The Clinical Implication of Serogroup Distribution and Drug Resistance of Non-Typhoidal Salmonella in Children: A Single Center Study in Southern Taiwan during 2004–2019
Abstract
:1. Introduction
2. Materials and Methods
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Majowicz, S.E.; Musto, J.; Scallan, E.; Angulo, F.J.; Kirk, M.; O’Brien, S.J.; Jones, T.F.; Fazil, A.; Hoekstra, R.M.; International Collaboration on Enteric Disease ‘Burden of Illness’ Studies. The global burden of nontyphoidal Salmonella gastroenteritis. Clin. Infect. Dis. 2010, 50, 882–889. [Google Scholar] [CrossRef]
- Stutman, H.R. Salmonella, Shigella, and Campylobacter: Common bacterial causes of infectious diarrhea. Pediatr. Ann. 1994, 23, 538–543. [Google Scholar] [CrossRef] [PubMed]
- Chen, S.M.; Ni, Y.H.; Chen, H.L.; Chang, M.H. Microbial etiology of acute gastroenteritis in hospitalized children in Taiwan. J. Formos. Med. Assoc. 2006, 105, 964–970. [Google Scholar] [CrossRef]
- Scallan, E.; Mahon, B.E.; Hoekstra, R.M.; Griffin, P.M. Estimates of illnesses, hospitalizations and deaths caused by major bacterial enteric pathogens in young children in the United States. Pediatr. Infect. Dis. J. 2013, 32, 217–221. [Google Scholar] [CrossRef]
- Su, L.H.; Chiu, C.H. Salmonella: Clinical importance and evolution of nomenclature. Chang Gung Med. J. 2007, 30, 210–219. [Google Scholar] [PubMed]
- Li, Y.; Xie, X.; Xu, X.; Wang, X.; Chang, H.; Wang, C.; Wang, A.; He, Y.; Yu, H.; Wang, X. Nontyphoidal salmonella infection in children with acute gastroenteritis: Prevalence, serotypes, and antimicrobial resistance in Shanghai, China. Foodborne Pathog. Dis. 2014, 11, 200–206. [Google Scholar] [CrossRef]
- Chang, Y.J.; Chen, M.C.; Feng, Y.; Su, L.H.; Li, H.C.; Yang, H.P.; Yu, M.J.; Chen, C.L.; Chiu, C.H. Highly antimicrobial-resistant Nontyphoidal Salmonella from retail meats and clinical impact in children, Taiwan. Pediatr. Neonatol. 2020, 61, 432–438. [Google Scholar] [CrossRef]
- Su, L.H.; Wu, T.L.; Chia, J.H.; Chu, C.; Kuo, A.J.; Chiu, C.H. Increasing ceftriaxone resistance in Salmonella isolates from a university hospital in Taiwan. J. Antimicrob. Chemother. 2005, 55, 846–852. [Google Scholar] [CrossRef]
- 14th Informational Supplement. M100-S14; Clinical and Laboratory Standards Institute: Performance Standards for Antimicrobial Susceptibility Testing. Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2004.
- Hung, Y.T.; Lay, C.J.; Wang, C.L.; Koo, M. Characteristics of nontyphoidal Salmonella gastroenteritis in Taiwanese children: A 9-year period retrospective medical record review. J. Infect. Public Health 2017, 10, 518–521. [Google Scholar] [CrossRef] [PubMed]
- Lo, H.Y.; Lai, F.P.; Yang, Y.J. Changes in epidemiology and antimicrobial susceptibility of nontyphoid Salmonella in children in southern Taiwan, 1997–2016. J. Microbiol. Immunol. Infect. 2020, 53, 585–591. [Google Scholar] [CrossRef]
