Preliminary Incidence and Trends of Infections with Pathogens Transmitted Commonly Through Food — Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 2015–2018

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Abstract

Foodborne diseases represent a major health problem in the United States. The Foodborne Diseases Active Surveillance Network (FoodNet) of CDC’s Emerging Infections Program monitors cases of laboratory-diagnosed infection caused by eight pathogens transmitted commonly through food in 10 U.S. sites.* This report summarizes preliminary 2018 data and changes since 2015. During 2018, FoodNet identified 25,606 infections, 5,893 hospitalizations, and 120 deaths. The incidence of most infections is increasing, including those caused by Campylobacter and Salmonella, which might be partially attributable to the increased use of culture-independent diagnostic tests (CIDTs). The incidence of Cyclospora infections increased markedly compared with 2015–2017, in part related to large outbreaks associated with produce ( 1 ). More targeted prevention measures are needed on produce farms, food animal farms, and in meat and poultry processing establishments to make food safer and decrease human illness. FoodNet conducts active, population-based surveillance for laboratory-diagnosed infections caused by Campylobacter, Cyclospora, Listeria, Salmonella, Shiga toxin–producing Escherichia coli (STEC), Shigella, Vibrio, and Yersinia in 10 sites covering 15% of the U.S. population (approximately 49 million persons in 2017). FoodNet is a collaboration among 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 bacterium from a clinical specimen or detection of pathogen antigen, nucleic acid sequences, or, for STEC, † Shiga toxin or Shiga toxin genes. Listeria cases 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 cases of miscarriage or stillbirth. Cyclospora infections are defined as detection of the parasite from a clinical specimen by direct fluorescent antibody, polymerase chain reaction, or light microscopy. Hospitalizations occurring within 7 days of specimen collection are attributed to the infection, as is the patient’s vital status at hospital discharge, or 7 days after specimen collection if the patient was not hospitalized. Incidence per 100,000 population was calculated by dividing the number of infections in 2018 by U.S. Census estimates of the surveillance area population for 2017. A negative binomial model with 95% confidence intervals (CIs) was calculated using SAS (version 9.4; SAS Institute) to estimate changes in incidence. Surveillance for physician-diagnosed postdiarrheal hemolytic uremic syndrome, a complication of STEC infection characterized by renal failure, thrombocytopenia, and microangiopathic anemia, is conducted through a network of nephrologists and infection preventionists and by hospital discharge data review. This report includes pediatric hemolytic uremic syndrome cases (those occurring in persons aged <18 years) identified during 2017, the most recent year for which data are available. Cases of Infection, Incidence, and Trends During 2018, FoodNet identified 25,606 cases of infection, 5,893 hospitalizations, and 120 deaths. The incidence of infection (per 100,000 population) was highest for Campylobacter (19.5) and Salmonella (18.3), followed by STEC (5.9), Shigella (4.9), Vibrio (1.1), Yersinia (0.9), Cyclospora (0.7), and Listeria (0.3) (Table). Compared with 2015–2017, the incidence significantly increased for Cyclospora (399%), Vibrio (109%), Yersinia (58%), STEC (26%), Campylobacter (12%), and Salmonella (9%). The number of bacterial infections diagnosed by CIDT (with or without reflex culture § ) increased 65% in 2018 compared with the average annual number diagnosed during 2015–2017; the increase ranged from 29% for STEC to 311% for Vibrio (Figure 1). In 2018, the percentage of infections diagnosed by DNA-based syndrome panels was highest for Yersinia (68%) and Cyclospora (67%), followed by STEC (55%), Vibrio (53%), Shigella (48%), Campylobacter (43%), Salmonella (33%), and was lowest for Listeria (2%). In 2018, a reflex culture was attempted on 75% of specimens with positive CIDT results, ranging from 64% for Campylobacter to 100% for Listeria (Figure 1). The percentage of specimens with a reflex culture in 2018 was 14% higher than that during 2015–2017, ranging from a 7% decrease for STEC to a 55% increase for Shigella (Figure 2). Among specimens with reflex culture in 2018, the percentage that yielded the pathogen was highest for Listeria (100%) and Salmonella (86%), followed by STEC (64%), Campylobacter (59%), Shigella (56%), Yersinia (50%), and Vibrio (37%) (Figure 1) (Figure 2). TABLE Number of cases, hospitalizations, and deaths caused by