The emergence of carbapenemase bla NDM genotype among carbapenem-resistant Enterobacteriaceae isolates from Egyptian cancer patients
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Date
2020-02
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Article
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Springer
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European Journal of Clinical Microbiology and Infectious Diseases;
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Abstract
Carbapenem resistance among Enterobacteriaceae is a major concern that is increasingly reported worldwide. The objective of this study is to determine the incidence of carbapenem resistance as well as to investigate for carbapenemase-encoding genes among Enterobacteriaceae clinical isolates from cancer patients at different cancer institutes in Egypt. This determination was a cross-sectional study with a total of 135 clinical isolates collected over a period of 1 year. All isolates were sub-cultured on ChromID agar and subjected to phenotypic and molecular detection of carbapenemases. Most of the Enterobacteriaceae isolates were MDR with high resistance rates against tested antimicrobials. Overall, the results of PCR assays revealed that 89.62% (121/135) of isolates harbored one or more of the carbapenemase-encoding genes, while phenotypic assays revealed the production of carbapenemases in 68.88% (93/135) of isolates. BlastN analysis against the non-redundant genome sequences available in the GenBank database revealed that the blaNDM-1 gene was the most prevalent genotype of carbapenemases in 93/135 (68.88%), followed by blaOXA-48 44/135 (32.59%), blaOXA-23 42/135 (31.11%), and blaKPC-2 2/135 (1.48%). Klebsiella pneumoniae isolates harbored the highest number of carbapenemase-encoding genes 34/121 (28.09%). The high prevalence of carbapenemases and/or their encoding genes among MDR Enterobacteriaceae bacteria in Egypt is alarming, thus, the management of serious infections caused by Enterobacteriaceae, particularly in cancer patients will be challenging to clinicians. Carbapenemase blaNDM genotype is emerging in cancer healthcare settings in Egypt, which could be the cause of the current increase in carbapenemase-producing Enterobacteriaceae. © 2020, Springer-Verlag GmbH Germany, part of Springer Nature.
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Keywords
university of Resistance, MDR, Enterobacteriaceae, Carbapenemases, Cancer patients, blaNDM
Citation
Nordmann, P., Dortet, L., Poirel, L. Carbapenem resistance in Enterobacteriaceae: Here is the storm! (2012) Trends in Molecular Medicine, 18 (5), pp. 263-272. Cited 460 times. doi: 10.1016/j.molmed.2012.03.003 View at Publisher 2 Nordmann, P., Naas, T., Poirel, L. Global spread of carbapenemase producing Enterobacteriaceae (Open Access) (2011) Emerging Infectious Diseases, 17 (10), pp. 1791-1798. Cited 1232 times. http://wwwnc.cdc.gov/eid/article/17/10/pdfs/11-0655.pdf doi: 10.3201/eid1710.110655 View at Publisher 3 Paterson, D.L. Resistance in gram-negative bacteria: Enterobacteriaceae (2006) American Journal of Infection Control, 34 (5 SUPPL.), pp. S20-S28. Cited 129 times. doi: 10.1016/j.ajic.2006.05.238 View at Publisher 4 Ghaith, D.M., Zafer, M.M., Said, H.M., Elanwary, S., Elsaban, S., Al-Agamy, M.H., Bohol, M.F.F., (...), Al-Ahdal, M.N. Genetic diversity of carbapenem-resistant