The efforts of the joint University Health Network medical imaging departments where Narinder Paul, MD, is a division chief for chest and cardiac imaging, were coordinated with an international research effort to identify the radiological signs of SARS.

For the health care community in Toronto, Canada, March came in like a lion, but it did not go out like a lamb. It was not until June that the SARS (severe acute respiratory syndrome) cases, caused by a virus imported unknowingly by a traveler returning from Hong Kong, were said to have peaked. By that time the Toronto hospital system had been tested and changedpotentially for the better, some people say. Caught in the thick of the battle against SARS were radiologists at four coadministered hospitals aligned with the University of Toronto. This is the story of how their joint departments responded to the SARS outbreak and what it meant in business terms to do so.

The initial reaction, says Andrew Holt,? MHS, director of medical imaging for Mt Sinai Hospital and the University Health Network (UHN), was “counterintuitive.”

Logic would dictate that in a major external disaster (Code Orange alert) emergency, medical, and support staff would be called to the hospital in high numbers. With the SARS epidemic the opposite was the case. Staff, eager to join in the fight against the disease, was told instead to go homeand stay. The immediate response as SARS patients were admitted was to isolate them and shut down everything else. Within hours of the Code Orange, all but emergent cases were canceled across the hospital. Medical imaging canceled thousands of procedures. Literally overnight, SARS wards were constructed and staffed in order to isolate and contain SARS within the hospital and prevent it from spreading to the community. Within a day or two, the hospital was a place where masked and gowned hospital staff moved with lonely purpose, forbidden to congregate or even to eat together. “The lounges and cafeterias were shut down,” Holt says. “It was a ghost town around here.”

For those who remained on site, there was a huge amount of work to be done. Because all but emergent surgeries had been halted, operating room staff was sent to man the single ground level entrance at each hospital through which people had access. Body temperatures were checked at the door. Everyone had to say if they felt feverish or were experiencing the other flu-like symptoms associated with SARS: muscle aches, severe headaches, shortness of breath, and dry coughs. Once inside, they had to be masked, gowned, and gloved during their entire time in the hospital.

The SARS epidemic in Toronto began after an elderly female traveler returned from Hong Kong feeling ill. In Hong Kong she had stayed on the same hotel floor as a single Chinese physician who is believed to have set off the spread of the disease. Back in Canada, the woman fell ill. Believing that she had the flu, she stayed home, and in doing so spread SARS to other relatives. Eventually, she and other family members were admitted into a hospital in Scarborough in late February. By mid March, Toronto and Canadian health officials realized they had a problem. On March 30, the Ontario Ministry of Health issued a Code Orange for Toronto, and the battle to contain the as yet undiagnosed disease intensified.

The radiological signs of SARS include unilateral focal airspace opacity in the lung (a), present in nearly half the SARS cases seen at the hospital. In nearly a third of all cases, patients had either bilateral multifocal opacities (b) or diffuse opacities (c), associated with the highest death rate. Images courtesy of Narinder Paul, MD, Princess Margaret Hospital.

Mt Sinai Hospital and the UHN was in the thick of that battle. UHN is composed of three hospitalsToronto General (TGH), Toronto Western (TWH), and Princess Margaret. SARS patients were admitted to all four sites and isolated in SARS wards with strict infection control in place. The first cluster of SARS patients had been at Scarborough Grace Hospital, unaffiliated with UHN-Sinai. Some victims in the original cluster were medical workers who had no idea SARS was a threat. Sinai and the UHN hospitals are affiliated with the University of Toronto, and are teaching hospitals. Holt says they have a combined bed count of about 1,500. According to its web site, UHN is one of Canada’s largest teaching hospitals with an annual budget of close to $850 million (Canadian). Between them, UHN and Sinai have about 13,500 employees.

The First objective

In the first 48 hours after the Code Orange was declared, Holt says, the whole focus was on halting the spread of SARS. That meant drastically limiting physical contact with any SARS patient or any probable or possible patient. At the time, Holt adds, health officials did not know what disease they were dealing with. But several people had died. The war in Iraq was ongoing and the threat of bioterrorism was a remote consideration. “That was the backdrop,” Holt says. “You didn’t think that was what it was, but you didn’t know.

“The entire health care system responded as one system,” recalls Holt. “From a public policy perspective, this is the most extraordinary part of the story. We are talking coordination all the way from the bedside to the World Health Organization (WHO) to international research groups. We as an imaging service had to coordinate with that. The medical imaging team mobilized along with the large-scale mobilization, and within that we set up, on international, provincial, hospital, site, and departmental levels, a mechanism for communications and changes in practices as information became available from the international effort that was churning out data.”

