An Overview on Phenotypic and Genotypic Characterisation of Carbapenem-Resistant Enterobacterales

Amal A Sabour 10, Maha A Alshiekheid 10, Jumana M Al-Jishi 11, Faryal Khamis 12, Sara Alwarthan 13, Mashael Alhajri 13, Amal H Alfaraj 14, Huseyin Tombuloglu 15, Mohammed Garout 16, Duaa M Alabdullah 17, Elmoeiz Ali Elnagi Mohammed 18, Fatimah S Al Yami 19, Haifa A Almuhtaresh 20, Kovy Arteaga Livias 21 22, Abbas Al Mutair 23 24 25 26, Shawqi A Almushrif 27, Mai Abdel Haleem A Abusalah 28, Naveed Ahmed 29

Affiliations

19 November 2022

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doi: 10.3390/medicina58111675

Abstract

Improper use of antimicrobials has resulted in the emergence of antimicrobial resistance (AMR), including multi-drug resistance (MDR) among bacteria. Recently, a sudden increase in Carbapenem-resistant Enterobacterales (CRE) has been observed. This presents a substantial challenge in the treatment of CRE-infected individuals. Bacterial plasmids include the genes for carbapenem resistance, which can also spread to other bacteria to make them resistant. The incidence of CRE is rising significantly despite the efforts of health authorities, clinicians, and scientists. Many genotypic and phenotypic techniques are available to identify CRE. However, effective identification requires the integration of two or more methods. Whole genome sequencing (WGS), an advanced molecular approach, helps identify new strains of CRE and screening of the patient population; however, WGS is challenging to apply in clinical settings due to the complexity and high expense involved with this technique. The current review highlights the molecular mechanism of development of Carbapenem resistance, the epidemiology of CRE infections, spread of CRE, treatment options, and the phenotypic/genotypic characterisation of CRE. The potential of microorganisms to acquire resistance against Carbapenems remains high, which can lead to even more susceptible drugs such as colistin and polymyxins. Hence, the current study recommends running the antibiotic stewardship programs at an institutional level to control the use of antibiotics and to reduce the spread of CRE worldwide.

Keywords: Carbapenem; Enterobacterales; Enterobacteriaceae; MDR; antibiotic resistance; carbapenemase; multi-drug resistance; β-lactamase.

Conflict of interest statement

The authors declare no conflict of interest.

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References

  1.  
    1. Willyard C. The drug-resistant bacteria that pose the greatest health threats. Nature. 2017;543:15. doi: 10.1038/nature.2017.21550. - DOI - PubMed
  2.  
    1. Lee C.-M., Lai C.-C., Chiang H.-T., Lu M.-C., Wang L.-F., Tsai T.-L., Kang M.-Y., Jan Y.-N., Lo Y.-T., Ko W.-C. Presence of multidrug-resistant organisms in the residents and environments of long-term care facilities in Taiwan. J. Microbiol. Immunol. Infect. 2017;50:133–144. doi: 10.1016/j.jmii.2016.12.001. - DOI - PubMed
  3.  
    1. Rodríguez-Baño J., Gutiérrez-Gutiérrez B., Machuca I., Pascual A. Treatment of infections caused by extended-spectrum-b-lactamase-, AmpC-, and carbapenemase-producing Enterobacteriaceae. Clin. Microbiol. Rev. 2018;31:e00079-17. doi: 10.1128/CMR.00079-17. - DOI - PMC - PubMed
  4.  
    1. Tang H.-J., Hsieh C.-F., Chang P.-C., Chen J.-J., Lin Y.-H., Lai C.-C., Chao C.-M., Chuang Y.-C. Clinical significance of community- and healthcare-acquired carbapenem-resistant Enterobacterales isolates. PLoS ONE. 2016;11:e0151897. - PMC - PubMed
  5.  
    1. Sheu C.-C., Lin S.-Y., Chang Y.-T., Lee C.-Y., Chen Y.-H., Hsueh P.-R. Management of infections caused by extended-spectrum b-lactamaseproducing Enterobacteriaceae: Current evidence and future prospects. Expert Rev. Anti-Infect. Ther. 2018;16:205–218. doi: 10.1080/14787210.2018.1436966. - DOI - PubMed
  6.  
    1. Kohanski M.A., Dwyer D.J., Collins J.J. How antibiotics kill bacteria: From targets to networks. Nat. Rev. Microbiol. 2010;8:423–435. doi: 10.1038/nrmicro2333. - DOI - PMC - PubMed
  7.  
    1. Ma J., Song X., Li M., Yu Z., Cheng W., Yu Z., Zhang W., Zhang Y., Shen A., Sun H. Global Spread of Carbapenem-Resistant Enterobacteriaceae: Epidemiological Features, Resistance Mechanisms, Detection and Therapy. Microbiol. Res. 2022;266:127249. doi: 10.1016/j.micres.2022.127249. - DOI - PubMed
  8.  
    1. Zerdan M.B., Al Hassan S., Shaker W., El Hajjar R., Allam S., Zerdan M.B., Naji A., Zeineddine N. Carbapenemase Inhibitors: Updates on Developments in 2021. J. Clin. Med. Res. 2022;14:251. doi: 10.14740/jocmr4764. - DOI - PMC - PubMed
  9.  
    1. Nordmann P., Naas T., Poirel L. Global spread of Carbapenemase-producing Enterobacteriaceae. Emerg. Infect. Dis. 2011;17:1791–1798. doi: 10.3201/eid1710.110655. - DOI - PMC - PubMed
  10.  
    1. Bassetti M., Peghin M., Vena A. Treatment of Infections Due to MDR Gram-Negative Bacteria. Front. Med. 2019;16:74. doi: 10.3389/fmed.2019.00074. - DOI - PMC - PubMed
  11.  
