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      Preliminary Incidence and Trends of Infections with Pathogens Transmitted Commonly Through Food — Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 2016–2019

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          Abstract

          To evaluate progress toward prevention of enteric illnesses, the Foodborne Diseases Active Surveillance Network (FoodNet) of CDC’s Emerging Infections Program monitors the incidence of laboratory-diagnosed infections caused by eight pathogens transmitted commonly through food at 10 U.S. sites.* This report summarizes preliminary 2019 data and describes changes in incidence compared with that during 2016–2018. The incidence of enteric infections caused by these eight pathogens reported by FoodNet sites in 2019 continued to increase or remained unchanged, indicating progress in controlling major foodborne pathogens in the United States has stalled. Campylobacter and Salmonella caused the largest proportion of illnesses; trends in incidence varied by Salmonella serotype. Widespread adoption of whole genome sequencing (WGS) of bacteria has improved the ability to identify outbreaks, emerging strains, and sources of pathogens. To maximize the potential of WGS to link illnesses to particular sources, testing of isolates by clinical and public health laboratories is needed. Reductions in Salmonella serotype Typhimurium suggest that targeted interventions (e.g., vaccinating chickens and other food animals) might decrease human infections. Reducing contamination during food production, processing, and preparation will require more widespread implementation of known prevention measures and of new strategies that target particular pathogens and serotypes. Members of FoodNet conduct active, population-based surveillance for laboratory-diagnosed infections caused by Campylobacter, Cyclospora, Listeria, Salmonella, Shiga toxin-producing Escherichia coli (STEC), Shigella, Vibrio, and Yersinia at 10 sites covering approximately 15% of the U.S. population (an estimated 49 million persons in 2018). FoodNet is a collaboration of CDC, 10 state health departments, the U.S. Department of Agriculture’s Food Safety and Inspection Service (USDA-FSIS), and the Food and Drug Administration (FDA). Bacterial infections are defined as isolation of the bacteria from a clinical specimen by culture or detection of pathogen antigen, nucleic acid sequences, or, for STEC, † Shiga toxin or Shiga toxin genes, by a culture-independent diagnostic test (CIDT). § A CIDT-positive–only bacterial infection is a positive CIDT result not confirmed by culture. ¶ Listeria infections are defined as isolation of L. monocytogenes or detection of its nucleic acid sequences from a normally sterile site, or from placental or fetal tissue in the instance of miscarriage or stillbirth. Cyclospora infections are defined as detection of the parasite by microscopy using ultraviolet fluorescence or specific stains or by polymerase chain reaction. Cases with no documentation of international travel or unknown travel are considered domestically acquired infections.** The patient’s disposition at hospital discharge, or 7 days after specimen collection if not hospitalized, is attributed to the infection. Incidence per 100,000 population was calculated by dividing the number of infections in 2019 by the U.S. Census estimates of the surveillance area population for 2018. Incidence measures include all laboratory-diagnosed infections. A negative binomial model with 95% confidence intervals (CIs) was used to estimate change in incidence during 2019 compared with that during 2016–2018, adjusting for changes in the population over time; CIs not including zero were considered statistically significant. Analyses were performed using SAS statistical software (version 9.4; SAS Institute). Surveillance for physician-diagnosed post-diarrheal hemolytic uremic syndrome (HUS), a complication of STEC infection characterized by renal failure, thrombocytopenia, and microangiopathic anemia, is conducted by reviewing hospital discharge data and by working with a network of nephrologists and infection preventionists. This report includes HUS data for children for 2018, the most recent year for which data are available. Cases of Infection, Incidence, and Trends During 2019, FoodNet identified 25,866 cases of infection, 6,164 hospitalizations, and 122 deaths (Table 1). The overall incidence per 100,000 population was highest for Campylobacter (19.5), followed by Salmonella (17.1), STEC (6.3), Shigella (4.8), Cyclospora (1.5), Yersinia (1.4), Vibrio (0.9), and Listeria (0.3). The respective incidences were slightly lower for domestically acquired infections (Table 2). Eighty-six percent of infections were acquired domestically, ranging from 77% for Shigella to 96% for Listeria. TABLE 1 Number of laboratory-diagnosed bacterial and parasitic infections, hospitalizations, and deaths, incidence and percentage change compared with 2016–2018 average annual incidence rate, by pathogen —10 U.S. sites, Foodborne Diseases Active Surveillance Network,* 2016–2019 † Pathogen 2019 % Change in incidence from 2016–2018 to 2019 (95% CI)¶ No. of