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Letters to the Editor

Prevalent Serotypes and Antibiotic Resistance Patterns of Salmonella Strains Isolated from Diarrheic Children during a 10-year Period in a Tertiary Referral Center in Chengdu, China

Xiao, Guoguang MD; Zhou, Wei MD; Shu, Min MD; Tan, Shan MD; Zhu, Yu MD; Deng, Jianjun MD; Guo, Qin MD; Wan, Chaomin MD, PhD

Author Information
The Pediatric Infectious Disease Journal: July 2015 - Volume 34 - Issue 7 - p 798-799
doi: 10.1097/INF.0000000000000495
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To the Editors:

Acute gastroenteritis is a leading cause of morbidity and mortality in children younger than 5-years old worldwide. It is estimated that about 1.731 billion episodes of diarrhea occurred in children under 5-years old in 2010, and 0.71 million episodes of diarrhea led to death in 2011.1Salmonella is one of the most important causes of childhood diarrheal disease.2 As the resistance of Salmonella strains to many commonly used antibiotics in the clinical practice has been reported by many studies,2,3 the management of severe Salmonella infections could become more and more difficult for physicians. Studies investigating the epidemiology of the prevalent serotypes of Salmonella species within the child population in Chengdu district have been scarce so far. Here, we conducted a retrospective analysis of the prevalent serotypes and antibiotic resistance patterns of the Salmonella strains isolated from hospitalized children with diarrheal illness over a 10-year period.

Medical records of patients whose stool was culture-positive for Salmonella species at West China Second Hospital, Sichuan University between January 2004 and December 2013 were reviewed. Fecal samples were cultured directly on the xylose lysine desoxycholate medium and MacConkey agar (Oxoid Ltd, Basingstoke, UK) within 2 hours after sample collection at 35 ± 1°C for 24–48 hours at the clinical microbiology laboratory. Isolates were identified by an automated VITEK card system (bioMérieux, Hazelwood, MO). The identified Salmonella strains were serogrouped using somatic group Salmonella A–F anti-sera, and Salmonella serovars were identified by agglutination with specific anti-sera for O and H antigens (Lanzhou Institute of Biological Products Co., Ltd, Lanzhou, China). The antibiotic susceptibility testing was performed using an automated VITEK system with Gram-negative bacteria cards (bioMérieux). In this analysis, strains showing intermediate susceptibility were regarded as sensitive.3 χ2 test or Fisher exact test was employed for statistical comparisons using SPSS version 13.0 (SPSS Inc., Chicago, IL) where appropriate. A P value <0.05 was considered to be statistically significant. The study protocol was approved by the hospital review board.

During the 10-year period, a total of 96 Salmonella strains were isolated from the fecal specimens of 96 hospitalized child patients with diarrheal illness. Salmonella enterica serovar typhimurium (42/96, 43.8%) and Salmonella enterica serovar dublin (20/96, 20.8%) were the 2 most commonly isolated strains, followed by Salmonella enterica serovar Enteritidis (6/96, 6.3%). The resistance patterns of the identified Salmonella strains to some antibiotics during the 2 study periods are shown in Table, Supplemental Digital Content 1, As shown in Table 1, strains isolated within the 2009–2013 period were more resistant to many antibiotics than between 2004 and 2008. No strains were found to be resistant to imipenem or meropenem. Resistance to amoxicillin (26/44, 59.1%), cefotaxime (6/44, 13.6%) and netilmicin (12/44, 27.3%) was tested in strains isolated during 2004–2010, and ampicillin (40/52, 76.9%), cefazolin (52/52, 100%), ceftriaxone (22/52, 42.3%), levofloxacin (0/51, 0.0%) and tetracycline (11/13, 84.6%) during 2010–2013.

The Resistance Patterns of the Identified Salmonella Strains to some Antibiotics During the 2 Study Periods

In the present study, Salmonella typhimurium was the most prevalent strains. These results are different from those reported in other parts of world.2–4Salmonella enteritidis, which have been reported as the most common Salmonella serotype worldwide,4 accounted for only 6.3% of all the isolated Salmonella strains in this study. S. typhimurium was the most prevalent strains in North America and Taiwan as reported in previous studies.4,5

Although mainly adapted to bovines and a relatively uncommon cause of human diseases,6 and not even being reported among the 10 most common serotypes in some large studies,4,5Salmonella dublin was the second most commonly isolated strain in our study. S. dublin can cause severe invasive infections in humans.7 The only fatal case in this study was infected with S. dublin. Cephalosporins were considered the drug of choice for children with severe Salmonella gastroenteritis. However, the tested strains exhibited resistance to cefazolin and to many third-generation cephalosporins. Ceftazidine was commonly used in the treatment of diarrheal diseases caused by Salmonella in our center, and resistance to ceftazidine increased from 5.9% to 29.0% during the 2 periods. The resistance rates for third-generation cephalosporins in this study are higher than that reported from other parts of Mainland China3,8 and other countries.2 The increased resistance to third-generation cephalosporins may be related to the extensive and sometimes inappropriate use of these antibiotics.

Resistance to ciprofloxacin was relatively low and had a declining trend, although not significantly different, between the 2 periods, and no isolates were resistant to levofloxacin, similar to the results in other studies.3,8 Of note, there were 12.5% (12/96) of the strains displaying intermediate susceptibility to ciprofloxacin, and 1.9% (1/52) to levofloxacin.

Guoguang Xiao, MD

Department of Pediatrics

West China Second Hospital

Sichuan University

Chengdu, China

Wei Zhou, MD

Department of Clinical Microbiology Laboratory

West China Second Hospital

Sichuan University

Chengdu, China

Min Shu, MD

Shan Tan, MD

Yu Zhu, MD

Jianjun Deng, MD

Qin Guo, MD

Chaomin Wan, MD, PhD

Department of Pediatrics

West China Second Hospital

Sichuan University

Chengdu, China


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2. Ince OT, Yalçin SS, Yurdakök K, et al. Salmonella gastroenteritis in children (clinical characteristics and antibiotic susceptibility): comparison of the years 1995-2001 and 2002-2008. Turk J Pediatr. 2012;54:465–473
3. Li Y, Xie X, Xu X, et al. Nontyphoidal salmonella infection in children with acute gastroenteritis: prevalence, serotypes, and antimicrobial resistance in Shanghai, China. Foodborne Pathog Dis. 2014;11:200–206
4. Galanis E, Lo Fo Wong DM, Patrick ME, et al.World Health Organization Global Salm-Surv. Web-based surveillance and global Salmonella distribution, 2000-2002. Emerg Infect Dis. 2006;12:381–388
5. Lee HY, Su LH, Tsai MH, et al. High rate of reduced susceptibility to ciprofloxacin and ceftriaxone among nontyphoid Salmonella clinical isolates in Asia. Antimicrob Agents Chemother. 2009;53:2696–2699
6. Allerberger F, Liesegang A, Grif K, et al. Occurrence of Salmonella enterica serovar Dublin in Austria. Wien Med Wochenschr. 2003;153:148–152
7. Helms M, Vastrup P, Gerner-Smidt P, et al. Short and long term mortality associated with foodborne bacterial gastrointestinal infections: registry based study. BMJ. 2003;326:357
8. Cui S, Li J, Sun Z, et al. Characterization of Salmonella enterica isolates from infants and toddlers in Wuhan, China. J Antimicrob Chemother. 2009;63:87–94

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