Cited by 69

The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.

High prevalence of multiple antibiotic resistance in clinical E. coli isolates from Bangladesh and prediction of molecular resistance determinants using WGS of an XDR isolate

Jain, Preeti, Bepari, Asim Kumar, Sen, Prosengit Kumer, Rafe, Tanzir, Imtiaz, Rashed, Hossain, Maqsud, Reza, Hasan Mahmud·2021·Scientific Reports

Abstract

Multi-drug-resistance (MDR) is a severe public health concern worldwide, and its containment is more challenging in developing countries due to poor antimicrobial resistance (AMR) surveillance and irrational use of antibiotics. The current study investigated 100 clinical E. coli isolates and revealed that 98% of them were MDR. PCR analysis using 25 selected isolates showed the predominance of metallo-β-lactamase gene bla NDM (80%) and ESBL genes bla OXA (48%) and bla CTX-M-15 (32%). The AmpC gene was detected in 68% of the isolates, while 32% was tet C positive. Notably, 34% of the isolates were resistant to carbapenem. Whole genome sequence (WGS) analysis of an extensively drug-resistant (XDR) isolate (L16) revealed the presence of the notorious sequence type 131 responsible for multi-drug-resistant infections, multiple antibiotic resistance genes (ARGs), virulence genes, and mobile genetic elements that pose risks to environmental transmission. Our results indicate that MDR is alarmingly increasing in Bangladesh that critically limits the treatment option against infections and contributes to further aggravation to the prevailing situation of MDR worldwide. The findings of this study will be valuable in designing sustainable strategies to contain MDR in the region.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41598-021-02251-w

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Multidrug-resistant bacteria have previously been associated with severe human illnesses like cholera, diarrhea, and other water-borne diseases in the Bangladeshi population.

    “Multidrug-resistant bacteria have previously been associated with severe human illnesses like cholera, diarrhea, and other water-borne diseases in the Bangladeshi population18,71–74.”

    From Impact of untreated tannery wastewater in the evolution of multidrug-resistant bacteria in Bangladesh (2024) · cites this paper as [73]

    The Introduction (page unavailable) identifies E. coli as a cause of enteric infections in Bangladesh and links its clinical threat to antibiotic resistance. The Discussion (page unavailable) reports multidrug-resistant E. coli in clinical settings and drinking water. The paper does not specifically associate resistant bacteria with cholera or establish that its clinical isolates caused the listed water-borne diseases. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 79

