Dana Cole

Outbreak-associated Salmonella enterica Serotypes and Food Commodities, United States, 1998–2008

Salmonella enterica infections are transmitted not only by animal-derived foods but also by vegetables, fruits, and other plant products. To clarify links between Salmonella serotypes and specific foods, we examined the diversity and predominance of food commodities implicated in outbreaks of salmonellosis during 1998–2008. More than 80% of outbreaks caused by serotypes Enteritidis, Heidelberg, and Hadar were attributed to eggs or poultry, whereas >50% of outbreaks caused by serotypes Javiana, Litchfield, Mbandaka, Muenchen, Poona, and Senftenberg were attributed to plant commodities. Serotypes Typhimurium and Newport were associated with a wide variety of food commodities. Knowledge about these associations can help guide outbreak investigations and control measures.

Distribution, Diversity, and Seasonality of Waterborne Salmonellae in a Rural Watershed

ABSTRACT Salmonella outbreaks from contaminated water and nonanimal foods (e.g., produce) are increasingly reported. To address the environment as a potential source of pathogenic Salmonella, we investigated levels of salmonellae and the geographic and temporal variation of Salmonella serotypes from surface waters in a region of Georgia (United States) with a history of high salmonellosis case rates. Monthly water samples were collected from six stations in the Little River (Upper Suwannee Basin) for 12 months (April 2005 to April 2006). Salmonellae were enumerated using a three-step most-probable-number (MPN) assay. Salmonellae were detected in 57 of the 72 water samples collected (79.2%). Monthly Salmonella densities ranged from an MPN of 2.5 liter−1 in April 2005 to 36.3 liter−1 in August 2005; concentrations were significantly higher in the summer months compared to other seasons (P < 0.05). Concentrations were not significantly different between stations. Levels of salmonellae were correlated with average daily watershed rainfall for the 1 and 2 days preceding each sample collection (r = 0.77 and 0.68, respectively; P < 0.005). Additionally, water temperature was also positively associated with total Salmonella levels (r = 0.44; P < 0.05). In total, 13 S. enterica serotypes were identified among 197 Salmonella isolates. Eighty (40.6%) were identified as S. enterica subsp. arizonae. Muenchen and Rubislaw were the most frequently identified serotypes of the remaining 117 isolates (28 and 26 isolates, respectively). Serotype diversity peaked in the summer, with 9 serotypes observed in August compared to only one serotype (S. enterica subsp. arizonae) observed in April (2005 and 2006) (P < 0.05). Furthermore, all samples collected in August (6/6) contained multiple serotypes (two to five per sample). The results of this study suggest that Salmonella abundance and diversity in the environment vary temporally and are strongly influenced by seasonal precipitation and water temperature.

Evaluation of F+ RNA and DNA coliphages as source-specific indicators of fecal contamination in surface waters.

ABSTRACT Male-specific (F+) coliphages have been investigated as viral indicators of fecal contamination that may provide source-specific information for impacted environmental waters. This study examined the presence and proportions of the different subgroups of F+ coliphages in a variety of fecal wastes and surface waters with well-defined potential waste impacts. Municipal wastewater samples had high proportions of F+ DNA and group II and III F+ RNA coliphages. Bovine wastewaters also contained a high proportion of F+ DNA coliphages, but group I and IV F+ RNA coliphages predominated. Swine wastewaters contained approximately equal proportions of F+ DNA and RNA coliphages, and group I and III F+ RNA coliphages were most common. Waterfowl (gull and goose) feces contained almost exclusively F+ RNA coliphages of groups I and IV. No F+ coliphages were isolated from the feces of the other species examined. F+ coliphage recovery from surface waters was influenced by precipitation events and animal or human land use. There were no significant differences in coliphage density among land use categories. Significant seasonal variation was observed in the proportions of F+ DNA and RNA coliphages. Group I F+ RNA coliphages were the vast majority (90%) of those recovered from surface waters. The percentage of group I F+ RNA coliphages detected was greatest at background sites, and the percentage of group II F+ RNA coliphages was highest at human-impacted sites. Monitoring of F+ coliphage groups can indicate the presence and major sources of microbial inputs to surface waters, but environmental effects on the relative occurrence of different groups need to be considered.

Free-living Canada geese and antimicrobial resistance.

We describe antimicrobial resistance among Escherichia coli isolated from free-living Canada Geese in Georgia and North Carolina (USA). Resistance patterns are compared to those reported by the National Antimicrobial Resistance Monitoring System. Canada Geese may be vectors of antimicrobial resistance and resistance genes in agricultural environments.

Plankton composition and environmental factors contribute to Vibrio seasonality

Plankton represent a nutrient-rich reservoir capable of enriching Vibrio species, which can include human pathogens, at higher densities than the surrounding water column. To better understand the relationship between vibrios and plankton, the partitioning of culturable vibrios, on TCBS, between free living and plankton associated (63–200- and >200-μm-size fractions) was monitored over a 1-year period in coastal waters of Georgia, USA. Seasonal changes in the total Vibrio concentration were then compared with changes in environmental parameters as well as changes in the relative composition of the plankton community. Using univariate analyses, Vibrio concentrations were strongly associated with temperature, especially when those vibrios were plankton associated (R2=0.69 and 0.88 for the water and both plankton fractions; respectively) (P<0.01). Multivariate general linear models revealed that Vibrio concentrations in the plankton fractions were also correlated to shifts in the relative abundance of specific plankton taxa. In the 63–200-μm fraction, Vibrio concentrations were inversely associated with copepods, cyanobacteria and diatoms. In the >200-μm fraction, Vibrio concentrations were positively associated with copepods and negatively associated with decapod larvae. Our results confirm the role of temperature in Vibrio seasonality and highlight an important and independent role for plankton composition in explaining seasonal changes in Vibrio concentration.

