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Expert Review of Anti-infective Therapy Volume 14, 2016 - Issue 2
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Reviews

Prevention of infections in nursing homes: antibiotic prophylaxis versus infection control and antimicrobial stewardship measures

Maddalena GiannellaClinic of Infectious Diseases, Department of Medical and Surgical Sciences, University of Bologna, Bologna, ItalyCorrespondence[email protected]
,
Sara TedeschiClinic of Infectious Diseases, Department of Medical and Surgical Sciences, University of Bologna, Bologna, Italy
,
Michele BartolettiClinic of Infectious Diseases, Department of Medical and Surgical Sciences, University of Bologna, Bologna, Italy
&
Pierluigi VialeClinic of Infectious Diseases, Department of Medical and Surgical Sciences, University of Bologna, Bologna, Italy
Pages 219-230 | Received 13 Oct 2015, Accepted 11 Dec 2015, Published online: 21 Jan 2016

References

  • Papers of special note have been highlighted as:
  • •• of considerable interest
  • Yoshikawa TT. Epidemiology and unique aspects of aging and infectious diseases. Clin Infect Dis. 2000;30(6):931–933.
  • Shang J, Ma C, Poghosyan L, et al. The prevalence of infections and patient risk factors in home health care: a systematic review. Am J Infect Control. 2014;42(5):479–484.
  • Gavazzi G, Krause K-H. Ageing and infection. Lancet Infect Dis. 2002;2(11):659–666.
  • Loeb M. Antibiotic use in long-term-care facilities: many unanswered questions. Infect Control Hosp Epidemiol. 2000;21(10):680–683.
  • D’Agata E, Loeb MB, Mitchell SL. Challenges in assessing nursing home residents with advanced dementia for suspected urinary tract infections. J Am Geriatr Soc. 2013;61(1):62–66.
  • Ingarfield SL, Finn JC, Jacobs IG, et al. Use of emergency departments by older people from residential care: a population based study. Age Ageing. 2009;38(3):314–318.
  • Tsan L, Davis C, Langberg R, et al. Prevalence of nursing home-associated infections in the Department of Veterans Affairs nursing home care units. Am J Infect Control. 2008;36(3):173–179.
  • Eikelenboom-Boskamp A, Cox-Claessens JH, Boom-Poels PG, et al. Three-year prevalence of healthcare-associated infections in Dutch nursing homes. J Hosp Infect. 2011;78(1):59–62.
  • Lim CJ, McLellan SC, Cheng AC, et al. Surveillance of infection burden in residential aged care facilities. Med J Aust. 2012;196(5):327–331.
  • Engelhart ST, Hanses-Derendorf L, Exner M, et al. Prospective surveillance for healthcare-associated infections in German nursing home residents. J Hosp Infect. 2005;60(1):46–50.
  • Cotter M, Donlon S, Roche F, et al. Healthcare-associated infection in Irish long-term care facilities: results from the First National Prevalence Study. J Hosp Infect. 2012;80(3):212–216.
  • Moro ML, Ricchizzi E, Morsillo F, et al. Infections and antimicrobial resistance in long term care facilities: a national prevalence study. Ann Ig. 2013;25(2):109–118.
  • Smith M, Atkins S, Worth L, et al. Infections and antimicrobial use in Australian residential aged care facilities: a comparison between local and international prevalence and practices. Aust Health Rev. 2013;37(4):529–534.
  • Stone ND, Ashraf MS, Calder J, et al. Surveillance definitions of infections in long-term care facilities: revisiting the McGeer criteria. Infect Control Hosp Epidemiol. 2012;33(10):965–977.
  • Smith PW, Bennett G, Bradley S, et al. SHEA/APIC guideline: infection prevention and control in the long-term care facility, July 2008. Infect Control Hosp Epidemiol. 2008;29(9):785–814.
