Journal of Food and Nutrition Research
ISSN (Print): 2333-1119 ISSN (Online): 2333-1240 Website: http://www.sciepub.com/journal/jfnr Editor-in-chief: Prabhat Kumar Mandal
Open Access
Journal Browser
Go
Journal of Food and Nutrition Research. 2018, 6(10), 626-637
DOI: 10.12691/jfnr-6-10-3
Open AccessArticle

Prevalence of Antibiotic Resistance in Enterococci: A 14 Year Survey

Carmela Calonico1, , Giovanna Pesavento1, Vania Delfino1, Sara Forni1 and Antonella Lo Nostro1

1Department of Health Sciences, University of Florence, Florence, Italy

Pub. Date: October 26, 2018

Cite this paper:
Carmela Calonico, Giovanna Pesavento, Vania Delfino, Sara Forni and Antonella Lo Nostro. Prevalence of Antibiotic Resistance in Enterococci: A 14 Year Survey. Journal of Food and Nutrition Research. 2018; 6(10):626-637. doi: 10.12691/jfnr-6-10-3

Abstract

Enterococci are leading causes of nosocomial bacteremia, surgical wound and urinary tract infections. They are ubiquitous bacteria commonly occurring in foods, and in recent years there has been increased attention towards multidrug strains incidence, since they may cause the failure of therapeutic treatments. Therefore, we analyzed the occurrence of Enterococcus species isolated from raw meat (beef, chicken and pork), cheese, and ready-to-eat salads, and the change of the antibiotic resistance in Enterococcus faecium and E. faecalis strains in a 14 year survey. Among the 589 Enterococcus strains, E. faecium and E. faecalis represented the most numerous species in all types of food examined (42.8% and 38.7% respectively). Antibiotic resistance and number of Multi Drug Resistant strains have increased, reaching very high levels from 2002 to 2015. In the last two years, E. faecalis isolates sometimes reached percentages of resistance higher than 40% against tetracycline, vancomycin, linezolid, erythromycin, and ampicillin. Antibiotic resistance in E. faecium was lower than in E. faecalis for almost all antimicrobials tested. The highest percentage of resistance in 2014-2015 was registered for erythromycin (42.5%), followed by tetracycline (30%), ciprofloxacin, and linezolid (both 27.5%). The number of resistant phenotypes also increased during this survey in both species to more than 20 in 2014-2015. Despite the fact that Enterococcus spp. do not represent a problem for immunocompetent individuals, surveillance of antibiotic resistance in this kind of micro-organism continues to be important because, as shown in our results, antibiotic resistance has sharply increased in recent years.

Keywords:
Enterococcus raw meat cheese salads Multi Drug Resistance survey

Creative CommonsThis work is licensed under a Creative Commons Attribution 4.0 International License. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

References:

[1]  Giraffa, G., “Enterococci from foods”, FEMS Microbiol. Rev. 2002, 26: 163-171.
 
[2]  Ronconi, M.C., Merino, L.A. and Fernández, G., “Detection of Enterococcus with high-level aminoglycoside and glycopeptide resistance in Lactuca sativa (lettuce)”, Enferm. Infecc. Microbiol. Clin. 2002, 20: 380-383.
 
[3]  Torre, I., Pennino, F., Diana, M.V., De Marco, G., Trotta, A.M., Borriello, T. and Troiano, E., “Antimicrobial susceptibility and glycopeptide-resistance of enterococci in vegetables”, Ital. J. Public Health. 2010, 7: 47-53.
 
[4]  Wheeler, A.L., Hartel, P.G, Godfrey, D.G, Hill, J.L., and Segars, W.I., “Potential of Enterococcus faecalis as a human fecal indicator for microbial source tracking”, J. Environ. Qual. 2002, 31: 1286-1293.
 
[5]  Cocolin, L., Foschino, R., Comi, G. and Fortina, M.G., “Description of the bacteriocins produced by two strains of Enterococcus faecium isolated from Italian goat milk”, Food Microbiol. 2007, 24:752-758.
 
[6]  Foulquié Moreno, M.R, Sarantinopoulos, P., Tsakalidou, E. and De Vuyst, L., “The role and application of Enterococci in food and health”, Int. J. Food Microbiol. 2006, 106:1-24.
 
[7]  Ali, S.A., Hasan, K.A., Bin Asif, H. and Abbasi, A., “Environmental enterococci: Prevalence of virulence, antibiotic resistance and species distribution in poultry and its related environment in Karachi, Pakistan”, Lett. Appl. Microbiol. 2013, 58:423-432.
 
