1887

Abstract

Fluoroquinolone (FQ)-resistant Salmonella spp. were listed by the WHO in 2017 as priority pathogens for which new antibiotics were urgently needed. The overall global burden of Salmonella infections is high, but differs per region. Whereas typhoid fever is most prevalent in South and South-East Asia, non-typhoidal salmonellosis is prevalent across the globe and associated with a mild gastroenteritis. By contrast, invasive non-typhoidal Salmonella cause bloodstream infections associated with high mortality, particularly in sub-Saharan Africa. Most Salmonella strains from clinical sources are resistant to first-line antibiotics, with FQs now being the antibiotic of choice for treatment of invasive Salmonella infections. However, FQ resistance is increasingly being reported in Salmonella, and multiple molecular mechanisms are already described. Whole-genome sequencing (WGS) is becoming more frequently used to analyse bacterial genomes for antibiotic-resistance markers, and to understand the phylogeny of bacteria in relation to their antibiotic-resistance profiles. This mini-review provides an overview of FQ resistance in Salmonella, guided by WGS studies that demonstrate that WGS is a valuable tool for global surveillance.

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2018-07-05
2024-11-12
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References

  1. Parry CM, Hien TT, Dougan G, White NJ, Farrar JJ et al. Typhoid fever. N Engl J Med 2002; 347:1770–1782 [View Article][PubMed]
    [Google Scholar]
  2. Parry CM, Basnyat B, Crump JA. The management of antimicrobial-resistant enteric fever. Expert Rev Anti Infect Ther 2013; 11:1259–1261 [View Article][PubMed]
    [Google Scholar]
  3. Crump JA, Luby SP, Mintz ED. The global burden of typhoid fever. Bull World Health Organ 2004; 82:346–353[PubMed]
    [Google Scholar]
  4. Buckle GC, Walker CL, Black RE. Typhoid fever and paratyphoid fever: systematic review to estimate global morbidity and mortality for 2010. J Glob Health 2012; 2:10401 [View Article][PubMed]
    [Google Scholar]
  5. Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M et al. The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 2010; 50:882–889 [View Article][PubMed]
    [Google Scholar]
  6. Ao TT, Feasey NA, Gordon MA, Keddy KH, Angulo FJ et al. Global burden of invasive nontyphoidal Salmonella disease, 2010. Emerg Infect Dis 2015; 21:941–949 [View Article][PubMed]
    [Google Scholar]
  7. Gordon MA. Salmonella infections in immunocompromised adults. J Infect 2008; 56:413–422 [View Article][PubMed]
    [Google Scholar]
  8. Feasey NA, Dougan G, Kingsley RA, Heyderman RS, Gordon MA. Invasive non-typhoidal Salmonella disease: an emerging and neglected tropical disease in Africa. Lancet 2012; 379:2489–2499 [View Article][PubMed]
    [Google Scholar]
  9. Kariuki S, Gordon MA, Feasey N, Parry CM. Antimicrobial resistance and management of invasive Salmonella disease. Vaccine 2015; 33:C21–C29 [View Article][PubMed]
    [Google Scholar]
  10. Feasey NA, Hadfield J, Keddy KH, Dallman TJ, Jacobs J et al. Distinct Salmonella Enteritidis lineages associated with enterocolitis in high-income settings and invasive disease in low-income settings. Nat Genet 2016; 48:1211–1217 [View Article][PubMed]
    [Google Scholar]
  11. Carden SE, Walker GT, Honeycutt J, Lugo K, Pham T et al. Pseudogenization of the secreted effector gene ssei confers rapid systemic dissemination of S. Typhimurium ST313 within migratory dendritic cells. Cell Host Microbe 2017; 21:182–194 [View Article][PubMed]