  • Wang L, Lansing B, Symons K, et al. Infection rate and colonization with antibiotic-resistant organisms in skilled nursing facility residents with indwelling devices. Eur J Clin Microbiol Infect Dis. 2012;31(8):1797–1804.
  • Smith PW, Seip CW, Schaefer SC, et al. Microbiologic survey of long-term care facilities. Am J Infect Control. 2000;28(1):8–13.
  • Mody L, Juthani-Mehta M. Urinary tract infections in older women: a clinical review. JAMA. 2014;311(8):844–854.
  • Lammers RL, Gibson S, Kovacs D, et al. Comparison of test characteristics of urine dipstick and urinalysis at various test cutoff points. Ann Emerg Med. 2001;38(5):505–512.
  • Tambyah PA, Maki DG. The relationship between pyuria and infection in patients with indwelling urinary catheters: a prospective study of 761 patients. Arch Intern Med. 2000;160(5):673–677.
  • Rogers MAM, Mody L, Kaufman SR, et al. Use of urinary collection devices in skilled nursing facilities in five states. J Am Geriatr Soc. 2008;56(5):854–861.
  • Nicolle LE. Urinary catheter-associated infections. Infect Dis Clin North Am. 2012;26(1):13–27.
  • Maki DG, Tambyah PA. Engineering out the risk for infection with urinary catheters. Emerg Infect Dis. 2001;7(2):342–347.
  • Nicolle LE. Urinary tract infections in long-term-care facilities. Infect Control Hosp Epidemiol. 2001;22(3):167–175.
  • Terpenning MS, Bradley SF, Wan JY, et al. Colonization and infection with antibiotic-resistant bacteria in a long-term care facility. J Am Geriatr Soc. 1994;42(10):1062–1069.
  • El-Solh AA, Niederman MS, Drinka P. Nursing home-acquired pneumonia: a review of risk factors and therapeutic approaches. Curr Med Res Opin. 2010;26(12):2707–2714.
  • Muder RR, Aghababian RV, Loeb MB, et al. Nursing home-acquired pneumonia: an emergency department treatment algorithm. Curr Med Res Opin. 2004;20(8):1309–1320.
  • Liapikou A, Polverino E, Cilloniz C, et al. A worldwide perspective of nursing home-acquired pneumonia compared with community-acquired pneumonia. Respir Care. 2014;59(7):1078–1085.
  • Myint PK, Kamath AV, Vowler SL, et al. Severity assessment criteria recommended by the British Thoracic Society (BTS) for community-acquired pneumonia (CAP) and older patients. Should SOAR (systolic blood pressure, oxygenation, age and respiratory rate) criteria be used in older people? A compilation study of two prospective cohorts. Age Ageing. 2006;35(3):286–291.
  • Kollef MH, Shorr A, Tabak YP, et al. Epidemiology and outcomes of health-care-associated pneumonia: results from a large US database of culture-positive pneumonia. Chest. 2005;128(6):3854–3862.
  • Micek ST, Kollef KE, Reichley RM, et al. Health care-associated pneumonia and community-acquired pneumonia: a single-center experience. Antimicrob Agents Chemother. 2007;51(10):3568–3573.
  • Carratala J, Mykietiuk A, Fernandez-Sabe N, et al. Health care-associated pneumonia requiring hospital admission: epidemiology, antibiotic therapy, and clinical outcomes. Arch Intern Med. 2007;167(13):1393–1399.
  • Giannella M, Pinilla B, Capdevila JA, et al. Pneumonia treated in the internal medicine department: focus on healthcare-associated pneumonia. Clin Microbiol Infect. 2012;18(8):786–794.
  • Pawar D, Tsay R, Nelson DS, et al. Burden of Clostridium difficile infection in long-term care facilities in Monroe County, New York. Infect Control Hosp Epidemiol. 2012;33(11):1107–1112.
  • Gaynes R, Rimland D, Killum E, et al. Outbreak of Clostridium difficile infection in a long-term care facility: association with gatifloxacin use. Clin Infect Dis. 2004;38(5):640–645.