Klebsiella Pneumoniae causing neonatal sepsis in intensive care unit, Cairo, Egypt (2019) European Journal of Clinical Microbiology and Infectious Diseases link.springer.de/link/service/journals/10096/index.htm doi: 10.1007/s10096-019-03761-2 View at Publisher 5 Mushi, M.F., Mshana, S.E., Imirzalioglu, C., Bwanga, F. Carbapenemase genes among multidrug resistant gram negative clinical isolates from a tertiary hospital in Mwanza, Tanzania (Open Access) (2014) BioMed Research International, 2014, art. no. 303104. Cited 31 times. doi: 10.1155/2014/303104 View at Publisher 6 Moquet, O., Bouchiat, C., Kinana, A., Seck, A., Arouna, O., Bercion, R., Breurec, S., (...), Garin, B. Class D OXA-48 Carbapenemase in Multidrug-Resistant Enterobacteria, Senegal (Open Access) (2011) Emerging Infectious Diseases, 17 (1), pp. 143-144. Cited 53 times. http://www.cdc.gov/eid/content/17/1/pdfs/143.pdf doi: 10.3201/eid1701.100244 View at Publisher 7 Karuniawati, A., Saharman, Y.R., Lestari, D.C. Detection of carbapenemase encoding genes in Enterobacteriace, Pseudomonas aeruginosa, and Acinetobacter baumanii isolated from patients at Intensive Care Unit Cipto Mangunkusumo Hospital in 2011. (2013) Acta medica Indonesiana, 45 (2), pp. 101-106. Cited 31 times. 8 Abdulall, A.K., Tawfick, M.M., El Manakhly, A.R., El Kholy, A. Carbapenem-resistant Gram-negative bacteria associated with catheter-related bloodstream infections in three intensive care units in Egypt (2018) European Journal of Clinical Microbiology and Infectious Diseases, 37 (9), pp. 1647-1652. Cited 5 times. link.springer.de/link/service/journals/10096/index.htm doi: 10.1007/s10096-018-3294-7 View at Publisher 9 Bratu, S., Landman, D., Haag, R., Recco, R., Eramo, A., Alam, M., Quale, J. Rapid spread of carbapenem-resistant Klebsiella pneumoniae in New York City: A new threat to our antibiotic armamentarium (Open Access) (2005) Archives of Internal Medicine, 165 (12), pp. 1430-1435. Cited 456 times. http://archinte.ama-assn.org/cgi/reprint/165/12/1430.pdf doi: 10.1001/archinte.165.12.1430 View at Publisher 10 Queenan, A.M., Bush, K. Carbapenemases: The versatile β-lactamases (Open Access) (2007) Clinical Microbiology Reviews, 20 (3), pp. 440-458. Cited 1361 times. doi: 10.1128/CMR.00001-07 View at Publisher 11 Miriagou, V., Cornaglia, G., Edelstein, M., Galani, I., Giske, C.G., Gniadkowski, M., Malamou-Lada, E., (...), Cantón, R. Acquired carbapenemases in Gram-negative bacterial pathogens: Detection and surveillance issues (Open Access) (2010) Clinical Microbiology and Infection, 16 (2), pp. 112-122. Cited 244 times. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1469-0691 doi: 10.1111/j.1469-0691.2009.03116.x View at Publisher 12 Huang, T.-D., Poirel, L., Bogaerts, P., Berhin, C., Nordmann, P., Glupczynski, Y. Temocillin and piperacillin/tazobactam resistance by disc diffusion as antimicrobial surrogate markers for the detection of carbapenemase-producing enterobacteriaceae in geographical areas with a high prevalence of OXA-48 producers (Open Access) (2014) Journal of Antimicrobial Chemotherapy, 69 (2), art. no. dkt367, pp. 445-450. Cited 66 times. doi: 10.1093/jac/dkt367 View at Publisher 13 Nordmann, P., Gniadkowski, M., Giske, C.G., Poirel, L., Woodford, N., Miriagou, V., Akova, M., (...), Cornaglia, G. Identification and screening of carbapenemase-producing Enterobacteriaceae (Open Access) (2012) Clinical Microbiology and Infection, 18 (5), pp. 432-438. Cited 221 times. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1469-0691 doi: 10.1111/j.1469-0691.2012.03815.x View at Publisher 14 (2016) Performance Standards for Antimicrobial Susceptibility Testing CLSI Supplement M100S. Cited 419 times. 15 Pasteran, F., Mendez, T., Guerriero, L., Rapoport, M., Corso, A. Sensitive screening tests for suspected class A carbapenemase production in species of Enterobacteriaceae (Open Access) (2009) Journal of Clinical Microbiology, 47 (6), pp. 1631-1639. Cited 145 times. http://jcm.asm.org/cgi/reprint/47/6/1631 doi: 10.1128/JCM.00130-09 View at Publisher 16 Tsakris, A., Kristo, I., Poulou, A., Markou, F., Ikonomidis, A., Pournaras, S. First occurrence of KPC-2-possessing Klebsiella pneumoniae in a Greek hospital and recommendation for detection with boronic acid disc tests (Open Access) (2008) Journal of Antimicrobial Chemotherapy, 62 (6), pp. 1257-1260. Cited 67 times. doi: 10.1093/jac/dkn364 View at Publisher 17 Kaore, N., Nagdeo, N., Thombare, V. Phenotypic methods for detection of various β-lactamases in Gram-negative clinical isolates: need of the hour (2012) Chronicles Young Sci, 3, p. 292. Cited 6 times. 18 Pournaras, S., Poulou, A., Tsakris, A. Inhibitor-based methods for the detection of KPC carbapenemase- producing Enterobacteriaceae in clinical practice by using boronic acid compounds (Open Access) (2010) Journal of Antimicrobial Chemotherapy, 65 (7), art. no. dkq124, pp. 1319-1321. Cited 58 times. http://jac.oxfordjournals.org/ doi: 10.1093/jac/dkq124 View at Publisher 19 Bakthavatchalam, Y.D., Veeraraghavan, B., Peter, J.V., Rajinikanth, J., Inbanathan, F.Y., Devanga Ragupathi, N.K., Rajamani Sekar, S.K. Novel observations in 11 heteroresistant vancomycin-intermediate methicillin-resistant Staphylococcus aureus strains from South India (Open Access) (2016) Genome Announcements, 4 (6), art. no. e0142516. Cited 2 times. http://genomea.asm.org/content/4/6/e01425-16.full.pdf doi: 10.1128/genomeA.01425-16 View at Publisher 20 Kabir, M.I., Rahman, Md.B., Smith, W., Lusha, M.A.F., Azim, S., Milton, A.H. Knowledge and perception about climate change and human health: Findings from a baseline survey among vulnerable communities in Bangladesh (Open Access) (2016) BMC Public Health, 16 (1), art. no. 2930. Cited 18 times. http://www.biomedcentral.com/bmcpublichealth doi: 10.1186/s12889-016-2930-3 View at Publisher 21 Maurer, A., Draba, V., Jiang, Y., Schnaithmann, F., Sharma, R., Schumann, E., Kilian, B., (...), Pillen, K. Modelling the genetic architecture of flowering time control in barley through nested association mapping (Open Access) (2015) BMC Genomics, 16 (1), art. no. 290. Cited 69 times. http://www.biomedcentral.com/bmcgenomics doi: 10.1186/s12864-015-1459-7 View at Publisher 22 Pitout, J.D.D., Nordmann, P., Poirel, L. Carbapenemase-producing Klebsiella pneumoniae, a key pathogen set for global nosocomial dominance (Open Access) (2015) Antimicrobial Agents and Chemotherapy, 59 (10), pp. 5873-5884. Cited 251 times. http://aac.asm.org/content/59/10/5873.full.pdf+html doi: 10.1128/AAC.01019-15 View at Publisher 23 Hrabák, J., Chudáčková, E., Papagiannitsis, C.C. Detection of carbapenemases in Enterobacteriaceae: A challenge for diagnostic microbiological laboratories (Open Access) (2014) Clinical Microbiology and Infection, 20 (9), pp. 839-853. Cited 119 times. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1469-0691 doi: 10.1111/1469-0691.12678 View at Publisher 24 Huang, M., Parker, M.J., Stubbe, J. Choosing the right metal: Case studies of class i ribonucleotide reductases (Open Access) (2014) Journal of Biological Chemistry, 289 (41), pp. 28104-28111. Cited 21 times. http://www.jbc.org/content/289/41/28104.full.pdf+html doi: 10.1074/jbc.R114.596684 View at Publisher 25 Van Der Zee, H.H., Jemec, G.B.E. New insights into the diagnosis of hidradenitis suppurativa: Clinical presentations and phenotypes (2015) Journal of the American Academy of Dermatology, 73 (5), pp. S23-S26. Cited 64 times. http://www.elsevier.com/inca/publications/store/6/2/3/3/7/0/index.htt doi: 10.1016/j.jaad.2015.07.047 View at Publisher 26 Maulana, F., Ayalew, H., Anderson, J.D., Kumssa, T.T., Huang, W., Ma, X.-F. Genome-wide association mapping of seedling heat tolerance in winter wheat (Open Access) (2018) Frontiers in Plant Science, 9, art. no. 1272. Cited 4 times. https://www.frontiersin.org/journals/plant-science doi: 10.3389/fpls.2018.01272 View at Publisher 27 Liao, Q., Xie, Y., Wang, C., Zong, Z., Wu, S., Liu, Y., Zhang, W., (...), Kang, M. Development and evaluation of the method for detecting metallo-carbapenemases among carbapenemase-producing Enterobacteriaceae (2019) Journal of Microbiological Methods, 163, art. no. 105652. www.elsevier.com/locate/jmicmeth doi: 10.1016/j.mimet.2019.105652 View at Publisher 28 Abd El-Hamid, M.I., Bendary, M.M., Merwad, A.M.A., Elsohaby, I., Mohammad Ghaith, D., Alshareef, W.A. What is behind phylogenetic analysis of hospital-, community- and livestock-associated methicillin-resistant Staphylococcus aureus? (2019) Transboundary and Emerging Diseases, 66 (4), pp. 1506-1517. Cited 2 times. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1865-1682 doi: 10.1111/tbed.13170 View at Publisher 29 Bendary, M.M., Solyman, S.M., Azab, M.M., Mahmoud, N.F., Hanora, A.M. Characterization of methicillin resistant staphylococcus aureus isolated from human and animal samples in Egypt (2016) Cellular and Molecular Biology, 62 (2), pp. 94-100. http://www.cellmolbiol.com/admin/articles_generaux/cmb2016.62.2.16.pdf doi: 10.14715/cmb/2016.62.2.16 View at Publisher 30 Grundmann, H., Glasner, C., Albiger, B., Aanensen, D.M., Tomlinson, C.T., Andrasević, A.T., Cantón, R., (...), Adler, A. Occurrence of carbapenemase-producing Klebsiella pneumoniae and Escherichia coli in the European survey of carbapenemase-producing Enterobacteriaceae (EuSCAPE): a prospective, multinational study (2017) The Lancet Infectious Diseases, 17 (2), pp. 153-163. Cited 171 times. http://www.journals.elsevier.com/the-lancet-infectious-diseases doi: 10.1016/S1473-3099(16)30257-2 View at Publisher 31 Health service coverage (2014) World health statistics 2014, pp. 104-115. WHO Press, Geneva 32 Kádár, B., Kocsis, B., Tóth, A., Damjanova, I., Szász, M., Kristóf, K., Nagy, K., (...), Szabó, D. Synergistic antibiotic combinations for colistin-resistant Klebsiella pneumoniae (2013) Acta Microbiologica et Immunologica Hungarica, 60 (2), pp. 201-209. Cited 7 times. doi: 10.1556/AMicr.60.2013.2.10 View at Publisher 33 Baran, I., Aksu, N. Phenotypic and genotypic characteristics of carbapenem-resistant Enterobacteriaceae in a tertiary-level reference hospital in Turkey (Open Access) (2016) Annals