Characterization and risk factors of vancomycin-resistant Enterococci (VRE) among animal-affiliated workers in Malaysia

Journal of Applied Microbiology

Volumn 113, Issue 5, 2012, Pages 1184-1195

  Getachew, Y ^a   Hassan, L ^a   Zakaria, Z ^a   Zaid, C Z M ^b   Yardi, A ^c   Shukor, R A ^d   Marawin, L T ^d   Embong, F ^d   Aziz, S A ^a  

^a UNIVERSITY PUTRA MALAYSIA   (Malaysia)

^b Department of Veterinary Service   (Malaysia)

^c Selangor State Resource Office   (Malaysia)

^d Department of Veterinary Services ^*  (Malaysia)

Author keywords

Enterococcus; esp; Human; Pigs; Poultry; van genes; Virulence genes; VRE

Indexed keywords

ANIMALS; BACILLI; HOSPITALS;

ENTEROCOCCUS; ESP; HUMAN; MALAYSIA; PIG; RISK FACTORS; VAN GENE; VANCOMYCIN-RESISTANT ENTEROCOCCI; VIRULENCE GENE; WORKERS';

GENES;

ANTIBIOTIC RESISTANCE; BACTERIUM; COLONIZATION; DISEASE PREVALENCE; EPIDEMIOLOGY; GENE; GENOTYPE; OCCUPATIONAL EXPOSURE; PIG; POULTRY; RISK FACTOR; VIRULENCE; WORKING CONDITIONS;

ADULT; ANIMAL HUSBANDRY; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATION; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; ENTEROCOCCUS GALLINARUM; FEMALE; GENE IDENTIFICATION; GENOTYPE; HUMAN; INFECTION RISK; MAJOR CLINICAL STUDY; MALAYSIA; MALE; OCCUPATIONAL HAZARD; PREVALENCE; VANB GENE; VANCOMYCIN RESISTANT ENTEROCOCCUS;

MALAYSIA;

ANIMALIA; ENTEROCOCCUS; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; ENTEROCOCCUS GALLINARUM; SUIDAE;

EID: 84867738591     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2012.05406.x     Document Type: Article

References (74)

