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AbstractPurposeThis study was performed to compare clinical features and emergency department (ED) outcomes between children and adults with non‑typhoidal Salmonella (NTS) gastroenteritis in a single‑center cohort.
MethodsWe retrospectively reviewed electronic medical records of ED patients with stool multiplex polymerase chain reaction-confirmed NTS at CHA Bundang Medical Center from January 2016 through December 2021. Demographics, presentation, laboratory and imaging findings, microbiology, and treatments were abstracted. Primary outcomes were the high acuity (a Korean Triage and Acuity Scale level 1-2), ED length of stay, and disposition.
ResultsOf 189 patients, 134 were children and 55 adults. The children had fewer comorbidities (5.2% vs. 56.4%; P < 0.001) and high acuity (children, 0% vs. adults, 14.5%), shorter median ED length of stay (237.0 minutes [interquartile range, 188.0-336.0] vs. 360.0 minutes [335.0-569.0]; difference, 123.0 minutes [95% confidence interval, 85.0-328.0]; P < 0.001), and less frequent hospitalizations to the intensive care unit (children, 0% vs. adults, 14.5%; P < 0.001). Fever (94.8% vs. 63.6%) and hematochezia (37.3% vs. 0%) were more common in the children (Ps < 0.001), while adults had higher frequencies of abdominal pain (87.3% vs. 71.6%; P = 0.020) and enteritis/ileus on radiography (63.3% vs. 45.3%; P = 0.033), and higher median values of segmented white blood cells (79.0% vs. 69.4%; P = 0.010) and C‑reactive protein concentration (7.2 vs. 6.3mg/dL; P < 0.001). Ceftriaxone was more commonly used in the children (children, 72.7% vs. adults, 51.9%; P < 0.001).
ConclusionCompared with the adults, the children with NTS gastroenteritis presented with lower clinical acuity, shorter ED stays, and no hospitalizations to the intensive care unit, despite more common fever and hematochezia. These findings may support a conservative ED approach in children with careful, indication‑based antibiotic use and highlight opportunities for antimicrobial stewardship.
IntroductionNon-typhoidal Salmonella (NTS), primarily caused by Salmonella enterica serovars Enteritidis and Typhimurium, is a leading pathogen of acute infectious gastroenteritis (GE) transmitted through ingestion of contaminated food and the fecal-oral route (1-4). Globally, the annual occurrence of NTS GE and associated mortality is approximately 93,800,000 cases, of which 80,300,000 cases were foodborne, with 155,000 deaths (5). Although most cases of NTS GE clinically resolve spontaneously, the risk of invasive complications increases in infants younger than 3 months and in adults aged ≥ 65 years, as well as in patients with comorbidities or immunocompromised status, for whom antibiotic therapy may be required (6-10). Age is a factor used for early risk stratification in the emergency department (ED). Nevertheless, few authors have directly compared children and adults with NTS GE within the same cohort from the perspective of ED treatment. This study was performed to characterize the clinical features of children with stool polymerase chain reaction (PCR) confirmed NTS GE presenting to a single university hospital ED, and to compare them with those of adults in the same ED. Through this, we sought to identify age-related differences in initial presentation and ED care.
Methods1. Study design and settingThis study was a single-center retrospective cohort study based on ED visit data from CHA Bundang Medical Center between January 1, 2016 and December 31, 2021. Eligibility criteria and case definitions (PCR-confirmed NTS) are detailed in the “selection of participants” section. Annually, the ED provides care for approximately 55,000 adults and 25,000 children. The study received approval from the institutional review board (IRB no. CHAMC 2022-11-032) and was conducted as a retrospective design, exempting the need for participant consent.
2. Selection of participantsWe included patients who presented with GE during the study period and tested positive for NTS (hereafter “NTS GE”) in stool multiplex real-time PCR for bacterial enteropathogens (Acute Diarrheal Bacteria Panel; EONE Laboratories). The PCR kit simultaneously detects major pathogens including Salmonella spp., Vibrio spp., Campylobacter spp., Aeromonas spp., Clostridioides difficile toxin B, Yersinia enterocolitica, and Shigella spp., or enteroinvasive Escherichia coli. Those who did not undergo PCR or tested negative/non-NTS were excluded. To prevent duplicate visits, only the index visit per patient was analyzed.
