Download PDF
Semin Respir Crit Care Med 2017; 38(03): 381-390
DOI: 10.1055/s-0037-1602584
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Oropharyngeal Decontamination with Antiseptics to Prevent Ventilator-Associated Pneumonia: Rethinking the Benefits of Chlorhexidine

Michael Klompas
1   Department of Population Medicine, Harvard Medical School and Harvard Pilgrim Health Care Institute, Boston, Massachusetts
2   Department of Medicine, Brigham and Women's Hospital, Boston, Massachusetts
› Author Affiliations
Further Information

Publication History

Publication Date:
04 June 2017 (online)

    Permissions and Reprints

Abstract

Daily oral care with chlorhexidine for mechanically ventilated patients is ubiquitous in contemporary intensive care practice. The practice is predicated upon meta-analyses suggesting that adding chlorhexidine to daily oral care regimens can reduce ventilator-associated pneumonia (VAP) rates by up to 40%. Close analysis, however, raises three concerns: (1) the meta-analyses are dominated by studies in cardiac surgery patients in whom average duration of mechanical ventilation is < 1 day and thus their risk of VAP is very different from other populations, (2) diagnosing VAP is subjective and nonspecific yet the meta-analyses gave equal weight to blinded and nonblinded studies, potentially biasing them in favor of chlorhexidine, and (3) there is circularity between diagnostic criteria for VAP and chlorhexidine; as an antiseptic, chlorhexidine may decrease the frequency of positive respiratory cultures but fewer cultures does not necessarily mean fewer pneumonias. It is therefore important to look at other outcomes for corollary evidence on whether or not oral chlorhexidine benefits patients. An updated meta-analysis restricted to double-blinded studies in noncardiac surgery patients showed no impact on VAP rates, duration of mechanical ventilation, or intensive care unit length of stay. Instead, there was a possible signal that oral chlorhexidine may increase mortality rates. Observational data have raised similar concerns. This article will review the theoretical basis for adding chlorhexidine to oral care regimens, delineate potential biases in randomized controlled trials comparing oral care regimens with and without chlorhexidine, explore the unexpected mortality signal associated with oral chlorhexidine, and provide practical recommendations.

Keywords

ventilator-associated pneumonia - oral care - chlorhexidine - quality improvement - ventilator bundles
 

  • References

  • 1 Magill SS, Edwards JR, Bamberg W. , et al; Emerging Infections Program Healthcare-Associated Infections and Antimicrobial Use Prevalence Survey Team. Multistate point-prevalence survey of health care-associated infections. N Engl J Med 2014; 370 (13) 1198-1208
    CrossrefPubMedGoogle Scholar
  • 2 Metersky ML, Wang Y, Klompas M, Eckenrode S, Bakullari A, Eldridge N. Trend in ventilator-associated pneumonia rates between 2005 and 2013. JAMA 2016; 316 (22) 2427-2429
    CrossrefPubMedGoogle Scholar
  • 3 Krein SL, Fowler KE, Ratz D, Meddings J, Saint S. Preventing device-associated infections in US hospitals: national surveys from 2005 to 2013. BMJ Qual Saf 2015; 24 (06) 385-392
    CrossrefPubMedGoogle Scholar
  • 4 Rello J, Koulenti D, Blot S. , et al. Oral care practices in intensive care units: a survey of 59 European ICUs. Intensive Care Med 2007; 33 (06) 1066-1070
