Proteus mirabilis carrying NTEKPC-IId, blaNDM-1, blaOXA-10, aph(3')-VI, qnrD1 and IncQ and Col3M plasmids from a hospital in Recife-PE, Brazil

Authors

DOI:

https://doi.org/10.33448/rsd-v10i15.22919

Keywords:

Proteus mirabilis; NTEKPC-IId; IncQ; Col3M.

Abstract

The present study objective to characterize the clinical aspects of a patient infected with two strains of P. mirabilis and the presence of resistance determinants in the two isolates from a patient at a public hospital in Recife-PE, Brazil. The total DNA of the isolates was extracted and submitted to PCR and amplicon sequencing for the investigation of resistance genes, blaKPC, blaOXA-10, blaOXA-23, blaOXA-48, blaOXA-58, blaVIM, blaIMP, blaSPM, blaGES, blaNDM, qnrD and aac(6')-Ib). Isolate P21-A2 harbored the aac(6')-Ib, blaOXA-10 and qnrD genes. One of the isolates, P20-A2, was selected for plasmid DNA sequencing. The results showed that the patient developed multiple infections with various pathogens including two strains of P. mirabilis. The patient was hospitalized for 103 days, had septic shock of skin, abdominal, pulmonary and ulcer focus, and died. Isolate P20-A2 harbored the genes blaNDM, qnrD, aph(3')-VI, blaKPC and blaOXA-10, and plasmids IncQ and Col3M, together with NTEKPC-IId. To our knowledge, this is the first report of P. mirabilis harboring NTEKPC-IId. Although P. mirabilis is standing out as a cause of nosocomial infections and a resistant multidrug pathogen, this species is still neglected, the emergence of these P. mirabilis isolates harboring aforementioned resistance determinants and the plasmids IncQ and Col3M demonstrate the potential for dissemination of important resistance genes, mainly in the case of P. mirabilis.

References

Almeida, A. C. S., Vilela, M. A., Cavalcanti, F. L. S., Martins, W. M. B. S., Morais, M. A., & Morais, M. M. C. (2012). First description of KPC-2-producing Pseudomonas putida in Brazil. Antimicrobial Agents and Chemotherapy, 56(4), 2205–2206. https://doi.org/10.1128/AAC.05268-11

Beirão, E. M., Jose, J., Furtado, D., Girardello, R., Ferreira Filho, H., & Gales, A. C. (2011). Clinical and microbiological characterization of KPC-producing Klebsiella pneumoniae infections in Brazil. Brazilian Journal Infectious Diseases, 15(1), 69-73. https://doi.org/10.1016/s1413-8670(11)70143-x

Beltrão, E. M. B., de Oliveira, É. M., & Lopes, A. C. D. S. (2021). First report of blaGES-1 in Proteus mirabilis clinical isolates. Revista Da Sociedade Brasileira de Medicina Tropical, 54. https://doi.org/10.1590/0037-8682-0864-2020

Bert, F., Branger, C., & Lambert-Zechovsky, N. (2002). Identification of PSE and OXA β-lactamase genes in Pseudomonas aeruginosa using PCR-restriction fragment length polymorphism. Journal of Antimicrobial Chemotherapy, 50(1), 11–18. https://doi.org/10.1093/jac/dkf069

Beltrão, E. M. B., de Oliveira, É. M., dos Santos Vasconcelos, C. R., Cabral, A. B., Rezende, A. M., & Souza Lopes, A. C. (2020b). Multidrug-resistant Klebsiella aerogenes clinical isolates from Brazil carrying IncQ1 plasmids containing the blaKPC-2 gene associated with non-Tn4401 elements (NTEKPC-IId). In Journal of Global Antimicrobial Resistance (Vol. 22, pp. 43–44). Elsevier Ltd. https://doi.org/10.1016/j.jgar.2020.05.001

Bontron, S., Poirel, L., Kieffer, N., Savov, E., Trifonova, A., Todorova, I., Kueffer, G., & Nordmann, P. (2019). Increased resistance to carbapenems in proteus mirabilis mediated by amplification of the blaVIM-1-carrying and IS26-associated class 1 integron. Microbial Drug Resistance, 25(5), 663–667. https://doi.org/10.1089/mdr.2018.0365

