Incubation periods of enteric illnesses in foodborne outbreaks, United States, 1998-2013.

Early in a foodborne disease outbreak investigation, illness incubation periods can help focus case interviews, case definitions, clinical and environmental evaluations and predict an aetiology. Data describing incubation periods are limited. We examined foodborne disease outbreaks from laboratory-confirmed, single aetiology, enteric bacterial and viral pathogens reported to United States foodborne disease outbreak surveillance from 1998-2013. We grouped pathogens by clinical presentation and analysed the reported median incubation period among all illnesses from the implicated pathogen for each outbreak as the outbreak incubation period. Outbreaks from preformed bacterial toxins (Staphylococcus aureus, Bacillus cereus and Clostridium perfringens) had the shortest outbreak incubation periods (4-10 h medians), distinct from that of Vibrio parahaemolyticus (17 h median). Norovirus, salmonella and shigella had longer but similar outbreak incubation periods (32-45 h medians); campylobacter and Shiga toxin-producing Escherichia coli had the longest among bacteria (62-87 h medians); hepatitis A had the longest overall (672 h median). Our results can help guide diagnostic and investigative strategies early in an outbreak investigation to suggest or rule out specific etiologies or, when the pathogen is known, the likely timeframe for exposure. They also point to possible differences in pathogenesis among pathogens causing broadly similar syndromes.

Produce-associated foodborne disease outbreaks, USA, 1998-2013.

The US Food Safety Modernization Act (FSMA) gives food safety regulators increased authority to require implementation of safety measures to reduce the contamination of produce. To evaluate the future impact of FSMA on food safety, a better understanding is needed regarding outbreaks attributed to the consumption of raw produce. Data reported to the US Centers for Disease Control and Prevention's Foodborne Disease Outbreak Surveillance System during 1998-2013 were analysed. During 1998-2013, there were 972 raw produce outbreaks reported resulting in 34 674 outbreak-associated illnesses, 2315 hospitalisations, and 72 deaths. Overall, the total number of foodborne outbreaks reported decreased by 38% during the study period and the number of raw produce outbreaks decreased 19% during the same period; however, the percentage of outbreaks attributed to raw produce among outbreaks with a food reported increased from 8% during 1998-2001 to 16% during 2010-2013. Raw produce outbreaks were most commonly attributed to vegetable row crops (38% of outbreaks), fruits (35%) and seeded vegetables (11%). The most common aetiologic agents identified were norovirus (54% of outbreaks), Salmonella enterica (21%) and Shiga toxin-producing Escherichia coli (10%). Food-handling errors were reported in 39% of outbreaks. The proportion of all foodborne outbreaks attributable to raw produce has been increasing. Evaluation of safety measures to address the contamination on farms, during processing and food preparation, should take into account the trends occurring before FSMA implementation.

Multistate outbreak of listeriosis caused by imported cheese and evidence of cross-contamination of other cheeses, USA, 2012.

Listeria monocytogenes is a foodborne pathogen that can cause bacteraemia, meningitis, and complications during pregnancy. In July 2012, molecular subtyping identified indistinguishable L. monocytogenes isolates from six patients and two samples of different cut and repackaged cheeses. A multistate outbreak investigation was initiated. Initial analyses identified an association between eating soft cheese and outbreak-related illness (odds ratio 17·3, 95% confidence interval 2·0-825·7) but no common brand. Cheese inventory data from locations where patients bought cheese and an additional location where repackaged cheese yielded the outbreak strain were compared to identify cheeses for microbiological sampling. Intact packages of imported ricotta salata yielded the outbreak strain. Fourteen jurisdictions reported 22 cases from March-October 2012, including four deaths and a fetal loss. Six patients ultimately reported eating ricotta salata; another reported eating cheese likely cut with equipment also used for contaminated ricotta salata, and nine more reported eating other cheeses that might also have been cross-contaminated. An FDA import alert and US and international recalls followed. Epidemiology-directed microbiological testing of suspect cheeses helped identify the outbreak source. Cross-contamination of cheese highlights the importance of using validated disinfectant protocols and routine cleaning and sanitizing after cutting each block or wheel.