  1. Islam, S., Aldstadt, J. & Aga, D. Global antimicrobial resistance: A complex and dire threat with few definite answers. Trop. Med. Int. Health 24, 658–662 (2019). · DOI
  2. Safain, K. S. et al. Situation of antibiotic resistance in Bangladesh and its association with resistance genes for horizontal transfer. BioRxiv. https://doi.org/10.1101/2020.04.06.027391 (2020). · DOI
  3. Rahman, M. D. M. et al. Isolation and molecular characterization of multidrug-resistant Escherichia coli from chicken meat. Sci. Rep. 10, 21999 (2020). · DOI
  4. Kpoda, D. S. et al. Distribution of resistance genes encoding ESBLs in Enterobacteriaceae isolated from biological samples in health centers in Ouagadougou, Burkina Faso. BMC Res. Notes 11, 471 (2018). · DOI
  5. Zeng, X. et al. Comparative genome analysis of an extensively drug-resistant isolate of avian sequence type 167 Escherichia coli strain sanji with novel in silico serotype O89b:H9. mSystems 4, e00242 (2019). · DOI
  6. Ragupathi, N. K. D. et al. First Indian report on genome-wide comparison of multidrug-resistant Escherichia coli from blood stream infections. PLoS ONE 15, e0220428 (2020). · DOI
  7. Algammal, A. M. et al. Virulence-determinants and antibiotic-resistance genes of MDR-E. coli isolated from secondary infections following FMD-outbreak in cattle. Sci. Rep. 10, 19779 (2020). · DOI
  8. Deter, H. S., Hossain, T. & Butzin, N. C. Antibiotic tolerance is associated with a broad and complex transcriptional response in E. coli. Sci. Rep. 11, 6112 (2021). · DOI
  9. Herring, C. D. et al. Comparative genome sequencing of Escherichia coli allows observation of bacterial evolution on a laboratory timescale. Nat. Genet. 38, 1406–1412 (2006). · DOI
  10. Ben Zakour, N. L. et al. Sequential acquisition of virulence and fluoroquinolone resistance has shaped the evolution of Escherichia coli ST131. MBio 7, e00347 (2016).
  11. Hasman, H. et al. Rapid whole-genome sequencing for detection and characterization of microorganisms directly from clinical samples. J. Clin. Microbiol. 52, 139–146 (2014). · DOI
  12. Niemann, S. et al. Genomic diversity among drug sensitive and multidrug resistant isolates of Mycobacterium tuberculosis with identical DNA fingerprints. PLoS ONE 4, e7407 (2009). · DOI
  13. Nobel, F. et al. Prevalence of multidrug resistance patterns of Escherichia coli from suspected urinary tract infection in Mymensingh city, Bangladesh. J. Adv. Biotechnol. Exp. Ther. 4, 256 (2021). · DOI
  14. Talukdar, P. K. et al. Antimicrobial resistance, virulence factors and genetic diversity of Escherichia coli isolates from household water supply in Dhaka, Bangladesh. PLoS ONE 8, e61090 (2013). · DOI · Paper page
  15. Hassan, M. A. et al. Insight into multidrug-resistant microorganisms from microbial infected diabetic foot ulcers. Diabetes Metab. Syndr. 13, 1261–1270 (2019). · DOI
  16. Nji, E. et al. High prevalence of antibiotic resistance in commensal Escherichia coli from healthy human sources in community settings. Sci. Rep. 11, 3372 (2021). · DOI
  17. Faiz, A. & Basher, A. Antimicrobial resistance: Bangladesh experience. Reg. Health Forum 15, 9 (2011).
  18. Hoque, R. et al. Tackling antimicrobial resistance in Bangladesh: A scoping review of policy and practice in human, animal and environment sectors. PLoS ONE 15, e0227947 (2020). · DOI · Paper page
  19. Rahman, M. S. & Huda, S. Antimicrobial resistance and related issues: An overview of Bangladesh situation. Bangl. J. Pharmacol. 9, 218–224 (2014).
  20. Wattam, A. R. et al. Improvements to PATRIC, the all-bacterial bioinformatics database and Analysis Resource Center. Nucleic Acids Res. 45, D535–D542 (2017). · DOI
