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Background. Salmonella enterica ser. Typhi and Salmonella enterica ser. Paratyphi are agents of typhoid fever, a severe systemic disease, which remains to be a public health concern in the Philippines. Infection due to non-typhoidal Salmonella (NTS), on the other hand, most often results in a self-limiting acute gastroenteritis but may result in invasive disease in some cases. There is scarcity of information on the Salmonella serotypes in the Philippines which limits understanding of the distribution, transmission and antimicrobial resistance of these bacteria.
Objective. This study describes the serotype distribution and antimicrobial resistance of Salmonella in the Philippines over a 15-year period.
Methodolgy. Salmonella isolates were collected through the Philippine Department of Health-Antimicrobial Resistance Surveillance Program (DOH-ARSP) from January 1, 2004 to December 31, 2018. The isolates were serotyped using Sven Gard method for slide agglutination using antigens from Denka Seiken (Japan), and S and A serotest (Thailand). Antigenic formula obtained were classified according to White-Kauffmann-LeMinor scheme. Antimicrobial susceptibility testing for ampicillin, ceftriaxone, cefotaxime, chloramphenicol, ciprofloxacin, and trimethoprim-sulfamethoxazole, were performed using both automated and conventional methods (Kirby Bauer disk diffusion and gradient diffusion method). Antimicrobial susceptibility results were interpreted using Clinical and Laboratory Standards Institute (CLSI) 2018 interpretive criteria (M100Ed28E).
Results. A total of 2,387 isolates were collected from human specimens during the 15-year study period. There were 69 serotypes of Salmonella identified with the most common being Salmonella enterica ser. Typhi: n=1895 (79.39%), Salmonella enterica ser. Enteritidis: n=182 (7.62%), Salmonella enterica ser. Typhimurium: n=87 (3.64%), Salmonella enterica ser. Weltevreden: n=24 (1.00%), Salmonella enterica ser. Paratyphi A: n=17 (0.71%), Salmonella enterica ser. Stanley: n=17 (0.71%), Salmonella enterica ser. Anatum: n=13 (0.54%), Salmonella enterica ser. Heidelberg: n=12 (0.50%), Salmonella enterica ser. Choleraesuis var. Kunzendorf: n=9 (0.38%). The multidrug resistant Salmonella serotypes reported in this study were mostly resistant to ampicillin, cefotaxime, ciprofloxacin combinations.
Conclusion. This present study showed that prevailing Salmonella serotypes in the Philippines were similar with Salmonella serotypes reported from other Asian countries. Typhoidal isolates were high among 6-17 years old and were mostly from males. The antimicrobial resistance rates for typhoidal Salmonella isolates to ampicillin, chloramphenicol, trimethoprim-sulfamethoxazole, ciprofloxacin, ceftriaxone and cefotaxime were lower compared with the antimicrobial resistance rates for non-typhoidal Salmonella isolates. Multidrug resistance for both Salmonella Typhi and NTS were relatively low. Continued and enhanced surveillance is needed to monitor the rising levels of antimicrobial resistance, determine risk factors and exposures associated with Salmonella Typhi and NTS infection to guide prevention and control measures.
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The Philippine Journal of Pathology is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License. Based on works made open access at http://philippinejournalofpathology.org
2. Bennet JE, Doilin R, Blaser MJ, eds. Mandell, Douglas, and Bennett's Principles and Practice of Infectious Diseases Principles and Practice of Infectious diseases. Elsevier Inc., 8th ed; 2015.
3. Department of Health. Epidemiology Bureau Public Health Surveillance Division. Food and Waterborne Diseases. https://www.doh.gov.ph/sites/default/files/statistics/Food%20and%20Waterborne%20Diseases%20Monthly%20Report_MW1-MW30_2018_No.7.pdf. Accessed November 6, 2019
4. National Antibiotic Guidelines Committee. National Antibiotics Guidelines 2017. https://drive.google.com/file/d/11yc2OggVkTAim3fNG7rgmyEloHanQKnR/view.