    1. Tseng S.-P., Wang S.-F., Ma L., Wang T.-Y., Yang T.-Y., Siu L.K., Chuang Y.-C., Lee P.-S., Wang J.-T., Wu T.-L. The plasmid-mediated fosfomycin resistance determinants and synergy of fosfomycin and meropenem in carbapenem-resistant Klebsiella pneumonia isolates in Taiwan. J. Microbiol. Immunol. Infect. 2017;50:653–661. doi: 10.1016/j.jmii.2017.03.003. - DOI - PubMed
  12.  
    1. Rabaan A.A., Alhumaid S., Mutair A.A., Garout M., Abulhamayel Y., Halwani M.A., Alestad J.H., Bshabshe A.A., Sulaiman T., AlFonaisan M.K. Application of Artificial Intelligence in Combating High Antimicrobial Resistance Rates. Antibiotics. 2022;11:784. doi: 10.3390/antibiotics11060784. - DOI - PMC - PubMed
  13.  
    1. Elbediwi M., Li Y., Paudyal N., Pan H., Li X., Xie S., Rajkovic A., Feng Y., Fang W., Rankin S.C. Global burden of colistin-resistant bacteria: Mobilized colistin resistance genes study (1980–2018) Microorganisms. 2019;7:461. doi: 10.3390/microorganisms7100461. - DOI - PMC - PubMed
  14.  
    1. European Centre for Disease Prevention and Control. Rapid Risk Assessment: Plasmid-mediated colistin resistance in Enterobacteriaceae. 2016. [(accessed on 16 March 2022)]. Stockholm: ECDC. Available online: https://ecdc.europa.eu/sites/portal/files/media/en/publications/Publicat....
  15.  
    1. Giamarellou H., Galani L., Baziaka F., Karaiskos I. Effectiveness of a double-carbapenem regimen for infections in humans due to carbapenemase-producing pandrug-resistant Klebsiella pneumoniae. Antimicrob. Agents Chemother. 2013;57:2388–2390. doi: 10.1128/AAC.02399-12. - DOI - PMC - PubMed
  16.  
    1. Camargo J.F., Simkins J., Beduschi T., Tekin A., Aragon L., Pérez-Cardona A., Prado C.E., Morris M.I., Abbo L.M., Cantón R. Successful treatment of Carbapenemase-producing pandrug-resistant Klebsiella pneumoniae bacteremia. Antimicrob Agents Chemother. 2015;59:5903–5908. doi: 10.1128/AAC.00655-15. - DOI - PMC - PubMed
  17.  
    1. Douka E., Perivolioti E., Kraniotaki E., Fountoulis K., Economidou F., Tsakris A., Skoutelis A., Routsi C. Emergence of a pandrug-resistant VIM-1-producing Providencia stuartii clonal strain causing an outbreak in a Greek intensive care unit. Int. J. Antimicrob. Agents. 2015;45:533–536. doi: 10.1016/j.ijantimicag.2014.12.030. - DOI - PubMed
  18.  
    1. Zowawi H.M., Forde B.M., Alfaresi M., Alzarouni A., Farahat Y., Chong T.-M., Yin W.-F., Chan K.-G., Li J., Schembri M.A. Stepwise evolution of pandrug-resistance in Klebsiella pneumoniae. Sci. Rep. 2015;5:15082. doi: 10.1038/srep15082. - DOI - PMC - PubMed
  19.  
    1. Ghafur A., Lakshmi V., Kannain P., Murali A., Thirunarayan M. Emergence of Pan-drug resistance amongst gram negative bacteria! The First case series from India. J. Microbiol. Infect Dis. 2014;4:86–91. doi: 10.5799/ahinjs.02.2014.03.0145. - DOI
  20.  
    1. Eljaaly K., Alharbi A., Alshehri S., Ortwine J.K., Pogue J.M. Plazomicin: A novel aminoglycoside for the treatment of resistant gram-negative bacterial infections. Drugs. 2019;79:243–269. doi: 10.1007/s40265-019-1054-3. - DOI - PubMed
  21.  
    1. Ahmed N., Khalid H., Mushtaq M., Basha S., Rabaan A.A., Garout M., Halwani M.A., Al Mutair A., Alhumaid S., Al Alawi Z. The Molecular Characterization of Virulence Determinants and Antibiotic Resistance Patterns in Human Bacterial Uropathogens. Antibiotics. 2022;11:516. doi: 10.3390/antibiotics11040516. - DOI - PMC - PubMed
  22.  
    1. Zahra N., Zeshan B., Qadri M.M.A., Ishaq M., Afzal M., Ahmed N. Phenotypic and genotypic evaluation of antibiotic resistance of Acinetobacter baumannii bacteria isolated from surgical intensive care unit patients in Pakistan. Jundishapur. J. Microbiol. 2021;14:e113008. doi: 10.5812/jjm.113008. - DOI
  23.  
    1. US Centers for Disease Control and Prevention (CDC) Facility Guidance for Control of Carbapenem-Resistant Enterobacterales(CRE)—November 2015 Update CRE Toolkit. [(accessed on 4 June 2016)]; Available online: http://www.cdc.gov/hai/organisms/cre/cre-toolkit/
  24.  
    1. National Institute of Allergy and Infectious Diseases (NIAID) NIAID’s Antibacterial Resistance Program: Current Status and Future Directions 2014. [(accessed on 19 June 2017)]; Available online: https://www.niaid.nih.gov/sites/default/files/arstrategicplan2014.pdf.
  25.  
    1. Bush K. Proliferation and significance of clinically relevant β-lactamases. Ann. N. Y. Acad. Sci. 2013;1277:84–90. doi: 10.1111/nyas.12023. - DOI - PubMed
  26.  
    1. Schwaber M.J., Lev B., Israeli A., Solter E., Smollan G., Rubinovitch B., Shalit I., Carmeli Y. Containment of a country-wide outbreak of carbapenem-resistant Klebsiella pneumoniae in Israeli hospitals via a nationally implemented intervention. Clin. Infect. Dis. 2011;52:848–855. doi: 10.1093/cid/cir025. - DOI - PubMed
  27.  
