The Study of Antimicrobial Resistance among Salmonella enterica Strains Isolated from Children with Gastroenteritisin in Tehran, Iran
-
Fatemeh Fardsanei
,
Mohammad Mehdi Soltan Dallal
,
Mojtaba Memariani
,
Sarah Sharifi-Yazdi
,
Fariba Nabatchian
,
Mohammad Kazem Sharifi-Yazdi
Abstract
Background: Salmonella enterica is one of the predominant causes of the food-borne salmonellosis in humans. The aim of this study was to determine antimicrobial resistance patterns of Salmonella enterica isolated from stool samples of children with gastroenteritisin in Tehran, Iran.
Methods: Stool samples of patients with diarrhea in a pediatric hospital in were collected from June 2017 to May 2018. Microbiological methods were used for identification of Salmonella. The identity of Salmonella enterica serotype enteritidis (S. enteritidis) was also confirmed by a multiplex-PCR. Antibiotic susceptibility testing was performed according to the standard procedure of the Clinical and Laboratory Standards Institute (CLSI).
Results: Of 800 samples, 24 were identified as Salmonella. The most prevalent serotype was S. enteritidis (n=10, 41.7%), followed by S. paratyphi C, (n=6, 25%), S. paratyphi B (n=4, 16.7%), S. arizonae 2 (n=2, 8.3%), and S. paratyphi A (n=2, 8.3%). The highest rates of antibiotic resistance were obtained for nitrofurantoin (100%), followed by nalidixic acid (45.8%), and tetracycline (16.7%). Of 24 S. enteritidis, 9 distinct antibiotypes (Abs) were observed. In this respect, 3 isolates (12.5%) were resistant to at least three or more antibiotics. The most prevalent antibiotype was AB1 (n=8, 33%), which was indicative of resistance to nitrofurantoin.
Conclusion: Considering the constant changes in antibiotic resistance patterns among food-borne pathogens over time, continuous monitoring of multidrug-resistant Salmonella isolates would definitely improve infection control strategies.
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2. WHO Estimates of the global burden of foodborne diseases.2015; Foodborne diseases burden epidemiology reference group 2007-2015.
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7. Ziebell K, Chui L, King R, et al. Subtyping of Canadian isolates of Salmonella enteritidis using multiple locus variable number Tandem Repeat Analysis (MLVA) alone and in combination with pulsed-field gel electrophoresis (PFGE) and phage typing. J Microbiol Methods 2017; 139:29-36.
8. Fardsanei F, Nikkhahi F, Bakhshi B, et al. Molecular characterization of Salmonella enterica serotype enteritidis isolates from food and human samples by serotyping, antimicrobial resistance, plasmid profiling, (GTG)5-PCR and ERIC-PCR. New Microbe New Infect 2016; 14: 24-30.
9. Parker CT, Huynh S, Quiñones B, et al. Comparison of genotypes of Salmonella enterica serovar enteritidis phage type 30 and 9c strains isolated during three outbreaks associated with raw almonds. Appl Environ Microbiol 2010; 76(11):3723-31.
10. Tapia MD, Tennant SM, Bornstein K, et al. Invasive Nontyphoidal Salmonella infections among children in Mali, 2002-2014: microbiological and epidemiologic features guide vaccine development. Clin Infect Dis 2015; 61(4):S332-8.
11. Falay D, Kuijpers LM, Phoba MF, et al. Microbiological, clinical and molecular findings of non- typhoidal Salmonella bloodstream infections associated with malaria, Oriental Province, Democratic Republic of the Congo. BMC Infect Dis 2016; 10(16):27.
12. Langendorf C, Le Hello S, Moumouni A, et al. Enteric bacterial pathogens in children with diarrhea in Niger: diversity and antimicrobial resistance. PLoSOne 2015; 23; 10(3):e0120275.
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15. Clinical and laboratory standard institute (CLSI), 2015. Performance standards for antimicrobial susceptibility testing; twenty-fifth informational supplement, Wayne, PA, M100-S25, 35(3).
16. Suh DK, Song JC: Analysis of Salmonella enterica serotype enteritidis isolated from human and chickens by repetitive sequence-PCR Fingerprinting, antibiotic resistance and plasmid profiles. J Vet Sci 2006; 7: 37-41.
17. Rasschaert G, Houf K, Imberechts H, et al. Comparison of five repetitive sequence-based PCR typing methods for molecular discrimination of Salmonella enterica isolates. J ClinMicrobiol 2005; 43:3615-23.
18. Fardsanei F, Soltan Dallal MM, Douraghi M, et al. Genetic diversity and virulence genes of Salmonella enterica subspecies enterica serotype enteritidis isolated from meats and eggs. Microbial Pathog 2017; 17:451-6.
19. Rahman H, Roychaudhury P, Saikia M, et al. Prevalence of Salmonella in enteric infection in man and animals. Indian J Animal Sci 2004; 74:936-937.
20. Ena J, Afonso-Carrillo RG, Bou-Collado M, et al. Epidemiology of severe acute diarrhea in patients requiring hospital admission. J Emerg Med 2019; 57(3):290-8.