infections No. of hospitalizations (%) No. of deaths (%) Incidence§ Bacteria Campylobacter 9,731 1,988 (20) 26 (0.3) 19.5 13 (5 to 21) Salmonella 8,556 2,430 (28) 46 (0.5) 17.1 5 (−1 to 12) STEC 3,127 660 (21) 10 (0.3) 6.3 34 (14 to 58) Shigella 2,416 644 (27) 3 (0.1) 4.8 7 (−17 to 37) Yersinia 681 142 (21) 4 (0.6) 1.4 153 (102 to 217) Vibrio 466 131 (28) 12 (2.6) 0.9 79 (47 to 117) Listeria 134 131 (98) 21 (16) 0.3 1 (−19 to 27) Parasite Cyclospora 755 38 (5) 0 (0) 1.5 1,209 (708 to 2,020) Total 25,866 6,164 (24) 122 (0.5) N/A N/A Abbreviations: CI = confidence interval; N/A = not applicable; STEC = Shiga toxin-producing Escherichia coli. * Data collected from laboratories in Connecticut, Georgia, Maryland, Minnesota, New Mexico, Oregon, Tennessee, and selected counties in California, Colorado, and New York. † Data are preliminary. § Cases per 100,000 population. ¶ Percentage change reported as increase or decrease. CIs not including zero are statistically significant. TABLE 2 Number, percentage of all cases, and incidence of domestically acquired* laboratory-diagnosed bacterial and parasitic infections in 2019, by pathogen — 10 U.S. sites, Foodborne Diseases Active Surveillance Network, † 2019 § Pathogen Domestically acquired cases No. (% of all cases)¶ Incidence** Bacteria Campylobacter 8,264 (85) 16.5 Salmonella 7,677 (90) 15.4 STEC 2,514 (80) 5.0 Shigella 1,860 (77) 3.7 Yersinia 646 (95) 1.3 Vibrio 420 (90) 0.8 Listeria 129 (96) 0.3 Parasite Cyclospora 646 (86) 1.3 Total 22,156 (86) N/A Abbreviations: N/A = not applicable; STEC = Shiga toxin-producing Escherichia coli. * Includes patients who did not have international travel in the 30 days before illness onset for Listeria and Salmonella serotypes Typhi and Paratyphi; 15 days for Cyclospora; and 7 days for all other pathogens and patients for whom information on international travel was not available. Information on international travel was available for 79%–89% of patients with Campylobacter, Listeria, Salmonella, Shigella, Vibrio, and Yersinia infections, and for 90% or more of patients with Cyclospora and STEC infection. † Data collected from laboratories in Connecticut, Georgia, Maryland, Minnesota, New Mexico, Oregon, Tennessee, and selected counties in California, Colorado, and New York. § Data are preliminary. ¶ Denominator is all cases, including those for which information on international travel was not available. Among patients with travel information available, the percentages of domestically acquired cases were as follows: Campylobacter (81%), Cyclospora (84%), Listeria (95%), Salmonella (87%), Shigella (72%), STEC (78%), Vibrio (89%), and Yersinia (94%). ** Cases per 100,000 population. Compared with 2016–2018, the incidence in 2019 increased significantly for Cyclospora (1,209%), Yersinia (153%), Vibrio (79%), STEC (34%), and Campylobacter (13%) (Table 1). The number of bacterial infections diagnosed using a CIDT increased 32%, ranging from 18% for STEC to 253% for Listeria. The percentage of infections diagnosed only by CIDT, including specimens that were culture-negative and those not tested by culture, was highest for Yersinia (57%), followed by STEC (45%), Campylobacter (42%), Vibrio (41%), Shigella (40%), Salmonella (13%), and Listeria (1%). Overall, culture was attempted on 75% of positive bacterial CIDT results, ranging from 63% for Campylobacter to 100% for Listeria (Figure). FIGURE Number of infections diagnosed by culture or culture-independent diagnostic tests (CIDTs), by pathogen, year, and culture status — 10 U.S. sites, Foodborne Diseases Active Surveillance Network,* 2016–2019 † Abbreviation: STEC = Shiga toxin-producing Escherichia coli. * Data collected from laboratories in Connecticut, Georgia, Maryland, Minnesota, New Mexico, Oregon, Tennessee, and selected counties in California, Colorado, and New York. † Data for 2019 are preliminary. The figure is a series of bar charts showing the number of infections diagnosed by culture or culture-independent diagnostic tests, by pathogen, year, and culture status, identified by the Foodborne Diseases Active Surveillance Network at 10 U.S. sites during 2016–2019. Among 6,656 (90%) fully serotyped Salmonella isolates, the six most common serotypes were Enteritidis (2.6 per 100,000 population); Newport (1.4); Typhimurium (1.3); Javiana (1.1); I 4,[5],12:i:- (0.7); and Infantis (0.5). Compared with 2016–2018, incidence was significantly lower for Typhimurium (13% decrease; 95% CI = 1–24) and I 4,[5],12:i:- (28% decrease; 95% CI = 8–44); Infantis was significantly higher (69% increase; 95% CI = 31–118). Among 1,725 STEC isolates, most (397; 23%) were O157, followed by O103 (305; 18%), O26 (254; 15%), and O111 (175; 10%). The incidence of STEC O157 infections (0.8 per 100,000) decreased by 20% (95% CI = 3–34), compared with that during 2016–2018; the incidence of non-O157 STEC infections (2.7) increased by 35% (95% CI = 18–56). FoodNet identified 62 cases of post-diarrheal HUS in children (0.6 cases per 100,000) during 2018; 31 (50%) cases occurred in children aged <5 years (1.1 cases per 100,000). These rates were not significantly different from those during 2015–2017. Discussion In 2019, compared with the