    CrossrefPubMedGoogle Scholar
  • 5 Coffin SE, Klompas M, Classen D. , et al. Strategies to prevent ventilator-associated pneumonia in acute care hospitals. Infect Control Hosp Epidemiol 2008; 29 (Suppl. 01) S31-S40
    CrossrefPubMedGoogle Scholar
  • 6 Muscedere J, Dodek P, Keenan S, Fowler R, Cook D, Heyland D. ; VAP Guidelines Committee and the Canadian Critical Care Trials Group. Comprehensive evidence-based clinical practice guidelines for ventilator-associated pneumonia: diagnosis and treatment. J Crit Care 2008; 23 (01) 138-147
    CrossrefPubMedGoogle Scholar
  • 7 Rello J, Lode H, Cornaglia G, Masterton R. ; VAP Care Bundle Contributors. A European care bundle for prevention of ventilator-associated pneumonia. Intensive Care Med 2010; 36 (05) 773-780
    CrossrefPubMedGoogle Scholar
  • 8 de Latorre FJ, Pont T, Ferrer A, Rosselló J, Palomar M, Planas M. Pattern of tracheal colonization during mechanical ventilation. Am J Respir Crit Care Med 1995; 152 (03) 1028-1033
    CrossrefPubMedGoogle Scholar
  • 9 Torres A, Serra-Batlles J, Ros E. , et al. Pulmonary aspiration of gastric contents in patients receiving mechanical ventilation: the effect of body position. Ann Intern Med 1992; 116 (07) 540-543
    CrossrefPubMedGoogle Scholar
  • 10 Bonten MJ, Gaillard CA, van Tiel FH, Smeets HG, van der Geest S, Stobberingh EE. The stomach is not a source for colonization of the upper respiratory tract and pneumonia in ICU patients. Chest 1994; 105 (03) 878-884
    CrossrefPubMedGoogle Scholar
  • 11 Garrouste-Orgeas M, Chevret S, Arlet G. , et al. Oropharyngeal or gastric colonization and nosocomial pneumonia in adult intensive care unit patients. A prospective study based on genomic DNA analysis. Am J Respir Crit Care Med 1997; 156 (05) 1647-1655
    CrossrefPubMedGoogle Scholar
  • 12 El-Solh AA, Pietrantoni C, Bhat A. , et al. Colonization of dental plaques: a reservoir of respiratory pathogens for hospital-acquired pneumonia in institutionalized elders. Chest 2004; 126 (05) 1575-1582
    CrossrefPubMedGoogle Scholar
  • 13 Unertl K, Ruckdeschel G, Selbmann HK. , et al. Prevention of colonization and respiratory infections in long-term ventilated patients by local antimicrobial prophylaxis. Intensive Care Med 1987; 13 (02) 106-113
    PubMedGoogle Scholar
  • 14 Rodríguez-Roldán JM, Altuna-Cuesta A, López A. , et al. Prevention of nosocomial lung infection in ventilated patients: use of an antimicrobial pharyngeal nonabsorbable paste. Crit Care Med 1990; 18 (11) 1239-1242
    CrossrefPubMedGoogle Scholar
  • 15 Pugin J, Auckenthaler R, Lew DP, Suter PM. Oropharyngeal decontamination decreases incidence of ventilator-associated pneumonia. A randomized, placebo-controlled, double-blind clinical trial. JAMA 1991; 265 (20) 2704-2710
    CrossrefPubMedGoogle Scholar
  • 16 DeRiso II AJ, Ladowski JS, Dillon TA, Justice JW, Peterson AC. Chlorhexidine gluconate 0.12% oral rinse reduces the incidence of total nosocomial respiratory infection and nonprophylactic systemic antibiotic use in patients undergoing heart surgery. Chest 1996; 109 (06) 1556-1561
    CrossrefPubMedGoogle Scholar
  • 17 Gjermo P. Chlorhexidine in dental practice. J Clin Periodontol 1974; 1 (03) 143-152
    CrossrefPubMedGoogle Scholar
  • 18 Briner WW, Grossman E, Buckner RY. Effect of chlorhexidine gluconate mouthrinse on plaque bacteria. J Periodontal Res 1986; 21 (Suppl. 16) 44-52