[8]  Furlaneto-Maia, L., Real Rocha, K., Henrique, F.C., Giazzi, A. and Furlaneto Márcia, C., “Antimicrobial Resistance in Enterococcus sp isolated from soft cheese in Southern Brazil”, Adv. Microbiol. 2014, 4: 175-181.
 
[9]  Hayes, J.R., English, L.L., Carter, P.J., Proescholdt, T., Lee, K.Y., Wagner, D.D. and White, D.G., “Prevalence and Antimicrobial Resistance of Enterococcus Species Isolated from Retail Meats”, Appl. Env. Microbiol. 2003, 69: 7153-7160.
 
[10]  Jahan, M., Krause, D.O. and Holley, R.A., “Antimicrobial resistance of Enterococcus species from meat and fermented meat products isolated by a PCR-based rapid screening method”, Int. J. Food Microbiol. 2013, 163: 89-95.
 
[11]  Klein, G., Pack, A. and Reuter, G., “Antibiotic resistance patterns of enterococci and occurrence of vancomycin-resistant enterococci in raw minced beef and pork in Germany”, Appl. Env. Microbiol. 1998, 64: 1825-1830.
 
[12]  Li, P., Wu, D., Liu, K., Suolang, S., He, T., Liu, X., Wu, C., Wang, Y. and Lin, D., “Investigation of Antimicrobial Resistance in Escherichia coli and Enterococci Isolated from Tibetan Pigs”, PLoS ONE. 2014, 9(4):e95623.
 
[13]  Moore, D.F., Guzman, J.A. and McGee, C., “Species distribution and antimicrobial resistance of enterococci isolated from surface and ocean water”, J. Appl. Microbiol. 2008, 105: 1017-1025.
 
[14]  Turtura, G.C. and Lorenzelli, P., “Gram-positive cocci isolated from slaughtered poultry”, Microbiol. Res. 1994, 149: 203-213.
 
[15]  Alfonsi, V., Camilli, R., Del Manso, M., D’Ambrosio, F., D’Ancona, F., Del Grosso, M., Giannitelli, S., Monaco, M., Sanchini, A., Sisto, A., Pantosti, A. e i referenti dei laboratori AR-ISS, “AR-ISS: sorveglianza dell’antibiotico-resistenza in Italia. Rapporto del triennio 2006-2008. Rapporti Istisan 10/37”, Istituto Superiore di Sanità. [Online]. Available: http://old.iss.it/binary/publ/cont/10_37.pdf. [Accessed 25 September 2018].
 
[16]  Rathnayake, I.U., Hargreaves, M. and Huygens, F., “Antibiotic resistance and virulence traits in clinical and environmental Enterococcus faecalis and Enterococcus faecium isolates”, Syst. Appl. Microbiol. 2012, 35: 326-333.
 
[17]  Bonten, M.J, Willems, R. and Weinstein, R.A., “Vancomycin-resistant enterococci: why are they here, and where do they come from?”, Lancet Infect. Dis. 2001, 1(5): 314-25.
 
[18]  Deshpande, L.M., Fritsche, T.R., Moet, G.J., Biedenbach, D.J. and Jones, R.N., “Antimicrobial resistance and molecular epidemiology of vancomycin-resistant enterococci from North America and Europe: a report from the SENTRY antimicrobial surveillance program”, Diagn. Micr. Infec. Dis. 2007, 58: 163-70.
 
[19]  European Antimicrobial Resistance Surveillance System Management Team, Advisory Board and National Representatives, “EARSS Annual Report 2008. On-going surveillance of S. pneumoniae, S. aureus, E. coli, E. faecium, E. faecalis, K. pneumoniae, P. aeruginosa”, RIVM, Bilthoven, The Netherlands, 2009.
 
[20]  Kayser, F.H, “Safety aspects of enterococci from the medical point of view”, Int. J. Food Microbiol. 2003, 88: 255-262.
 
[21]  Poulsen, L.L., Bisgaard, M., Son, N.T., Trung, N.V., An, H.M. and Dalsgaard, A., “Enterococcus faecalis clones in poultry and in humans with urinary tract infections, Vietnam”, Emerg. Infect. Dis. 2012, 18: 1096-1100.
 
[22]  Sapkota, A.R., Hulet, R.M., Zhang, G., McDermott, P., Kinney, E.L., Schwab Kellogg, J. and Joseph, S.W., “Lower prevalence of antibiotic resistant Enterococci on U.S. conventional poultry farms that transitioned to organic practices”, Environ. Health Perspect. 2011, 119: 1622-1628.
 