previous 3 years, the incidence of infections caused by pathogens transmitted commonly through food increased (for Campylobacter, Cyclospora, STEC, Vibrio, Yersinia) or remained unchanged (for Listeria, Salmonella, Shigella). These data indicate that Healthy People 2020 targets for reducing foodborne illness will not be met. The identification of infections that might not have been detected before adoption of CIDTs cannot explain this overall lack of progress. Better implementation of known prevention approaches and new strategies is needed to overcome the continued challenges to reducing foodborne illnesses. Serotype Enteritidis has been the most common cause of Salmonella infections at FoodNet sites since 2007 and incidence has not decreased. Eggs were the major source of Enteritidis infections in the 1980s ( 1 ). Chicken was recognized as another important source during the late 1990s ( 2 , 3 ). Infantis moved from the ninth most common Salmonella serotype among infected persons during 1996–1998 to the sixth most common in 2019. Many infections are now caused by a new, highly resistant strain found in chicken ( 4 , 5 ). The incidence of some serotypes has declined. Typhimurium moved from the most common serotype during 1996–1998 to the third most common in 2019. Heidelberg, the third most common serotype during 1996–1998, is no longer among the top 20. These decreases might be partly related to the widespread practice of vaccinating chickens against Typhimurium, which shares antigens with Heidelberg ( 6 ). This observation, combined with a marked decline in Enteritidis infections in the United Kingdom after implementation of widespread chicken vaccination and improved farm hygiene ( 7 ), suggests that targeting other serotypes through poultry vaccination could be one way to reduce human illnesses in the United States. Laboratory-diagnosed non-O157 STEC infections continue to increase. Although STEC O157 infections appear to be decreasing, outbreaks linked to leafy greens continue ( 8 ). Produce is also an important source for Cyclospora, Listeria, and Salmonella ( 9 , 10 ). Although adoption of syndromic panels †† could be contributing to the large increase in Cyclospora, increased exposure to this pathogen cannot be excluded. Continued implementation of FDA’s Produce Safety Rule §§ (e.g., expanded surveillance inspections of foreign and domestically grown produce) is needed, as are innovative approaches for preventing contamination. Advances in laboratory science continue to revolutionize enteric disease clinical diagnostics and surveillance. Many laboratories now use CIDTs to detect infections that would have previously been undiagnosed. In 2019, public health laboratories fully transitioned the standard subtyping method for clinical bacterial isolates from pulsed-field gel electrophoresis to WGS. WGS provides detailed information to more effectively recognize outbreaks, determine resistance patterns, and investigate reoccurring, emerging, and persisting strains. However, because CIDTs do not yield isolates needed to perform WGS, the full potential of these new technologies can only be realized when laboratories are fully able to culture CIDT-positive specimens. The findings in this report are subject to at least three limitations. First, part of the observed increase in incidence is likely due to increased use of CIDTs that identify previously unrecognized infections. Changes in clinicians’ ordering practices and varying test sensitivities and specificities might also contribute to this observation. Second, changes in health care–seeking behavior, access to health services, or other population characteristics might have changed. Finally, year-to-year changes in incidence might not reflect sustained trends. The landscape of foodborne disease continues to change, as do the methods to determine the incidence and sources of these infections. FoodNet surveillance data indicate that progress in controlling major foodborne pathogens in the United States has stalled. To better protect the public and achieve forthcoming Healthy People 2030 foodborne disease reduction goals, more widespread implementation of known prevention measures and new strategies that target particular pathogens and serotypes are needed. Summary What is already known about this topic? The incidence of most infections transmitted commonly through food has not declined for many years. What is added by this report? Incidence of infections caused by Listeria, Salmonella, and Shigella remained unchanged, and those caused by all other pathogens reported to FoodNet increased during 2019. Infections caused by Salmonella serotype Enteritidis, did not decline; however, serotype Typhimurium infections continued to decline. What are the implications for public health practice? New strategies that target particular serotypes and more widespread implementation of known prevention measures are needed to reduce Salmonella illnesses. Reductions in Salmonella serotype Typhimurium suggest that targeted interventions (e.g., vaccinating chickens and other food animals) might decrease human infections. Isolates are needed to subtype bacteria so that sources of illnesses can be determined.

