Hostname: page-component-857557d7f7-v48vw Total loading time: 0 Render date: 2025-11-23T01:31:27.077Z Has data issue: false hasContentIssue false
  • English
  • Français

Spread of Vancomycin-Resistant Enterococci: Why Did It Happen in the United States?

Published online by Cambridge University Press:  02 January 2015

William J. Martone
William J. Martone*
Affiliation:
National Foundation for Infectious Diseases, Bethesda, Maryland
*
National Foundation for Infectious Diseases, 4733 Bethesda Ave, Suite 750, Bethesda, MD, 20814; e-mail, wjmartone@aol.com.
Get access Rights & Permissions [Opens in a new window]

Abstract

The question of why vancomycin-resistant enterococci (VRE) became epidemic in the United States can be answered on at least three basic levels: (1) molecular and genetic, (2) factors affecting host-microbe interactions, and (3) epidemiological. This article will address the epidemiological issues and seek to defend the assertion that, once VRE had evolved, its spread throughout hospitals in the United States was all but assured. Nosocomial VRE outbreaks were reported first in the mid- and late-1980s. Since that time, scientific reports of VRE have increased over 20-fold. Among hospitals participating in the National Nosocomial Infection Surveillance System from 1989 to 1997, the percentage of enterococci reported as resistant to vancomycin increased from 0.4% to 23.2% in intensive-care settings and from 0.3% to 15.4% in non-intensive-care settings. Factors leading to the spread of VRE in US hospitals include (1) antimicrobial pressure, (2) sub-optimal clinical laboratory recognition and reporting, (3) unrecognized “silent” carriage and prolonged fecal carriage, (4) environmental contamination and survival, (5) intrahospital and interhospital transfer of colonized patients, (6) introduction of unrecognized carriers from community settings such as nursing homes, and (7) inadequate compliance with hand washing and barrier precautions. Guidelines developed by the Centers for Disease Control and Prevention's Hospital Infection Control Practices Advisory Committee address each of these factors. The impact of these guidelines on the spread of VRE within individual institutions has been variable, and the overall impact of the guidelines nationally is unknown.

Information

Type
From the Fifth International Conference on the Prevention of Infection
Information
Infection Control & Hospital Epidemiology , Volume 19 , Issue 8 , August 1998 , pp. 539 - 545
Copyright
Copyright © The Society for Healthcare Epidemiology of America 1998 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

1. Toala, P, McDonald, A, Wilcox, C, Finland, M. Susceptibility of group D streptococcus (enterococcus) to 21 antibiotics in vitro with special reference to species differences. Am J Med Sci 1969;258:416–430.Google Scholar
2. Leclercq, R, Derlot, E, Duval, J, Courvalin, P. Plasmid-mediated resistance to vancomycin and teicoplanin in Enterococcus faecium . N Engl J Med 1988;319:157–161.Google Scholar
3. Uttley, AHC, George, RC, Naidoo, J, Woodford, N, Johnson, AP, Collins, CH, et al. High-level vancomycin-resistant enterococci causing hospital infections. Epidemiol Infect 1989;103:173–181.Google Scholar
4. Lequercq, R, Courvalin, P. Resistance to glycopeptides in enterococci. Clin Infect Dis 1997;24:545–556.Google Scholar
5. Murray, B. Editorial response: what can we do about vancomycin-resistant enterococci? Clin Infect Dis 1995;20:1134–1136.Google Scholar
6. McGowan, JE Jr. Antimicrobial resistance in hospital organisms and its relation to antibiotic use. Rev Infect Dis 1983;5:1033–1048.Google Scholar