- Tseng, C.F.; Chiu, N.C.; Huang, C.Y.; Huang, D.T.; Chang, L.; Kung, Y.H.; Huang, F.Y.; Chi, H. The epidemiology of non-typhoidal Salmonella gastroenteritis and Campylobacter gastroenteritis in pediatric inpatients in northern Taiwan. J. Microbiol. Immunol. Infect. 2019, 52, 449–455. [Google Scholar] [CrossRef] [PubMed]
- Chang, Y.J.; Chen, Y.C.; Chen, N.W.; Hsu, Y.J.; Chu, H.H.; Chen, C.L.; Chiu, C.H. Changing Antimicrobial Resistance and Epidemiology of Non-Typhoidal Salmonella Infection in Taiwanese Children. Front. Microbiol. 2021, 12, 648008. [Google Scholar] [CrossRef] [PubMed]
- Ince, O.T.; Yalcin, S.S.; Yurdakok, K.; Ozmert, E.N.; Aydin, A.; Baris, Z.; Gur, D. 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. [Google Scholar]
- Jones, T.F.; Ingram, L.A.; Cieslak, P.R.; Vugia, D.J.; Tobin-D’Angelo, M.; Hurd, S.; Medus, C.; Cronquist, A.; Angulo, F.J. Salmonellosis outcomes differ substantially by serotype. J. Infect. Dis. 2008, 198, 109–114. [Google Scholar] [CrossRef]
- Gordon, M.A.; Graham, S.M.; Walsh, A.L.; Wilson, L.; Phiri, A.; Molyneux, E.; Zijlstra, E.E.; Heyderman, R.S.; Hart, C.A.; Molyneux, M.E. Epidemics of invasive Salmonella enterica serovar enteritidis and S. enterica Serovar typhimurium infection associated with multidrug resistance among adults and children in Malawi. Clin. Infect. Dis. 2008, 46, 963–969. [Google Scholar] [CrossRef]
- Lee, C.M.; Lee, M.S.; Yang, T.L.; Lee, K.L.; Yen, T.Y.; Lu, C.Y.; Hsueh, P.R.; Lee, P.I.; Chen, J.M.; Huang, L.M. Clinical features and risk factors associated with bacteremia of nontyphoidal salmonellosis in pediatric patients, 2010–2018. J. Formos. Med. Assoc. 2021, 120 Pt 1, 196–203. [Google Scholar] [CrossRef]
- Wu, H.M.; Huang, W.Y.; Lee, M.L.; Yang, A.D.; Chaou, K.P.; Hsieh, L.Y. Clinical features, acute complications, and outcome of Salmonella meningitis in children under one year of age in Taiwan. BMC Infect. Dis. 2011, 11, 30. [Google Scholar] [CrossRef] [PubMed]
- Keddy, K.H.; Sooka, A.; Musekiwa, A.; Smith, A.M.; Ismail, H.; Tau, N.P.; Crowther-Gibson, P.; Angulo, F.J.; Klugman, K.P.; GERMS-SA. Clinical and Microbiological Features of Salmonella Meningitis in a South African Population, 2003–2013. Clin. Infect. Dis. 2015, 61 (Suppl. 4), S272–S282. [Google Scholar] [CrossRef]
- Rodrigues, G.L.; Panzenhagen, P.; Ferrari, R.G.; Paschoalin, V.M.F.; Conte-Junior, C.A. Antimicrobial Resistance in Nontyphoidal Salmonella Isolates from Human and Swine Sources in Brazil: A Systematic Review of the Past Three Decades. Microb. Drug Resist. 2020, 26, 1260–1270. [Google Scholar] [CrossRef]
- Duong, V.T.; The, H.C.; Nhu, T.D.H.; Tuyen, H.T.; Campbell, J.I.; Minh, P.V.; Phuc, H.L.; Chau, T.T.H.; Ngoc, N.M.; Vi, L.L. Genomic Serotyping, Clinical Manifestations, and Antimicrobial Resistance of Nontyphoidal Salmonella Gastroenteritis in Hospitalized Children in Ho Chi Minh City, Vietnam. J. Clin. Microbiol. 2020, 58, e01465-20. [Google Scholar] [CrossRef]
