Transmission of Multidrug-Resistant Salmonella enterica Subspecies enterica 4,,12:i:- Sequence Type 34 between Europe and the United States. Comment submitted successfully, thank you for your feedback. Phytophagous insects are largely recognized as vectors of enteric phytobacterial pathogens that cause important diseases on many crops (18, 19). Proportion of S. enterica-positive samples resulting from transmission from inoculated leaf discs to noninoculated leaf discs (horizontal-stripe bars) or from inoculated liquid diets confined in Parafilm sachets to noninoculated leaf discs (black bars) or to noninoculated liquid diets confined in Parafilm sachets (gray bars) at different inoculation access periods (IAP). The exponential growth rate of the population was estimated at 0.316/year (averaged across all subset means; Figure 1). Salmonella enterica is one of the most commonly reported zoonotic pathogens worldwide. Statistical analysis.Consistently, S. enterica was not recovered from noninoculated control leaves, liquid diets, insects, or honeydew in any of the experiments; therefore, these data are not shown. Leaf discs and liquid diets were placed and confined, respectively, inside the cap of sterile microcentrifuge tubes and were used to feed individual Macrosteles quadrilineatus and Myzus persicae. At the end of each 12-h period, the corresponding leaf discs were homogenized and subsequently enriched and plated on LB-kan and XLD-kan, respectively, and the percentage of S. enterica-contaminated leaf discs was determined. The surface of fruits and vegetables may be contaminated by human or animal feces. Please use the form below to submit correspondence to the authors or contact them at the following address: Ehud Elnekave, Koret School of Veterinary Medicine, Robert H. Smith Faculty of Agricultural, Food and Environmental Sciences, The Hebrew University, PO Box 12, Rehovot 76100, Israel. Salmonella sp. However, the increase since 2011 can be the result of rapid propagation of the ST34 population, possibly associated with swine (4). 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). 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. In fact, only the proportions of honeydew samples at the 24-h AAP time point were significantly higher than the corresponding noninoculated leaf disc at the 24-h IAP time point and the external wash sample and homogenized S. enterica-positive samples at the 48-h IAP time point. In summary, it appears that diet interacts with the inoculation interval following acquisition to influence localization and excretion. Insects were scored as S. enterica positive after external wash (A) or homogenization of the whole sample (B). Typhi (S. Typhi) and Salmonella enterica sv. Thus, the risk of a food-borne illness outbreak due to consumption of contaminated crop plants can be influenced by biotic factors, including phytophagous insects. 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. S. enterica populations tend to decline steadily over time on leaves of agricultural crops (2, 8, 9). Plant inoculation.Lettuce (Lactuca sativa cv. This question is for testing whether or not you are a human visitor and to prevent automated spam submissions. In addition, the United States-Israel Binational Agricultural Research and Development Fund awarded a Vaadia-BARD postdoctoral fellowship (no. At each sampling point, insects were sampled and both the external wash and the homogenate were tested as described above. Transmission is an essential stage of a pathogen's life cycle and remains poorly understood. Red circles represent XLD agar plates, and small black circles within represent colonies of S. enterica. A homogenate sample was scored as positive for internal contamination only if the corresponding external wash was negative, and those samples were considered containing surviving S. enterica within the insect. Such insects that encounter S. enterica on the leaf surface for brief periods of time could further distribute the pathogen along the same or adjacent leaves, simply by adhesion to the exoskeleton. Although the mechanisms of internalization, survival, and/or transmission of these enteric phytobacterial pathogens by their insect vectors have been widely studied, the actual multiplication of these bacteria inside their insect vector remains unconfirmed. However, the transmission rates were reduced at both the 24- and 48-h IAP time points, independent of the source of inoculum (Fig. Using a hemipteran insect pest-lettuce system, we investigated the potential for transmission and retention of S. enterica. The level of specificity and complexity of these symbiotic relationships vary depending on the bacteria-insect combination and the frequency of cooccurrence of both organisms within the same plant or ecological niche (19). Most human cases are foodborne; however, nonfoodborne Salmonella infection may be transmitted during contact with animals, contaminated water, or the environment (3 – 9). In the current study, the fact that S. enterica was excreted in honeydew by both M. quadrilineatus and M. persicae insects demonstrates that ingested bacteria survived the passage through the alimentary canal and could subsequently be dispersed on plants by the carrier insect. Elnekave, E., Hong, S. L., Lim, S., Boxrud, D., Rovira, A., Mather, A. E....Alvarez, J. BEAST: Bayesian evolutionary analysis by sampling trees. CDC is not responsible for Section 508 compliance (accessibility) on other federal or private website. CDC twenty four seven. Vertical transmission occurs in birds, with contamination of the vitelline membrane, albumen and possibly the yolk of eggs. This result demonstrated that acquired S. enterica is excreted and transmitted, but honeydew is unlikely the sole source of contamination to plants. The occurrence of several additional smaller introductions was suggested by 48 sequences (6 from Europe and 42 from the United States). However, at high population densities, insects can also come into contact with honeydew or droplets released on the plant surface (37). Salmonella Typhi lacks acid tolerance, so a high infectious dose of 103 to 106 bacilli is needed for infection. In contrast, when M. quadrilineatus insects were fed noninoculated liquid diets following acquisition, the proportions of positive honeydew samples at the 24-h AAP and the 24- or 48-h IAP time points were significantly higher than the proportions of samples positive for external wash (0.36, 0.40, and 0.29 compared to 0.06, 0.02, and 