    1. Kim Y., Cunningham M.A., Mire J., Tesar C., Sacchettini J., Joachimiak A. NDM-1, the ultimate promiscuous enzyme: Substrate recognition and catalytic mechanism. FASEB J. 2013;27:1917–1927. doi: 10.1096/fj.12-224014. - DOI - PMC - PubMed
  28.  
    1. US Centers for Disease Control and Prevention (CDC) Healthcare-associated infections (HAIs) Tracking CRE infections. [(accessed on 4 June 2016)]; Available online: http://www.cdc.gov/hai/organisms/cre/TrackingCRE.html#CREmap.
  29.  
    1. Gonçalves I.R., Ferreira M., Araujo B., Campos P., Royer S., Batistão D., Souza L., Brito C., Urzedo J., Gontijo-Filho P. Outbreaks of colistin-resistant and colistin susceptible KPC-producing Klebsiella pneumoniae in a Brazilian intensive care unit. J. Hosp. Infect. 2016;94:322–329. doi: 10.1016/j.jhin.2016.08.019. - DOI - PubMed
  30.  
    1. Ergönül Ö., Aydin M., Azap A., Başaran S., Tekin S., Kaya Ş., Gülsün S., Yörük G., Kurşun E., Yeşilkaya A. Healthcare-associated Gram-negative bloodstream infections: Antibiotic resistance and predictors of mortality. J Hosp. Infect. 2016;94:381–385. doi: 10.1016/j.jhin.2016.08.012. - DOI - PubMed
  31.  
    1. McGann P., Snesrud E., Maybank R., Corey B., Ong A.C., Clifford R., Hinkle M., Whitman T., Lesho E., Schaecher K.E. Escherichia coli harboring mcr-1 and blaCTX-M on a novel IncF plasmid: First report of mcr-1 in the USA. Antimicrob Agents Chemother. 2016;60:5107. doi: 10.1128/AAC.01353-16. - DOI - PMC - PubMed
  32.  
    1. Guh A.Y., Bulens S.N., Mu Y., Jacob J.T., Reno J., Scott J., Wilson L.E., Vaeth E., Lynfield R., Shaw K.M. Epidemiology of Carbapenem-Resistant Enterobacterales in 7 US Communities, 2012–2013. JAMA. 2015;314:1479–1487. doi: 10.1001/jama.2015.12480. - DOI - PMC - PubMed
  33.  
    1. Gohil S.K., Singh R., Chang J., Gombosev A., Tjoa T., Zahn M., Steger P., Huang S.S. Emergence of carbapenem-resistant Enterobacterales in Orange County, California, and support for early regional strategies to limit spread. Am. J. Infect. Control. 2017;45:1177–1182. doi: 10.1016/j.ajic.2017.06.004. - DOI - PMC - PubMed
  34.  
    1. Ray M.J., Lin M.Y., Weinstein R.A., Trick W.E. Spread of carbapenem-resistant Enterobacterales among Illinois healthcare facilities: The role of patient sharing. Clin. Infect. Dis. 2016;63:889–893. doi: 10.1093/cid/ciw461. - DOI - PMC - PubMed
  35.  
    1. Satlin M.J., Chen L., Patel G., Gomez-Simmonds A., Weston G., Kim A.C., Seo S.K., Rosenthal M.E., Sperber S.J., Jenkins S.G. Multicenter clinical and molecular epidemiological analysis of bacteremia due to carbapenem-resistant Enterobacterales (CRE) in the CRE epicenter of the United States. Antimicrob. Agents Chemother. 2017;61:e02349-16. doi: 10.1128/AAC.02349-16. - DOI - PMC - PubMed
  36.  
    1. Centers for Disease Control and Prevention Antibiotic Resistance Threats in the United States. [(accessed on 17 January 2018)];2013 Available online: http://www.cdc.gov/drugresistance/threat-report-2013/
  37.  
    1. Livorsi D.J., Chorazy M.L., Schweizer M.L., Balkenende E.C., Blevins A.E., Nair R., Samore M.H., Nelson R.E., Khader K., Perencevich E.N. A systematic review of the epidemiology of carbapenem-resistant Enterobacterales in the United States. Antimicrob. Resist. Infect. Control. 2018;7:55. doi: 10.1186/s13756-018-0346-9. - DOI - PMC - PubMed
  38.  
    1. Netikul T., Kiratisin P. Genetic characterization of carbapenem-resistant Enterobacterales and the spread of carbapenem-resistant Klebsiella pneumonia ST340 at a university hospital in Thailand. PLoS ONE. 2015;10:e0139116. doi: 10.1371/journal.pone.0139116. - DOI - PMC - PubMed
  39.  
    1. Chotiprasitsakul D., Srichatrapimuk S., Kirdlarp S., Pyden A.D., Santanirand P. Epidemiology of carbapenem-resistant Enterobacteriaceae: A 5-year experience at a tertiary care hospital. Infect. Drug Resist. 2019;12:461–468. doi: 10.2147/IDR.S192540. - DOI - PMC - PubMed
  40.  
    1. Wei Z.-Q., Du X.-X., Yu Y.-S., Shen P., Chen Y.-G., Li L.-J. Plasmid-mediated KPC-2 in a Klebsiella pneumoniae isolate from China. Antimicrob. Agents Chemother. 2007;51:763–765. doi: 10.1128/AAC.01053-06. - DOI - PMC - PubMed
  41.  
    1. Zhang R., Chan E.W.-c., Zhou H., Chen S. Prevalence and genetic characteristics of carbapenem-resistant Enterobacterales strains in China. Lancet Infect Dis. 2017;17:256–257. doi: 10.1016/S1473-3099(17)30072-5. - DOI - PubMed
  42.  
