Distribution of antimicrobial resistance among clinical and food Listeria monocytogenes isolated in Moscow in 2019–2021

Clinical Microbiology and Antimicrobial Chemotherapy. 2022; 24(2):156-164

​ Ermolaeva S.A., Karpova T.I., Andriyanov P.A., Zhurilov P.A., Voronina O.L., Ryzhova N.N., Aksenova E.I., Kunda M.S., Liskova E.A., Gruzdeva O.A., Klimova E.A., Posukhovsky E.A., Karetkina G.N., Melkumyan A.R., Orlova O.E., Burmistrova E.N., Pronina T.V., Tartakovsky I.S.
10.36488/cmac.2022.2.156-164
Listeria monocytogenes listeriosis antimicrobial resistance
Section
Antimicrobial Resistance
Type
Original Article
Publication
Clinical Microbiology and Antimicrobial Chemotherapy. 2022; 24(2):156-164

Objective.

To determine the current state-of-art of acquired resistance to antimicrobial drugs among L. monocytogenes strains associated with listeriosis in humans and food contamination in Moscow.

Materials and Methods.

We used 39 L. monocytogenes strains isolated in Moscow in 2019–2021 from clinical material (n = 24) and food (n = 15). Resistance to 12 antibiotics of the first and second lines of defense was studied using disk-diffusion method. The parameters recommended for L. monocytogenes were used to interpret the results; in the absence of recommendations for L. monocytogenes, the criteria for Staphylococcus aureus and/or Enterococcus spp. were used.

Results.

All strains were susceptible to ampicillin, benzylpenicillin, erythromycin, vancomycin, imipenem, linezolid, and the amoxicillin/clavulanic acid. Resistance was observed to gentamicin (23%) as well as to meropenem, trimethoprim/sulfamethoxazole and ciprofloxacin (5%, 74% and 28% of strains, respectively). A total of 15 strains with multiple antibiotic resistance were identified (13 and 2 isolates were resistant to three and four antibiotics, respectively). Simultaneous resistance to trimethoprim/sulfamethoxazole, ciprofloxacin and levofloxacin was observed in 9 strains, 6 strains were resistant to gentamicin and trimethoprim/sulfamethoxazole, including 3 strains – to gentamicin, trimethoprim/sulfamethoxazole, levofloxacin, and 2 strains – to gentamicin, trimethoprim/sulfamethoxazole, ciprofloxacin. Comparison of the growth inhibition zones by ampicillin and benzylpenicillin in the studied strains with historical data on the strains isolated in Russia in 1950–1980 showed a significant downward shift in the size of growth inhibition zones. Comparison of the distribution of strains with different diameters of growth inhibition zones depending on the source of isolation did not show significant differences between clinical strains and strains of food origin isolated in 2019–2021.

Conclusions.

A wide spread of acquired resistance was shown among L. monocytogenes strains of clinical and food origin isolated in Moscow in 2019–2021. Despite the fact that all strains were susceptible to penicillins, the distribution of growth inhibition zone diameters showed a significant shift towards decreasing sensitivity to ampicillin and benzylpenicillin in strains isolated in 2019–2021 compared with L. monocytogenes strains isolated in Russia before 1980.

Svetlana A. Ermolaeva

N.F. Gamaleya National Research Center of Epidemiology and Microbiology, Moscow, Russia
Nizhny Novgorod Research Veterinary Institute – Branch of Federal Research Center for Virology and Microbiology, Nizhny Novgorod, Russia

Karpova T.I.

N.F. Gamaleya National Research Center of Epidemiology and Microbiology, Moscow, Russia

Andriyanov P.A.

Nizhny Novgorod Research Veterinary Institute – Branch of Federal Research Center for Virology and Microbiology, Nizhny Novgorod, Russia

Zhurilov P.A.

Nizhny Novgorod Research Veterinary Institute – Branch of Federal Research Center for Virology and Microbiology, Nizhny Novgorod, Russia

Olga L. Voronina

N.F. Gamaleya National Research Center of Epidemiology and Microbiology, Moscow, Russia

Ryzhova N.N.

N.F. Gamaleya National Research Center of Epidemiology and Microbiology, Moscow, Russia

Aksenova E.I.

N.F. Gamaleya National Research Center of Epidemiology and Microbiology, Moscow, Russia

Kunda M.S.

N.F. Gamaleya National Research Center of Epidemiology and Microbiology, Moscow, Russia

Liskova E.A.

Nizhny Novgorod Research Veterinary Institute – Branch of Federal Research Center for Virology and Microbiology, Nizhny Novgorod, Russia

Gruzdeva O.A.

Russian Medical Academy of Continuous Professional Education, Moscow, Russia

Klimova E.A.

A.I. Yevdokimov Moscow State University of Medicine and Dentistry, Moscow, Russia

Posukhovsky E.A.

A.I. Yevdokimov Moscow State University of Medicine and Dentistry, Moscow, Russia

Karetkina G.N.

A.I. Yevdokimov Moscow State University of Medicine and Dentistry, Moscow, Russia

Melkumyan A.R.

City Clinical Hospital named after F.I. Inozemtsev, Moscow, Russia

Orlova O.E.