[23]  Rizzotti, L., Simeoni, D., Cocconcelli, P., Gazzola, S., Dellaglio, F. and Torriani, S., “Contribution of enterococci to the spread of antibiotic resistance in the production chain of swine meat commodities”, J. Food Prot. 2005, 68:955-965.
 
[24]  Charpentier, E. and Courvalin, P., “Antibiotic resistance in Listeria spp.”, Antimicrob. Agents Ch. 1999, 43:2103-2108.
 
[25]  Courvalin, P., “Transfer of antibiotic resistance genes between gram-positive and gram-negative bacteria”, Antimicrob. Agents Ch. 1994, 38: 1447-1451.
 
[26]  Sparo, M., Urbizu, L., Solana, M.V., Pourcel, G., Delpech, G., Confalonieri, A., Ceci, M. and Sanchez Bruni, S.F., “High-level resistance to gentamycin: genetic transfer between Enterococcus faecalis isolated from food of animal origin and human microbiota”, Lett. Appl. Microbiol. 2011, 54: 119-125.
 
[27]  Walsh, D., Duffy, G., Sheridan, J.J., Blair, I.S. and McDowell, DA., “Antibiotic resistance among Listeria, including Listeria monocytogenes, in retail foods”, J. Appl. Microbiol. 2001, 90: 517-522.
 
[28]  Shaked, H., Carmeli, Y., Schwartz, D. and Siegman-Igra, Y., “Enterococcal bacteraemia: epidemiological, microbiological, clinical and prognostic characteristics, and the impact of high level gentamicin resistance”, Scand. J. Inf. Dis. 2006, 38:995-1000.
 
[29]  Leclercq, R., Derlot, E., Duval, J. and Courvalin, P., “Plasmid Mediated Resistance to Vancomycin and Teicoplanin Resistance in Enterococcus faecium”, New Engl. J. Med. 1988, 319:157-161.
 
[30]  Shepard, B.D. and Gilmore, M.S., “Antibiotic-Resistant Enterococci: the mechanisms and dynamics of drug introduction and resistance”, Microbes Infect. 2002, 4.215-224.
 
[31]  Eaton, T.J. and Gasson, M.J., “Molecular Screening of Enterococcus Virulence Determinants and Potential for Genetic Exchange between Food and Medical Isolates”, Appl. Environ. Microbiol. 2001, 67: 1628-1635.
 
[32]  Huys, G., D’Haene, K., Collard, J.C. and Swings, J., “Prevalence and Molecular Characterization of Tetracycline Resistance in Enterococcus Isolates from Food”, Appl. Env. Microbiol. 2004, 70: 1555-1562.
 
[33]  Scheetz, M.H., Knechtel, S.A., Malczynski, M., Postelnick, M.J. and Qi, C., “Increasing incidence of linezolid-intermediate or - resistant, vancomycin-resistant Enterococcus faecium strains parallels increasing linezolid consumption”, Antimicrob. Agents Ch. 2008, 52: 2256-2259.
 
[34]  Barbosa, J., Ferreira, V., Teixeira, P., “Antibiotic susceptibility of enterococci isolated from traditional fermented meat products”, Food Microbiol. 2009, 26:527-532.
 
[35]  Pesavento, G., Calonico, C., Ducci, B., Magnanini, A. and Lo Nostro, A., “Prevalence and Antibiotic Resistance of Enterococcus spp. isolated from retail cheese, ready-to-eat salads, ham, and raw meat”, Food Microbiol. 2014, 41:1-7.
 
[36]  Bauer, A.W., Kirby, W.M., Sherris, J.C., Turck, M., “Antibiotic susceptibility testing by a standardized single disk method”, Am. J. Clin. Pathol. 1966, 45: 493-496.
 
[37]  The European Committee on Antimicrobial Susceptibility testing, EUCAST disk diffusion method for antimicrobial susceptibility testing. Version 6.0, 2017. [Online]. Available: http://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Disk_test_documents/Version_5/Manual_v_6.0_ EUCAST_Disk_Test_final.pdf. [Accessed 25 September 2018].
 
[38]  The European Committee on Antimicrobial Susceptibility testing, Breakpoint tables for interpretation of MICs and zone diameters. Version 7.1, 2017. [Online]. Available: http://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_7.1_Breakpoint_Tables.pdf. [Accessed 25 September 2018].
 
[39]  Clinical and Laboratory Standard Institute, Performance standards for antimicrobial susceptibility testing. 27th ed. CLSI supplement M100. Clinical and Laboratory Standards Institute, Wayne, PA, 2017.
 
