Antibiotic resistome of Salmonella typhi: molecular determinants for the emergence of drug resistance

Abstract

Resistome is a cluster of microbial genes encoding proteins with necessary functions to resist the action of antibiotics. Resistome governs essential and separate biological functions to develop resistance against antibiotics. The widespread clinical and nonclinical uses of antibiotics over the years have combined to select antibiotic-resistant determinants and develop resistome in bacteria. At present, the emergence of drug resistance because of resistome is a significant problem faced by clinicians for the treatment of Salmonella infection. Antibiotic resistome is a dynamic and ever-expanding component in Salmonella. The foundation of resistome in Salmonella is laid long before; therefore, the antibiotic resistome of Salmonella is reviewed, discussed, and summarized. We have searched the literature using PubMed, MEDLINE, and Google Scholar with related key terms (resistome, Salmonella, antibiotics, drug resistance) and prepared this review. In this review, we summarize the status of resistance against antibiotics in S. typhi, highlight the seminal work in the resistome of S. typhi and the genes involved in the antibiotic resistance, and discuss the various methods to identify S. typhi resistome for the proactive identification of this infection and quick diagnosis of the disease.

Keywords

S. typhi / antibiotic resistance / mechanism / resistome / identification methods

References

[1] Abakpa GO, Umoh VJ, Ameh JB, Yakubu SE, Kwaga JKP, Kamaruzaman S. Diversity and antimicrobial resistance of Salmonella enterica isolated from fresh produce and environmental samples. Environ Nanotechnol Monit Manag 2015; 3: 38–46

[2] Wei LS, Wee W, Siong JYF, Syamsumir DF. Characterization of anticancer, antimicrobial, antioxidant properties and chemical compositions of Peperomia pellucida leaf extract. Acta Med Iran 2011; 49(10): 670–674

[3] Mahapatra A, Patro S, Choudhury S, Padhee A, Das R. Emerging enteric fever due to switching biotype of Salmonella (paratyphi A) in Eastern Odisha. Indian J Pathol Microbiol 2016; 59(3): 327–329

[4] Crump JA, Mintz ED. Global trends in typhoid and paratyphoid fever. Clin Infect Dis 2010; 15; 50(2): 241–246

[5] Tatavarthy A, Luna VA, Amuso PT. How multidrug resistance in typhoid fever affects treatment options. Ann N Y Acad Sci 2014; 1323(1): 76–90

[6] WHO. Vaccine-preventable diseases surveillance standards: typhoid and other invasive salmonellosis. WHO 2019; 1–13.accessed January 11, 2020)

[7] Chitnis S, Chitnis V, Hemvani N, Chitnis DS. Ciprofloxacin therapy for typhoid fever needs reconsideration. J Infect Chemother 2006; 12(6): 402–404

[8] Chiou CS, Lauderdale TL, Phung DC, Watanabe H, Kuo JC, Wang PJ, Liu YY, Liang SY, Chen PC. Antimicrobial resistance in Salmonella enterica serovar typhi isolates from Bangladesh, Indonesia, Chinese Taiwan, and Vietnam. Antimicrob Agents Chemother 2014; 58(11): 6501–6507

[9] Rai S, Jain S, Prasad KN, Ghoshal U, Dhole TN. Rationale of azithromycin prescribing practices for enteric fever in India. Indian J Med Microbiol 2012; 30(1): 30–33

[10] Hassing RJ, Goessens WH, van Pelt W, Mevius DJ, Stricker BH, Molhoek N, Verbon A, van Genderen PJ. Salmonella subtypes with increased MICs for azithromycin in travelers returned to The Netherlands. Emerg Infect Dis 2014; 20(4): 705–708

[11] Das S, Samajpati S, Ray U, Roy I, Dutta S. Antimicrobial resistance and molecular subtypes of Salmonella enterica serovar typhi isolates from Kolkata, India over a 15 years period 1998–2012. Int J Med Microbiol 2017; 307(1): 28–36

[12] El-Tayeb MA, Ibrahim ASS, Al-Salamah AA, Almaary KS, Elbadawi YB. Prevalence, serotyping and antimicrobials resistance mechanism of Salmonella enterica isolated from clinical and environmental samples in Saudi Arabia. Braz J Microbiol 2017; 48(3): 499–508

[13] Sood S, Kapil A, Dash N, Das BK, Goel V, Seth P. Paratyphoid fever in India: an emerging problem. Emerg Infect Dis 1999; 5(3): 483–484

