Strategies and challenges of antimicrobial stewardship in long-term care facilities

Clinical Microbiology and Infection

Volumn 21, Issue 1, 2015, Pages 10-19

  Dyar, O J ^a   Pagani, L ^b   Pulcini, C ^c,d  

^a NORTH DEVON DISTRICT HOSPITAL   (United Kingdom)

^b CENTRAL HOSPITAL OF BOLZANO   (Italy)

^c UNIVERSITY HOSPITAL OF NANCY   (France)

^d UNIVERSITÉ DE LORRAINE   (France)

Author keywords

Antibiotic prescribing; Bacterial resistance; Elderly; Infectious diseases; Nursing home; Review

Indexed keywords

ANTIINFECTIVE AGENT;

ANTIBIOTIC PROPHYLAXIS; ANTIBIOTIC RESISTANCE; ANTIBIOTIC THERAPY; BACTERIAL COLONIZATION; CLINICAL EXAMINATION; EUROPE; FEVER; HEALTH CARE FACILITY; HEALTH SURVEY; HUMAN; IRELAND; LONG TERM CARE; LONG TERM CARE FACILITY; MEDICAL EDUCATION; MEDICAL STAFF; NURSING STAFF; PATIENT COMFORT; PATIENT EDUCATION; PNEUMONIA; PRESCRIPTION; PREVALENCE; PREVENTION AND CONTROL; PRIORITY JOURNAL; REVIEW; UNITED STATES; URINALYSIS; URINARY TRACT INFECTION; INAPPROPRIATE PRESCRIBING; PHARMACY;

BACTERIA (MICROORGANISMS);

ANTI-INFECTIVE AGENTS; DRUG RESISTANCE, BACTERIAL; HUMANS; INAPPROPRIATE PRESCRIBING; LONG-TERM CARE; PHARMACEUTICAL SERVICES;

EID: 84926286090     PISSN: 1198743X     EISSN: 14690691     Source Type: Journal    
DOI: 10.1016/j.cmi.2014.09.005     Document Type: Review

References (83)

