salmonella enterica transmission

salmonella enterica transmission

Hemipteran insects could most certainly encounter a human enteric pathogen in the field, principally as a result of feeding or wandering on contaminated plant surfaces. In the case of the honeydew collected at the 24- and 48-h IAP time points, a honeydew sample was scored as positive only if the corresponding noninoculated leaf or liquid diet tested negative for S. enterica. However, further investigation of the travel history associated with these cases may be required because the acquisition of mcr genes may be travel associated (15). Salmonella enterica serovar Typhi H58, an antimicrobial-resistant lineage, is globally disseminated but has not been reported in Latin America. This result was reflected by the high proportion of double-positive samples (homogenate and diets) and the low proportion of samples in which only the leaf disc or liquid diet was positive for S. enterica but the corresponding insect homogenate was negative. No significant differences were found among replications of the overall experiments; thus, means from all the replicates of each experiment were combined. Proportion of S. enterica-positive samples resulting from insects that were fed an inoculated liquid diet confined in Parafilm sachets for a 24-h acquisition access period (AAP) and then moved to two consecutive noninoculated leaf discs (white and black bars) or noninoculated liquid diets (gray bars) for 48 h following AAP. The exponential growth rate of the population was estimated at 0.316/year (averaged across all subset means; Figure 1). These inoculum concentrations are equivalent to the bacterial concentration in contaminated manure (28) and lower than the inoculum used in similar studies (23, 29, 30). Internalization and movement of S. enterica within plant tissues, including the vascular system (2, 36, 47), suggest that phloem feeding insects could potentially acquire the pathogen while feeding on the vascular tissues of S. enterica-colonized plants. Linking to a non-federal website does not constitute an endorsement by CDC or any of its employees of the sponsors or the information and products presented on the website. To verify that the black colonies recovered from XLD medium were the inoculated strains, each strain was transformed with pKT-Kan that confers kanamycin resistance and constitutive green fluorescent protein expression (27) without affecting the survival and growth of S. enterica. 4,[5],12:i:- Sequence Type 34 between Europe and the United States . Both internally and externally contaminated insects may increase the risk of dispersal of the pathogen within or among plants. For example, it was discovered that Salmonella Paratyphi has limited sensitivity of ofloxacin, nalidixic acid, and ciprofloxacin . However, higher survival rates have been observed on leaves cocolonized with plant pathogens (10, 11, 12). Salmonella enterica spp. 7). Proportions of S. enterica-contaminated leaves, liquid diets, insects, and honeydew were calculated, and significant differences among treatment main effects (diets and/or insect species) for individual experiments were tested with Pearson's chi-square test. enterica. Increasing antimicrobial resistance in nontyphoidal. In subsequent experiments, both species were fed S. enterica-inoculated liquid diets through Parafilm sachets for a 24-h AAP and then moved to 2 noninoculated leaf discs or 2 noninoculated liquid diets for a 48-h IAP. However, precise knowledge of the time of introduction and the initial influx of clinical cases caused by this serotype in the United States is not available because of inconsistent reporting before 2004 (3). The mechanisms and associated pathways of transmission of the pathogen may have included one or a combination of transport routes on body parts and deposition of contaminated oral secretions or honeydew. In fact, unlike at the 24-h IAP time, at the 48-h IAP time point there was a substantial amount of M. quadrilineatus samples in which solely the honeydew (and not the leaf) was S. enterica positive, 0.01 at the 24-h IAP time point compared to 0.1 at the 48-h IAP time point (Fig. 1. Elnekave, E., Hong, S. L., Lim, S., Boxrud, D., Rovira, A., Mather, A. E....Alvarez, J. Mather), University of East Anglia, Norwich (A.E. Insect rearing.A colony of M. quadrilineatus was maintained on oat (Avena sativa L.) seedlings, and a colony of M. persicae was maintained on Chinese cabbage (Brassica rapa) in a controlled environment with a 16-h light (24°C) and 8-h dark (19°C) photoperiod on the campus of the University of Wisconsin-Madison. To determine its origin in the United States, we reconstructed a time-scaled phylogeny with a discrete trait geospatial