Search for other papers by Stephanie Radeva in
Current site
Google Scholar
PubMed
Laboratory of Microbiology, University Hospital “Saint Marina”- Varna,
Search for other papers by Denis Niyazi in
Current site
Google Scholar
PubMed
Laboratory of Microbiology, University Hospital “Saint Marina”- Varna,
Search for other papers by Milena Bozhkova in
Current site
Google Scholar
PubMed
Laboratory of Microbiology, University Hospital “Saint Marina”- Varna,
Search for other papers by Temenuga Stoeva in
Current site
Google Scholar
PubMed
Abstract
The aim of this study is to evaluate the antimicrobial susceptibility of invasive isolates of Serratia marcescens, associated with blood stream infections (BSIs) in patients hospitalized in Varna University Hospital, Bulgaria, as well as to identify the genetic mechanisms responsible for 3rd generation cephalosporin and carbapenem-resistance among these isolates. A total of 45 consecutive S. marcescens isolates, obtained from blood cultures of 45 patients with BSIs, hospitalized during an 8-year period (2016–2023) were included. Species identification and antimicrobial susceptibility testing were done by Phoenix (BD, USA) and Vitek 2 (BioMerieux, France) systems and the results were interpreted according to EUCAST guidelines. The genetic mechanisms of beta-lactam resistance were studied by PCR. During the study period, a total of 45 patients were diagnosed with S. marcescens-associated BSIs. All infections were defined as nosocomial, predominantly intensive care unit-acquired (42.2%) and 28.8% were central venous catheter-associated. The following antimicrobial resistance rates were found: ceftriaxone, piperacillin/tazobactam, 57.8%; ceftazidime, 55.6%; cefepime, trimethoprime/sulfamethoxazole, 53.3%; gentamicin, 48.8%; ciprofloxacin, 44.5%; amikacin, 15.6%; carbapenems, 2.2%. The blaCTX-M was identified in 88.9% of the tested 3rd generation cephalosporin resistant isolates. Among these, 50% were also blaTEM positive. The single carbapenem-resistant isolate harboured blaKPC, blaCTX-M1/9, blaCMY-2 and blaTEM. This study demonstrates S. marcescens as a problematic nosocomial pathogen and we report a KPC-producing S. marcescens clinical isolate from a BSI in Bulgaria.
-
1.
Adeolu M, Alnajar S, Naushad S, Gupta R. Genome-based phylogeny and taxonomy of the ‘Enterobacteriales’: proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. Int J Syst Evol Microbiol 2016; 66: 5575–5599.
-
2.
Martin SL, Patterson C, Jerabek J. A rare case of Serratia marcescens pacemaker infection and cerebrovascular accident. Chest 2022; 162: A567.
-
3.
Global, regional, and national age-sex specific all-cause and cause-specific mortality for 240 causes of death, 1990-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 2015; 385, 117–171.
-
4.
Hattori H, Maeda M, Nagatomo Y, Takuma T, Niki Y, Naito Y, et al. Epidemiology and risk factors for mortality in bloodstream infections: a single-center retrospective study in Japan. Am J Infect Control 2018; 46: e75–e79.
-
5.
Nielsen SL. The incidence and prognosis of patients with bacteremia. Dan Med J 2015; 62: B5128.
-
6.
The European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters, version 11.0, 2021. Available from: http://www.eucast.org/clinical_breakpoints/.
-
7.
Tóth A, Mаkаi A, Jánvári L, Dаmjаnovа I, Gаjdács M, Urbán E. Chаrаctеrizаtion of а rаrе blаVIM-4 mеtаllo-β-lаctаmаsе-рroducing Sеrrаtiа mаrcеscеns clinicаl isolаtе in Hungаry. Hеliyon 2020; 6: e04231.
-
8.
Cullеn MM, Trаil A, Robinson M, Kеаnеy M, Chаdwick PR. Sеrrаtiа mаrcеscеns outbrеаk in а nеonаtаl intеnsivе cаrе unit рromрting rеviеw of dеcontаminаtion of lаryngoscoреs. J Hosр Infеct 2005; 59 (1): 68–70.
-
9.
