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Dispersal of Staphylococcus aureus Into the Air Associated With a Rhinovirus Infection

Published online by Cambridge University Press:  21 June 2016

Stefano Bassetti
Section on Infectious Diseases, Wake Forest University School of Medicine, Winston-Salem, North Carolina
Werner E. Bischoff
Section on Infectious Diseases, Wake Forest University School of Medicine, Winston-Salem, North Carolina
Mark Walter
Section on Infectious Diseases, Wake Forest University School of Medicine, Winston-Salem, North Carolina
Barbara A. Bassetti-Wyss
Section on Infectious Diseases, Wake Forest University School of Medicine, Winston-Salem, North Carolina
Lori Mason
Section on Infectious Diseases, Wake Forest University School of Medicine, Winston-Salem, North Carolina
Beth A. Reboussin
Section on Biostatistics, Wake Forest University School of Medicine, Winston-Salem, North Carolina
Ralph B. D'Agostino Jr
Section on Biostatistics, Wake Forest University School of Medicine, Winston-Salem, North Carolina
Jack M. Gwaltney Jr
Division of Epidemiology and Virology, University of Virginia Health Sciences Center, Charlottesville, Virginia
Michael A. Pfaller
Medical Microbiology Division, The University of Iowa Hospitals and Clinics, Iowa City, Iowa
Robert J. Sherertz*
Section on Infectious Diseases, Wake Forest University School of Medicine, Winston-Salem, North Carolina
Section on Infectious Diseases, Wake Forest University School of Medicine, Medical Center Boulevard, Winston-Salem, NC



To determine whether healthy adult nasal carriers of Staphylococcus aureus can disperse S. aureus into the air after rhinovirus infection.


We investigated the “cloud” phenomenon among adult nasal carriers of S. aureus experimentally infected with a rhinovirus. Eleven volunteers were studied for 16 days in an airtight chamber wearing street clothes, sterile garb, or sterile garb plus surgical mask; rhinovirus inoculation occurred on day 2. Daily quantitative air, nasal, and skin cultures for S. aureus; cold symptom assessment; and nasal rhinovirus cultures were performed.


Wake Forest University School of Medicine, Winston-Salem, North Carolina.


Wake Forest University undergraduate or graduate students who had persistent nasal carriage of S. aureus for 4 or 8 weeks.


After rhinovirus inoculation, dispersal of S. aureus into the air increased 2-fold with peak increases up to 34-fold. Independent predictors of S. aureus dispersal included the time period after rhinovirus infection and wearing street clothes (P < .05). Wearing barrier garb but not a mask decreased dispersal of S. aureus into the air (P < .05).


Virus-induced dispersal of S. aureus into the air may have an important role in the transmission of S. aureus and other bacteria.

Original Articles
Copyright © The Society for Healthcare Epidemiology of America 2005