    [Google Scholar]
  12. Kingsley RA, Msefula CL, Thomson NR, Kariuki S, Holt KE et al. Epidemic multiple drug resistant Salmonella Typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype. Genome Res 2009; 19:2279–2287 [View Article][PubMed]
    [Google Scholar]
  13. Okoro CK, Kingsley RA, Connor TR, Harris SR, Parry CM et al. Intracontinental spread of human invasive Salmonella Typhimurium pathovariants in sub-Saharan Africa. Nat Genet 2012; 44:1215–1221 [View Article][PubMed]
    [Google Scholar]
  14. Crump JA, Sjölund-Karlsson M, Gordon MA, Parry CM. Epidemiology, clinical presentation, laboratory diagnosis, antimicrobial resistance, and antimicrobial management of invasive Salmonella infections. Clin Microbiol Rev 2015; 28:901–937 [View Article][PubMed]
    [Google Scholar]
  15. Shane AL, Mody RK, Crump JA, Tarr PI, Steiner TS et al. Infectious Diseases Society of America clinical practice guidelines for the diagnosis and management of infectious diarrhea. Clin Infect Dis 2017; 65:e45e80
    [Google Scholar]
  16. Wain J, Hendriksen RS, Mikoleit ML, Keddy KH, Ochiai RL. Typhoid fever. Lancet 2015; 385:1136–1145 [View Article][PubMed]
    [Google Scholar]
  17. Crump JA, Mintz ED. Global trends in typhoid and paratyphoid fever. Clin Infect Dis 2010; 50:241–246 [View Article][PubMed]
    [Google Scholar]
  18. NARMS National Antimicrobial Resistance Monitoring System: Enteric Bacteria – Human Isolates Final Report Atlanta, GA: Centers for Disease Control and Prevention; 2013
    [Google Scholar]
  19. Fang FC. Fluoroquinolone resistance in Salmonella and the utility of pefloxacin disk diffusion. J Clin Microbiol 2015; 53:3401–3404 [View Article][PubMed]
    [Google Scholar]
  20. Tacconelli E, Carrara E, Savoldi A, Harbarth S, Mendelson M et al. Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis. Lancet Infect Dis 2018; 18:318–327 [View Article][PubMed]
    [Google Scholar]
  21. Correia S, Poeta P, Hébraud M, Capelo JL, Igrejas G. Mechanisms of quinolone action and resistance: where do we stand?. J Med Microbiol 2017; 66:551–559 [View Article][PubMed]
    [Google Scholar]
  22. Redgrave LS, Sutton SB, Webber MA, Piddock LJ. Fluoroquinolone resistance: mechanisms, impact on bacteria, and role in evolutionary success. Trends Microbiol 2014; 22:438–445 [View Article][PubMed]
    [Google Scholar]
  23. Aldred KJ, Kerns RJ, Osheroff N. Mechanism of quinolone action and resistance. Biochemistry 2014; 53:1565–1574 [View Article][PubMed]
    [Google Scholar]
  24. Drlica K, Malik M, Kerns RJ, Zhao X. Quinolone-mediated bacterial death. Antimicrob Agents Chemother 2008; 52:385–392 [View Article][PubMed]
    [Google Scholar]
  25. Hooper DC, Jacoby GA. Topoisomerase inhibitors: fluoroquinolone mechanisms of action and resistance. Cold Spring Harb Perspect Med 2016; 6:a025320 [View Article][PubMed]
    [Google Scholar]
  26. Wolfson JS, Hooper DC. The fluoroquinolones: structures, mechanisms of action and resistance, and spectra of activity in vitro . Antimicrob Agents Chemother 1985; 28:581–586 [View Article][PubMed]
    [Google Scholar]
  27. Andriole VT. The quinolones: past, present, and future. Clin Infect Dis 2005; 41:S113–S119 [View Article][PubMed]
    [Google Scholar]
  28. Hopkins KL, Davies RH, Threlfall EJ. Mechanisms of quinolone resistance in Escherichia coli and Salmonella: recent developments. Int J Antimicrob Agents 2005; 25:358–373 [View Article][PubMed]