21. Aldrich C, Hartman H, Feasey N, et al. Emergence of phylogenetically diverse and fluoroquinolone resistant Salmonella enteritidis as a cause of invasive nontyphoidal Salmonella disease in Ghana. PLoS Negl Trop Dis 2019; 20; 13(6):e0007485.
22. Rahimi Nadi Z, Zahraei Salehi T, Ashrafi Tamai I, et al. Evaluation of antibiotic resistance and prevalence of common Salmonella enterica serovars isolated from foodborne outbreaks. Microchemical J 2020; 155:104660.
23. Soltan Dallal MM, Sharifi Yazdi MK, Mirzaei N, et al. Prevalence of Salmonella spp. in packed and unpacked red meat and chicken in South of Tehran. Jundishapur J Microbiol 2014; 7(4): e9254.
24. Soltan Dallal MM, Doyle MP, Rezadehbashi M, et al. Prevalence and antimicrobial resistance profiles of Salmonella serotypes, Campylobacter and Yersinia spp. isolated from retail chicken and beef, Tehran, Iran. Food Control 2010; 21(4):388–92.
25. Shi C, Singh P, Ranieri ML, et al. Molecular methods for serovar determination of Salmonella. Crit Rev Microbiol 2015; 41(3):309-25.
26. Ranieri ML, Shi C, Moreno Switt AI, et al. Comparison of typing methods with a new procedure based on sequence characterization for Salmonella serovar prediction. J Clin Microbiol 2013; 51(6):1786-97.
27. Eshaghi zadeh SH, Fahimi H, Fardsanei F, Soltan Dallal MM. Antimicrobial Resistance and Presence of Class 1 Integrons Among Different Serotypes of Salmonella spp. Recovered From Children With Diarrhea In Tehran, Iran. Infect Disord Drug Targets 2020; 20(2):160-6.
28. Baratto CM, Gelinski JMLN, Bernardi AZ, Marafon A, Braun F. Potential use of molecular-typing methods for the identification and characterization of Salmonella enterica serotypes isolated in the poultry production chain. Rev Bras Cienc Avic 2012; 14(3):173-9.
29. Yoshida C, Gurnik S, Ahmad A, Blimkie T, Murphy SA, Kropinski AM et al. Evaluation of molecular methods for identification of Salmonella serovars. J Clin Microbiol 2016; 54(8):1992–8.
30. Eshraghi S. Soltan-Dalal M.M. Fardsanei F. Salmonella enteritidis and antibiotic resistance patterns: a study on 1950 children with diarrhea. Tehran Univ Med 2010. J67:876–82.
2. WHO Estimates of the global burden of foodborne diseases.2015; Foodborne diseases burden epidemiology reference group 2007-2015.
3. Kang MS, Oh JY, Kwon YK, et al. Public health significance of major genotypes of Salmonella enterica serovar enteritidis present in both human and chicken isolates in Korea. Res Vet Sci 2017; 112:125-31.
4. Soltan Dallal MM, Khalilian M, Masoumi Asl H, et al. Molecular epidemiology and antimicrobial resistance of Salmonella spp. isolated from resident patients in Mazandaran Province, Northern Iran. J Food Qual Haz Cont 2016; 3: 146-51.
5. Lund BM, O'Brien SJ. The occurrence and prevention of foodborne disease in vulnerable people. Foodborne Pathog Dis 2011; 8(9):961-73.
6. Lund BM. Microbiological food safety for vulnerable people. Int J Environ Res Public Health 2015; 12(8):10117-32.
7. Ziebell K, Chui L, King R, et al. Subtyping of Canadian isolates of Salmonella enteritidis using multiple locus variable number Tandem Repeat Analysis (MLVA) alone and in combination with pulsed-field gel electrophoresis (PFGE) and phage typing. J Microbiol Methods 2017; 139:29-36.
8. Fardsanei F, Nikkhahi F, Bakhshi B, et al. Molecular characterization of Salmonella enterica serotype enteritidis isolates from food and human samples by serotyping, antimicrobial resistance, plasmid profiling, (GTG)5-PCR and ERIC-PCR. New Microbe New Infect 2016; 14: 24-30.
9. Parker CT, Huynh S, Quiñones B, et al. Comparison of genotypes of Salmonella enterica serovar enteritidis phage type 30 and 9c strains isolated during three outbreaks associated with raw almonds. Appl Environ Microbiol 2010; 76(11):3723-31.
10. Tapia MD, Tennant SM, Bornstein K, et al. Invasive Nontyphoidal Salmonella infections among children in Mali, 2002-2014: microbiological and epidemiologic features guide vaccine development. Clin Infect Dis 2015; 61(4):S332-8.
11. Falay D, Kuijpers LM, Phoba MF, et al. Microbiological, clinical and molecular findings of non- typhoidal Salmonella bloodstream infections associated with malaria, Oriental Province, Democratic Republic of the Congo. BMC Infect Dis 2016; 10(16):27.