Boyd, D., Taylor, G., Fuller, J., Bryce, E., Embree, J., Gravel, D., Katz, K., Kibsey, P., Kuhn, M., Langley, J., Mataseje, L., Mitchell, R., Roscoe, D., Simor, A., Thomas, E., Turgeon, N., & Mulvey, M. (2015). Complete Sequence of Four Multidrug-Resistant MOBQ1 Plasmids Harboring blaGES-5 Isolated from Escherichia coli and Serratia marcescens Persisting in a Hospital in Canada. Microbial Drug Resistance, 21(3), 253–260. https://doi.org/10.1089/mdr.2014.0205

Cabral, A. B., Melo, R. de C. de A., Maciel, M. A. V, & Lopes, A. C. S. (2012). Multidrug resistance genes, including blaKPC and blaCTX-M-2, among Klebsiella pneumoniae isolated in Recife, Brazil. Revista Da Sociedade Brasileira de Medicina Tropical, 45(5), 572–578.

Cantón, R., Oliver, A., Coque, T. M., Varela, M. del C., Pérez-Díaz, J. C., & Baquero, F. (2002). Epidemiology of extended-spectrum ??-lactamase-producing Enterobacter isolates in a Spanish hospital during a 12-year period. Journal of Clinical Microbiology, 40(4), 1237–1243. https://doi.org/10.1128/JCM.40.4.1237-1243.2002

Cavaco, L. M., Hasman, H., Xia, S., & Aarestrup, F. M. (2009). qnrD, a novel gene conferring transferable quinolone resistance in Salmonella enterica serovar Kentucky and Bovismorbificans strains of human origin. Antimicrobial Agents and Chemotherapy, 53(2), 603–608. https://doi.org/10.1128/AAC.00997-08

Cerdeira, L. T., Cunha, M. P. V., Francisco, G. R., Bueno, M. F. C., Araujo, B. F., Ribas, R. M., Gontijo-Filho, P. P., Knöbl, T., de Oliveira Garcia, D., & Lincopan, N. (2017). IncX3 plasmid harboring a non-Tn4401 genetic element (NTEKPC) in a hospital-associated clone of KPC-2-producing Klebsiella pneumoniae ST340/CG258. Diagnostic Microbiology and Infectious Disease, 89(2), 164–167. https://doi.org/10.1016/j.diagmicrobio.2017.06.022

Cunha, B. A., Baron, J., & Cunha, C. B. (2017). Once daily high dose tigecycline - pharmacokinetic/pharmacodynamic based dosing for optimal clinical effectiveness: dosing matters, revisited. In Expert Review of Anti-Infective Therapy (Vol. 15, Issue 3, pp. 257–267). Taylor and Francis Ltd. https://doi.org/10.1080/14787210.2017.1268529

Dalmolin, T. V., Martins, A. F., Zavascki, A. P., de Lima-Morales, D., & Barth, A. L. (2018). Acquisition of the mcr-1 gene by a high-risk clone of KPC-2-producing Klebsiella pneumoniae ST437/CC258, Brazil. Diagnostic Microbiology and Infectious Disease, 90(2), 132–133. https://doi.org/10.1016/j.diagmicrobio.2017.09.016

Danilo de Oliveira, W., Lopes Barboza, M. G., Faustino, G., Yamanaka Inagaki, W. T., Sanches, M. S., Takayama Kobayashi, R. K., Vespero, E. C., & Dejato Rocha, S. P. (2021). Virulence, resistance and clonality of Proteus mirabilis isolated from patients with community-acquired urinary tract infection (CA-UTI) in Brazil. Microbial Pathogenesis, 152. https://doi.org/10.1016/j.micpath.2020.104642

Lima, G. J., Scavuzzi, A. M. L., Beltrão, E. M. B., Firmo, E. F., de Oliveira, É. M., de Oliveira, S. R., Rezende, A. M., & Lopes, A. C. de S. (2020). Identification of plasmid incQ1 and NTEKPC-IId harboring blaKPC-2 in isolates from Klebsiella pneumoniae infections in patients from Recife-PE, Brazil. Revista Da Sociedade Brasileira de Medicina Tropical, 53, 1–5. https://doi.org/10.1590/0037-8682-0526-2019

