Comments
To the Editor:
The recently updated Cystic Fibrosis Foundation infection control guidelines advise people with cystic fibrosis (CF) to wear a surgical mask in healthcare settings to reduce the risk for transmission or acquisition of CF pathogens (1). A study from Liverpool, United Kingdom, demonstrated a threefold higher risk for death or lung transplantation in those infected with an epidemic Pseudomonas aeruginosa strain compared with those infected with environmentally acquired bacteria, highlighting the concern about transmission of epidemic strains in clinical care settings (2). The new recommendation for patients with CF to wear masks was supported by studies showing “infectious droplets in the air” of CF clinics. Cough aerosol particles smaller than 60 μm will evaporate to particles smaller than 5 μm before touching the ground, classically referred to as airborne droplet nuclei (3). Droplets are larger particles that do not stay in the air beyond 30 seconds. Both Burkholderia cepacia complex and P. aeruginosa have been isolated from patient room air samples (1, 4). It has been suggested that airborne dissemination may be the most important factor in patient-to-patient spread of epidemic strains of P. aeruginosa during CF center outbreaks, but this remains undetermined (4, 5). Also, for emerging mycobacterial infections in patients with CF, there are concerns about airborne transmission (1).
Surgical masks were originally developed to prevent droplet contamination of operating fields. Very little is known about their ability to prevent droplet nuclei generation. Some investigators suggest that droplet nuclei cannot be formed, as the originator droplets will be impacted on the mask (6). Others argue that small infectious particles originating from the lung, rather than impacting on an obstructing mask, will follow airstreams flowing around the edges of relatively loose fitting surgical masks (7). Both arguments relate directly to Newton’s laws of motion: Newton’s first law states objects in motion will continue to move in the same direction unless acted on by an unbalanced force. Therefore, large particles will impact on an obstructing object (a mask), whereas small particles do not need much force (F = ma; Newton’s second law) to change direction and might be able to follow airstreams around the mask’s edges.
We aimed to determine whether surgical masks were effective in reducing the airborne spread of P. aeruginosa by people with CF when coughing.
We recruited patients with CF for whom our repository laboratory received a P. aeruginosa isolate both in 2012 and 2013. We used a modification (see Figure E1 in the online supplement) of our previously developed controlled human aerosol model (8) to evaluate the effect of surgical masks (Kimberly-Clark Type 1 procedure masks; Kimberly-Clark Corporation, Dallas, TX) on the viable P. aeruginosa cough aerosol load. Because we were primarily interested in airborne transmission, we only took delayed aerosol samples collected 1 minute after coughing. Statistical comparisons were performed using generalized linear mixed models. (See online supplement for more detailed methods.)
The Children's and Women's Health Centre Research Ethics Board approved the study, and written consent was obtained from all subjects.
Eleven participants aged 16–77 years were evaluated in 22 cough sessions. Sixteen otherwise eligible people declined participation. Table E1 lists clinical characteristics of study participants.
Aerosolized viable P. aeruginosa were recovered after 12 sessions from six participants (Figure 1).
Figure 1. Effect of surgical masks on the airborne Pseudomonas aeruginosa load originating from cough aerosols. The dashed lines represent 12 cough sessions from six different subjects. The solid line at the bottom of the graph represents 10 cough sessions from five different subjects in whom no viable P. aeruginosa from cough aerosols could be sampled in the control or in the mask cylinder.
[More] [Minimize]Among those producing infected aerosol particles (6/11; 55%), the airborne Pseudomonas load was reduced by 88% when wearing a surgical mask compared with no mask (95% confidence interval [CI], 81–96%; P = 0.03). The protective effect of surgical masks was 86% (95% CI, 74–99%) when stratifying only for aerosol particles smaller than 4.7 μm (P = 0.03). There was no significant difference related to the session order (control vs. intervention; data not shown). A Pearson correlation coefficient between 0.98 and 1.00 demonstrated an excellent fit for the statistical models.
