Cluster of Severe Acute Respiratory Syndrome Cases Among Protected Health Care Workers

Note: This article is being made available on the Web prior to publication in the Canada Communicable Disease Report (CCDR). It will be published in an upcoming issue of the CCDR.

Infections among healthcare workers (HCWs) have been a common feature of severe acute respiratory syndrome (SARS) since its emergence. The majority of these infections have occurred in locations where infection control precautions either had not been instituted or had been instituted but were not followed. Recommended infection control precautions include the use of negative pressure isolation rooms where available; N95 or higher level of respiratory protection; gloves, gowns, and eye protection; and careful hand hygiene. This report summarizes a cluster of SARS among HCWs in a hospital that occurred despite apparent compliance with recommended infection control precautions(1).

The index patient was a Canadian family physician aged 54 years with a history of hyperlipidemia, hypertension, and noninsulin-dependent diabetes controlled with oral medications. During 1-2 April, 2003, he examined three patients who were family members involved in a community cluster of SARS in Toronto, Ontario(2). No infection control precautions were used. On 4 April, he had fever, myalgia, headache, mild diarrhea, and a dry cough; on medical evaluation, he had a clear chest radiograph, but he continued to feel ill during home isolation. On 8 April, he was reevaluated and found to have a left upper lobe infiltrate on a repeat chest radiograph; he was admitted to the SARS ward of hospital A.

Over the next several days the patient remained febrile with increasing cough, although his diarrhea resolved. On 12 April, the patient's temperature reached 40.4 º C (104.7 º F), his chest radiograph showed worsening pneumonia, and he required supplemental oxygen for hypoxia. He was treated with ipratropium bromide and albuterol sulfate by metered dose inhaler, intravenous (IV) ribavirin, and steroids. On 12 April, he had a nearly constant cough and was assessed for transfer to the intensive care unit (ICU). On 13 April, the patient was transported to the ICU in a wheelchair on 100% oxygen through nonrebreather facemask.

Soon after his arrival in the ICU, his measured oxygen saturation decreased to 60%, and he was placed on positive pressure ventilation through facemask (BiPAP). Because of severe cough and agitation, he removed the mask repeatedly despite administration of intravenous (IV) sedation. After an approximately 2-hour attempt to provide oxygen through BiPAP, the patient was intubated. During intubation, he had frothy secretions that later obstructed the ventilator tubing, requiring disconnection and drainage. Once supported with mechanical ventilation, the patient was sedated further by using IV midazolam/morphine sulfate.

Later that evening, the patient was switched from assist-control ventilation to high-frequency oscillatory ventilation (HFOV) because of continued inadequate oxygenation. At this point, the patient's condition stabilized, and he was maintained on HFOV for 7 days, after which he was switched back to assist-control mode. As of 14 May, the patient remained in critical condition. Both a sputum sample collected from the patient on 13 April and a stool sample collected on 5 May were positive for the SARS-associated coronavirus (SARS-CoV) by polymerase chain reaction.

Between 15 and 21 April, nine HCWs who had cared for this patient around the time he was intubated developed illnesses consistent with the World Health Organization case definitions for suspect or probable SARS(3); another two HCWs had symptoms that were not consistent with the case definition (Table). Six of these 11 HCWs had been present during the intubation procedure. Interviews with affected HCWs indicated that they all had worn the recommended personal protective equipment (PPE) each time they entered the patient's room, including gown, gloves, PCM2000™ duckbill masks (Kimberly Clark Health Care, Roswell, GA), and goggles with or without an overlying face shield.

The room in which the intubation took place was at negative pressure to the hallway, and all air was vented to the outside after high-efficiency particulate air filtration; however, no anteroom was available, and removal of PPE took place in a staged manner both inside and outside the room, with the door kept closed between each entry and exit. Understanding the correct order to remove PPE (i.e. gloves first followed by mask and goggles) varied among HCWs.

Masks worn by HCWs inside ICU rooms and halls were changed on leaving each patient's room; however, no formal respiratory protection program existed at the hospital, and individual workers had not been fit tested. In addition, the primary nurse for the patient had a small beard and reported that his mask did not fit well. Although he wore both a PCM2000™ and a surgical mask with face shield, he could sometimes feel air entering around the sides of his mask

Table. Characteristics of health care workers who had symptoms of severe acute respiratory syndrome (SARS) following exposure to the index patient during the time of his intubation - Toronto, 15-21 April, 2003

Health care worker Symptom onset date Suspect or probable SARS case Occupation Exposure 1 April 15 Suspect Respiratory therapist Provided care before, during, and after intubation in ICU* 2 April 16 Suspect ICU nurse assigned primarily to another patient Provided care before, during, and after intubation in ICU 3 April 16 Suspect ICU primary nurse Provided care before, during, and after intubation in ICU 4 April 16 Suspect Respiratory therapist Provided care before, during, and after intubation in ICU 5 April 16 Probable Ward physician Examined patient on ward during morning of 13 April 6 April 17 Probable ICU physician Provided care before, during, and after intubation in ICU 7 April 17 Suspect ICU charge nurse Provided care before, during, and after intubation in ICU 8 April 18 Suspect ICU physician Examined patient on ward during early morning of 13 April 9 April 18 Suspect Radiology technician Performed chest radiograph of patient on ward during early morning of 13 April 10 April 18 Not a case† ICU nurse assigned primarily to another patient Provided care after intubation in ICU 11 April 21 Not a case‡ ICU physician Provided care before intubation in ICU

