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Abstract

Salmonella serotypes linked to tomato-associated outbreaks were evaluated for survival in soil and water over a 40-day period. Salmonella enterica serotypes Anatum, Baildon, Braenderup, Montevideo, Newport, and Javiana were inoculated separately into sterile soil and water, followed by plating onto TSAYE and XLT4 at 10-day intervals. Biofilm production by Salmonella serotypes was measured on both quartz particles (soil surrogate) and glass coverslips, and was evaluated using a crystal violet dye assay. Salmonella populations in soil and water over 40 days indicated no significant differences between Salmonella serotypes tested (p > 0.05). Over a 40-day period, there was a 1.84-0.22 log CFU/g and 1.56-0.54 CFU/mL decrease in populations of Salmonella in soil and water, respectively. Enumeration indicated that Salmonella population fluctuated in water but decreased linearly in soil. All serotypes tested produced the ''red dry and rough'' morphotype on Congo Red agar. Biofilm produced by all the Salmonella serotypes tested was significantly different on quartz particles than on glass coverslips (p < 0.0001), indicating that material and surface characteristics could affect biofilm development. The ability of Salmonella serotypes to persist in soil or water and attach to abiotic surfaces through biofilm formation affirms that contact surfaces, soil, water, and sediment should be considered as possible sources of cross-contamination in the farm environment.

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... Wetland coverage is considerably diminished in Connecticut [66] and agricultural production covers the smallest area of the included states [67]; however, approximately 23% of its population are served by private well systems [68] compared to the national estimated average of 13% [69]. This could underscore the importance of private well contamination following periods of excessive rainfall, as well as the persistence of Salmonella serovars, such as S. Javiana in the soil and water [53,70,71]. ...
... S. Newport has also been found to survive for extensive periods of time in soil and water [53,70], particularly in moist organic soil [71] which is prevalent in Maryland [72]. Studies have found that both extreme heat and precipitation can lead to an increased prevalence of Salmonella in crops such as lettuce, either through internalization or transfer of pathogens with contaminated surface waters [54]. ...
... Overall, our study indicated a stronger association between extreme precipitation events and salmonellosis across the U.S., compared to extreme heat events. Previous works have described the role of excessive rainfall in the proliferation of Salmonella in the soil, water, and a range of food commodities [12,19,61,62,70,73]. Furthermore, the elevated risk of Salmonella infection associated with poultry and livestock reservoirs, as observed with S. Typhimurium and S. Enteriditis [4], may be of special consideration even in states without large animal production facilities, such as Oregon and New Mexico [67]. ...
Article
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Background Infections with nontyphoidal Salmonella cause an estimated 19,336 hospitalizations each year in the United States. Sources of infection can vary by state and include animal and plant-based foods, as well as environmental reservoirs. Several studies have recognized the importance of increased ambient temperature and precipitation in the spread and persistence of Salmonella in soil and food. However, the impact of extreme weather events on Salmonella infection rates among the most prevalent serovars, has not been fully evaluated across distinct U.S. regions. Methods To address this knowledge gap, we obtained Salmonella case data for S. Enteriditis, S. Typhimurium, S. Newport, and S. Javiana (2004-2014; n = 32,951) from the Foodborne Diseases Active Surveillance Network (FoodNet), and weather data from the National Climatic Data Center (1960-2014). Extreme heat and precipitation events for the study period (2004-2014) were identified using location and calendar day specific 95th percentile thresholds derived using a 30-year baseline (1960-1989). Negative binomial generalized estimating equations were used to evaluate the association between exposure to extreme events and salmonellosis rates. Results We observed that extreme heat exposure was associated with increased rates of infection with S. Newport in Maryland (Incidence Rate Ratio (IRR): 1.07, 95% Confidence Interval (CI): 1.01, 1.14), and Tennessee (IRR: 1.06, 95% CI: 1.04, 1.09), both FoodNet sites with high densities of animal feeding operations (e.g., broiler chickens and cattle). Extreme precipitation events were also associated with increased rates of S. Javiana infections, by 22% in Connecticut (IRR: 1.22, 95% CI: 1.10, 1.35) and by 5% in Georgia (IRR: 1.05, 95% CI: 1.01, 1.08), respectively. In addition, there was an 11% (IRR: 1.11, 95% CI: 1.04-1.18) increased rate of S. Newport infections in Maryland associated with extreme precipitation events. Conclusions Overall, our study suggests a stronger association between extreme precipitation events, compared to extreme heat, and salmonellosis across multiple U.S. regions. In addition, the rates of infection with Salmonella serovars that persist in environmental or plant-based reservoirs, such as S. Javiana and S. Newport, appear to be of particular significance regarding increased heat and rainfall events.