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          Salmonella enterica serotype Enteritidis and eggs: a national epidemic in the United States.

          Beginning in the 1970s, the incidence of Salmonella enterica serotype Enteritidis (SE) infection and the number of related outbreaks in the United States has increased dramatically. By 1994, SE was the most commonly reported Salmonella serotype, with an incidence of >10 laboratory-confirmed infections per 100,000 population in the Northeast. Intensive epidemiologic and laboratory investigations identified shell eggs as the major vehicle for SE infection in humans, and that the eggs had been internally contaminated by transovarian transmission of SE in the laying hen. Three key interventions aimed at preventing the contamination and growth of SE in eggs have included farm-based programs to prevent SE from being introduced into egg-laying flocks, early and sustained refrigeration of shell eggs, and education of consumers and food workers about the risk of consuming raw or undercooked eggs. Since 1996, the incidence of SE infection in humans has decreased greatly, although many cases and outbreaks due to SE contaminated eggs continue to occur.
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            The “Decline and Fall” of Nontyphoidal Salmonella in the United Kingdom

            Nontyphoidal Salmonella species are important foodborne pathogens worldwide [1], causing diarrhea, vomiting, nausea, fever, and abdominal pain. Illness has been linked to a wide range of food items including eggs, chicken, beef, pork, salad vegetables, and dairy products, and other risk factors including overseas travel [2–7]. Outbreaks are fairly common [5]. The burden of illness, defined as morbidity and mortality, is substantial. In the United States, nontyphoidal Salmonella species are estimated to cause 1 million foodborne illnesses [8] and are the leading cause of death among foodborne bacterial pathogens [9]. Across the 27 member states of the European Union (EU), there were estimated to be 6.2 million cases of salmonellosis in 2009 [10]. In a population-based study in the United Kingdom (UK) in 2008–2009, there were >38 600 estimated cases and nearly 11 300 patients presenting to a primary care physician [11]. This represented a marked reduction in incidence compared with a similar study conducted more than a decade earlier [12, 13]. The purpose of this article is to discuss the factors associated with a substantial decline in nontyphoidal salmonellosis in the United Kingdom since the mid-1990s. A BRIEF HISTORY OF NONTYPHOIDAL SALMONELLOSIS IN THE UNITED KINGDOM Remarkable changes in the epidemiology of human nontyphoidal salmonellosis have occurred in the United Kingdom over the last century. Prior to 1942, the dominant foodborne salmonellas causing disease were Salmonella enterica subspecies enterica serovar Typhimurium, Salmonella Enteritidis, Salmonella Thompson, Salmonella Newport, Salmonella Bovismorbificans, and Salmonella Choleraesuis [14]. Salmonella Typhimurium remained the dominant serovar causing human disease for much of the 20th century, although there were fluctuations in other salmonellas in the “top 10” over time. For example, Salmonella Agona emerged as an important serovar in the 1960s following its introduction into pigs and poultry through contaminated fish meal imported from Peru [15]. Salmonella Hadar became the second most commonly isolated cause of human nontyphoidal salmonellosis in the mid-1970s when particular genetic lines of turkeys became infected [15]. Against this background, the incidence of Salmonella Enteritidis increased fairly gradually from around 150 to approximately 900 laboratory-confirmed cases per year between 1961 and 1980 [16]. During this time, phage type (PT) 8 dominated and was responsible for several turkey-associated outbreaks in the late 1960s [16]. By 1975 Salmonella Enteritidis was consistently the second or third most frequently isolated serovar annually [17]. Between 1981 and 1991, the incidence of nontyphoidal salmonellosis in the United Kingdom rose by >170% [18], driven primarily by an epidemic of Salmonella Enteritidis PT4 [16, 18–20] (Figure 1). In 1981 Salmonella Enteritidis accounted for approximately 10% of human Salmonella illnesses, but by 1993 this proportion had risen to nearly 70% [20]. In the early 1980s, PT4 overtook PT8 to become the predominant phage type in 1983, comprising 46% of isolations that year. By 1988 PT4 had risen to account for 81% of Salmonella Enteritidis strains isolated [16] and had ended the political career of a prominent government minister [21]. The United Kingdom was not alone; analysis of data submitted to the World