[40]  Aarestrup, F.M., Hasman, H., Jensen, L.B., Moreno, M., Herrero, I.A., Domínguez, L., Finn, M. and Franklin, A., “Antimicrobial Resistance among Enterococci from Pigs in Three European Countries”, Appl. Environ. Microbiol. 2002, 68(8): 4127-4129.
 
[41]  Kilonzo-Nthenge, A., Brown, A., Nahashon, S. N. and Long D., “Occurrence and Antimicrobial Resistance of Enterococci Isolated from Organic and Conventional Retail Chicken”, J. Food Prot. 2015, 78(4): 760-766.
 
[42]  Giraffa, G., Olivari, A.M and Neviani, E., “Isolation of vancomycin-resistant Enterococcus faecium from Italian cheeses”, Food Microbiol. 2000, 17: 671-677.
 
[43]  European Food Safety Authority and European Centre for Disease Prevention and Control, EU Summary Report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2013, EFSA J. 2015, 13(2):4036.
 
[44]  Obeng, A,S., Rickard, H., Ndi, O., Sexton, M. and Barton., M., “Prevalence of antimicrobial resistance in Enterococci and Escherichia coli in meat chicken flocks during a production cycle and egg layer pullet during rearing”, Int. J. Poultry Sci. 2014, 13:489-503.
 
[45]  Amaechi, N. and Nwankwo, I.U., “Evaluation of Prevalence and Antimicrobial Resistance using Enterococci Isolates from Pigs and Poultry Birds in Abia State, Nigeria”, Int. J. Curr. Microbiol. App. Sci. 2015, 4(2): 825-833.
 
[46]  Ayeni, F.A., Odumosu, B.T., Oluseyi, A.E. and Ruppitsch, W., “Identification and prevalence of tetracycline resistance in enterococci isolated from poultry in Ilishan, Ogun State, Nigeria”, J. Pharm. Bioall. Sci. 2016, 8: 69-73.
 
[47]  European Food Safety Authority and European Centre for Disease Prevention and Control, “The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2014”, EFSA J. 2016, 14(2):4380.
 
[48]  Angulo, F.J., Heuer, O.E., Hammerum, A.M., Collignon, P. and Wegener, H.C., “Human health hazard from antimicrobial-resistant enterococci in animals and food”, Clin. Infect. Dis. 2006, 43: 911-916.
 
[49]  Witte W., “Ecological impact of antibiotic use in animals on different complex microflora: environment”, Int. J. Antimicrob. Ag. 2000, 14:321-325.
 
[50]  European Centre for Disease Prevention and Control, “Antimicrobial resistance surveillance in Europe 2014. Annual Report of the European Antimicrobial Resistance Surveillance Network (EARS-Net)”, European Centre for Disease Prevention and Control, Stockholm: ECDC, 2015.
 
[51]  O’Driscoll, T. and Crank, C.W., “Vancomycin-resistant enterococcal infections: epidemiology, clinical manifestations, and optimal management”, Infect. Drug Resist. 2015, 8: 217-230.
 
[52]  Gaglio, R., Couto, N., Marques, C., de Fatima Silva Lopes, M., Moschetti, G., Pomba C. and Settanni, L., “Evaluation of virulence and antimicrobial resistance of enterococci isolated along the traditional cheese production chains”, Int. J. Food Microbiol. 2016, 236: 107-114.
 
[53]  McGowan, L.L., Jackson, C.R., Barrett, J.B., Hiott, L.M. and Fedorka-Cray, P.J., “Prevalence and antimicrobial resistance of enterococci isolated from retail fruits, vegetables, and meats”, J. Food Prot. 2006, 69:2976-2982.
 
[54]  Garrido, A.M., Gálvez, A. and Pulido, R.P., “Antimicrobial Resistance in Enterococci”, J. Infect. Dis. Ther. 2014, 2:150.
 
[55]  Jahan, M., Zhanel, G.G., Sparling, R. and Holley, R.A., “Horizontal transfer of antibiotic resistance from Enterococcus faecium of fermented meat origin to clinical isolates of E. faecium and Enterococcus faecalis”, Int. J. Food Microbiol. 2015, 16: 78-85.
 
[56]  Guerrero-Ramos, E., Cordero, J., Molina-Gonzalez, D., Poeta, P., Igrejas, G., Alonso-Calleja, C. and Capita, R., “Antimicrobial resistance and virulence genes in enterococci from wild game meat in Spain”, Food Microbiol. 2016, 53:156-164.
 
[57]  Citak, S., Yucel, N.L. and Mendi, A., “Antibiotic resistance of enterococcal isolates in raw milk”, J. Food Process. Pres. 2005, 29: 183-195.
 