1. Suetens C. Healthcare-associated infections in European long-term care facilities: how big is the challenge?. Euro Surveill 2012, 17(35). pii=20259.
2. Jump R.L., Olds D.M., Jury L.A., Sitzlar B., Saade E., Watts B., et al. Specialty care delivery: bringing infectious disease expertise to the residents of a Veterans Affairs long-term care facility. JAm Geriatr Soc 2013, 61:782-787.
3. Gavazzi G., Krause K.H. Ageing and infection. Lancet Infect Dis 2002, 2:659-666.
4. Nicolle L.E., Bentley D.W., Garibaldi R., Neuhaus E.G., Smith P.W. Antimicrobial use in long-term-care facilities. SHEA long-term-care committee. Infect Control Hosp Epidemiol 2000, 21:537-545.
5. Stuart R.L., Wilson J., Bellaard-Smith E., Brown R., Wright L., Vandergraaf S., et al. Antibiotic use and misuse in residential aged care facilities. Intern Med J 2012, 42:1145-1149.
6. McClean P., Tunney M., Gilpin D., Parsons C., Hughes C. Antimicrobial prescribing in residential homes. JAntimicrob Chemother 2012, 67:1781-1790.
7. van Buul L.W., van der Steen J.T., Veenhuizen R.B., Achterberg W.P., Schellevis F.G., Essink R.T., et al. Antibiotic use and resistance in long term care facilities. JAm Med Dir Assoc 2012, 13(6). 568.e1-13.
8. Daneman N., Gruneir A., Bronskill S.E., Newman A., Fischer H.D., Rochon P.A., et al. Prolonged antibiotic treatment in long-term care: role of the prescriber. JAMA Intern Med 2013, 173:673-682.
9. Loeb M., Simor A.E., Landry L., Walter S., McArthur M., Duffy J., et al. Antibiotic use in Ontario facilities that provide chronic care. JGen Intern Med 2001, 16:376-383.
10. Daneman N., Gruneir A., Newman A., Fischer H.D., Bronskill S.E., Rochon P.A., et al. Antibiotic use in long-term care facilities. JAntimicrob Chemother 2011, 66:2856-2863.
11. McClean P., Hughes C., Tunney M., Goossens H., Jans B. Antimicrobial prescribing in European nursing homes. JAntimicrob Chemother 2011, 66:1609-1616.
12. Rotjanapan P., Dosa D., Thomas K.S. Potentially inappropriate treatment of urinary tract infections in two Rhode Island nursing homes. Arch Intern Med 2011, 171:438-443.
13. Loeb M. Antibiotic use in long-term-care facilities: many unanswered questions. Infect Control Hosp Epidemiol 2000, 21:680-683.
14. Peron E.P., Hirsch A.A., Jury L.A., Jump R.L., Donskey C.J. Another setting for stewardship: high rate of unnecessary antimicrobial use in a Veterans Affairs long-term care facility. JAm Geriatr Soc 2013, 61:289-290.
15. Mathei C., Niclaes L., Suetens C., Jans B., Buntinx F. Infections in residents of nursing homes. Infect Dis Clin North Am 2007, 21:761-772. ix.
16. Moro M.L., Gagliotti C. Antimicrobial resistance and stewardship in long-term care settings. Future Microbiol 2013, 8:1011-1025.
17. Lim C.J., Kong D.C., Stuart R.L. Reducing inappropriate antibiotic prescribing in the residential care setting: current perspectives. Clin Interv Aging 2014, 9:165-177.
18. Nicolle L.E. Antimicrobial stewardship in long term care facilities: what is effective?. Antimicrob Resist Infect Control 2014, 3:6.
19. Rhee S.M., Stone N.D. Antimicrobial stewardship in long-term care facilities. Infect Dis Clin North Am 2014, 28:237-246.
20. Donlon S., Roche F., Byrne H., Dowling S., Cotter M., Fitzpatrick F. Anational survey of infection control and antimicrobial stewardship structures in Irish long-term care facilities. Am J Infect Control 2013, 41:554-557.
21. European Surveillance of Antimicrobial Consumption (ESAC) Report on point prevalence survey of antimicrobial prescription in European nursing homes 2009, Available from:, [accessed 07.11.14]. http://www.ecdc.europa.eu/en/activities/surveillance/ESAC-Net/publications.
22. European Surveillance of Antimicrobial Consumption (ESAC) Results from the national survey of characteristics of nursing homes 2009, Available from:, [accessed 7.11.14]. http://www.ecdc.europa.eu/en/activities/surveillance/ESAC-Net/publications.
23. Van Schooneveld T., Miller H., Sayles H., Watkins K., Smith P.W. Survey of antimicrobial stewardship practices in Nebraska long-term care facilities. Infect Control Hosp Epidemiol 2011, 32:732-734.
24. Healthcare-associated infections in long-term care facilities (HALT) Results of the pilot point-prevalence survey 2009, Available from:, [accessed 07.11.14]. http://halt.wiv-isp.be.