  21. Wick, R. R., Judd, L. M., Gorrie, C. L. & Holt, K. E. Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput. Biol. 13, e1005595 (2017). · DOI
  22. Brettin, T. et al. RASTtk: A modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci. Rep. 5, 8365 (2015). · DOI
  23. Overbeek, R. et al. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res. 33, 5691–5702 (2005). · DOI
  24. Nicolas-Chanoine, M.-H. et al. Intercontinental emergence of Escherichia coli clone O25:H4-ST131 producing CTX-M-15. J. Antimicrob. Chemother. 61, 273–281 (2008). · DOI
  25. Russo, T. A. & Johnson, J. R. Proposal for a new inclusive designation for extraintestinal pathogenic isolates of Escherichia coli: ExPEC. J. Infect. Dis. 181, 1753–1754 (2000). · DOI
  26. Johansson, M. H. K. et al. Detection of mobile genetic elements associated with antibiotic resistance in Salmonella enterica using a newly developed web tool: MobileElementFinder. J. Antimicrob. Chemother. 76, 101–109 (2021). · DOI · Paper page
  27. Wilson, L. A. & Sharp, P. M. Enterobacterial repetitive intergenic consensus (ERIC) sequences in Escherichia coli: Evolution and implications for ERIC-PCR. Mol. Biol. Evol. 23, 1156–1168 (2006). · DOI
  28. Rasko, D. A. et al. The pangenome structure of Escherichia coli: Comparative genomic analysis of E. coli commensal and pathogenic isolates. J. Bacteriol. 190, 6881–6893 (2008). · DOI
  29. Harris, R. S. Improved Pairwise Alignment of Genomic DNA (The Pennsylvania State University, 2007).
  30. WHO. Prioritization of Pathogens to Guide Discovery, Research and Development of New Antibiotics for Drug-Resistant Bacterial Infections, Including Tuberculosis (WHO, 2017).
  31. Nahar, A., Hasnat, S., Akhter, H. & Begum, N. Evaluation of antimicrobial resistance pattern of uropathogens in a tertiary care hospital in Dhaka city, Bangladesh. South East Asia J. Public Health 7, 12–18 (2017). · DOI
  32. Hossain, A. et al. Age and gender-specific antibiotic resistance patterns among Bangladeshi patients with urinary tract infection caused by Escherichia coli. Heliyon 6, e04161 (2020). · DOI
  33. Jaggi, N. et al. Carbapenem resistance in Escherichia coli and Klebsiella pneumoniae among Indian and international patients in North India. Acta Microbiol. Immunol. Hung. 66, 367–376 (2019). · DOI
  34. Ansari, S. et al. Community acquired multi-drug resistant clinical isolates of Escherichia coli in a tertiary care center of Nepal. Antimicrob. Resist. Infect. Control 4, 15 (2015). · DOI
  35. Govindaswamy, A. et al. Prevalence and characterization of beta-lactamase-producing Escherichia coli isolates from a tertiary care hospital in India. J. Lab. Phys. 11, 123–127 (2019).
  36. Haroon, R. M. et al. Antibacterial resistance patterns of bacteria isolated from clinical specimens at Uttara IbnSina Diagnostic Centre, Dhaka. Afr. J. Microbiol. Res. 14, 175–181 (2020). · DOI
  37. Rashid, M., Rakib, M. M. & Hasan, B. Antimicrobial-resistant and ESBL-producing Escherichia coli in different ecological niches in Bangladesh. Infect. Ecol. Epidemiol. 5, 26712 (2015).
  38. Islam, M. S. Irrational use of drugs, healthcare level and healthcare expenditure in Bangladesh. Int. J. Health Econ. Policy 2, 152 (2017).
  39. Begum, N. & Shamsuzzaman, S. M. Emergence of carbapenemase-producing urinary isolates at a Tertiary Care Hospital in Dhaka, Bangladesh. Tzu Chi Med. J. 28, 94–98 (2016). · DOI
  40. Rakhi, N. N., Alam, A. S. M. R. U., Sultana, M., Rahaman, M. M. & Hossain, M. A. Diversity of carbapenemases in clinical isolates: The emergence of blaVIM-5 in Bangladesh. J. Infect. Chemother. 25, 444–451 (2019). · DOI
  41. Livermore, D. M. et al. OXA-1 β-lactamase and non-susceptibility to penicillin/β-lactamase inhibitor combinations among ESBL-producing Escherichia coli. J. Antimicrob. Chemother. 74, 326–333 (2019). · DOI