Health Organization's Salmonella surveillance system showed that Salmonella Enteritidis in the late 1980s was increasing on several continents, with North America, South America, and Europe appearing to bear the brunt [22]. Figure 1. Laboratory reports of human Salmonella cases in the United Kingdom, 1981–2010. Abbreviations: CMO, Chief Medical Officer; PT, phage type. EVIDENCE THAT THE DECLINE IN SALMONELLA IS REAL Compelling evidence that the decline in Salmonella is real is derived from 3 sources. The first comprises 2 population-based prospective cohort studies of infectious intestinal disease (IID) in the community conducted more than a decade apart [11–13]. The primary outcome measures in both studies were estimates of the incidence of IID in the community, presenting to primary healthcare and reported to national surveillance. They were conducted using identical study designs and case definitions and employed similar microbiological methods, the exception being that molecular microbiological techniques were used alongside traditional microbiology in the second study of infectious intestinal disease (IID2). In the first study of infectious intestinal disease (IID1) in 1993–1996, the incidence of nontyphoidal Salmonella in the community in England was 2.2 cases per 1000 person-years (95% confidence interval [CI], 1.1–4.3) but by 2008–2009 this had fallen to 0.7 cases per 1000 person-years (95% CI, .2–3.0). For nontyphoidal Salmonella cases presenting to primary care in England, the incidence rate had fallen from 1.6 cases per 1000 person-years (95% CI, 1.2–2.1) in IID1 to 0.2 cases per 1000 person-years (95% CI, .1–.5) in IID2. The decline in incidence in the community was not statistically significant because in IID2 the study power was insufficient to detect statistically significant changes in organism-specific incidence—to do this would have required >100 000 person-years of follow-up, based on incidence rates in IID1. Nevertheless, the reduction in presentations to primary healthcare was statistically significant. Second, there has been a substantial fall in laboratory-confirmed Salmonella cases reported to national surveillance (Figure 1). Phage typing of Salmonella Enteritidis was implemented from 1981 as an addition to the centralized, national service already in existence for confirmation and further typing [17], and all clinical diagnostic laboratories have continued to refer all Salmonella isolates to the national reference laboratories since that date. At the beginning of 1992, 2 separate national Salmonella databases were merged to form a single national dataset, which became patient-based rather than isolate-based, thus eliminating potential duplication if people were tested more than once [18]. Laboratory testing methods have remained constant since then and reporting algorithms have not changed [23], suggesting that the reduction in Salmonella is real. When Salmonella Enteritidis PT4 peaked in 1993 in the United Kingdom, >18 000 laboratory-confirmed cases of illness were recorded in national surveillance statistics, yet by 2010 PT4 isolations had fallen to just 459 [24]. Thus, the decline in nontyphoidal salmonellosis witnessed in the United Kingdom in recent years reflects this major contraction in reports of Salmonella Enteritidis PT4. Finally, outbreaks of salmonellosis have declined. Standardized reporting of outbreaks of gastrointestinal infection was introduced in 1992 in England and Wales and in 1996 in Scotland partly in response to the increase in nontyphoidal salmonellosis. A foodborne outbreak is defined in European legislation as “an incidence, observed under given circumstances, of two of more human cases of the same disease and/or infection, or a situation in which the observed number of human cases exceeds the expected number and where the cases are linked, or are probably linked, to the same source” [25]. Between 1992 and 2008, foodborne Salmonella outbreaks reported to national surveillance fell from nearly 150 per year to just over 20 annually, and the pattern of decline closely mirrors that of laboratory-confirmed cases [25]. EPIDEMIOLOGY OF SALMONELLA ENTERITIDIS IN THE UNITED KINGDOM Epidemiologic investigations of outbreaks and sporadic cases repeatedly showed that Salmonella Enteritidis PT4 infection in humans was frequently associated with consumption of poultry meat and hens' eggs on both sides of the Atlantic [25–31]. In nearly 2500 foodborne disease outbreaks reported to the UK Health Protection Agency between 1992 and 2008, Salmonella species accounted for 47% of all outbreaks, 46% of cases, 70% of hospital admissions, and 76% of deaths [25]. Salmonella Enteritidis PT4 was the causative organism in 51% of all the