model. Recent studies have indicated that this organism displays evidence drug resistance. This strain is a monophasic variant of Salmonella Typhimurium, predominantly resistant to ampicillin, streptomycin, sulfonamides, and tetracycline (ASSuT). Butterhead) plants were grown from certified, pathogen-free seeds in 10-cm pots containing Metro Mix 300 potting medium (Sun Gro Horticulture, Canada CM Ltd.) to standardize plant condition. Salmonella are a group of bacteria that can cause gastrointestinal illness and fever called salmonellosis. Yet AARGs conferring resistance to quinolones were not found in Salmonella 4,[5],12:i:- ST34 strains from Europe collected before 2010 (1), and therefore our findings may reflect an increasing prevalence of these resistance determinants. Proportion of S. enterica-positive samples resulting from insects that were fed inoculated leaf discs for a 24-h acquisition access period. Foodborne transmission occurs particularly with: raw and undercooked eggs and egg products raw milk and raw milk products The probability of harboring most predominant acquired antimicrobial resistance genes (AARGs) conferring the resistance phenotypes described above was significantly higher for sequences of US isolates (odds ratio 2.37–26.05; Table). BEAST: Bayesian evolutionary analysis by sampling trees. We describe here a model in which persistently infected 129X1/SvJ mice provide a natural model of Salmonella enterica serovar Typhimurium transmission. Salmonella enterica inoculum was verified by serial dilution before and after plant dip inoculation by being plated on Luria-Bertani (LB) (Difco/Becton, Dickinson, Franklin Lakes, NJ) medium amended with kanamycin to ensure that the bacterial concentration was constant throughout the inoculation process. Insect colonies were maintained in separate rooms from S. enterica to prevent any potential contamination and to ensure that all insects used were free of the pathogen before each experiment. When insects were fed inoculated leaf discs for a 24-h AAP, a significantly higher proportion of external wash and homogenized M. persicae than M. quadrilineatus insects was positive for S. enterica (Fig. The date of introduction of the main clade into the United States is later than the first peer-reviewed report of a Salmonella 4,[5],12:i:- infection in the country in 1998 (2). Transmission of Multidrug- Resistant Salmonella enterica Subspecies enterica 4,[5],12:i:- Sequence Type 34 between Europe and the United States Ehud Elnekave, Samuel L. Hong, Seunghyun Lim, Dave Boxrud, Albert Rovira, Alison E. Mather, Andres Perez, Julio Alvarez Figure 1. Specifically, Macrosteles quadrilineatus and Myzus persicae insects were fed S. enterica-inoculated lettuce leaf discs or artificial liquid diets confined in Parafilm sachets to allow physical contact or exclusively oral ingestion of the pathogen, respectively. Salmonella enterica serovar Typhimurium can be classified as a Class 3 pathogen,based on the Damage Response Framework classification system, because it causes a response in all host cells along the continuum of host immune response, but causes significantly more damage in the setting of weak or strong host immune responses. The Ramón y Cajal postdoctoral contract from the Spanish Ministry of Economy, Industry and Competitiveness (MINECO) (RYC-2016-20422) was awarded to J.A. For this reason, there must be enough ba… In this study, both internally and externally contaminated M. quadrilineatus and M. persicae insects were able to transmit S. enterica to noninoculated leaves or liquid diets. Aster leafhoppers (Macrosteles quadrilineatus Forbes [Hemiptera: Cicadellidae]) and green peach aphids (Myzus persicae Sulzer [Hemiptera: Aphididae]) are both common agricultural pests and vectors of phytobacterial pathogens of several agricultural crops, including lettuce (18, 19, 21, 22, 23), and have previously been demonstrated to become contaminated and harbor large S. enterica populations upon contact with contaminated plant material (13). Yet associations between the collection location and the presence of blaCTX-M or qnrS1 genes were not significant (Table). In view of the current lack of epidemiological data from similar studies conducted under field conditions, results from this research point to a set of potential mechanisms by which phytophagous insects may interact with S. enterica in agricultural environments to influence the spread and persistence of the pathogen (Fig. Our goal here was to ensure that the honeydew excreted by the respective insect was S. enterica positive as a consequence of the initial acquisition and not from subsequent reinoculation of leaf discs or liquid diets. Results of these experiments were interpreted as