    1. Zhang Y., Wang Q., Yin Y., Chen H., Jin L., Gu B., Xie L., Yang C., Ma X., Li H. Epidemiology of Carbapenem-Resistant Enterobacterales Infections: Report from the China CRE Network. Antimicrob. Agents Chemother. 2018;62:e01882-17. doi: 10.1128/AAC.01882-17. - DOI - PMC - PubMed
  43.  
    1. Vergara-López S., Dominguez M., Conejo M., Pascual A., Rodriguez-Bano J. Lessons from an outbreak of metallo-beta-lactamase-producing Klebsiella oxytoca in an intensive care unit: The importance of time at risk and combination therapy. J. Hosp. Infect. 2015;89:123–131. doi: 10.1016/j.jhin.2013.12.008. - DOI - PubMed
  44.  
    1. Voulgari E., Gartzonika C., Vrioni G., Politi L., Priavali E., Levidiotou-Stefanou S., Tsakris A. The Balkan region: NDM-1-producing Klebsiella pneumoniae ST11 clonal strain causing outbreaks in Greece. J. Antimicrob. Chemother. 2014;69:2091–2097. doi: 10.1093/jac/dku105. - DOI - PubMed
  45.  
    1. Hrabák J., Walková R., Študentová V., Chudáčková E., Bergerová T. Carbapenemase-producing Klebsiella pneumoniae in the Czech Republic in 2011. Euro Surveill. 2013;18:20626. doi: 10.2807/1560-7917.ES2013.18.45.20626. - DOI - PubMed
  46.  
    1. Zweigner J., Gastmeier P., Kola A., Klefisch F.-R., Schweizer C., Hummel M.A. A carbapenem-resistant Klebsiella pneumoniae outbreak following bronchoscopy. Am. J. Infect. Control. 2014;42:936–937. doi: 10.1016/j.ajic.2014.04.022. - DOI - PubMed
  47.  
    1. Gharbi M., Moore L., Gilchrist M., Thomas C., Bamford K., Brannigan E., Holmes A. Forecasting carbapenem resistance from antimicrobial consumption surveillance: Lessons learnt from an OXA-48-producing Klebsiella pneumoniae outbreak in a West London renal unit. Int. J. Antimicrob. Agents. 2015;46:150–156. doi: 10.1016/j.ijantimicag.2015.03.005. - DOI - PMC - PubMed
  48.  
    1. Sambri V. Successful containment and infection control of a Carbapenem-resistant Klebsiella pneumoniae outbreak in an Italian hospital. New Microbiol. 2014;37:87–90. - PubMed
  49.  
    1. Brizendine K.D., Richter S.S., Cober E.D., van Duin D. Carbapenem-resistant Klebsiella pneumoniae urinary tract infection following solid organ transplantation. Antimicrob. Agents Chemother. 2015;59:553–557. doi: 10.1128/AAC.04284-14. - DOI - PMC - PubMed
  50.  
    1. Savard P., Perl T.M. Combating the spread of carbapenemases in Enterobacteriaceae: A battle that infection prevention should not lose. Clin. Microbiol. Infect. 2014;20:854–861. doi: 10.1111/1469-0691.12748. - DOI - PubMed
  51.  
    1. Ben-David D., Masarwa S., Navon-Venezia S., Mishali H., Fridental I., Rubinovitch B., Smollan G., Carmeli Y., Schwaber M.J., Israel P. Carbapenem-resistant Klebsiella pneumoniae in post-acute-care facilities in Israel. Infect. Control Hosp. Epidemiol. 2011;32:845–853. doi: 10.1086/661279. - DOI - PubMed
  52.  
    1. Nucleo E., Caltagirone M., Marchetti V.M., D’Angelo R., Fogato E., Confalonieri M., Reboli C., March A., Sleghel F., Soelva G. Colonization of long-term care facility residents in three Italian Provinces by multidrug-resistant bacteria. Antimicrob. Resist. Infect. Control. 2018;7:33. doi: 10.1186/s13756-018-0326-0. - DOI - PMC - PubMed
  53.  
    1. O’Connor M., Mc Namara C., Doody O. Healthcare workers’ experiences of caring for patients colonized with carbapenemase-producing Enterobacterales (CPE) in an acute hospital setting–A scoping review. J. Hosp. Infect. :2022. doi: 10.1016/j.jhin.2022.10.011. - DOI - PubMed
  54.  
    1. Ahmed N., Zeshan B., Naveed M., Afzal M., Mohamed M. Antibiotic resistance profile in relation to virulence genes fimH, hlyA and usp of uropathogenic E. coli isolates in Lahore, Pakistan. Trop. Biomed. 2019;36:559–568. - PubMed
  55.  
    1. Tischendorf J., de Avila R.A., Safdar N. Risk of infection following colonization with carbapenem-resistant Enterobactericeae: A systematic review. Am. J. Infect Control. 2016;44:539–543. doi: 10.1016/j.ajic.2015.12.005. - DOI - PMC - PubMed
  56.  
    1. Oren I., Sprecher H., Finkelstein R., Hadad S., Neuberger A., Hussein K., Raz-Pasteur A., Lavi N., Saad E., Henig I. Eradication of carbapenem-resistant Enterobacterales gastrointestinal colonization with nonabsorbable oral antibiotic treatment: A prospective controlled trial. Am. J. Infect. Control. 2013;41:1167–1172. doi: 10.1016/j.ajic.2013.04.018. - DOI - PubMed
  57.  
    1. Lübbert C., Lippmann N., Busch T., Kaisers U.X., Ducomble T., Eckmanns T., Rodloff A.C. Long-term carriage of Klebsiella pneumoniae carbapenemase-2-producing K pneumoniae after a large single-center outbreak in Germany. Am. J. Infect. Control. 2014;42:376–380. doi: 10.1016/j.ajic.2013.12.001. - DOI - PubMed
  58.  
    1. Kizny Gordon A.E., Mathers A.J., Cheong E.Y., Gottlieb T., Kotay S., Walker A.S., Peto T.E., Crook D.W., Stoesser N. The Hospital Water Environment as a Reservoir for Carbapenem-Resistant Organisms Causing Hospital-Acquired Infections-A Systematic Review of the Literature. Clin. Infect. Dis. 2017;64:1435–1444. doi: 10.1093/cid/cix132. - DOI - PubMed
  59.  
