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Volume 8, Issue 10

Endemic erythromycin resistant in Vietnam in the 1990s Open Access

Abstract

Diphtheria is a potentially fatal respiratory disease caused by toxigenic forms of the Gram-positive bacterium . Despite the availability of treatments (antitoxin and antimicrobials) and effective vaccines, the disease still occurs sporadically in low-income countries and in higher income where use of diphtheria vaccine is inconsistent. Diphtheria was highly endemic in Vietnam in the 1990s; here, we aimed to provide some historical context to the circulation of erythromycin resistant organisms in Vietnam during this period. After recovering 54 . isolated from clinical cases of diphtheria in Ho Chi Minh City between 1992 and 1998 we conducted whole genome sequencing and analysis. Our data outlined substantial genetic diversity among the isolates, illustrated by seven distinct Sequence Types (STs), but punctuated by the sustained circulation of ST67 and ST209. With the exception of one isolate, all sequences contained the gene, which was classically located on a corynebacteriophage. All erythromycin resistant isolates, accounting for 13 % of organisms in this study, harboured a novel 18 kb )-carrying plasmid, which exhibited limited sequence homology to previously described resistance plasmids in . Our study provides historic context for the circulation of antimicrobial resistant in Vietnam; these data provide a framework for the current trajectory in global antimicrobial resistance trends.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): antimicrobial resistance , Corynebacterium diphtheriae , diphtheria , erythromycin and outbreak
Funding
This study was supported by the:
  • Wellcome Trust (Award 215515/Z/19/Z)
    • Principle Award Recipient: StephenBaker
© 2022 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2022-10-19
2024-04-28
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References

  1. Hadfield TL, McEvoy P, Polotsky Y, Tzinserling VA, Yakovlev AA. The pathology of diphtheria. J Infect Dis 2000; 181 Suppl 1:S116–20 [View Article]
     [Google Scholar]
  2. Hong K-W, Asmah Hani AW, Nurul Aina Murni CA, Pusparani RR, Chong CK et al. Comparative genomic and phylogenetic analysis of a toxigenic clinical isolate of Corynebacterium diphtheriae strain B-D-16-78 from Malaysia. Infect Genet Evol 2017; 54:263–270 [View Article]
     [Google Scholar]
  3. Centres for Disease Control and Prevention Diphtheria; 2016
  4. Parande MV, Parande AM, Lakkannavar SL, Kholkute SD, Roy S. Diphtheria outbreak in rural North Karnataka, India. JMM Case Rep 2014; 1:3–5 [View Article]
     [Google Scholar]
  5. Saikia L, Nath R, Saikia NJ, Choudhury G, Sarkar M. A diphtheria outbreak in Assam, India. Southeast Asian J Trop Med Public Health 2010; 41:647–652
     [Google Scholar]
  6. Rasmussen I, Wallace S, Mengshoel AT, Høiby EA, Brandtzæg P. Diphtheria outbreak in Norway: lessons learned. Scand J Infect Dis 2011; 43:986–989 [View Article]
     [Google Scholar]
  7. Nanthavong N, Black AP, Nouanthong P, Souvannaso C, Vilivong K et al. Diphtheria in Lao PDR: insufficient coverage or ineffective vaccine?. PLoS One 2015; 10:e0121749 [View Article]
     [Google Scholar]
  8. Moghalles SA, Aboasba BA, Alamad MA, Khader YS. Epidemiology of diphtheria in yemen, 2017-2018: surveillance data analysis. JMIR Public Health Surveill 2021; 7:e27590 [View Article]
     [Google Scholar]
  9. Badell E, Alharazi A, Criscuolo A, Almoayed KAA, Lefrancq N et al. Ongoing diphtheria outbreak in Yemen: a cross-sectional and genomic epidemiology study. Lancet Microbe 2021; 2:e386–e396 [View Article]
