Biofilm formation on three different endotracheal tubes: a prospective clinical trial

Hulda R Thorarinsdottir, Thomas Kander, Anna Holmberg, Sarunas Petronis, Bengt Klarin, Hulda R Thorarinsdottir, Thomas Kander, Anna Holmberg, Sarunas Petronis, Bengt Klarin

Abstract

Background: Biofilm formation on endotracheal tubes (ETTs) is an early and frequent event in mechanically ventilated patients. The biofilm is believed to act as a reservoir for infecting microorganisms and thereby contribute to development and relapses of ventilator-associated pneumonia (VAP). Once a biofilm has formed on an ETT surface, it is difficult to eradicate. This clinical study aimed to compare biofilm formation on three widely used ETTs with different surface properties and to explore factors potentially predictive of biofilm formation.

Methods: We compared the grade of biofilm formation on ETTs made of uncoated polyvinyl chloride (PVC), silicone-coated PVC, and PVC coated with noble metals after > 24 h of mechanical ventilation in critically ill patients. The comparison was based on scanning electron microscopy of ETT surfaces, biofilm grading, surveillance and biofilm cultures, and occurrence of VAP.

Results: High-grade (score ≥ 7) biofilm formation on the ETTs was associated with development of VAP (OR 4.17 [95% CI 1.14-15.3], p = 0.031). Compared to uncoated PVC ETTs, the silicone-coated and noble-metal-coated PVC ETTs were independently associated with reduced high-grade biofilm formation (OR 0.18 [95% CI 0.06-0.59], p = 0.005, and OR 0.34 [95% CI 0.13-0.93], p = 0.036, respectively). No significant difference was observed between silicon-coated ETTs and noble-metal-coated ETTs (OR 0.54 [95% CI 0.17-1.65], p = 0.278). In 60% of the oropharyngeal cultures and 58% of the endotracheal cultures collected at intubation, the same microorganism was found in the ETT biofilm at extubation. In patients who developed VAP, the causative microbe remained in the biofilm in 56% of cases, despite appropriate antibiotic therapy. High-grade biofilm formation on ETTs was not predicted by either colonization with common VAP pathogens in surveillance cultures or duration of invasive ventilation.

Conclusion: High-grade biofilm formation on ETTs was associated with development of VAP. Compared to the uncoated PVC ETTs, the silicone-coated and noble-metal-coated PVC ETTs were independently associated with reduced high-grade biofilm formation. Further research on methods to prevent, monitor, and manage biofilm occurrence is needed.

Trial registration: ClinicalTrials.gov NCT02284438 . Retrospectively registered on 21 October 2014.

Keywords: Alloys; Biofilm; Critical illness; Intratracheal; Intubation; Pneumonia; Polyvinyl chloride; Silicones; Ventilator-associated.

Conflict of interest statement

This study was performed as part of a national project entitled Innovation against Infection (in Swedish: Innovation Mot Infektion [IMI]) and was conducted in collaboration with Skåne University Hospital, Lund, and RISE Research Institutes of Sweden, Borås, Sweden. The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Flow chart showing inclusion of patients in the study. “No consent” refers to cases in which the patient did not give consent to participate after the ICU stay. Endotracheal tube materials: PVC uncoated polyvinyl chloride; SC silicon-coated PVC; NbMC noble-metal-coated PVC
Fig. 2
Fig. 2
Scanning electron microscopy of biofilm formation on the surface of endotracheal tubes. a Typical low-grade (score < 4) biofilm formation. b Typical high-grade (score ≥ 7) biofilm formation (low magnification). c Colonies of microorganisms embedded in biofilm matrix (high magnification). d Scrape marks on the surface of an endotracheal tube probably caused by use of a suction catheter