Рursеll K, Liаngрunsаkul S. Community-аcquirеd nеcrotising fаsciitis cаusеd by Sеrrаtiа mаrcеscеns: cаsе rерort аnd rеviеw. Еur J Clin Microbiol Infеct Dis 2001; 20: 509–521.
-
10.
Mеndеs JC, Cаsаdo A. Sеrrаtiа mаrcеscеns outbrеаk in а COVID-19 intеnsivе cаrе unit – Аrе thеrе аny fаctors sреcific to COVID-19 units thаt fаcilitаtе bаctеriаl cross-contаminаtion bеtwееn COVID-19 раtiеnts? Аm J Infеct Control 2022; 50: 223–225.
-
11.
Anonymous. Annual epidemiological report on communicable diseases in Europe 2010. Stockholm, Sweden: European Centre for Disease Prevention and Control; 2010.
-
12.
Géry A, Mouet A, Gravey F, Fines-Guyon M, Guerin F, Ethuin F, et al. Investigation of Serratia marcescens surgical site infection outbreak associated with peroperative ultrasonography probe. J Hosp Infect 2021; 111: 184–188.
-
13.
Cilli F, Nazli-Zeka A, Arda B, Sipahi OR, Aksit-Barik S, Kepeli N, et al. Serratia marcescens sepsis outbreak caused by contaminated propofol. Аm J Infеct Control 2019; 47: 582–584.
-
14.
Liu D, Zhang LP, Huang SF, Wang Z, Chen P, Wang H, et al. Outbreak of Serratia marcescens infection due to contamination of multiple-dose vial of heparin-saline solution used to flush deep venous catheters or peripheral trocars. J Hosp Infect 2011; 77: 175–176.
-
15.
The European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters, version 11.0, 2021. Available from: http://www.eucast.org/clinical_breakpoints/.
-
16.
Jarlier V, Nicolas MH, Fournier G, Philippon A. Extended broad-spectrum beta-lactamases conferring transferable resistance to newer beta-lactam agents in Enterobacteriaceae: hospital prevalence and susceptibility patterns. Rev Infect Dis 1988; 10: 867–878.
-
17.
Niyazi D, Radeva S, Bozhkova M, Savova D, Stoeva T. A cheap and simple method for DNA isolation from endonuclease producing Serratia marcescens. Iran J Public Health 2023; 52: 1089–1091.
-
18.
Markovska R, Schneider I, Keuleyan E, Sredkova M, Ivanova D, Markova B, et al. Extended-spectrum beta-lactamase-producing Enterobacteriaceae in Bulgarian hospitals. Microb Drug Resist 2008; 14: 119–128.
-
19.
Antimicrobial Resistance Collaborators. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet 2022; 399: 629–655.
-
20.
Measuring infectious causes and resistance outcomes for burden estimation. https://vizhub.healthdata.org/microbe/ [Accessed 10 Oct 2023].
-
21.
European Centre for Disease Prevention and Control. Antimicrobial consumption in the EU/EEA [ESAC-Net] -annual epidemiological report 2022. Stockholm: ECDC; 2023.
-
22.
Simsek M. Determination of the antibiotic resistance rates of Serratia marcescens isolates obtained from various clinical specimens. Niger J Clin Pract 2019; 22: 125–130.
-
23.
Bozkurt H, Güdücüoğlu H, Bayram Y, Gülmez S, Kutluay N, Bozkurt EN, et al. The role of serratia bacteria produced from clinical specimens in various infections and susceptibility to antimicrobials. Van Med J 2005; 12: 182–188.
-
24.
Ferreira RL, Rezende GS, Damas MSF, Oliveira-Silva M, Pitondo-Silva A, Brito MCA, et al. Characterization of KPC-producing Serratia marcescens in an intensive care unit of a Brazilian tertiary hospital. Front Microbiol 2020; 20: 956.
-
25.
Stock I, Grueger T, Wiedemann B. Natural antibiotic susceptibility of strains of Serratia marcescens and the S. liquefaciens complex: S. liquefaciens sensu stricto, S. proteamaculans and S. grimesii. Int J Antimicrob Agents 2003; 22: 35–47.
-
26.