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1.Hospital Infections Program, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Public Health Service, U.S. Department of Health and Human Services. National Nosocomial Infections Surveillance (NNIS) system report: data summary from January 1990-May 1999, issued June 1999. Am J Infect Control 1999;27: 520532.CrossRefGoogle Scholar
2.John, JF Jr, Barg, NL. Staphylococcus aureus. In: Mayhall, CG, ed. Hospital Epidemiology and Infection Control, ed. 2. Philadelphia: Lippincott Williams & Wilkins; 1999:325345.Google Scholar
3.Pittet, D, Tarara, D, Wenzel, RP. Nosocomial bloodstream infection in critically ill patients: excess length of stay, extra costs, and attributable mortality. JAMA 1994;271:15981601.CrossRefGoogle ScholarPubMed
4.Kirkland, KB, Briggs, JP, Trivette, SL, Wilkinson, WE, Sexton, DJ. The impact of surgical-site infections in the 1990s: attributable mortality, excess length of hospitalization, and extra costs. Infect Control Hosp Epidemiol 1999;20:725730.CrossRefGoogle ScholarPubMed
5.Smith, TL, Pearson, ML, Wilcox, KR, et al.Emergence of vancomycin resistance in Staphylococcus aureus. N Engl J Med 1999;340:493501.CrossRefGoogle ScholarPubMed
6.Eichenwald, HF, Kotsevalov, O, Fasso, LA. The “cloud baby”: an example of bacterial-viral interaction. Am J Dis Child 1960;100:161173.Google Scholar
7.Sherertz, RJ, Reagan, DR, Hampton, KD, et al.A cloud adult: the Staphylococcus aureus-virus interaction revisited. Ann Intern Med 1996;124:539547.Google Scholar
8.Andersen, AA. New sampler for the collection, sizing, and enumeration of viable airborne particles. J Bacterial 1958;76:471484.Google Scholar
9.Jensen, PA, Todd, WF, Davis, GN, Scarpino, PV. Evaluation of eight bioaerosol samplers challenged with aerosols of free bacteria. American Industrial Hygiene Association Journal 1992;53:660667.Google Scholar
10.White, A, Hemmerly, T, Martin, MP, Knight, V. Studies on the origin of drug-resistant staphylococci in a mental hospital. Am J Med 1959;27:2639.Google Scholar
11.Stone, AA, Bovbjerg, DH, Neale, JM, et al.Development of common cold symptoms following experimental rhinovirus infection is related to prior stressful life events. Behav Med 1992;18:115120.Google Scholar
12.Harris, JM II, Gwaltney, JM Jr.Incubation periods of experimental rhinovirus infection and illness. Clin Infect Dis 1996;23:12871290.Google Scholar
13.Hollis, RJ, Bruce, JL, Fritschel, SJ, Pfaller, MA. Comparative evaluation of an automated ribotyping instrument versus pulsed-field gel electrophoresis for epidemiological investigation of clinical isolates of bacteria. Diagn Microbiol Infect Dis 1999;34:263268.Google Scholar
14.Tenover, FC, Arbeit, RD, Goering, RV, et al.Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 1995;33:22332239.Google Scholar
15.Bischoff, WE, Bassetti, S, Bassetti-Wyss, BA, et al.Airborne dispersal as a novel transmission route of coagulase-negative staphylococci: interaction between coagulase-negative staphylococci and rhinovirus infection. Infect Control Hosp Epidemiol 2004;25:504511.Google Scholar
16.Bethune, DW, Blowers, R, Parker, M, Pask, EADispersal of Staphylococcus aureus by patients and surgical staff. Lancet 1965;40:480483.CrossRefGoogle Scholar
17.Noble, WC. The dispersal of staphylococci in hospital wards. J Clin Pathol 1962;15:552558.Google Scholar
18.Gwaltney, JM. Rhinovirus. In: Mandeli, GL, Bennett, JE, Dolin, R, eds. Principles and Practice of Infectious Diseases. Philadelphia: Churchill Livingstone; 2000:19401948.Google Scholar
19.Hamre, D, Connelly, AP Jr, Procknow, JJ. Virologie studies of acute respiratory disease in young adults. Am J Epidemiol 1966;83:238249.Google Scholar
20.von Eiff, C, Becker, K, Machka, K, Stammer, H, Peters, G. Nasal carriage as a source of Staphylococcus aureus bacteremia. N Engl J Med 2001; 344:1116.CrossRefGoogle ScholarPubMed
21.Tanner, EI, Bullin, J, Bullin, CH, Gamble, DR. An outbreak of post-operative sepsis due to a staphylococcal disperser. Journal of Hygiene 1980;85:219225.Google Scholar
22.Belani, A, Sherertz, RJ, Sullivan, ML, Russell, BA, Reumen, PD. Outbreak of staphylococcal infection in two hospital nurseries traced to a single nasal carrier. Infect Control 1986;7:487490.Google Scholar
23.Boyce, JM, Opal, SM, Potter-Bynoe, G, Medeiros, AA. Spread of methicillin-resistant Staphylococcus aureus in a hospital after exposure to a health care worker with chronic sinusitis. Ann Intern Med 1993;17:496504.Google Scholar
24.Dunkle, LM, Naqvi, SH, McCallum, R, Lofgren, JP. Eradication of epidemic methicillin-gentamicin-resistant Staphylococcus aureus in an intensive care nursery. Am J Med 1981;70:455458.Google Scholar
