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1.  Molecular Phylogeny of the Salmonellae: Relationships among Salmonella Species and Subspecies Determined from Four Housekeeping Genes and Evidence of Lateral Gene Transfer Events▿ †  
Journal of Bacteriology  2008;190(21):7060-7067.
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.
doi:10.1128/JB.01552-07
PMCID: PMC2580703  PMID: 18757540
2.  Epidemic cholera in Mali: high mortality and multiple routes of transmission in a famine area. 
Epidemiology and Infection  1988;100(2):279-289.
During the 1984 cholera epidemic in Mali, 1793 cases and 406 deaths were reported, a death-to-case ratio of 23%. In four affected villages, the mean clinical attack rate was 1.5 and 29% of affected persons died. In 66% of cases the illness began more than 48 h after the village outbreak began, when supplies from outside the village were potentially available. Deaths occurred because patients failed to seek care or received only limited rehydration therapy when they did. Case-control studies identified two routes of transmission: drinking water from one well in a village outside the drought area, and eating left-over millet gruel in a drought-affected village. Drought-related scarcity of curdled milk may permit millet gruel to be a vehicle for cholera. Cholera mortality in the Sahel could be greatly reduced by rapid intervention in affected villages, wide distribution of effective rehydration materials, and educating the population to seek treatment quickly.
PMCID: PMC2249226  PMID: 3356224
3.  PulseNet: the molecular subtyping network for foodborne bacterial disease surveillance, United States. 
Emerging Infectious Diseases  2001;7(3):382-389.
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.
PMCID: PMC2631779  PMID: 11384513
5.  Food-related illness and death in the United States. 
Emerging Infectious Diseases  1999;5(5):607-625.
To better quantify the impact of foodborne diseases on health in the United States, we compiled and analyzed information from multiple surveillance systems and other sources. We estimate that foodborne diseases cause approximately 76 million illnesses, 325,000 hospitalizations, and 5,000 deaths in the United States each year. Known pathogens account for an estimated 14 million illnesses, 60, 000 hospitalizations, and 1,800 deaths. Three pathogens, Salmonella, Listeria, and Toxoplasma, are responsible for 1,500 deaths each year, more than 75% of those caused by known pathogens, while unknown agents account for the remaining 62 million illnesses, 265,000 hospitalizations, and 3,200 deaths. Overall, foodborne diseases appear to cause more illnesses but fewer deaths than previously estimated.
PMCID: PMC2627714  PMID: 10511517
7.  Emerging foodborne diseases: an evolving public health challenge. 
Emerging Infectious Diseases  1997;3(4):425-434.
The epidemiology of foodborne disease is changing. New pathogens have emerged, and some have spread worldwide. Many, including Salmonella, Escherichia coli O157:H7, Campylobacter, and Yersinia enterocolitica, have reservoirs in healthy food animals, from which they spread to an increasing variety of foods. These pathogens cause millions of cases of sporadic illness and chronic complications, as well as large and challenging outbreaks over many states and nations. Improved surveillance that combines rapid subtyping methods, cluster identification, and collaborative epidemiologic investigation can identify and halt large, dispersed outbreaks. Outbreak investigations and case-control studies of sporadic cases can identify sources of infection and guide the development of specific prevention strategies. Better understanding of how pathogens persist in animal reservoirs is also critical to successful long-term prevention. In the past, the central challenge of foodborne disease lay in preventing the contamination of human food with sewage or animal manure. In the future, prevention of foodborne disease will increasingly depend on controlling contamination of feed and water consumed by the animals themselves.
PMCID: PMC2640074  PMID: 9366593
9.  Epidemic cholera in Guatemala, 1993: transmission of a newly introduced epidemic strain by street vendors. 
Epidemiology and Infection  1996;116(2):121-126.