     [Google Scholar]
  10. Zakikhany K, Efstratiou A. Diphtheria in Europe: current problems and new challenges. Future Microbiol 2012; 7:595–607 [View Article]
     [Google Scholar]
  11. Daskalaki I. Corynebacterium diphtheriae. In Principles and Practice of Pediatric Infectious Diseases, 4th. edn 2012 [View Article]
     [Google Scholar]
  12. Vitek CR, Wharton M. Diphtheria in the former Soviet Union: reemergence of a pandemic disease. Emerg Infect Dis 1998; 4:539–550 [View Article]
     [Google Scholar]
  13. Havaldar PV, Sankpal MN, Doddannavar RP. Diphtheritic myocarditis: clinical and laboratory parameters of prognosis and fatal outcome. Ann Trop Paediatr 2000; 20:209–215 [View Article]
     [Google Scholar]
  14. Solders G, Nennesmo I, Persson A. Diphtheritic neuropathy, an analysis based on muscle and nerve biopsy and repeated neurophysiological and autonomic function tests. J Neurol Neurosurg Psychiatry 1989; 52:876–880 [View Article]
     [Google Scholar]
  15. Sharma NC, Efstratiou A, Mokrousov I, Mutreja A, Das B et al. Diphtheria. Nat Rev Dis Primers 2019; 5:81 [View Article]
     [Google Scholar]
  16. Zajdowicz SLW, Holmes RK. Phage Conversion and the Role of Bacteriophage and Host Functions in Regulation of Diphtheria Toxin Production by Corynebacterium diphtheriae. In The Mechanistic Benefits of Microbial Symbionts 2016 pp 15–45 [View Article]
     [Google Scholar]
  17. Pereira GA, Pimenta FP, dos Santos FRW, Damasco PV, Hirata Júnior R et al. Antimicrobial resistance among Brazilian Corynebacterium diphtheriae strains. Mem Inst Oswaldo Cruz 2008; 103:507–510 [View Article]
     [Google Scholar]
  18. Sariadji K, Sunarno S, Puspandari N, Sembiring M. Antibiotic susceptibility pattern of Corynebacterium diphtheriae isolated from outbreaks in Indonesia 2010-2015. Indones Biomed J 2016; 10:51 [View Article]
     [Google Scholar]
  19. Mina NV, Burdz T, Wiebe D, Rai JS, Rahim T et al. Canada’s first case of a multidrug-resistant Corynebacterium diphtheriae strain, isolated from a skin abscess. J Clin Microbiol 2011; 49:4003–4005 [View Article] [PubMed]
     [Google Scholar]
  20. Rockhill RC, Sumarmo, Hadiputranto H, Siregar SP, Muslihun B. Tetracycline resistance of Corynebacterium diphtheriae isolated from diphtheria patients in Jakarta, Indonesia. Antimicrob Agents Chemother 1982; 21:842–843 [View Article]
     [Google Scholar]
  21. Will RC, Ramamurthy T, Sharma NC, Veeraraghavan B, Sangal L et al. Spatiotemporal persistence of multiple, diverse clades and toxins of Corynebacterium diphtheriae. Nat Commun 2021; 12:1500 [View Article]
     [Google Scholar]
  22. Forde BM, Henderson A, Playford EG, Looke D, Henderson BC et al. Fatal respiratory Diphtheria Caused by ß-Lactam-Resistant Corynebacterium diphtheriae. Clin Infect Dis 2021; 73:e4531–e4538 [View Article]
     [Google Scholar]
  23. Hennart M, Panunzi LG, Rodrigues C, Gaday Q, Baines SL et al. Population genomics and antimicrobial resistance in Corynebacterium diphtheriae. Genome Med 2020; 12:107 [View Article]
     [Google Scholar]
  24. Olender A. Mechanisms of Antibiotic Resistance in Corynebacterium spp. Causing Infections in People. In Antibiot Resist Bact - A Contin Chall New Millenn 2012 [View Article]
     [Google Scholar]
  25. Murakami H, Phuong NM, Thang HV, Chau NV, Giao PN et al. Endemic diphtheria in Ho Chi Minh City; Viet Nam: A matched case-control study to identify risk factors of incidence. Vaccine 2010; 28:8141–8146 [View Article] [PubMed]
     [Google Scholar]
  26. Inouye M, Dashnow H, Raven L-A, Schultz MB, Pope BJ et al. SRST2: Rapid genomic surveillance for public health and hospital microbiology labs. Genome Med 2014; 6:90 [View Article]