[14] Bhattacharya SS, Dash U. A sudden rise in occurrence of Salmonella paratyphi a infection in Rourkela, Orissa. Indian J Med Microbiol 2007; 25(1): 78–79

[15] Veeraraghavan B, Anandan S, Muthuirulandi Sethuvel DP, Puratchiveeran N, Walia K, Devanga Ragupathi NK. Molecular characterization of intermediate susceptible typhoidal Salmonella to ciprofloxacin, and its impact. Mol Diagn Ther 2016; 20(3): 213–219

[16] Frye JG, Jackson CR. Genetic mechanisms of antimicrobial resistance identified in Salmonella enterica, Escherichia coli, and Enteroccocus spp. isolated from U.S. food animals. Front Microbiol 2013; 4(4): 135

[17] Bertolini A, Castelli M, Genedani S, Garuti M. Trimethoprim enhances the antibacterial activity of nalidixic and oxolinic acids and delays the emergence of resistance. Experientia 1980; 36(2): 243–244

[18] Datta N, Richards H, Datta C. Salmonella typhi in vivo acquires resistance to both chloramphenicol and co-trimoxazole. Lancet 1981; 317(8231): 1181–1183

[19] Mandal S, Mandal MD, Pal NK. Synergism of ciprofloxacin and trimethoprim against Salmonella enterica serovar typhi isolates showing reduced susceptibility to ciprofloxacin. Chemotherapy 2004; 50(3): 152–154

[20] Amira OC, Okubadejo NU. Frequency of complementary and alternative medicine utilization in hypertensive patients attending an urban tertiary care centre in Nigeria. BMC Complement Altern Med 2007; 7: 30

[21] Lewis WH, Elvin-Lewis MP. Medicinal plants as sources of new therapeutics. Ann Mo Bot Gard 1995; 82(1): 16–24

[22] Guilhelmelli F, Vilela N, Albuquerque P, Derengowski LS, Silva-Pereira I, Kyaw CM. Antibiotic development challenges: the various mechanisms of action of antimicrobial peptides and of bacterial resistance. Front Microbiol 2013; 4: 353

[23] Zaki SA, Karande S. Multidrug-resistant typhoid fever: a review. J Infect Dev Ctries 2011; 5(5): 324–337

[24] Ugboko H, De N. Mechanisms of antibiotic resistance in Salmonella typhi. Int J Curr Microbiol Appl Sci 2014; 3: 461–476

[25] Nishino K, Nikaido E, Yamaguchi A. Regulation and physiological function of multidrug efflux pumps in Escherichia coli and Salmonella. Biochim Biophys Acta 2009; 1794(5): 834–843

[26] Shaheen A, Ismat F, Iqbal M, Haque A, De Zorzi R, Mirza O, Walz T, Rahman M. Characterization of putative multidrug resistance transporters of the major facilitator-superfamily expressed in Salmonella typhi. J Infect Chemother 2015; 21(5): 357–362

[27] van Duijkeren E, Schink AK, Roberts MC, Wang Y, Schwarz S. Mechanisms of bacterial resistance to antimicrobial agents. Microbiol Spectr 2018; 6(1): 10

[28] Sharma V, Dahiya S, Jangra P, Das BK, Kumar R, Sood S, Kapil A. Study of the role of efflux pump in ciprofloxacin resistance in Salmonella enterica serotype typhi. Indian J Med Microbiol 2013; 31(4): 374–378

[29] Miller SI. Antibiotic resistance and regulation of the Gram-negative bacterial outer membrane barrier by host innate immune molecules. MBio 2016; 7(5): e01541–e16

[30] Mascher T. Signaling diversity and evolution of extracytoplasmic function (ECF) s factors. Curr Opin Microbiol 2013; 16(2): 148–155

[31] Mutalik VK, Nonaka G, Ades SE, Rhodius VA, Gross CA. Promoter strength properties of the complete sigma E regulon of Escherichia coli and Salmonella enterica. J Bacteriol 2009; 191(23): 7279–7287

[32] Xie X, Zhang H, Zheng Y, Li A, Wang M, Zhou H, Zhu X, Schneider Z, Chen L, Kreiswirth BN, Du H. RpoE is a putative antibiotic resistance regulator of Salmonella enteric serovar typhi. Curr Microbiol 2016; 72(4): 457–464

[33] Du H, Wang M, Luo Z, Ni B, Wang F, Meng Y, Xu S, Huang X. Coregulation of gene expression by sigma factors RpoE and RpoS in Salmonella enterica serovar typhi during hyperosmotic stress. Curr Microbiol 2011; 62(5): 1483–1489

