; Available from: http://www.foodbase.org.uk//admintools/reportdocuments/876-1-1619_M01054.pdf - 73.
Unicomb LE, Simmons G, Merritt T, Gregory J, Nicol C, Jelfs P, Kirk M, Tan A, Thomson R, Adamopoulos J, Little CL, Currie A, Dalton CB. Sesame seed products contaminated with Salmonella: three outbreaks associated with tahini. Epidemiol Infect. 2005; 133: 1065–1072. - 74.
Kretsinger K, Noviello S, Moll M. Tomatoes sicken hundreds: multistate outbreak of Salmonella Newport. In: Proceedings of the 52nd Annual Epidemic Intelligence Service Conference; 2003; Atlanta, Georgia, USA. - 75.
CDC. National antimicrobial resistance monitoring system for enteric bacteria (NARMS): human isolates final report, 2007. Atlanta, GA: U.S. Department of Health and Human Services, CDC, 2009. Available from: http://www.cdc.gov/narms/annual/2007/NARMSAnnualReport2007.pdf - 76.
Greene SK, Daly ER, Talbot EA, Demma LJ, Holzbauer S, Patel NJ, Hill TA, Walderhaug MO, Hoekstra RM, Lynch MF, Painter JA. Recurrent multistate outbreak of Salmonella Newport associated with tomatoes from contaminated fields, 2005. Epidemiol Infect. 2008; 136(2): 157–165. - 77.
Jain S, Bidol SA, Austin JL, Berl E, Elson F, Lemaile-Williams M, Deasy M 3rd, Moll ME, Rea V, Vojdani JD, Yu PA, Hoekstra RM, Braden CR, Lynch MF. Multistate outbreak of Salmonella Typhimurium and Saintpaul infections associated with unpasteurized orange juice—United States, 2005. Clin Infect Dis. 2009; 48(8): 1065–1071. - 78.
Vojdani JD, Beuchat LR, Tauxe RV. Juice-associated outbreaks of human illness in the United States, 1995 through 2005. J Food Prot. 2008; 71(2): 356–364. - 79.
Nygård K, Lassen J, Vold L, Andersson Y, Fisher I, Löfdahl S, Threlfall J, Luzzi I, Peters T, Hampton M, Torpdahl M, Kapperud G, Aavitsland P. Outbreak of Salmonella Thompson infections linked to imported rucola lettuce. Foodborne Pathog Dis. 2008; 5(2): 165–173. - 80.
Little CL, Gillespie IA. Prepared salads and public health. J Appl Microbiol. 2008; 105(6): 1729–1743. DOI: 10.1111/j.1365-2672.2008.03801.x. Epub 2008 Apr 4. - 81.
EFSA. The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food. EFSA J. 2016; 14(2): 4380. - 82.
European Centre for Disease Prevention and Control (ECDC), European Food Safety Authority (EFSA), European Drugs Agency (EMEA), Scientific Committee on Emerging and Newly Identified Health Risks (SCENIHR). Joint opinion on antimicrobial resistance (AMR) focused on zoonotic infections. EFSA J. 2009; 7(11): 1372. Available from: http://www.ema.europa.eu/docs/en_GB/document_library/Other/2009/11/WC500015452.pdf - 83.
Chen S,Zhao S, White DG, Schroeder CM, Lu R, Yang H, McDermott PF, Ayers S, Meng J. Characterization of multiple-antimicrobial-resistant Salmonella serovars isolated from retail meats. Appl Environ Microbiol. 2004;70(1): 1–7. DOI:10.1128/AEM.70.1.1-7.2004 DOI:10.1128%2FAEM.70.1.1-7.2004#pmc_ext - 84.
Le Hello S, Bekhit A, Granier SA, Barua H, Beutlich J, Zając M, Münch S, Sintchenko V, Bouchrif B, Fashae K, Pinsard JL, Sontag L, Fabre L, Garnier M, Guibert V, Howard P, Hendriksen RS, Christensen JP, Biswas PK, Cloeckaert A, Rabsch W, Wasyl D, Doublet B, Weill FX. The global establishment of a highly-fluoroquinolone resistant Salmonella enterica serotype Kentucky ST198 strain. Front Microbiol. 2013; 4: 395. DOI:10.3389/fmicb.2013.00395 - 85.
Brisabois A, Cazin I, Breuil J, Collatz E. Surveillance of antibiotic resistance in Salmonella. Euro Surveill. 1997; 2 (3 ):pii=181. Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=181 - 86.
Voogd CE, van Leeuwen WJ, Guinée PA, Manten A, Valkenburg JJ. Incidence of resistance to ampicillin, chloramphenicol, kanamycin and tetracycline among Salmonella species isolated in the Netherlands in 1972, 1973 and 1974. Antonie van Leeuwenhoek. 1977; 43(3–4): 269–281. - 87.
NARMS report for human isolates final report. National Center for Emerging and Zoonotic Infectious Disease; 2013.