    1. Tofteland S., Naseer U., Lislevand J.H., Sundsfjord A., Samuelsen Ø. A long-term low-frequency hospital outbreak of KPC-producing Klebsiella pneumoniae involving Intergenus plasmid diffusion and a persisting environmental reservoir. PLoS ONE. 2013;8:e59015. doi: 10.1371/journal.pone.0059015. - DOI - PMC - PubMed
  60.  
    1. Weingarten R.A., Johnson R.C., Conlan S., Ramsburg A.M., Dekker J.P., Lau A.F., Khil P., Odom R.T., Deming C., Park M. Genomic Analysis of Hospital Plumbing Reveals Diverse Reservoir of Bacterial Plasmids Conferring Carbapenem Resistance. MBio. 2018;9:e02011-17. doi: 10.1128/mBio.02011-17. - DOI - PMC - PubMed
  61.  
    1. Conlan S., Thomas P.J., Deming C., Park M., Lau A.F., Dekker J.P., Snitkin E.S., Clark T.A., Luong K., Song Y. Single-molecule sequencing to track plasmid diversity of hospital-associated carbapenemase-producing Enterobacteriaceae. Sci. Transl. Med. 2014;6:254ra126. doi: 10.1126/scitranslmed.3009845. - DOI - PMC - PubMed
  62.  
    1. Viau R., Frank K.M., Jacobs M.R., Wilson B., Kaye K., Donskey C.J., Perez F., Endimiani A., Bonomo R.A. Intestinal carriage of Carbapenemase-producing organisms: Current status of surveillance methods. Clin. Microbiol. Rev. 2016;29:1–27. doi: 10.1128/CMR.00108-14. - DOI - PMC - PubMed
  63.  
    1. Averbuch D., Tridello G., Hoek J., Mikulska M., Akan H., Yaňez San Segundo L., Pabst T., Özçelik T., Klyasova G., Donnini I. Antimicrobial Resistance in Gram-Negative Rods Causing Bacteremia in Hematopoietic Stem Cell Transplant Recipients: Intercontinental Prospective Study of the Infectious Diseases Working Party of the European Bone Marrow Transplantation Group. Clin. Infect. Dis. 2017;65:1819–1828. doi: 10.1093/cid/cix646. - DOI - PubMed
  64.  
    1. Nour I., Eldegla H.E., Nasef N., Shouman B., Abdel-Hady H., Shabaan A.E. Risk factors and clinical outcomes for carbapenem-resistant Gram-negative late-onset sepsis in a neonatal intensive care unit. J. Hosp. Infect. 2017;97:52–58. doi: 10.1016/j.jhin.2017.05.025. - DOI - PubMed
  65.  
    1. European Centre for Disease Prevention and Control . Systematic Review of the Effectiveness of Infection Control Measures to prevent The Transmission of Carbapenemase-Producing Enterobacteralesthrough Cross-Border Transfer of Patients. ECDC; Stockholm, Sweden: 2014.
  66.  
    1. Fournier S., Desenfant L., Monteil C., Nion-Huang M., Richard C., Jarlier V. Efficiency of different control measures for preventing carbapenemase-producing enterobacteria and glycopeptide-resistant Enterococcus faecium outbreaks: A 6-year prospective study in a French multihospital institution, January 2010 to December 2015. Euro Surveill. 2018;23:17–78. doi: 10.2807/1560-7917.ES.2018.23.8.17-00078. - DOI - PMC - PubMed
  67.  
    1. World Health Organization . Guidelines for the Prevention and Control of Carbapenem-Resistant Enterobacteriaceae, Acinetobacter baumannii and Pseudomonas aeruginosa in Health Care Facilities. World Health Organization; Geneva, Switzerland: 2017. - PubMed
  68.  
    1. Manges A.R., Johnson J.R. Food-borne origins of Escherichia coli causing extraintestinal infections. Clin. Infect. Dis. 2012;55:712–719. doi: 10.1093/cid/cis502. - DOI - PubMed
  69.  
    1. Kluytmans J.A., Overdevest I.T., Willemsen I., Kluytmans-Van Den Bergh M.F., Van Der Zwaluw K., Heck M., Rijnsburger M., Vandenbroucke-Grauls C.M., Savelkoul P.H., Johnston B.D. Extended-spectrum beta-lactamase-producing Escherichia coli from retail chicken meat and humans: Comparison of strains, plasmids, resistance genes, and virulence factors. Clin. Infect. Dis. 2013;56:478–487. doi: 10.1093/cid/cis929. - DOI - PubMed
  70.  
    1. Kola A., Kohler C., Pfeifer Y., Schwab F., Kühn K., Schulz K., Balau V., Breitbach K., Bast A., Witte W. High prevalence of extended-spectrum-beta-lactamase-producing Enterobacterales in organic and conventional retail chicken meat, Germany. J. Antimicrob. Chemother. 2012;67:2631–2634. doi: 10.1093/jac/dks295. - DOI - PubMed
  71.  
    1. Zarfel G., Galler H., Luxner J., Petternel C., Reinthaler F.F., Haas D., Kittinger C., Grisold A.J., Pless P., Feierl G. Multiresistant bacteria isolated from chicken meat in Austria. Int. J. Environ. Res. Public Health. 2014;11:12582–12593. doi: 10.3390/ijerph111212582. - DOI - PMC - PubMed
  72.  
    1. Ghodousi A., Bonura C., Di Noto A.M., Mammina C. Extended-Spectrum ss-Lactamase, AmpC-Producing, and Fluoroquinolone-Resistant Escherichia coli in retail broiler chicken meat, Italy. Foodborne Pathog. Dis. 2015;12:619–625. doi: 10.1089/fpd.2015.1936. - DOI - PubMed
  73.  