- Maraki, S.; Samonis, G.; Mantadakis, E.; Nioti, E.; Tselentis, Y. Serotype distribution and antimicrobial resistance of Salmonella enterica from patients with gastroenteritis in Crete, Greece. Eur. J. Clin. Microbiol. Infect. Dis. 2006, 25, 116–119. [Google Scholar] [CrossRef] [PubMed]
- Winokur, P.L.; Brueggemann, A.; DeSalvo, D.L.; Hoffmann, L.; Apley, M.D.; Uhlenhopp, E.K.; Pfaller, M.A.; Doern, G.V. Animal and human multidrug-resistant, cephalosporin-resistant salmonella isolates expressing a plasmid-mediated CMY-2 AmpC beta-lactamase. Antimicrob. Agents Chemother. 2000, 44, 2777–2783. [Google Scholar] [CrossRef] [PubMed]
- Patel, K.; Goldman, J.L. Safety Concerns Surrounding Quinolone Use in Children. J. Clin. Pharmacol. 2016, 56, 1060–1075. [Google Scholar] [CrossRef] [PubMed]
- Fey, P.D.; Safranek, T.J.; Rupp, M.E.; Dunne, E.F.; Ribot, E.; Iwen, P.C.; Bradford, P.A.; Angulo, F.J.; Hinrichs, S.H. Ceftriaxone-resistant salmonella infection acquired by a child from cattle. N. Engl. J. Med. 2000, 342, 1242–1249. [Google Scholar] [CrossRef]
- Su, L.H.; Chiu, C.H.; Chu, C.; Ou, J.T. Antimicrobial resistance in nontyphoid Salmonella serotypes: A global challenge. Clin. Infect. Dis. 2004, 39, 546–551. [Google Scholar] [CrossRef]
- Alcaine, S.D.; Sukhnanand, S.S.; Warnick, L.D.; Su, W.L.; McGann, P.; McDonough, P.; Wiedmann, M. Ceftiofur-resistant Salmonella strains isolated from dairy farms represent multiple widely distributed subtypes that evolved by independent horizontal gene transfer. Antimicrob. Agents Chemother. 2005, 49, 4061–4067. [Google Scholar] [CrossRef]
- Su, L.H.; Teng, W.S.; Chen, C.L.; Lee, H.Y.; Li, H.C.; Wu, T.L.; Chiu, C.H. Increasing ceftriaxone resistance in Salmonellae, Taiwan. Emerg. Infect. Dis. 2011, 17, 1086–1090. [Google Scholar] [CrossRef]
- Chen, K.; Dong, N.; Chan, E.W.; Chen, S. Transmission of ciprofloxacin resistance in Salmonella mediated by a novel type of conjugative helper plasmids. Emerg. Microbes. Infect. 2019, 8, 857–865. [Google Scholar] [CrossRef] [Green Version]
Year Serogroup | 2004 | 2005 | 2006 | 2007 | 2008 | 2009 | 2010 | 2011 | 2012 | 2013 | 2014 | 2015 | 2016 | 2017 | 2018 | 2019 | Total | The Trend of Prevalence |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Serogroup B | 8 (61.5%) | 70 (58.8%) | 69 (53.5%) | 74 (54.0%) | 64 (44.8%) | 50 (31.6%) | 41 (35.7%) | 62 (54.9%) | 45 (42.1%) | 48 (39.7%) | 38 (39.2%) | 39 (41.1%) | 36 (40.9%) | 21 (25.9%) | 20 (37.7%) | 3 (21.4%) | 688 | |
Serogroup C1 | 0 (0%) | 7 (5.9%) | 7 (5.4%) | 13 (9.5%) | 18 (12.6%) | 17 (10.8%) | 6 (5.2%) | 10 (8.8%) | 9 (8.4%) | 13 (10.7%) | 11 (11.3%) | 10 (10.5%) | 6 (6.8%) | 7 (8.6%) | 4 (7.5%) | 1 (7.1%) | 139 | |
Serogroup C2 | 1 (7.7%) | 17 (14.3%) | 16 (12.4%) | 20 (14.6%) | 21 (14.7%) | 24 (15.2%) | 25 (21.7%) | 9 (8.0%) | 17 (15.9%) | 15 (12.4%) | 7 (7.2%) | 7 (7.4%) | 10 (11.4%) | 10 (12.3%) | 6 (11.3%) | 2 (14.3%) | 207 | |
Serogroup D | 3 (23.1%) | 22 (18.5%) | 33 (25.6%) | 29 (21.2%) | 36 (25.2%) | 65 (41.1%) | 41 (35.7%) | 29 (25.7%) | 35 (32.7%) | 44 (36.4%) | 40 (41.2%) | 35 (36.8%) | 27 (30.7%) | 23 (28.4%) | 14 (26.4%) | 5 (35.7%) | 481 | |