1. Aubry-Damon, H., Grenet, K., Sall-Ndiaye, P., Che, D., Cordeiro, E., Bougnoux, M.-E., Rigaud, E., Le Strat, Y. et al. (2004) Antimicrobial resistance in commensal flora of pig farmers. Emerg Infect Dis 10, 873-879.
2. Bates, J. (1997) Epidemiology of vancomycin-resistant enterococci in the community and the relevance of farm animals to human infection. J Hosp Infect 37, 89-101.
3. Bates, J., Jordens, J.Z. and Griffiths, D.T. (1994) Farm animals as a putative reservoir for vancomycin-resistant enterococcal infection in man. J Antimicrob Chemother 34, 507-514.
4. Bell, J.M., Paton, J.C. and Turnidge, J. (1998) Emergence of vancomycin-resistant Enterococci in Australia: phenotypic and genotypic characteristics of isolates. J Clin Microbiol 36, 2187-2190.
5. Biavasco, F., Foglia, G., Paoletti, C., Zandri, G., Magi, G., Guaglianone, E., Sundsfjord, A., Pruzzo, C. et al. (2007) VanA-type enterococci from humans, animals, and food: species distribution, population structure, tn1546 typing and location, and virulence determinants. Appl Environ Microbiol 73, 3307-3319.
6. Billström, H., Sullivan, Å. and Lund, B. (2008) Cross-transmission of clinical Enterococcus faecium in relation to esp and antibiotic resistance. J Appl Microbiol 105, 2115-2122.
7. Bittencourt De Marques, E. and Suzart, S. (2004) Occurrence of virulence-associated genes in clinical Enterococcus faecalis strains isolated in Londrina, Brazil. J Med Microbiol 53, 1069-1073.
8. Boerlin, P., Wissing, A., Aarestrup, F.M., Frey, J. and Nicolet, J. (2001) Antimicrobial growth promoter ban and resistance to macrolides and vancomycin in enterococci from pigs. J Clin Microbiol 39, 4193-4195.
9. Bonten, M.J., Willems, R. and Weinstein, R.A. (2001) Vancomycin-resistant enterococci: why are they here, and where do they come from? Lancet Infect Dis 1, 314-325.
10. Borgmann, S., Schulte, B., Wolz, C., Gruber, H., Werner, G., Goerke, C., Klare, I., Beyser, K. et al. (2007) Discrimination between epidemic and non-epidemic glycopeptide-resistant E. faecium in a post-outbreak situation. J Hosp Infect 67, 49-55.
11. Camargo, I.L.B., Barth, A.L., Pilger, K., Seligman, B.G., Machado, A.R. and Darini, A.L. (2004) Enterococcus gallinarum carrying the VanA gene cluster: first report in Brazil. Braz J Med Biol Res 37, 1669-1671.
12. Camargo, I.L.B.C., Gilmore, M.S. and Darini, A.L.C. (2006) Multilocus sequence typing and analysis of putative virulence factors in vancomycin-resistant and vancomycin-sensitive Enterococcus faecium isolates from Brazil. Clin Microbiol Infect 12, 1123-1130.
13. Cheng, S., McCleskey, F.K., Gress, M.J., Petroziello, J.M., Liu, R., Namdari, H., Beninga, K., Salmen, A. et al. (1997) A PCR assay for identification of Enterococcus faecium. J Clin Microbiol 35, 1248-1250.
14. Clark, N.C., Cooksey, R.C., Hill, B.C., Swenson, J.M. and Tenover, F.C. (1993) Characterization of glycopeptide-resistant Enterococci from U.S. Hospitals. Antimicrob Agents Chemother 37, 2311-2317.
15. Clinical and Laboratory Standards Institute (2006) Performance Standards for Antimicrobial Susceptibility Testing; CLSI approved standard, vol. M100-S16. Wayne, PA: Clinical and Laboratory Standards Institute.
16. Coque, T.M., Patterson, J.E., Steckelberg, J.M. and Murray, B.E. (1995) Incidence of hemolysin, gelatinase, and aggregation substance among enterococci isolated from patients with endocarditis and other infections and from feces of hospitalized and community-based persons. J Infect Dis 171, 1223-1229.
17. Coque, T.M., Tomayko, J.F., Ricke, S.C., Okhyusen, P.C. and Murray, B.E. (1996) Vancomycin-resistant enterococci from nosocomial, community, and animal sources in the United States. Antimicrob Agents Chemother 40, 2605-2609.
18. Cuellar-Rodríguez, J., Galindo-Fraga, A., Guevara, V., Pérez-Jiménez, C., Espinosa-Aguilar, L., Rolón, A.L., Hernández-Cruz, A., López-Jácome, E. et al. (2007) Vancomycin-resistant Enterococci, Mexico City. Emerg Infect Dis 13, 798-799.
19. D'Agata, E.M.C., Jirjis, J., Gouldin, C. and Tang, Y.-W. (2001) Community dissemination of vancomycin-resistant Enterococcus faecium. Am J Infect Control 29, 316-320.