Salmonella outbreaks throughout the surveillance period but the percentage of outbreaks caused by Salmonella Enteritidis PT4 declined from the late 1990s onward. At least one food vehicle was identified in 75% of outbreaks reported, and poultry meat was the vehicle most often implicated (19% of outbreaks). Desserts were also implicated commonly (11% of outbreaks), and raw shell eggs were used as an ingredient in 70% of these desserts. Eggs were implicated separately in an additional 6% of outbreaks. Analysis of outbreak data also showed that nearly 50% of foodborne Salmonella outbreaks occurred in the food service/catering sector. Salmonella Gallinarum and Salmonella Pullorum had been the dominant Salmonella serovars in UK poultry until the early 1970s. These strains both caused clinical disease in the birds and were virtually eradicated by a combination of slaughtering of seropositive hens and vaccination [20]. However, the ecological niche left by these 2 serovars was filled by Salmonella Enteritidis. Complete genome sequencing of a host-promiscuous Salmonella Enteritidis PT4 isolate (P125109) and a chicken-restricted Salmonella Gallinarum isolate (287/91) has indicated that Salmonella Gallinarum 287/91 is a recently evolved descendent of Salmonella Enteritidis [32]. Importantly, Salmonella Enteritidis infects poultry without causing overt disease, which probably facilitated its rapid spread internationally [20]. Another key feature of Salmonella Enteritidis is colonization of the reproductive tissues leading to the production of eggs with Salmonella-positive contents [20, 33] and, in some eggs, the numbers of organisms can be very high [34]. CONTROLLING SALMONELLOSIS AND OTHER FOODBORNE ILLNESSES In August 1988, as evidence of a link between Salmonella Enteritidis PT4 and raw shell eggs strengthened, the Chief Medical Officer issued advice to consumers to avoid eating raw eggs or uncooked foods in which raw eggs were an ingredient. In December of the same year, he issued further advice to vulnerable people such as the elderly, individuals with chronic illness, infants, and pregnant women. They were counseled only to eat eggs that had been cooked until the yolks and whites were solid [18]. Caterers were encouraged to use pasteurized eggs, especially where foodstuffs were not going to be cooked further (eg, mayonnaise), and it was recommended that eggs be considered short shelf-life products. They should be refrigerated 600 000 birds from 58 infected flocks were slaughtered. In 1992, <300 000 birds from 38 infected flocks were slaughtered [18]. Alongside legislation was a voluntary, industry-led vaccination scheme that began in broiler-breeder flocks in 1994 and in laying flocks in 1998 [16]. A “Lion Mark,” stamped on eggs, which had been introduced in 1957 but dropped by 1971, was revived in 1998 (http://www.lioneggs.co.uk/page/lionmark). The Lion Mark can only be used by subscribers to the British Egg Industry Council for eggs that have been produced in accordance with UK and EU law and the Lion Quality Code of Practice. The code of practice requires mandatory vaccination of all pullets destined to lay Lion eggs against Salmonella; independent auditing; full traceability of hens, eggs, and feed; and a “best-before” date stamped on the shell and pack, in addition to on-farm stamping of eggs and packing station hygiene controls. When, in 1989, a Junior Health Minister stated in a British television interview that “Most of the egg production in this country, sadly, is now infected with Salmonella,” the sale of eggs collapsed by 60% almost overnight. Moreover, despite government efforts to improve the safety of eggs, sales continued to fall by around 8% per year over the next 10 years, which was a disaster for the industry. The British Egg Industry Service began a major consumer research program in 1997 and, in 1998, the majority of UK producers and packers made a voluntary investment of £8 million to assist the British Egg Industry Council to relaunch British eggs. A total of £4 million was spent on the stringent new Code of Practice described above, and £4 million supported a new promotional campaign to restore consumer confidence and increase consumption. The cost of the vaccination program (including Lion sampling and testing) is estimated to be around £52 million to date (Mark Williams, written personal communication, September 2012). However, between 1998 and 2009, the egg market grew from 9.8 billion to 11 billion eggs per year, and Lion eggs now account for around 85% of the total market. Within the retail sector the market share of Lion eggs share rose from approximately 60% in 1998 to 95% in 2010 (http://www.lioneggs.co.uk/files/lioneggs.co.uk/pdfs/marketing.pdf). Alas, Salmonella