  42. Poirel, L., Naas, T. & Nordmann, P. Diversity, epidemiology, and genetics of class D β-lactamases. Antimicrob. Agents Chemother. 54, 24–38 (2010). · DOI
  43. Mazumder, R., Abdullah, A., Ahmed, D. & Hussain, A. High prevalence of blaCTX-M-15 gene among extended-spectrum β-lactamase-producing Escherichia coli isolates causing extraintestinal infections in Bangladesh. Antibiotics 9, 796 (2020). · DOI
  44. Ramadan, A. A., Abdelaziz, N. A., Amin, M. A. & Aziz, R. K. Novel bla CTX-M variants and genotype-phenotype correlations among clinical isolates of extended spectrum beta lactamase-producing Escherichia coli. Sci. Rep. 9, 4224 (2019). · DOI
  45. Jadhav, S. et al. Virulence characteristics and genetic affinities of multiple drug resistant uropathogenic Escherichia coli from a semi urban locality in India. PLoS ONE 6, e18063 (2011). · DOI
  46. Ahsan, S. & Islam, R. Beta-lactamase-producing Escherichia coli in Bangladesh: Their phenotypic and molecular characteristics. Dhaka Univ. J. Biol. Sci. 28, 71–81 (2019). · DOI
  47. Zhang, X.-X., Zhang, T. & Fang, H. H. P. Antibiotic resistance genes in water environment. Appl. Microbiol. Biotechnol. 82, 397–414 (2009). · DOI
  48. Huang, J., Lan, F., Lu, Y. & Li, B. Characterization of integrons and antimicrobial resistance in Escherichia coli sequence type 131 isolates. Can. J. Infect. Dis. Med. Microbiol. 2020, e3826186 (2020). · DOI
  49. Singh, T. et al. Changing paradigm of antibiotic resistance amongst Escherichia coli isolates in Indian pediatric population. PLoS ONE 14, e0213850 (2019). · DOI
  50. Bush, K. & Jacoby, G. A. Updated functional classification of β-lactamases. Antimicrob. Agents Chemother. 54, 969–976 (2010). · DOI · Paper page
  51. Estaleva, C. E. L. et al. High prevalence of multidrug resistant ESBL- and plasmid mediated AmpC-producing clinical isolates of Escherichia coli at Maputo Central Hospital, Mozambique. BMC Infect. Dis. 21, 16 (2021). · DOI
  52. Jacoby, G. A. AmpC beta-lactamases. Clin. Microbiol. Rev. 22, 161–182 (2009). · DOI
  53. Khari, F. I. M., Karunakaran, R., Rosli, R. & Tay, S. T. Genotypic and phenotypic detection of AmpC β-lactamases in Enterobacter spp. isolated from a Teaching Hospital in Malaysia. PLoS ONE 11, e0150643 (2016). · DOI
  54. Satter, S., Mahbub, H. & Shamsuzzaman, S. M. Phenotypic and molecular characterization of AmpC beta-lactamase enzyme producing Escherichia coli and Klebsiella species isolated from A Tertiary Care Hospital in Bangladesh. Mymensingh Med. J. 29, 895–900 (2020).
  55. Rensing, K. L. et al. Prevalence of plasmid-mediated AmpC in Enterobacteriaceae isolated from humans and from retail meat in Zagazig, Egypt. Antimicrob. Resist. Infect. Control 8, 45 (2019). · DOI
  56. Aryal, S. C. et al. Plasmid-mediated AmpC β-lactamase CITM and DHAM genes among gram-negative clinical isolates. Infect. Drug Resist. 13, 4249–4261 (2020). · DOI
  57. Rogers, B. A., Sidjabat, H. E. & Paterson, D. L. Escherichia coli O25b-ST131: A pandemic, multiresistant, community-associated strain. J. Antimicrob. Chemother. 66, 1–14 (2011). · DOI
  58. Chakraborty, A. et al. Characterization of Escherichia coli phylogenetic groups associated with extraintestinal infections in South Indian population. Ann. Med. Health Sci. Res. 5, 241–246 (2015). · DOI
  59. Fang, X. et al. Escherichia coli B2 strains prevalent in inflammatory bowel disease patients have distinct metabolic capabilities that enable colonization of intestinal mucosa. BMC Syst. Biol. 12, 66 (2018). · DOI
  60. Haldorsen, B. et al. The AmpC phenotype in Norwegian clinical isolates of Escherichia coli is associated with an acquired ISEcp1-like ampC element or hyperproduction of the endogenous AmpC. J. Antimicrob. Chemother. 62, 694–702 (2008). · DOI