25.Hedberg, K, Ristinen, TL, Soler, JT, et al.Outbreak of erythromycin-resistant staphylococcal conjunctivitis in a newborn nursery. Fed J Infect Dis 1990;9:268273.CrossRefGoogle Scholar
26.Coovadia, YM, Bhana, RH, Johnson, AP, Haffejee, I, Marples, RR. A laboratory-confirmed outbreak of rifampin-methicillin resistant Staphylococcus aureus (MRSA) in a newborn nursery. J Hosp Infect 1989;14:303312.Google Scholar
27.Dancer, SJ, Poston, SM, East, J, Simmons, NA, Noble, WC. An outbreak of pemphigus neonatorum. J Infect 1990;20:7382.Google Scholar
28.Gaynes, R, Marosok, R, Mowry-Hanley, J, et al.Mediastinitis following coronary mitry bypass surgery: a 3-year review. J Infect Dis 1991; 163:117121.Google Scholar
29.Simon, PA, Chen, RT, Elliott, JA, Schwartz, B. Outbreak of pyogenic abscesses after diphtheria and tetanus toxoids and pertussis vaccination. Ped J Infect Dis 1993;12:368371.Google Scholar
30.Nakashima, AK, Allen, JR, Martone, WJ, et al.Epidemic bullous impetigo in a nursery due to a nasal carrier of Staphylococcus aureus: role of epidemiology and control measures. Infect Control 1984;5:326331.Google Scholar
31.Hoeger, PH, Eisner, P. Staphylococcal scaled skin syndrome: transmission of exfoliatin-producing Staphylococcus aureus by an asymptomatic carrier. Ped Infect Dis J 1988;7:340342.Google Scholar
32.Richardson, JFQuoraishi, AH, Francis, BJ, Marples, RR. Beta-lactamase-negative, methicillin-resistant Staphylococcus aureus in a newborn nursery: report of an outbreak and laboratory investigations. J Hosp Infect 1990;16:109121.Google Scholar
33.Back, NA, Linnemann, CC Jr, Pfaller, MA, Staneck, JL, Morthland, V. Recurrent epidemics caused by a single strain of erythromycin-resis-tant Staphylococcus aureus: the importance of molecular epidemiology. JAMA 1993;270:13631364.Google Scholar
34.Chowdhury, MN, Kambal, AM. An outbreak of infection due to Staphylococcus aureus phage type 52 in a neonatal intensive care unit. J Hosp Infect 1992;186:22:299305.CrossRefGoogle Scholar
35.Walter, CW, Kundsin, RB, Brubaker, MM. The incidence of airborne wound infection during operation. JAMA 1963;186:908913.CrossRefGoogle ScholarPubMed
36.Venezia, RA, Harris, V, Miller, C, Peck, H, San Antanio, M. Investigation of an outbreak of methicillin-resistant Staphylococcus aureus in patients with skin disease using DNA restriction patterns. Infect Control Hosp Epidemiol 1992;13:472476.Google Scholar
37.Trilla, A, Nettleman, MD, Hollis, RJ, Fredrickson, M, Wenzel, RP, Pfaller, MA. Restriction endonuclease analysis of plasmid DNA from methicillin-resistant Staphylococcus aureus: clinical application over a three-year period. Infect Control Hosp Epidemiol 1993;14:2935.Google Scholar
38.Payne, RW. Severe outbreak of surgical sepsis due to Staphylococcus aureus of unusual type and origin. Br Med J 1967;4:1720.Google Scholar
39.Allen, KD, Anson, JJ, Parsons, LA, Frost, NG. Staff carriage of methicillin-resistant Staphylococcus aureus (EMRSA15) and the home environment: a case report. J Hosp Infect 1997;37:7475.Google Scholar
40.Hilton, M, Chen, JM, Barry, C, Vearncombe, M, Simor, A, Deoxyribonucleic acid fingerprinting in an outbreak of Staphylococcus aureus intracranial infection after neurotologic surgery. Otol Neurotol 2002;23:550554.Google Scholar
41.Groves, RJ, Mason, C, Boxrud, D, Cheek J. Nosocomial transmission of a community-associated strain of methicillin-resistant Staphylococcus aureus by a colonized health-care worker. Presented at the Annual Meeting of the Centers for Disease Control and Prevention, Epidemic Intelligence Service; March 24-27, 2002; Atlanta, GA.Google Scholar
42.Bassetti, S, Pfaller, MA, Sherertz, RJ. Airborne dispersal of Staphylococcus aureus associated with symptomatic rhinitis allergica. Ann Intern Med 2003;139:E236.Google Scholar
43.Ramirez-Ronda, CH, Fuxench-Lopez, Z, Nevarez, M. Increased pharyngeal bacterial colonization during viral illness. Arch Intern Med 1981;141:15991603.Google Scholar
44.Shuter, J, Hatcher, VB, Lowy, FD. Staphylococcus aureus binding to human nasal mucin. Infect Immun 1996;64:310318.Google Scholar
45.Nichol, KP, Cherry, JD. Bacterial-viral interrelations in respiratory infections of children. N Engl J Med 1967;277:667672.Google Scholar
46.Gwaltney, JM, Sande, MA, Austrian, R, Hendley, JO. Spread of Streptococcus pneumoniae in families: relation of transfer of S. pneumoniae to incidence of colds and serum antibody. J Infect Dis 1975;132:6268.Google Scholar
47.Harrison, LH, Armstrong, CW, Jenkins, SR, et al.A cluster of meningococcal disease on a school bus following epidemic influenza. Arch Intern Med 1991;151:10051009.CrossRefGoogle ScholarPubMed
48.Gwaltney, JM, Hayden, FG. The nose and infection. In: Proctor, DF, Andersen, I, eds. The Nose: Upper Airway Physiology and the Atmospheric Environment. Amsterdam: Elsevier; 1982:399422.Google Scholar