was not the only “food scare” during the 1980s and 1990s. Scandals surrounding, for example, bovine spongiform encephalopathy in the United Kingdom, dioxins in Belgium, and Salmonella EU-wide prompted new legislation providing for a risk-based “farm to fork” approach to food safety policy, which was enacted in 2002 (European General Food Law [Regulation (EC) No. 178/2002]) [24]. EU Zoonoses Regulation (EC) No. 2160/2003 required member states to take effective measures to detect and control Salmonella species of public health significance in specified animal species at all relevant stages of production [24]. Each EU member state was obliged to undertake a standardized baseline survey to determine the prevalence of Salmonella within their industry sectors. EC Regulation (EC) 1168/2006 laid down an annual reduction target for Salmonella Enteritidis and Salmonella Typhimurium for each member state. NATIONAL CONTROL PROGRAMS FOR SALMONELLA IN THE POULTRY SECTOR Four National Control Programmes (NCPs) for Salmonella have been implemented in the UK poultry sector between 2007 and 2010. These postdate the rapid decline in Salmonella Enteritidis in the United Kingdom but are designed to achieve and maintain low rates EU-wide. For the most part, the targets set by the EU have already been met or exceeded in the United Kingdom [24]. The NCP for breeding chickens (implemented in 2007): The target for this NCP was that no more than 1% of adult breeding flocks should be infected with 5 specific regulated serovars (Salmonella Enteritidis, Salmonella Typhimurium, Salmonella Hadar, Salmonella Infantis, and Salmonella Virchow) by the end of 2009. Results from UK holdings have been significantly below the EU target of 1% every year for the last 4 years [24]. The NCP for commercial laying chickens (implemented in 2008): An EU-wide baseline survey of commercial laying chicken flock holdings was undertaken in 2004–2005. In a survey of Salmonella species on 454 commercial layer flock holdings in the United Kingdom, 54 (11.7%) were Salmonella positive [35]. Salmonella Enteritidis was the serovar most commonly identified (prevalence = 5.8%) and PTs 4, 6, 7, and 35 comprised 70% of isolates. Salmonella Typhimurium was the second most commonly identified serovar (prevalence = 1.8%). The UK prevalence figures were among the lowest of the major egg-producing countries (7.9% of holdings positive compared with a 20.4% average across the EU) [36]. Across the EU, the incidence rate of salmonellosis in member states varies between 16 and 11 800 per 100 000 population and has been shown to be significantly correlated with the prevalence of Salmonella Enteritidis in laying hens [10], so controlling levels of Salmonella Enteritidis in laying flocks is important for improving public health. The NCP for broilers (implemented in 2009): The target for this NCP was that no more than 1% of flocks should be infected with Salmonella Enteritidis and Salmonella Typhimurium by the end of 2011. In a baseline survey of broiler chickens in 2005–2006 in the United Kingdom, the prevalence of Salmonella Enteritidis and Salmonella Typhimurium was very low (0.2% [37] compared with an EU average of 11.0% [38]) and remains well below the EU target [24]. The NCP for turkeys (implemented in 2010): A baseline survey for Salmonella in turkey breeding and fattening flocks was carried out across the EU in 2006–2007. In the United Kingdom, the prevalence of Salmonella in breeding flock holdings was 20.1% and in fattening flocks the holdings prevalence was 37.7% [39]. The flock prevalence of Salmonella Typhimurium was very low on breeding holdings at 0.7% (EU weighted average = 1.8%) but higher on fattening holdings at 4.6% (EU weighted average = 3.7%) [24]. The target for Salmonella reduction is that only 1% of breeding flocks and 1% of fattening flocks should be positive by the end of 2012. Early indications are that this target will be met. WHAT NEXT? There is no room for complacency. During the 2000s, new Salmonella problems emerged. Notable among these were national outbreaks of Salmonella Enteritidis PT14b linked to raw shell eggs originating in Spain [40, 41]. Unbelievably, perhaps, hospital caterers in the United Kingdom were found serving raw shell eggs again to patients, with consequent outbreaks [42]. The first outbreak of Salmonella Typhimurium PT8 linked to consumption of duck eggs since 1949 occurred in the United Kingdom [43], and Salmonella outbreaks linked to fresh produce were increasingly recognized [44, 45], reflecting a pattern also seen in the United States [46]. CONCLUSIONS The nature of public health interventions often means that evaluating their impact is complex as they are often