25. Lim C.J., Kwong M.W., Stuart R.L., Buising K.L., Friedman N.D., Bennett N.J., et al. Antibiotic prescribing practice in residential aged care facilities - health care providers' perspectives. Med J Aust 2014, 201:101-105.
26. D'Agata E., Loeb M.B., Mitchell S.L. Challenges in assessing nursing home residents with advanced dementia for suspected urinary tract infections. JAm Geriatr Soc 2013, 61:62-66.
27. Loeb M., Bentley D.W., Bradley S., Crossley K., Garibaldi R., Gantz N., et al. Development of minimum criteria for the initiation of antibiotics in residents of long-term-care facilities: results of a consensus conference. Infect Control Hosp Epidemiol 2001, 22:120-124.
28. Schweizer A.K., Hughes C.M., Macauley D.C., O'Neill C. Managing urinary tract infections in nursing homes: a qualitative assessment. Pharm World Sci 2005, 27:159-165.
29. Zabarsky T.F., Sethi A.K., Donskey C.J. Sustained reduction in inappropriate treatment of asymptomatic bacteriuria in a long-term care facility through an educational intervention. Am J Infect Control 2008, 36:476-480.
30. Mylotte J.M. Measuring antibiotic use in a long-term care facility. Am J Infect Control 1996, 24:174-179.
31. Nicolle L.E. Urinary tract infection in long-term-care facility residents. Clin Infect Dis 2000, 31:757-761.
32. Rummukainen M.L., Jakobsson A., Matsinen M., Jarvenpaa S., Nissinen A., Karppi P., et al. Reduction in inappropriate prevention of urinary tract infections in long-term care facilities. Am J Infect Control 2012, 40:711-714.
33. van der Steen J.T., Lane P., Kowall N.W., Knol D.L., Volicer L. Antibiotics and mortality in patients with lower respiratory infection and advanced dementia. JAm Med Dir Assoc 2012, 13:156-161.
34. D'Agata E., Mitchell S.L. Patterns of antimicrobial use among nursing home residents with advanced dementia. Arch Intern Med 2008, 168:357-362.
35. Leibovici L., Paul M. Ethical dilemmas in antibiotic treatment: focus on the elderly. Clin Microbiol Infect 2014, [e-published ahead of print].
36. Arnold S.R., Straus S.E. Interventions to improve antibiotic prescribing practices in ambulatory care. Cochrane Database Syst Rev 2005, CD003539.
37. Davey P., Brown E., Charani E., Fenelon L., Gould I.M., Holmes A., et al. Interventions to improve antibiotic prescribing practices for hospital inpatients. Cochrane Database Syst Rev 2013, 4:CD003543.
38. Fleming A., Browne J., Byrne S. The effect of interventions to reduce potentially inappropriate antibiotic prescribing in long-term care facilities: a systematic review of randomised controlled trials. Drugs Aging 2013, 30:401-408.
39. Loeb M., Brazil K., Lohfeld L., McGeer A., Simor A., Stevenson K., et al. Effect of a multifaceted intervention on number of antimicrobial prescriptions for suspected urinary tract infections in residents of nursing homes: cluster randomised controlled trial. BMJ 2005, 331:669.
40. Naughton B.J., Mylotte J.M., Ramadan F., Karuza J., Priore R.L. Antibiotic use, hospital admissions, and mortality before and after implementing guidelines for nursing home-acquired pneumonia. JAm Geriatr Soc 2001, 49:1020-1024.
41. Pettersson E., Vernby A., Molstad S., Lundborg C.S. Can a multifaceted educational intervention targeting both nurses and physicians change the prescribing of antibiotics to nursing home residents? A cluster randomized controlled trial. JAntimicrob Chemother 2011, 66:2659-2666.
42. Monette J., Miller M.A., Monette M., Laurier C., Boivin J.F., Sourial N., et al. Effect of an educational intervention on optimizing antibiotic prescribing in long-term care facilities. JAm Geriatr Soc 2007, 55:1231-1235.
43. Fleet E., Gopal Rao G., Patel B., Cookson B., Charlett A., Bowman C., et al. Impact of implementation of a novel antimicrobial stewardship tool on antibiotic use in nursing homes: a prospective cluster randomized control pilot study. JAntimicrob Chemother 2014, 69:2265-2273.
44. Jump R.L., Olds D.M., Seifi N., Kypriotakis G., Jury L.A., Peron E.P., et al. Effective antimicrobial stewardship in a long-term care facility through an infectious disease consultation service: keeping a LID on antibiotic use. Infect Control Hosp Epidemiol 2012, 33:1185-1192.
45. Linnebur S.A., Fish D.N., Ruscin J.M., Radcliff T.A., Oman K.S., Fink R., et al. Impact of a multidisciplinary intervention on antibiotic use for nursing home-acquired pneumonia. Am J Geriatr Pharmacother 2011, 9:442-450. e1.