0.08, respectively). Salmonella bacteria typically live in animal and human intestines and are shed through feces. Contrastingly, at the same time point, a significantly higher proportion of S. enterica-positive honeydew samples was detected when M. quadrilineatus insects were fed a noninoculated liquid diet confined in Parafilm sachets (Fig. 1 and 7 and Nicholas Keuler of the College of Agriculture and Life Sciences' Statistical Consulting Laboratory, UW-Madison, for his assistance with statistical analysis. To determine if S. enterica transmissions, excretions, and localizations are similar among phytophagous hemipterans, we conducted the same matched-pair analysis for M. persicae insects fed inoculated liquid diets for 24 h and subsequently transferred to 2 consecutive noninoculated leaf discs (see Table S1 in the supplemental material). In addition, the estimated (averaged) main introduction into the United States was 2004 (95% HPD 2000–2006; Appendix 2 Table 1). The presence of mcr resistance genes conferring resistance to colistin in sequences from Europe (n = 5) is alarming, given their recent worldwide spread (14). Introduction. Proportion of S. enterica-positive samples resulting from insects that were fed inoculated leaf discs for a 24-h acquisition access period. In the United States, approximately 80 cases of paratyphoid fever caused by S. Paratyphi A are reported each year, 90% of which are acquired during international travel. Salmonella enterica is excreted by phytophagous hemipterans.Multiple assays were conducted in which the honeydew of M. quadrilineatus and M. persicae insects was collected at different time points following exposure to S. enterica-inoculated liquid diets. Insects were scored as contaminated after external wash (A) or homogenization of the whole sample (B). Multidrug-resistant Salmonella enterica subspecies enterica 4,,12:i:- sequence type 34 represents a worldwide public health risk. Mode of transmission of Salmonella. In our experiments, 200 μl of the liquid diet was initially pipetted into the inside of the cap of each sterile microcentrifuge tube and then tightly covered with 2 layers of stretched Parafilm to limit physical contact of the insect body with the diet but allowing oral ingestion. The six strains were mixed in a cocktail inoculum that was prepared as previously described (13). Here again, these results were interpreted as the proportion of individual insects capable of bacterial transmission from inoculated to noninoculated liquid diet. 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. A nonspecific association between the fireblight pathogen Erwinia amylovora and pollinating insects is now widely recognized, in which flower-visiting insects spread bacteria attached to their external surfaces to new infection sites (19). 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. Yet associations between the collection location and the presence of blaCTX-M or qnrS1 genes were not significant (Table). The difference between the date of main introduction into the United States found in this study and the later sharp increase in its prevalence in animals and humans may in part result from changes in reporting practices and increasing awareness (8). Localization of Salmonella enterica in or within phytophagous hemipterans. The presence of AARGs conferring resistance to quinolones and extended-spectrum cephalosporins has mainly been observed since 2014 and may be biased by the lack of sequences before 2013 (Appendix 2 Figure 12). Bacterial strains, media, and culture conditions.Six S. enterica serovars, Cubana strain 98A9878 (24), Enteritidis strain 99A-23 (California Health Department [CHD], July 2005 tomato outbreak), Newport strain 96E01152C-TX (25), Poona strain 00A3563 (CHD, cantaloupe outbreak), Schwarzengrund strain 96E01152C (25), Baildon strain 05x-02123 (26), and Mbandaka strain 99A1670 (CHD, alfalfa seed isolate), were used in this study. Insects can become contaminated upon contact with S. enterica surface-contaminated plants (purple dots). In addition, the incidence of Salmonella 4,,12:i:- in humans increased only modestly (9.5%) during 2006–2011 but increased dramatically (78.3%) during 2011–2016 (8). 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. Our results demonstrated that two commonly occurring hemipteran insect pests, M. quadrilineatus and M. persicae, acquired S. enterica upon feeding on an inoculated diet. 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. NOTE: We request your email address only to inform the recipient that it was you who recommended this article, and that it is not junk mail. Salmonella enterica. is subdivided into 6 subspecies (enterica (I), salamae (II), arizonae (IIIa), diarizonae (IIIb), houtenae (IV) and indica (VI) ). His primary research interest is the epidemiology of bacterial foodborne pathogens. Thus, the main objective of this study was to investigate the potential acquisition, retention, and transmission of S. enterica by these phytophagous hemipteran insects. A recent outbreak investigation of sources of S. Wangata recovered isolates from humans, domestic animals, wildlife and the environment. Outbreaks of disease associated with food imported into the United States, 1996–2014. 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. Our study unifies these observations and demonstrates that phytophagous hemipterans can be sources of S. enterica, and these insects are regarded as key pest species of crops implicated in food-borne illness outbreaks, such as lettuce and tomatoes (1, 3, 26). Salmonella enterica subspecies enterica can be separated into more than 2400 antigenically different serovars and the pathogenicity of most of these serovars is unspecified. In addition, AARGs conferring resistance to colistin (mcr-1/mcr-3/mcr-5; Appendix 1) were detected in isolates from Europe only (n = 5). It is known that the high protein content in honeydew attracts many other insects, such as flies, ants, and other predators, which require a substantial amount of protein to develop mature eggs (29, 44). Many different animals and pets can carry these germs. can attach, survive, and even replicate in or on confinement insects (42). All statistical analyses were performed using R software (34). Salmonella Enteritidis frequently contain plasmids that range from 55-60 kbp . Approximately 12–72 hours, but it can be excreted in droplets of honeydew that are released onto.. 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