The controlled human aerosol model used in our study produced relatively precise and repeatable results despite a small sample size. Among patients with CF colonized with P. aeruginosa and producing infectious aerosol particles (55%), we demonstrated a greater than 80% reduction in infectious aerosol particle production when wearing a surgical mask while coughing.
Three previous studies examined the effect of surgical masks on the dispersal of airborne viable microorganisms from patients. Milton asked patients with influenza to cough into a cone and sampled their aerosols with slit impactors (9). The influenza copy number in the 5 μm or less fraction (the airborne droplet nuclei) was reduced by 64% (95% CI, 33–81%) in mask sessions compared with preceding control sessions. Not surprisingly, the copy number in the greater than 5 μm fraction (the droplets) was reduced to a greater extent (96%; 95% CI, 71–99%). Dharmadhikari monitored tuberculosis (TB) skin test conversion in guinea pigs housed in cages receiving exhaust air from a TB treatment facility in eMalahleni, South Africa (10). The study reported a 56% (95% CI, 33–71%) reduction in infectious aerosol production, as measured by fewer guinea pigs becoming infected, when patients with TB wore surgical masks. Zuckerman reported 8% air contamination when sampling exam rooms with cascade impactors placed 3 feet from patients with CF (11). In a follow-up study at 6 feet, few samples were positive, both for occupants with (2/149) or without (1/154) masks (12). The Cystic Fibrosis Foundation does not recommend the wearing of masks inside (well-ventilated) exam rooms (1).
Our study has several limitations. First, aerosols from strong coughs may impact more effectively onto surgical masks (F = ma), and the strong artificial coughs produced during the study could have led to an overestimation of the protective effect. In real life, patients would not be coughing as frequently and might cover their coughs (e.g., cough in their hand or elbow). Second, although we demonstrated that smoke particles below 10 μm were homogenously mixed before sampling (Figure E2), this is not a guarantee that the same- sized particles from real cough aerosols were equally well mixed. Third, although our study demonstrated an important reduction in P. aeruginosa–containing airborne particles, we do not know the contagiousness of airborne P. aeruginosa. It would, however, seem reasonable to assume that masks are at least as effective in reducing droplet spread of P. aeruginosa as they are against airborne spread (9). Last, we only studied the outward protective effect of masks. The inward protection of surgical masks (to protect the wearer) has yet to be established (13).
Despite these study limitations, we demonstrated that surgical masks were effective in reducing the airborne load of P. aeruginosa when colonized individuals with CF cough. Our data provide evidence for the new Cystic Fibrosis Foundation guideline to wear surgical masks in healthcare settings.
The authors thank their colleagues at the Centre for Understanding and Preventing Infection in Children (University of British Columbia [UBC]) and the microbiology laboratories of Children's and Women's Health Centre of BC (UBC) and St. Paul’s Hospital (UBC) for their help and support: Rebecca Hickman, Trevor Hird, Maureen Campbell, Carolyn Smith, Suk Dhaliwal, and Sylvie Champagne. We also thank Maggie McIlwaine (Pediatric Physiotherapy, UBC) Brigette Wilkins (Physiotherapy, UBC), and Joanne Laviolette (CF clinic, UBC) for helping with the recruitment process. We are grateful for expert advice from Julie Bettinger (Vaccine Evaluation Center, UBC), Karen Bartlett (School of Population & Public Health, UBC), and Amir A. Aliabadi (AAA Scientists).
