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Concept: Salmonella

169

Globally, norovirus is associated with approximately one-fifth of all diarrhea cases, with similar prevalence in both children and adults, and is estimated to cause over 200,000 deaths annually in developing countries. Norovirus is an important pathogen in a number of high-priority domains: it is the most common cause of diarrheal episodes globally, the principal cause of foodborne disease outbreaks in the United States, a key health care-acquired infection, a common cause of travel-associated diarrhea, and a bane for deployed military troops. Partly as a result of this ubiquity and burden across a range of different populations, identifying target groups and strategies for intervention has been challenging. And, on top of the breadth of this public health problem, there remain important gaps in scientific knowledge regarding norovirus, especially with respect to disease in low-income settings. Many pathogens can cause acute gastroenteritis. Historically, rotavirus was the most common cause of severe disease in young children globally. Now, vaccines are available for rotavirus and are universally recommended by the World Health Organization. In countries with effective rotavirus vaccination programs, disease due to that pathogen has decreased markedly, but norovirus persists and is now the most common cause of pediatric gastroenteritis requiring medical attention. However, the data supporting the precise role of norovirus in low- and middle-income settings are sparse. With vaccines in the pipeline, addressing these and other important knowledge gaps is increasingly pressing. We assembled an expert group to assess the evidence for the global burden of norovirus and to consider the prospects for norovirus vaccine development. The group assessed the evidence in the areas of burden of disease, epidemiology, diagnostics, disease attribution, acquired immunity, and innate susceptibility, and the group considered how to bring norovirus vaccines from their current state of development to a viable product that will benefit global health.

Concepts: Salmonella, Vaccine, World Health Organization, Public health, Vaccination, Diarrhea, Immune system, Gastroenteritis

168

Salmonella enterica serovar Heidelberg is among the most detected serovars in swine and poultry, ranks among the top five serotypes associated with human salmonellosis and is disproportionately associated with invasive infections and mortality in humans. Salmonella are known to carry plasmids associated with antimicrobial resistance and virulence. To identify plasmid-associated genes in multidrug resistant S. enterica serovar Heidelberg, antimicrobial resistance plasmids from five isolates were sequenced using the 454 LifeSciences pyrosequencing technology. Four of the isolates contained incompatibility group (Inc) A/C multidrug resistance plasmids harboring at least eight antimicrobial resistance genes. Each of these strains also carried a second resistance plasmid including two IncFIB, an IncHI2 and a plasmid lacking an identified Inc group. The fifth isolate contained an IncI1 plasmid, encoding resistance to gentamicin, streptomycin and sulfonamides. Some of the IncA/C plasmids lacked the full concert of transfer genes and yet were able to be conjugally transferred, likely due to the transfer genes carried on the companion plasmids in the strains. Several non-IncA/C resistance plasmids also carried putative virulence genes. When the sequences were compared to previously sequenced plasmids, it was found that while all plasmids demonstrated some similarity to other plasmids, they were unique, often due to differences in mobile genetic elements in the plasmids. Our study suggests that Salmonella Heidelberg isolates harbor plasmids that co-select for antimicrobial resistance and virulence, along with genes that can mediate the transfer of plasmids within and among other bacterial isolates. Prevalence of such plasmids can complicate efforts to control the spread of S. enterica serovar Heidelberg in food animal and human populations.

Concepts: Plasmid, 1984 Rajneeshee bioterror attack, Molecular biology, Salmonella, Bacteria, DNA, Microbiology, Salmonella enterica

168

Salmonella enterica serotype Typhi (S. Typhi) was estimated to cause over 200,000 deaths and more than 21 million illnesses worldwide, including over 400,000 illnesses in Africa. The current study was conducted in four villages on Pemba Island, Zanzibar, in 2010. We present data on policy makers', health administrators', and village residents' and leaders' perceptions of typhoid fever, and hypothetical and actual health care use among village residents for typhoid fever. Qualitative data provided descriptions of home-based treatment practices and use of western pharmaceuticals, and actual healthcare use for culture-confirmed typhoid fever. Survey data indicate health facility use was associated with gender, education, residency, and perceptions of severity for symptoms associated with typhoid fever. Data have implications for education of policy makers and health administrators, design and implementation of surveillance studies, and community-based interventions to prevent disease outbreaks, decrease risks of complications, and provide information about disease recognition, diagnosis, and treatment.

