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Anti-Infective Agents

Author(s): Abhi Mallick, Mili Barik, Soma Sarkar and Surojit Das*

DOI: 10.2174/0122113525279277231223035547

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β-lactamase and Plasmid-mediated Quinolone Resistance Determinants Among Proteus spp. Isolates at a Tertiary-care Hospital in Kolkata, India

Article ID: e170124225724 Pages: 5

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Abstract

Background: Emerging antibiotic resistance (ABR) in Proteus spp., especially to third-generation cephalosporins (3GCc), carbapenems, and fluoroquinolones, challenges the treatment outcome and infection prevention. Limited studies pose a knowledge gap between them and ABR.

Methods: We investigated the in vitro efficacy of therapeutic options and prevalence of β-lactamase and plasmid-mediated quinolone resistance (PMQR) traits in 3GC- and/or fluoroquinolone- nonsusceptible Proteus (P.) spp. (n=27) in Kolkata, India, during 2021–2022. P. mirabilis was commonly isolated (>80%) from superficial and urine samples. The majority of the isolates (48-78%) remained susceptible to piperacillin-tazobactam, meropenem, amikacin, cefoperazonesulbactam, and cefepime.

Results: All isolates showed >0.2 multiple-antibiotic resistance index, with >65% being multidrug and >30% being extensively drug-resistant. blaTEM (n=9), blaNDM (n=9), and qnrA (n=6) were commonly noted with the co-production of β-lactamases and PMQR in ten (37%) isolates. More than 50% of the isolates were devoid of the tested acquired genes.

Conclusion: The study concludes that superbugs dominate, with limited occurrence of plasmidborne markers in this geographic location.

Keywords: Proteus spp., antimicrobial resistance, β-lactamase, plasmid-mediated quinolone resistance, acquired genes, human gut.

