Sains Malaysiana 52(9)(2023): 2625-2632

http://doi.org/10.17576/jsm-2023-5209-12

Mechanisms of Gentamicin Resistance in Listeria monocytogenes: A Mini Review

(Mekanisme Rintangan Gentamisin dalam Listeria monocytogenes: Suatu Kajian Mini)

HIEN FUH NG^#, JAMIE MAY LING NG^# & YUN FONG NGEOW*

Dr. Wu Lien-Teh Centre for Research in Communicable Diseases, M. Kandiah Faculty of Medicine and Health Sciences, Universiti Tunku Abdul Rahman, Jalan Sungai Long, Bandar Sungai Long, 43000 Kajang, Selangor, Malaysia

Diserahkan: 24 Jun 2023/Diterima: 28 Ogos 2023

Abstract

Listeria monocytogenes is a Gram-positive foodborne pathogen capable of causing a foodborne infectionknown as listeriosis. There are two main types of listeriosis: a non-invasive gastroenteritis and an invasive infection which is often associated with a high mortality and hospitalization rate among susceptible individuals. Gentamicin, used as an adjunct therapy with ampicillin, remains the treatment of choice for the life-threatening invasive listeriosis. Nevertheless, there is little data on gentamicin resistance determinants in L. monocytogenes. Several well-controlled studies have reported that mechanisms of gentamicin resistance in this organism involve active efflux and genetic determinants that affect the uptake of the antibiotic through altered membrane potential. This mini review summarises current knowledge of genetic determinants of gentamicin resistance in L. monocytogenes, with the aim of contributing information that could facilitate the discovery of new therapeutic approaches to overcome, delay or avoid developments of drug resistance in this foodborne pathogen.

Keywords: atpG2; efflux; gentamicin resistance mechanisms; heme gene; Listeria monocytogenes; membrane potential

Abstrak

Listeria monocytogenes ialah patogen bawaan makanan Gram-positif yang mampu menyebabkan jangkitan bawaan makanan yang dikenali sebagai listeriosis. Terdapat dua jenis listeriosis utama: gastroenteritis bukan invasif dan jangkitan invasif yang sering dikaitkan dengan kadar kematian yang tinggi dan kemasukan ke hospital dalam kalangan individu yang terdedah. Gentamisin yang digunakan sebagai terapi tambahan dengan ampisilin, kekal sebagai rawatan pilihan untuk listeriosis invasif yang mengancam nyawa. Namun begitu, terdapat sedikit data tentang penentu rintangan gentamisin dalam L. monocytogenes. Beberapa kajian terkawal telah melaporkan bahawa mekanisme rintangan gentamisin dalam organisma ini melibatkan efluks aktif dan penentu genetik yang mempengaruhi pengambilan antibiotik melalui potensi membran yang diubah. Kajian mini ini meringkaskan pengetahuan semasa tentang penentu genetik rintangan gentamisin dalam L. monocytogenes bertujuan untuk menyumbang maklumat yang boleh memudahkan penemuan pendekatan terapeutik baharu untuk mengatasi, menangguhkan atau mengelakkan perkembangan rintangan dadah dalam patogen bawaan makanan ini.

Kata kunci: atpG2; efluks; gen heme; Listeria monocytogenes; mekanisme rintangan gentamisin; potensi membran

RUJUKAN

Beganovic, M., Luther, M.K., Rice, L.B., Arias, C.A., Rybak, M.J. & Laplante, K.L. 2018. A review of combination antimicrobial therapy for Enterococcus faecalis bloodstream infections and infective endocarditis. Clinical Infectious Diseases 67(2): 303.

Bremer, P.J., Monk, I. & Osborne, C.M. 2001. Survival of Listeria monocytogenes attached to stainless steel surfaces in the presence or absence of Flavobacterium spp. Journal of Food Protection 64(9): 1369-1376.

Brouwer, M.C., Van De Beek, D., Heckenberg, S.G.B., Spanjaard, L. & De Gans, J. 2006. Community-acquired Listeria monocytogenes meningitis in adults. Clinical Infectious Diseases 43(10): 1233-1238.

Bryan, L.E., Kowand, S.K. & Van den Elzen, H.M. 1979. Mechanism of aminoglycoside antibiotic resistance in anaerobic bacteria: Clostridium perfringensand Bacteroides fragilis. Antimicrobial Agents and Chemotherapy 15(1): 7-13.

Buchanan, R.L., Gorris, L.G.M., Hayman, M.M., Jackson, T.C. & Whiting, R.C. 2017. A review of Listeria monocytogenes: An update on outbreaks, virulence, dose-response, ecology, and risk assessments. Food Control 75: 1-13.