... Similar to previous studies, we found that Salmonella survived up to 60 dpi in soil (Dev Kumar et al., 2018). However, some serovars (Poona and Typhimurium) were undetectable using standard culture methods in soil by 60 dpi. ...
... However, some serovars (Poona and Typhimurium) were undetectable using standard culture methods in soil by 60 dpi. Dev Kumar et al. (2018) showed that, while Salmonella survived over a period of 40 dpi, populations decreased by 30 and 40 dpi due to cell injury. In previous studies, the survival and persistence of Salmonella in the soil environment was attributed to the ability of the bacteria to form biofilms (Dev Kumar et al., 2018;Kumar and Micallef, 2017). ...
... Dev Kumar et al. (2018) showed that, while Salmonella survived over a period of 40 dpi, populations decreased by 30 and 40 dpi due to cell injury. In previous studies, the survival and persistence of Salmonella in the soil environment was attributed to the ability of the bacteria to form biofilms (Dev Kumar et al., 2018;Kumar and Micallef, 2017). Investigation of biofilm production potential for those serovars demonstrating the best long-term survival would be an interesting avenue for future research. ...
Article
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Cantaloupes have emerged as significant vehicles of widespread foodborne illness outbreaks caused by bacterial pathogens, including Salmonella. The purpose of this study was to investigate the efficiency of Salmonella colonization and internalization in cantaloupes by relevant routes of contamination. Cantaloupe plants (Cucumis melo ‘reticulatus’) from two cultivars ‘Athena’ (Eastern) and ‘Primo’ (Western) were grown from commercial seed. Plants were maintained in the NCSU BSL-3P phytotron greenhouse. Salmonella enterica (a cocktail of cantaloupe-associated outbreak serovars Javiana, Newport, Panama, Poona and Typhimurium) contamination was introduced via blossoms or soil at ca. 4.4 log10 CFU/blossom or 8.4 log10 CFU/root zone, respectively. Cantaloupes were analyzed for Salmonella by enrichment in accordance with modified FDA-BAM methods. Five randomly chosen colonies from each Salmonella-positive sample were typed using the Agilent 2100 bioanalyzer following multiplex PCR. Data were analyzed for prevalence of contamination and serovar predominance in fruit, stems and soil. Of the total cantaloupe fruit harvested from Salmonella-inoculated blossoms (n = 63), 89% (56/63) were externally contaminated and 73% (46/63) had Salmonella internalized into the fruit. Serovar Panama was the most commonly isolated from the surface of fruit while S. Panama and S. Poona were the most prevalent inside the fruit. When soil was inoculated with Salmonella at one day post-transplant, 13% (8/60) of the plants were shown to translocate the organism to the lower stem (ca. 4 cm) by 7 days post-inoculation (dpi). We observed Salmonella persistence in the soil up to 60 dpi with S. Newport being the predominant serovar at 10 and 20 dpi. These data demonstrate that contaminated soil and blossoms can lead to Salmonella internalization into the plant or fruit at a relatively high frequency.
... According to the Centers for Disease Control and Prevention, from 2006 to 2019, foodborne outbreaks of the Salmonella serotypes Newport, Infantis, and Typhimurium were linked to the consumption of fresh products with maradol papaya, cucumber, cantaloupe, avocado, tomato, frozen raw tuna, and other products in the United States [2]. The ability of Salmonella serotypes to form biofilms has been demonstrated on stainless steel and polyethylene food contact surfaces or on polystyrene, glass, plastic, cement, and rubber [3,4]. In fact, biofilms formed in food processing environments are a constant source of microbial contamination that may lead to food spoilage or Appl. ...