20. Dean, A., Sullivan, K. and Soe, M. (2003) OpenEpi: Open Source Epidemiologic Statistics for Public Health. Emory University. Version 2.3.1. www.OpenEpi.com (accessed 1 March 2012).
21. Domig, K.J., Mayer, H.K. and Kneifel, W. (2003) Methods used for the isolation, enumeration, characterisation and identification of Enterococcus spp.: 1. Media for isolation and enumeration. Int J Food Microbiol 88, 147-164.
22. Dutka-Malen, S., Evers, S. and Courvalin, P. (1995) Detection of glycopeptide resistance genotypes and identification to the species level of clinically relevant Enterococci by PCR". J Clin Microbiol 33, 24-27.
23. Eisner, A., Feierl, G., Gorkiewicz, G., Dieber, F., Kessler, H.H., Marth, E. and Köfer, J. (2005) High prevalence of VanA-type vancomycin-resistant enterococci in Austrian poultry. Appl Environ Microbiol 71, 6407-6409.
24. Elsayed, S., Hamilton, N., Boyd, D. and Mulvey, M. (2001) Improved primer design for multiplex PCR analysis of vancomycin-resistant Enterococcus spp. J Clin Microbiol 39, 2367-2368.
25. Endtz, H.P., Van Den Braak, N., Van Belkum, A., Kluytmans, J.A., Koeleman, J.G., Spanjaard, L., Voss, A., Weersink, A.J. et al. (1997) Fecal carriage of vancomycin-resistant enterococci in hospitalized patients and those living in the community in The Netherlands. J Clin Microbiol 35, 3026-3031.
26. Franz, C.M.A.P., Holzapfel, W.H. and Stiles, M.E. (1999) Enterococci at the crossroads of food safety? Int J Food Microbiol 47, 1-24.
27. Freitas, A.R., Coque, T.M., Novais, C., Hammerum, A.M., Lester, C.H., Zervos, M.J., Donabedian, S., Jensen, L.B. et al. (2011) Human and swine hosts share vancomycin-resistant Enterococcus faecium CC17 and CC5 and Enterococcus faecalis CC2 clonal clusters harboring TN1546 on indistinguishable plasmids. J Clin Microbiol 49, 925-931.
28. Gambarotto, K., Ploy, M.-C., Turlure, P., Grélaud, C., Martin, C., Bordessoule, D. and Denis, F. (2000) Prevalence of vancomycin-resistant Enterococci in fecal samples from hospitalized patients and nonhospitalized controls in a cattle-rearing area of France. J Clin Microbiol 38, 620-624.
29. Getachew, Y.M., Hassan, L., Zakaria, Z., Saleha, A.A., Kamaruddin, M.I. and Che Zalina, M.Z. (2009) Characterization of vancomycin-resistant Enterococcus isolates from broilers in Selangor, Malaysia. Trop Biomed 26, 280-288.
30. Getachew, Y., Hassan, L., Zakaria, Z. and Lokman, N. (2010) Species distribution and resistance phenotypes of vancomycin- resistant Enterococcus isolated from pigs in Pulau Pinang, Malaysia. Pertanika J Trop Agric Sci 33, 15-25.
31. Goossens, H. (1998) Spread of vancomycin-resistant Enterococci: differences between the United States and Europe. Infect Control Hosp Epidemiol 19, 546-551.
32. Hammerum, A.M., Lester, C.H. and Heuer, O.E. (2010) Antimicrobial-resistant enterococci in animals and meat: a human health hazard? Foodborne Pathog Dis 7, 1137-1146.
33. Hijazi, N., Elmanama, A. and Al-Hindi, A. (2009) Vancomycin-resistant enterococci in fecal samples from hospitalized patients and non-hospitalized individuals in Gaza City. J Public Health 17, 243-249.
34. Homan, W.L., Tribe, D., Poznanski, S., Li, M., Hogg, G., Spalburg, E., Van Embden, J.D.A. and Willems, R.J.L. (2002) Multilocus sequence typing scheme for Enterococcus faecium. J Clin Microbiol 40, 1963-1971.
35. Jordens, J.Z., Bates, J. and Griffiths, D.T. (1994) Faecal carriage and nosocomial spread of vancomycin-resistant Enterococcus faecium. J Antimicrob Chemother 34, 515-528.
36. Jung, W.K., Hong, S.K., Lim, J.Y., Lim, S.K., Kwon, N.H., Kim, J.M., Koo, H.C., Kim, S.H. et al. (2006) Phenotypic and genetic characterization of vancomycin-resistant enterococci from hospitalized humans and from poultry in Korea, Phenotypic and genetic characterization of vancomycin-resistant enterococci from hospitalized humans and from poultry in Korea. FEMS Microbiol Lett 260, 193-200.
37. Ke, D., Picard, F.J., Martineau, F., Ménard, C., Roy, P.H., Ouellette, M. and Bergeron, M.G. (1999) Development of a PCR assay for rapid detection of enterococci. J Clin Microbiol 37, 3497-3503.
38. Klare, I., Heier, H., Claus, H., Böhme, G., Marin, S., Seltmann, G., Hakenbeck, R., Antanassova, V. et al. (1995) Enterococcus faecium strains with VanA-mediated high-level glycopeptide resistance isolated from animal foodstuffs and fecal samples of humans in the community. Microb Drug Resist 1, 265-272.