5. Antimicrobial Resistance Surveillance Reference Laboratory. Antimicrobial Resistance Surveillance Program Annual Report 2018. Accessed November 8, 2019
6. Chau TT, Campbell JI, Galindo CM, et al. Antimicrobial drug resistance of Salmonella enterica serovar Typhi in Asia and molecular mechanism of reduced susceptibility to the fluoroquinolones. Antimicrob Agents Chemother. 2007;51(12):4315-23. https://www.ncbi.nlm.nih.gov/pubmed/17908946. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2167998. https://doi.org/10.1128/AAC.00294-07.
7. Gupta SK, Sharma P, McMillan EA, et al. Genomic comparison of diverse Salmonella serovars isolated from swine. PLoS ONE. 2019;14(11): e0224518. https://www.ncbi.nlm.nih.gov/pubmed/31675365. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6824618. https://doi.org/10.1371/journal.pone.0224518.
8. Galanis E, Lo Fo Wong DM, Patrick ME, et al. Web-based surveillance and global Salmonella distribution, 2000–2002.2006. Emerg Infect Dis. 2006;12(3):381–8. https://www.ncbi.nlm.nih.gov/pubmed/16704773. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3291443. https://doi.org/10.3201/eid1205.050854.
9. Popoff M, Bockemüh J, Gheesling L. Supplement 2002 (no. 46) to the Kauffmann–White scheme. 2002;155(7):568-70. https://doi.org/10.1016/j.resmic.2004.04.005.
10. Department of Health- Epidemiology Bureau Public Health Surveillance Division. Food and Waterborne Diseases Monthly Surveillance Report No. 2; 2019. https://www.doh.gov.ph/sites/default/files/statistics/2019_Monthly_FWBD_Report_N2.pdf. Accessed November 25, 2019.
11. Philippine Statistics Authority. Male to Female Sex Ratio 2004-2015. https://psa.gov.ph/ Accessed November 27, 2019.
12. Green MS. The male predominance in the incidence of infectious diseases in children: a postulated explanation for disparities in the literature. Int J Epidemiol. 1992; 21(2):381–6. https://doi.org/10.1093/ije/21.2.381.
13. Philippine Progress Report on the Millennium Development Goals. 2010. https://www.scribd.com/doc/58268821/Philippines-2010-Progress-Report-on-the-Millenium-Development-Goals/. Accessed November 2, 2019
14. Denyer SP, Hodges NA, Gorman, SP, Gilmore BF .Hugo and Russell s Pharmaceutical Microbiology, 8th ed. New Delhi, India: Wiley- Blackwell Publishing House; 2011.
15. Shrestha KL, Pant ND, Bhandari R, Khatri S. et al. Re-emergence of the susceptibility of the Salmonella spp. isolated from blood samples to conventional first line antibiotics. Antimicrob Resist Infect Control. 2016;5:22. https://www.ncbi.nlm.nih.gov/pubmed/27231547. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4881163. https://doi.org/10.1186/s13756-016-0121-8.
16. Ugboko H, De N. Mechanisms of Antibiotic resistance in Salmonella typhi. 2014. Int J Curr Microbiol App Sci. 2014;3(12):461–76. https://www.ijcmas.com/vol-3-12/Harriet%20Ugboko%20and%20Nandita%20De.pdf.
17. Phan MD, Kidgell C, Nair S, et al. Variation in Salmonella enterica serovar Typhi IncHI1 plasmids during the global spread of resistant typhoid fever. Antimicrob Agents Chemother. 2009;53(2):716-27. https://www.ncbi.nlm.nih.gov/pubmed/19015365. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2630618. https://doi.org/10.1128/AAC.00645-08.
18. Holt KE, Phan MD, Baker S, et al. Emergence of a globally dominant IncHI1 plasmid type associated with multiple drug resistant typhoid. PLoS Negl Trop Dis. 2011;5(7):e1245. https://www.ncbi.nlm.nih.gov/pubmed/21811646. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3139670. https://doi.org/10.1371/journal.pntd.0001245.