7. Boyle, JF, Soumakis, SA, Rendo, A, Herrington, JA, Gianarkis, DG, Thurberg, BE, et al. Epidemiologic analysis and genotypic characterization of a nosocomial outbreak of vancomycin-resistant enterococci. J Clin Microbiol 1993;31:1280–1285.Google Scholar
8. Karanfil, LV, Murphy, M, Josephson, A, Gaynes, R, Mandel, L, Hill, BC, et al. A cluster of vancomycin-resistant Enterococcus faecium in an intensive care unit. Infect Control Hosp Epidemiol 1992;13:195–200.Google Scholar
9. Handwerger, S, Raucher, B, Altarac, D, Monka, J, Marchione, S, Singh, KV, et al. Nosocomial outbreak due to Enterococcus faecium highly resistant to vancomycin, penicillin, and gentamicin. Clin Infect Dis 1993;16:750–755.Google Scholar
10. Rubin, LG, Tucci, V, Cercenado, E, Eliopoulos, G, Isenberg, HD. Vancomycin-resistant Enterococcus faecium in hospitalized children. Infect Control Hosp Epidemiol 1992;13:700–705.Google Scholar
11. Livornese, LL, Dias, S, Samel, C, Romanowski, B, Taylor, S, May, P, et al. Hospital-acquired infection with vancomycin-resistant Enterococcus fae-cium transmitted by electronic thermometers. Ann Intern Med 1992;117:112–116.Google Scholar
12. Boyce, JM, Opal, SM, Chow, JW, Zervos, MJ, Potter-Bynoe, G, Sherman, CB, et al. Outbreak of multidrug-resistant Enterococcus faecium with transferable vanB class vancomycin resistance. J Clin Microbiol 1994;32;1148–1153.Google Scholar
13. Beezhold, DW, Slaughter, S, Hayden, MK, Matushek, M, Nathan, C, Tren- holme, GM, et al. Skin colonization with vancomycin-resistant entero-cocci among hospitalized patients with bacteremia. Clin Infect Dis 1997;24:704–706.Google Scholar
14. Slaughter, S, Hayden, MK, Nathan, C, et al. A comparison of the effect of universal use of gloves and gowns with that of glove use alone on acquisition of vancomycin-resistant enterococci in a medical intensive care unit. Ann Intern Med 1996;125:448–456.Google Scholar
15. Tornieporth, NG, Roberts, RB, John, J, Hafner, A, Riley, L. Risk factors associated with vancomycin-resistant Enterococcus faecium infection or colonization in 145 matched case patients and control patients. Clin Infect Dis 1996;23:767–772.Google Scholar
16. Dembry, LM, Uzokwe, K, Zervos, MJ. Control of endemic glycopeptide-resistant enterococci. Infect Control Hosp Epidemiol 1996;17:286–292.Google Scholar
17. Gordts, B, Van Landuyt, H, Ieven, M, Vandamme, P, Goossens, H. Vancomycin-resistant enterococci colonizing the intestinal tracts of hospitalized patients. J Clin Microbiol 1995;33:2842–2846.Google Scholar
18. Moreno, F, Grota, P, Crisp, C, Magnon, K, Melcher, GP, Jorgensen, JH, et al. Clinical and molecular epidemiology of vancomycin-resistant Enterococcus faecium during its emergence in a city in southern Texas. Clin Infect Dis 1995;21:1234–1237.Google Scholar
19. Morris, JG, Shay, DK, Hebden, JN, McCarter, RJ, Perdue, BE, Jarvis, W, et al. Enterococci resistant to multiple antimicrobial agents, including vancomycin. Establishment of endemicity in a university medical center. Ann Intern Med 1995;123:250–259.Google Scholar
20. Pegues, DA, Pegues, CF, Hibberd, PL, Ford, DS, Hooper, DC. Emergence and dissemination of a highly vancomycin-resistant vanA strain of Enterococcus faecium at a large teaching hospital. J Clin Microbiol 1997;35:1565–1570.Google Scholar
21. Porwancher, R, Sheth, A, Remphrey, S, Taylor, E, Hinkle, C, Zervos, M. Epidemiological study of hospital-acquired infection with vancomycin-resis-tant Enterococcus faecium: possible transmission by an electronic earprobe thermometer. Infect Control Hosp Epidemiol 1997;18:771–773.Google Scholar
22. Quale, J, Landman, D, Saurina, G, Atwood, E, DiTore, V, Patel, K. Manipulation of a hospital antimicrobial formulary to control an outbreak of vancomycin-resistant enterococci. Clin Infect Dis 1996;23:1020–1025.Google Scholar