[1]
O’Hara, C.M.; Brenner, F.W.; Miller, J.M. Classification, identification, and clinical significance of Proteus, Providencia, and Morganella. Clin. Microbiol. Rev., 2000, 13(4), 534-546.
[http://dx.doi.org/10.1128/CMR.13.4.534] [PMID: 11023955]
[2]
Schaffer, J.N.; Pearson, M.M. Proteus mirabilis and urinary tractinfections. Microbiol. Spectr., 2015, 3(5), 3.5.10.
[http://dx.doi.org/10.1128/microbiolspec.UTI-0017-2013] [PMID: 26542036]
[3]
Wang, J.T.; Chen, P.C.; Chang, S.C.; Shiau, Y.R.; Wang, H.Y.; Lai, J.F.; Huang, I.W.; Tan, M.C.; Lauderdale, T.L.Y. Antimicrobial susceptibilities of Proteus mirabilis: A longitudinal nationwide study from the Taiwan surveillance of antimicrobial resistance (TSAR) program. BMC Infect. Dis., 2014, 14(1), 486.
[http://dx.doi.org/10.1186/1471-2334-14-486] [PMID: 25192738]
[4]
Warren, J.W.; Tenney, J.H.; Hoopes, J.M.; Muncie, H.L.; Anthony, W.C. A prospective microbiologic study of bacteriuria in patients with chronic indwelling urethral catheters. J. Infect. Dis., 1982, 146(6), 719-723.
[http://dx.doi.org/10.1093/infdis/146.6.719] [PMID: 6815281]
[5]
El-Kazzaz, S.S. Virulence factors associated with quinolone resistance in Proteus species isolated from patients with urinary tract infection. Egypt. J. Med. Microbiol., 2021, 30(1), 115-123.
[http://dx.doi.org/10.51429/EJMM30115]
[6]
Stock, I. Natural antibiotic susceptibility of Proteus spp., with special reference to P. mirabilis and P. penneri strains. J. Chemother., 2003, 15(1), 12-26.
[http://dx.doi.org/10.1179/joc.2003.15.1.12] [PMID: 12678409]
[7]
Girlich, D.; Bonnin, R.A.; Dortet, L.; Naas, T. Genetics of acquired antibiotic resistance genes in Proteus spp. Front. Microbiol., 2020, 11(11), 256.
[http://dx.doi.org/10.3389/fmicb.2020.00256] [PMID: 32153540]
[8]
Shaaban, M.; Elshaer, S.L.; Abd El-Rahman, O.A.; Ola, A. Prevalence of extended-spectrum β-lactamases, AmpC, and carbapenemases in Proteus mirabilis clinical isolates. BMC Microbiol., 2022, 22(1), 247.
[http://dx.doi.org/10.1186/s12866-022-02662-3] [PMID: 36221063]
[9]
Neuwirth, C.; Siébor, E.; Duez, J.M.; Péchinot, A.; Kazmierczak, A. Imipenem resistance in clinical isolates of Proteus mirabilis associated with alterations in penicillin-binding proteins. J. Antimicrob. Chemother., 1995, 36(2), 335-342.
[http://dx.doi.org/10.1093/jac/36.2.335] [PMID: 8522463]
[10]
ICMR (2022) Antimicrobial resistance research and surveillance network. Annual report, January 2021 to December 2021. The Indian Council of Medical Research, India. https://main.icmr.nic.in/sites/default/files/upload_documents/AMR_Annual_Report_2021.pdf (Accessed 9 September 2023).
[11]
The Clinical and Laboratory Standards Institute (2021) Performance standards for antimicrobial susceptibility testing. 31sted., CLSIM100. Wayne, PA. https://clsi.org/standards/products/microbiology/documents/m100/
[12]
Pal, N.; Sharma, N.; Sharma, R.; Hooja, S.; Maheshwari, R.K. Prevalence of multidrug (MDR) and extensively drug resistant (XDR) Proteus species in a tertiary care hospital, India. Int. J. Curr. Microbiol. Appl. Sci., 2014, 3, 243-252.
[13]
Lee, J.J.; Lee, J.H.; Kwon, D.B.; Jeon, J.H.; Park, K.S.; Lee, C.R.; Lee, S.H. Fast and accurate large-scale detection of ß-lactamase genes conferring antibiotic resistance. Antimicrob. Agents Chemother., 2015, 59(10), 5967-5975.
[http://dx.doi.org/10.1128/AAC.04634-14] [PMID: 26169415]
[14]
Ciesielczuk, H.; Hornsey, M.; Choi, V.; Woodford, N.; Wareham, D.W. Development and evaluation of a multiplex PCR for eight plasmid-mediated quinolone-resistance determinants. J. Med. Microbiol., 2013, 62(12), 1823-1827.
[http://dx.doi.org/10.1099/jmm.0.064428-0] [PMID: 24000223]