Epidemic cholera reached Guatemala in July 1991. By mid-1993, Guatemala ranked third in the hemisphere in reported cases of cholera. We conducted a case-control study with two age-, sex-, and neighbourhood-matched controls per patient in periurban Guatemala City. Twenty-six patients hospitalized for cholera and 52 controls were enrolled. Seven (47%) of 15 stool cultures obtained after admission yielded toxigenic Vibrio cholerae O1. All seven were resistant to furazolidone, sulfisoxazole, and streptomycin, and differed substantially by pulsed-field gel electrophoresis from the Latin American epidemic strain dominant in the hemisphere since 1991. In univariate analysis, illness was associated with consumption of left-over rice (odds ratio [OR] = 7.0, 95% confidence interval [CI] = 1.4-36), flavored ices (-helados') (OR = 3.6, CI = 1.1 - 12), and street-vended non-carbonated beverages (OR = 3.8, CI = 1.2-12) and food items (OR = 11.0, CI = 2.3-54). Street-vended food items remained significantly associated with illness in multivariate analysis (OR = 6.5, CI = 1.4-31). Illness was not associated with drinking municipal tap water. Maintaining water safety is important, but slowing the epidemic in Guatemala City and elsewhere may also require improvement in street vendor food handling and hygiene.
PMCID: PMC2271612  PMID: 8620902
12.  Dose-response effects in an outbreak of Salmonella enteritidis. 
Epidemiology and Infection  1994;112(1):13-23.
The effects of ingested Salmonella enteritidis (SE) dose on incubation period and on the severity and duration of illness were estimated in a cohort of 169 persons who developed gastroenteritis after eating hollandaise sauce made from grade-A shell eggs. The cohort was divided into three groups based on self-reported dose of sauce ingested. As dose increased, median incubation period decreased (37 h in the low exposure group v. 21 h in the medium exposure group v. 17.5 h in the high exposure group, P = 0.006) and greater proportions reported body aches (71 v. 85 v. 94%, P = 0.0009) and vomiting (21 v. 56 v. 57%, P = 0.002). Among 118 case-persons who completed a follow-up questionnaire, increased dose was associated with increases in median weight loss in kilograms (3.2 v. 4.5 v. 5.0, P = 0.0001), maximum daily number of stools (12.5 v. 15.0 v. 20.0, P = 0.02), subjective rating of illness severity (P = 0.0007), and the number of days of confinement to bed (3.0 v. 6.5 v. 6.5, P = 0.04). In this outbreak, ingested dose was an important determinant of the incubation period, symptoms and severity of acute salmonellosis.
PMCID: PMC2271488  PMID: 8119352
13.  Sources of sporadic Yersinia enterocolitica infections in Norway: a prospective case-control study. 
Epidemiology and Infection  1994;112(1):133-141.
Yersinia enterocolitica is a recognized cause of gastroenteritis in northern Europe. During October 1988-January 1990, a prospective case-control study was performed to address risk factors associated with sporadic Y. enterocolitica infections in southeastern Norway. Sixty-seven case-patients (mean age 23.4 years, range 8 months-88 years) and 132 age-, sex- and geographically-matched controls were enrolled in the study. Multivariate analysis of the data showed that persons with Y. enterocolitica infection reported having eaten significantly more pork items (3.79 v. 2.30 meals, P = 0.02) and sausage (2.84 v. 2.20 meals, P = 0.03) in the 2 weeks before illness onset than their matched controls; only one patient had eaten raw pork. Patients were also more likely than controls to report a preference for eating meat prepared raw or rare (47 v. 27%, P = 0.01), and to report drinking untreated water (39 v. 25%, P = 0.01) in the 2 weeks before illness onset. Each of these factors was independently associated with disease, suggesting a link between yersiniosis and consumption of undercooked pork and sausage products and untreated water. Efforts should be directed towards developing techniques to reduce Y. enterocolitica contamination of pork and educating consumers about (1) proper handling and preparation of pork items and (2) the hazards of drinking untreated water.
PMCID: PMC2271483  PMID: 8119353
14.  Epidemic cholera in Ecuador: multidrug-resistance and transmission by water and seafood 
Epidemiology and Infection  1994;112(1):1-11.
