Distribution of multidrug-resistant Enterococcus faecalis and Enterococcus faecium isolated from clinical specimens in the Zainoel Abidin General Hospital, Banda Aceh, Indonesia




Abstract. Hayati Z, Desfiana UH, Suhartono S. 2022. Distribution of multidrug-resistant Enterococcus faecalis and Enterococcus faecium isolated from clinical specimens in the Zainoel Abidin General Hospital, Banda Aceh, Indonesia. Biodiversitas 23: 5043-5049. Enterococcus faecalis and Enterococcus faecium are two predominant enterococcal species associated with opportunistic infections, especially in clinical settings. This study aimed to determine the distribution and antibiotic sensitivity of E. faecalis and E. faecium isolated from clinical specimens in the Zainoel Abidin General Hospital during 2019-2022. This study involved isolation, identification, and testing of antibiotic susceptibility of E. faecalis and E. faecium isolates. A total number of 299 enterococcal isolates detected in this study consisting of 233 (7.92%) isolates of E. faecalis and 66 (2.18%) isolates of E. faecium. Both E. faecalis and E. faecium shared phenotypic features in common. Enterococcus faecalis isolates exhibited less sensitivity to benzathine penicillin G, ciprofloxacin, levofloxacin, tetracycline, high-level streptomycin, doxycycline, and fosfomycin. Enterococcus faecium had less sensitive to all tested antibiotics, except for linezolid, vancomycin, and tigecycline. Based on the clinical specimens, enterococci were predominantly found in urine specimens accounting for 42.80%, while based on patient’s age, enterococci were prevalently found in patients aged >46 years accounting for 72%. The distribution of both enterococci was evenly detected in both male and female patients. Based on the wards, enterococci were predominantly detected (50.65%) in patients treated in the internal medicine wards. Overall, the present study suggested the susceptibility of enterococcal pathogens and determined the most effective antimicrobials as empirical therapy to treat the infections. The surveillance programs and infections control should be effectively implemented to manage these multidrug-resistant enterococcal infections particularly within healthcare settings.