The included patients were categorized as children (< 18 years) or adults. For subgroup analysis, 4 age strata were defined: < 5, 5-17, 18-64, and ≥ 65 years. These categories reflect guideline- and literature-based risk groups: children younger than 5 years are recognized at high risk of invasive disease and indications for antibiotics (8-10), whereas adults aged 65 years or older are at high risk of bacteremia, other complications, or mortality (4,5,11,12).
3. Data collection and measurementsData were extracted from the electronic medical records. Variables of interest included age, age group, sex, comorbidity, visit during outbreak period, PCR co-detection, high acuity (a Korean Triage and Acuity Scale level 1-2 (13,14)), ED length of stay (EDLOS) (minutes; from the time of arrival or bed assignment to the time of discharge decision), ED disposition (discharge, hospitalization to ward or intensive care unit [ICU], death, transfer, or discharge against medical advice), symptoms (diarrhea, fever, abdominal pain, hematochezia, or vomiting), laboratory and imaging findings, culture positivity from the blood or stool, and number and type of prescribed antibiotics. Of these variables, outcomes were predefined as the high acuity, EDLOS, and disposition, which were considered to reflect ED triage results and resource utilization.
The comorbidity was defined as the presence of any of the following: diabetes mellitus, hypertension, ischemic heart disease, chronic kidney disease, malignancy, or immunosuppression. The outbreak period was derived to reflect the surge of NTS GE observed in August 2021 (Figure 1). The PCR co-detection was defined as the simultaneous detection of an additional non-Salmonella pathogen by the stool PCR. The laboratory findings included overall and segmented white blood cell count, C-reactive protein, blood urea nitrogen/creatinine, and natrium. The enteritis/ileus on radiography was defined as radiologists’ impression compatible with enteritis or ileus (e.g., abnormal bowel gas pattern or bowel wall thickening). The culture positivity from the blood was considered a case of NTS bacteremia. Microbiological variables included recovery of Salmonella spp. from stool culture, isolation of Salmonella spp. from blood culture (i.e., NTS bacteremia).
4. Statistical analysisAll analyses were performed using SAS ver. 9.4/SAS Studio (SAS Institute). Continuous variables were summarized as median (interquartile range) and compared using the Wilcoxon rank-sum test. Ninety‑five percent confidence intervals for the median EDLOS and the between‑group median difference were calculated using a nonparametric bootstrap method. Categorical variables were expressed as frequencies and percentages and compared using the Pearson chi-square test or Fisher exact test, as appropriate. A P < 0.05 was considered significant.
ResultsDuring the study period, 189 patients including 134 children visited the ED with PCR-confirmed NTS GE (Figure 2). Figure 1 shows the monthly counts of the patients, revealing an annual increase in August to September, with a spike observed in August 2021.
Baseline characteristics are summarized in Table 1. Among the children, 52.2% were younger than 5 years, while among the adults, 27.3% were aged 65 years or older. The children showed lower proportions of the comorbidities (5.2% vs. 56.4%), occurrence during the outbreak (17.9% vs. 41.8%), high-acuity (0% vs. 14.5%), and hospitalization to the ICU (0% vs. 14.5%), as well as a shorter median EDLOS (237.0 minutes [interquartile range, 188.0-336.0] vs. 360.0 minutes [335.0-569.0]; difference, 123.0 minutes [95% confidence interval, 85.0-328.0]; P < 0.001)), than the adults. All children were triaged as a Korean Triage and Acuity Scale 3-4.