... isolated from raw poultry. In addition, Dev-Kumar et al. [4] and Tassinari et al. [38] reported the rdar morphotype on CRA at 28 • C in monophasic Salmonella Typhimurium, Salmonella Anatum, Salmonella Baildon, Salmonella Braenderup, Salmonella Javiana, Salmonella Montevideo, and Salmonella Newport isolated from water sources, feed, the environment, and feces. In contrast, Trmcic et al. [28] reported that Salmonella Newport isolated from humans and Salmonella Typhimurium and Salmonella Enteritidis isolated from irrigation water exhibited the sar morphotype, while Salmonella Daytona isolated from irrigation water exhibited the bdar morphotype on CRA. ...
Article
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Salmonella serotypes can develop biofilms in fresh food products. This study focused on determining the antimicrobial resistance profile and the effects of different growth media and environmental conditions on biofilm formation by multidrug-resistant serotypes of Salmonella. All 49.4% of the Salmonella strains (five serotypes) were multidrug resistant. Assessment of the ability to form biofilms using the crystal violet staining method revealed that 95.6% of the strains of Salmonella were strong biofilm producers in 96-well polystyrene microtiter plates. Overall, 59.3% of the Salmonella strains showed the rdar (red dry and rough colony) morphotype, 2.1% pdar (pink dry and rough colony), 27.4% bdar (brown dry and rough colony) and 10.9% saw (smooth and white colony), at two temperatures (22 and 35 °C). Mono-species biofilms of Salmonella serotypes showed a mean cell density of 8.78 log10 CFU/cm2 ± 0.053 in TSBS (1/20 diluted TSB (tryptic soy broth) + 1% strawberry residues) and 8.43 log10 CFU/cm2 ± 0.050 in TSBA (1/20 diluted TSB + 1% avocado residues) on polypropylene type B (PP) (p < 0.05). In addition, epifluorescence microscopy and scanning electron microscopy (SEM) enabled visualizing the bacteria and extracellular polymeric substances of biofilms on PP. Salmonella form biofilms depending on the serotype of the strains and the environmental conditions. Mono-species biofilms formed by Salmonella serotypes respond to nutrient limitation with the use of simplified culture media such as TSBA and TSBS.
... In addition to dispersal and colonization via water, Salmonella have been shown to survive for long periods of time in the environment (Kumar et al., 2018). For example, Salmonella was shown to survive in the soil environment over a period of 40 days (Kumar et al., 2018). ...
... In addition to dispersal and colonization via water, Salmonella have been shown to survive for long periods of time in the environment (Kumar et al., 2018). For example, Salmonella was shown to survive in the soil environment over a period of 40 days (Kumar et al., 2018). They are able to transition between hosts and can survive and persist under harsh desiccant and temperature conditions and exposure to UV radiation, all of which are common to the agricultural environment (reviewed in Brandl, 2006;Fatica and Schneider, 2011). ...
Article
Consumption of cucumbers (Cucumis sativus var. sativus) has been linked to several foodborne outbreaks involving Salmonella enterica. The purpose of this work was to investigate the efficiency of colonization and internalization of S. enterica into cucumber plants by various routes of contamination. Produce-associated outbreak strains of Salmonella (a cocktail of serovars Javiana, Montevideo, Newport, Poona, and Typhimurium) were introduced to three cultivars of cucumber plants (two slicing cultivars and one pickling) via blossoms (ca. 6.4 log10 CFU/blossom, 4.5 log10 CFU/blossom, or 2.5 log10 CFU/blossom) or soil (ca. 8.3 log10 CFU/root zone) and were analyzed for prevalence of Salmonella contamination (internal and external) and serovar predominance in fruit and stems. Of the total slicing fruit harvested from Salmonella-inoculated blossoms (ca. 6.4, 4.5, or 2.5 log10 CFU/blossom), 83.9% (47/56), 81.4% (48/59) or 71.2% (84/118) were found colonized and 67.9% (38/56), 35.6% (21/59) or 22.0% (26/118) had Salmonella internalized into the fruit, respectively. S. Poona was the most prevalent serovar isolated on or in cucumber fruits at all inoculation levels. When soil was inoculated at 1 day post-transplant (dpt), 8% (10/120) of the plants were shown to translocate Salmonella to the lower stem 7 days post-inoculation (dpi). Results identified blossoms as an important route by which Salmonella internalized at a high percentage into cucumbers, and S. Poona, the same strain isolated from the 2015 outbreak of cucumbers imported from Mexico, was shown to be well-adapted to the blossom niche.