Concepts: Epidemiology, Typhoid fever, Health, Salmonella, Zanzibar, Health care, Salmonella enterica, Medicine

141

An outbreak of salmonellosis occurred following attendance at a school camp between 5 and 8 August 2014 in a remote area of the Northern Territory, Australia. We conducted a retrospective cohort study via telephone interviews, using a structured questionnaire that recorded symptoms and exposures to foods and activities during the camp. A case was anyone with laboratory confirmed Salmonella Saintpaul infection or a clinically compatible illness after attending the camp. Environmental health officers from the Environmental Health Branch undertook an investigation and collected water and environmental samples. We interviewed 65 (97%) of the 67 people who attended the camp. There were 60 students and 7 adults. Of the 65 people interviewed, 30 became ill (attack rate 46%); all were students; and 4 had laboratory confirmed S. Saintpaul infection. The most commonly reported symptoms were diarrhoea (100% 30/30), abdominal pain (93% 28/30), nausea (93% 28/30) and fever (70% 21/30). Thirteen people sought medical attention but none required hospitalisation. Illness was significantly associated with drinking cordial at lunch on 7 August (RR 3.8, 95% CI 1.3-11, P < 0.01), as well as drinking cordial at lunch on 8 August (RR 2.1, 95% CI 1.1-4.2, P=0.01). Salmonella spp. was not detected in water samples or wallaby faeces collected from the camp ground. The epidemiological investigation suggests the outbreak was caused by environmental contamination of food or drink and could have occurred during ice preparation or storage, preparation of the cordial or from inadequate sanitising of the cooler from which the cordial was served. This outbreak highlights the risks of food or drink contamination with environmental Salmonella. Those preparing food and drink in campground settings should be vigilant with cleaning, handwashing and disinfection to prevent outbreaks of foodborne disease.

Concepts: Diarrhea, Environmental health officer, Illness, Cohort study, Epidemiology, Gastroenteritis, Salmonella, Foodborne illness

141

We show in this report that traces of juices released from salad leaves as they became damaged can significantly enhance Salmonella enterica salad leaf colonisation. Salad juices in water increased Salmonella growth by 110% over the un-supplemented control, and in host-like serum based media by more than 2400-fold over controls. In serum based media salad juices induced growth of Salmonella via provision of Fe from transferrin, and siderophore production was found to be integral to the growth induction process. Other aspects relevant to salad leaf colonisation and retention were enhanced, such as motility and biofilm formation, which increased over controls by >220% and 250% respectively; direct attachment to salad leaves increased by >350% when a salad leaf juice was present. In terms of growth and biofilm formation the endogenous salad leaf microbiota was largely unresponsive to leaf juice, suggesting that Salmonella gains a marked advantage from fluids released from salad leaf damage. Salad leaf juices also enhanced pathogen attachment to the salad bag plastic. Over 5 days refrigeration (a typical storage time for bagged salad leaves) even traces of juice within the salad bag fluids increased Salmonella growth in water by up to 280-fold over control cultures, as well as enhancing salad bag colonisation, which could be an unappreciated factor in pathogen fresh produce retention. Collectively, this study shows that exposure to salad leaf juice may contribute to the persistence of Salmonella on salad leaves, and strongly emphasizes the importance of ensuring the microbiological safety of fresh produce.

Concepts: Lettuce, Salmonella enterica, Salmonella, Bacteria, Iron, Leaf vegetable, Leaf, Microbiology

113

The microbiological safety of fresh produce is monitored almost exclusively by culture-based detection methods. However, bacterial food-borne pathogens are known to enter a viable-but-nonculturable (VBNC) state in response to environmental stresses such as chlorine, which is commonly used for fresh produce decontamination. Here, complete VBNC induction of green fluorescent protein-tagged Listeria monocytogenes and Salmonella enterica serovar Thompson was achieved by exposure to 12 and 3 ppm chlorine, respectively. The pathogens were subjected to chlorine washing following incubation on spinach leaves. Culture data revealed that total viable L. monocytogenes and Salmonella Thompson populations became VBNC by 50 and 100 ppm chlorine, respectively, while enumeration by direct viable counting found that chlorine caused a <1-log reduction in viability. The pathogenicity of chlorine-induced VBNC L. monocytogenes and Salmonella Thompson was assessed by using Caenorhabditis elegans Ingestion of VBNC pathogens by C. elegans resulted in a significant life span reduction (P = 0.0064 and P < 0.0001), and no significant difference between the life span reductions caused by the VBNC and culturable L. monocytogenes treatments was observed. L. monocytogenes was visualized beyond the nematode intestinal lumen, indicating resuscitation and cell invasion. These data emphasize the risk that VBNC food-borne pathogens could pose to public health should they continue to go undetected.IMPORTANCE Many bacteria are known to enter a viable-but-nonculturable (VBNC) state in response to environmental stresses. VBNC cells cannot be detected by standard laboratory culture techniques, presenting a problem for the food industry, which uses these techniques to detect pathogen contaminants. This study found that chlorine, a sanitizer commonly used for fresh produce, induces a VBNC state in the food-borne pathogens Listeria monocytogenes and Salmonella enterica It was also found that chlorine is ineffective at killing total populations of the pathogens. A life span reduction was observed in Caenorhabditis elegans that ingested these VBNC pathogens, with VBNC L. monocytogenes as infectious as its culturable counterpart. These data show that VBNC food-borne pathogens can both be generated and avoid detection by industrial practices while potentially retaining the ability to cause disease.