[15]
Nakano, R.; Nakano, A.; Abe, M.; Inoue, M.; Okamoto, R. Regional outbreak of CTX-M-2 β-lactamase-producing Proteus mirabilis in Japan. J. Med. Microbiol., 2012, 61(12), 1727-1735.
[http://dx.doi.org/10.1099/jmm.0.049726-0] [PMID: 22935848]
[16]
Priya, P.S. Manonmoney; Leela, K.V. Phenotypic characterisation of Proteus species isolated from different clinical samples with special reference to antibiotic resistance pattern in a tertiary care centre. J. Clin. Diagn. Res., 2022, 16(1)
[http://dx.doi.org/10.7860/JCDR/2022/51928.15901]
[17]
Caubey, M.; Suchitra, M. S. Occurrence of TEM, SHV and CTX-M β lactamases in clinical isolates of Proteus species in a tertiary care center. Infect. Disord. Drug Targets, 2018, 18(1), 68-71.
[http://dx.doi.org/10.2174/1871526517666170425125217] [PMID: 28443500]
[18]
Pagani, L.; Dell’Amico, E.; Migliavacca, R.; D’Andrea, M.M.; Giacobone, E.; Amicosante, G.; Romero, E.; Rossolini, G.M. Multiple CTX-M-type extended-spectrum β-lactamases in nosocomial isolates of Enterobacteriaceae from a hospital in northern Italy. J. Clin. Microbiol., 2003, 41(9), 4264-4269.
[http://dx.doi.org/10.1128/JCM.41.9.4264-4269.2003] [PMID: 12958255]
[19]
Chanal, C.; Bonnet, R.; De Champs, C.; Sirot, D.; Labia, R.; Sirot, J. Prevalence of β-lactamases among 1,072 clinical strains of Proteus mirabilis: A 2-year survey in a French hospital. Antimicrob. Agents Chemother., 2000, 44(7), 1930-1935.
[http://dx.doi.org/10.1128/AAC.44.7.1930-1935.2000] [PMID: 10858357]
[20]
Ho, P.L.; Ho, A.Y.M.; Chow, K.H.; Wong, R.C.W.; Duan, R.S.; Ho, W.L.; Mak, G.C.; Tsang, K.W.; Yam, W.C.; Yuen, K.Y. Occurrence and molecular analysis of extended-spectrum β-lactamase-producing Proteus mirabilis in Hong Kong, 1999–2002. J. Antimicrob. Chemother., 2005, 55(6), 840-845.
[http://dx.doi.org/10.1093/jac/dki135] [PMID: 15857942]
[21]
Fursova, N.K.; Astashkin, E.I.; Knyazeva, A.I.; Kartsev, N.N.; Leonova, E.S.; Ershova, O.N.; Alexandrova, I.A.; Kurdyumova, N.V.; Sazikina, S.Y.; Volozhantsev, N.V.; Svetoch, E.A.; Dyatlov, I.A. The spread of bla OXA-48 and bla OXA-244 carbapenemase genes among Klebsiella pneumoniae, Proteus mirabilis and Enterobacter spp. isolated in Moscow, Russia. Ann. Clin. Microbiol. Antimicrob., 2015, 14(1), 46.
[http://dx.doi.org/10.1186/s12941-015-0108-y] [PMID: 26526183]
[22]
Bonnet, R. Growing group of extended-spectrum β-lactamases: The CTX-M enzymes. Antimicrob. Agents Chemother., 2004, 48(1), 1-14.
[http://dx.doi.org/10.1128/AAC.48.1.1-14.2004] [PMID: 14693512]
[23]
Mallick, A.; Roy, A.; Sarkar, S.; Mondal, K.C.; Das, S. Customized molecular diagnostics of bacterial bloodstream infections for carbapenem resistance: A convenient and affordable approach. Pathog. Glob. Health, 2023, 117(7), 631-638.
[http://dx.doi.org/10.1080/20477724.2023.2201982] [PMID: 37069793]
[24]
Das, S.; Mallick, A.; Barik, M.; Sarkar, S.; Saha, P. The emergence of clonally diverse carbapenem-resistant Enterobacter cloacae complex in West Bengal, India: A dockyard of β-lactamases periling nosocomial infections. Int. Microbiol., 2023, 1-1.
[http://dx.doi.org/10.1007/s10123-023-00451-0] [PMID: 37985632]
[25]
Naas, T.; Cuzon, G.; Villegas, M.V.; Lartigue, M.F.; Quinn, J.P.; Nordmann, P. Genetic structures at the origin of acquisition of the beta-lactamase blaKPC gene. Antimicrob. Agents Chemother., 2008, 52, 1257-1263.
[26]
Ohno, Y.; Nakamura, A.; Hashimoto, E.; Matsutani, H.; Abe, N.; Fukuda, S.; Hisashi, K.; Komatsu, M.; Nakamura, F. Molecular epidemiology of carbapenemase-producing Enterobacteriaceae in a primary care hospital in Japan, 2010–2013. J. Infect. Chemother., 2017, 23(4), 224-229.