... Airborne soil particulates have been shown to serve as vehicles for Salmonella contamination of plants (Kumar et al. 2017). Outbreak-associated Salmonella serotypes have been shown to survive in soil and water for a long time-more than 40 days in soil-and the role of biofilms in abiotic surface attachment has been investigated (Kumar et al. 2018). In investigations dealing with fitness of human enteric pathogens on plants and plant environments, Salmonella has been shown to be a resilient organism under stressful plant cultivation environments with respect to water, temperature, and UV radiation (Brandl 2006, Fatica andSchneider 2011). ...
... This is consistent with the abundance of data showing robust survival abilities of Salmonella spp. (Stocker and Makela 1986;Rychlik and Barrow 2005;Semenov et al. 2011;Jacobson et al. 2017;Spector and Kenyon 2012;Kumar et al. 2018). ...
Article
Aims: This study measured the survival of Listeria monocytogenes and Salmonella enterica subsp. enterica serovar Javiana over a 10-day period on four soil-free cultivation matrix (SFCM) types in the absence of microgreens and fertilizers. Methods and results: Coco coir (CC), a Sphagnum peat/vermiculite mix, Biostrate® , and hemp mat samples were inoculated with 3 x 106 CFU mL-1 bacteria, incubated at room temperature, and analyzed on day 0, 1, 3, 6, and 10. Statistically significant differences in pathogen survival were observed across multiple time points for hemp and Biostrate® compared to CC, peat, and bacteria in PBS (p<0.05). S. Javiana showed greater overall survival compared to Listeria (p<0.0002). By day 10, S. Javiana persisted at the initial inoculum concentration for hemp and Biostrate® while declining by 1-2 log CFU mL-1 in CC, peat, and PBS. Listeria also persisted at the initial concentration in hemp and Biostrate® but decreased to 1 log CFU mL-1 in peat and below the detection limit in CC and PBS. Conclusions: Overall, there are survival differences between bacterial pathogens in SFCM used in microgreen production systems. To our knowledge, this is the first comparison of survival among SFCM involving a S. enterica serovar and L. monocytogenes, and the first study comparing CC, Biostrate® , and hemp. Significance and impact of the study: Microgreens production systems predominantly utilize soil alternatives, and it is not well understood how pathogen transmission risk may be affected by the type of soil-free cultivation matrix (SFCM). The results of this study impact the microgreen industry as media selection may be used to reduce the risk of bacterial pathogen proliferation and transmission to the plant potentially resulting in potential foodborne illness.
... Increased production efforts toward organic, local, and sustainable practices in poultry products have been commercialized due to consumer demand (Oberholtzer et al., 2006;Sossidou et al., 2011). It is important to analyze the risk associated with these types of farming practices since pathogens such as Salmonella can be present in the pastured poultry farm environments, and even form biofilms (Kumar et al., 2018;Kumar and Micallef, 2017). According to the American Pastured Poultry Producers Association (APPPA), pastured poultry farming practices involve floorless pens that provide protection. ...
Article
Consumer demand has increased for pastured poultry products as the drive for sustainable farming practices and ethical treatments of livestock have become popular in the press. It is necessary to identify the important meteorological factors associated with the prevalence of Salmonella in the pastured poultry settings since the presence of Salmonella in the environment could lead to contamination of the final product. The objective of this study was to develop a model to describe the relationship between meteorological factors and the presence of Salmonella on the pastured poultry farms. The random forest method was used to develop a model where 83 meteorological factors were included as the predicting variables. The soil model identified humidity as the most important variable associated with Salmonella prevalence, while high wind gust speed and average temperature were identified as important meteorological variables in the feces model. The developed models were robust in predicting the prevalence of Salmonella in pastured poultry farms with the area under receiver operating characteristic (ROC) curve values of 0.884 and 0.872 for the soil model and feces model, respectively. The predictive models developed in this study can provide users with practical and effective tools to make informed decisions with scientific evidence regarding the meteorological parameters that are important to monitor for increased on-farm Salmonella prevalence.