*Intensive care unit †Illness marked by headache, cough, and diarrhea but without fever ‡Illness marked by cough and infiltrate on chest radiograph but without fever

Source: M Ofner, Division of Blood Safety, Nosocomial and Occupational Infections, Health Canada; M Lem and S Sarwal, Field Epidemiology Training Program, Health Canada;M Vearncombe and A Simor, Sunnybrook and Women's College Health Sciences Centre, Toronto, Ontario, Canada, SARS Investigative Team, CDC.

Transmission of SARS appears to result primarily from direct patient contact or contact with large respiratory droplets within the close vicinity of an infected person. Despite apparent limited modes of transmission, SARS has been known to spread extensively among HCWs in various settings. For example, among 138 cases of secondary and tertiary spread in Hong Kong, 85 (62%) occurred among HCWs(4); among 144 cases in Toronto, 73 (51%) were HCWs(5). SARS infection of HCWs might be related to increased contact with respiratory secretions, contact with patients during a more contagious phase of critical illness, contact with particular patients at increased likelihood of spreading SARS (i.e. super-spreaders), or exposure to aerosol-generating patient care procedures(6).

Health Canada and CDC are aware of several unpublished reports of SARS clusters among unprotected HCWs involved with intubation, both in Canada and outside North America. The cluster described in this report might be unique, as HCWs appear to have followed infection control precautions recommended by Health Canada. The Health Canada recommendations, although similar to those of CDC, differ from CDC guidelines with respect to respiratory protection. CDC guidelines specify use of respirators approved by the National Institute for Occupational Safety and Health (NIOSH) rated at an N95 level of protection or greater(7). Health Canada recommends use of "N95 equivalent" respirators(8). The respirators used in hospital A, although compliant with Canadian public health recommendations, were not NIOSH approved. In addition, at the time these exposures occurred, fit testing was not recommended by Canadian public health authorities; such testing but has been mandated in the United States since 1972.

Endotrachial intubation might cause an awake or a semiconscious patient to cough and often necessitates open suctioning of respiratory secretions. In addition, other potentially aerosol-generating procedures were performed on this patient, including BiPAP, during which air might be forced out around the facemask and thereby aerosolize secretions, and HFOV, during which exhaust from the ventilator tubing is more likely to escape without passing through an antibacterial/antiviral filter. The patient also was in his second week of illness with clinical deterioration and severe cough, possibly explaining why HCWs who were exposed to the patient only before his transfer to the ICU became infected, as the viral loads of patients at this stage of illness appear high(9).

Direct contact with the patient or contact with an environment contaminated by large respiratory droplets might have led to HCWs infecting themselves as they removed their PPE. For example, HCWs have been known to spread other nosocomial pathogens from patient to patient despite the use of barrier precautions; even in the best of circumstances, correct use of PPE might be suboptimal. If contact or droplet spread alone were responsible for this cluster, a lapse in technique would be required on the part of each infected HCW. Many HCWs apparently lacked a clear understanding of how best to remove PPE without contaminating themselves. Alternatively, aerosolizing procedures or the patient's own cough might have led to airborne spread, and either the level of respiratory protection used or the manner in which it was used did not prevent transmission.

This cluster is part of a larger number of cases in HCWs in hospitals in the greater Toronto area who have become infected while caring for SARS patients since directives for contact, droplet, and airborne precautions were instituted at the provincial level on 28 March(1). Further investigation is necessary to determine factors associated with transmission despite the apparent use of recommended infection control precautions.

HCWs caring for SARS patients should be properly trained in the correct use and removal of PPE. Patients who are experiencing rapid clinical progression with severe cough during their second week of illness should be considered particularly infectious. Procedures that might generate aerosols (e.g. nebulized medications, BiPAP, or HFOV) should be avoided if possible. When intubation is necessary, measures should taken to reduce unnecessary exposure to HCWs, including reducing the number of HCWs present and adequately sedating or paralyzing the patient to reduce cough. Infection control precautions for SARS precautions are available on the Health Canada SARS Website at http://www.hc-sc.gc.ca/pphb-dgspsp/sars-sras/prof_e.html#control or http://www.SARS.gc.ca and click on Health Professionals and then Infection Control.