Ben Braïek O, Smaoui S. 2019. Enterococci: between emerging pathogens and potential probiotics. BioMed Res Int 2019: 5938210. DOI: https://doi.org/10.1155/2019/5938210.
Bender JK, Cattoir V, Hegstad K, Sadowy E, Coque TM, Westh H, Hammerum AM, Schaffer K, Burns K, Murchan S, Novais C, Freitas AR, Peixe L, Del Grosso M, Pantosti A, Werner G. 2018. Update on prevalence and mechanisms of resistance to linezolid, tigecycline and daptomycin in enterococci in Europe: Towards a common nomenclature. Drug Resist Updat 40: 25-39. DOI: https://doi.org/https://doi.org/10.1016/j.drup.2018.10.002.
Bi R, Qin T, Fan W, Ma P, Gu B. 2018. The emerging problem of linezolid-resistant enterococci. J Glob Antimicrob Resist 13: 11-19. DOI: https://doi.org/https://doi.org/10.1016/j.jgar.2017.10.018.
Billington EO, Phang SH, Gregson DB, Pitout JDD, Ross T, Church DL, Laupland KB, Parkins MD. 2014. Incidence, risk factors, and outcomes for Enterococcus spp. blood stream infections: A population-based study. Int J Infect Dis 26: 76-82. DOI: https://doi.org/10.1016/j.ijid.2014.02.012.
Boccella M, Santella B, Pagliano P, De Filippis A, Casolaro V, Galdiero M, Borrelli A, Capunzo M, Boccia G, Franci G. 2021. Prevalence and antimicrobial resistance of Enterococcus Species: A retrospective cohort study in Italy. Antibiotics 10: 1552. DOI: https://www.mdpi.com/2079-6382/10/12/1552.
Carmeli Y, Eliopoulos G, Mozaffari E, Samore M. 2002. Health and economic outcomes of vancomycin-resistant enterococci. Arch Intern Med 162: 2223-2228. DOI: https://doi.org/10.1001/archinte.162.19.2223.
Cattoir V. 2022. The multifaceted lifestyle of enterococci: genetic diversity, ecology and risks for public health. Curr Opin Microbiol 65: 73-80. DOI: https://doi.org/https://doi.org/10.1016/j.mib.2021.10.013.
Ch’ng J-H, Chong KKL, Lam LN, Wong JJ, Kline KA. 2019. Biofilm-associated infection by enterococci. Nat Rev Microbiol 17: 82-94. DOI: https://doi.org/10.1038/s41579-018-0107-z.
Chaj?cka-Wierzchowska W, Zadernowska A, Zarzecka U, Zakrzewski A, Gajewska J. 2019. Enterococci from ready-to-eat food – horizontal gene transfer of antibiotic resistance genes and genotypic characterization by PCR melting profile. J Sci Food Agric 99: 1172-1179. DOI: https://doi.org/https://doi.org/10.1002/jsfa.9285.
Correa-Martínez CL, Schuler F, Kampmeier S. 2021. Sex differences in vancomycin-resistant enterococci bloodstream infections-a systematic review and meta-analysis. Biol Sex Differ 12: 36. DOI: https://doi.org/10.1186/s13293-021-00380-5.
Jabbari Shiadeh SM, Pormohammad A, Hashemi A, Lak P. 2019. Global prevalence of antibiotic resistance in blood-isolated Enterococcus faecalis and Enterococcus faecium: a systematic review and meta-analysis. Infect Drug Resist 12: 2713-2725. DOI: https://doi.org/10.2147/idr.S206084.
Kajihara T, Nakamura S, Iwanaga N, Oshima K, Takazono T, Miyazaki T, Izumikawa K, Yanagihara K, Kohno N, Kohno S. 2015. Clinical characteristics and risk factors of enterococcal infections in Nagasaki, Japan: a retrospective study. BMC Infect Dis 15: 426. DOI: https://doi.org/10.1186/s12879-015-1175-6.
Kallstrom G, Doern CD, Dunne WM. 2010. Evaluation of a chromogenic agar under development to screen for VRE colonization. J Clin Microbiol 48: 999-1001. DOI: https://doi.org/doi:10.1128/JCM.02011-09.
Manero A, Blanch AR. 1999. Identification of Enterococcus spp. with a biochemical key. Appl Environ Microbiol 65: 4425-4430. DOI: https://doi.org/10.1128/aem.65.10.4425-4430.1999.
Moghimbeigi A, Moghimbeygi M, Dousti M, Kiani F, Sayehmiri F, Sadeghifard N, Nazari A. 2018. Prevalence of vancomycin resistance among isolates of enterococci in Iran: a systematic review and meta-analysis. Adolesc Health Med Ther 9: 177-188. DOI: https://doi.org/10.2147/ahmt.S180489.
Quiloan MLG, Vu J, Carvalho J. 2012. Enterococcus faecalis can be distinguished from Enterococcus faecium via differential susceptibility to antibiotics and growth and fermentation characteristics on mannitol salt agar. Front Biol 7: 167-177. DOI: https://doi.org/10.1007/s11515-012-1183-5.
Sakka V, Tsiodras S, Galani L, Antoniadou A, Souli M, Galani I, Pantelaki M, Siafakas N, Zerva L, Giamarellou H. 2008. Risk-factors and predictors of mortality in patients colonised with vancomycin-resistant enterococci. Clin MicrobioL Infect 14: 14-21. DOI: https://doi.org/10.1111/j.1469-0691.2007.01840.x.
Shrestha S, Kharel S, Homagain S, Aryal R, Mishra SK. 2021. Prevalence of vancomycin-resistant enterococci in Asia—A systematic review and meta-analysis. J Clin Pharm Ther 46: 1226-1237. DOI: https://doi.org/https://doi.org/10.1111/jcpt.13383.
Suhartono S, Mahdani W, Hayati Z, Nurhalimah N. 2021. Species distribution of Enterobacteriaceae and non-Enterobacteriaceae responsible for urinary tract infections at the Zainoel Abidin Hospital in Banda Aceh, Indonesia. Biodiversitas J Biol Divers 22: 3313-3318 .DOI: https://doi.org/10.13057/biodiv/d220826.
Toc DA, Mihaila RM, Botan A, Bobohalma CN, Risteiu GA, Simut-Cacuci BN, Steorobelea B, Troanca S, Junie LM. 2022. Enterococcus and COVID-19: The emergence of a perfect storm? Int J Transl Med 2: 220-229. DOI: https://doi.org/10.3390/ijtm2020020.
Turjeman A, Babich T, Pujol M, Carratalà J, Shaw E, Gomila-Grange A, Vuong C, Addy I, Wiegand I, Grier S, MacGowan A, Vank C, Cuperus N, van den Heuvel L, Leibovici L, Eliakim-Raz N, Group CMWRS, Study S. 2021. Risk factors for enterococcal urinary tract infections: a multinational, retrospective cohort study. Eur J Clin Microbiol Infect Dis 40: 2005-2010. https://doi.org/10.1007/s10096-021-04207-4.

Most read articles by the same author(s)