implemented in combination and/or simultaneously. It is interesting to reflect on the fact that the various legislative measures in the United Kingdom in the late 1980s and early 1990s appear to have slowed down the increase in Salmonella Enteritidis PT4, whereas the decrease in laboratory-confirmed human cases coincides quite closely with the introduction of vaccination programs in broiler-breeder and laying flocks and prior to much of the EU legislation being implemented. It is probable that no single measure contributed to the decline in Salmonella Enteritidis PT4 and that the combination of measures was successful, but the temporal relationship between vaccination programs and the reduction in human disease is compelling and suggests that these programs have made a major contribution to improving public health. There has also been a reduction in reported human salmonellosis cases across the EU (on average 12% per year between 2005 and 2009). The European Commission and European Food Safety Authority are attributing this, at least in part, to successful control of Salmonella in broiler, laying, and breeding hen flocks and eggs [24]. If success in public health is defined by illnesses averted, then the story of Salmonella Enteritidis PT4 in the United Kingdom, which has come down and stayed down, is good news. However, history teaches us that something else may come along to take its place. Robust surveillance, incorporating state-of-the-art microbiological, epidemiological, and biostatistical methods, and maintaining a prompt and comprehensive response to outbreaks is just as important now as it ever was.
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              CTX-M-65 Extended-Spectrum β-Lactamase–Producing Salmonella enterica Serotype Infantis, United States 1

              Extended-spectrum β-lactamases (ESBLs) confer resistance to clinically important third-generation cephalosporins, which are often used to treat invasive salmonellosis. In the United States, ESBLs are rarely found in Salmonella. However, in 2014, the US Food and Drug Administration found bla CTX-M-65 ESBL-producing Salmonella enterica serotype Infantis in retail chicken meat. The isolate had a rare pulsed-field gel electrophoresis pattern. To clarify the sources and potential effects on human health, we examined isolates with this pattern obtained from human surveillance and associated metadata. Using broth microdilution for antimicrobial susceptibility testing and whole-genome sequencing, we characterized the isolates. Of 34 isolates, 29 carried the bla CTX-M-65 gene with <9 additional resistance genes on 1 plasmid. Of 19 patients with travel information available, 12 (63%) reported recent travel to South America. Genetically, isolates from travelers, nontravelers, and retail chicken meat were similar. Expanded surveillance is needed to determine domestic sources and potentially prevent spread of this ESBL-containing plasmid.
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                Author and article information

                Journal
                MMWR Morb Mortal Wkly Rep
                MMWR Morb. Mortal. Wkly. Rep
                WR
                Morbidity and Mortality Weekly Report
                Centers for Disease Control and Prevention
                0149-2195
                1545-861X
                01 May 2020
                01 May 2020
                : 69
                : 17
                : 509-514
                Affiliations
                Division of Foodborne, Waterborne, and Environmental Diseases, National Center for Emerging and Zoonotic Infectious Diseases, CDC; Oregon Health Authority; Tennessee Department of Health; Connecticut Emerging Infections Program; Colorado Department of Public Health and Environment; University of New Mexico, Albuquerque; New York State Department of Health; Maryland Department of Health; Minnesota Department of Health; Georgia Department of Public Health; California Department of Public Health; Food Safety and Inspection Service, U.S. Department of Agriculture, Washington, DC; Center for Food Safety and Applied Nutrition, Food and Drug Administration, Silver Spring, Maryland.
                Author notes
                Corresponding author: Danielle M. Tack, dot7@ 123456cdc.gov , 404-718-3254.
                Article
                mm6917a1
                10.15585/mmwr.mm6917a1
                7206985
                32352955
                42f4dacb-247d-480f-bc05-6d0f16b9607e

                All material in the MMWR Series is in the public domain and may be used and reprinted without permission; citation as to source, however, is appreciated.

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