2013 multistate outbreaks of Cyclospora cayetanensis infections associated with fresh produce: focus on the Texas investigations.

The 2013 multistate outbreaks contributed to the largest annual number of reported US cases of cyclosporiasis since 1997. In this paper we focus on investigations in Texas. We defined an outbreak-associated case as laboratory-confirmed cyclosporiasis in a person with illness onset between 1 June and 31 August 2013, with no history of international travel in the previous 14 days. Epidemiological, environmental, and traceback investigations were conducted. Of the 631 cases reported in the multistate outbreaks, Texas reported the greatest number of cases, 270 (43%). More than 70 clusters were identified in Texas, four of which were further investigated. One restaurant-associated cluster of 25 case-patients was selected for a case-control study. Consumption of cilantro was most strongly associated with illness on meal date-matched analysis (matched odds ratio 19·8, 95% confidence interval 4·0-∞). All case-patients in the other three clusters investigated also ate cilantro. Traceback investigations converged on three suppliers in Puebla, Mexico. Cilantro was the vehicle of infection in the four clusters investigated; the temporal association of these clusters with the large overall increase in cyclosporiasis cases in Texas suggests cilantro was the vehicle of infection for many other cases. However, the paucity of epidemiological and traceback information does not allow for a conclusive determination; moreover, molecular epidemiological tools for cyclosporiasis that could provide more definitive linkage between case clusters are needed.

Outbreak of Salmonella enterica serotype I 4,5,12:i:- infections: the challenges of hypothesis generation and microwave cooking.

We investigated an outbreak of 396 Salmonella enterica serotype I 4,5,12:i:- infections to determine the source. After 7 weeks of extensive hypothesis-generation interviews, no refined hypothesis was formed. Nevertheless, a case-control study was initiated. Subsequently, an iterative hypothesis-generation approach used by a single interviewing team identified brand A not-ready-to-eat frozen pot pies as a likely vehicle. The case-control study, modified to assess this new hypothesis, along with product testing indicated that the turkey variety of pot pies was responsible. Review of product labels identified inconsistent language regarding preparation, and the cooking instructions included undefined microwave wattage categories. Surveys found that most patients did not follow the product's cooking instructions and did not know their oven's wattage. The manufacturer voluntarily recalled pot pies and improved the product's cooking instructions. This investigation highlights the value of careful hypothesis-generation and the risks posed by frozen not-ready-to-eat microwavable foods.

Real-time modelling used for outbreak management during a cholera epidemic, Haiti, 2010-2011.

The emergence of epidemic cholera in post-earthquake Haiti portended a public health disaster of uncertain magnitude. In order to coordinate relief efforts in an environment with limited healthcare infrastructure and stretched resources, timely and realistic projections of the extent of the cholera outbreak were crucial. Projections were shared with Government and partner organizations beginning 5 days after the first reported case and were updated using progressively more advanced methods as more surveillance data became available. The first projection estimated that 105 000 cholera cases would occur in the first year. Subsequent projections using different methods estimated up to 652 000 cases and 163 000-247 000 hospitalizations during the first year. Current surveillance data show these projections to have provided reasonable approximations of the observed epidemic. Providing the real-time projections allowed Haitian ministries and external aid organizations to better plan and implement response measures during the evolving epidemic.

Common source outbreaks of Campylobacter infection in the USA, 1997-2008.

Campylobacter is a common but decreasing cause of foodborne infections in the USA. Outbreaks are uncommon and have historically differed from sporadic cases in seasonality and contamination source. We reviewed reported outbreaks of campylobacteriosis. From 1997 to 2008, 262 outbreaks were reported, with 9135 illnesses, 159 hospitalizations, and three deaths. The annual mean was 16 outbreaks for 1997-2002, and 28 outbreaks for 2003-2008. Almost half occurred in warmer months. Foodborne transmission was reported in 225 (86%) outbreaks, water in 24 (9%), and animal contact in seven (3%). Dairy products were implicated in 65 (29%) foodborne outbreaks, poultry in 25 (11%), and produce in 12 (5%). Reported outbreaks increased during a period of declining overall incidence, and seasonality of outbreaks resembled that of sporadic infections. Unlike sporadic illnesses, which are primarily attributed to poultry, dairy products are the most common vehicle identified for outbreaks.