  61. Han, C.-G., Shiga, Y., Tobe, T., Sasakawa, C. & Ohtsubo, E. Structural and functional characterization of IS679 and IS66-family elements. J. Bacteriol. 183, 4296–4304 (2001). · DOI
  62. Mahillon, J. & Chandler, M. Insertion sequences. Microbiol. Mol. Biol. Rev. 62, 725–774 (1998). · DOI
  63. Abadi, A. T. B., Mobarez, A. M., Bonten, M. J., Wagenaar, J. A. & Kusters, J. G. Clinical relevance of the cagA, tnpA and tnpB genes in Helicobacter pylori. BMC Gastroenterol. 14, 33 (2014). · DOI
  64. Ramisetty, B. C. M. & Sudhakari, P. A. Bacterial ‘grounded’ prophages: Hotspots for genetic renovation and innovation. Front. Genet. https://doi.org/10.3389/fgene.2019.00065 (2019). · DOI
  65. Hanai, R. et al. Molecular dissection of a protein SopB essential for Escherichia coli F plasmid partition. J. Biol. Chem. 271, 17469–17475 (1996). · DOI
  66. Hanai, R. & Arai, Y. New roles of DNA and SopB in polymerization of SopA of Escherichia coli F plasmid. J. Biochem. (Tokyo) 157, 459–466 (2015). · DOI
  67. Biswas, T., Houghton, J. L., Garneau-Tsodikova, S. & Tsodikov, O. V. The structural basis for substrate versatility of chloramphenicol acetyltransferase CATI. Protein Sci. Publ. Protein Soc. 21, 520–530 (2012). · DOI
  68. Shaw, W. V. The Enzymatic acetylation of chloramphenicol by extracts of R factor-resistant Escherichia coli. J. Biol. Chem. 242, 687–693 (1967). · DOI
  69. Zhang, Z. et al. Characterization of unexpressed extended-spectrum beta-lactamase genes in antibiotic-sensitive Klebsiella pneumoniae isolates. Microb. Drug Resist. 24, 799–806 (2018). · DOI
  70. CLSI. Performance Standards for Antimicrobial Disk Susceptibility Tests Vol. 32 (Clinical and Laboratory Standards Institute, 2012).
  71. Ng, L.-K., Martin, I., Alfa, M. & Mulvey, M. Multiplex PCR for the detection of tetracycline resistant genes. Mol. Cell. Probes 15, 209–215 (2001). · DOI
  72. Fernando, D. M. et al. Detection of antibiotic resistance genes in source and drinking water samples from a first nations Community in Canada. Appl. Environ. Microbiol. 82, 4767–4775 (2016). · DOI
  73. Larsen, M. V. et al. Multilocus sequence typing of total-genome-sequenced bacteria. J. Clin. Microbiol. 50, 1355–1361 (2012). · DOI
  74. Wirth, T. et al. Sex and virulence in Escherichia coli: An evolutionary perspective. Mol. Microbiol. 60, 1136–1151 (2006). · DOI
  75. Joensen, K. G., Tetzschner, A. M. M., Iguchi, A., Aarestrup, F. M. & Scheutz, F. Rapid and easy in silico serotyping of Escherichia coli isolates by use of whole-genome sequencing data. J. Clin. Microbiol. 53, 2410–2426 (2015). · DOI · Paper page
  76. Beghain, J., Bridier-Nahmias, A., Le Nagard, H., Denamur, E. & Clermont, O. ClermonTyping: An easy-to-use and accurate in silico method for Escherichia genus strain phylotyping. Microb. Genomics 4, e000192 (2018). · DOI
  77. Joensen, K. G. et al. Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic Escherichia coli. J. Clin. Microbiol. 52, 1501–1510 (2014). · DOI
  78. Tetzschner, A. M. M., Johnson, J. R., Johnston, B. D., Lund, O. & Scheutz, F. In silico genotyping of Escherichia coli isolates for extraintestinal virulence genes by use of whole-genome sequencing data. J. Clin. Microbiol. https://doi.org/10.1128/JCM.01269-20 (2020). · DOI
  79. Seemann, T. Prokka: Rapid prokaryotic genome annotation. Bioinformatics 30, 2068–2069 (2014). · DOI

Cited by

Sorted by citations

Metadata

Authors
Jain, P., Bepari, A. K., Sen, P. K., Rafe, T., Imtiaz, R., Hossain, M., & Reza, H. M.
Venue
Scientific Reports
Published
2021-11-24
Volume
11
Issue
1
ISSN
2045-2322
Cited by
69
References
1
Language
en

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review