Bolourchi N, Noori Goodarzi N, Giske CG, Nematzadeh S, Haririzadeh Jouriani F, Solgi H, et al. Comprehensive pan-genomic, resistome and virulome analysis of clinical OXA-48 producing carbapenem-resistant Serratia marcescens strains. Gene 2022; 822: 146355.
-
27.
Miao M, Wen H, Xu P, Niu S, Lv J, Xie X, et al. Genetic diversity of Carbapenem-Resistant Enterobacteriaceae [CRE] clinical isolates from a tertiary hospital in eastern China. Front Microbiol 2019; 9: 3341.
-
28.
Gajdács M, Urbán E. Resistance trends and epidemiology of Citrobacter-Enterobacter-Serratia in urinary tract infections of inpatients and outpatients [RECESUTI]: a 10-year survey. Medicina [Kaunas] 2019; 55: 285.
-
29.
Markovska R, Stoeva T, Bojkova K, Mitov I. Epidemiology and molecular characterization of extended-spectrum beta-lactamase-producing Enterobacter spp., Pantoea agglomerans, and Serratia marcescens isolates from a Bulgarian hospital. Microb Drug Resist 2014; 20: 131–137.
-
30.
Ivanova D, Markovska R, Hadjieva N, Schneider I, Mitov I, Bauernfeind A. Extended-spectrum beta-lactamase-producing Serratia marcescens outbreak in a Bulgarian hospital. J Hosp Infect 2008; 70: 60–65.
-
31.
Mlynarczyk A, Szymanek K, Sawicka-Grzelak A, Pazik J, Buczkowska T, Durlik M, et al. CTX-M and TEM as predominant types of extended spectrum beta-lactamases among Serratia marcescens isolated from solid organ recipients. Transpl Proc 2009; 41: 3253–3255.
-
32.
Jacoby GA. AmpC beta-lactamases. Clin Microbiol Rev 2009; 22: 161–182.
-
33.
Harris PN, Ferguson JK. Antibiotic therapy for inducible AmpC β-lactamase-producing Gram-negative bacilli: what are the alternatives to carbapenems, quinolones and aminoglycosides? Int J Antimicrob Agents 2012; 40: 297–305.
-
34.
Pruss A, Kwiatkowski P, Sienkiewicz M, Masiuk H, Łapińska A, Kot B, et al. Similarity analysis of Klebsiella pneumoniae producing carbapenemases isolated from UTI and other infections. Antibiotics 2023; 12: 1224.
-
35.
Pérez-Viso B, Hernández-García M, Ponce-Alonso M, Morosini MI, Ruiz-Garbajosa P, del Campo R, et al. Characterization of carbapenemase-producing Serratia marcescens and whole-genome sequencing for plasmid typing in a hospital in Madrid, Spain [2016–18]. J Antimicrob Chemother 2021; 76: 110–116.
-
36.
Hopkins K, Findlay J, Meunier D, Cummins M, Curtis S, Kustos I, et al. Serratia marcescens producing SME carbapenemases: an emerging resistance problem in the UK? J Antimicrob Chemother 2017; 72: 1535–1537.
-
37.
Ymaña B, Luque N, Pons M, Ruiz J. KPC-2-NDM-1-producing Serratia marcescens: first description in Peru. New Microbes New Infect 2022; 49–50: 101051.
-
38.
Overmeyer AJ, Prentice E, Brink A, Lennard K, Moodley C. The genomic characterization of carbapenem-resistant Serratia marcescens at a tertiary hospital in South Africa. JAC-Antimicrob Resist 2023; 5: dlad089.
-
39.
Özcan N, Atmaca S, Özbek E. P11 the ratio and antibiotic resistance profiles of Serratia species among other causative bacteria isolated from blood cultures between 2015 and 2020. JAC-Antimicrob Resist 2022; 4: dlac004–010.
-
40.
Xu Q, Fu Y, Zhao F, Jiang Y, Yu Y. Molecular characterization of carbapenem-resistant Serratia marcescens clinical isolates in a tertiary hospital in Hangzhou, China. Infect Drug Resist 2020; 13: 999–1008.
-
41.