    1. Egea P., López-Cerero L., Torres E., del Carmen Gómez-Sánchez M., Serrano L., Sánchez-Ortiz M.D.N., Rodriguez-Baño J., Pascual A. Increased raw poultry meat colonization by extended spectrum beta-lactamase-producing Escherichia coli in the south of Spain. Int. J. Food Microbiol. 2012;159:69–73. doi: 10.1016/j.ijfoodmicro.2012.08.002. - DOI - PubMed
  74.  
    1. van Hoek A.H., Veenman C., van Overbeek W.M., Lynch G., de Roda Husman A.M., Blaak H. Prevalence and characterization of ESBL- and AmpC-producing Enterobacterales on retail vegetables. Int. J. Food Microbiol. 2015;204:1–8. doi: 10.1016/j.ijfoodmicro.2015.03.014. - DOI - PubMed
  75.  
    1. Woodford N., Wareham D.W., Guerra B., Teale C. Carbapenemase-producing Enterobacterales and non-Enterobacterales from animals and the environment: An emerging public health risk of our own making? J. Antimicrob. Chemother. 2014;69:287–291. doi: 10.1093/jac/dkt392. - DOI - PubMed
  76.  
    1. Akiba M., Sekizuka T., Yamashita A., Kuroda M., Fujii Y., Murata M., Lee K.-i., Joshua D.I., Balakrishna K., Bairy I. Distribution and relationships of antimicrobial resistance determinants among extended-spectrum cephalosporin or carbapenem-resistant Escherichia coli isolated from rivers and sewage treatment plants in India. Antimicrob. Agents Chemother. 2016;60:2972–2980. doi: 10.1128/AAC.01950-15. - DOI - PMC - PubMed
  77.  
    1. Kieffer N., Poirel L., Bessa L.J., Barbosa-Vasconcelos A., da Costa P.M., Nordmann P. VIM-1, VIM-34, and IMP-8 Carbapenemase-Producing Escherichia coli Strains Recovered from a Portuguese River. Antimicrob Agents Chemother. 2016;60:2585–2586. doi: 10.1128/AAC.02632-15. - DOI - PMC - PubMed
  78.  
    1. Köck R., Daniels-Haardt I., Becker K., Mellmann A., Friedrich A.W., Mevius D., Schwarz S., Jurke A. Carbapenem-resistant Enterobacterales in wildlife, food-producing and companion animals—A systematic review. Clin. Microbiol. Infect. 2018;24:1241–1250. doi: 10.1016/j.cmi.2018.04.004. - DOI - PubMed
  79.  
    1. Salomão M.C., Maristela P.F., Levin Anna S.S. Patients with carbapenem-resistant Enterobacteriaceae in emergency room; is this a real problem? Future Microbiol. 2019;14:1527–1530. doi: 10.2217/fmb-2019-0263. - DOI - PubMed
  80.  
    1. Kotb S., Lyman M., Ismail G., Abd El Fattah M., Girgis S.A., Etman A., Hafez S., El-Kholy J., Zaki M.E., Hebat-allah G.R., et al. Epidemiology of carbapenem-resistant Enterobacteriaceae in Egyptian intensive care units using National Healthcare–associated Infections Surveillance Data, 2011–2017. Antimicrob. Resist. Infect. Control. 2020;9:1–9. doi: 10.1186/s13756-019-0639-7. - DOI - PMC - PubMed
  81.  
    1. Castanheira M., Deshpande L.M., Mendes R.E., Canton R., Sader H.S., Jones R.N. Variations in the occurrence of resistance phenotypes and carbapenemase genes among Enterobacteriaceae isolates in 20 years of the SENTRY antimicrobial surveillance program. Open Forum Infect. Dis. 2019;6:S23–S33. doi: 10.1093/ofid/ofy347. - DOI - PMC - PubMed
  82.  
    1. Friedman N.D., Carmeli Y., Walton A.L., Schwaber M.J. Carbapenem-resistant Enterobacteriaceae: A strategic roadmap for infection control. Infect. Control Hosp. Epidemiol. 2017;38:580–594. doi: 10.1017/ice.2017.42. - DOI - PubMed
  83.  
    1. Potter R.F., D’Souza A.W., Dantas G. The rapid spread of carbapenem-resistant Enterobacteriaceae. Drug Resist. Updat. 2016;29:30–46. doi: 10.1016/j.drup.2016.09.002. - DOI - PMC - PubMed
  84.  
    1. Bonnin R.A., Jousset A.B., Emeraud C., Oueslati S., Dortet L., Naas T. Genetic diversity, biochemical properties, and detection methods of minor carbapenemases in Enterobacterales. Front. Med. 2021;7:1061. doi: 10.3389/fmed.2020.616490. - DOI - PMC - PubMed
  85.  
    1. Caltagirone M., Nucleo E., Spalla M., Zara F., Novazzi F., Marchetti V.M., Piazza A., Bitar I., De Cicco M., Paolucci S. Occurrence of extended spectrum β-lactamases, KPC-type, and MCR-1.2-producing Enterobacteriaceae from wells, river water, and wastewater treatment plants in Oltrepo Pavese area, northern Italy. Front. Microbiol. 2017;8:1–12. doi: 10.3389/fmicb.2017.02232. - DOI - PMC - PubMed
  86.  
    1. Kelly A.M., Mathema B., Larson E.L. Carbapenem-resistant Enterobacteriaceae in the community: A scoping review. Int. J. Antimicrob. Agents. 2017;50:127–134. doi: 10.1016/j.ijantimicag.2017.03.012. - DOI - PMC - PubMed
  87.  
    1. Bartley P.S., Domitrovic T.N., Moretto V.T., Santos C.S., Ponce-Terashima R., Reis M.G., Barbosa L.M., Blanton R.E., Bonomo R.A., Perez F. Antibiotic resistance in Enterobacteriaceae from surface waters in urban Brazil highlights the risks of poor sanitation. Am. J. Trop. Med. Hyg. 2019;100:1369–1377. - PMC - PubMed
  88.  