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In the U.S., tomatoes have become the most implicated vehicle for produce-associated Salmonellosis with 12 outbreaks since 1998. Although unconfirmed, trace backs suggest pre-harvest contamination with Salmonella enterica. Routes of tomato crop contamination by S. enterica in the absence of direct artificial inoculation have not been investigated. This work examined the role of contaminated soil, the potential for crop debris to act as inoculum from one crop to the next, and any interaction between the seedbourne plant pathogen Xanthomonas campestris pv. vesicatoria and S. enterica on tomato plants. Our results show S. enterica can survive for up to six weeks in fallow soil with the ability to contaminate tomato plants. We found S. enterica can contaminate a subsequent crop via crop debris; however a fallow period between crop incorporation and subsequent seeding can affect contamination patterns. Throughout these studies, populations of S. enterica declined over time and there was no bacterial growth in either the phyllosphere or rhizoplane. The presence of X. campestris pv. vesicatoria on co-colonized tomato plants had no effect on the incidence of S. enterica tomato phyllosphere contamination. However, growth of S. enterica in the tomato phyllosphere occurred on co-colonized plants in the absence of plant disease. S. enterica contaminated soil can lead to contamination of the tomato phyllosphere. A six week lag period between soil contamination and tomato seeding did not deter subsequent crop contamination. In the absence of plant disease, presence of the bacterial plant pathogen, X. campestris pv. vesicatoria was beneficial to S. enterica allowing multiplication of the human pathogen population. Any event leading to soil contamination with S. enterica could pose a public health risk with subsequent tomato production, especially in areas prone to bacterial spot disease.
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The efficacy of ozone and ultraviolet light (UV) treatment as hurdles against Listeria monocytogenes suspended in fresh (9% NaCl, 91.86% transmittance) and spent brines (20.5% NaCl, 0.01% transmittance) was evaluated. Brines were inoculated with a cocktail of L. monocytogenes-strains N1-227, N3-031, and R2-499. Ozonation was performed by sparging gaseous ozone into brine. This was followed by UV irradiation (253.7 nm) of the brine in sterile quartz cuvettes. Enumeration was performed by spread plating on modified Oxford medium and Trypticase Soy agar supplemented with yeast extract. In fresh brines containing L. monocytogenes, ten minutes of ozonation lead to a 7.44±0.13 log CFU/ml mean reduction and 10 minutes of UV radiation caused a 1.95±0.41 log CFU/ml mean reduction. Sequential exposure of ten minutes of ozonation and UV resulted in > 9 log CFU/ml reduction in L. monocytogenes populations in fresh brine. Sixty minutes of ozonation of spent brines resulted in a 4.85±0.61 log CFU/ml mean reduction of L. monocytogenes populations. Ten minutes of UV exposure in spent brines resulted in 0.49±0.14 log CFU/ml mean reduction in L. monocytogenes. A sequential treatment of 60 minutes ozonation and 10 minute UV resulted in an excess of 5 log CFU/ml reduction in L. monocytogenes cells in spent brine. Ozonation did not cause a significant increase in the transmittance of the spent brine to aid UV penetration but resulted in color change. Sequential treatments of Ozonation andUV maybe effective in reducing L. monocytogenes in chill brines.