23. Rafferty, ME, McCormick, MI, Bopp, LH, Baltch, AL, George, M, Smith, RP, et al. Vancomycin-resistant enterococci in stool specimens submitted for Clostridium difficile cytotoxin assay. Infect Control Hosp Epidemiol 1997;18:342–344.Google Scholar
24. Rao, GG, Ojo, F, Kolokithas, D. Vancomycin-resistant gram-positive cocci: Risk factors for faecal carriage. J Hosp Infect 1997;35:63–69.Google Scholar
25. Ena, J, Dick, RW, Jones, RN, Wenzel, RP. The epidemiology of intravenous vancomycin usage in a university hospital: a 10-year study. JAMA 1993;269:598–602.Google Scholar
26. Gaynes, R. The impact of antimicrobial use on the emergence of antimicrobial-resistant bacteria in hospitals. Infect Dis Clin North Am 1997:11:757–765.Google Scholar
27. Edlund, C, Barkholt, L, Olsson-Liljequist, B, Nord, CE. Effect of van- comycin on the intestinal flora of patients who previously received antimicrobial therapy. Clin Infect Dis 1997;25:729–732.Google Scholar
28. Van der Auwera, P, Pensart, N, Korten, V, Murray, BE, Leclercq, R. Influence of oral glycopeptides on the fecal flora of human volunteers: selection of highly glycopeptide-resistant enterococci. J Infect Dis 1996;173:1129–1136.Google Scholar
29. Boyce, JM, Mermel, LA, Zervos, MJ, Rice, LB, G, Potter-Bynoe, Giorgio, C, et al. Controlling vancomycin-resistant enterococci. Infect Control Hosp Epidemiol 1995;16:634–637.Google Scholar
30. Bonilla, HF, Zervos, MA, Lyons, MJ, Bradley, SF, Hedderwick, SA, Ramsey, MA, et al. Colonization with vancomycin-resistant Enterococcus faecium: comparison of a long-term-care unit with an acute-care hospital. Infect Control Hosp Epidemiol 1997;18:333–339.Google Scholar
31. Edmond, MB, Ober, JF, Weinbaum, DL, Pfaller, MA, Hwang, T, Sanford, MD, et al. Vancomycin-resistant Enterococcus faecium bacteremia: risk factors for infection. Clin Infect Dis 1995;20:1126–1133.Google Scholar
32. Roghmann, MC, McCarter, RJ, Brewrink, J, Cross, AS, Morris, JG. Clostrid-ium difficile infection is a risk factor for bacteremia due to vancomycin-resistant enterococci (VRE) in VRE-colonized patients with acute leukemia. Clin Infect Dis 1997;25:1056–1059.Google Scholar
33. Tucci, V, Haran, MA, Isenberg, HD. Epidemiology and control of vancomycin-resistant enterococci in an adult and children's hospital. Am J Infect Control 1997;25:371–376.Google Scholar
34. McNeeley, DF, Brown, AE, Noel, GJ, Chung, M, de Lencastre, H. An investigation of vancomycin-resistant Enterococcus faecium within the pediatric service of a large urban medical center. Pediatr Infect Dis J 1998;17:184–188.Google Scholar
35. Montecalvo, MA, de Lencastre, H, Carraher, M, Gedris, C, Chung, M, VanHorn, K, et al. Natural history of colonization with vancomycin-resistant Enterococcus faecium . Infect Control Hosp Epidemiol 1995;16:680–685.Google Scholar
36. Montecalvo, MA, Shay, DK, Gedris, C, Petrullo, C, Uman, J, Rodney, K, et al. A semiquantitative analysis of the fecal flora of patients with vancomycin-resistant enterococci: colonized patients pose an infection control risk. Clin Infect Dis 1997;25:929–930.Google Scholar
37. Yamaguchi, E, Valena, F, Smith, SM, Simmons, A, Eng, RHK. Colonization pattern of vancomycin-resistant Enterococcus faecium . Am J Infect Control 1994;22:202–206.Google Scholar
38. Linden, P, Pasculle, AW, Kramer, DJ, Kusner, S, Manez, R. The duration of fecal carriage on vancomycin-resistant Enterococcus faecium (VREF). The 34th Interscience Conference on Antimicrobial Agents and Chemotherapy; Orlando, FL; 10 1994. Abstract J150.Google Scholar