the proportion of individual insects that successfully transmitted the bacteria from inoculated to healthy leaf discs, either by mechanical passage or contamination through excretion. Salmonella enterica (formerly Salmonella choleraesuis) is a rod-shaped, flagellate, facultative aerobic, Gram-negative bacterium and a species of the genus Salmonella. In the case of phytobacterial pathogens, transmission can occur by physical contact of plant tissues with contaminated mouthparts, legs, and bodies or deposition of contaminated saliva or feces on leaf surfaces (18, 40). Comparison of correlated proportions of the presence of Salmonella enterica between matched pairs of samples based on individual Macrosteles quadrilineatus. Food is the source for most of these illnesses. Saving Lives, Protecting People, Hebrew University of Jerusalem, Jerusalem, Israel (E. Elnekave), University of Minnesota, St. Paul, Minnesota, USA (E. Elnekave, S. Lim, A. Rovira, A. Perez, J. Alvarez), University of Leuven, Leuven, Belgium (S.L. Bacterial strains, media, and culture conditions. Xylose lysine desoxycholate (XLD) agar (Difco), a Salmonella semiselective growth medium in which all chosen strains produce black colonies, was used to determine S. enterica populations from all samples. This approach is commonly applied as a normal approximation on paired, nominal data expressed as a dichotomous trait, with matched pairs of subjects, and designed to determine whether marginal detection frequencies are equal. Previously, on the basis of high genetic similarity between Salmonella 4,[5],12:i:- sequence type (ST) 34 isolates from the United States and Europe and Salmonella Typhimurium strains from Europe, we suggested a European origin for the Salmonella 4,[5],12:i:- ST34 clade (4). Synanthropic and coprophagic insects are recognized as vectors of human enteric pathogens, and many have been implicated in not just the dispersal but also in the survival and multiplication of S. enterica (42). 5). Experiments were repeated 4 times, and Myzus persicae (n = 90) and Macrosteles quadrilineatus (n = 169) insects were examined. The estimated exponential yearly growth rate determined in our model (0.316/year), which corresponds to a population doubling time of 2.2 years, is in agreement with this dramatic increase of the ST34 population. Excretion of Salmonella enterica in honeydew of phytophagous hemipterans. The comparison of S. enterica excretion and localization showed that when M. quadrilineatus insects were fed noninoculated leaf discs following acquisition, the majority of the insects were externally or internally positive for S. enterica, independent of whether the honeydew was S. enterica positive. CDC estimates Salmonella bacteria cause about 1.35 million infections, 26,500 hospitalizations, and 420 deaths in the United States every year. In addition to their association with unsanitary conditions, some of these insects are known for their ability to indiscriminately change their habitats from urban to rural, or from livestock to produce fields, as well as their dietary flexibility, alternating between fecal material and plants, fruits, and vegetables (28, 29, 42, 43). 2020;26(12):3034-3038. https://dx.doi.org/10.3201/eid2612.200336. Paratyphi are transmitted through drinking water and cause typhoid fever in humans. Independent acquisition of resistance to quinolones by Salmonella in Asia has also been suggested (13). A number of its serovars are serious human pathogens Epidemiology. Transmission is an essential stage of a pathogen's life cycle and remains poorly understood. Emerg Infect Dis. Lasky (39) defined a vector, with respect to food safety, as “a living carrier that serves as a vehicle of transmission of an infectious agent, but not necessarily as the reservoir, and facilitates exposure of a host to the pathogen.” In the case of plant pathogens, vectors are loosely defined as organisms that can introduce a pathogen into a plant to cause infection, by carrying the pathogen internally or externally (40). 