    [Google Scholar]
  29. Madurga S, Sánchez-Céspedes J, Belda I, Vila J, Giralt E. Mechanism of binding of fluoroquinolones to the quinolone resistance-determining region of DNA gyrase: towards an understanding of the molecular basis of quinolone resistance. Chembiochem 2008; 9:2081–2086 [View Article][PubMed]
    [Google Scholar]
  30. Tran JH, Jacoby GA, Hooper DC. Interaction of the plasmid-encoded quinolone resistance protein Qnr with Escherichia coli DNA gyrase. Antimicrob Agents Chemother 2005; 49:118–125 [View Article][PubMed]
    [Google Scholar]
  31. Tran JH, Jacoby GA, Hooper DC. Interaction of the plasmid-encoded quinolone resistance protein QnrA with Escherichia coli topoisomerase IV. Antimicrob Agents Chemother 2005; 49:3050–3052 [View Article][PubMed]
    [Google Scholar]
  32. Robicsek A, Jacoby GA, Hooper DC. The worldwide emergence of plasmid-mediated quinolone resistance. Lancet Infect Dis 2006; 6:629–640 [View Article][PubMed]
    [Google Scholar]
  33. Clinical and Laboratory Standards Institute Performance Standards for Antimicrobial Susceptibility Testing, 28th ed. CLSI supplement M100 Wayne, PA: Clinical and Laboratory Standards Institute; 2018
    [Google Scholar]
  34. Parry CM, Threlfall EJ. Antimicrobial resistance in typhoidal and nontyphoidal Salmonellae . Curr Opin Infect Dis 2008; 21:531–538 [View Article]
    [Google Scholar]
  35. Humphries RM, Fang FC, Aarestrup FM, Hindler JA. In vitro susceptibility testing of fluoroquinolone activity against Salmonella: recent changes to CLSI standards. Clin Infect Dis 2012; 55:1107–1113 [View Article][PubMed]
    [Google Scholar]
  36. Wong VK, Baker S, Pickard DJ, Parkhill J, Page AJ et al. Phylogeographical analysis of the dominant multidrug-resistant H58 clade of Salmonella Typhi identifies inter- and intracontinental transmission events. Nat Genet 2015; 47:632–639 [View Article][PubMed]
    [Google Scholar]
  37. Pham Thanh D, Karkey A, Dongol S, Ho Thi N, Thompson CN et al. A novel ciprofloxacin-resistant subclade of H58 Salmonella Typhi is associated with fluoroquinolone treatment failure. Elife 2016; 5:1–13 [View Article][PubMed]
    [Google Scholar]
  38. Pham Thanh D, Thompson CN, Rabaa MA, Sona S, Sopheary S et al. The molecular and spatial epidemiology of typhoid fever in rural Cambodia. PLoS Negl Trop Dis 2016; 10:e0004785 [View Article][PubMed]
    [Google Scholar]
  39. Kuijpers LMF, Phe T, Veng CH, Lim K, Ieng S et al. The clinical and microbiological characteristics of enteric fever in Cambodia, 2008-2015. PLoS Negl Trop Dis 2017; 11:e0005964 [View Article][PubMed]
    [Google Scholar]
  40. Matono T, Morita M, Yahara K, Lee KI, Izumiya H et al. Emergence of resistance mutations in Salmonella enterica serovar Typhi against fluoroquinolones. Open Forum Infect Dis 2017; 4:1–17 [View Article][PubMed]
    [Google Scholar]
  41. Baker S, Duy PT, Nga TV, Dung TT, Phat VV et al. Fitness benefits in fluoroquinolone-resistant Salmonella Typhi in the absence of antimicrobial pressure. Elife 2013; 2:e01229 [View Article][PubMed]
    [Google Scholar]
  42. Hendriksen RS, Leekitcharoenphon P, Lukjancenko O, Lukwesa-Musyani C, Tambatamba B et al. Genomic signature of multidrug-resistant Salmonella enterica serovar Typhi isolates related to a massive outbreak in Zambia between 2010 and 2012. J Clin Microbiol 2015; 53:262–272 [View Article][PubMed]
    [Google Scholar]