City Clinical Hospital No. 67 named after L.A. Vorokhobov, Moscow, Russia

Burmistrova E.N.

City Clinical Hospital named after S.S. Yudin, Moscow, Russia

Pronina T.V.

City Infectious Clinical Hospital No. 1, Moscow, Russia

Tartakovsky I.S.

N.F. Gamaleya National Research Center of Epidemiology and Microbiology, Moscow, Russia

  • 1. Tartakovsky I., Maleev V., Ermolaeva S. Listeria: role in human infectious pathology and laboratory diagnostics. Medicina dlja vseh: Moscow, 2002. ISBN 5-93649-0076. Russian.
  • 2. Allerberger F., Wagner M. Listeriosis: a resurgent foodborne infection. Clin Microbiol Infect. 2010;16:16-23. DOI: 10.1111/J.1469-0691.2009.03109.X
  • 3. Pagliano P., Arslan F., Ascione T. Epidemiology and treatment of the commonest form of listeriosis: meningitis and bacteraemia. Le Infez Med. 2017;25:210-216. PMID: 28956537
  • 4. de Noordhout C.M., Devleesschauwer B., Angulo F.J., Verbeke G., Haagsma J., Kirk M., et al. The global burden of listeriosis: a systematic review and meta-analysis. Lancet Infect Dis. 2014;14:1073-1082. DOI: 10.1016/S14733099(14)70870-9
  • 5. Lamont R., Sobel J., Mazaki-Tovi S., Kusanovic J., Vaisbuch E., Kim S., et al. Listeriosis in human pregnancy: a systematic review. J Perinat Med. 2011;39:227-236. DOI: 10.1515/JPM.2011.035
  • 6. Ragon M., Wirth T., Hollandt F., Lavenir R., Lecuit M., Le Monnier A., et al. A new perspective on Listeria monocytogenes evolution. PLoS Pathog. 2008;4:e1000146. DOI: 10.1371/journal.ppat.1000146
  • 7. Orsi R.H., Bakker H.C., Wiedmann M. Listeria monocytogenes lineages: genomics, evolution, ecology, and phenotypic characteristics. Int J Med Microbiol. 2011;301:7996. DOI: 10.1016/j.ijmm.2010.05.002
  • 8. Psareva E., Egorova I., Liskova E., Razheva I., Gladkova N., Sokolova E., et al. Retrospective study of Listeria monocytogenes isolated in the territory of inner Eurasia from 1950 to 1999. Pathogens. 2019;8(4):184. DOI: 10.3390/pathogens8040184
  • 9. Voronina O., Ryzhova N., Kunda M., Kurnaeva M., Semenov A., Aksenova E., et al. Diversity and pathogenic potential of Listeria monocytogenes isolated from environmental sources in the Russian Federation. Int J Mod Emg Res. 2015;5:5-13. DOI: 10.3390/foods10112790
  • 10. Voronina O.L., Kunda M.S., Ryzhova N.N., Kutuzova A.V., Aksenova E.I., Karpova T.I., et al. Listeriosis: genotyping as a key for identification a possible source of infection. Kliniceskaa mikrobiologia i antimikrobnaa himioterapia. 2019;21:261273. Russian. DOI: 10.36488/cmac.2019.4.261-273
  • 11. Charlier C., Perrodeau E., Leclercq A., Cazenave B., Pilmis B., Henry B., et al. Clinical features and prognostic factors of listeriosis: the MONALISA national prospective cohort study. Lancet Infect Dis. 2017;17:510-519. DOI: 10.1016/S1473-3099(16)30521-7
  • 12. Troxler R., von Graevenitz A., Funke G., Wiedemann B., Stock I. Natural antibiotic susceptibility of Listeria species: L. grayi, L. innocua, L. ivanovii, L. monocytogenes, L. seeligeri and L. welshimeri strains. Clin Microbiol Infect. 2000;6:525535. DOI: 10.1046/J.1469-0691.2000.00168.X
  • 13. Temple M., Nahata M. Treatment of listeriosis. Ann Pharmacother. 2000;34:656-661. DOI: 10.1345/APH.19315
  • 14. Andriyanov P.A., Zhurilov P.A., Liskova E.A., Karpova T.I., Sokolova E.V., Yushina Y.K., et al. Antimicrobial resistance of Listeria monocytogenes strains isolated from humans, animals, and food products in Russia in 1950-1980, 20002005, and 2018-2021. Antibiotics. 2021;10(10):1206. DOI: 10.3390/antibiotics10101206
  • 15. Morvan A., Moubareck C., Leclercq A., Hervé-Bazin M., Bremont S., Lecuit M., et al. Antimicrobial resistance of Listeria monocytogenes strains isolated from humans in France. Antimicrob Agents Chemother. 2010;54:27282731. DOI: 10.1128/AAC.01557-09
  • 16. Noll M., Kleta S., Al Dahouk S. Antibiotic susceptibility of 259 Listeria monocytogenes strains isolated from food, food-processing plants and human samples in Germany. J Infect Public Health. 2018;11:572-577. DOI: 10.1016/J.JIPH.2017.12.007