Evolving public health approaches to the global challenge of foodborne infections.

The landscape of foodborne infections is in flux. New pathogens emerge, established pathogens may acquire new characteristics and appear in unexpected food vehicles, while many existing problems remain unsolved. Consumers want more fresh foods year round, populations age and migrate, and the technologies and trade practices that produce foods change. Protecting the public health and minimizing the burden of foodborne illness mean expecting the unexpected, and being prepared to understand it when it occurs, so that prevention can be improved. Public health surveillance is also constantly evolving, as new diseases emerge and are judged worthy of notification, as new diagnostic tests change the ease and specificity of routine diagnosis and as social interest in particular issues waxes and wanes. Accurate health information, including reliable estimates of the burden of foodborne disease, can improve foodborne disease prevention, foster global health security, promote economic growth and development and strengthen evidence-based policy making.

The growing burden of foodborne outbreaks due to contaminated fresh produce: risks and opportunities.

Foodborne outbreaks from contaminated fresh produce have been increasingly recognized in many parts of the world. This reflects a convergence of increasing consumption of fresh produce, changes in production and distribution, and a growing awareness of the problem on the part of public health officials. The complex biology of pathogen contamination and survival on plant materials is beginning to be explained. Adhesion of pathogens to surfaces and internalization of pathogens limits the usefulness of conventional processing and chemical sanitizing methods in preventing transmission from contaminated produce. Better methods of preventing contamination on the farm, or during packing or processing, or use of a terminal control such as irradiation could reduce the burden of disease transmission from fresh produce. Outbreak investigations represent important opportunities to evaluate contamination at the farm level and along the farm-to-fork continuum. More complete and timely environmental assessments of these events and more research into the biology and ecology of pathogen-produce interactions are needed to identify better prevention strategies.

Molecular phylogeny of the salmonellae: relationships among Salmonella species and subspecies determined from four housekeeping genes and evidence of lateral gene transfer events.

The salmonellae are a diverse group of bacteria within the family Enterobacteriaceae that includes two species, Salmonella enterica and Salmonella bongori. In order to characterize the phylogenetic relationships of the species and subspecies of Salmonella, we analyzed four housekeeping genes, gapA, phoP, mdh and recA, comprising 3,459 bp of nucleotide sequence data for each isolate sequenced. Sixty-one isolates representing the most common serotypes of the seven subspecies of Salmonella enterica and six isolates of Salmonella bongori were included in this study. We present a robust phylogeny of the Salmonella species and subspecies that clearly defines the lineages comprising diphasic and monophasic subspecies. Evidence of intersubspecies lateral gene transfer of the housekeeping gene recA, which has not previously been reported, was obtained.

Excess salmonellosis in women in the United States: 1968-2000.

We describe recent epidemiological changes in salmonellosis. Linking 1968-2000 National Salmonella Surveillance System to census data, we calculated population-based age- and sex-stratified rates of non-urinary salmonellosis for the top 30 non-typhoidal serotypes. Using 1996-1997, 1998-1999, and 2000-2001 population-based FoodNet surveys, we compared reported diarrhoea, medical visits, and stool cultures. Despite an overall female-to-male incidence rate ratio (FMRR) of 0.99, the sex-specific burden of salmonellosis varied by age (<5 years FMRR 0.92; 5-19 years 0.85; 20-39 years 1.09; 40-59 years 1.23, and 60 years 1.08) and serotype (FMRR range 0.87 for Mississippi to 1.25 for Senftenberg). Serotype-specific FMRRs and median age (range 2 years for Derby to 29 years for Senftenberg) were related (correlation 0.76, P<0.0001). Recently, the relative burden of salmonellosis in women has increased. FoodNet data suggest that this change is real rather than due to differential reporting. Excess salmonellosis in women may reflect differences in exposure or biological susceptibility.

The use of clinical profiles in the investigation of foodborne outbreaks in restaurants: United States, 1982-1997.