  43. International Typhoid Consortium Wong VK, Holt KE, Okoro C, Baker S et al. Molecular surveillance identifies multiple transmissions of typhoid in West Africa. PLoS Negl Trop Dis 2016; 10:e0004781 [View Article][PubMed]
    [Google Scholar]
  44. Tadesse G, Tessema TS, Beyene G, Aseffa A. Molecular epidemiology of fluoroquinolone resistant Salmonella in Africa: a systematic review and meta-analysis. PLoS One 2018; 13:e0192575 [View Article][PubMed]
    [Google Scholar]
  45. Dougan G. Typhoid in Africa and vaccine deployment. Lancet Glob Health 2017; 5:e236e237 [View Article][PubMed]
    [Google Scholar]
  46. Phoba MF, Barbé B, Lunguya O, Masendu L, Lulengwa D et al. Salmonella enterica serovar Typhi producing CTX-M-15 extended spectrum β-Lactamase in the Democratic Republic of the Congo. Clin Infect Dis 2017; 65:1229–1231 [View Article][PubMed]
    [Google Scholar]
  47. Rodrigues C, Kapil A, Sharma A, Devanga Ragupathi NK, Inbanathan FY et al. Whole-genome shotgun sequencing of cephalosporin-resistant Salmonella enterica serovar Typhi. Genome Announc 2017; 5:e01639-16 [View Article][PubMed]
    [Google Scholar]
  48. Chiou CS, Lauderdale TL, Phung DC, Watanabe H, Kuo JC et al. Antimicrobial resistance in Salmonella enterica serovar Typhi isolates from Bangladesh, Indonesia, Taiwan, and Vietnam. Antimicrob Agents Chemother 2014; 58:6501–6507 [View Article][PubMed]
    [Google Scholar]
  49. Klemm EJ, Shakoor S, Page AJ, Qamar FN, Judge K et al. Emergence of an extensively drug-resistant Salmonella enterica serovar Typhi clone harboring a promiscuous plasmid encoding resistance to fluoroquinolones and third-generation cephalosporins. MBio 2018; 9:e00105-18 [View Article][PubMed]
    [Google Scholar]
  50. Robicsek A, Sahm DF, Strahilevitz J, Jacoby GA, Hooper DC et al. Broader distribution of plasmid-mediated quinolone resistance in the United States. Antimicrob Agents Chemother 2005; 49:3001–3003 [View Article][PubMed]
    [Google Scholar]
  51. Poirel L, Cattoir V, Nordmann P. Is plasmid-mediated quinolone resistance a clinically significant problem?. Clin Microbiol Infect 2008; 14:295–297 [View Article][PubMed]
    [Google Scholar]
  52. Thompson CN, Karkey A, Dongol S, Arjyal A, Wolbers M et al. Treatment response in enteric fever in an era of increasing antimicrobial resistance: an individual patient data analysis of 2092 participants enrolled into 4 randomized, controlled trials in Nepal. Clin Infect Dis 2017; 64:1522–1531 [View Article][PubMed]
    [Google Scholar]
  53. Joshi S, Amarnath SK. Fluoroquinolone resistance in Salmonella typhi and S. paratyphi A in Bangalore, India. Trans R Soc Trop Med Hyg 2007; 101:308–310 [View Article][PubMed]
    [Google Scholar]
  54. Dutta S, Das S, Mitra U, Jain P, Roy I et al. Antimicrobial resistance, virulence profiles and molecular subtypes of Salmonella enterica serovars Typhi and Paratyphi A blood isolates from Kolkata, India during 2009–2013. PLoS One 2014; 9:e101347 [View Article][PubMed]
    [Google Scholar]
  55. Zellweger RM, Basnyat B, Shrestha P, Prajapati KG, Dongol S et al. A 23-year retrospective investigation of Salmonella Typhi and Salmonella Paratyphi isolated in a tertiary Kathmandu hospital. PLoS Negl Trop Dis 2017; 11:e0006051 [View Article][PubMed]
    [Google Scholar]
  56. Michael GB, Schwarz S. Antimicrobial resistance in zoonotic nontyphoidal Salmonella: an alarming trend?. Clin Microbiol Infect 2016; 22:968–974 [View Article][PubMed]
    [Google Scholar]