The symptom profile and laboratory, imaging, and microbiological findings are summarized in Table 2. Fever and hematochezia were more common in the children (fever, 94.8% vs. 63.6%; hematochezia, 37.3% vs. 0%), whereas abdominal pain was more frequent in the adults (71.6% vs. 87.3%). The enteritis/ileus on radiography was more often observed in the adults (45.3% vs. 63.3%). The laboratory findings showed lower median values of segmented white blood cell count and neutrophil percentages and C-reactive protein concentration in the children than in the adults (segmented, 69.4 × 10³/μL [interquartile range, 58.0-76.0] vs. 79.0 × 10³/μL [69.0-87.0]; C-reactive protein, 6.3 mg/dL [3.2-9.7] vs. 7.2 mg/dL [4.0-12.9]). Microbiologically, NTS bacteremia was identified in 6 patients including 3 children: 1, < 5 years; 2, 5-17 years; and 3, 18-64 years. No invasive complications such as meningitis or osteomyelitis were identified.
Table 3 summarizes antibiotic prescriptions by age groups. Most patients received antibiotics (128 of the 134 children [95.5%] and 52 of the 55 adults [94.5%]). Ceftriaxone was more commonly used in the children (72.7% vs. 51.9%). In the children, azithromycin was prescribed to 1 patient.
DiscussionThis study has clinical implications as follows. First, the children’s low acuity or favorable outcome, such as a shorter EDLOS, suggests that their management should be focused on oral rehydration, electrolyte correction, and observation rather than on routine hospitalization. Second, due to the low rate of bacteremia, empirical antibiotic therapy or blood cultures may be reserved for children with suspected bacteremia or at high risk of it.
These study findings are broadly consistent with relevant pediatric NTS studies that describe fever and hematochezia as common features and emphasize the generally low risk of invasive complications in children (9,10,15). In our cohort, the ward hospitalization was more frequent in children despite their lower acuity, consistent with pediatric NTS series where short-term hospitalizations were often driven by rehydration or observation rather than the true acuity (9,10). By contrast, adults with NTS GE exhibited a higher acuity, in terms of the inflammatory markers, abnormal radiography, prolonged EDLOS, and ICU hospitalization. These findings are consistent with adult NTS studies, suggesting that comorbidities and immunosuppression are more common in adults than in children, and that these conditions are associated with bacteremia and poor prognosis (11,12,16).
The patterns of antibiotic use also deserve attention. The predominance of ceftriaxone monotherapy in the children aligns with recommendations favoring a single-agent therapy when antibiotics are indicated (9,10). However, it is recently recommended against antibiotic therapy for noninvasive NTS GE in immunocompetent children, reserving the therapy for patients suspicious of or at a high risk of bacteremia (e.g., age < 3 months, immunocompromised, severe colitis, suspected bacteremia, or extra-intestinal foci) (8-10).
It is notable that the rate of antibiotic use was 95.5% in our pediatric cohort despite the absence of ICU hospitalization and the rarity of bacteremia. This finding suggests that the antibiotic therapy, rather than the choice of agent, was not adherent to the current recommendations (8-10). This discrepancy underscores the need for antimicrobial stewardship in EDs (8).
This study has several limitations. First, the single-center retrospective study design limits external validity and leaves potential residual confounding. Second, the test-based selection of patients with GE who underwent stool PCR may have introduced selection bias, as PCR positivity can reflect carriage or inactive infection. Third, regional outbreaks in 2021 accounted for a large proportion of cases and may have overrepresented specific serotypes/exposure factors. Fourth, information on the return visits was collected only within our hospital and may have been underestimated compared to the actual figures. Finally, because multivariate adjustment was not performed, confounding factors related to comorbidities, timing of presentation, or testing practices may persist (17,18).
In summary, the children with NTS GE who visited the ED had lower acuity, shorter EDLOS, no ICU hospitalization, and were more often characterized by fever, hematochezia, and ceftriaxone monotherapy, compared with the adults with the same disease. These findings highlight the generally favorable outcome of NTS GE in children, and support conservative management with judicious antibiotic use. Further research is needed to confirm these patterns and to inform evidence-based management strategies.