Castellazzi, M.L., Marchisio, P. & Bosis, S. 2018. Listeria monocytogenes meningitis in immunocompetent and healthy children: A case report and a review of the literature. Italian Journal of Pediatrics 44(1): 152.

Chaves, B. 2023. Gentamicin - StatPearls - NCBI Bookshelf.

Christensen, E.G., Gram, L. & Kastbjerg, V.G. 2011. Sublethal triclosan exposure decreases susceptibility to gentamicin and other aminoglycosides in Listeria monocytogenes. Antimicrobial Agents and Chemotherapy 55(9): 4064.

CLSI. 2016. CLSI Supplement M100S 26th ed. In Clinical and Laboratory Standards Institute, edited by Wayne, P.A.

Crum, N.F. 2002. Update on Listeria monocytogenes infection. Current Gastroenterology Reports 4(4): 287-296.

Curtis, T.D., Gram, L. & Knudsen, G.M. 2016. The small colony variant of Listeria monocytogenes is more tolerant to antibiotics and has altered survival in raw 264.7 murine macrophages. Frontiers in Microbiology 7(JUL): 1056.

Dalton, C.B., Austin, C.C., Sobel, J., Hayes, P.S., Bibb, W.F., Graves, L.M., Swaminathan, B., Proctor, M.E. & Griffin, P.M. 1997. An outbreak of gastroenteritis and fever due to Listeria monocytogenes in milk. The New England Journal of Medicine 336(2): 100-106.

Desai, A.N., Anyoha, A., Madoff, L.C. & Lassmann, B. 2019. Changing epidemiology of Listeria monocytogenes outbreaks, sporadic cases, and recalls globally: A review of ProMED reports from 1996 to 2018. International Journal of Infectious Diseases 84: 48-53.

Elsayed, M.M., Elkenany, R.M., Zakaria, A.I. & Badawy, B.M. 2022. Epidemiological study on Listeria monocytogenes in Egyptian dairy cattle farms’ insights into genetic diversity of multi-antibiotic-resistant strains by ERIC-PCR. Environmental Science and Pollution Research 29(36): 54359-54377.

EUCAST. 2023. Clinical breakpoints and dosing of antibiotics. https://www.eucast.org/clinical_breakpoints. Accessed on 24 April 2023.

Fharok, M.Y. 2019. Incidence of Listeria monocytogenes in dairy and food products of animal origin in central region of peninsular Malaysia. Malaysian Journal of Veterinary Research 10(2): 106-112.

Freitag, N.E., Port, G.C. & Miner, M.D. 2009. Listeria monocytogenes - from saprophyte to intracellular pathogen. Nature Reviews Microbiology 7(9): 623-628.

Gandhi, M. & Chikindas, M.L. 2007. Listeria: A foodborne pathogen that knows how to survive. International Journal of Food Microbiology 113(1): 1-15.

Godreuil, S., Galimand, M., Gerbaud, G., Jacquet, C. & Courvalin, P. 2003. Efflux pump lde is associated with fluoroquinolone resistance in Listeria monocytogenes. Antimicrobial Agents and Chemotherapy 47(2): 704-708.

Goulet, V., Hebert, M., Hedberg, C., Laurent, E., Vaillant, V., De Valk, H. & Desenclos, J.C. 2012. Incidence of listeriosis and related mortality among groups at risk of acquiring listeriosis. Clinical Infectious Diseases 54(5): 652-660.

Hof, H. 2004. An update on the medical management of listeriosis. Expert Opinion on Pharmacotherapy 5(8): 1727-1735.

Horaud, T., De Céspèdes, G. & Trieu-Cuot, P. 1996. Chromosomal gentamicin resistance transposon Tn3706 in Streptococcus agalactiae B128. Antimicrobial Agents and Chemotherapy 40(5): 1085-1090.

Jamali, H., Chai, L.C. & Thong, K.L. 2013. Detection and isolation of Listeria spp. and Listeria monocytogenes in ready-to-eat foods with various selective culture media. Food Control 32(1): 19-24.

Kastbjerg, V.G., Hein-Kristensen, L. & Gram, L. 2014. Triclosan-induced aminoglycoside-tolerant Listeria monocytogenes isolates can appear as small-colony variants. Antimicrobial Agents and Chemotherapy 58(6): 3124.

Knudsen, G.M., Fromberg, A., Ng, Y. & Gram, L. 2016. Sublethal concentrations of antibiotics cause shift to anaerobic metabolism in Listeria monocytogenes and induce phenotypes linked to antibiotic tolerance. Frontiers in Microbiology 7: 1091.