46. Schwartz D.N., Abiad H., DeMarais P.L., Armeanu E., Trick W.E., Wang Y., et al. An educational intervention to improve antimicrobial use in a hospital-based long-term care facility. JAm Geriatr Soc 2007, 55:1236-1242.
47. Hutt E., Ruscin J.M., Corbett K., Radcliff T.A., Kramer A.M., Williams E.M., et al. Amultifaceted intervention to implement guidelines improved treatment of nursing home-acquired pneumonia in a state Veterans home. JAm Geriatr Soc 2006, 54:1694-1700.
48. Zimmerman S., Sloane P.D., Bertrand R., Olsho L.E., Beeber A., Kistler C., et al. Successfully reducing antibiotic prescribing in nursing homes. JAm Geriatr Soc 2014, 62:907-912.
49. Pulcini C., Botelho-Nevers E., Dyar O.J., Harbarth S. The impact of infectious diseases specialists on antibiotic prescribing in hospitals. Clin Microbiol Infect 2014, [e-published ahead of print].
50. Sloane P.D., Zimmerman S., Brown L.C., Ives T.J., Walsh J.F. Inappropriate medication prescribing in residential care/assisted living facilities. JAm Geriatr Soc 2002, 50:1001-1011.
51. Pulcini C., Gyssens I.C. How to educate prescribers in antimicrobial stewardship practices. Virulence 2013, 4:192-202.
52. Ohl C.A., Luther V.P. Health care provider education as a tool to enhance antibiotic stewardship practices. Infect Dis Clin North Am 2014, 28:177-193.
53. Dellit T.H., Owens R.C., McGowan J.E., Gerding D.N., Weinstein R.A., Burke J.P., et al. Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America guidelines for developing an institutional program to enhance antimicrobial stewardship. Clin Infect Dis 2007, 44:159-177.
54. Pulcini C., Lions C., Ventelou B., Verger P. Drug-specific quality indicators assessing outpatient antibiotic use among French general practitioners. Eur J Public Health 2013, 23:262-264.
55. Pulcini C., Lions C., Ventelou B., Verger P. Approaching the quality of antibiotic prescriptions in primary care using reimbursement data. Eur J Clin Microbiol Infect Dis 2013, 32:325-332.
56. Rummukainen M.L., Karki T., Kanerva M., Haapasaari M., Ollgren J., Lyytikainen O. Antimicrobial prescribing in nursing homes in Finland: results of three point prevalence surveys. Infection 2013, 41:355-360.
57. Albert X., Huertas I., Pereiro I.I., Sanfelix J., Gosalbes V., Perrota C. Antibiotics for preventing recurrent urinary tract infection in non-pregnant women. Cochrane Database Syst Rev 2004, CD001209.
58. Nicolle L.E., Bradley S., Colgan R., Rice J.C., Schaeffer A., Hooton T.M. Infectious Diseases Society of America guidelines for the diagnosis and treatment of asymptomatic bacteriuria in adults. Clin Infect Dis 2005, 40:643-654.
59. Phillips C.D., Adepoju O., Stone N., Moudouni D.K., Nwaiwu O., Zhao H., et al. Asymptomatic bacteriuria, antibiotic use, and suspected urinary tract infections in four nursing homes. BMC Geriatr 2012, 12:73.
60. Tinelli M., Cataldo M.A., Mantengoli E., Cadeddu C., Cunietti E., Luzzaro F., et al. Epidemiology and genetic characteristics of extended-spectrum beta-lactamase-producing Gram-negative bacteria causing urinary tract infections in long-term care facilities. JAntimicrob Chemother 2012, 67:2982-2987.
61. Couderc C., Jolivet S., Thiebaut A.C., Ligier C., Remy L., Alvarez A.S., et al. Fluoroquinolone use is a risk factor for methicillin-resistant Staphylococcus aureus acquisition in long-term care facilities: a nested case-case-control study. Clin Infect Dis 2014, 59:206-215.
62. Dimopoulos G., Matthaiou D.K., Karageorgopoulos D.E., Grammatikos A.P., Athanassa Z., Falagas M.E. Short- versus long-course antibacterial therapy for community-acquired pneumonia: a meta-analysis. Drugs 2008, 68:1841-1854.
63. Hepburn M.J., Dooley D.P., Skidmore P.J., Ellis M.W., Starnes W.F., Hasewinkle W.C. Comparison of short-course (5 days) and standard (10 days) treatment for uncomplicated cellulitis. Arch Intern Med 2004, 164:1669-1674.
64. Lutters M., Vogt-Ferrier N.B. Antibiotic duration for treating uncomplicated, symptomatic lower urinary tract infections in elderly women. Cochrane Database Syst Rev 2008, CD001535.
65. Walker S., McGeer A., Simor A.E., Armstrong-Evans M., Loeb M. Why are antibiotics prescribed for asymptomatic bacteriuria in institutionalized elderly people? A qualitative study of physicians' and nurses' perceptions. CMAJ 2000, 163:273-277.