Cai JC, Zhou HW, Zhang R, Chen GX. Emergence of Serratia marcescens, Klebsiella pneumoniae, and Escherichia coli isolates possessing the plasmid-mediated carbapenem-hydrolyzing beta-lactamase KPC-2 in intensive care units of a Chinese hospital. Antimicrob Agents Chemother 2008; 52: 2014–2018.
-
42.
Taggar G, Rehman MA, Boerlin P, Diarra MS. Molecular epidemiology of carbapenemases in Enterobacteriales from humans, animals, food and the environment. Antibiotics 2020; 9: 693.
-
43.
Codjoe FS, Donkor ES. Carbapenem resistance: a review. Med Sci 2017; 6: 1.
-
44.
Martin SL, Patterson C, Jerabek J. A rare case of Serratia marcescens pacemaker infection and cerebrovas-cular accident. Chest 2022; 162: A567.
-
45.
Tan CY, Chiu NC, Lee KS, Chi H, Huang FY, Huang DTN, et al. Respiratory tract infections in children with tracheostomy. J Microbiol Immunol Infect 2020; 53: 315–320.
-
46.
Tsakris A, Voulgari E, Poulou A, Kimouli M, Pournaras S, Ranellou K, et al. In vivo acquisition of a plasmid-mediated bla [KPC-2] gene among clonal isolates of Serratia marcescens. J Clin Microbiol 2010; 48: 2546–2549.
-
47.
Bes T, Nagano D, Martins R, Marchi P, Perdigão-Neto L, Higashino H, et al. Bloodstream Infections caused by Klebsiella pneumoniae and Serratia marcescens isolates co-harboring NDM-1 and KPC-2. Ann Clin Microbiol Antimicrob 2021; 20: 57.
-
48.
Vilacoba E, Quiroga C, Pistorio M, Famiglietti A, Rodríguez H, Kovensky J, et al. A blaVIM-2 plasmid disseminating in extensively drug-resistant clinical Pseudomonas aeruginosa and Serratia marcescens isolates. Antimicrob Agents Chemother 2014; 58: 7017–7018.
-
49.
Sabtcheva S, Stoikov I, Ivanov IN, Donchev D, Lesseva M, Georgieva S, et al. Genomic characterization of carbapenemase-producing Enterobacter hormaechei, Serratia marcescens, Citrobacter freundii, Providencia stuartii, and Morganella morganii clinical isolates from Bulgaria. Antibiotics 2024; 13: 455.
-
50.
Ambretti S, Bassetti M, Clerici P, Petrosillo N, Tumietto F, Viale P, et al. Screening for carriage of carbapenem-resistant Enterobacteriaceae in settings of high endemicity: a position paper from an Italian working group on CRE infections. Antimicrob Resist Infect Control 2019; 8: 136.
-
51.
Antimicrobial resistance surveillance in Europe surveillance report [2016]. https://ecdc.europa.eu/en/publications-data/antimicrobial-resistance-surveillance-europe-2016.
-
52.
Markovska R, Stoeva T, Boyanova L, Stankova P, Schneider I, Keuleyan E, et al. Multicentre investigation of carbapenemase-producing Klebsiella pneumoniae and Escherichia coli in Bulgarian hospitals – interregional spread of ST11 NDM-1-producing K. pneumoniae. Infect Genet Evol 2019; 69: 61–67.
-
53.
Savova D, Niyazi D, Bozhkova M, Stoeva T. Molecular epidemiology of carbapenem-resistant Enterobacteriaceae isolated from patients in COVID-19 wards and ICUs in a Bulgarian University Hospital. Acta Microbiol Immunol Hung 2023; 70: 142–146.
-
54.
Kostyanev T, Strateva T, Xavier BB, Marteva-Proevska Y, Lammens C, Markova B, et al. Detection and characterization of two NDM-1-producing Klebsiella pneumoniae strains from Bulgaria. J Antimicrob Chemother 2016; 71: 1428–1430.
-
55.
Savov E, Politi L, Spanakis N, Trifonova A, Kioseva E, Tsakris A. NDM-1 hazard in the Balkan States: evidence of the first outbreak of NDM-1-producing Klebsiella pneumoniae in Bulgaria. Microb Drug Resist 2018; 24: 253–259.