    1. Ahmed N., Tahir K., Aslam S., Cheema S.M., Rabaan A.A., Turkistani S.A., Garout M., Halwani M.A., Aljeldah M., Al Shammari B.R., et al. Heavy Metal (Arsenic) Induced Antibiotic Resistance among Extended-Spectrum β-Lactamase (ESBL) Producing Bacteria of Nosocomial Origin. Pharmaceuticals. 2022;15:1426. doi: 10.3390/ph15111426. - DOI - PMC - PubMed
  89.  
    1. Kost K., Yi J., Rogers B., Jerris R. Comparison of clinical methods for detecting carbapenem-resistant Enterobacteriaceae. Pract. Lab. Med. 2017;8:18–25. doi: 10.1016/j.plabm.2017.03.002. - DOI - PMC - PubMed
  90.  
    1. Al-Zahrani I.A. Routine detection of carbapenem-resistant gram-negative bacilli in clinical laboratories. A review of current challenge. Saudi Med. J. 2018;39:861–872. doi: 10.15537/smj.2018.9.22840. - DOI - PMC - PubMed
  91.  
    1. Kruse E.B., Aurbach U., Wisplinghoff H. Carbapenem-Resistant Enterobacteriaceae: Laboratory Detection and Infection Control Practices. Curr. Infect. Dis. Rep. 2013:12. doi: 10.1007/s11908-013-0373-x. - DOI - PubMed
  92.  
    1. Banerjee R., Humphries R. Clinical and laboratory considerations for the rapid detection of carbapenem-resistant Enterobacteriaceae. Virulence. 2017;8:427–439. doi: 10.1080/21505594.2016.1185577. - DOI - PMC - PubMed
  93.  
    1. EUCAST The European Committee on Antimicrobial Susceptibility Testing. Breakpoint Tables for Interpretation of MICs and Zone Diameters. Version 8.0. 2018. [(accessed on 16 March 2022)]. Available online: http://www.eucast.org.
  94.  
    1. Richter S.S., Marchaim D. Screening for carbapenem-resistant Enterobacteriaceae: Who, When, and How? Virulence. 2017;8:417–426. doi: 10.1080/21505594.2016.1255381. - DOI - PMC - PubMed
  95.  
    1. CLSI (Clinical Laboratory Standards Institute) Performance Standards for Antimicrobial Susceptibilty Testing, Supplement, M100S28. 28th ed. Clinical Laboratory Standards Institute; Wayne, PA, USA: 2018.
  96.  
    1. Karlsson M., Lutgring J.D., Ansari U., Lawsin A., Albrecht V., McAllister G., Daniels J., Lonsway D., McKay S.L., Beldavs Z. Molecular characterization of carbapenem-resistant Enterobacterales collected in the United States. Microbial Drug Resistance. 2022;28:389–397. doi: 10.1089/mdr.2021.0106. - DOI - PubMed
  97.  
    1. Van Dijk K., Voets G., Scharringa J., Voskuil S., Fluit A., Rottier W., Leverstein-Van Hall M., Stuart J.C. A disc diffusion assay for detection of class A, B and OXA-48 carbapenemases in Enterobacterales using phenyl boronic acid, dipicolinic acid and temocillin. Clin. Microbiol. Infect. 2014;20:345–349. doi: 10.1111/1469-0691.12322. - DOI - PubMed
  98.  
    1. Al-Zahrani I.A., Alsiri B.A. The emergence of carbapenem resistant Klebsiella pneumoniae isolates producing OXA-48 and NDM in the Southern (Asir) province, Saudi Arabia. Saudi Med. J. 2018;39:23–30. doi: 10.15537/smj.2018.1.21094. - DOI - PMC - PubMed
  99.  
    1. Doyle D., Peirano G., Lascols C., Lloyd T., Church D.L., Pitout J.D. Laboratory detection of Enterobacterales that produce carbapenemases. J. Clin. Microbiol. 2012;50:3877–3880. doi: 10.1128/JCM.02117-12. - DOI - PMC - PubMed
  100.  
    1. Tsakris A., Poulou A., Bogaerts P., Dimitroulia E., Pournaras S., Glupczynski Y. Evaluation of a new phenotypic OXA-48 disk test for differentiation of OXA-48 carbapenemase-producing Enterobacterales clinical isolates. J. Clin. Microbiol. 2015;53:1245–1251. doi: 10.1128/JCM.03318-14. - DOI - PMC - PubMed
  101.  
    1. Simner P.J., Martin I., Opene B., Tamma P.D., Carroll K.C., Milstone A.M. Evaluation of Multiple Methods for Detection of Gastrointestinal Colonization of Carbapenem-Resistant Organisms from Rectal Swabs. J. Clin. Microbiol. 2016;54:1664–1667. doi: 10.1128/JCM.00548-16. - DOI - PMC - PubMed
  102.  
    1. Zarakolu P., Day K., Sidjabat H., Kamolvit W., Lanyon C., Cummings S., Paterson D., Akova M., Perry J. Evaluation of a new chromogenic medium, chromID OXA-48, for recovery of carbapenemase producing Enterobacterales from patients at a university hospital in Turkey. Eur. J. Clin. Microbiol. Infect. Dis. 2015;34:519–525. doi: 10.1007/s10096-014-2255-z. - DOI - PubMed
  103.  
    1. Girlich D., Poirel L., Nordmann P. Comparison of the SUPERCARBA, CHROM agar KPC, and Brilliance CRE screening media for detection of Enterobacterales with reduced susceptibility to carbapenems. Diagn. Microbiol. Infect. Dis. 2013;75:214–217. doi: 10.1016/j.diagmicrobio.2012.10.006. - DOI - PubMed
  104.  