NotesAuthor contributions Conceptualization, Methodology, Project administration, Resources, Supervision, and Validation: MJ Kim and SH Paek Data curation: DS Hwang Formal analysis: DS Hwang and HS Moon Investigation: DS Hwang, HS Moon and MJ Kim Visualization: DS Hwang and MJ Kim Writing-original draft: DS Hwang and HS Moon Writing-review and editing: MJ Kim and SH Paek All authors read and approved the final manuscript. Fig. 1.Monthly counts of polymerase chain reaction‑confirmed non‑typhoidal Salmonella gastroenteritis by the age groups (2016-2021). Lines show monthly case counts in children and adults, with the overall total shown for reference. The arrow indicates the overall peak (45 cases, August 2021). Fig. 2.Selection of study population. Children (n = 134) and adults (n = 55) were analyzed as separate groups; reasons for exclusion are shown in the boxes. ED: emergency department, PCR: polymerase chain reaction, NTS: non‑typhoidal Salmonella. Table 1.Comparison of baseline characteristics at the index ED visits in non-typhoidal Salmonella gastroenteritis between children and adults Table 2.Symptom profile and laboratory, imaging, and microbiological findings Table 3.Antibiotic prescriptions by the age groups References2. Eng SK, Pusparajah P, Ab Mutalib NS, Ser HL, Chan KG, Lee LH. Salmonella: a review on pathogenesis, epidemiology, and antibiotic resistance. Front Life Sci 2015;8:284–93.
3. Eun JS, Han J, Lim JH, Shin E, Kim J, Ko DJ, et al. Salmonellosis outbreaks linked to eggs at 2 gimbap restaurants in Korea. Epidemiol Health 2024;46:e2024036.
4. Moffatt CR, Musto J, Pingault N, Miller M, Stafford R, Gregory J, et al. Salmonella Typhimurium and outbreaks of egg-associated disease in Australia, 2001 to 2011. Foodborne Pathog Dis 2016;13:379–85.
5. Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, et al. The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 2010;50:882–9.
6. Ao TT, Feasey NA, Gordon MA, Keddy KH, Angulo FJ, Crump JA, et al. Global burden of invasive nontyphoidal Salmonella disease, 2010. Emerg Infect Dis 2015;21:941–9.
7. Marchello CS, Birkhold M, Crump JA. Complications and mortality of non-typhoidal salmonella invasive disease: a global systematic review and meta-analysis. Lancet Infect Dis 2022;22:692–705.
8. Shane AL, Mody RK, Crump JA, Tarr PI, Steiner TS, Kotloff K, et al. 2017 Infectious Diseases Society of America clinical practice guidelines for the diagnosis and management of infectious diarrhea. Clin Infect Dis 2017;65:e45–80.
9. Bula-Rudas FJ, Rathore MH, Maraqa NF. Salmonella infections in childhood. Adv Pediatr 2015;62:29–58.
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11. Israel Y, Muhsen K, Rokney A, Adler A. Epidemiological and clinical characteristics of non-typhoidal Salmonella bloodstream infections in central Israel: a case-control study. Microorganisms 2022;10:1942.
12. Mori N, Szvalb AD, Adachi JA, Tarrand JJ, Mulanovich VE. Clinical presentation and outcomes of non-typhoidal Salmonella infections in patients with cancer. BMC Infect Dis 2021;21:1021.
13. Park JB, Lee J, Kim YJ, Lee JH, Lim TH. Reliability of Korean Triage and Acuity Scale: interrater agreement between two experienced nurses by real-time triage and analysis of influencing factors to disagreement of triage levels. J Korean Med Sci 2019;34:e189.
14. Ryu JH, Min MK, Lee DS, Yeom SR, Lee SH, Wang IJ, et al. Changes in relative importance of the 5-level triage system, Korean Triage and Acuity Scale, for the disposition of emergency patients induced by forced reduction in its level number: a multi-center registry-based retrospective cohort study. J Korean Med Sci 2019;34:e114.
15. Ke Y, Lu W, Liu W, Zhu P, Chen Q, Zhu Z, et al. Non-typhoidal Salmonella infections among children in a tertiary hospital in Ningbo, Zhejiang, China, 2012-2019. PLoS Negl Trop Dis 2020;14:e0008732.
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