-
56.
Markovska R, Stoeva T, Schneider I, Boyanova L, Popova V, Dacheva D, et al. Clonal dissemination of multilocus sequence type ST15 KPC-2-producing Klebsiella pneumoniae in Bulgaria. Acta Pathol Microbiol Scand 2015; 123: 887–894.
-
57.
Tiri B, Sensi E, Marsiliani V, Cantarini M, Priante G, Vernelli C, et al. Antimicrobial stewardship program, COVID-19, and infection control: spread of carbapenem-resistant Klebsiella pneumoniae colonization in ICU COVID-19 patients. What did not work? J Clin Med 2020; 9: 2744.
Editorial Office:
Akadémiai Kiadó Zrt.
Budafoki út 187-187, A/3, H-1117 Budapest, Hungary
Editorial Correspondence:
Acta Microbiologica et Immunologica Hungarica
Institute of Medical Microbiology
Semmelweis University
P.O. Box 370
H-1445 Budapest, Hungary
Phone: + 36 1 459 1500 ext. 56101
Fax: (36 1) 210 2959
E-mail: amih@med.semmelweis-univ.hu
Indexing and Abstracting Services:
- Biological Abstracts
- BIOSIS Previews
- CAB Abstracts
- CABELLS Journalytics
- Chemical Abstracts
- Global Health
- Index Medicus
- Index Veterinarius
- Medline
- Referativnyi Zhurnal
- SCOPUS
- Science Citation Index Expanded
| 2023 | |
|---|---|
| Web of Science | |
| Journal Impact Factor | 1.3 |
| Rank by Impact Factor | Q4 (Immunology) |
| Journal Citation Indicator | 0.31 |
| Scopus | |
| CiteScore | 2.3 |
| CiteScore rank | Q3 (Infectious Diseases) |
| SNIP | 0.389 |
| Scimago | |
| SJR index | 0.308 |
| SJR Q rank | Q3 |
| Acta Microbiologica et Immunologica Hungarica | |
|---|---|
| Publication Model | Hybrid |
| Submission Fee | none |
| Article Processing Charge | 1100 EUR/article (only for OA publications) |
| Regional discounts on country of the funding agency | World Bank Lower-middle-income economies: 50% World Bank Low-income economies: 100% |
| Further Discounts | Editorial Board / Advisory Board members: 50% Corresponding authors, affiliated to an EISZ member institution subscribing to the journal package of Akadémiai Kiadó: 100% |
| Subscription fee 2025 | Online subsscription: 772 EUR / 848 USD Print + online subscription: 860 EUR / 944 USD |
| Subscription Information | Online subscribers are entitled access to all back issues published by Akadémiai Kiadó for each title for the duration of the subscription, as well as Online First content for the subscribed content. |
| Purchase per Title | Individual articles are sold on the displayed price. |
| Acta Microbiologica et Immunologica Hungarica | |
|---|---|
| Language | English |
| Size | A4 |
| Year of Foundation |
1954 |
| Volumes per Year |
1 |
| Issues per Year |
4 |
| Founder | Magyar Tudományos Akadémia |
| Founder's Address |
H-1051 Budapest, Hungary, Széchenyi István tér 9. |
| Publisher | Akadémiai Kiadó |
| Publisher's Address |
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245. |
| Responsible Publisher |
Chief Executive Officer, Akadémiai Kiadó |
| ISSN | 1217-8950 (Print) |
| ISSN | 1588-2640 (Online) |
Monthly Content Usage
| Abstract Views | Full Text Views | PDF Downloads | |
|---|---|---|---|
| Jun 2024 | 0 | 0 | 0 |
| Jul 2024 | 0 | 0 | 0 |
| Aug 2024 | 877 | 16 | 10 |
| Sep 2024 | 260 | 7 | 8 |
| Oct 2024 | 327 | 5 | 8 |
| Nov 2024 | 214 | 4 | 5 |
| Dec 2024 | 9 | 0 | 0 |
Copyright Akadémiai Kiadó AKJournals is the trademark of Akadémiai Kiadó's journal publishing business branch.