bacterial and parasitic infections, incidence rate, and percentage change compared with 2015–2017 average annual incidence rate, by pathogen — CDC’s Foodborne Diseases Active Surveillance Network,* 2018 † Pathogen 2018 2018 compared with 2015–2017 No. of cases No. (%) of hospitalizations No. (%) of deaths IR§ % (95% CI) Change in IR¶ Bacteria Campylobacter 9,723 1,811 (18) 30 (0.3) 19.6 12 (4 to 20) Salmonella 9,084 2,416 (27) 36 (0.4) 18.3 9 (3 to 16) Shiga toxin–producing Escherichia coli** 2,925 648 (22) 13 (0.4) 5.9 26 (7 to 48) Shigella 2,414 632 (26) 1 (0.04) 4.9 −2 (−24 to 26) Vibrio 537 151 (28) 9 (2) 1.1 109 (72 to 154) Yersinia 465 95 (20) 4 (0.9) 0.9 58 (26 to 99) Listeria 126 121 (96) 26 (21) 0.3 −4 (−23 to 21) Parasite Cyclospora 332 19 (5) 1 (0.3) 0.7 399 (202 to 725) Total 25,606 5,893 (23) 120 (0.5) — — Abbreviation: CI = confidence interval; IR = incidence rate. * Connecticut, Georgia, Maryland, Minnesota, New Mexico, Oregon, Tennessee, and selected counties in California, Colorado, and New York. † Data are preliminary. § Per 100,000 population. ¶ Increase or decrease. ** All serogroups were combined because it is not possible to distinguish among them using culture-independent diagnostic tests. FIGURE 1 Number of infections diagnosed by culture or culture-independent diagnostic tests (CIDTs), by pathogen, year, and culture status — CDC’s Foodborne Diseases Active Surveillance Network,* 2015–2018 † Abbreviation: STEC = Shiga toxin–producing Escherichia coli. * Connecticut, Georgia, Maryland, Minnesota, New Mexico, Oregon, Tennessee, and selected counties in California, Colorado, and New York. † Data for 2018 are preliminary. The figure is a histogram showing the number of infections diagnosed by culture or culture-independent diagnostic tests, by pathogen, year, and culture status, during 2015–2018, using data from CDC’s Foodborne Diseases Active Surveillance Network. FIGURE 2 Percentage of infections diagnosed by culture-independent diagnostic tests (CIDTs), positive CIDTs with a reflex culture,* and reflex cultures that yielded the pathogen, by pathogen — CDC’s Foodborne Diseases Active Surveillance Network, † 2015–2017 and 2018 § Abbreviation: STEC = Shiga toxin–producing Escherichia coli. * Culture of a specimen with a positive CIDT result. † Connecticut, Georgia, Maryland, Minnesota, New Mexico, Oregon, Tennessee, and selected counties in California, Colorado, and New York. § Data for 2018 are preliminary. The figure is a line chart showing the percentage of infections diagnosed by culture-independent diagnostic tests (CIDTs), positive CIDTs with a reflex culture, and reflex cultures that yielded the pathogen, by pathogen, during 2015–2017 and 2018, using data from CDC’s Foodborne Diseases Active Surveillance Network. Among 7,013 (87%) serotyped Salmonella isolates, the three most common were Enteritidis (2.6 per 100,000 population), Newport (1.6), and Typhimurium (1.5), similar to those during 2015–2017. Among 1,570 STEC isolates tested, 440 (28%) were determined to be O157. Among 662 non-O157 STEC isolates serogrouped, the most common were O103 (31%), O26 (28%), and O111 (24%). The incidence compared with 2015–2017 remained unchanged for both O157 and non-O157 STEC. FoodNet identified 54 cases of postdiarrheal hemolytic uremic syndrome in children (0.49 cases per 100,000) during 2017; 36 (67%) occurred among children aged <5 years (1.22 cases per 100,000). Incidence was not significantly different compared with that during 2014–2016. Discussion Campylobacter has been the most commonly identified infection in FoodNet since 2013. It causes diarrhea, sometimes bloody, and 18% of persons are hospitalized. A rare outcome of Campylobacter infection is Guillain-Barré syndrome, a type of autoimmune-mediated paralysis. Poultry is a major source of Campylobacter ( 2 ). In August 2018, FSIS began using a new testing method; in a study of that method, Campylobacter was isolated from 18% of chicken carcasses and 16% of chicken parts sampled ( 3 ). FSIS currently makes aggregated test results available and intends to update performance standards for Campylobacter contamination. The incidence of infections with Enteritidis, the most common Salmonella serotype, has not declined in over 10 years. Enteritidis is adapted to live in poultry, and eggs are an important source of infection ( 4 ). By 2012, FDA had implemented the Egg Safety Rule, ¶ which requires preventive measures during the production of eggs in poultry houses and requires subsequent refrigeration during storage and transportation, for all farms with ≥3,000 hens. In 2018, a multistate outbreak of Enteritidis infections was traced to eggs from a farm that had not implemented the required egg safety measures after its size