Improving the efficiency of outbreak investigation in restaurants is critical to reducing outbreak-associated illness and improving prevention strategies. Because clinical characteristics of outbreaks are usually available before results of laboratory testing, we examined their use for determining contributing factors in outbreaks caused by restaurants. All confirmed foodborne outbreaks reported to the Centers for Disease Control and Prevention (CDC) from 1982 to 1997 were reviewed. Clinical profiles were developed based on outbreak characteristics. We compared the percentage of contributing factors by known agent and clinical profile to their occurrence in outbreaks of unclassified aetiology. In total, 2246 foodborne outbreaks were included: 697 (31%) with known aetiology and 1549 (69%) with aetiology undetermined. Salmonella accounted for 65% of outbreaks with a known aetiology. Norovirus-like clinical profiles were noted in 54% of outbreaks with undetermined aetiology. Improper holding times and temperatures were associated with outbreaks caused by Clostridium perfringens, Bacillus cereus, Staphylococcus aureus, and Salmonella, and also with outbreaks of undetermined aetiology that fitted diarrhoea-toxin and vomiting-toxin clinical profiles. Poor personal hygiene was associated with norovirus, Shigella, and Salmonella, and also with outbreaks that fitted norovirus-like and vomiting-toxin clinical profiles. Contributing factors were similar for outbreaks with known aetiology and for those where aetiology was assigned by corresponding clinical profile. Rapidly categorizing outbreaks by clinical profile, before results of laboratory testing are available, can help identification of factors which contributed to the occurrence of the outbreak and will promote timely and efficient outbreak investigations.

Salmonella bacteriuria: an increasing entity in elderly women in the United States.

Salmonellosis is a major cause of gastroenteritis in the United States and can lead to septicaemia, and other extra-intestinal illness including urinary tract infections (UTIs). To examine trends in Salmonella bacteriuria in the United States, surveillance data from the National Salmonella Surveillance System from 1980 to the end of 1999 were reviewed. Overall, 17442 urinary Salmonella isolates were reported, representing 2% of all Salmonella isolates from a known source. This proportion increased from 2% during 1980--1984 to 4% during 1995--1999. The median age of persons from whom these isolates came was 51 years; 12,176 (70 %) were women. Compared to the last national survey conducted between 1968 and 1979, the rate of Salmonella bacteriuria increased among women, from 2.0 per million persons in 1980 to 3.7 in 1999; the highest rate occurring in women > or = 70 years. National reporting of Salmonella bacteriuria increased in absolute incidence and as a proportion of all Salmonella, especially in elderly women and may represent an increase in the incidence of Salmonella UTIs. Better understanding of the uropathogenicity of Salmonella serotypes may further clarify the mechanisms of Salmonella UTIs.

A multistate outbreak of Salmonella enterica Serotype Newport infection linked to mango consumption: impact of water-dip disinfestation technology.

Fresh produce increasingly is recognized as an important source of salmonellosis in the United States. In December 1999, the Centers for Disease Control and Prevention detected a nationwide increase in Salmonella serotype Newport (SN) infections that had occurred during the previous month. SN isolates recovered from patients in this cluster had indistinguishable pulsed-field gel electrophoresis (PFGE) patterns (which identified the outbreak strain), suggesting a common source. Seventy-eight patients from 13 states were infected with the outbreak strain. Fifteen patients were hospitalized; 2 died. Among 28 patients enrolled in the matched case-control study, 14 (50%) reported they ate mangoes in the 5 days before illness onset, compared with 4 (10%) of the control subjects during the same period (matched odds ratio, 21.6; 95% confidence interval, 3.53- infinity; P=.0001). Traceback of the implicated mangoes led to a single Brazilian farm, where we identified hot water treatment as a possible point of contamination; this is a relatively new process to prevent importation of an agricultural pest, the Mediterranean fruit fly. This is the first reported outbreak of salmonellosis implicating mangoes. PFGE was critical to the timely recognition of this nationwide outbreak. This outbreak highlights the potential global health impact of foodborne diseases and newly implemented food processes.

Outbreaks of typhoid fever in the United States, 1960-99.