    CrossrefPubMedGoogle Scholar
  • 19 Hua F, Xie H, Worthington HV, Furness S, Zhang Q, Li C. Oral hygiene care for critically ill patients to prevent ventilator-associated pneumonia. Cochrane Database Syst Rev 2016; 10: CD008367
    PubMedGoogle Scholar
  • 20 Segers P, Speekenbrink RG, Ubbink DT, van Ogtrop ML, de Mol BA. Prevention of nosocomial infection in cardiac surgery by decontamination of the nasopharynx and oropharynx with chlorhexidine gluconate: a randomized controlled trial. JAMA 2006; 296 (20) 2460-2466
    CrossrefPubMedGoogle Scholar
  • 21 Özçaka Ö, Başoğlu OK, Buduneli N, Taşbakan MS, Bacakoğlu F, Kinane DF. Chlorhexidine decreases the risk of ventilator-associated pneumonia in intensive care unit patients: a randomized clinical trial. J Periodontal Res 2012; 47 (05) 584-592
    CrossrefPubMedGoogle Scholar
  • 22 Fourrier F, Cau-Pottier E, Boutigny H, Roussel-Delvallez M, Jourdain M, Chopin C. Effects of dental plaque antiseptic decontamination on bacterial colonization and nosocomial infections in critically ill patients. Intensive Care Med 2000; 26 (09) 1239-1247
    CrossrefPubMedGoogle Scholar
  • 23 Chan EY, Ruest A, Meade MO, Cook DJ. Oral decontamination for prevention of pneumonia in mechanically ventilated adults: systematic review and meta-analysis. BMJ 2007; 334 (7599): 889
    CrossrefPubMedGoogle Scholar
  • 24 Labeau SO, Van de Vyver K, Brusselaers N, Vogelaers D, Blot SI. Prevention of ventilator-associated pneumonia with oral antiseptics: a systematic review and meta-analysis. Lancet Infect Dis 2011; 11 (11) 845-854
    CrossrefPubMedGoogle Scholar
  • 25 Klompas M. Ventilator-associated pneumonia: is zero possible?. Clin Infect Dis 2010; 51 (10) 1123-1126
    CrossrefPubMedGoogle Scholar
  • 26 Berwick DM, Calkins DR, McCannon CJ, Hackbarth AD. The 100,000 Lives Campaign: setting a goal and a deadline for improving health care quality. JAMA 2006; 295 (03) 324-327
    CrossrefPubMedGoogle Scholar
  • 27 Institute for Healthcare Improvement. IHI Ventilator Bundle: Daily Oral Care with Chlorhexidine. 2011 . Available at http://www.ihi.org/knowledge/Pages/Changes/DailyOralCarewithChlorhexidine.aspx . Accessed August 6, 2013.
    PubMedGoogle Scholar
  • 28 Lambert ML, Palomar M, Agodi A. , et al. Prevention of ventilator-associated pneumonia in intensive care units: an international online survey. Antimicrob Resist Infect Control 2013; 2 (01) 9
    CrossrefPubMedGoogle Scholar
  • 29 Saddki N, Mohamad Sani FE, Tin-Oo MM. Oral care for intubated patients: a survey of intensive care unit nurses. Nurs Crit Care 2017; 22 (02) 89-98
    CrossrefPubMedGoogle Scholar
  • 30 Miranda AF, de Paula RM, de Castro Piau CG, Costa PP, Bezerra AC. Oral care practices for patients in intensive care units: a pilot survey. Indian J Crit Care Med 2016; 20 (05) 267-273
    CrossrefPubMedGoogle Scholar
  • 31 Feider LL, Mitchell P, Bridges E. Oral care practices for orally intubated critically ill adults. Am J Crit Care 2010; 19 (02) 175-183
    CrossrefPubMedGoogle Scholar
  • 32 Zhang TT, Tang SS, Fu LJ. The effectiveness of different concentrations of chlorhexidine for prevention of ventilator-associated pneumonia: a meta-analysis. J Clin Nurs 2014; 23 (11-12): 1461-1475
    CrossrefPubMedGoogle Scholar