19. Kariuki S, Revathi G, Kiiru J, et al. Typhoid in Kenya is associated with a dominant multidrug-resistant Salmonella enterica serovar Typhi haplotype that is also widespread in Southeast Asia. J Clin Microbiol. 2010;48(6):2171–6. https://www.ncbi.nlm.nih.gov/pubmed/20392916. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2884483. https://doi.org/10.1128/JCM.01983-09.
20.Ochiai RL, Acosta CJ, DanovaroHolliday MC, et al. A study of typhoid fever in five Asian countries: disease burden and implications for controls. 2008;86(4):260–8. https://www.ncbi.nlm.nih.gov/pubmed/18438514. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2647431. https://doi.org/10.2471/blt.06.039818.
21. Crump JA, Heyderman RS. A perspective on invasive Salmonella disease in Africa. 2015.Clin Infect Dis. 2015.61(Suppl 4):S235–40. https://www.ncbi.nlm.nih.gov/pubmed/26449937. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4596931. https://doi.org/10.1093/cid/civ709.
22. Uche IV, MacLennan CA, Saul A. A systematic review of the incidence, risk factors and case fatality rates of invasive nontyphoidal Salmonella (iNTS) disease in Africa (1966 to 2014). PLoS Negl Trop Dis. 2017:11:e0005118. https://doi.org/10.1371/journal.pntd.0005118.
23. Freeman R, Dabrera G, Lane C, et al. Association between use of proton pump inhibitors and nontyphoidal salmonellosis identified following investigation into an outbreak of Salmonella mikawasima in the UK, 2013. Epidemiol Infect. 2016;144(5):968–75. https://www.ncbi.nlm.nih.gov/pubmed/26424497. https://doi.org/10.1017/S0950268815002332.
24. Mahon BE, Fields PI. Invasive infections with nontyphoidal Salmonella in Sub-Saharan Africa. Microbiol Spectr. 2016;4(3). https://www.ncbi.nlm.nih.gov/pubmed/27337467. https://doi.org/10.1128/microbiolspec.EI10-0015-2016.
25. Britto CD, Wong VK, Dougan G, Pollard AJ. A systematic review of antimicrobial resistance in Salmonella enterica serovar Typhi, the etiological agent of typhoid. PLoS Negl Trop Dis. 2018;12(10):e0006779. https://www.ncbi.nlm.nih.gov/pubmed/30307935. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6198998. https://doi.org/10.1371/journal.pntd.0006779.
26. Acharya D, Malla S, Adhikari N, Dumre SP. Current fluoroquinolone susceptibility criteria for Salmonella needs re-evaluation. Kathmandu Univ Med J (KUMJ). 2012;37(1):24–9. https://www.ncbi.nlm.nih.gov/pubmed/22971857. https://doi.org/10.3126/kumj.v10i1.6909.
27. Whistler T, Sapchookul P, McCormick D, et al. Epidemiology and antimicrobial resistance of invasive non-typhoidal Salmonellosis in rural Thailand from 2006-2014. 2018;12(8): e0006718. https://www.ncbi.nlm.nih.gov/pubmed/30080897. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6095622. https://doi.org/10.1371/journal.pntd.0006718.
28. Punpanich W, Netsawang S, Thippated C. Invasive salmonellosis in urban Thai children: a ten-year review. Pediatr Infect Dis J. 2012;31(8):e105–10. https://www.ncbi.nlm.nih.gov/pubmed/22531240. https://doi.org/10.1097/INF.0b013e31825894b0.
29. Reddy EA, Shaw AV, Crump JA. Community-acquired bloodstream infections in Africa: a systematic review and meta-analysis. Lancet Infect Dis. 2010;10(6):417–32. https://www.ncbi.nlm.nih.gov/pubmed/20510282. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3168734. https://doi.org/10.1016/S1473-3099(10)70072-4.