References

    1. Melsen WG, Rovers MM, Koeman M, Bonten MJM. Estimating the attributable mortality of ventilator-associated pneumonia from randomized prevention studies. Crit Care Med. 2011;39:2736–2742.
    1. Kollef MH, Hamilton CW, Ernst FR. Economic impact of ventilator-associated pneumonia in a large matched cohort. Infect Control Hosp Epidemiol. 2012;33:250–256.
    1. Muscedere JG, Day A, Heyland DK. Mortality, attributable mortality, and clinical events as end points for clinical trials of ventilator-associated pneumonia and hospital-acquired pneumonia. Clin Infect Dis. 2010;51:120–125.
    1. Melsen WG, Rovers MM, Groenwold RHH, Bergmans DCJJ, Camus C, Bauer TT, et al. Attributable mortality of ventilator-associated pneumonia: a meta-analysis of individual patient data from randomised prevention studies. Lancet Infect Dis. 2013;13:665–671.
    1. Morris AC, Hay AW, Swann DG, Everingham K, McCulloch C, McNulty J, et al. Reducing ventilator-associated pneumonia in intensive care: impact of implementing a care bundle. Crit Care Med. 2011;39:2218–2224.
    1. Haas CF, Eakin RM, Konkle MA, Blank R. Endotracheal tubes: old and new. Respir Care. 2014;59:933–935.
    1. Wang Y, Eldridge N, Metersky ML, Verzier NR, Meehan TP, Pandolfi MM, et al. National trends in patient safety for four common conditions, 2005-2011. N Engl J Med. 2014;370:341–351.
    1. Inglis TJ, Millar MR, Jones JG, Robinson DA. Tracheal tube biofilm as a source of bacterial colonization of the lung. J Clin Microbiol. 1989;27:2014–2018.
    1. Sottile FD, Marrie TJ, Prough DS, Hobgood CD, Gower DJ, Webb LX, et al. Nosocomial pulmonary infection: possible etiologic significance of bacterial adhesion to endotracheal tubes. Crit Care Med. 1986;14:265–270.
    1. Adair CG, Gorman SP, Feron BM, Byers LM, Jones DS, Goldsmith CE, et al. Implications of endotracheal tube biofilm for ventilator-associated pneumonia. Intensive Care Med. 1999;25:1072–1076.
    1. Wilson A, Gray D, Karakiozis J, Thomas J. Advanced endotracheal tube biofilm stage, not duration of intubation, is related to pneumonia. J Trauma Acute Care Surg. 2012;72:916–923.
    1. Gil-Perotin S, Ramirez P, Marti V, Sahuquillo JM, Gonzalez E, Calleja I, et al. Implications of endotracheal tube biofilm in ventilator-associated pneumonia response: a state of concept. Crit Care. 2012;16:R93.
    1. Feldman C, Kassel M, Cantrell J, Kaka S, Morar R, Mahomed AG, et al. The presence and sequence of endotracheal tube colonization in patients undergoing mechanical ventilation. Eur Respir J. 1999;13:546–551.
    1. Sands KM, Wilson MJ, Lewis MAO, Wise MP, Palmer N, Hayes AJ, et al. Respiratory pathogen colonization of dental plaque, the lower airways, and endotracheal tube biofilms during mechanical ventilation. J Crit Care. 2017;37:30–37.
    1. Tokmaji G, Vermeulen H, Müller MCA, Kwakman PHS, Schultz MJ, Zaat SAJ. Silver-coated endotracheal tubes for prevention of ventilator-associated pneumonia in critically ill patients. Cochrane Database Syst Rev. 2015;12(8):CD009201.
    1. Karchmer TB, Giannetta ET, Muto CA, Strain BA, Farr BM. A randomized crossover study of silver-coated urinary catheters in hospitalized patients. Arch Intern Med. 2000;160:3294–3298.
    1. Vandenbroucke JP, von Elm E, Altman DG, Gøtzsche PC, Mulrow CD, Pocock SJ, et al. Strengthening the Reporting of Observational Studies in Epidemiology (STROBE): explanation and elaboration. Int J Surg. 2014;12:1500–1524.
    1. Tranberg A, Thorarinsdottir HR, Holmberg A, Schött U, Klarin B. Proton pump inhibitor medication is associated with colonisation of gut flora in the oropharynx. Acta Anaesthesiol Scand. 2018;62:791–800.
    1. Torres A, Martos A, De la Bellacasa JP, Ferrer M, El-Ebiary M, Gonzalez J, et al. Specificity of endotracheal aspiration, protected specimen brush, and bronchoalveolar lavage in mechanically ventilated patients. Am Rev Respir Dis. 1993;147:952–957.
    1. Visscher S, Schurink CAM, Melsen WG, Lucas PJF, Bonten MJM. Effects of systemic antibiotic therapy on bacterial persistence in the respiratory tract of mechanically ventilated patigents. Intensive Care Med. 2008;34:692–699.
    1. Lopez-Lopez G, Pascual A, Perea EJ. Effect of plastic catheter material on bacterial adherence and viability. J Med Microbiol. 1991;34:349–353.
    1. Hawser SP, Douglas LJ. Biofilm formation by Candida species on the surface of catheter materials in vitro. Infect Immun. 1994;62:915–921.