Del Franco, M., Paone, L., Novati, R., Giacomazzi, C. G., Bagattini, M., Galotto, C., Montanera, P. G., Triassi, M., & Zarrilli, R. (2015). Molecular epidemiology of carbapenem resistant Enterobacteriaceae in Valle d’Aosta region, Italy, shows the emergence of KPC-2 producing Klebsiella pneumoniae clonal complex 101 (ST101 and ST1789). BMC Microbiology, 15(1), 260. https://doi.org/10.1186/s12866-015-0597-z

Firmo, E. F., Beltrão, E. M. B., Silva, F. R. F. da, Alves, L. C., Brayner, F. A., Veras, D. L., & Lopes, A. C. S. (2020). Association of blaNDM-1 with blaKPC-2 and aminoglycoside-modifying enzyme genes among Klebsiella pneumoniae, Proteus mirabilis and Serratia marcescens clinical isolates in Brazil. Journal of Global Antimicrobial Resistance, 21, 255–261. https://doi.org/10.1016/j.jgar.2019.08.026

Fuga, B., Ferreira, M. L., Cerdeira, L. T., de Campos, P. A., Dias, V. L., Rossi, I., Machado, L. G., Lincopan, N., Gontijo-Filho, P. P., & Ribas, R. M. (2020). Novel small IncX3 plasmid carrying the blaKPC-2 gene in high-risk Klebsiella pneumoniae ST11/CG258. Diagnostic Microbiology and Infectious Disease, 96(2), 114900. https://doi.org/10.1016/j.diagmicrobio.2019.114900

Gales, A. C., Menezes, L. C., Silbert, S., & Sader, H. S. (2003). Dissemination in distinct Brazilian regions of an epidemic carbapenem-resistant Pseudomonas aeruginosa producing SPM metallo-β-lactamase. Journal of Antimicrobial Chemotherapy, 52(4), 699–702. https://doi.org/10.1093/jac/dkg416

Girlich, D., Bonnin, R. A., Dortet, L., & Naas, T. (2020). Genetics of Acquired Antibiotic Resistance Genes in Proteus spp. In Frontiers in Microbiology (Vol. 11). Frontiers Media S.A. https://doi.org/10.3389/fmicb.2020.00256

Huang, J., Deng, S., Ren, J., Tu, J., Ye, M., & Wang, M. (2017). Characterization of a blaNDM-1-harboring plasmid from a Salmonella enterica clinical isolate in China. Molecular Medicine Reports, 16(2), 1087–1092. https://doi.org/10.3892/mmr.2017.6733

Lerminiaux, N. A., & Cameron, A. D. S. (2019). Horizontal transfer of antibiotic resistance genes in clinical environments. Canadian Journal of Microbiology, 65(1), 34–44. https://doi.org/10.1139/cjm-2018-0275

Lima, G. J. de, Scavuzzi, A. M. L., Beltrão, E. M. B., Firmo, E. F., Oliveira, É. M. de, Oliveira, S. R. de, Rezende, A. M., & Lopes, A. C. de S. (2020). Identification of plasmid IncQ1 and NTEKPC-IId harboring bla KPC-2 in isolates from Klebsiella pneumoniae infections in patients from Recife-PE, Brazil. Revista Da Sociedade Brasileira de Medicina Tropical, 53, e20190526. https://doi.org/10.1590/0037-8682-0526-2019

Oliveira, É. M. de, Beltrão, E. M. B., Scavuzzi, A. M. L., Barros, J. F., & Lopes, A. C. S. (2020). High plasmid variability, and the presence of IncFIB, IncQ, IncA/C, IncHI1B, and IncL/M in clinical isolates of Klebsiella pneumoniae with bla KPC and bla NDM from patients at a public hospital in Brazil. Revista Da Sociedade Brasileira de Medicina Tropical, 53, e20200397. https://doi.org/10.1590/0037-8682-0397-2020