Although the incidence of typhoid fever in the United States has been low since the 1940s, Salmonella Typhi continues to cause outbreaks. We reviewed reported outbreaks of typhoid fever from 1960 to 1999. There were 60 outbreaks; in 54, exposure occurred within the United States. These 54 outbreaks accounted for 957 total cases (median 10) and 4 deaths. In 36 (67%) outbreaks the route of transmission was identified, and in 16 (62%) of the 26 foodborne outbreaks an asymptomatic carrier was identified by culture or serology. The median incubation period was 2 weeks. Isolates from 10 (40%) of 25 outbreaks were phage type E1. The average frequency of outbreaks decreased from 1.85/year during 1960-79 to 0.85/year during 1980-99 (P=0.0001). S. Typhi outbreaks in the United States are generally small in size but can cause significant morbidity, and are often foodborne, warranting thorough investigation.

Salmonella surveillance: a global survey of public health serotyping.

To better understand the global epidemiology of salmonellosis and the national surveillance programmes used for salmonella infections in humans, we conducted a global survey of the 191 WHO Member States. We gathered information on the total number of salmonella isolates serotyped, and the 15 most commonly isolated serotypes from humans in 1990 and 1995. Of the 104 countries that responded, 76 (73.1%) conducted public health surveillance for salmonella and 69 of these (90.8%) conducted serotyping as part of the surveillance. Fifty-nine countries (56.7% of those responding) provided information about the most commonly isolated serotypes in 1995. Three serotypes, Enteritidis, Typhimurium and Typhi accounted for 76.1% of all isolates reported in 1995. One of these three was the most common serotype identified in 93.2% of countries reporting data for that year. In 1995, Enteritidis was the most frequently isolated serotype in 35 countries, followed by Typhi (12 countries) and Typhimurium (8 countries). The global pandemic of Salmonella Enteritidis continued to expand. The mean national proportion of all salmonella isolates that were Enteritidis increased globally from 25.6% in 1990 to 36.3% in 1995. Serotyping is a frequently used component of a public health response to the global challenge of salmonellosis. Support for serotyping as part of national salmonella surveillance, and for rapid international communication of the results via a new WHO electronic website will help target future prevention strategies.

Complaints of foodborne illness in San Francisco, California, 1998.

Foodborne diseases are an important public problem affecting millions of Americans each year and resulting in substantial morbidity and mortality. Many foodborne infections occur in outbreak settings. Outbreaks are often detected by complaints from the public to health authorities. This report reviews complaints received by the San Francisco Department of Public Health involving suspected foodborne illness in 1998. Although such foodborne complaints are commonly received by health officials, we provide the first review of population-based data describing such complaints. We use a broad definition of a foodborne disease outbreak. We judged a complaint to be a "likely foodborne disease outbreak" if it involved more than one person and more than one family; no other common meals were shared recently by ill persons; diarrhea, vomiting, or both was reported; and the incubation period was more than one hour. In 1998, 326 complaints of foodborne illness, involving a total of 599 ill people, were received by the Communicable Disease Control Unit in San Francisco. The complaints involved from 1 to 36 ill persons, with 61% involving one ill person and 25% involving two ill persons. Of the 126 reports involving illness in more than one person, 77 (61%) were judged to be likely foodborne disease outbreaks. Three of these 77 outbreaks had been investigated prior to our review. This project confirms that more foodborne disease outbreaks occur than are reported to state and national outbreak surveillance systems. Our review of the San Francisco system highlights opportunities for gleaning valuable information from the foodborne disease complaint systems in place in most jurisdictions.

PulseNet: the molecular subtyping network for foodborne bacterial disease surveillance, United States.

PulseNet, the national molecular subtyping network for foodborne disease surveillance, was established by the Centers for Disease Control and Prevention and several state health department laboratories to facilitate subtyping bacterial foodborne pathogens for epidemiologic purposes. PulseNet, which began in 1996 with 10 laboratories typing a single pathogen (Escherichia coli O157:H7), now includes 46 state and 2 local public health laboratories and the food safety laboratories of the U.S. Food and Drug Administration and the U.S. Department of Agriculture. Four foodborne pathogens (E. coli O157:H7; nontyphoidal Salmonella serotypes, Listeria monocytogenes and Shigella) are being subtyped, and other bacterial, viral, and parasitic organisms will be added soon.