  • 33 Houston S, Hougland P, Anderson JJ, LaRocco M, Kennedy V, Gentry LO. Effectiveness of 0.12% chlorhexidine gluconate oral rinse in reducing prevalence of nosocomial pneumonia in patients undergoing heart surgery. Am J Crit Care 2002; 11 (06) 567-570
    PubMedGoogle Scholar
  • 34 Chastre J, Fagon JY. Ventilator-associated pneumonia. Am J Respir Crit Care Med 2002; 165 (07) 867-903
    CrossrefPubMedGoogle Scholar
  • 35 Caroff DA, Szumita PM, Klompas M. The relationship between sedatives, sedative strategy, and healthcare-associated infection: a systematic review. Infect Control Hosp Epidemiol 2016; 37 (10) 1234-1242
    CrossrefPubMedGoogle Scholar
  • 36 Klompas M. Does this patient have ventilator-associated pneumonia?. JAMA 2007; 297 (14) 1583-1593
    CrossrefPubMedGoogle Scholar
  • 37 Ego A, Preiser JC, Vincent JL. Impact of diagnostic criteria on the incidence of ventilator-associated pneumonia. Chest 2015; 147 (02) 347-355
    CrossrefPubMedGoogle Scholar
  • 38 Tejerina E, Esteban A, Fernández-Segoviano P. , et al. Accuracy of clinical definitions of ventilator-associated pneumonia: comparison with autopsy findings. J Crit Care 2010; 25 (01) 62-68
    CrossrefPubMedGoogle Scholar
  • 39 Klompas M. Interobserver variability in ventilator-associated pneumonia surveillance. Am J Infect Control 2010; 38 (03) 237-239
    CrossrefPubMedGoogle Scholar
  • 40 Kerlin MP, Trick WE, Anderson DJ. , et al. Interrater reliability of surveillance for ventilator-associated events and pneumonia. Infect Control Hosp Epidemiol 2017; 38 (02) 172-178
    CrossrefPubMedGoogle Scholar
  • 41 Schurink CA, Van Nieuwenhoven CA, Jacobs JA. , et al. Clinical pulmonary infection score for ventilator-associated pneumonia: accuracy and inter-observer variability. Intensive Care Med 2004; 30 (02) 217-224
    CrossrefPubMedGoogle Scholar
  • 42 Klein Klouwenberg PM, Ong DS, Bos LD. , et al. Interobserver agreement of Centers for Disease Control and Prevention criteria for classifying infections in critically ill patients. Crit Care Med 2013; 41 (10) 2373-2378
    CrossrefPubMedGoogle Scholar
  • 43 Klompas M. The paradox of ventilator-associated pneumonia prevention measures. Crit Care 2009; 13 (05) 315
    CrossrefPubMedGoogle Scholar
  • 44 Kalil AC, Metersky ML, Klompas M. , et al. Management of adults with hospital-acquired and ventilator-associated pneumonia: 2016 Clinical Practice Guidelines by the Infectious Diseases Society of America and the American Thoracic Society. Clin Infect Dis 2016; 63 (05) e61-e111
    CrossrefPubMedGoogle Scholar
  • 45 Postma DF, Sankatsing SU, Thijsen SF, Endeman H. Effects of chlorhexidine oral decontamination on respiratory colonization during mechanical ventilation in intensive care unit patients. Infect Control Hosp Epidemiol 2012; 33 (05) 527-530
    CrossrefPubMedGoogle Scholar
  • 46 Klompas M. Prevention of ventilator-associated pneumonia. Expert Rev Anti Infect Ther 2010; 8 (07) 791-800
    CrossrefPubMedGoogle Scholar
  • 47 Bonten MJ. Healthcare epidemiology: ventilator-associated pneumonia: preventing the inevitable. Clin Infect Dis 2011; 52 (01) 115-121
    CrossrefPubMedGoogle Scholar
  • 48 Bouadma L, Wolff M, Lucet JC. Ventilator-associated pneumonia and its prevention. Curr Opin Infect Dis 2012; 25 (04) 395-404
    CrossrefPubMedGoogle Scholar
  • 49 Klompas M, Speck K, Howell MD, Greene LR, Berenholtz SM. Reappraisal of routine oral care with chlorhexidine gluconate for patients receiving mechanical ventilation: systematic review and meta-analysis. JAMA Intern Med 2014; 174 (05) 751-761