  57. Veldman K, Cavaco LM, Mevius D, Battisti A, Franco A et al. International collaborative study on the occurrence of plasmid-mediated quinolone resistance in Salmonella enterica and Escherichia coli isolated from animals, humans, food and the environment in 13 European countries. J Antimicrob Chemother 2011; 66:1278–1286 [View Article][PubMed]
    [Google Scholar]
  58. Tran-Dien A, Le Hello S, Bouchier C, Weill FX. Early transmissible ampicillin resistance in zoonotic Salmonella enterica serotype Typhimurium in the late 1950s: a retrospective, whole-genome sequencing study. Lancet Infect Dis 2018; 18:207–214 [View Article][PubMed]
    [Google Scholar]
  59. van Puyvelde S, Deborggraeve S, Jacobs J. Why the antibiotic resistance crisis requires a one health approach. Lancet Infect Dis 2018; 18:1–2 [View Article][PubMed]
    [Google Scholar]
  60. Pikkemaat M, Yassin H, van der Fels-Klerx H, Berendsen BJA. Antibiotic Residues and Resistance in the Environment Wageningen: RIKILT Wageningen UR; 2016
    [Google Scholar]
  61. Roth N, Mayrhofer S, Gierus M, Weingut C, Schwarz C et al. Effect of an organic acids based feed additive and enrofloxacin on the prevalence of antibiotic-resistant E. coli in cecum of broilers. Poult Sci 2017; 96:4053–4060 [View Article][PubMed]
    [Google Scholar]
  62. Collignon PC, Conly JM, Andremont A, McEwen SA, Aidara-Kane A et al. World Health Organization ranking of antimicrobials according to their importance in human medicine: a critical step for developing risk management strategies to control antimicrobial resistance from food animal production. Clin Infect Dis 2016; 63:1087–1093 [View Article][PubMed]
    [Google Scholar]
  63. Cheng AC, Turnidge J, Collignon P, Looke D, Barton M et al. Control of fluoroquinolone resistance through successful regulation, Australia. Emerg Infect Dis 2012; 18:1453–1460 [View Article][PubMed]
    [Google Scholar]
  64. Fonteneau L, Jourdan da Silva N, Fabre L, Ashton P, Torpdahl M et al. Multinational outbreak of travel-related Salmonella Chester infections in Europe, summers 2014 and 2015. Euro Surveill 2017; 22:1–11 [View Article][PubMed]
    [Google Scholar]
  65. Toro M, Retamal P, Ayers S, Barreto M, Allard M et al. Whole-genome sequencing analysis of Salmonella enterica serovar enteritidis isolates in Chile provides insights into possible transmission between gulls, poultry, and humans. Appl Environ Microbiol 2016; 82:6223–6232 [View Article][PubMed]
    [Google Scholar]
  66. Elnekave E, Hong S, Mather AE, Boxrud D, Taylor AJ et al. Salmonella enterica serotype 4,[5],12:i:- in swine in the United States Midwest: an emerging multidrug resistant clone. Clin Infect Dis 2018; 66:877–885 [View Article][PubMed]
    [Google Scholar]
  67. Mather AE, Reid SWJ, Maskell DJ, Parkhill J, Fookes MC et al. Distinguishable epidemics within different hosts of the multidrug resistant zoonotic pathogen Salmonella Typhimurium. Science 2013; 341:1514–1517
    [Google Scholar]
  68. Carroll LM, Wiedmann M, den Bakker H, Siler J, Warchocki S et al. Whole-genome sequencing of drug-resistant Salmonella enterica isolates from dairy cattle and humans in New York and Washington States reveals source and geographic associations. Appl Environ Microbiol 2017; 83:e00140-17 [View Article][PubMed]
    [Google Scholar]
  69. McDermott PF, Tyson GH, Kabera C, Chen Y, Li C et al. Whole-genome sequencing for detecting antimicrobial resistance in nontyphoidal Salmonella . Antimicrob Agents Chemother 2016; 60:5515–5520 [View Article][PubMed]
    [Google Scholar]