    1. Garcia-Quintanilla M., Poirel L., Nordmann P. CHROMagar mSuperCARBA and RAPIDECR Carba NP test for detection of carbapenemase-producing Enterobacteriaceae. Diagn. Microbiol. Infect. Dis. 2018;90:77–80. doi: 10.1016/j.diagmicrobio.2017.10.009. - DOI - PubMed
  105.  
    1. Gniadek T.J., Carroll K.C., Simner P.J. Carbapenem-Resistant Non-Glucose-Fermenting Gram-Negative Bacilli: The Missing Piece to the Puzzle. J. Clin. Microbiol. 2016;54:1700–1710. doi: 10.1128/JCM.03264-15. - DOI - PMC - PubMed
  106.  
    1. Lutgring J.D., Limbago B.M. The Problem of Carbapenemase- Producing-Carbapenem-Resistant-Enterobacterales Detection. J. Clin. Microbiol. 2016;54:529–534. doi: 10.1128/JCM.02771-15. - DOI - PMC - PubMed
  107.  
    1. Shinde S., Gupta R., Raut S.S., Nataraj G., Mehta P.R. Carba NP as a simpler, rapid, cost-effective, and a more sensitive alternative to other phenotypic tests for detection of carbapenem resistance in routine diagnostic laboratories. J. Lab. Physicians. 2017;9:100–103. doi: 10.4103/0974-2727.199628. - DOI - PMC - PubMed
  108.  
    1. Papagiannitsis C.C., Študentová V., Izdebski R., Oikonomou O., Pfeifer Y., Petinaki E., Hrabák J. Matrix-assisted laser desorption ionization-time of flight mass spectrometry meropenem hydrolysis assay with NH4HCO3, a reliable tool for direct detection of carbapenemase activity. J. Clin. Microbiol. 2015;53:1731–1735. doi: 10.1128/JCM.03094-14. - DOI - PMC - PubMed
  109.  
    1. Yamada K., Kashiwa M., Arai K., Nagano N., Saito R. Comparison of the Modified-Hodge test, Carba NP test, and carbapenem inactivation method as screening methods for carbapenemase producing Enterobacteriaceae. J. Microbiol. Methods. 2016;128:48–51. doi: 10.1016/j.mimet.2016.06.019. - DOI - PubMed
  110.  
    1. Glupczynski Y., Evrard S., Ote I., Mertens P., Huang T.-D., Leclipteux T., Bogaerts P. Evaluation of two new commercial immunochromatographic assays for the rapid detection of OXA-48 and KPC carbapenemases from cultured bacteria. J. Antimicrob. Chemother. 2016;71:1217–1222. doi: 10.1093/jac/dkv472. - DOI - PubMed
  111.  
    1. Wareham D.W., Phee L.M., Abdul Momin M.H.F. Direct detection of carbapenem resistance determinants in clinical specimens using immunochromatographic lateral flow devices. J. Antimicrob. Chemother. 2018;73:1997–1998. doi: 10.1093/jac/dky095. - DOI - PubMed
  112.  
    1. Hrabak J., Chudackova E., Walkova R. Matrix-assisted laser desorption ionization-time of flight (maldi-tof) mass spectrometry for detection of antibiotic resistance mechanisms: From research to routine diagnosis. Clin. Microbiol. Rev. 2013;26:103–114. doi: 10.1128/CMR.00058-12. - DOI - PMC - PubMed
  113.  
    1. Hrabák J., Walková R., Študentová V., Chudáčková E., Bergerová T. Carbapenemase activity detection by matrix-assisted laser desorption ionization-time of flight mass spectrometry. J. Clin. Microbiol. 2011;49:3222–3227. doi: 10.1128/JCM.00984-11. - DOI - PMC - PubMed
  114.  
    1. Hrabak J., Chudackova E., Papagiannitsis C.C. Detection of carbapenemases in Enterobacteriaceae: A challenge for diagnostic microbiological laboratories. Clin. Microbiol. Infect. 2014;20:839–853. doi: 10.1111/1469-0691.12678. - DOI - PubMed
  115.  
    1. Poirel L., Walsh T.R., Cuvillier V., Nordmann P. Multiplex PCR for detection of acquired carbapenemase genes. Diagn. Microbiol. Infect. Dis. 2011;70:119–123. doi: 10.1016/j.diagmicrobio.2010.12.002. - DOI - PubMed
  116.  
    1. Anandan S., Damodaran S., Gopi R., Bakthavatchalam Y.D., Veeraraghavan B. Rapid Screening for Carbapenem Resistant Organisms: Current Results and Future Approaches. J. Clin. Diagn Res. 2015;9:DM01–DM03. - PMC - PubMed
  117.  
    1. Lindsay J.A. Staphylococci. In: Ivano de Filippis M.M., editor. Molecular Typing in Bacterial Infections. Springer; New York, NY, USA: 2013. pp. 385–406.
  118.  
    1. McNicholas S., Shore A.C., Coleman D.C., Humphreys H., Hughes D.F. DNA microarray genotyping and virulence and antimicrobial resistance gene profiling of methicillin-resistant Staphylococcus aureus bloodstream isolates from renal patients. J. Clin. Microbiol. 2011;49:4349–4351. doi: 10.1128/JCM.05017-11. - DOI - PMC - PubMed
  119.  
    1. Leekitcharoenphon P., Nielsen E.M., Kaas R.S., Lund O., Aarestrup F.M. Evaluation of whole genome sequencing for outbreak detection of Salmonella enterica. PLoS ONE. 2014;9:e87991. doi: 10.1371/journal.pone.0087991. - DOI - PMC - PubMed
  120.  
    1. Köser C.U., Holden M.T., Ellington M.J., Cartwright E.J., Brown N.M., Ogilvy-Stuart A.L., Hsu L.Y., Chewapreecha C., Croucher N.J., Harris S.R. Rapid whole-genome sequencing for investigation of a neonatal MRSA outbreak. N. Engl. J. Med. 2012;366:2267–2275. doi: 10.1056/NEJMoa1109910. - DOI - PMC - PubMed

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