39. Klein, G., Pack, A. and Reuter, G. (1998) Antibiotic resistance patterns of enterococci and occurrence of vancomycin-resistant enterococci in raw minced beef and pork in Germany. Appl Environ Microbiol 64, 1825-1830.
40. Kolar, M., Pantucek, R., Bardon, J., Cekanova, L., Kesselova, M., Sauer, P., Vagnerova, I. and Koukalová, D. (2005) occurrence of vancomycin-resistant enterococci in humans and animals in the Czech Republic between 2002 and 2004. J Med Microbiol 54, 965-967.
41. Kühn, I., Iversen, A., Finn, M., Greko, C., Burman, L.G., Blanch, A.R., Vilanova, X., Manero, A. et al. (2005) Occurrence and relatedness of vancomycin-resistant Enterococci in animals, humans, and the environment in different European regions. Appl Environ Microbiol 71, 5383-5390.
42. Kumarasamy, K.K., Toleman, M.A., Walsh, T.R., Bagaria, J., Butt, F., Balakrishnan, R., Chaudhary, U., Doumith, M. et al. (2010) Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study. Lancet Infect Dis 10, 597-602.
43. Leclercq, R. and Leclercq, R. (2009) Epidemiological and resistance issues in multidrug-resistant staphylococci and enterococci. Clin Microbiol Infect 15, 224, 224-231, 231.
44. Lemcke, R. and Bülte, M. (2000) Occurrence of the vancomycin-resistant genes VanA, VanB, vanC1, vanC2 and vanC3 in Enterococcus strains isolated from poultry and pork. Int J Food Microbiol 60, 185-194.
45. Malhotra-Kumar, S., Haccuria, K., Michiels, M., Ieven, M., Poyart, C., Hryniewicz, W. and Goossens, H. (2008) Current trends in rapid diagnostics for methicillin-resistant Staphylococcus aureus and glycopeptide-resistant Enterococcus species. J Clin Microbiol 46, 1577-1587.
46. Martin, B., Garriga, M., Hugas, M. and Aymerich, T. (2005) Genetic diversity and safety aspects of enterococci from slightly fermented sausages. J Appl Microbiol 98, 1177-1190.
47. Pahang, J. (2006) Hospital-acquired vancomycin-resistant enterococci: now appearing in Kuala Lumpur Hospital. Med J Malaysia 61, 487-489.
48. Pangallo, D., Drahovská, H., Harichová, J., Karelová, E., Chovanová, K., Ferianc, P., Turňa, J. and Timko, J. (2008) Assessment of environmental enterococci: bacterial antagonism, pathogenic capacity and antibiotic resistance. Antonie Van Leeuwenhoek 94, 555-562.
49. Qadri, S.M. and Postle, A.G. (1996) Vancomycin-resistant enterococci (VRE) as normal flora of the intestine in patients at a tertiary care hospital. Ann Saudi Med 16, 625-628.
50. Raja, N.S., Karunakaran, R., Ngeow, Y.F. and Awang, R. (2005) Community-acquired vancomycin-resistant Enterococcus faecium: a case report from Malaysia. J Med Microbiol 54, 901-903.
51. Safdar, N. and Maki, D.G. (2002) The commonality of risk factors for nosocomial colonization and infection with antimicrobial-resistant Staphylococcus aureus, Enterococcus, Gram-negative bacilli, Clostridium difficile, and Candida. Ann Intern Med 136, 834-844.
52. Satake, S., Clark, N., Rimland, D., Nolte, F.S. and Tenover, F.C. (1997) Detection of vancomycin-resistant Enterococci in fecal samples by PCR. J Clin Microbiol 35, 2325-2330.
53. Seo, K.S., Lim, J.Y., Yoo, H.S., Bae, W.K. and Park, Y.H. (2005) Comparison of vancomycin-resistant enterococci isolates from human, poultry and pigs in Korea. Vet Microbiol 106, 225-233.
54. Son, R., Nimita, F., Rusul, G., Nasreldin, E., Samuel, L. and Nishibuchi, M. (2002) Isolation and molecular characterization of vancomycin-resistant Enterococcus faecium in Malaysia. Lett Appl Microbiol 29, 118-122.
55. Song, J.Y., Cheong, H.J., Jo, Y.M., Choi, W.S., Noh, J.Y., Heo, J.Y. and Kim, W.J. (2009) Vancomycin-resistant Enterococcus colonization before admission to the intensive care unit: a clinico-epidemiologic analysis. Am J Infect Control 37, 734-740.
56. Sørum, M., Johnsen, P.J., Aasnes, B., Rosvoll, T., Kruse, H., Sundsfjord, A. and Simonsen, G.S. (2006) Prevalence, persistence, and molecular characterization of glycopeptide-resistant enterococci in Norwegian poultry and poultry farmers 3 to 8 years after the ban on avoparcin. Appl Environ Microbiol 72, 516-521.