     [Google Scholar]
  27. Doanh PV, Pham T D, Vu N L, Chu V T, Do T H H et al. An outbreak of diphtheria in K’Bang District, Gia Lai, Vietnam, October 2013 – July 2014. Int J Infect Dis 2016; 45:172 [View Article]
     [Google Scholar]
  28. Kitamura N, Le TTT, Le LT, Nguyen LD, Dao AT et al. Diphtheria outbreaks in schools in Central Highland Districts, Vietnam, 2015-2018. Emerg Infect Dis 2020; 26:596–600 [View Article]
     [Google Scholar]
  29. Kneen R, Nguyen MD, Solomon T, Pham NG, Parry CM et al. Clinical features and predictors of diphtheritic cardiomyopathy in Vietnamese children. Clin Infect Dis 2004; 39:1591–1598 [View Article]
     [Google Scholar]
  30. Kneen R, Pham NG, Solomon T, Tran TM, Nguyen TT et al. Penicillin vs. erythromycin in the treatment of diphtheria. Clin Infect Dis 1998; 27:845–850 [View Article]
     [Google Scholar]
  31. Zasada AA, Mosiej E. Contemporary microbiology and identification of Corynebacteria spp. causing infections in human. Lett Appl Microbiol 2018; 66:472–483 [View Article] [PubMed]
     [Google Scholar]
  32. EUCAST EUCAST Definitive Document E.DEF 3.1, June 2000: Determination of minimum inhibitory concentrations (MICs) of antibacterial agents by agar dilution. Clin Microbiol Infect 2000; 6:509–515 [View Article]
     [Google Scholar]
  33. Clinical and Laboratory Standards Institute (CLSI) M45 - Methods for Antimicrobial Dilution and Disk Susceptibility Testing of Infrequently Isolated or Fastidious Bacteria - 3rd edition 2016
     [Google Scholar]
  34. Corporation P. Wizard ® genomic DNA purification kit. Tech Man Wizard ® Genomic DNA Purif Kit 2012608–277
     [Google Scholar]
  35. Thermo Fisher Scientific n.d User guide: qubit dsdna HS assay kits.
  36. Illumina Nextera XT DNA library prep refrence guide 2016
     [Google Scholar]
  37. Andrews S. FastQC: A quality control tool for high throughput sequence data. Babraham Bioinformatics 2010
     [Google Scholar]
  38. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357–359 [View Article] [PubMed]
     [Google Scholar]
  39. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [View Article]
     [Google Scholar]
  40. Lam MMC, Wyres KL, Wick RR, Judd LM, Fostervold A et al. Convergence of virulence and MDR in a single plasmid vector in MDR Klebsiella pneumoniae ST15. J Antimicrob Chemother 2019; 74:1218–1222 [View Article]
     [Google Scholar]
  41. Holt KE, Wertheim H, Zadoks RN, Baker S, Whitehouse CA et al. Genomic analysis of diversity, population structure, virulence, and antimicrobial resistance in Klebsiella pneumoniae, an urgent threat to public health. Proc Natl Acad Sci U S A 2015; 112:E3574–81 [View Article]
     [Google Scholar]
  42. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res 2015; 43:e15 [View Article]
     [Google Scholar]
  43. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article] [PubMed]
     [Google Scholar]
  44. Segata N, Waldron L, Ballarini A, Narasimhan V, Jousson O et al. Metagenomic microbial community profiling using unique clade-specific marker genes. Nat Methods 2012; 9:811–814 [View Article]
     [Google Scholar]
  45. Wick RR, Schultz MB, Zobel J, Holt KE. Bandage: interactive visualization of de novo genome assemblies. Bioinformatics 2015; 31:3350–3352 [View Article]
     [Google Scholar]
  46. Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA. BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 2011; 12:402 [View Article]
     [Google Scholar]
  47. Ton-That H, Marraffini LA, Schneewind O. Sortases and pilin elements involved in pilus assembly of Corynebacterium diphtheriae. Mol Microbiol 2004; 53:251–261 [View Article]