of Clinical Microbiology and Antimicrobials, 15 (1), art. no. 20. Cited 23 times. http://www.ann-clinmicrob.com/start.asp doi: 10.1186/s12941-016-0136-2 View at Publisher 34 Rossi, B., Gasperini, M.L., Leflon-Guibout, V., Gioanni, A., de Lastours, V., Rossi, G., Dokmak, S., (...), Lefort, A. Hypervirulent klebsiella pneumoniae in cryptogenic liver abscesses, Paris, France (Open Access) (2018) Emerging Infectious Diseases, 24 (2), pp. 221-229. Cited 8 times. https://wwwnc.cdc.gov/eid/article/24/2/pdfs/17-0957.pdf doi: 10.3201/eid2402.170957 View at Publisher 35 Oduyebo, O., Falayi, O., Oshun, P., Ettu, A. Phenotypic determination of carbapenemase producing Enterobacteriaceae isolates from clinical specimens at a tertiary hospital in Lagos, Nigeria (2015) Niger Postgrad Med J, 22, p. 223. Cited 8 times. 36 Rudresh, S.M., Ravi, G.S., Sunitha, L., Hajira, S.N., Kalaiarasan, E., Harish, B.N. Simple, rapid, and cost-effective modified Carba NP test for carbapenemase detection among Gram-negative bacteria (2017) J Lab Physicians, 9, pp. 303-307. Cited 5 times. 37 AlTamimi, M., AlSalamah, A., AlKhulaifi, M., AlAjlan, H. Comparison of phenotypic and PCR methods for detection of carbapenemases production by Enterobacteriaceae (Open Access) (2017) Saudi Journal of Biological Sciences, 24 (1), pp. 155-161. Cited 8 times. http://www.ksu.edu.sa/sites/Colleges/CollegeofScinces/BotanyDepartment/SJBS/Default.aspx doi: 10.1016/j.sjbs.2016.07.004 View at Publisher 38 Solanki, R., Vanjari, L., Subramanian, S., Aparna, B., Nagapriyanka, E., Lakshmi, V. Comparative evaluation of multiplex PCR and routine laboratory phenotypic methods for detection of carbapenemases among gram negative Bacilli (Open Access) (2014) Journal of Clinical and Diagnostic Research, 8 (12), pp. DC23-DC26. Cited 13 times. http://www.jcdr.net/articles/PDF/5322/10794_CE%28Ra%29_F%28Sh%29_PF1%28SNAK%29_PFA%28Sh%29.pdf doi: 10.7860/JCDR/2014/10794.5322 View at Publisher 39 Kumar, S., Mehra, S.K. Performance of modified Hodge test and combined disc test for detection of carbapenemases in clinical isolates of Enterobacteriaceae (2015) Int J Curr Microbiol App Sci, 4, pp. 255-261. Cited 4 times. https://www.ijcmas.com/vol-4-5/SanjeevKumarandS.K.Mehra.pdf 40 Kazi, M., Drego, L., Nikam, C., Ajbani, K., Soman, R., Shetty, A., Rodrigues, C. Molecular characterization of carbapenem-resistant Enterobacteriaceae at a tertiary care laboratory in Mumbai (2015) European Journal of Clinical Microbiology and Infectious Diseases, 34 (3), pp. 467-472. Cited 30 times. link.springer.de/link/service/journals/10096/index.htm doi: 10.1007/s10096-014-2249-x View at Publisher 41 El-Sweify, M.A., Gomaa, N.I., El-maraghy, N.N. Phenotypic detection of carbapenem resistance among Klebsiella pneumoniae in Suez Canal University Hospitals, Ismailiya, Egypt (2015) Int J Curr Microbiol App Sci, 4, pp. 10-18. Cited 3 times. COI: 1:CAS:528:DC%2BC1cXjt1CjtbY%3D 42 Studentova, V., Papagiannitsis, C.C., Izdebski, R., Pfeifer, Y., Chudackova, E., Bergerova, T., Gniadkowski, M., (...), Hrabak, J. Detection of OXA-48-type carbapenemase-producing Enterobacteriaceae in diagnostic laboratories can be enhanced by addition of bicarbonates to cultivation media or reaction buffers (Open Access) (2015) Folia Microbiologica, 60 (2), pp. 119-129. Cited 17 times. www.biomed.cas.cz/mbu/folia/index.html doi: 10.1007/s12223-014-0349-8 