66. Boivin Y., Talon D., Leroy J., Floret N., Gbaguidi-Haore H., Bertrand X. Antibiotic prescription in nursing homes for dependent elderly people: a cross-sectional study in Franche-Comté. Med Mal Infect 2013, 43:163-169.
67. Pulcini C., Defres S., Aggarwal I., Nathwani D., Davey P. Design of a 'day 3 bundle' to improve the reassessment of inpatient empirical antibiotic prescriptions. JAntimicrob Chemother 2008, 61:1384-1388.
68. Coupat C., Pradier C., Degand N., Hofliger P., Pulcini C. Selective reporting of antibiotic susceptibility data improves the appropriateness of intended antibiotic prescriptions in urinary tract infections: a case-vignette randomised study. Eur J Clin Microbiol Infect Dis 2013, 32:627-636.
69. Leis J.A., Rebick G.W., Daneman N., Gold W.L., Poutanen S.M., Lo P., et al. Reducing antimicrobial therapy for asymptomatic bacteriuria among noncatheterized inpatients: a proof-of-concept study. Clin Infect Dis 2014, 58:980-983.
70. Church D.L., Davies H.D., Mitton C., Semeniuk H., Logue M., Maxwell C., et al. Clinical and economic evaluation of rapid influenza a virus testing in nursing homes in Calgary, Canada. Clin Infect Dis 2002, 34:790-795.
71. Sundvall P.D., Gunnarsson R.K. Evaluation of dipstick analysis among elderly residents to detect bacteriuria: a cross-sectional study in 32 nursing homes. BMC Geriatr 2009, 9:32.
72. Stucker F., Herrmann F., Graf J.D., Michel J.P., Krause K.H., Gavazzi G. Procalcitonin and infection in elderly patients. JAm Geriatr Soc 2005, 53:1392-1395.
73. Lim C.J., Kwong M., Stuart R.L., Buising K.L., Friedman N.D., Bennett N., et al. Antimicrobial stewardship in residential aged care facilities: need and readiness assessment. BMC Infect Dis 2014, 14:410.
74. van Buul L.W., Sikkens J.J., van Agtmael M.A., Kramer M.H., van der Steen J.T., Hertogh C.M. Participatory action research in antimicrobial stewardship: a novel approach to improving antimicrobial prescribing in hospitals and long-term care facilities. JAntimicrob Chemother 2014, 69:1734-1741.
75. Pulcini C., Crofts S., Campbell D., Davey P. Design, measurement, and evaluation of an education strategy in the hospital setting to combat antimicrobial resistance. Dis Manage Health Outcomes 2007, 15:151-163.
76. Huttner B. The importance of the infectious diseases consultant in a geriatric hospital. Clin Microbiol Infect 2014, [e-published ahead of print].
77. Policy statement on antimicrobial stewardship by the Society for Healthcare Epidemiology of America (SHEA), the Infectious Diseases Society of America (IDSA), and the Pediatric Infectious Diseases Society (PIDS). Infect Control Hosp Epidemiol 2012, 33:322-327.
78. Carlet J., Pulcini C., Piddock L.J. Antibiotic resistance: a geo-political issue. Clin Microbiol Infect 2014, [e-published ahead of print].
79. Cookson B., Mackenzie D., Kafatos G., Jans B., Latour K., Moro M.L., et al. Development and assessment of national performance indicators for infection prevention and control and antimicrobial stewardship in European long-term care facilities. JHosp Infect 2013, 85:45-53.
80. Craig P., Dieppe P., Macintyre S., Michie S., Nazareth I., Petticrew M. Developing and evaluating complex interventions: the new medical research council guidance. BMJ 2008, 337:a1655.
81. Stone S.P., Cooper B.S., Kibbler C.C., Cookson B.D., Roberts J.A., Medley G.F., et al. The ORION statement: guidelines for transparent reporting of outbreak reports and intervention studies of nosocomial infection. Lancet Infect Dis 2007, 7:282-288.
82. Buising K.L., Thursky K.A., Black J.F., MacGregor L., Street A.C., Kennedy M.P., et al. Improving antibiotic prescribing for adults with community acquired pneumonia: Does a computerised decision support system achieve more than academic detailing alone?-a time series analysis. BMC Med Inform Decis Mak 2008, 8:35.
83. Demonchy E., Dufour J.C., Gaudart J., Cervetti E., Michelet P., Poussard N., et al. Impact of a computerized decision support system on compliance with guidelines on antibiotics prescribed for urinary tract infections in emergency departments: a multicentre prospective before-and-after controlled interventional study. JAntimicrob Chemother 2014, 69:2857-2863.