To determine risk factors for cholera in an epidemic-disease area in South America, a case—control investigation was performed in Guayaquil, Ecuador, in July 1991. Residents > 5 years old who were hospitalized for treatment of acute, watery diarrhoea and two matched controls for each were interviewed regarding sources of water and food, and eating, drinking, and hygienic habits. Interviewers inspected homes of case-patients and controls to document water treatment, food-handling, and hygienic practices. Faecal specimens and shellfish were cultured for Vibrio cholerae O 1. Isolates were tested for susceptibility to a variety of antimicrobial agents. Drinking unboiled water (odds ratio [OR] = 4·0, confidence interval [CI] = 1·8—7·5), drinking a beverage from a street vendor (OR = 2·8, CI = 1·3—5·9), eating raw seafood (OR = 3·4, CI = 1·4—11·5), and eating cooked crab (OR = 5·1, CI = 1·4—19·2) were associated with illness. Always boiling drinking water at home (OR = 0·5, CI = 0·2—0·9) was protective against illness. The presence of soap in either the kitchen (OR = 0·3, CI = 0·2—0·8) or bathroom (OR = 0·4, CI = 0·2—0·9) at home was also protective. V. cholerae O 1 was recovered from a pooled sample of a bivalve mollusc and from 68% of stool samples from case-patients. Thirty-six percent of the isolates from stool specimens were resistant to multiple antimicrobial agents. Specific prevention measures may prevent transmission through these vehicles in the future. The appearance of antimicrobial resistance suggests the need for changes in current methods of prevention and treatment.
PMCID: PMC2271476  PMID: 8119348
15.  A comparison of Salmonella enteritidis phage types from egg-associated outbreaks and implicated laying flocks. 
Epidemiology and Infection  1993;110(1):17-22.
Infections due to Salmonella enteritidis are increasing worldwide. In the United States, between 1985 and 1989, 78% of the S. enteritidis outbreaks in which a food vehicle was identified implicated a food containing raw or lightly cooked shell eggs. Under a US Department of Agriculture regulation published in 1990, eggs implicated in human food-borne S. enteritidis outbreaks were traced back to the source flock. The flock environment and the internal organs of a sample of hens were tested for S. enteritidis. We compared the S. enteritidis phage types of isolates from 18 human, egg-associated outbreaks and the 15 flocks implicated through traceback of these outbreaks. The predominant human outbreak phage type was recovered from the environment in 100% of implicated flocks and from the internal organs of hens in 88% of implicated flocks we tested. The results support the use of phage typing as a tool to identify flocks involved in human S. enteritidis outbreaks.
PMCID: PMC2271964  PMID: 8432319
16.  Salmonella enteritidis outbreak in a restaurant chain: the continuing challenges of prevention. 
Epidemiology and Infection  1993;110(1):49-61.
In 1990, a Salmonella enteritidis (SE) outbreak occurred in a restaurant chain in Pennsylvania. To determine its cause(s), we conducted a case-control study and a cohort study at one restaurant, and a survey of restaurants. Egg dishes were associated with illness (P = 0.03). Guests from one hotel eating at the restaurant had a diarrhoeal attack rate of 14%, 4.7-fold higher than among those not eating there (P = 0.04). There were no differences in egg handling between affected and unaffected restaurants. Eggs supplied to affected restaurants were medium grade AA eggs from a single farm, and were reportedly refrigerated during distribution. Human and hen SE isolates were phage type 8 and had similar plasmid profiles and antibiograms. We estimate the prevalence of infected eggs during the outbreak to be as high as 1 in 12. Typical restaurant egg-handling practices and refrigeration during distribution appear to be insufficient by themselves to prevent similar outbreaks.
PMCID: PMC2271955  PMID: 8432323
17.  International increase in Salmonella enteritidis: a new pandemic? 
Epidemiology and Infection  1990;105(1):21-27.
Over the past 5 years Salmonella enteritidis infections in humans have increased on both sides of the Atlantic ocean. The WHO salmonella surveillance data for 1979-87 were reviewed and show that S. enteritidis appears to be increasing on at least the continents of North America, South America, and Europe, and may include Africa. S. enteritidis isolates increased in 24 (69%) of 35 countries between 1979 and 1987. In 1979, only 2 (10%) of 21 countries with reported data reported S. enteritidis as their most common salmonella serotype; in 1987, 9 (43%) of 21 countries reported S. enteritidis as their most common serotype; 8 (89%) of 9 were European countries. Although the reason for the global increase is not yet clear, investigations in individual countries suggest it is related to consumption of eggs and poultry which harbour the organism.