  • Birgand G, Blanckaert K, Carbonne A, et al. Investigation of a large outbreak of Clostridium difficile PCR-ribotype 027 infections in northern France, 2006-2007 and associated clusters in 2008-2009. Euro Surveill. 2010;15(25):1–6.
  • Simor AE, Yake SL, Tsimidis K. Infection due to Clostridium difficile among elderly residents of a long-term-care facility. Clin Infect Dis. 1993;17(4):672–678.
  • Thomas DR, Bennett RG, Laughon BE, et al. Postantibiotic colonization with Clostridium difficile in nursing home patients. J Am Geriatr Soc. 1990;38(4):415–420.
  • Al-Tureihi FIJ, Hassoun A, Wolf-Klein G, et al. Albumin, length of stay, and proton pump inhibitors: key factors in Clostridium difficile-associated disease in nursing home patients. J Am Med Dir Assoc. 2005;6(2):105–108.
  • Leekha S, Aronhalt KC, Sloan LM, et al. Asymptomatic Clostridium difficile colonization in a tertiary care hospital: admission prevalence and risk factors. Am J Infect Control. 2013;41(5):390–393.
  • Loo VG, Bourgault A-M, Poirier L, et al. Host and pathogen factors for Clostridium difficile infection and colonization. N Engl J Med. 2011;365(18):1693–1703.
  • Tsan L, Langberg R, Davis C, et al. Nursing home-associated infections in Department of Veterans Affairs community living centers. Am J Infect Control. 2010;38(6):461–466.
  • Van Buul LW, Veenhuizen RB, Achterberg WP, et al. Antibiotic prescribing in Dutch nursing homes: how appropriate is it? J Am Med Dir Assoc. 2015;16(3):229–237.
  • Kirk MD, Veitch MG, Hall GV. Gastroenteritis and food-borne disease in elderly people living in long-term care. Clin Infect Dis. 2010;50(3):397–404.
  • Jones TF. When diarrhea gets deadly: a look at gastroenteritis outbreaks in nursing homes. Clin Infect Dis. 2010;51(8):915–916.
  • Kirk MD, Fullerton KE, Hall GV, et al. Surveillance for outbreaks of gastroenteritis in long-term care facilities, Australia, 2002-2008. Clin Infect Dis. 2010;51(8):907–914.
  • Greig JD, Lee MB. Enteric outbreaks in long-term care facilities and recommendations for prevention: a review. Epidemiol Infect. 2009;137(2):145–155.
  • Ellis SE, Coffey CS, Mitchel EF Jr, et al. Influenza- and respiratory syncytial virus-associated morbidity and mortality in the nursing home population. J Am Geriatr Soc. 2003;51(6):761–767.
  • Ikram R, Psutka R, Carter A, et al. An outbreak of multi-drug resistant Escherichia coli urinary tract infection in an elderly population: a case-control study of risk factors. BMC Infect Dis. 2015;15:224.
  • Ben-Ami R, Schwaber MJ, Navon-Venezia S, et al. Influx of extended-spectrum beta-lactamase-producing enterobacteriaceae into the hospital. Clin Infect Dis. 2006;42(7):925–934.
  • Pop-Vicas A, Mitchell SL, Kandel R, et al. Multidrug-resistant gram-negative bacteria in a long-term care facility: prevalence and risk factors. J Am Geriatr Soc. 2008;56(7):1276–1280.
  • Hudson LO, Reynolds C, Spratt BG, et al. Diversity of methicillin-resistant Staphylococcus aureus strains isolated from residents of 26 nursing homes in Orange County, California. J Clin Microbiol. 2013;51(11):3788–3795.
  • Epstein L, Mu Y, Belflower R, et al. Risk factors for invasive methicillin-resistant Staphylococcus aureus infection after recent discharge from an acute care hospitalization, 2011-2013. Clin Infect Dis. 2015;62(1):45–52.
  • O’Fallon E, Pop-Vicas A, D’Agata E. The emerging threat of multidrug-resistant gram-negative organisms in long-term care facilities. J Gerontol A Biol Sci Med Sci. 2009;64(1):138–141.
  • Lim CJ, Cheng AC, Kennon J, et al. Prevalence of multidrug-resistant organisms and risk factors for carriage in long-term care facilities: a nested case-control study. J Antimicrob Chemother. 2014;69(7):1972–1980.