Patrice Bret, MD

Holt camped out in his office and began working on the logistics of shutting down nearly all imaging. Typically, the four hospitals see as many as 1,500 imaging patients per day. They conduct about 650,000 studies per year. “We went from about 2,000 examinations to, on that first Monday, just over 400, and then a day later 300 examinations,” Holt says. “We held at that level for the first week. At about week three, we had canceled close to 6,000 patients.” Radiological interpretations at UHN-Sinai are done by a single physician groupMedical Imaging Consultantsmade up of about 60 radiologists. The hospitals employ another 450 technical and support personnel in imaging. The imaging equipmentabout 170 devices in all, including MR, CT, ultrasound, digital and plain film mammography, nuclear medicine, and general and portable x-rayis owned by the hospitals.

Imaging was not all that came to a halt. Only emergent surgical, medical, and other health services were provided. Because there were no incoming patients to speak of, all departments slowed to a crawl. Construction on a new hospital wing was stopped. Engineers were quickly called in to construct negative-pressure SARS isolation rooms for a SARS ward at each site. The negative pressure kept air contaminated by patients from leaving the rooms and infecting others. Staff members who were thought to have been exposed to the SARS virus were sent home to quarantine. Like thousands of others, including whole schools of teachers and students, they were required to spend 10 days in separate rooms in their houses or apartments, not mingling with and not eating with family members. “Anytime people met within three feet of each other, there was the potential for contamination,” says Holt. “It was very simple; if you didn’t cut down the physical transmission, it was going to spread.”

Andrew Holt, MHS

A pathologist at Mt Sinai isolated the cause as a coronavirus. At the same time, the spread of SARS in Singapore, Hong Kong, and other areas in China was being flagged. Canadian health officials then realized that Toronto was host to a SARS epidemic. Toronto doctors began communicating with doctors in Asia. Every day, Holt says, protocols were adjusted. “Should you put on your mask first and then wash your hands, or should you wash your hands and then put on your mask? There were hundreds of things like that to be deliberated.” Holt says his phone bill “was huge” afterward. Teleconferences between health officials and administrators were organized and expedited by the phone company. A month later Holt had in his SARS file more than 3,000 emails.

Imaging the disease

Narinder Paul, MD, is a diagnostic radiologist, trained in Britain, who has been at UHN-Sinai for about 3 years. He is division chief for chest and cardiac imaging, and he was one of the first who set about compiling x-ray profiles on SARS patients. Because the patients were in isolation, technicians shot films of their lungs once or twice daily on portable machines. There was no transporting of patients down to radiology suites. Paul was never in contact with patients himself, and therefore has nothing to say about personal danger.

“For radiology, we were asked to rule if we had a suspect SARS case. We were asked to look for abnormalities and rule out other causes of fever. The diagnosis itself was clinical, so everybody with symptoms initially was a suspect case,” he says.

Many of the patients Paul examined did turn out to have other reasons for their fevers. “They had community-acquired pneumonia or tuberculosis or something else,” he says. Those patients who could not be ruled out on the basis of “classical presentations” were marked for further study. As Paul was developing profiles of probable SARS patients, he began communicating with doctors in Hong Kong, where the first SARS outbreak had been confirmed. “They started publishing on the web site all of the cases they had. That was quite useful,” Paul says. “The University of Hong Kong and Prince of Wales Hospital put both CT and plain film images on the web.”

Asked what distinguished the SARS cases, Paul says, “Mainly, it was not looking like the normal bacterial pneumonias that we see. The key thing at first was to make sure there weren’t other causes, and then as we got more experienced, we saw there were patterns involved, and we could then say with some confidence in a given situation whether it was a SARS patient or not.”

Eventually, Paul defined four different patterns of chest abnormalities that were variations of SARS. About one fourth of the patients initially exhibited normal radiographs, which a short time later “converted to abnormalities,” he says. Another group of patients, just under half, showed mid- and low-lung pneumonias, but for most of these patients the disease did not progress. “It resolves over several days to a few weeks,” he says. The third group showed “multifocal disease, small diffuse areas, patches of pneumonia in both lungs, a patch in the mid-zone or the low-zone.” Sometimes the patches would move from one part of the lung to another part quickly, like overnight. “About 60% of these patients stayed relatively stable,” Paul adds. Then, there was the fourth group, the group from which all of the deaths came. In this group there was widespread diffusion, “a near whiteout, opacity of both lungs,” Paul says.

Patients who succumbed to SARS were elderly in the main, according to Ontario Ministry of Health numbers listed on its web site. The youngest victim was a 39-year-oldmale who died on April 30; the oldest a 99-year-old woman who died on April 17. By June 10, there had been 33 deaths out of 425 possible or probable cases in Toronto. But there were no deaths for days before that, and on June 9 Toronto health officials said they were cautiously optimistic the epidemic had peaked. On June 10 another 176 cases remained under investigation. On June 5, the WHO declared that SARS was “over its peak worldwide.” Paul says many of the patients who died had other complicating factors like heart disease or diabetes.