Serogroup E | 1 (7.7%) | 3 (2.5%) | 4 (3.1%) | 1 (0.7%) | 4 (2.8%) | 2 (1.3%) | 2 (1.7%) | 3 (2.7%) | 1 (0.9%) | 1 (0.8%) | 1 (1.0%) | 4 (4.2%) | 9 (10.2%) | 20 (24.7%) | 9 (17.0%) | 3 (21.4%) | 68 | |
Total | 13 | 119 | 129 | 137 | 143 | 158 | 115 | 113 | 107 | 121 | 97 | 95 | 88 | 81 | 53 | 14 |
Serogroup B | Serogroup C1 | Serogroup C2 | Serogroup D | Serogroup E | |||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Non-Susceptibility | B | Non-B | p-Value | C1 | Non-C1 | p-Value | C2 | Non-C2 | p-Value | D | Non-D | p-Value | E | Non-E | p-Value |
Ampicillin | 66.4% | 24.8% | 0.000 * | 15.1% | 45.6% | 0.000 * | 29.0% | 45.0% | 0.000 * | 20.8% | 52.5% | 0.000 * | 60.3% | 42.1% | 0.004 * |
Chloramphenicol | 51.7% | 13.4% | 0.000 * | 11.5% | 31.9% | 0.004 * | 26.6% | 30.6% | 0.256 | 2.3% | 42.4% | 0.000 * | 55.9% | 28.9% | 0.000 * |
Ciprofloxacin | 2.6% | 1.6% | 0.152 | 2.2% | 2.0% | 0.756 | 2.9% | 1.9% | 0.296 | 0.2% | 2.8% | 0.000 * | 5.9% | 1.8% | 0.045 * |
Ceftriaxone | 9.7% | 3.0% | 0.000 * | 4.3% | 6.1% | 0.571 | 3.4% | 6.3% | 0.114 | 1.9% | 7.7% | 0.000 * | 7.4% | 5.9% | 0.596 |
Sulfamethoxazole-Trimethoprim | 29.9% | 18.7% | 0.000 * | 23.0% | 23.6% | 0.917 | 25.6% | 23.3% | 0.482 | 8.9% | 29.9% | 0.000 * | 57.4% | 22.0% | 0.000 * |
iNTS | Non-iNTS | |||||
---|---|---|---|---|---|---|
2004~2011 | 2012~2019 | p-Value | 2004~2011 | 2012~2019 | p-Value | |
Antibiotics non-susceptibility | ||||||
Ampicillin | 29.1% | 29.4% | 1.000 | 39.4% | 49.1% | 0.000 * |
Chloramphenicol | 27.3% | 29.4% | 1.000 | 34.1% | 24.9% | 0.000 * |
Ciprofloxacin | 14.5% | 17.6% | 0.714 | 1.1% | 1.7% | 0.379 |
Ceftriaxone | 5.5% | 0.0% | 1.000 | 6.1% | 5.9% | 1.000 |
Sulfamethoxazole-Trimethoprim | 23.6% | 29.4% | 0.750 | 23.6% | 23.3% | 0.902 |
Serogroup | ||||||
B | 41.8% | 23.5% | 0.253 | 47.6% | 38.5% | 0.000 * |
C1 | 7.3% | 23.5% | 0.083 | 8.5% | 8.9% | 0.782 |
C2 | 29.1% | 23.5% | 0.764 | 13.4% | 11.0% | 0.156 |
D | 21.8% | 29.4% | 0.527 | 28.2% | 34.1% | 0.015 * |
E | 0.0% | 0.0% | 1.000 | 2.3% | 7.5% | 0.000 * |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Lee, M.-C.; Lee, Z.-M.; Yeh, Y.-C.; Yu, H.-R.; Kuo, K.-C. The Clinical Implication of Serogroup Distribution and Drug Resistance of Non-Typhoidal Salmonella in Children: A Single Center Study in Southern Taiwan during 2004–2019. Children 2022, 9, 1403. https://doi.org/10.3390/children9091403
Lee M-C, Lee Z-M, Yeh Y-C, Yu H-R, Kuo K-C. The Clinical Implication of Serogroup Distribution and Drug Resistance of Non-Typhoidal Salmonella in Children: A Single Center Study in Southern Taiwan during 2004–2019. Children. 2022; 9(9):1403. https://doi.org/10.3390/children9091403
Chicago/Turabian StyleLee, Meng-Chien, Zon-Min Lee, Yi-Chun Yeh, Hong-Ren Yu, and Kuang-Che Kuo. 2022. "The Clinical Implication of Serogroup Distribution and Drug Resistance of Non-Typhoidal Salmonella in Children: A Single Center Study in Southern Taiwan during 2004–2019" Children 9, no. 9: 1403. https://doi.org/10.3390/children9091403