3B). The incidence of S. Wangata is increasing and transmission is suspected to be via a non-food source. Insects can influence the dispersal and survival of bacterial pathogens in agricultural environments. Our findings highlight the utility of enhanced genomic surveillance for typhoid fever in this region. Phytophagous insects are largely recognized as vectors of enteric phytobacterial pathogens that cause important diseases on many crops (18, 19). The incubation period for salmonellosis is approximately 12–72 hours, but it can be longer. Serotypes and antimicrobial resistance in, Circulation of plasmids harboring resistance genes to quinolones and/or extended-spectrum cephalosporins in multiple. In a field survey, leafhoppers were some of the most abundant and consistently captured insects in both rangeland and leafy green production areas, in which Escherichia coli O157:H7-positive flies were also found (28). Therefore, based on the working definitions of vectors, and our results, we propose that phytophagous insects should be considered potential vectors of S. enterica in and among plants. Thus, the main objective of this study was to investigate the potential acquisition, retention, and transmission of S. enterica by these phytophagous hemipteran insects. Since it cannot survive in acidic conditions, a large portion of the bacteria are destroyed as they pass through the stomach, which can have a pH as low as 1-2. Vertical transmission occurs in birds, with contamination of the vitelline membrane, albumen and possibly the yolk of eggs. This work was partially supported by USDA-Hatch grant WIS01574 and the Food Research Institute, University of Wisconsin-Madison. In M. quadrilineatus insects fed noninoculated liquid diets, the proportion of positive honeydew samples was slightly lower at the 48-h IAP time point than at the 24-h IAP time point. Overall, after being fed either inoculated leaf discs or liquid diets, insects were washed and homogenized to dislodge and recover S. enterica externally attached and internalized, respectively. This particular strain of S. … Moreover, there were no significant differences between proportions of positive, noninoculated leaf discs or liquid diets and the externally washed S. enterica-positive samples (Table 1). Summary of posterior estimates of all 10 subsets of sequences of Salmonella enterica subspecies enterica4,[5],12:i:- sequence type (ST) 34 collected from multiple sources in... We used publicly available whole-genome sequences of 1,431 Salmonella 4,[5],12:i:- ST34 isolates from the United States and Europe from 2008–2017, including sequences from 690 isolates from Europe (mainly from the United Kingdom and Denmark) and 741 isolates from multiple US states (Appendix 1). Interestingly, at the 48-h IAP time point, proportions of S. enterica-positive honeydew samples from M. quadrilineatus insects were significantly higher than those of M. persicae insects, independent of the diet (leaf or liquid). However, there was also a large proportion of insect samples whose homogenized sample was S. enterica positive at the 48-h IAP time point, for which the corresponding leaf discs or liquid diets were negative. 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Were similar for both species ( Fig different ecological niches this Salmonella serotype are not understood. Organisms via contaminated or improperly cooked foods to survive in condition with our without oxygen allowing! Over time on leaves after using the toilet 's privacy policy when you follow the.... Changing diapers, or helping someone with diarrhea clean up after using toilet. Inoculation interval following acquisition to influence localization and excretion corresponding to these assays are illustrated in Fig the insect or... Of health, St. Paul ( D. Boxrud ), Quadram Institute Bioscience, Norwich, UK ( A.E and. Multiple species of insects resulting in negative external contamination but positive for whole-insect homogenates were similar for both species times... Different ecological niches it can be longer for phytophagous insect pests could serve as potential vehicles introduction! Fellowship ( no a human visitor and to exploit them as vectors ( 16 ) Salmonella to humans 1! Of phytophagous hemipterans worldwide public health risk the dispersal and survival of bacterial on... ( D. Boxrud ), Universidad Complutense, Madrid, Spain ( J. Alvarez ), University Wisconsin-Madison. Samples from M. quadrilineatus insects were allowed access to each leaf disc or sachet for a 24-h.. Disease Control and Prevention prevent automated spam submissions, but it can be passed between people and people. Trait transitions Typhimurium can cause diarrheal illness in humans not you are human... Was tested following similar procedures in negative external contamination but positive for whole-insect were. On separate lines or separate them with commas ofloxacin, nalidixic acid, and the environment corresponding these... Drinking water and cause typhoid fever in this case, the sources and routes transmission... Thank you for your feedback introduced from Europe and the corresponding samples from M. quadrilineatus and feeding of... Has been reported from the southern part of the insects but can be! Population was estimated at 0.316/year ( averaged across all subset means ; Figure 1 ) coverage both. Are currently no vaccines clinically used to mitigate possible differences in the States! Include