•• Point prevalence survey describing the epidemiology and risk factors for colonization with MRSA or MDR GNB among nursing homes residents.

  • D’Agata EM, Habtemariam D, Mitchell S. Multidrug-resistant gram-negative bacteria: inter- and intradissemination among nursing homes of residents with advanced dementia. Infect Control Hosp Epidemiol. 2015;36(8):930–935.
  • March A, Aschbacher R, Dhanji H, et al. Colonization of residents and staff of a long-term-care facility and adjacent acute-care hospital geriatric unit by multiresistant bacteria. Clin Microbiol Infect. 2010;16(7):934–944.
  • Marquez P, Terashita D, Dassey D, et al. Population-based incidence of carbapenem-resistant Klebsiella pneumoniae along the continuum of care, Los Angeles County. Infect Control Hosp Epidemiol. 2013;34(2):144–150.
  • Lin MY, Lyles-Banks RD, Lolans K, et al. The importance of long-term acute care hospitals in the regional epidemiology of Klebsiella pneumoniae carbapenemase-producing Enterobacteriaceae. Clin Infect Dis. 2013;57(9):1246–1252.
  • Van Buul LW, Van Der Steen JT, Veenhuizen RB, et al. Antibiotic use and resistance in long term care facilities. J Am Med Dir Assoc. 2012;13(6):568 e561–513.
  • McClean P, Hughes C, Tunney M, et al. Antimicrobial prescribing in European nursing homes. J Antimicrob Chemother. 2011;66(7):1609–1616.
  • Nicolle LE, Bentley DW, Garibaldi R, et al. Antimicrobial use in long-term-care facilities. SHEA Long-Term-Care Committee. Infect Control Hosp Epidemiol. 2000;21(8):537–545.
  • Loeb M, Simor AE, Landry L, et al. Antibiotic use in Ontario facilities that provide chronic care. J Gen Intern Med. 2001;16(6):376–383.
  • Peron EP, Hirsch AA, Jury LA, et al. Another setting for stewardship: high rate of unnecessary antimicrobial use in a veterans affairs long-term care facility. J Am Geriatr Soc. 2013;61(2):289–290.
  • Mitchell SL, Shaffer ML, Loeb MB, et al. Infection management and multidrug-resistant organisms in nursing home residents with advanced dementia. JAMA Intern Med. 2014;174(10):1660–1667.

•• Prospective study describing the frequent use of antibiotics in nursing home residents with dementia without clinical indication and its impact on the risk of acquiring colonization with MDROs.

  • Daneman N, Bronskill SE, Gruneir A, et al. Variability in antibiotic use across nursing homes and the risk of antibiotic-related adverse outcomes for individual residents. JAMA Intern Med. 2015;175(8):1331–1339.
  • Latour K, Catry B, Broex E, et al. Indications for antimicrobial prescribing in European nursing homes: results from a point prevalence survey. Pharmacoepidemiol Drug Saf. 2012;21(9):937–944.

•• Point-prevalence survey reporting a very frequent use of antibiotic prophylaxis in European nursing homes, mainly to prevent UTI, despite lack of evidence to support this practice.

  • Daneman N, Gruneir A, Newman A, et al. Antibiotic use in long-term care facilities. J Antimicrob Chemother. 2011;66(12):2856–2863.
  • Bergman J, Schjott J, Blix HS. Prevention of urinary tract infections in nursing homes: lack of evidence-based prescription? BMC Geriatr. 2011;11:69.
  • Albert X, Huertas I, Pereiro II, et al. Antibiotics for preventing recurrent urinary tract infection in non-pregnant women. Cochrane Database Syst Rev. 2004;3:CD001209.
  • Lee BB, Simpson JM, Craig JC, et al. Methenamine hippurate for preventing urinary tract infections. Cochrane Database Syst Rev. 2007;4:CD003265.
  • Lee BS, Bhuta T, Simpson JM, et al. Methenamine hippurate for preventing urinary tract infections. Cochrane Database Syst Rev. 2012;10:CD003265.
  • Lim CJ, Kong DC, Stuart RL. Reducing inappropriate antibiotic prescribing in the residential care setting: current perspectives. Clin Interv Aging. 2014;9:165–177.
  • Dyar OJ, Pagani L, Pulcini C. Strategies and challenges of antimicrobial stewardship in long-term care facilities. Clin Microbiol Infect. 2015;21(1):10–19.
  • Rummukainen ML, Jakobsson A, Matsinen M, et al. Reduction in inappropriate prevention of urinary tract infections in long-term care facilities. Am J Infect Control. 2012;40(8):711–714.