    1. Zur KB, Mandell DL, Gordon RE, Holzman I, Rothschild MA. Electron microscopic analysis of biofilm on endotracheal tubes removed from intubated neonates. Otolaryngol Head Neck Surg. 2004;130:407–414.
    1. Bayazian G, Sayyahfar S, Safdarian M, Kalantari F. Is there any association between adenoid biofilm and upper airway infections in pediatric patients? Turk Pediatr Ars. 2018;53:71–77.
    1. Chole RA, Faddis BT. Anatomical evidence of microbial biofilms in tonsillar tissues: a possible mechanism to explain chronicity. Arch Otolaryngol. 2003;129:634–636.
    1. Kaplan JB. Biofilm dispersal: mechanisms, clinical implications, and potential therapeutic uses. J Dent Res. 2010;89:205–218.
    1. Diaz-Blanco J, Clawson RC, Roberson SM, Sanders CB, Pramanik AK, Herbst JJ. Electron microscopic evaluation of bacterial adherence to polyvinyl chloride endotracheal tubes used in neonates. Crit Care Med. 1989;17:1335–1340.
    1. Kurmoo Y, Hook AL, Harvey D, Dubern J-F, Williams P, Morgan SP, et al. Real time monitoring of biofilm formation on coated medical devices for the reduction and interception of bacterial infections. Biomater Sci. 2020;8:1464–1477.
    1. Berra L, Coppadoro A, Bittner EA, Kolobow T, Laquerriere P, Pohlmann JR, et al. A clinical assessment of the Mucus Shaver: a device to keep the endotracheal tube free from secretions. Crit Care Med. 2012;40:119–124.
    1. Zangirolami AC, Inada NM, Bagnato VS, Blanco KC. Biofilm destruction on endotracheal tubes by photodynamic inactivation. Infect Disord Drug Target. 2018;18:218–223.
    1. Torres A, Gatell JM, Aznar E, el-Ebiary M, Puig de la Bellacasa J, González J, et al. Re-intubation increases the risk of nosocomial pneumonia in patients needing mechanical ventilation. Am J Respir Crit Care Med. 1995;152:137–141.
    1. Hall-Stoodley L, Costerton JW, Stoodley P. Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol. 2004;2:95–108.
    1. Rosan B, Lamont RJ. Dental plaque formation. Microbes Infect. 2000;13:1599–1607.
    1. Johanson WG, Pierce AK, Sanford JP. Changing pharyngeal bacterial flora of hospitalized patients. Emergence of gram-negative bacilli. N Engl J Med. 1969;281:1137–1140.
    1. Estes RJ, Meduri GU. The pathogenesis of ventilator-associated pneumonia: I. mechanisms of bacterial transcolonization and airway inoculation. Intensive Care Med. 1995;21:365–383.
    1. Vandecandelaere I, Matthijs N, van Nieuwerburgh F, Deforce D, Vosters P, de Bus L, et al. Assessment of microbial diversity in biofilms recovered from endotracheal tubes using culture dependent and independent approaches. PLoS One. 2012;7:e38401.
    1. Vandecandelaere I, Coenye T. Microbial composition and antibiotic resistance of biofilms recovered from endotracheal tubes of mechanically ventilated patients. Adv Exp Med Biol. 2015;830:137–155.
    1. Haghighi F, Mohammadi SR, Mohammadi P, Eskandari M, Hosseinkhani S. The evaluation of Candida albicans biofilms formation on silicone catheter, PVC and glass coated with titanium dioxide nanoparticles by XTT method and ATPase assay. Bratisl Lek Listy. 2012;113:707–711.
    1. Teughels W, Van Assche N, Sliepen I, Quirynen M. Effect of material characteristics and/or surface topography on biofilm development. Clin Oral Implants Res. 2006;17:68–81.
    1. Bjorling G, Johansson D, Bergstrom L, Jalal S, Kohn I, Frostell C, et al. Tolerability and performance of BIP endotracheal tubes with noble metal alloy coating – a randomized clinical evaluation study. BMC Anesthesiol. 2015;15:174-z.
    1. Chung PHY, Wong CWY, Lai CKC, Siu HK, Tsang DNC, Yeung KY, et al. A prospective interventional study to examine the effect of a silver alloy and hydrogel-coated catheter on the incidence of catheter-associated urinary tract infection. Hong Kong Med J. 2017;23:239–245.
    1. Magnusson B, Kai-Larsen Y, Granlund P, Seiger Å, Lindbo L, Sanchez J, et al. Long-term use of noble metal alloy coated urinary catheters reduces recurrent CAUTI and decreases proinflammatory markers. Ther Adv Urol. 2019;11:1–13.
    1. Brosnahan J, Jull A, Tracy C. Types of urethral catheters for management of short-term voiding problems in hospitalised adults. Cochrane Database Syst Rev. 2004;(1):CD004013.
    1. Jones DS, Mcgovern JG, Woolfson AD, Gorrnan SP. Role of physiological conditions in the oropharynx on the adherence of respiratory bacterial isolates to endotracheal tube poly (viny1 chloride) Biomoteriols. 1997;18:503–510.

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