Article
Irrigation water has been implicated as a likely source of produce contamination by Salmonella enterica. Therefore, the distribution of S. enterica was surveyed monthly in irrigation ponds (n=10) located within a prime agricultural region in Southern Georgia and Northern Florida. All ponds and 28.2% of all samples (n=635) were positive for Salmonella with an overall geometric mean concentration (0.26 MPN/L) that was relatively low compared to prior reports for rivers in this region. Salmonella peaks were seasonal; levels correlated with increased temperature and rainfall (p<0.05). Numbers and occurrence were significantly higher in water (0.32 MPN/L and 37%) compared to sediment (0.22 MPN/L and 17%) but did not vary with depth. Representative isolates (n=185) from different ponds, sample types, and seasons were examined for resistance to 15 different antibiotics; most strains were resistant to streptomycin (98.9%), while 20% were multidrug resistant (MDR) for 2-6 antibiotics. DiversiLab rep-PCR revealed genetic diversity and showed 43 genotypes among 191 isolates, as defined by >95% similarity. Genotypes did not partition by pond, season, or sample type. Genetic similarity to known serotypes indicated Hadar, Montevideo, and Newport as the most prevalent. All ponds achieved the current safety standards for generic Escherichia coli in agricultural water, and regression modeling showed E. coli levels were a significant predictor for the probability of Salmonella occurrence. However, persistent populations of Salmonella were widely distributed in irrigation ponds, and associated risks for produce contamination and subsequent human exposure are unknown, supporting continued surveillance of this pathogen in agricultural settings. Copyright © 2015, American Society for Microbiology. All Rights Reserved.
Article
We examined multistate outbreaks attributed to raw tomatoes in the United States from 1990 to 2010. We summarized the demographic and epidemiological characteristics of 15 outbreaks resulting in 1959 illnesses, 384 hospitalizations, and three deaths. Most (80%) outbreaks were reported during 2000–2010; 73% occurred May–September. Outbreaks commonly affected adult (median age 34 years) women (median 58% of outbreak cases). All outbreaks were caused by Salmonella [serotypes Newport ( n = 6 outbreaks), Braenderup ( n = 2), Baildon, Enteritidis, Javiana, Montevideo, Thompson, Typhimurium ( n = 1 each); multiple serotypes ( n = 1)]. Red, round (69% of outbreaks), Roma (23%), and grape (8%) tomatoes were implicated. Most (93%) outbreaks were associated with tomatoes served predominantly in restaurants. However, traceback investigations suggested that contamination occurred on farms, at packinghouses, or at fresh-cut processing facilities. Government agencies, academia, trade associations, and the fresh tomato industry should consider further efforts to identify interventions to reduce contamination of tomatoes during production and processing.
Article
Several methods were used to study survival of Salmonella typhimurium LT2 in soil. An ion exchange resin-based extraction method was used to concentrate biomass from soil, from which DNA was extracted in order to quantify a Salmonella-specific sequence by a quantitative polymerase chain reaction (QPCR). S. typhimurium LT2 was detected at a minimum density of 103 cells g−1 in non-sterile soil, and the method proved to be specific for this organism in microcosm experiments. Non-sterile soil microcosms were inoculated with S. typhimurium LT2 at 107 cfu g−1 dry soil and survival monitored at three matric potentials. Viable counts on XLD indicated a rapid decline in cell density over 54 days, whereas direct counts of active cells using the respiration-sensitive dye 5-cyano-2,3-ditolyl tetrazolium chloride (CTC) remained relatively constant. XLD did not underestimate culturable cells in comparison to non-selective agar. QPCR revealed that the number of salmonella targets (H-li) remained constant up to day 13. After that time, a decrease occurred, corresponding to that of the plate counts, due to an increase in resistance of the cells to lysis, as incorporation of a lysozyme step into the DNA extraction method allowed more efficient DNA extraction. This resulted in a constant QPCR signal over 54 days which correlated with direct, active cell counts. QPCR showed H-li was present at levels only slightly lower than those at day 0. There was no difference in survival between the three different moisture regimes. Direct CTC counts of S. typhimurium LT2 in the soil microcosms confirmed that intact cells were present in a metabolising state after 54 days in non-sterile soil, indicating a significant proportion of uncultured but active cells.