Concepts: 1984 Rajneeshee bioterror attack, Caenorhabditis, Salmonella, Listeria monocytogenes, Caenorhabditis elegans, Salmonella enterica, Bacteria, Microbiology

103

Backyard poultry flocks have increased in popularity concurrent with an increase in live poultry-associated salmonellosis (LPAS) outbreaks. Better understanding of practices that contribute to this emerging public health issue is needed. We reviewed outbreak reports to describe the epidemiology of LPAS outbreaks in the United States, examine changes in trends, and inform prevention campaigns. LPAS outbreaks were defined as ≥2 culture-confirmed human Salmonella infections linked to live poultry contact. Outbreak data were obtained through multiple databases and a literature review. During 1990-2014, a total of 53 LPAS outbreaks were documented, involving 2,630 illnesses, 387 hospitalizations, and 5 deaths. Median patient age was 9 years (range <1 to 92 years). Chick and duckling exposure were reported by 85% and 38% of case-patients, respectively. High-risk practices included keeping poultry inside households (46% of case-patients) and kissing birds (13%). Comprehensive One Health strategies are needed to prevent illnesses associated with live poultry.

Concepts: Foodborne illness, Health care, Salmonellosis, Salmonella, United States, Health, Public health, Epidemiology

66

Crohn’s disease (CD) is a chronic inflammatory condition of diverse etiology. Exposure to foodborne pathogens causing acute gastroenteritis produces a long-term risk of CD well into the post-infectious period but the mechanistic basis for this ongoing relationship to disease onset is unknown. We developed two novel models to study the comorbidity of acute gastroenteritis caused by Salmonella Typhimurium or Citrobacter rodentium in mice colonized with adherent-invasive Escherichia coli (AIEC), a bacterial pathobiont linked to CD. Here, we show that disease activity in the post-infectious period after gastroenteritis is driven by the tissue-associated expansion of the resident AIEC pathobiont, with an attendant increase in immunopathology, barrier defects, and delays in mucosal restitution following pathogen clearance. These features required AIEC resistance to host defense peptides and a fulminant inflammatory response to the enteric pathogen. Our results suggest that individuals colonized by AIEC at the time of acute infectious gastroenteritis may be at greater risk for CD onset. Importantly, our data identify AIEC as a tractable disease modifier, a finding that could be exploited in the development of therapeutic interventions following infectious gastroenteritis in at-risk individuals.

Concepts: Bacteria, Immune system, Microbiology, Salmonella, Foodborne illness, Escherichia coli, Diarrhea, Gastroenteritis

48

Illness and death from diseases caused by contaminated food are a constant threat to public health and a significant impediment to socio-economic development worldwide. To measure the global and regional burden of foodborne disease (FBD), the World Health Organization (WHO) established the Foodborne Disease Burden Epidemiology Reference Group (FERG), which here reports their first estimates of the incidence, mortality, and disease burden due to 31 foodborne hazards. We find that the global burden of FBD is comparable to those of the major infectious diseases, HIV/AIDS, malaria and tuberculosis. The most frequent causes of foodborne illness were diarrheal disease agents, particularly norovirus and Campylobacter spp. Diarrheal disease agents, especially non-typhoidal Salmonella enterica, were also responsible for the majority of deaths due to FBD. Other major causes of FBD deaths were Salmonella Typhi, Taenia solium and hepatitis A virus. The global burden of FBD caused by the 31 hazards in 2010 was 33 million Disability Adjusted Life Years (DALYs); children under five years old bore 40% of this burden. The 14 subregions, defined on the basis of child and adult mortality, had considerably different burdens of FBD, with the greatest falling on the subregions in Africa, followed by the subregions in South-East Asia and the Eastern Mediterranean D subregion. Some hazards, such as non-typhoidal S. enterica, were important causes of FBD in all regions of the world, whereas others, such as certain parasitic helminths, were highly localised. Thus, the burden of FBD is borne particularly by children under five years old-although they represent only 9% of the global population-and people living in low-income regions of the world. These estimates are conservative, i.e., underestimates rather than overestimates; further studies are needed to address the data gaps and limitations of the study. Nevertheless, all stakeholders can contribute to improvements in food safety throughout the food chain by incorporating these estimates into policy development at national and international levels.

Concepts: Food safety, Infectious disease, Epidemiology, Salmonella enterica, Foodborne illness, Gastroenteritis, Microbiology, Salmonella

37

Salmonella is a leading cause of acute gastroenteritis worldwide. Patterns of salmonellosis have been linked to weather events. However, there is a dearth of data regarding the association between extreme events and risk of salmonellosis, and how this risk may disproportionately impact coastal communities.

Concepts: Extreme weather, Diarrhea, Climate, Climate change, Gastroenteritis, 1984 Rajneeshee bioterror attack, Weather, Salmonella