    CrossrefPubMedGoogle Scholar
  • 50 Bopp M, Darby M, Loftin KC, Broscious S. Effects of daily oral care with 0.12% chlorhexidine gluconate and a standard oral care protocol on the development of nosocomial pneumonia in intubated patients: a pilot study. J Dent Hyg 2006; 80 (03) 9
    PubMedGoogle Scholar
  • 51 Jafari S, Ranjbar H, Kamrani F. , et al. Effects of chlorhexidine and normal saline on plaque formation in ICU patients: a comparative study. J Nurs Midwifery 2007; 17 (56) 36-43
    PubMedGoogle Scholar
  • 52 Tantipong H, Morkchareonpong C, Jaiyindee S, Thamlikitkul V. Randomized controlled trial and meta-analysis of oral decontamination with 2% chlorhexidine solution for the prevention of ventilator-associated pneumonia. Infect Control Hosp Epidemiol 2008; 29 (02) 131-136
    CrossrefPubMedGoogle Scholar
  • 53 Panchabhai TS, Dangayach NS, Krishnan A, Kothari VM, Karnad DR. Oropharyngeal cleansing with 0.2% chlorhexidine for prevention of nosocomial pneumonia in critically ill patients: an open-label randomized trial with 0.01% potassium permanganate as control. Chest 2009; 135 (05) 1150-1156
    CrossrefPubMedGoogle Scholar
  • 54 Berry AM, Davidson PM, Masters J, Rolls K, Ollerton R. Effects of three approaches to standardized oral hygiene to reduce bacterial colonization and ventilator associated pneumonia in mechanically ventilated patients: a randomised control trial. Int J Nurs Stud 2011; 48 (06) 681-688
    CrossrefPubMedGoogle Scholar
  • 55 Macnaughton PD, Bailey J, Donlin N. , et al. A randomised controlled trial assessing the efficacy of oral chlorhexidine in ventilated patients. Intensive Care Med 2004; 30: S12
    PubMedGoogle Scholar
  • 56 Fourrier F, Dubois D, Pronnier P. , et al; PIRAD Study Group. Effect of gingival and dental plaque antiseptic decontamination on nosocomial infections acquired in the intensive care unit: a double-blind placebo-controlled multicenter study. Crit Care Med 2005; 33 (08) 1728-1735
    CrossrefPubMedGoogle Scholar
  • 57 Koeman M, van der Ven AJ, Hak E. , et al. Oral decontamination with chlorhexidine reduces the incidence of ventilator-associated pneumonia. Am J Respir Crit Care Med 2006; 173 (12) 1348-1355
    CrossrefPubMedGoogle Scholar
  • 58 Bellissimo-Rodrigues F, Bellissimo-Rodrigues WT, Viana JM. , et al. Effectiveness of oral rinse with chlorhexidine in preventing nosocomial respiratory tract infections among intensive care unit patients. Infect Control Hosp Epidemiol 2009; 30 (10) 952-958
    CrossrefPubMedGoogle Scholar
  • 59 Scannapieco FA, Yu J, Raghavendran K. , et al. A randomized trial of chlorhexidine gluconate on oral bacterial pathogens in mechanically ventilated patients. Crit Care 2009; 13 (04) R117
    CrossrefPubMedGoogle Scholar
  • 60 Meinberg MC, Cheade MdeF, Miranda AL, Fachini MM, Lobo SM. The use of 2% chlorhexidine gel and toothbrushing for oral hygiene of patients receiving mechanical ventilation: effects on ventilator-associated pneumonia [in Portuguese]. Rev Bras Ter Intensiva 2012; 24 (04) 369-374
    CrossrefPubMedGoogle Scholar
  • 61 Price R, MacLennan G, Glen J. ; SuDDICU Collaboration. Selective digestive or oropharyngeal decontamination and topical oropharyngeal chlorhexidine for prevention of death in general intensive care: systematic review and network meta-analysis. BMJ 2014; 348: g2197