View at Publisher 43 Devi, U., Bora, R., Das, J.K., Mahanta, J. Extended-spectrum β-lactamase & carbapenemase-producing gram-negative bacilli in neonates from a tertiary care centre in Dibrugarh, Assam, India (Open Access) (2018) Indian Journal of Medical Research, 147 (January), pp. 110-114. http://www.icmr.nic.in/ijmr/2018/january/0117.pdf doi: 10.4103/ijmr.IJMR_1288_16 View at Publisher 44 Khosravi, Y., Loke, M.F., Chua, E.G., Tay, S.T., Vadivelu, J. Phenotypic detection of metallo-β-lactamase in imipenem-resistant pseudomonas aeruginosa (Open Access) (2012) The Scientific World Journal, 2012, art. no. 654939. Cited 14 times. doi: 10.1100/2012/654939 View at Publisher 45 Poirel, L., Revathi, G., Bernabeu, S., Nordmann, P. Detection of NDM-1-producing Klebsiella pneumoniae in Kenya (Open Access) (2011) Antimicrobial Agents and Chemotherapy, 55 (2), pp. 934-936. Cited 135 times. http://aac.asm.org/cgi/reprint/55/2/934 doi: 10.1128/AAC.01247-10 View at Publisher 46 Brink, A.J., Coetzee, J., Clay, C.G., Sithol, S., Richards, G.A., Poirel, L., Nordmann, P. Emergence of New Delhi metallo-beta-lactamase (NDM-1) and Klebsiella pneumoniae carbapenemase (KPC-2) in South Africa (Open Access) (2012) Journal of Clinical Microbiology, 50 (2), pp. 525-527. Cited 60 times. http://jcm.asm.org/content/50/2/525.full.pdf+html doi: 10.1128/JCM.05956-11 View at Publisher 47 Coetzee, J., Brink, A. The emergence of carbapenem resistance in Enterobacteriaceae in South Africa (2011) South African J Epidemiol Infect, 26, pp. 239-240. Cited 6 times. 48 Iman, F.E.G., Marwa, A.M., Doaa, A.Y. Phenotypic and genotypic methods for detection of metallo beta lactamases among carbapenem resistant Enterobacteriaceae clinical isolates in Alexandria Main University Hospital (2016) Afr J Microbiol Res, 10, pp. 32-40. Cited 2 times. 49 Lutgring, J.D., Zhu, W., De Man, T.J.B., Avillan, J.J., Anderson, K.F., Lonsway, D.R., Rowe, L.A., (...), Limbago, B.M. Phenotypic and genotypic characterization of enterobacteriaceae producing oxacillinase-48-like carbapenemases, United States (Open Access) (2018) Emerging Infectious Diseases, 24 (4), pp. 700-709. Cited 18 times. https://wwwnc.cdc.gov/eid/article/24/4/pdfs/17-1377.pdf doi: 10.3201/eid2404.171377 View at Publisher 50 Lloyd, N.A., Nazaret, S., Barkay, T. Whole genome sequences to assess the link between antibiotic and metal resistance in three coastal marine bacteria isolated from the mummichog gastrointestinal tract (2018) Marine Pollution Bulletin, 135, pp. 514-520. Cited 2 times. www.elsevier.com/locate/marpolbul doi: 10.1016/j.marpolbul.2018.07.051 View at Publisher 51 Hamprecht, A., Vehreschild, J.J., Seifert, H., Saleh, A. Rapid detection of NDM, KPC and OXA-48 carbapenemases directly from positive blood cultures using a new multiplex immunochromatographic assay (Open Access) (2018) PLoS ONE, 13 (9), art. no. e0204157. Cited 15 times. https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0204157&type=printable doi: 10.1371/journal.pone.0204157 View at Publisher 52 Vali, L., Dashti, A.A., Jadaon, M.M., El-Shazly, S. The emergence of plasmid mediated quinolone resistance qnrA2 in extended spectrum β-lactamase producing Klebsiella pneumoniae in the Middle East (Open Access) (2015) DARU, Journal of Pharmaceutical Sciences, 23 (1), art. no. 34. Cited 12 times. http://www.darujps.com/content doi: 10.1186/s40199-015-0116-7