reached ≥3,000 hens ( 5 ). Chicken meat is also an important source of Enteritidis infections ( 4 ). In December 2018, FSIS reported that 22% of establishments that produce chicken parts failed to meet the Salmonella performance standard (USDA-FSIS Salmonella verification testing program**). The percentage of samples of chicken meat and intestinal contents that yielded Enteritidis were similar in 2018 to those during 2015–2017 (USDA-FSIS, unpublished data). In contrast, a decline in serotype Typhimurium isolated from the same sources was observed during the same period. This trend coincides with declines in Typhimurium human illnesses. Changes in poultry production practices, including vaccination against Typhimurium, might have resulted in these declines ( 6 ). In the United Kingdom, vaccination of both broiler and layer chickens against Enteritidis, along with improved hygiene, was followed by a marked decrease in human Enteritidis infections ( 7 ). Produce is a major source of foodborne illnesses ( 2 ). During 2018, romaine lettuce was linked to two multistate outbreaks of STEC O157 infections ( 8 ). The marked increase in reported Cyclospora infections was likely attributable to several factors including produce outbreaks and continued adoption of DNA-based syndrome panel tests ( 1 ). Improved agricultural practices are needed to prevent produce-associated infections. FDA provides technical assistance to task forces created by the produce industry, to determine how to prevent contamination of romaine lettuce and facilitate outbreak investigations by improving product labeling and traceability. In 2018, FDA expanded surveillance sampling of foreign and domestically grown produce to assess its safety ( 9 ). FDA is implementing the Produce Safety Rule, †† with routine inspections of large produce farms planned this spring. Because produce is a major component of a healthy diet and is often consumed raw, making it safer is important for improving human health ( 10 ). The findings in this report are subject to at least three limitations. First, the changing diagnostic landscape makes interpretation of incidence and trends more complex. Increases in reported incidence might be attributable entirely, or in part, to changes in clinician ordering practices, increased use of DNA-based syndrome panels that identify pathogens not routinely captured by traditional methods, and changes in laboratory practices in response to the availability of these panels. Second, some CIDT results might be false positives. Finally, year-to-year variations, attributable in part to large outbreaks, might not indicate sustained trends. The need to obtain and subtype isolates from ill persons is becoming an increasing burden to state health departments but is critical for maintaining surveillance to detect and investigate outbreaks, evaluating prevention efforts, and developing targeted control measures. Measures that might decrease foodborne illnesses include enhanced efforts targeting Campylobacter contamination of chicken; strengthening prevention measures during egg production, especially within small flocks; vaccinating poultry against Salmonella serotype Enteritidis; decreasing Salmonella contamination of produce, poultry, and meat; and continued implementation of the Food Safety Modernization Act, specifically FDA’s Produce Safety Rule. FoodNet continues to collect data and develop analytic tools to adjust for changes in diagnostic testing practices and test characteristics. These actions, along with FoodNet’s robust surveillance, provide data to help evaluate the effectiveness of prevention efforts and determine when additional measures are needed. Summary What is already known about this topic? The incidence of foodborne infections has remained largely unchanged. Clinical laboratories are increasingly using culture-independent diagnostic tests (CIDTs) to detect enteric infections. CIDTs benefit public health surveillance by identifying pathogens not routinely detected by previous methods but complicate data interpretation. What is added by this report? The incidence of most infections increased during 2018 compared with 2015–2017; this might be partially attributable to increased CIDT use. The incidence of Cyclospora infections increased markedly, in part related to large outbreaks associated with produce. The number of human infections caused by Campylobacter and Salmonella, especially serotype Enteritidis, remains high. What are the implications for public health practice? As use of CIDTs increases, it is important to obtain and subtype isolates and interview ill persons to monitor prevention efforts and develop more targeted prevention and control measures to make food safer and decrease human illness.