    CrossrefPubMedGoogle Scholar
  • 62 Munro CL, Grap MJ, Jones DJ, McClish DK, Sessler CN. Chlorhexidine, toothbrushing, and preventing ventilator-associated pneumonia in critically ill adults. Am J Crit Care 2009; 18 (05) 428-437 , quiz 438
    CrossrefPubMedGoogle Scholar
  • 63 Cabov T, Macan D, Husedzinović I. , et al. The impact of oral health and 0.2% chlorhexidine oral gel on the prevalence of nosocomial infections in surgical intensive-care patients: a randomized placebo-controlled study. Wien Klin Wochenschr 2010; 122 (13-14): 397-404
    CrossrefPubMedGoogle Scholar
  • 64 Klompas M, Li L, Kleinman K, Szumita PM, Massaro AF. Associations between ventilator bundle components and outcomes. JAMA Intern Med 2016; 176 (09) 1277-1283
    CrossrefPubMedGoogle Scholar
  • 65 Jácomo AD, Carmona F, Matsuno AK, Manso PH, Carlotti AP. Effect of oral hygiene with 0.12% chlorhexidine gluconate on the incidence of nosocomial pneumonia in children undergoing cardiac surgery. Infect Control Hosp Epidemiol 2011; 32 (06) 591-596
    CrossrefPubMedGoogle Scholar
  • 66 Kusahara DM, Peterlini MA, Pedreira ML. Oral care with 0.12% chlorhexidine for the prevention of ventilator-associated pneumonia in critically ill children: randomised, controlled and double blind trial. Int J Nurs Stud 2012; 49 (11) 1354-1363
    CrossrefPubMedGoogle Scholar
  • 67 Sebastian MR, Lodha R, Kapil A, Kabra SK. Oral mucosal decontamination with chlorhexidine for the prevention of ventilator-associated pneumonia in children - a randomized, controlled trial. Pediatr Crit Care Med 2012; 13 (05) e305-e310
    CrossrefPubMedGoogle Scholar
  • 68 Hirata K, Kurokawa A. Chlorhexidine gluconate ingestion resulting in fatal respiratory distress syndrome. Vet Hum Toxicol 2002; 44 (02) 89-91
    PubMedGoogle Scholar
  • 69 Kempen PM. A tale of silent aspiration: are guidelines good for every patient?. Anesth Analg 2015; 121 (03) 829-831
    CrossrefPubMedGoogle Scholar
  • 70 Orito K, Hashida M, Hirata K, Kurokawa A, Shirai M, Akahori F. Effects of single intratracheal exposure to chlorhexidine gluconate on the rat lung. Drug Chem Toxicol 2006; 29 (01) 1-9
    CrossrefPubMedGoogle Scholar
  • 71 Xue Y, Zhang S, Yang Y. , et al. Acute pulmonary toxic effects of chlorhexidine (CHX) following an intratracheal instillation in rats. Hum Exp Toxicol 2011; 30 (11) 1795-1803
    CrossrefPubMedGoogle Scholar
  • 72 Massano G, Ciocatto E, Rosabianca C, Vercelli D, Actis GC, Verme G. Striking aminotransferase rise after chlorhexidine self-poisoning. Lancet 1982; 1 (8266): 289
    PubMedGoogle Scholar
  • 73 Seguin P, Laviolle B, Dahyot-Fizelier C. , et al; Study of Povidone Iodine to Reduce Pulmonary Infection in Head Trauma and Cerebral Hemorrhage Patients (SPIRIT) ICU Study Group; AtlanRéa Group. Effect of oropharyngeal povidone-iodine preventive oral care on ventilator-associated pneumonia in severely brain-injured or cerebral hemorrhage patients: a multicenter, randomized controlled trial. Crit Care Med 2014; 42 (01) 1-8
    CrossrefPubMedGoogle Scholar
  • 74 Plantinga NL, Wittekamp BH, Leleu K. , et al. Oral mucosal adverse events with chlorhexidine 2% mouthwash in ICU. Intensive Care Med 2016; 42 (04) 620-621
    CrossrefPubMedGoogle Scholar
  • 75 Branch-Elliman W, Wright SB, Gillis JM, Howell MD. Estimated nursing workload for the implementation of ventilator bundles. BMJ Qual Saf 2013; 22 (04) 357-361