[http://dx.doi.org/10.1016/j.jiac.2016.12.013] [PMID: 28161293]
[27]
Cabral, A.B.; Maciel, M.A.V.; Barros, J.F.; Antunes, M.M.; Lopes, A.C.S. Detection of bla KPC-2 in Proteus mirabilis in Brazil. Rev. Soc. Bras. Med. Trop., 2015, 48(1), 94-95.
[http://dx.doi.org/10.1590/0037-8682-0152-2014] [PMID: 25860472]
[28]
Di Pilato, V.; Chiarelli, A.; Boinett, C.J.; Riccobono, E.; Harris, S.R.; D’Andrea, M.M.; Thomson, N.R.; Rossolini, G.M.; Giani, T. Complete genome sequence of the first KPC-type carbapenemase-positive Proteus mirabilis strain from a bloodstream infection. Genome Announc., 2016, 4(3), e00607-e00616.
[http://dx.doi.org/10.1128/genomeA.00607-16] [PMID: 27340072]
[29]
Shen, P.; Wei, Z.; Jiang, Y.; Du, X.; Ji, S.; Yu, Y.; Li, L. Novel genetic environment of the carbapenem-hydrolyzing β-lactamase KPC-2 among enterobacteriaceae in China. Antimicrob. Agents Chemother., 2009, 53(10), 4333-4338.
[http://dx.doi.org/10.1128/AAC.00260-09] [PMID: 19620332]
[30]
Ramos, A.C.; Cayô, R.; Carvalhaes, C.G.; Jové, T.; da Silva, G.P.; Sancho, F.M.P.; Chagas-Neto, T.; Medeiros, E.A.S.; Gales, A.C. Dissemination of multidrug-resistant Proteus mirabilis clones carrying a novel integron-borne blaIMP-1 in a tertiary hospital. Antimicrob. Agents Chemother., 2018, 62(2), e01321-e17.
[http://dx.doi.org/10.1128/AAC.01321-17] [PMID: 29158274]
[31]
Jannat, H.; Shamsuzzaman, S.M.; Faisal, M.A.; Nila, S.S. Prevalence of qnr and aac(6′)-Ib-cr genes in clinical isolates of Proteus spp. at a tertiary care hospital in Dhaka, Bangladesh. Mymensingh Med. J., 2022, 31(1), 31-36.
[PMID: 34999676]
[32]
Zhang, S.; Sun, J.; Liao, X.P.; Hu, Q.J.; Liu, B.T.; Fang, L.X.; Deng, H.; Ma, J.; Xiao, X.; Zhu, H.Q.; Liu, Y.H. Prevalence and plasmid characterization of the qnrD determinant in Enterobacteriaceae isolated from animals, retail meat products, and humans. Microb. Drug Resist., 2013, 19(4), 331-335.
[http://dx.doi.org/10.1089/mdr.2012.0146] [PMID: 23557071]
[33]
Albornoz, E.; Lucero, C.; Romero, G.; Rapoport, M.; Guerriero, L.; Andres, P.; Galas, M.; Corso, A.; Petroni, A.; Petroni, A. Analysis of plasmid-mediated quinolone resistance genes in clinical isolates of the tribe Proteeae from Argentina: First report of qnrD in the Americas. J. Glob. Antimicrob. Resist., 2014, 2(4), 322-326.
[http://dx.doi.org/10.1016/j.jgar.2014.05.005] [PMID: 27873695]
[34]
Ogbolu, D.O.; Daini, O.A.; Ogunledun, A.; Alli, A.O.; Webber, M.A. High levels of multidrug resistance in clinical isolates of Gram-negative pathogens from Nigeria. Int. J. Antimicrob. Agents, 2011, 37(1), 62-66.
[http://dx.doi.org/10.1016/j.ijantimicag.2010.08.019] [PMID: 21074376]
[35]
Mazzariol, A.; Kocsis, B.; Koncan, R.; Kocsis, E.; Lanzafame, P.; Cornaglia, G. Description and plasmid characterization of qnrD determinants in Proteus mirabilis and Morganella morganii. Clin. Microbiol. Infect., 2012, 18(3), E46-E48.
[http://dx.doi.org/10.1111/j.1469-0691.2011.03728.x] [PMID: 22192340]
[36]
Guillard, T.; Grillon, A.; de Champs, C.; Cartier, C.; Madoux, J.; Berçot, B.; Lebreil, A.L.; Lozniewski, A.; Riahi, J.; Vernet-Garnier, V.; Cambau, E. Mobile insertion cassette elements found in small non-transmissible plasmids in Proteeae may explain qnrD mobilization. PLoS One, 2014, 9(2), e87801.
[http://dx.doi.org/10.1371/journal.pone.0087801] [PMID: 24504382]
[37]
Mokracka, J. Gruszczyńska, B.; Kaznowski, A. Integrons, β‐lactamase andQNR genes in multidrug resistant clinical isolates ofP roteus mirabilis andP. vulgaris. Acta Pathol. Microbiol. Scand. Suppl., 2012, 120(12), 950-958.
[http://dx.doi.org/10.1111/j.1600-0463.2012.02923.x] [PMID: 23030307]