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The “Decline and Fall” of Nontyphoidal Salmonella in the United Kingdom

Sarah O’Brien (2012)

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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Effect of Salmonella vaccination of breeder chickens on contamination of broiler chicken carcasses in integrated poultry operations.

Fernanda Dórea, Dana Cole, Charles Hofacre … (2010)

While measures to control carcass contamination with Salmonella at the processing plant have been implemented with some success, on-farm interventions that reduce Salmonella prevalence in meat birds entering the processing plant have not translated well on a commercial scale. We determined the impact of Salmonella vaccination on commercial poultry operations by monitoring four vaccinated and four nonvaccinated breeder (parental) chicken flocks and comparing Salmonella prevalences in these flocks and their broiler, meat bird progeny. For one poultry company, their young breeders were vaccinated by using a live-attenuated Salmonella enterica serovar Typhimurium vaccine (Megan VAC-1) followed by a killed Salmonella bacterin consisting of S. enterica serovar Berta and S. enterica serovar Kentucky. The other participating poultry company did not vaccinate their breeders or broilers. The analysis revealed that vaccinated hens had a lower prevalence of Salmonella in the ceca (38.3% versus 64.2%; P < 0.001) and the reproductive tracts (14.22% versus 51.7%; P < 0.001). We also observed a lower Salmonella prevalence in broiler chicks (18.1% versus 33.5%; P < 0.001), acquired from vaccinated breeders, when placed at the broiler farms contracted with the poultry company. Broiler chicken farms populated with chicks from vaccinated breeders also tended to have fewer environmental samples containing Salmonella (14.4% versus 30.1%; P < 0.001). There was a lower Salmonella prevalence in broilers entering the processing plants (23.4% versus 33.5%; P < 0.001) for the poultry company that utilized this Salmonella vaccination program for its breeders. Investigation of other company-associated factors did not indicate that the difference between companies could be attributed to measures other than the vaccination program.

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Notes from the Field: Multiple Cyclosporiasis Outbreaks — United States, 2018

Shannon Casillas, Carolyne Bennett, Anne Straily (2018)