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The ability of Salmonella to form complex surface-associated communities, called biofilms, contributes to its resistance and persistence in both host and non-host environments and is especially important in food processing environments. In this review, the different types of abiotic (plastic, glass, cement, rubber, and stainless steel) and biotic surfaces (plant surfaces, epithelial cells, and gallstones) on which Salmonella biofilms have been described are discussed, as well as a number of commonly used laboratory setups to study Salmonella biofilm formation (rdar morphotype, pellicle formation, and biofilms on polystyrene pegs). Furthermore, the structural components important during Salmonella biofilm formation are described (curli and other fimbriae, BapA, flagella, cellulose, colanic acid, anionic O-antigen capsule and fatty acids), with special attention to the structural variations of biofilms grown on different surfaces and under different conditions. Indeed, biofilm formation is strongly influenced by different environmental signals, via a complex regulatory network. An extensive overview is given on the current understanding of this genetic network and the interactions between its different components (CsgD, RpoS, Crl, OmpR, IHF, H-NS, CpxR, MlrA, c-di-GMP, BarA/SirA, Csr, PhoPQ, RstA, Rcs, metabolic processes and quorum sensing). To further illustrate that biofilm formation is a mechanism of Salmonella to adapt to different environments, the resistance of Salmonella biofilms against different stress factors including desiccation stress, disinfectants (e.g. hypochlorite, glutaraldehyde, cationic tensides and triclosan) and antibiotics (e.g. ciprofloxacin) is described. Finally, a number of Salmonella biofilm inhibitors, identified through bottom-up- and top-down-approaches, are discussed, such as surfactin, glucose, halogenated furanones, 4(5)-aryl 2-aminoimidazoles, furocoumarins and salicylates. Also the potential of combination therapy (e.g. combinations of triclosan and quaternary ammonium salts or halogenated furanones and antibiotics/disinfectants) and nano- and micro-emulsions to inhibit Salmonella biofilm formation is discussed. Insight into the pathogen's complex biofilm process will eventually lead to further unraveling of its intricacies and more efficient strategies to combat Salmonella biofilms.
Article
Outbreaks of Salmonella enterica have increasingly been associated with tomatoes and traced back to production areas, but the spread of Salmonella from a point source onto plants has not been described. Splash dispersal by rain could be one means of dissemination. Green fluorescent protein-labeled, kanamycin-resistant Salmonella enterica sv. Typhimurium dispensed on the surface of plastic mulch, organic mulch, or soil at 10⁸ CFU/cm² was used as the point source in the center of a rain simulator. Tomato plants in soil with and without plastic or organic mulch were placed around the point source, and rain intensities of 60 and 110 mm/h were applied for 5, 10, 20, and 30 min. Dispersal of Salmonella followed a negative exponential model with a half distance of 3 cm at 110 mm/h. Dispersed Salmonella survived for 3 days on tomato leaflets, with a total decline of 5 log and an initial decimal reduction time of 10 h. Recovery of dispersed Salmonella from plants at the maximum observed distance ranged from 3 CFU/g of leaflet after a rain episode of 110 mm/h for 10 min on soil to 117 CFU/g of leaflet on plastic mulch. Dispersal of Salmonella on plants with and without mulch was significantly enhanced by increasing rain duration from 0 to 10 min, but dispersal was reduced when rainfall duration increased from 10 to 30 min. Salmonella may be dispersed by rain to contaminate tomato plants in the field, especially during rain events of 10 min and when plastic mulch is used.
Article
Several outbreaks caused by pathogenic bacteria are related to the consumption of raw produce contaminated by animal manure. The majority of these outbreaks have been linked to Salmonella spp. We examined the ability of Salmonella enterica serovar Weltevreden to persist and survive in manure and soil as well as disseminate to, and persist on, spinach roots and leaves. Significantly higher numbers of S. Weltevreden inoculated into manure and applied to soil before planting spinach were found in soil than in pot cultures, where the pathogen had been inoculated directly into soil 14 days postplanting. Moreover, the pathogen seemed to disperse from manure to spinach roots, as we observed a continuous increase in the number of contaminated replicate pot cultures throughout the evaluation period. We also found that, in some cases, S. Weltevreden present in the phyllosphere had the ability to persist for the entire evaluation period (21 days), with only slight reductions in cell numbers. The results from the present study show that S. Weltevreden is capable of persisting in soil, roots and shoots for prolonged periods, indicating the importance of strict monitoring of untreated animal manure before considering its application to agricultural land.