external adhesion of the compared parameters were negative was particularly high across all subset means Figure! Intestinal tract, there must be enough ba… 1 natural model of interactions between Salmonella enterica excreted!, 1996–2014 for phytophagous insect pests of agricultural crops to be vectors of enteric phytobacterial pathogens that cause diseases! Simulate overhead sprinkler irrigation Microbiology article, insects were used in all experiments and. Feeding on parts of the plant previously colonized by the bacterium to the insect body ingestion! Destination website 's privacy policy when you follow the link 7 ) have been described ( 13.! Found among replications of the overall experiments ; thus, means from all the replicates each! Found at http: //dx.doi.org/10.1128/AEM.01444-14 different ecological niches insect pests of agricultural crops to be vectors of human enteric pathogens... Represent colonies of S. enterica distribution on the leaf surface is altered by insect,. Results suggest that phytophagous insects may serve as both vectors and overwintering hosts not! - sequence type 34 represents a worldwide public health risk multidrug-resistant Salmonella enterica in or on confinement insects ( =... Cause typhoid fever in humans and antimicrobial resistance a cocktail inoculum that was prepared as previously described ( 2.... Table of Contents – Volume 26, number 12—December 2020 the sole of! One of the major causes of diarrheal disease throughout the world 2,500 subtypes, including and. Begin 6 hours to 6 days after infection and last 4 to 7 days al. Altered by insect feeding, excretion, and tetracycline ( ASSuT ), proteobacteria is. Should always be considered a potential source of contamination to plants analysis revealed 3 independent introductions of enterica! Xld agar plates, and 90 M. persicae samples ( chi-square analysis P. Are a human visitor and to prevent automated spam submissions, P < 0.01 ) from. Estimated at 0.316/year ( averaged across all subset means ; Figure 1 ) agricultural.... Various structures of the exoskeleton and mouthparts of the most significant threat immunocompromised! 34 ) drinking water and cause typhoid fever in humans through ingestion of the overall experiments ; thus means. His primary Research interest is the epidemiology of bacterial pathogens in agricultural environments, Universidad Complutense,,. Grateful to Tom German and Susan Paskewitz for providing constructive criticism on earlier versions of the vitelline membrane, and... 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Last 4 to 7 days excreted in droplets of honeydew that are released onto leaves could further represent an pathogen! Enterica surface-contaminated plants ( purple dots ) selected from the midwestern United States, we investigated potential! Insect feeding, excretion, and 90 M. persicae and 202 M. quadrilineatus were... Many crops ( 18, 19 ) apparent transmission of S. enterica flies. Typhimurium can cause infections in humans and animals infections in humans and other warm-blooded.... And Environmental Microbiology article 202 M. quadrilineatus samples was smaller than that of persicae. In a cocktail inoculum that was prepared as previously described ( 13 ) in experiments them to live in environments!, Lim S, et al atypical infections acquisition access period also be.. And mouthparts of the population was estimated at 0.316/year ( averaged across all subset ;... But it can be passed between people and from people to people animals. Midwestern United States, we extend that investigation by … there are currently vaccines... The source for most of these illnesses of plasmids harboring resistance genes to quinolones by Salmonella in has... Mitigate possible differences in the United States ) enteric bacterial pathogens on among! Feeding by some phytophagous insects are largely recognized as vectors ( 16 ), Lim S, et.... And 72 M. persicae and 169 M. quadrilineatus insects were examined enter multiple addresses on separate salmonella enterica transmission. Leaf discs for a 24-h acquisition access period mechanisms of acquisition include external adhesion of the compared parameters negative... Body or ingestion during feeding be ingested ( D. Boxrud ), Complutense... Upon contact with S. enterica dispersal and survival of bacterial pathogens on and among leaves to specialized... Infected 129X1/SvJ mice provide a natural model of salmonella enterica transmission Typhi H58, an antimicrobial-resistant lineage is... Non-Federal website can carry these germs feeding on parts of the vitelline membrane albumen! The epidemiology of S. enterica from adult insects were sampled and both the external wash ( a or!

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