PMCID: PMC2271793  PMID: 2200698
19.  Molecular characterization of Vibrio cholerae O1 strains by pulsed-field gel electrophoresis. 
Journal of Clinical Microbiology  1994;32(7):1685-1690.
Pulsed-field gel electrophoresis (PFGE) was performed on 180 isolates of Vibrio cholerae serogroup O1 representing 6 different multilocus enzyme electrophoresis (MEE) types and 27 rRNA restriction fragment length polymorphism types (ribotypes). Isolates were digested with the restriction enzyme NotI and were separated into 63 patterns on the basis of differences in band arrangements. In general, strains which were different by MEE or ribotyping also had different PGFE patterns. PFGE identified individual strains within a single MEE type or ribotype; isolates with one PFGE pattern were less frequently distinguished by ribotyping. All V. cholerae O1 isolates tested from the Latin American epidemic were indistinguishable by their MEE, ribotype, or PFGE patterns. PFGE could further distinguish strains of this same ribotype isolated in Africa, Europe, the South Pacific, or Southeast Asia. Although both MEE and PFGE could identify the strain from the Latin American epidemic, PFGE was more rapid and less labor intensive. PFGE also distinguished nontoxigenic isolates endemic to the U.S. Gulf Coast from unrelated nontoxigenic isolates. In the present study PFGE was more discriminating than other previously described subtyping assays for V. cholerae O1 and appears to be a useful epidemiologic tool.
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PMCID: PMC263762  PMID: 7929758
20.  Common somatic O and heat-labile serotypes among Campylobacter strains from sporadic infections in the United States. 
Journal of Clinical Microbiology  1993;31(6):1525-1530.
Somatic O (formerly heat-stable) and heat-labile (HL) serotyping methods are commonly used to type Campylobacter jejuni and Campylobacter coli isolates. Although both systems are effective, the labor and time required for each have limited their application. These systems can be simplified by reducing the number of antisera used. To find an appropriate panel of antisera, we determined the distribution of common serotypes in the United States among a representative sample of 298 Campylobacter isolates. The strains, obtained between July 1989 and June 1990 from persons with sporadic cases of diarrhea, were collected from 19 randomly chosen counties in all geographic (census) regions of the United States. All strains were serotyped by the O and HL systems. By phenotypic methods, 288 C. jejuni, 9 hippurate-negative C. jejuni/C. coli, and 1 Campylobacter lari were identified. Of 57 O antisera, 24 typed 252 (84.6%) strains. Of the 55 HL antisera, 23 serotyped 253 (84.9%) strains. All strains were typeable in the unabsorbed O antisera. In the absorbed HL antisera, four strains were nontypeable and 14 were rough and untypeable. In each geographic region, 9 or more O and HL serotypes were found. Serotypes O:1, O:4, and O:13,16,43,50 and HL 1 were identified in all regions. The combination of both schemes gave greater discrimination than either system alone, but the maintenance of both requires a large resource investment. A serotyping scheme incorporating the 24 most prevalent O and 23 most prevalent HL serotypes could be useful for outbreak support and for surveillance. In the near future, we anticipate using a molecular subtyping method in combination with limited serotyping to distinguish Campylobacter strains.
PMCID: PMC265572  PMID: 7686183
21.  Comparison of plasmid profiles, phage types, and antimicrobial resistance patterns of Salmonella enteritidis isolates in the United States. 
Journal of Clinical Microbiology  1992;30(4):854-857.