Application of Bayesian Techniques to Model the Burden of Human Salmonellosis Attributable to U.S. Food Commodities at the Point of Processing: Adaptation of a Danish Model

Mathematical models that estimate the proportion of foodborne illnesses attributable to food commodities at specific points in the food chain may be useful to risk managers and policy makers to formulate public health goals, prioritize interventions, and document the effectiveness of mitigations aimed at reducing illness. Using human surveillance data on laboratory-confirmed Salmonella infections from the Centers for Disease Control and Prevention and Salmonella testing data from U.S. Department of Agriculture Food Safety and Inspection Services regulatory programs, we developed a point-of-processing foodborne illness attribution model by adapting the Hald Salmonella Bayesian source attribution model. Key model outputs include estimates of the relative proportions of domestically acquired sporadic human Salmonella infections resulting from contamination of raw meat, poultry, and egg products processed in the United States from 1998 through 2003. The current model estimates the relative contribution of chicken (48%), ground beef (28%), turkey (17%), egg products (6%), intact beef (1%), and pork (<1%) across 109 Salmonella serotypes found in food commodities at point of processing. While interpretation of the attribution estimates is constrained by data inputs, the adapted model shows promise and may serve as a basis for a common approach to attribution of human salmonellosis and food safety decision-making in more than one country.

Source Attribution of Human Salmonellosis: An Overview of Methods and Estimates

Reducing the burden of foodborne salmonellosis is challenging. It requires identification of the most important food sources causing disease and prioritization of effective intervention strategies. For this purpose, a variety of methods to estimate the relative contribution of different sources of Salmonella infections have been applied worldwide. Each has strengths and limitations, and the usefulness of each depends on the public health questions being addressed. In this study, we reviewed the source attribution methods and outcomes of several studies developed in different countries and settings, comparing approaches and regional differences in attribution estimates. Reviewed results suggest that illnesses and outbreaks are most commonly attributed to exposure to contaminated food, and that eggs, broiler chickens, and pigs are among the top sources. Although most source attribution studies do not attribute salmonellosis to produce, outbreak data in several countries suggest that exposure to raw vegetables is also an important source. International travel was also a consistently important exposure in several studies. Still, the relative contribution of specific sources to human salmonellosis varied substantially between studies. Although differences in data inputs, methods, and the point in the food system where attribution was estimated contribute to variability between studies, observed differences also suggest regional differences in the epidemiology of salmonellosis.

Distribution and ecology of campylobacters in coastal plain streams (Georgia, United States of America).

ABSTRACT Campylobacter is the leading cause of bacterium-associated diarrhea in the United States and most developed countries. While this disease is considered a food-borne disease, many clinical cases cannot be linked to a food source. In rural and agrarian areas environmental transmission may be an important factor contributing to case loads. Here we investigated the waterborne prevalence of campylobacters in a mixed-use rural watershed in the coastal plain of southern Georgia (United States). Six sites representing various degrees of agricultural and human influence were surveyed biweekly to monthly for 1 year for the presence of culturable thermophilic campylobacters and other measures of water quality. Campylobacters were frequently present in agriculture- and sewage-impacted stretches of streams. The mean campylobacter counts and overall prevalence were highest downstream from a wastewater treatment plant that handled both human and poultry slaughterhouse waste (≤595 CFU ml−1; 100% positive); the concentrations were significantly higher than those for the four upstream sites (P < 0.05). The counts were significantly correlated with the number of fecal coliform bacteria, conductivity, pH, and concentrations of nutrients (NO3−, PO43−, and NH3). Campylobacters were isolated more frequently and larger numbers were present during the summer months, similar to the occurrence of clinical cases of campylobacteriosis in this region. A multivariate model showed that the levels were significantly influenced by increasing precipitation, which also peaked in the summer. The results indicate that loading from both human and domestic animal waste may be high in the watershed studied during the summer months. Mixed-use watersheds supporting agriculture production, human populations, and wildlife may be at risk for contamination by campylobacters and may be an important route for human exposure.

Effect of Salmonella Vaccination of Breeder Chickens on Contamination of Broiler Chicken Carcasses in Integrated Poultry Operations

ABSTRACT 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.

Survey of Biosecurity Protocols and Practices Adopted by Growers on Commercial Poultry Farms in Georgia, U. S. A

Abstract The integrated commercial poultry system is a highly connected network in which routine activities keep farms within a geographic area in constant contact. Consequently, biosecurity practices designed to minimize the transmission of infectious diseases between and within farms are an important component of modern flock health programs. A survey of Georgia poultry growers was conducted in order to assess the level of adoption of standard biosecurity measures by farm personnel and visitors. The results showed that compliance with recommended biosecurity practices did not significantly vary by company, farm size, or number of farms owned by the same grower. However, biosecurity was higher in the northern part of the state, where the density of farms is higher, and where there was an ongoing outbreak of infectious laryngotracheitis at the time of the study. The survey found that growers place more emphasis on biosecurity measures targeting farm visitors than those targeting farm personnel. Most growers reported that all visitors to the farm were required to wear shoe covers, although visitors were not typically required to park outside the farm entrance or to wash tires on their vehicles. No visitor type was reportedly excluded from poultry houses during grow out on all farms. The results highlight the need to evaluate the comparative efficacy of specific biosecurity measures in order to set priorities and attain feasible rates of implementation of targeted biosecurity practices.