Health Canada. SARS Among Ontario Health Care Workers - SARS Epidemiologic Summaries: April 26, 2003

Health Canada. Epi-Update: Interim Report on the SARS outbreak in the Greater Toronto Area, Ontario, Canada April 24, 2003

World Health Organization. Case Definitions for Surveillance of Severe Acute Respiratory Syndrome (SARS)

Lee N, Hui D, Wu A, Chan P, Cameron P, Joynt GM, Ahuja A, Yung MY, Leung CB, To KF, Lui SF, Szeto CC, Chung S, Sung JJ. A Major Outbreak of Severe Acute Respiratory Syndrome in Hong Kong. N Engl J Med 2003 Apr 14

Booth CM, Matukas LM, Tomlinson GA, Rachlis AR, Rose DB, Dwosh HA, Walmsley SL, Mazzulli T, Avendano M, Derkach P, Ephtimios IE, Kitai I, Mederski BD, Shadowitz SB, Gold WL, Hawryluck LA, Rea E, Chenkin JS, Cescon DW, Poutanen SM, Detsky AS. Clinical Features and Short-term Outcomes of 144 Patients With SARS in the Greater Toronto Area. JAMA. 2003;289

Seto WH, Tsang D,Yung RW, Ching TY, Ng TK, Ho M, Ho LM, Peiris JS, and Advisors of Expert SARS group of Hospital Authority. Effectiveness of precautions against droplets and contact in prevention of nosocomial transmission of severe acute respiratory syndrome (SARS). The Lancet Vol 361 May 3, 2003; 1519-20.

CDC. Interim Domestic Guidance on the Use of Respirators to Prevent Transmission of SARS: May 6, 2003.

Health Canada. Infection Control Guidance for Respirators (Masks) worn by Health Care Workers - Frequently Asked Questions: April 17, 2003.

Peiris JS, Chu CM, Cheng VC, Chan KS, Hung IF, Poon LL, Law KI, Tang BS, Hon TY, Chan CS, Chan KH, Ng JS, Zheng BJ, Ng WL, Lai RW, Guan Y, Yuen KY, and members of the HKU/UCH SARS Study Group Clinical progression and viral load in a community outbreak of coronavirus-associated SARS pneumonia: a prospective study. The Lancet. Published online May 9, 2003

This article is from May 15, 2003, but I'm hoping it's recent enough to post, because it contains a lot of information that we can find no where else--and I do mean a LOT.

It will greatly add to our FR knowledge base.

His lungs were clogged and his was drowning in his own secretions. Shades of the Spanish influenza (1918-1919), although this is a new flu...

I'm just now reading a book about the Congress of Vienna at the end of the Napoleonic Wars. Diplomats were already gathered at Vienna in the fall of 1814, before Napoleon's return to power and Waterloo. A lot of the diplomats came down with a severe flu in the fall of that year, while in Vienna. Similarly, many of the diplomats at the peace conference at Versailles in 1919 after WWI came down with the Spanish flu (and, in that case, some of them died.)

Thanks for this post. It is extremely informative. Death by drowning from a viral pneumonia is so horrible.

Maybe other doctors will now realize that infection control precautions really are valid and important.

I certainly hope that this article has been widely disseminated through the health care system in Canada and the US, at least in the areas where one would be likely to encounter a suspected SARS case!

Thank you for this timely and highly informative post. I am printing the report for my wife to share with her fellow E.R. staff members with a copy to the hospital training department.

Every time I read the story of the male nurse with the small beard feeling air on his face even though he was wearing a mask, I wonder how dense you have to be to wear a surgical mask over a beard.

I have never seen a surgeon or a scrub tech with a beard - I was a scrub tech for a while - you keep your nails cut very short so you can clean under them.

When I see male nurses with beards and female nurses with elaborate nail wraps, I question the sanity of the hospital administrators - unless they are working in a ward where there is no chance of spreading infection - the only one I can think of is mental health.

>>His lungs were clogged and his was drowning in his own secretions. <<

That's typical of severe pneumonia.

My 70 year old mother refused to go to the doctor for a chest infection until she was near death - I finally forced her to go and wish I had taken her sooner but she kept insisting she was getting better.

I was present when she was intubated - if you've never been intubated you have no idea how difficult it is - really they should spray the palate with anesthetic because you gag and that forces the tube back up - they tried for a long time and there was blood and sputum everywhere. It was horrible.

You're welcome. Knowledge is empowering.

I would be extremely interested in any anecdotal response you and/or your wife have, after passing out the information...without identifying anyone, would you please post anything you can?

I am so sorry to hear of your mother's illness, and the intubation. That is horrible.

I don't understand about SARS; is this coronavirus some super-pneumonia and that's why it is so easily mis-diagnosed in the early stages?

I think the reason it's easy to miss is this: Fever is the only consistent reliable early symptom of SARS. A lot of times, the cough only comes after being sick for a week or better, and pneumonia doesn't show on an x-ray right away, either. There's no reliable test for SARS, and especially no reliable EARLY test for SARS. The best ones aren't positive for up to three weeks after somebody gets sick.

Hope that helps...

A lot of times, the cough only comes after being sick for a week or better, and pneumonia doesn't show on an x-ray right away, either.

Yikes! My neighbor comes to mind. As of Thursday evening, he had a fever for 8 days, no cough.

I want to call over there and see how he is doing but I know she will know I am being nosey...

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