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A Cloud Adult: The Staphylococcus aureus-Virus Interaction Revisited

Robert J. Sherertz, MD; David R. Reagan, MD, PhD; Kenneth D. Hampton, BS; Kim L. Robertson, LPN; Stephen A. Streed, MS; Helena M. Hoen, MS; Robert Thomas, MD, Gwaltney Jack M. Jr. MD
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From Bowman Gray School of Medicine and North Carolina Baptist Hospitals, Inc., Winston-Salem, North Carolina; James H. Quillen College of Medicine, Johnson City, Tennessee; and University of Virginia School of Medicine, Charlottesville, Virginia. Acknowledgments: The authors thank Jean Kimbrell for secretarial assistance and physician 4 for agreeing to participate in this investigation. Requests for Reprints: Robert J. Sherertz, MD, Section of Infectious Diseases, Bowman Gray School of Medicine, Medical Center Boulevard, Winston-Salem, NC 27157-1042. Current Author Addresses: Dr. Sherertz: Section of Infectious Diseases, Bowman Gray School of Medicine, Medical Center Boulevard, Winston-Salem, NC 27157-1042.

Copyright ©2004 by the American College of Physicians

Ann Intern Med. 1996;124(6):539-547. doi:10.7326/0003-4819-124-6-199603150-00001
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Background: Nasal carriage of Staphylococcus aureus is common among health care workers, but outbreaks caused by such carriers are relatively uncommon. We previously reported outbreaks of S. aureus skin infections that affected newborn infants and were attributed to an S. aureus nasal carrier who had had an associated upper respiratory tract infection (URI) during the outbreak period.

Objective: To investigate the contribution of a nasal methicillin-resistant S. aureus (MRSA) carrier (physician 4) who contracted a URI to an outbreak of MRSA infections that involved 8 of 43 patients in a surgical intensive care unit during a 3-week period.

Design: An epidemiologic study of an outbreak of MRSA infections and a quantitative investigation of airborne dispersal of S. aureus associated with an experimentally induced rhinoviral infection.

Setting: A university hospital.

Participants: 43 patients in a surgical intensive care unit and 1 physician.

Measurements: Molecular typing was done, and risk factors for MRSA colonization were analyzed. Agar settle plates and volumetric air cultures were used to evaluate the airborne dispersal of S. aureus by physician 4 before and after a rhinoviral infection and with or without a surgical mask.

Results: A search for nasal carriers of MRSA identified a single physician (physician 4); molecular typing showed that the MRSA strain from physician 4 and those from the patients were identical. Multivariate logistic regression analysis identified exposure to physician 4 and duration of ventilation as independent risk factors for colonization with MRSA (P < equals 0.008). Air cultures showed that physician 4 dispersed little S. aureus in the absence of a URI. After experimental induction of a rhinovirus URI, physician 4's airborne dispersal of S. aureus without a surgical mask increased 40-fold; dispersal was significantly reduced when physician 4 wore a mask (P < equals 0.015).

Conclusions: Physician 4 became a “cloud adult,” analogous to the “cloud babies” described by Eichenwald and coworkers who shed S. aureus into the air in association with viral URIs. Airborne dispersal of S. aureus in association with a URI may be an important mechanism of transmission of S. aureus.


Grahic Jump Location
Figure 1.
Epidemic curve for methicillin-resistant Staphylococcus aureus (MRSA) colonization in a surgical intensive care unit.P

The eight colonizations that occurred during the outbreak period (March-April 1994) represent a statistically significant increase over the previous baseline ( < 0.05).

Grahic Jump Location
Grahic Jump Location
Figure 2.
Relation between stay in a surgical intensive care unit and colonization with methicillin-resistant Staphylococcus aureus (MRSA).

The horizontal lines after each patient number represent the time each patient spent in the surgical intensive care unit. Open squares represent lower respiratory tract colonization with MRSA, solid squares represent MRSA pneumonia, and the cross represents MRSA bacteremia. The bar at the top shows the duration of physician 4's upper respiratory tract infection (URI) relative to the times when patients were colonized with MRSA.

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Grahic Jump Location
Figure 3.
Location of the air culture plates in relation to physician 4.

The large rectangle represents a table; the small rectangle is an elevated platform just behind physician 4 at nose height. Each small black circle is an agar settle plate. The settle plates are arranged along arcs 2, 3, 4, 5, and 6 feet from physician 4 at approximately 15-degree intervals on the table. The circles labeled AS are volumetric air samplers located 2, 3, and 4 feet directly in front of physician 4.

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Grahic Jump Location
Figure 4.
Air culture results from a single volunteer (physician 4) nasally colonized with Staphylococcus aureus.[41][6]Figure 3Top.Bottom.S. aureus

Each bar represents a 1-hour culture period using a combination of agar settle plates and volumetric air cultures , arranged as shown in . Striped bars show the total number of colonies isolated from all 47 plates when physician 4 was not wearing a mask; black bars show the same data when physician 4 was wearing a mask. The Cold Symptom Score summarizes the severity of physician 4's cold symptoms after nasal inoculation with a rhinovirus (>6 = a cold). On one occasion, the room was cultured when physician 4 was absent. The asterisk denotes that physician 4 was talking during most of the period. All bacteria. Only of the same molecular type as physician 4's nasal strains. CFU = colony-forming units.

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Grahic Jump Location
Figure 5.
Pulsed field gel electrophoresis of different strains of Staphylococcus aureus.S. aureusFigure 4S. aureusFigure 4

Lanes 1 to 3 equals air culture isolates not attributable to physician 4; lanes 4 and 5 equals methicillin-resistant (MRSA) nasal isolates from physician 4 (March and June 1994); lanes 6 to 11 equals patient MRSA isolates (patients 2, 3, 4, 5, 7, 8); lane 12 equals MRSA air culture isolate (day 9; , bottom); lanes 13 and 14 equals methicillin-sensitive (MSSA) nasal isolates from physician 4 (May and June 1994); and lanes 15 and 16 equals MSSA air culture isolates (days 1 and 10; , bottom).

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