Article
Foodborne Salmonella spp. is a leading cause of foodborne illness in the United States each year. Traditionally, most cases of salmonellosis were thought to originate from meat and poultry products. However, an increasing number of salmonellosis outbreaks are occurring as a result of contaminated produce. Several produce items specifically have been identified in outbreaks, and the ability of Salmonella to attach or internalize into vegetables and fruits may be factors that make these produce items more likely to be sources of Salmonella. In addition, environmental factors including contaminated water sources used to irrigate and wash produce crops have been implicated in a large number of outbreaks. Salmonella is carried by both domesticated and wild animals and can contaminate freshwater by direct or indirect contact. In some cases, direct contact of produce or seeds with contaminated manure or animal wastes can lead to contaminated crops. This review examines outbreaks of Salmonella due to contaminated produce, the potential sources of Salmonella, and possible control measures to prevent contamination of produce.
Article
The gram-negative bacterial species Salmonella enterica and Escherichia coli are members of the family Enterobacteriaceae that spend a good part of their lives as residents of animal hosts. S. enterica is the etiologic agent of gastroenteritis and typhoid fever in humans (88), whereas E. coli is most com- monly known as a commensal of the lower intestine of mam- mals, although pathogenic variants also exist (77). The animal host is believed to be the primary habitat of these two enteric species (86), which are genetically endowed to do well in this environment. For example, Salmonella has genes that mediate invasion of and survival within host cells, including genes that promote resistance to different microbicidal host products (62, 88). Likewise, the E. coli genome encodes proteins that medi- ate resistance to acid pH as well as growth on lactose, which is critical for a commensal of mammals (11, 57). In this review, we discuss whether Salmonella and E. coli live in stable, dividing populations in nonhost environments and whether such environments constitute dead ends for these species (e.g., as a consequence of residing in the vertebrate lower intestine, whose contents are regularly excreted (86, 102)). In addition, we examine the role that genes specific to Salmonella and E. coli play in the different abilities of these species to proliferate outside animal hosts.
Article
The interaction of a range of Salmonella serovars with pre- and postharvest tomatoes was evaluated. Serovars were selected on the basis of previous association in tomato-linked outbreaks of salmonellosis (Salmonella Javiana, Salmonella Montevideo, and Salmonella Newport) or those typically isolated from animal or clinical infections (Salmonella Dublin, Salmonella Enteritidis, Salmonella Hadar, Salmonella Infantis, Salmonella Typhimurium, and Salmonella Senftenberg). Salmonella serovars introduced onto the flowers of growing plants were recovered on and within the developing tomato fruit. Of all the Salmonella serovars tested, Montevideo appeared to be more adapted to survival within tomatoes and was recovered from 90% of the fruit screened. All of the Salmonella serovars could persist and grow when introduced onto unripened (green) tomato fruit. In general, growth (internal and external) was promoted at the high incubation temperature (25 degrees C) and high relative humidity (95%), although this was serovar dependent. The growth and persistence of Salmonella introduced on and into ripened (red) tomatoes was serovar dependent. Salmonella serovars Enteritidis, Typhimurium, and Dublin were less adapted to grow in or on intact red tomatoes than were serovars Hadar, Montevideo, or Newport. The results illustrated that a diverse range of Salmonella serovars can become established within and/or on preharvest tomatoes. The majority of Salmonella can grow and become established both on and within unripened tomatoes, but growth on ripened fruit was serovar dependent. The results provide a possible explanation why only a narrow range of Salmonella serovars are associated with foodborne illness outbreaks linked to tomatoes.
Airborne soil particulates as vehicles for Salmonella contamination of tomatoes
  • G D Kumar
  • R C Williams
  • Al Qublan
  • H M Sriranganathan
  • N Boyer
  • R R Eifert
Kumar GD, Williams RC, Al Qublan HM, Sriranganathan N, Boyer RR, Eifert JD. Airborne soil particulates as vehicles for Salmonella contamination of tomatoes. Int J Food Microbiol 2017;243:90-95.