Cyclosporiasis is an intestinal illness caused by the parasite Cyclospora cayetanensis through ingestion of fecally contaminated food or water. Symptoms of cyclosporiasis might include watery diarrhea (most common), loss of appetite, weight loss, cramping, bloating, increased gas, nausea, and fatigue. Typically, increased numbers of cases are reported in the United States during spring and summer; since the mid-1990s, outbreaks have been identified and investigated almost every year. Past outbreaks have been associated with various types of imported fresh produce (e.g., basil, cilantro, and raspberries) ( 1 ). There are currently no validated molecular typing tools* to facilitate linking cases to each other, to food vehicles, or their sources. Therefore, cyclosporiasis outbreak investigations rely primarily on epidemiologic data. The 2018 outbreak season is noteworthy for multiple outbreaks associated with different fresh produce items and the large number of reported cases. Two multistate outbreaks resulted in 761 laboratory-confirmed illnesses. The first outbreak, identified in June, was associated with prepackaged vegetable trays (containing broccoli, cauliflower, and carrots) sold at a convenience store chain in the Midwest; 250 laboratory-confirmed cases were reported in persons with exposures in three states (illness onset mid-May–mid-June) ( 2 ). The supplier voluntarily recalled the vegetable trays ( 3 ). The second multistate outbreak, identified in July, was associated with salads (containing carrots, romaine, and other leafy greens) sold at a fast food chain in the Midwest; 511 laboratory-confirmed cases during May–July occurred in persons with exposures in 11 states who reported consuming salads ( 4 ). The fast food chain voluntarily stopped selling salads at approximately 3,000 stores in 14 Midwest states that received the implicated salad mix from a common processing facility ( 5 ). The traceback investigation conducted by the Food and Drug Administration (FDA) did not identify a single source or potential point of contamination for either outbreak. In addition to the multistate outbreaks, state public health authorities, CDC, and FDA investigated cyclosporiasis clusters associated with other types of fresh produce, including basil and cilantro. Two basil-associated clusters (eight confirmed cases each) were identified among persons in two different states who became ill during June. Investigation of one cluster, for which the state health department conducted an ingredient-specific case-control study, found consumption of basil to be significantly associated with illness. A formal analytic study was not conducted for the other cluster, but all patients reported consuming basil. Three clusters associated with Mexican-style restaurants in the Midwest have resulted in reports of 53 confirmed cases in persons who became ill during May–August. Analytic studies were conducted for two clusters; consumption of cilantro was found to be significantly associated with illness in both. Although a formal analytic study was not possible for the third cluster, all 32 identified patients reported consuming cilantro at the restaurant. FDA traceback of the basil and cilantro from these clusters is ongoing. Additional clusters associated with Mexican-style restaurants were identified in multiple states; but investigations to determine a single vehicle of infection were unsuccessful because of small case counts, limited exposure information, or because fresh produce items (including cilantro) were served as components of other dishes (e.g., in salsa). Many cases could not be directly linked to an outbreak, in part because of the lack of validated molecular typing tools for C. cayetanensis. As of October 1, 2018, a total of 2,299 laboratory-confirmed cyclosporiasis cases † have been reported by 33 states in persons who became ill during May 1–August 30 and did not have a history of international travel § during the 14 days preceding illness onset. Approximately one third of these cases were associated with either the convenience store chain outbreak or the fast food chain outbreak (Figure). The median patient age was 49 years (range = 3 days or who have any other concerning symptoms should see a health care provider if they think they might have become ill from eating contaminated food.

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Journal ID (nlm-ta): MMWR Morb Mortal Wkly Rep

Journal ID (iso-abbrev): MMWR Morb. Mortal. Wkly. Rep

Journal ID (publisher-id): WR

Title: Morbidity and Mortality Weekly Report

Publisher: Centers for Disease Control and Prevention

ISSN (Print): 0149-2195

ISSN (Electronic): 1545-861X

Publication date (Electronic): 26 April 2019

Publication date Collection: 26 April 2019

Volume: 68

Issue: 16

Pages: 369-373

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Division of Foodborne, Waterborne, and Environmental Diseases, National Center for Emerging and Zoonotic Infectious Diseases, CDC; Oregon Health Authority; Tennessee Department of Health; Connecticut Department of Public Health; University of Colorado, Boulder, Colorado; University of New Mexico, Albuquerque, New Mexico; 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, Atlanta, Georgia; Center for Food Safety and Applied Nutrition, Food and Drug Administration, Silver Spring, Maryland.

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Corresponding author: Danielle Tack, dot7@ 123456cdc.gov , 404-718-3254.

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Publisher ID: mm6816a2

DOI: 10.15585/mmwr.mm6816a2

PMC ID: 6483286

PubMed ID: 31022166

SO-VID: 371ee071-342a-4405-841b-c513424b212b

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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.

Preliminary Incidence and Trends of Infections with Pathogens Transmitted Commonly Through Food — Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 2015–2018

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Notes from the Field: Multiple Cyclosporiasis Outbreaks — United States, 2018

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