[58]  Regulation (EC) No 1831/2003 of the European Parliament and of the Council of 22 September 2003 on additives for use in animal nutrition, O. J. L. 268, 18.10.2003, 29-43.
 
[59]  Castanon, J.I.R., “History of the Use of Antibiotic as Growth Promoters in European Poultry Feeds”, Poultry Sci. 2007, 86(11): 2466-2471.
 
[60]  Raeisi, J., Saifi, M., Pourshafie, M.R., Habibi, M., Mohajerani, H.R., Akbari, N. and Karam, M.R.A., “Rapid Identification of Vancomycin Resistant Enterococcus Faecalis Clinical Isolates using a Sugar Fermentation Method”, J Clin Diagn Res. 2017, 11(3): DC14-DC17.
 
[61]  Novais, C., Freitas, A.R., Silveira, E., Antunes, P., Silva, R., Coque, T.M. and Peixe, L., “Spread of multidrug-resistant Enterococcus to animals and humans: an underestimated role for the pig farm environment”, J. Antimicrob. Chemother. 2013, 68(12): 2746-54.
 
[62]  Hershberger, E., Oprea, S.F., Donabedian, S.M., Perri, M., Bozigar, P., Bartlett, P. and Zervos M.J., “Epidemiology of antimicrobial resistance in enterococci of animal origin”, J Antimicrob Chemother. 2005, 55(1): 127-30.
 
[63]  Seputiene, V., Bogdaite, A., Ruzauskas, M. and Suziedeliene, E., “Antibiotic resistance genes and virulence factors in Enterococcus faecium and Enterococcus faecalis from diseased farm animals: pigs, cattle and poultry”, Pol J Vet Sci. 2012, 15(3):431-8.
 
[64]  Kim, M.C., Cha, M.H., Ryu, J.G and Woo, G.J., “Characterization of Vancomycin-Resistant Enterococcus faecalis and Enterococcus faecium Isolated from Fresh Produces and Human Fecal Samples”, Foodborne Pathog Dis. 2017, 14(4): 195-201.
 
[65]  Berglund, B., “Environmental dissemination of antibiotic resistance genes and correlation to anthropogenic contamination with antibiotics”, Infect Ecol Epidemiol. 2015, 8(5):28564.
 
[66]  Bortolaia, V., Mander, M., Jensen, L.B., Olsen, J.E. and Guardabassi, L., “Persistence of vancomycin resistance in multiple clones of Enterococcus faecium isolated from Danish broilers 15 years after the ban of avoparcin”, Antimicrob Agents Chemother. 2015, 59(5):2926-9.
 
[67]  European Medicines Agency, European Surveillance of Veterinary Antimicrobial Consumption (ESVAC), “Sales of veterinary antimicrobial agents in 30 European countries in 2015”, 2017. [Online]. Available: http://www.ema.europa.eu/docs/en_GB/document_library/Report/2017/10/WC500236750.pdf [Accessed 25 September 2018].
 
[68]  Donabedian, S.M., Thal, L.A., Hershberger, E., Perri, M.B., Chow, J.W., Bartlett, P., Jones, R., Joyce, K., Rossiter, S., Gay, K., Johnson, J., Mackinson, C., Debess, E., Madden, J., Angulo, F. and Zervos M.J., “Molecular characterization of gentamicin-resistant Enterococci in the United States: evidence of spread from animals to humans through food”, J. Clin. Microbiol. 2003, 41: 1109-1113.
 
[69]  Dubin, K. and Pamer, E.G., “Enterococci and Their Interactions with the Intestinal Microbiome”, Microbiol Spectr. 2014, 5(6).
 
[70]  European Centre for Disease Prevention and Control, “Antimicrobial resistance and causes of non-prudent use of antibiotics in human medicine in the EU”, European Centre for Disease Prevention and Control, Stockholm: ECDC, 2017.
 
[71]  Hidano, A., Yamamoto, T., Hayama, Y., Muroga, N., Kobayashi, S., Nishida, T. and Tsutsui, T., “Unraveling Antimicrobial Resistance Genes and Phenotype Patterns among Enterococcus faecalis Isolated from Retail Chicken Products in Japan”, PLoS ONE. 2015, 10(3): e0121189.
 
[72]  De Leener, E., Martel, A., Decostere, A. and Haesebrouck, F., “Distribution of the erm (B) gene, tetracycline resistance genes, and Tn1545-like transposons in macrolide- and lincosamide-resistant enterococci from pigs and humans”, Microb Drug Resist. 2004, 10(4): 341-345.