| 1. | Saiman L, Siegel JD, LiPuma JJ, Brown RF, Bryson EA, Chambers MJ, Downer VS, Fliege J, Hazle LA, Jain M, et al.; Cystic Fibrosis Foundation; Society for Healthcare Epidemiology of America. Infection prevention and control guideline for cystic fibrosis: 2013 update. Infect Control Hosp Epidemiol 2014;35:S1–S67. |
| 2. | Aaron SD, Vandemheen KL, Ramotar K, Giesbrecht-Lewis T, Tullis E, Freitag A, Paterson N, Jackson M, Lougheed MD, Dowson C, et al. Infection with transmissible strains of Pseudomonas aeruginosa and clinical outcomes in adults with cystic fibrosis. JAMA 2010;304:2145–2153. |
| 3. | Xie X, Li Y, Chwang AT, Ho PL, Seto WH. How far droplets can move in indoor environments--revisiting the Wells evaporation-falling curve. Indoor Air 2007;17:211–225. |
| 4. | Jones AM, Govan JR, Doherty CJ, Dodd ME, Isalska BJ, Stanbridge TN, Webb AK. Identification of airborne dissemination of epidemic multiresistant strains of Pseudomonas aeruginosa at a CF centre during a cross infection outbreak. Thorax 2003;58:525–527. |
| 5. | Wainwright CE, France MW, O’Rourke P, Anuj S, Kidd TJ, Nissen MD, Sloots TP, Coulter C, Ristovski Z, Hargreaves M, et al. Cough-generated aerosols of Pseudomonas aeruginosa and other Gram-negative bacteria from patients with cystic fibrosis. Thorax 2009;64:926–931. |
| 6. | Riley RL. Airborne infection. Am J Med 1974;57:466–475. |
| 7. | Tang JW, Liebner TJ, Craven BA, Settles GS. A schlieren optical study of the human cough with and without wearing masks for aerosol infection control. J R Soc Interface 2009;6:S727–S736. |
| 8. | Vanden Driessche K, Marais BJ, Wattenberg M, Magis-Escurra C, Reijers M, Tuinman IL, Boeree MJ, van Soolingen D, de Groot R, Cotton MF. The Cough Cylinder: a tool to study measures against airborne spread of (myco-) bacteria. Int J Tuberc Lung Dis 2013;17:46–53. |
| 9. | Milton DK, Fabian MP, Cowling BJ, Grantham ML, McDevitt JJ. Influenza virus aerosols in human exhaled breath: particle size, culturability, and effect of surgical masks. PLoS Pathog 2013;9:e1003205. |
| 10. | Dharmadhikari AS, Mphahlele M, Stoltz A, Venter K, Mathebula R, Masotla T, Lubbe W, Pagano M, First M, Jensen PA, et al. Surgical face masks worn by patients with multidrug-resistant tuberculosis: impact on infectivity of air on a hospital ward. Am J Respir Crit Care Med 2012;185:1104–1109. |
| 11. | Zuckerman JB, Zuaro DE, Prato BS, Ruoff KL, Sawicki RW, Quinton HB, Saiman L; Infection Control Study Group. Bacterial contamination of cystic fibrosis clinics. J Cyst Fibros 2009;8:186–192. |
| 12. | Zuckerman JB, Clock SA, Prato BS, McDevitt JJ, Zhou JJ, Leclair LW, Lucas FL, Saiman L. Air contamination with bacteria in cystic fibrosis clinics: implications for prevention strategies. Am J Respir Crit Care Med 2015;191:598–601. |
| 13. | MacIntyre CR, Chughtai AA. Facemasks for the prevention of infection in healthcare and community settings. BMJ 2015;350:h694. |
K.V.D. is supported by an European Society for Paediatric Infectious Diseases Fellowship Award for this study.
Author Contributions: K.V.D., P.T., M.A.C., and B.S.Q. acquired the data (recruitment, cough studies, and/or microbiology work-up). K.V.D. and N.H. conducted and are responsible for the data analysis. K.V.D., M.F.C., R.d.G., and B.J.M. conceived and designed the study and helped obtain funding. K.V.D., N.H., and J.E.A.Z. drafted the manuscript. All authors revised the manuscript before submission. D.P.S. and J.E.A.Z. supervised the study.
This letter has an online supplement, which is accessible from this issue's table of contents at www.atsjournals.org
Author disclosures are available with the text of this letter at www.atsjournals.org.