12. Langendorf C, Le Hello S, Moumouni A, et al. Enteric bacterial pathogens in children with diarrhea in Niger: diversity and antimicrobial resistance. PLoSOne 2015; 23; 10(3):e0120275.
13. Popoff MY, LeMinor L. Antigenic formulase of the Salmonella serovars. WHO collaborating center for reference and research on Salmonella. Institute Pasteur, Paris, France, 1997.
14. Winn WC, Allen SD, Janda WM, et al. Color atlas and textbook of diagnostic microbiology, sixth ed., Lippincott Williams & Wilkins, 2005.
15. Clinical and laboratory standard institute (CLSI), 2015. Performance standards for antimicrobial susceptibility testing; twenty-fifth informational supplement, Wayne, PA, M100-S25, 35(3).
16. Suh DK, Song JC: Analysis of Salmonella enterica serotype enteritidis isolated from human and chickens by repetitive sequence-PCR Fingerprinting, antibiotic resistance and plasmid profiles. J Vet Sci 2006; 7: 37-41.
17. Rasschaert G, Houf K, Imberechts H, et al. Comparison of five repetitive sequence-based PCR typing methods for molecular discrimination of Salmonella enterica isolates. J ClinMicrobiol 2005; 43:3615-23.
18. Fardsanei F, Soltan Dallal MM, Douraghi M, et al. Genetic diversity and virulence genes of Salmonella enterica subspecies enterica serotype enteritidis isolated from meats and eggs. Microbial Pathog 2017; 17:451-6.
19. Rahman H, Roychaudhury P, Saikia M, et al. Prevalence of Salmonella in enteric infection in man and animals. Indian J Animal Sci 2004; 74:936-937.
20. Ena J, Afonso-Carrillo RG, Bou-Collado M, et al. Epidemiology of severe acute diarrhea in patients requiring hospital admission. J Emerg Med 2019; 57(3):290-8.
21. Aldrich C, Hartman H, Feasey N, et al. Emergence of phylogenetically diverse and fluoroquinolone resistant Salmonella enteritidis as a cause of invasive nontyphoidal Salmonella disease in Ghana. PLoS Negl Trop Dis 2019; 20; 13(6):e0007485.
22. Rahimi Nadi Z, Zahraei Salehi T, Ashrafi Tamai I, et al. Evaluation of antibiotic resistance and prevalence of common Salmonella enterica serovars isolated from foodborne outbreaks. Microchemical J 2020; 155:104660.
23. Soltan Dallal MM, Sharifi Yazdi MK, Mirzaei N, et al. Prevalence of Salmonella spp. in packed and unpacked red meat and chicken in South of Tehran. Jundishapur J Microbiol 2014; 7(4): e9254.
24. Soltan Dallal MM, Doyle MP, Rezadehbashi M, et al. Prevalence and antimicrobial resistance profiles of Salmonella serotypes, Campylobacter and Yersinia spp. isolated from retail chicken and beef, Tehran, Iran. Food Control 2010; 21(4):388–92.
25. Shi C, Singh P, Ranieri ML, et al. Molecular methods for serovar determination of Salmonella. Crit Rev Microbiol 2015; 41(3):309-25.
26. Ranieri ML, Shi C, Moreno Switt AI, et al. Comparison of typing methods with a new procedure based on sequence characterization for Salmonella serovar prediction. J Clin Microbiol 2013; 51(6):1786-97.
27. Eshaghi zadeh SH, Fahimi H, Fardsanei F, Soltan Dallal MM. Antimicrobial Resistance and Presence of Class 1 Integrons Among Different Serotypes of Salmonella spp. Recovered From Children With Diarrhea In Tehran, Iran. Infect Disord Drug Targets 2020; 20(2):160-6.
28. Baratto CM, Gelinski JMLN, Bernardi AZ, Marafon A, Braun F. Potential use of molecular-typing methods for the identification and characterization of Salmonella enterica serotypes isolated in the poultry production chain. Rev Bras Cienc Avic 2012; 14(3):173-9.
29. Yoshida C, Gurnik S, Ahmad A, Blimkie T, Murphy SA, Kropinski AM et al. Evaluation of molecular methods for identification of Salmonella serovars. J Clin Microbiol 2016; 54(8):1992–8.
30. Eshraghi S. Soltan-Dalal M.M. Fardsanei F. Salmonella enteritidis and antibiotic resistance patterns: a study on 1950 children with diarrhea. Tehran Univ Med 2010. J67:876–82.
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| Issue | Vol 9 No 1-2 (2020) | |
| Section | Original Articles | |
| Keywords | ||
| Antibiotic resistance Antibiotypes Diarrhea Salmonella enteritidis Salmonellosis. | ||
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How to Cite
1.
Fardsanei F, Soltan Dallal MM, Memariani M, Sharifi-Yazdi S, Nabatchian F, Sharifi-Yazdi MK. The Study of Antimicrobial Resistance among Salmonella enterica Strains Isolated from Children with Gastroenteritisin in Tehran, Iran. J Med Bacteriol. 2020;9(1-2):25-32.