39. Polish, L, Hebden, J, Shay, D, Jarvis, W, Schwalbe, R, Morris, JG Jr. Duration of fecal carriage of vancomycin-resistant enterococci (VRE) in ICU patients. The 35th Interscience Conference on Antimicrobial Agents and Chemotherapy; San Francisco, CA; 09 1995. Abstract J37.Google Scholar
40. Henning, K, Eagan, J, Boone, N, Brown, AE, Wollner, N, de Lencastre, H, et al. Stool surveillance for vancomycin-resistant Enterococcus faecium (VREF) on a pediatric oncology ward: duration of shedding and incidence of clinical infections. The 35th Interscience Conference on Antimicrobial Agents and Chemotherapy; San Francisco, CA; 09 1995. Abstract J38.Google Scholar
41. Roghmann, MC, Qaiyumi, S, Johnson, JA, Schwalbe, R, Morris, JG. Recurrent vancomycin-resistant Enterococcus faecium bacteremia in a leukemia patient who was persistently colonized with vancomycin-resis-tant enterococci for two years. Clin Infect Dis 1997;24:514–515.Google Scholar
42. Lai, KK, Fontecchio, SA, Kelley, AL, Melvin, ZS, Baker, S. The epidemiology of fecal carriage of vancomycin-resistant enterococci. Infect Control Hosp Epidemiol 1997;18:762–765.Google Scholar
43. Hospital Infection Control Practices Advisory Committee. Recommendations for preventing the spread of vancomycin resistance. Infect Control Hosp Epidemiol 1995;16:105–113.Google Scholar
44. Wells, CL, Juni, BA, Cameron, SB, Mason, KR, Dunn, DL, Ferrieri, P, et al. Stool carriage, clinical isolation, and mortality during an outbreak of vancomycin-resistant enterococci in hospitalized medical and/or surgical patients. Clin Infect Dis 1995;21:45–50.Google Scholar
45. Shay, DK, Maloney, SA, Montecalvo, M, Banerjee, S, Wormser, GP, Arduino, MJ, et al. Epidemiology and mortality risk of vancomycin-resis-tant enterococcal bloodstream infections. J Infect Dis 1995;172:993–1000.Google Scholar
46. Noskin, GA, Stosor, V, Cooper, I, Peterson, LR. Recovery of vancomycin-resistant enterococci on fingertips and environmental surfaces. Infect Control Hosp Epidemiol 1995;16:577–581.Google Scholar
47. Anderson, RL, Carr, JH, Bond, WW, Favero, MS. Susceptibility of vancomycin-resistant enterococci to environmental disinfectants. Infect Control Hosp Epidemiol 1997;18:195–199.Google Scholar
48. Saurina, G, Landmann, D, Quale, JM. Activity of disinfectants against vancomycin-resistant Enterococcus faecium . Infect Control Hosp Epidemiol 1997;18:345–347.Google Scholar
49. Bradley, CR, Fraise, AP. Heat and chemical resistance of enterococci. J Hosp Infect 1996;34:191–196.Google Scholar
50. Byers, KE, Durbin, LJ, Simonton, BM, Anglim, AM, Adal, KA, Farr, BM. Disinfection of hospital rooms contaminated with vancomycin-resistant Enterococcus faecium . Infect Control Hosp Epidemiol 1998;19:261–264.Google Scholar
51. Torell, E, Fredlund, H, Tornquist, E, Myhre, EB, Sjoberg, L, Sundsfjord, A. Intrahospital spread of vancomycin-resistant Enterococcus faecium in Sweden. Scand J Infect Dis 1997;29:259–263.Google Scholar
52. McNeil, MM, Solomon, SL. The epidemiology of methicillin-resistant Staphylococcus aureus . Antimicrobic Newsletter 1985;2:49–56.Google Scholar
53. Chow, JW, Kuritza, A, Shlaes, DM, Green, M, Sahm, DF, Zervos, MJ. Clonal spread of vancomycin-resistant Enterococcus faecium between patients in three hospitals in two states. J Clin Microbiol 1993;31:1609–1611.Google Scholar
54. Tenover, FC, Tokars, J, Swenson, J, Paul, S, Spitalny, K, Jarvis, W. Ability of clinical laboratories to detect antimicrobial agent-resistant enterococci. J Clin Microbiol 1993;31:1695–1699.Google Scholar
55. Webb, R, Currier, M, Brackin, B, Nolan, R, Wilson, J. Capability to identify vancomycin resistant enterococci (VRE) and other emerging pathogens in clinical microbiology laboratories serving a rural state. Infect Control Hosp Epidemiol 1997;18:(suppl)P23. Abstract.Google Scholar