•• Article describing an intervention based on education and implementation of guidelines for diagnosis and treatment of infections, expecially UTI. The intervention resultd in a significant reduction of unnecessary antimicrobial use.

  • Leis JA, Rebick GW, Daneman N, et al. Reducing antimicrobial therapy for asymptomatic bacteriuria among noncatheterized inpatients: a proof-of-concept study. Clin Infect Dis. 2014;58(7):980–983.
  • Lohfeld L, Loeb M, Brazil K. Evidence-based clinical pathways to manage urinary tract infections in long-term care facilities: a qualitative case study describing administrator and nursing staff views. J Am Med Dir Assoc. 2007;8(7):477–484.
  • Trautner BW, Grigoryan L, Petersen NJ, et al. Effectiveness of an antimicrobial stewardship approach for urinary catheter-associated asymptomatic bacteriuria. JAMA Intern Med. 2015;175(7):1120–1127.
  • Benoit SR, Nsa W, Richards CL, et al. Factors associated with antimicrobial use in nursing homes: a multilevel model. J Am Geriatr Soc. 2008;56(11):2039–2044.
  • Rotjanapan P, Dosa D, Thomas KS. Potentially inappropriate treatment of urinary tract infections in two Rhode Island nursing homes. Arch Intern Med. 2011;171(5):438–443.
  • Lutters M, Vogt-Ferrier NB. Antibiotic duration for treating uncomplicated, symptomatic lower urinary tract infections in elderly women. Cochrane Database Syst Rev. 2008;3:CD001535.
  • Herath SC, Poole P. Prophylactic antibiotic therapy for chronic obstructive pulmonary disease (COPD). Cochrane Database Syst Rev. 2013;11:CD009764.
  • Albert RK, Connett J, Bailey WC, et al. Azithromycin for prevention of exacerbations of COPD. N Engl J Med. 2011;365(8):689–698.
  • Sethi S, Jones PW, Theron MS, et al. Pulsed moxifloxacin for the prevention of exacerbations of chronic obstructive pulmonary disease: a randomized controlled trial. Respir Res. 2010;11:10.
  • Teramoto S, Yoshida K, Hizawa N. Update on the pathogenesis and management of pneumonia in the elderly-roles of aspiration pneumonia. Respir Investig. 2015;53(5):178–184.
  • Thomas KS, Crook AM, Nunn AJ, et al. Penicillin to prevent recurrent leg cellulitis. N Engl J Med. 2013;368(18):1695–1703.
  • Castle N, Handler S, Wagner L. Hand hygiene practices reported by nurse aides in nursing homes. J Appl Gerontol. 2013;20(10):1–19.
  • Liu WI, Liang SY, Wu SF, et al. Hand hygiene compliance among the nursing staff in freestanding nursing homes in Taiwan: a preliminary study. Int J Nurs Pract. 2014;20(1):46–52.
  • Smith A, Carusone SC, Loeb M. Hand hygiene practices of health care workers in long-term care facilities. Am J Infect Control. 2008;36(7):492–494.
  • Murphy CR, Quan V, Kim D, et al. Nursing home characteristics associated with methicillin-resistant Staphylococcus aureus (MRSA) Burden and Transmission. BMC Infect Dis. 2012;12:269.
  • Schweon SJ, Kirk J. A realistic approach towards hand hygiene for long-term care residents and health care personnel. Am J Infect Control. 2011;39(4):336–338.
  • Hocine MN, Temime L. Impact of hand hygiene on the infectious risk in nursing home residents: a systematic review. Am J Infect Control. 2015;pii:S0196–6553(15)00656-2.
  • Schweon SJ, Edmonds SL, Kirk J, et al. Effectiveness of a comprehensive hand hygiene program for reduction of infection rates in a long-term care facility. Am J Infect Control. 2013;41(1):39–44.
  • Mody L, Meddings J, Edson BS, et al. Enhancing resident safety by preventing healthcare-associated infection: a national initiative to reduce catheter-associated urinary tract infections in nursing homes. Clin Infect Dis. 2015;61(1):86–94.
  • Mody L, Krein SL, Saint S, et al. A targeted infection prevention intervention in nursing home residents with indwelling devices: a randomized clinical trial. JAMA Intern Med. 2015;175(5):714–723.