57. Stobberingh, E., van den Bogaard, A., London, N., Driessen, C., Top, J. and Willems, R. (1999) Enterococci with glycopeptide resistance in turkeys, turkey farmers, turkey slaughterers, and (sub)urban residents in the south of the Netherlands: evidence for transmission of vancomycin resistance from animals to humans? Antimicrob Agents Chemother 43, 2215-2221.
58. Tacconelli, E. and Cataldo, M.A. (2008) Vancomycin-resistant enterococci (VRE): transmission and control. Int J Antimicrob Agents 31, 99-106.
59. Tornieporth, N.G., Roberts, R.B., John, J., Hafner, A. and Riley, L.W. (1996) Risk factors associated with vancomycin-resistant Enterococcus faecium infection or colonization in 145 matched case patients and control patients. Clin Infect Dis 23, 767-772.
60. Van de Klundert, J.A.M. and Vliegenthart, J.S. (1993) PCR detection of genes coding for aminoglycoside-modifying enzymes. In Diagnostic Molecular Microbiology eds Persing, D.H., Smith, T.F., Tenover, F.C. and White, T.J. pp. 547-552. Washington, DC: American Society for Microbiology.
61. Van den Bogaard, A.E., Jensen, L.B. and Stobberingh, E.E. (1997) Vancomycin-resistant enterococci in turkeys and farmers. N Engl J Med 337, 1558-1559.
62. Van Der Auwera, P., Pensart, N., Korten, V., Murray, B.E. and Leclercq, R. (1996) Influence of oral glycopeptides on the fecal flora of human volunteers: selection of highly glycopeptide-resistant enterococci. J Infect Dis 173, 1129-1136.
63. Vignaroli, C., Zandri, G., Aquilanti, L., Pasquaroli, S. and Biavasco, F. (2011) Multidrug-resistant enterococci in animal meat and faeces and co-transfer of resistance from Enterococcus durans to a human Enterococcus faecium. Curr Microbiol 62, 1438-1447.
64. Webb, M., Riley, L.W. and Roberts, R.B. (2001) Cost of hospitalization for and risk factors associated with vancomycin-resistant Enterococcus faecium infection and colonization. Clin Infect Dis 33, 445-452.
65. Weinstein, J.W., Roe, M., Towns, M., Sanders, L., Thorpe, J.J., Corey, G.R. and Sexton, D.J. (1996) Resistant enterococci: a prospective study of prevalence, incidence, and factors associated with colonization in a university hospital. Infect Control Hosp Epidemiol 17, 36-41.
66. Wendt, C., Krause, C., Xander, L.U., Löffler, D. and Floss, H. (1999) Prevalence of colonization with vancomycin-resistant enterococci in various population groups in Berlin, Germany. J Hosp Infect 42, 193-200.
67. Werner, G., Coque, T.M., Hammerum, A.M., Hope, R., Hryniewicz, W., Johnson, A., Klare, I., Kristinsson, K.G. et al. (2008) Emergence and spread of vancomycin resistance among enterococci in Europe. Euro Surveill 13, 1-11.
68. Whitman, R.L., Przybyla-Kelly, K., Shively, D.A. and Byappanahalli, M.N. (2007) Incidence of the enterococcal surface protein (esp) gene in human and animal fecal sources. Environ Sci Technol 41, 6090-6095.
69. Willems, R.J. and Bonten, M.J. (2007) Glycopeptide-resistant enterococci: deciphering virulence, resistance and epidemicity. Curr Opin Infect Dis 20, 384-390.
70. Willems, R.J.L., Top, J., Van Den Braak, N., Van Belkum, A., Endtz, H., Mevius, D., Stobberingh, E., Van Den Bogaard, A. et al. (2000) Host specificity of vancomycin-resistant Enterococcus faecium. J Infect Dis 182, 816-823.
71. Willems, R.J., Homan, W., Top, J., van Santen-Verheuvel, M., Tribe, D., Manzioros, X., Gaillard, C., Vandenbroucke-Grauls, C.M. et al. (2001) Variant esp gene as a marker of a distinct genetic lineage of vancomycin resistant Enterococcus faecium spreading in hospitals. Lancet 357, 853-855.
72. Woodford, N., Soltani, M. and Hardy, K. (2001) Frequency of esp in Enterococcus faecium isolates. Lancet 358, 584.
73. Worth, L.J., Slavin, M.A., Vankerckhoven, V., Goossens, H., Grabsch, E.A. and Thursky, K.A. (2008) Virulence determinants in vancomycin-resistant Enterococcus faecium VanB: clonal distribution, prevalence and significance of esp and hyl in Australian patients with haematological disorders. J Hosp Infect 68, 137-144.
74. Yang, K.S., Fong, Y.T., Lee, H.Y., Kurup, A., Koh, T.H., Koh, D. and Lim, M.K. (2007) Predictors of vancomycin-resistant Enterococcus (VRE) carriage in the first major VRE outbreak in Singapore. Ann Acad Med Singapore 36, 379-383.