56. Swenson, JM, Ferraro, MJ, Sahm, DF, Charache, P, the National Committee for Clinical Laboratory Standards Working Group on Enterococci, Tenover, FC. New vancomycin disk diffusion breakpoints for enterococci. J Clin Microbiol 1992;30:2525–2528.Google Scholar
57. Swenson, JM, Clark, NC, Ferraro, MJ, Sahm, DF, Doern, G, Pfaller, MA, et al. Development of a standardized screening method for detection of vancomycin-resistant enterococci. J Clin Microbiol 1994;32:1700–1704.Google Scholar
58. National Committee for Clinical Laboratory Standards. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Approved standard M7-A3. Villanova, PA: National Committee for Clinical Laboratory Standards; 1993.Google Scholar
59. National Committee for Clinical Laboratory Standards. Performance standards for antimicrobial disk susceptibility tests. Approved standard M2-A5. Villanova, PA: National Committee for Clinical Laboratory Standards; 1993.Google Scholar
60. Ribeiro, J, Chenevert, C, Miller, N, Boyce, J. Prevalence of vancomycin-resistant enterococci (VRE) among nursing home residents (NHR) admitted to a university-affiliated hospital. Infect Control Hosp Epidemiol 1997;18:(suppl)P23. Abstract.Google Scholar
61. Revuelta, MP, Nord, JA, Yarrish, RL, Kislak, JW, LaBombardi, V. Recycling of hospital-acquired colonization with vancomycin resistant enterococci via nursing home residents. Clin Infect Dis 1995;21:730. Abstract.Google Scholar
62. Sargent, SJ, Baselski, VS, Reed, LD, Wong, L, Sahm, DF. Simultaneous hospital and community emergence of vancomycin-resistant Enterococcus faecium . Clin Infect Dis 1995;21:729. Abstract.Google Scholar
63. Bates, J. Epidemiology of vancomycin-resistant enterococcus in the community and the relevance of farm animals to human infection. J Hosp Infect 1997;37:89–101.Google Scholar
64. Coque, TM, Tomayko, JF, Ricke, SC, Okhyusen, PC, Murray, BE. Vancomycin-resistant enterococci from nosocomial, community, and animal sources in the United States. Antimicrob Agents Chemother 1996;40:2605–2609.Google Scholar
65. Semmelweis, I. The Etiology, the Concept, and the Prophylaxis of Childbed Fever. Pest, CA: Hartlben's Verlag-Expedition; 1861. Translated by FP Murphy and republished, Classics of Medicine Library, Birmingham, AL; 1981.Google Scholar
66. Larson, E, Kretzer, EK. Compliance with handwashing and barrier precautions. J Hosp Infect 1995;30:88–106.Google Scholar
67. Jarvis, WR. Handwashing—the Semmelweis lesson forgotten? Lancet 1994;344:1311–1312.Google Scholar
68. Voss, A, Widmer, AF. No time for handwashing!? Handwashing versus alcoholic rub: can we afford 100% compliance? Infect Control Hosp Epidemiol 1997;18:205–208.Google Scholar
69. Larson, E, McGeer, A, Quraishi, A, Krenzischek, D, Parsons, BJ, Holdford, J, et al. Effect of an automated sink on handwashing practices and attitudes in high-risk units. Infect Control Hosp Epidemiol 1991;12:422–428.Google Scholar
70. Maki, DG, Zilz, MA, McCormick, R. The effectiveness of using pre-emptive barrier precautions routinely (protective isolation) in all high-risk patients to prevent nosocomial infection with resistant organisms, especially MRSA, VRE, and C difficile. The 34th Annual Meeting of the Infectious Diseases Society of America; New Orleans, LA; 09 1996. Abstract 43.Google Scholar
71. Goldmann, DA, Weinstein, RA, Wenzel, RP, Tablan, OC, Duma, RJ, Gaynes, RP, et al. Strategies to prevent and control antimicrobial-resistant microorganisms in hospitals: a challenge to hospital leadership. JAMA 1996;275:234–240.Google Scholar
72. Centers for Disease Control and Prevention. Update: Staphylococcus aureus with reduced susceptibility to vancomycin—United States. MMWR 1997;46:813–815.Google Scholar