Pereira, P. S., Borghi, M., Albano, R. M., Lopes, J. C. O., Silveira, M. C., Marques, E. A., Oliveira, J. C. R., Asensi, M. D., & Carvalho-Assef, A. P. D. (2015). Coproduction of NDM-1 and KPC-2 in Enterobacter hormaechei from Brazil. Microbial Drug Resistance (Larchmont, N.Y.), 21(2), 234–236. https://doi.org/10.1089/mdr.2014.0171

Pereira, P. S., de araujo, C. F. M., Seki, L. M., Zahner, V., Carvalho-Assef, A. P. D. A., & Asensi, M. D. (2013). Update of the molecular epidemiology of KPC-2-producing Klebsiella pneumoniae in Brazil: Spread of clonal complex 11 (ST11, ST437 and ST340). Journal of Antimicrobial Chemotherapy, 68(2), 312–316. https://doi.org/10.1093/jac/dks396

Poirel, L., Héritier, C., Tolün, V., & Nordmann, P. (2004). Emergence of Oxacillinase-Mediated Resistance to Imipenem in Klebsiella pneumoniae. Antimicrobial Agents and Chemotherapy, 48(1), 15–22. https://doi.org/10.1128/AAC.48.1.15-22.2004

Poirel, L., & Nordmann, P. (2006). Genetic structures at the origin of acquisition and expression of the carbapenem-hydrolyzing oxacillinase gene blaOXA-58 in Acinetobacter baumannii. Antimicrobial Agents and Chemotherapy, 50(4), 1442–1448. https://doi.org/10.1128/AAC.50.4.1442-1448.2006

Ranjbar, R., Zayeri, S., & Mirzaie, A. (n.d.). Development of multiplex PCR for rapid detection of metallo-β-lactamase genes in clinical isolates of Acinetobacter baumannii. http://ijm.tums.ac.ir

Rozwandowicz, M., Brouwer, M. S. M., Fischer, J., Wagenaar, J. A., Gonzalez-Zorn, B., Guerra, B., Mevius, D. J., & Hordijk, J. (2018). Plasmids carrying antimicrobial resistance genes in Enterobacteriaceae. Journal of Antimicrobial Chemotherapy, 73(5), 1121–1137. https://doi.org/10.1093/jac/dkx488

Sanches, M. S., Baptista, A. A. S., de Souza, M., Menck-Costa, M. F., Koga, V. L., Kobayashi, R. K. T., & Rocha, S. P. D. (2019). Genotypic and phenotypic profiles of virulence factors and antimicrobial resistance of Proteus mirabilis isolated from chicken carcasses: potential zoonotic risk. Brazilian Journal of Microbiology, 50(3), 685–694. https://doi.org/10.1007/s42770-019-00086-2

Wasfi, R., Hamed, S. M., Amer, M. A., & Fahmy, L. I. (2020). Proteus mirabilis Biofilm: Development and Therapeutic Strategies. In Frontiers in Cellular and Infection Microbiology (Vol. 10). Frontiers Media S.A. https://doi.org/10.3389/fcimb.2020.00414

Yigit, H., Queenan, A. M., Anderson, G. J., Domenech-Sanchez, A., Biddle, J. W., Steward, C. D., Alberti, S., Bush, K., & Tenover, F. C. (2001). Novel carbapenem-hydrolyzing β-lactamase, KPC-1, from a carbapenem-resistant strain of Klebsiella pneumoniae. Antimicrobial Agents and Chemotherapy, 45(4), 1151–1161. https://doi.org/10.1128/AAC.45.4.1151-1161.2001

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Published

28/11/2021

How to Cite

BELTRÃO, E. M. B.; OLIVEIRA, Érica M.; VASCONCELOS, C. R. dos S. V.; REZENDE, A. M. .; LOPES, A. C. de S. Proteus mirabilis carrying NTEKPC-IId, blaNDM-1, blaOXA-10, aph(3’)-VI, qnrD1 and IncQ and Col3M plasmids from a hospital in Recife-PE, Brazil. Research, Society and Development, [S. l.], v. 10, n. 15, p. e399101522919, 2021. DOI: 10.33448/rsd-v10i15.22919. Disponível em: https://www.rsdjournal.org/index.php/rsd/article/view/22919. Acesso em: 25 apr. 2024.

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Health Sciences