To evaluate the laboratory techniques for subtyping isolates of Salmonella enteritidis, we compared the plasmid profiles (PP), phage types (PT), and antimicrobial susceptibility patterns (AS) of two nationally representative samples of sporadic human S. enteritidis isolates from 1979 (n = 28) and 1984 (n = 37), 43 isolates from 20 outbreaks of S. enteritidis infections between 1983 and 1987, and 46 animal isolates selected from the U.S. Department of Agriculture Veterinary Services Laboratory in 1986 and 1987. Sporadic and outbreak isolates from humans showed similar rates of resistance to at least one of a panel of antimicrobial drugs (23 and 14%, respectively), PT (91 and 98%, respectively), and PP (97 and 100%, respectively). Sixteen different PP were identified in sporadic, outbreak, and animal isolates; two PP accounted for 76% of sporadic and outbreak isolates. Sporadic human isolates were of PT 8 (42%), of PT 13a (37%), nontypeable (9%), of PT 14b (8%), of PT 9a (3%), and of PT 13 (2%). Outbreak human isolates had similar distributions of PT. PT 8 was associated with poultry: 58% (7 of 12) of the poultry isolates but only 24% (8 of 34) of the isolates from other animals were of PT 8 (P less than 0.04). Although antimicrobial susceptibility patterns do not appear as useful as an epidemiologic marker, PP and PT effectively subtyped S. enteritidis.
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PMCID: PMC265173  PMID: 1572970
22.  Botulism among Alaska Natives. The role of changing food preparation and consumption practices. 
Western Journal of Medicine  1990;153(4):390-393.
Alaska Natives have one of the highest rates of food-borne botulism worldwide. All outbreaks have been associated with the consumption of native foods, but in recent years outbreaks have occurred in previously unaffected areas and have involved new food items. Five botulism outbreaks occurred between 1975 and 1985 in an area of southwestern Alaska without previous confirmed outbreaks and among one ethnic group, the Yupik Eskimo. Of the 5 outbreaks, 3 were associated with fermented beaver tail, a nontraditional native food recently introduced into the region. Preparation techniques vary widely within villages and among ethnic groups. Traditional fermentation techniques have changed over the past 50 years; current preparation methods used by some families and ethnic groups may be more favorable for Clostridium botulinum growth. Prevention efforts should be targeted at high-risk subgroups of Alaska Natives who appear to have modified traditional practices and increased their risk of food-borne botulism.
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PMCID: PMC1002567  PMID: 2244373
23.  Quality of commercially produced Shigella serogrouping and serotyping antisera. 
Journal of Clinical Microbiology  1988;26(3):438-442.
Shigella grouping antisera from five manufacturers and typing antisera from two were purchased and evaluated with homologous and heterologous Shigella strains in the slide agglutination test. Only 31 of 73 (42%) antisera were satisfactory. In many instances, the antisera gave negative, as opposed to weak, reactions when they should have given strong positive reactions. Four reagents cross-reacted with Shigella strains. Of the 19 polyvalent grouping antisera to subgroups Shigella dysenteriae serotypes 1 through 7, S. flexneri serotypes 1 through 6, S. boydii serotypes 1 through 7, and S. sonnei forms I, II, only one S. sonnei reagent and five S. flexneri reagents were satisfactory with greater than or equal to 90% of the homologous strains. The reagent of poorest quality was satisfactory with only 18% of the homologous strains. There were three polyvalent antisera to the higher types of S. dysenteriae and S. boydii, which were available from only one company, that adequately identified 80, 63, and 65% of the homologous strains. Typing antisera were available from only two companies, and 30 of 51 (59%) were satisfactory. Commercially available Shigella antisera are inadequate for the laboratory testing required for planning the development of and evaluating Shigella vaccines.
PMCID: PMC266309  PMID: 3281972
24.  Illness associated with Campylobacter laridis, a newly recognized Campylobacter species. 
Journal of Clinical Microbiology  1985;21(2):222-225.
Campylobacter laridis, a recently described thermophilic Campylobacter species found principally in seagulls, has not previously been linked to illness in humans. Six clinical isolates of this species were referred to the national campylobacter reference laboratory in 1982 and 1983. Each isolate was confirmed by biochemical characterization and by DNA relatedness studies. The six isolates were obtained during an illness: enteritis in four, severe crampy abdominal pain in one, and terminal bacteremia in an immunocompromised host in one. The infections occurred in persons 8 months to 71 years old. Neither the geographic distribution nor the reports of the patients suggest that seagulls played a direct role in the epidemiology of these infections. This potential human enteric pathogen appears to be clinically, epidemiologically, and microbiologically similar to Campylobacter jejuni and may be mistaken for it if nalidixic acid susceptibility screening is not routinely performed.
PMCID: PMC271617  PMID: 3972989

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