     [Google Scholar]
  48. Ton-That H, Schneewind O. Assembly of pili on the surface of Corynebacterium diphtheriae. Mol Microbiol 2003; 50:1429–1438 [View Article]
     [Google Scholar]
  49. Saito N, Dimapilis VO, Fujii H, Suzuki M, Telan EFO et al. Diphtheria in Metro Manila, the Philippines 2006-2017: a clinical, molecular, and spatial characterization. Clin Infect Dis 2021; 72:61–68 [View Article]
     [Google Scholar]
  50. Czajka U, Wiatrzyk A, Mosiej E, Formińska K, Zasada AA. Changes in MLST profiles and biotypes of Corynebacterium diphtheriae isolates from the diphtheria outbreak period to the period of invasive infections caused by nontoxigenic strains in Poland (1950-2016). BMC Infect Dis 2018; 18:1–8 [View Article] [PubMed]
     [Google Scholar]
  51. Paveenkittiporn W, Sripakdee S, Koobkratok O, Sangkitporn S, Kerdsin A. Molecular epidemiology and antimicrobial susceptibility of outbreak-associated Corynebacterium diphtheriae in Thailand, 2012. Infect Genet Evol 2019; 75:104007 [View Article]
     [Google Scholar]
  52. Xiaoli L, Benoliel E, Peng Y, Aneke J, Cassiday PK et al. Genomic epidemiology of nontoxigenic Corynebacterium diphtheriae from King County, Washington State, USA between July 2018 and May 2019. Microb Genom 2020; 6: [View Article]
     [Google Scholar]
  53. Stimson J, Gardy J, Mathema B, Crudu V, Cohen T et al. Beyond the SNP Threshold: identifying outbreak clusters using inferred transmissions. Mol Biol Evol 2019; 36:587–603 [View Article]
     [Google Scholar]
  54. Chorlton SD, Ritchie G, Lawson T, Romney MG, Lowe CF. Whole-genome sequencing of Corynebacterium diphtheriae isolates recovered from an inner-city population demonstrates the predominance of a single molecular strain. J Clin Microbiol 2020; 58:e01651-19 [View Article]
     [Google Scholar]
  55. Berger A, Dangel A, Schober T, Schmidbauer B, Konrad R et al. Whole genome sequencing suggests transmission of Corynebacterium diphtheriae-caused Cutaneous diphtheria in two siblings, Germany, 2018. Euro Surveill 2019; 24: [View Article]
     [Google Scholar]
  56. Maple PA, Efstratiou A, Tseneva G, Rikushin Y, Deshevoi S et al. The in-vitro susceptibilities of toxigenic strains of Corynebacterium diphtheriae isolated in northwestern Russia and surrounding areas to ten antibiotics. J Antimicrob Chemother 1994; 34:1037–1040 [View Article]
     [Google Scholar]
  57. Sekizuka T, Yamamoto A, Komiya T, Kenri T, Takeuchi F et al. Corynebacterium ulcerans 0102 carries the gene encoding diphtheria toxin on a prophage different from the C. diphtheriae NCTC 13129 prophage. BMC Microbiol 2012; 12:12–72 [View Article]
     [Google Scholar]
  58. Brüssow H, Canchaya C, Hardt W-D. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 2004; 68:560–602 [View Article]
     [Google Scholar]
  59. Liu Y, Harrison PM, Kunin V, Gerstein M. Comprehensive analysis of pseudogenes in prokaryotes: widespread gene decay and failure of putative horizontally transferred genes. Genome Biol 2004; 5:R64 [View Article]
     [Google Scholar]
  60. Mandlik A, Swierczynski A, Das A, Ton-That H. Corynebacterium diphtheriae employs specific minor pilins to target human pharyngeal epithelial cells. Mol Microbiol 2007; 64:111–124 [View Article] [PubMed]
     [Google Scholar]
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Endemic erythromycin resistant Corynebacterium diphtheriae in Vietnam in the 1990s
M Gen 8, 000861 (2022); https://doi.org/10.1099/mgen.0.000861
/content/journal/mgen/10.1099/mgen.0.000861
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