•• Randomized study to assess the efficacy of a multimodal targeted infection program resulting in a significant reduction of MDRO density and CA-UTI episodes.

  • El-Solh AA. Association between pneumonia and oral care in nursing home residents. Lung. 2011;189(3):173–180.
  • Russell SL, Boylan RJ, Kaslick RS, et al. Respiratory pathogen colonization of the dental plaque of institutionalized elders. Spec Care Dentist. 1999;19(3):128–134.
  • Kaneoka A, Pisegna JM, Miloro KV, et al. Prevention of healthcare-associated pneumonia with oral care in individuals without mechanical ventilation: a systematic review and meta-analysis of randomized controlled trials. Infect Control Hosp Epidemiol. 2015;36(8):899–906.

•• A systemic review and metanalysis including 5 randomized trials suggesting a preventive effect of oral care on pneumonia in nonventilated patients.

  • Juthani-Mehta M, Van Ness PH, McGloin J, et al. A cluster-randomized controlled trial of a multicomponent intervention protocol for pneumonia prevention among nursing home elders. Clin Infect Dis. 2015;60(6):849–857.

•• A randomized controlled trial including more than 800 nursing home residents randomized to receive multicomponent intervention protocol or usual care for prevention of pneumonia. The intervention did not significantly reduced the incidence of pneumonia.

  • Van Der Poll T, Opal SM. Pathogenesis, treatment, and prevention of pneumococcal pneumonia. Lancet. 2009;374(9700):1543–1556.
  • Namkoong H, Funatsu Y, Oishi K, et al. Comparison of the immunogenicity and safety of polysaccharide and protein-conjugated pneumococcal vaccines among the elderly aged 80 years or older in Japan: an open-labeled randomized study. Vaccine. 2015;33(2):327–332.
  • Washio M, Kondo K, Fujisawa N, et al. Hypoalbuminemia, influenza vaccination and other factors related to the development of pneumonia acquired outside hospitals in southern Japan: a case-control study. Geriatr Gerontol Int. 2015. doi:10.1111/ggi.12456.
  • Wendelboe AM, Avery C, Andrade B, et al. Importance of employee vaccination against influenza in preventing cases in long-term care facilities. Infect Control Hosp Epidemiol. 2011;32(10):990–997.
  • Nicolle LE. Infection prevention issues in long-term care. Curr Opin Infect Dis. 2014;27(4):363–369.

•• Review article adressing infection prevention issues and antimicrobial stewardship in LTCFs.

  • Bellini C, Petignat C, Masserey E, et al. Universal screening and decolonization for control of MRSA in nursing homes: a cluster randomized controlled study. Infect Control Hosp Epidemiol. 2015;36(4):401–408.
  • Lee BY, Singh A, Bartsch SM, et al. The potential regional impact of contact precaution use in nursing homes to control methicillin-resistant Staphylococcus aureus. Infect Control Hosp Epidemiol. 2013;34(2):151–160.
  • Jump RL, Olds DM, Seifi N, 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(12):1185–1192.
  • Davey P, Brown E, Charani E, et al. Interventions to improve antibiotic prescribing practices for hospital inpatients. Cochrane Database Syst Rev. 2013;4:CD003543.
  • 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(6):401–408.
  • Tjia J, Gurwitz JH, Briesacher BA. Challenge of changing nursing home prescribing culture. Am J Geriatr Pharmacother. 2012;10(1):37–46.
  • Hughes C, Lapane K, Kerse N. Prescribing for older people in nursing homes: challenges for the future. Int J Older People Nurs. 2011;6(1):63–70.
  • Crnich CJ, Jump R, Trautner B, et al. Optimizing antibiotic stewardship in nursing homes: a narrative review and recommendations for improvement. Drugs Aging. 2015;32(9):699–716.

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