Kohler, V., Vaishampayan, A. & Grohmann, E. 2018. Broad-host-range Inc18 plasmids: Occurrence, spread and transfer mechanisms. Plasmid 99: 11-21.

Kuan, C.H., Rukayadi, Y., Ahmad, S.H., Wan, C.W.J., Radzi, M., Thung, T.Y., Premarathne, J.M.K.J.K., Chang, W.S., Loo, Y.Y., Tan, C.W., Ramzi, O.B., Fadzil, S.N.M., Kuan, C.S., Yeo, S.K., Nishibuchi, M. & Radu, S. 2017. Comparison of the microbiological quality and safety between conventional and organic vegetables sold in Malaysia. Frontiers in Microbiology 8(1433): 1-10.

Kuch, A., Goc, A., Belkiewicz, K., Filipello, V., Ronkiewicz, P., Gołębiewska, A., Wróbel, I., Kiedrowska, M., Waśko, I., Hryniewicz, W., Lomonaco, S. & Skoczyńska, A. 2018. Molecular diversity and antimicrobial susceptibility of Listeria monocytogenes isolates from invasive infections in Poland (1997-2013). Scientific Reports 8: 14562.

Leclercq, R., Dutka-Malen, S., Brisson-Noël, A., Molinas, C., Derlot, E., Arthur, M., Duval, J. & Courvalin, P. 1992. Resistance of enterococci to aminoglycosides and glycopeptides. Clinical Infectious Diseases 15(3): 495-501.

Lewis, K. 2001. Riddle of biofilm resistance. Antimicrobial Agents and Chemotherapy 45(4): 999-1007.

Low, J.C. & Donachie, W. 1997. A review of Listeria monocytogenes and listeriosis. The Veterinary Journal 153(1): 9-29.

Luque-Sastre, L., Arroyo, C., Fox, E.M., McMahon, B.J., Bai, L., Li, F. & Fanning, S. 2018. Antimicrobial resistance in Listeria species. Microbiology Spectrum 6: 4.

Mates, S.M., Eisenberg, E.S., Mandel, L.J., Patel, L., Kaback, H.R. & Miller, M.H. 1982. Membrane potential and gentamicin uptake in Staphylococcus aureus. Proceedings of the National Academy of Sciences of the United States of America 79(21 I): 6693-6697.

McNamara, P.J. & Proctor, R.A. 2000. Staphylococcus aureus small colony variants, electron transport and persistent infections. International Journal of Antimicrobial Agents 14(2): 117-122.

Moazed, D. & Noller, H.F. 1987. Interaction of antibiotics with functional sites in 16S ribosomal RNA. Nature 327(6121): 389-394.

Mylonakis, E., Hohmann, E.L. & Calderwood, S.B. 1998. Central nervous system infection with Listeria monocytogenes. 33 years’ experience at a general hospital and review of 776 episodes from the literature. Medicine 77(5): 313-336.

Ng, J.M.L., Ngeow, Y.F., Saw, S.H., Ng, H.F. & Zin, T. 2022. Mutations in atpG2 may confer resistance to gentamicin in Listeria monocytogenes. Journal of Medical Microbiology 71(12): 001618.

Noll, M., Kleta, S. & Al Dahouk, S. 2018. Antibiotic susceptibility of 259 Listeria monocytogenes strains isolated from food, food-processing plants and human samples in Germany. Journal of Infection and Public Health 11(4): 572-577.

Nwaiwu, O. 2020. What are the recognized species of the genus Listeria? Access Microbiology 2(9): acmi000153.

Obaidat, M.M., Bani Salman, A.E., Lafi, S.Q. & Al-Abboodi, A.R. 2015. Characterization of Listeria monocytogenesfrom three countries and antibiotic resistance differences among countries and Listeria monocytogenes serogroups. Letters in Applied Microbiology 60(6): 609-614.

Olaimat, A.N., Al-Holy, M.A., Shahbaz, H.M., Al-Nabulsi, A.A., Abu Ghoush, M.H., Osaili, T.M., Ayyash, M.M. & Holley, R.A. 2018. Emergence of antibiotic resistance in Listeria monocytogenes isolated from food products: A comprehensive review. Comprehensive Reviews in Food Science and Food Safety 17(15): 1277-1292.

Orsi, R.H. & Wiedmann, M. 2016. Characteristics and distribution of Listeria spp., including Listeria species newly described since 2009. Applied Microbiology and Biotechnology 100(12): 5273-5287.