  70. Lunguya O, Lejon V, Phoba MF, Bertrand S, Vanhoof R et al. Antimicrobial resistance in invasive non-typhoid Salmonella from the Democratic Republic of the Congo: emergence of decreased fluoroquinolone susceptibility and extended-spectrum beta lactamases. PLoS Negl Trop Dis 2013; 7:e2103 [View Article][PubMed]
    [Google Scholar]
  71. Marks F, von Kalckreuth V, Aaby P, Adu-Sarkodie Y, El Tayeb MA et al. Incidence of invasive salmonella disease in sub-Saharan Africa: a multicentre population-based surveillance study. Lancet Glob Health 2017; 5:e310e323 [View Article][PubMed]
    [Google Scholar]
  72. Kariuki S, Onsare RS. Epidemiology and genomics of invasive nontyphoidal Salmonella infections in Kenya. Clin Infect Dis 2015; 61:S317–S324 [View Article][PubMed]
    [Google Scholar]
  73. Harrois D, Breurec S, Seck A, Delauné A, Le Hello S et al. Prevalence and characterization of extended-spectrum β-lactamase-producing clinical Salmonella enterica isolates in Dakar, Senegal, from 1999 to 2009. Clin Microbiol Infect 2014; 20:O109–O116 [View Article][PubMed]
    [Google Scholar]
  74. Fashae K, Ogunsola F, Aarestrup FM, Hendriksen RS. Antimicrobial susceptibility and serovars of Salmonella from chickens and humans in Ibadan, Nigeria. J Infect Dev Ctries 2010; 4:484–494[PubMed]
    [Google Scholar]
  75. Eguale T, Birungi J, Asrat D, Njahira MN, Njuguna J et al. Genetic markers associated with resistance to beta-lactam and quinolone antimicrobials in non-typhoidal Salmonella isolates from humans and animals in central Ethiopia. Antimicrob Resist Infect Control 2017; 6:1–10 [View Article][PubMed]
    [Google Scholar]
  76. Beyene G, Nair S, Asrat D, Mengistu Y, Engers H et al. Multidrug resistant Salmonella Concord is a major cause of salmonellosis in children in Ethiopia. J Infect Dev Ctries 2011; 5:23–33[PubMed]
    [Google Scholar]
  77. Eibach D, Al-Emran HM, Dekker DM, Krumkamp R, Adu-Sarkodie Y et al. The emergence of reduced ciprofloxacin susceptibility in Salmonella enterica causing bloodstream infections in rural Ghana. Clin Infect Dis 2016; 62:S32–S36 [View Article][PubMed]
    [Google Scholar]
  78. Hendriksen RS, Joensen KG, Lukwesa-Musyani C, Kalondaa A, Leekitcharoenphon P et al. Extremely drug-resistant Salmonella enterica serovar Senftenberg infections in patients in Zambia. J Clin Microbiol 2013; 51:284–286 [View Article][PubMed]
    [Google Scholar]
  79. Gordon MA. Invasive non-typhoidal Salmonella disease – epidemiology, pathogenesis and diagnosis. Curr Opin Infect Dis 2012; 24:484–489
    [Google Scholar]
  80. Li B, Yang X, Tan H, Ke B, He D et al. Whole genome sequencing analysis of Salmonella enterica serovar Weltevreden isolated from human stool and contaminated food samples collected from the southern coastal area of China. Int J Food Microbiol 2018; 266:317–323 [View Article][PubMed]
    [Google Scholar]
  81. Makendi C, Page AJ, Wren BW, Le Thi Phuong T, Clare S et al. A phylogenetic and phenotypic analysis of Salmonella enterica serovar Weltevreden, an emerging agent of diarrheal disease in tropical regions. PLoS Negl Trop Dis 2016; 10:e0004446 [View Article][PubMed]
    [Google Scholar]
  82. Arjyal A, Basnyat B, Nhan HT, Koirala S, Giri A et al. Gatifloxacin versus ceftriaxone for uncomplicated enteric fever in Nepal: an open-label, two-centre, randomised controlled trial. Lancet Infect Dis 2016; 16:535–545 [View Article][PubMed]
    [Google Scholar]
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