  • 17. GOST 32031-2012. Food products. Methods for detection of Listeria monocytogenes (with correction in the Information index "National standards" N 6-2019). Russian.
  • 18. Eurasian Economic Commission. Uniform Sanitary Epidemiological and Hygienic Requirements for the Goods Subject to Sanitary and Epidemiological Supervision (Control). Available at: www.eurasiancommission.org/en/act/texnreg/depsanmer/sanmeri/Pages/P2_299.aspx. Accessed April 2022.
  • 19. Rakhmanova A., Prigogine V. Listeriosis. Chapter: Handbook of Infectious Diseases. St. Petersburg, 1999. P. 172174. Russian.
  • 20. Listeriosis. Chapter: Guide to the epidemiology of infectious diseases. Volume 2. Edited by Briko N.I., Onishchenko G.G., Pokrovsky V.I. M: LLC Publishing House Medical Information Agency, 2019. 1648 p. Russian.
  • 21. Office of Rospotrebnadzor in Moscow. State report on the state of sanitary and epidemiological well-being of the population in Moscow in 2020; Moscow, 2021. Russian.
  • 22. Melkumyan A.R., Tsibin A.N. Microbiological service of Moscow: ways of optimization and model of reorganizatIon. Laboratornaja sluzhba. 2018;7:115-116. Russian.
  • 23. Susceptibility testing of microorganisms to antimicrobial drugs (2021). Version 2021-01. IACMAC. Available at: www.antibiotic.ru/files/321/clrec-dsma2021.pdf. Accessed April 2022. Russian.
  • 24. Iwu C., Okoh A. Characterization of antibiogram fingerprints in Listeria monocytogenes recovered from irrigation water and agricultural soil samples. PLoS One. 2020;15:e0228956. DOI: 10.1371/JOURNAL.PONE.0228956
  • 25. Sanlıbaba P., Tezel B.U., Cakmak G.A. Prevalence and antibiotic resistance of Listeria monocytogenes isolated from ready-to-eat foods in Turkey. J Food Qual. 2018;7693782. DOI: 10.1155/2018/7693782
  • 26. Voronina O.L., Tartakovsky I.S., Yuyshuk N.D., Ryzhova N.N., Aksenova E.I., Kunda M.S., et al. Analysis of sporadic cases of invasive listeriosis in a metropolis. Zhurnal mikrobiologii, jepidemiologii i immunobiologii. 2020; 97(6):547-555. Russian. DOI: 10.36233/0372-9311-2020-976-3
  • 27. Kutuzova A.V., Ryzhova N.N., Kunda M.S., Aksenova E.I., Tikulmina A.N., Klimova E.A., et al. Impact of the COVID-19 pandemic on pathogens of perinatal invasive listeriosis. Detskie infekcii. 2021;20(1S):60-61. Russian.
  • 28. Klimova E.A., Voronina O.L., Karetkina G.N., Posukhovsky E.A., Ryzhova N.N., Kunda M.S., et al. Listeriosis and the COVID-19 pandemic. Infekcionnye bolezni: novosti, mnenija, obuchenie. 2022;11(1):102-112. Russian. DOI: 10.33029/2305-3496-2022-11-1-102-112
  • 29. Fischer M., Wamp S., Fruth A., Allerberger F., Flieger A., Halbedel S. Population structure-guided profiling of antibiotic resistance patterns in clinical Listeria monocytogenes isolates from Germany identifies pbpB3 alleles associated with low levels of cephalosporin resistance. Emerg Microbes Infect. 2020:9:1804-1813. DOI: 10.1080/22221751.2020.1799722
  • 30. Capita R., Felices-Mercado A., García-Fernández C., AlonsoCalleja C. Characterization of Listeria monocytogenes originating from the Spanish meat-processing chain. Foods. 2019;8(11):542. DOI: 10.3390/foods8110542
  • 31. Maćkiw E., Stasiak M., Kowalska J., Kucharek K., Korsak D., Postupolski J. Occurrence and characteristics of Listeria monocytogenes in ready-to-eat meat products in Poland. J Food Prot. 2020;83:1002-1009. DOI: 10.4315/JFP-19525
  • 32. Rezai R., Ahmadi E., Salimi B. Prevalence and antimicrobial resistance profile of Listeria species isolated from farmed and on-sale rainbow trout (Oncorhynchus mykiss) in Western Iran. J Food Prot. 2018;81:886-891. DOI: 10.4315/0362-028X.JFP-17-428
  • 33. Tsakris A., Papa A., Douboyas J., Antoniadis A. Neonatal meningitis due to multi-resistant Listeria monocytogenes. J Antimicrob Chemother. 1997;39:553-554. DOI: 10.1093/JAC/39.4.553
  • 34. Korsak D., Borek A., Daniluk S., Grabowska A., Pappelbaum K. Antimicrobial susceptibilities of Listeria monocytogenes strains isolated from food and food processing environment in Poland. Int J Food Microbiol. 2012;158:203208. DOI: 10.1016/J.IJFOODMICRO.2012.07.016
Views
0 Abstract
0 PDF
0 Crossref citations
Shared