Prazak, A.M., Murano, E.A., Mercado, I. & Acuff, G.R. 2002. Antimicrobial resistance of Listeria monocytogenes isolated from various cabbage farms and packing sheds in Texas. Journal of Food Protection 65(11): 1796-1799.

Rakic-Martinez, M., Drevets, D.A., Dutta, V., Katic, V. & Kathariou, S. 2011. Listeria monocytogenes strains selected on ciprofloxacin or the disinfectant benzalkonium chloride exhibit reduced susceptibility to ciprofloxacin, gentamicin, benzalkonium chloride, and other toxic compounds. Applied and Environmental Microbiology 77(24): 8714-8721.

Ramaswamy, V., Cresence, V.M., Rejitha, J.S., Lekshmi, U., Dharsana, K.S., Prasad, P. & Vijila, M. 2007. Listeria-review of epidemiology and pathogenesis. Journal of Microbiology, Immunology and Infection 40: 4-13.

Ramirez, M.S. & Tolmasky, M.E. 2010. Aminoglycoside modifying enzymes. Drug Resistance Updates 13(6): 151.

Reda, W.W., Abdel-Moein, K., Hegazi, A., Mohamed, Y. & Abdel-Razik, K. 2016. Listeria monocytogenes: An emerging food-borne pathogen and its public health implications. Journal of Infection in Developing Countries 10(2): 149-154.

Scallan, E., Hoekstra, R.M., Angulo, F.J., Tauxe, R.V., Widdowson, M.A., Roy, S.L., Jones, J.L. & Griffin, P.M. 2011. Foodborne illness acquired in the United States--major pathogens. Emerging Infectious Diseases 17(1): 7-15.

Somer, L. & Kashi, Y. 2003. A PCR method based on 16S rRNA sequence for simultaneous detection of the genus Listeria and the species Listeria monocytogenes in food products. Journal of Food Protection 66(9): 1658-1665.

Sparo, M., Delpech, G. & Allende, N.G. 2018. Impact on public health of the spread of high-level resistance to gentamicin and vancomycin in enterococci. Frontiers in Microbiology 9: 3073.

Srinivasan, V., Nam, H.M., Nguyen, L.T., Tamilselvam, B., Murinda, S.E. & Oliver, S.P. 2005. Prevalence of antimicrobial resistance genes in Listeria monocytogenes isolated from dairy farms. Foodborne Pathogens and Disease 2(3): 201-211.

Su, M., Satola, S.W. & Read, T.D. 2019. Genome-based prediction of bacterial antibiotic resistance. Journal of Clinical Microbiology 57(3): 1405-1418.

Temple, M.E. & Nahata, M.C. 2000. Treatment of listeriosis. Annals of Pharmacotherapy 34(5): 656-661.

Tilney, L.G. & Portnoy, D.A. 1989. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. The Journal of Cell Biology 109(4 Pt 1): 1597-1608.

Tsakris, A.A., Douboyas, P.J. & Antoniadis, A. 1997. Neonatal meningitis due to multi-resistant Listeria monocytogenes. The Journal of Antimicrobial Chemotherapy 39(4): 553-554.

Vicente, M.F., Baquero, F. & Pérez-Diaz, J.C. 1988. Conjugative acquisition and expression of antibiotic resistance determinants in Listeria spp. Journal of Antimicrobial Chemotherapy 21(3): 309-318.

Wai, G.Y., Tang, J.Y.H., Alias, N., Kuan, C.H., Goh, S.G. & Radu, S. 2020. Risk of acquiring listeriosis from consumption of chicken offal among high risk group. Malaysian Journal of Fundamental and Applied Sciences 16(1): 59-63.

Winslow, D.L., Damme, J. & Dieckman, E. 1983. Delayed bactericidal activity of p-lactam antibiotics against Listeria monocytogenes: Antagonism of chloramphenicol and rifampin. Antimicrobial Agents and Chemotherapy 23(4): 555-558.

Wiśniewski, P., Zakrzewski, A.J., Zadernowska, A. & Chajęcka-Wierzchowska, W. 2022. Antimicrobial resistance and virulence characterization of Listeria monocytogenes strains isolated from food and food processing environments. Pathogens 11(10): 1099.

Zunabovic, M., Domig, K.J. & Kneifel, W. 2011. Practical relevance of methodologies for detecting and tracing of Listeria monocytogenes in ready-to-eat foods and manufacture environments - A review. LWT - Food Science and Technology 44(2): 351-362.

*Pengarang untuk surat-menyurat; email: ngeowyf@utar.edu.my