    CrossrefPubMedGoogle Scholar
  • 76 Kress JP, Pohlman AS, O'Connor MF, Hall JB. Daily interruption of sedative infusions in critically ill patients undergoing mechanical ventilation. N Engl J Med 2000; 342 (20) 1471-1477
    CrossrefPubMedGoogle Scholar
  • 77 Girard TD, Kress JP, Fuchs BD. , et al. Efficacy and safety of a paired sedation and ventilator weaning protocol for mechanically ventilated patients in intensive care (Awakening and Breathing Controlled trial): a randomised controlled trial. Lancet 2008; 371 (9607): 126-134
    CrossrefPubMedGoogle Scholar
  • 78 Schweickert WD, Pohlman MC, Pohlman AS. , et al. Early physical and occupational therapy in mechanically ventilated, critically ill patients: a randomised controlled trial. Lancet 2009; 373 (9678): 1874-1882
    CrossrefPubMedGoogle Scholar
  • 79 Balas MC, Vasilevskis EE, Olsen KM. , et al. Effectiveness and safety of the awakening and breathing coordination, delirium monitoring/management, and early exercise/mobility bundle. Crit Care Med 2014; 42 (05) 1024-1036
    CrossrefPubMedGoogle Scholar
  • 80 Klompas M, Anderson D, Trick W. , et al. The preventability of ventilator-associated events. The CDC Prevention Epicenters Wake Up and Breathe Collaborative. Am J Respir Crit Care Med 2015; 191 (03) 292-301
    CrossrefPubMedGoogle Scholar
  • 81 Klompas M. Potential strategies to prevent ventilator-associated events. Am J Respir Crit Care Med 2015; 192 (12) 1420-1430
    CrossrefPubMedGoogle Scholar
  • 82 Mori H, Hirasawa H, Oda S, Shiga H, Matsuda K, Nakamura M. Oral care reduces incidence of ventilator-associated pneumonia in ICU populations. Intensive Care Med 2006; 32 (02) 230-236
    CrossrefPubMedGoogle Scholar
  • 83 Alhazzani W, Smith O, Muscedere J, Medd J, Cook D. Toothbrushing for critically ill mechanically ventilated patients: a systematic review and meta-analysis of randomized trials evaluating ventilator-associated pneumonia. Crit Care Med 2013; 41 (02) 646-655
    CrossrefPubMedGoogle Scholar
  • 84 de Lacerda Vidal CF, Vidal AK, Monteiro Jr JG. , et al. Impact of oral hygiene involving toothbrushing versus chlorhexidine in the prevention of ventilator-associated pneumonia: a randomized study. BMC Infect Dis 2017; 17 (01) 112
    CrossrefPubMedGoogle Scholar
  • 85 Klompas M, Branson R, Eichenwald EC. , et al; Society for Healthcare Epidemiology of America (SHEA). Strategies to prevent ventilator-associated pneumonia in acute care hospitals: 2014 update. Infect Control Hosp Epidemiol 2014; 35 (08) 915-936
    CrossrefPubMedGoogle Scholar
  • 86 Hellyer TP, Ewan V, Wilson P. , et al. The Intensive Care Society recommended bundle of intereventions for the prevention of ventilator-associated pneumonia. Journal of the Intensive Care Society 2016; 17: 238-243
    CrossrefPubMedGoogle Scholar
  • 87 de Smet AM, Kluytmans JA, Cooper BS. , et al. Decontamination of the digestive tract and oropharynx in ICU patients. N Engl J Med 2009; 360 (01) 20-31
    CrossrefPubMedGoogle Scholar
  • 88 de Smet AM, Kluytmans JA, Blok HE. , et al. Selective digestive tract decontamination and selective oropharyngeal decontamination and antibiotic resistance in patients in intensive-care units: an open-label, clustered group-randomised, crossover study. Lancet Infect Dis 2011; 11 (05) 372-380
    CrossrefPubMedGoogle Scholar