[34] Seaver LC, Imlay JA. Hydrogen peroxide fluxes and compartmentalization inside growing Escherichia coli. J Bacteriol 2001; 183(24): 7182–7189

[35] Hébrard M, Viala JPM, Méresse S, Barras F, Aussel L. Redundant hydrogen peroxide scavengers contribute to Salmonella virulence and oxidative stress resistance. J Bacteriol 2009; 191(14): 4605–4614

[36] Hillion M, Antelmann H. Thiol-based redox switches in prokaryotes. Biol Chem 2015; 396(5): 415–444

[37] Wong VK, Baker S, Pickard DJ, Parkhill J, Page AJ, Feasey NA, Kingsley RA, Thomson NR, Keane JA, Weill FX, Edwards DJ, Hawkey J, Harris SR, Mather AE, Cain AK, Hadfield J, Hart PJ, Thieu NT, Klemm EJ, Glinos DA, Breiman RF, Watson CH, Kariuki S, Gordon MA, Heyderman RS, Okoro C, Jacobs J, Lunguya O, Edmunds WJ, Msefula C, Chabalgoity JA, Kama M, Jenkins K, Dutta S, Marks F, Campos J, Thompson C, Obaro S, MacLennan CA, Dolecek C, Keddy KH, Smith AM, Parry CM, Karkey A, Mulholland EK, Campbell JI, Dongol S, Basnyat B, Dufour M, Bandaranayake D, Naseri TT, Singh SP, Hatta M, Newton P, Onsare RS, Isaia L, Dance D, Davong V, Thwaites G, Wijedoru L, Crump JA, De Pinna E, Nair S, Nilles EJ, Thanh DP, Turner P, Soeng S, Valcanis M, Powling J, Dimovski K, Hogg G, Farrar J, Holt KE, Dougan G. Phylogeographical analysis of the dominant multidrug-resistant H58 clade of Salmonella typhi identifies inter- and intracontinental transmission events. Nat Genet 2015; 47(6): 632–639

[38] Pai H, Byeon JH, Yu S, Lee BK, Kim S. Salmonella enterica serovar typhi strains isolated in Korea containing a multidrug resistance class 1 integron. Antimicrob Agents Chemother 2003; 47(6): 2006–2008

[39] Pfeifer Y, Matten J, Rabsch W. Salmonella enterica serovar typhi with CTX-M β-lactamase, Germany. Emerg Infect Dis 2009; 15(9): 1533–1535

[40] Sy SK, Zhuang L, Derendorf H. Pharmacokinetics and pharmacodynamics in antibiotic dose optimization. Expert Opin Drug Metab Toxicol 2016; 12(1): 93–114

[41] Asín-Prieto E, Rodríguez-Gascón A, Isla A. Applications of the pharmacokinetic/pharmacodynamic (PK/PD) analysis of antimicrobial agents. J Infect Chemother 2015; 21(5): 319–329

[42] Ambrose PG, Bhavnani SM, Rubino CM, Louie A, Gumbo T, Forrest A, Drusano GL. Pharmacokinetics-pharmacodynamics of antimicrobial therapy: it’s not just for mice anymore. Clin Infect Dis 2007; 44(1): 79–86

[43] Li J, Hao H, Cheng G, Wang X, Ahmed S, Shabbir MAB, Liu Z, Dai M, Yuan Z. The effects of different enrofloxacin dosages on clinical efficacy and resistance development in chickens experimentally infected with Salmonella typhimurium. Sci Rep 2017; 7(1): 11676

[44] Lee SJ, Awji EG, Park NH, Park SC. Using in vitro dynamic models to evaluate fluoroquinolone activity against emergence of resistant Salmonella enterica serovar typhimurium. Antimicrob Agents Chemother 2017; 61(2): e01756-16

[45] Toutain PL, del Castillo JR, Bousquet-Mélou A. The pharmacokinetic-pharmacodynamic approach to a rational dosage regimen for antibiotics. Res Vet Sci 2002; 73(2): 105–114

[46] Song M, Husain M, Jones-Carson J, Liu L, Henard CA, Vázquez-Torres A. Low-molecular-weight thiol-dependent antioxidant and antinitrosative defences in Salmonella pathogenesis. Mol Microbiol 2013; 87(3): 609–622

[47] Song M, Kim JS, Liu L, Husain M, Vázquez-Torres A. Antioxidant defense by thioredoxin can occur independently of canonical thiol-disulfide oxidoreductase enzymatic activity. Cell Rep 2016; 14(12): 2901–2911

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