The economic impact

At the peak of the Toronto epidemic, the city made a WHO list of places for travelers to avoid. This WHO travel advisory angered many, especially small businessmen who relied on conventions and tourism to make their own livings. There wasand isa sense in Toronto that the SARS outbreak was sensationalized in the press. One headline in the Toronto Star warned “Every Ambulance a Trojan Horse.” (For a recap of the Star’s coverage, access its web site at .) Because more than 100 of those initially infected with the SARS virus were health care workers, many who worked in health care reported that they and their family members were being shunned.

Patrice Bret, MD, is chief of medical imaging at UHN-Sinai, and, like Narinder Paul, a diagnostician and professor of radiology at the University of Toronto. It has been left to Bret and administrators like Andrew Holt to assess the economic impact in the SARS aftermath.

“We’re no different than a Chinese restaurant or one of the hotels,” Bret says. “A huge number of businesses have been affected, and we’re one of them.” Unlike staff at the hospitals, the radiologists work on a fee-for-service contract paid by the government health service. When imaging was drastically curtailed at the start of the outbreak, fees for interpretations fell off to near nothing too.

“Overall, we canceled about 7,000 patients or about 15,000 exams in a 7-week period. In the first week we dropped to 5%-7% of our normal ambulatory volume,” Bret says. Like many Canadian doctors in other specialties, radiologists at UHN-Sinai tried to shift some patients to private offices, but there are far fewer privately owned MRIs and other imaging devices in Canada than in the United States. The impact of shifting patients was “a drop in the bucket,” Bret says.

Neither Bret nor Holt wants to say just how serious the income loss for radiology and the radiologists at UHN-Sinai has been. While the figures are proprietary, they are not minor. “If you do 30% of your regular imaging for a month, that’s a big hit,” Holt says. “Radiologists have mortgages and kids too.” Canada’s system of global health care financinga stipulated amount allocated up front, and when it is spent, there is no morealso makes the losses hard to compute, Holt adds.

Bret says there are ongoing negotiations with the government about covering some of the losses suffered by physicians, not just radiologists but surgeons and others on fee-for-service who lost out too. He says the government has indicated it may approve $700 million in SARS emergency funding, but how much would go to physicians is unknown.

It was not just the falloff in patients that impacted radiology. Bret says volumes are back now to 80% of normal. But radiologists and staff are working extended hours and weekends, and not all of this extra work is for catching up. To keep SARS under control, modalities that once got by with a change of sheets for patients to lie on now have to have tables thoroughly wiped with disinfectant. This adds 15 minutes between examinations. “So, if it takes 20 minutes to do a CT and 15 minutes to clean up the room, then your productivity has come down by 50%,” Bret says. Patients are still being screened at the door. All of this adds up to lost time and that turns into lost revenues. To get an idea of how cumbersome and time-consuming handling the SARS epidemic has been, health care workers told the Toronto Star they were going through 10 masks, 10 gowns, five sets of green scrubs, and 25 gloves in a single day.

There is also a patient care angle. UHN-Sinai is one of the largest cancer centers in North America. Cancer staging is an important part of its imaging. Bret says some patients at first went too long without follow-up to check disease progression or regression. The same applied to monitoring cancer treatment results. “Those are extremely time-sensitive. Staging and re-staging are absolutely essential and that is where we are mostly caught up,” says Bret. “In cardiology, we’re still behind. The electives like renal stones, abdominal pains, diarrheathose patients are still in the backlog.”

Both Bret and Paul decry what they see as alarmist media coverage that they claim continues to scare patients away.

“There is concern about SARS,” says Paul. “The death rate in our series was about 6%. That’s a concern. But there’s a difference between being concerned and being hysterical. This outbreak should be looked at with a degree of measured calm. After all, influenza kills thousands of people per year. You have to keep this in context.”

Bret says the hysteria over the disease continues to cause patients to stay away, sometimes to their own detriment. “In MRI we’re still way behind [capacity],” he says. “In CT we’re almost caught up, in general radiology we’re almost caught up; in ultrasound we’re behind, in mammography we’re behind because there are a lot of women who don’t come or who say they’ll wait. They’ll wait another year, and we’re going to see some negative effects from that.”

Bret estimates the number of no-shows for examinations at 10% to 15%. It is especially frustrating because no one knows who will show up and who will not. “People have their own sensitivities,” he says. “They feel anxious, or they think we’re still closed, or the news has been too complex for them to handle. They don’t come, and it makes it very difficult.”

Silver linings

The SARS epidemic in Toronto is not over. As of this writing, there was concern that dialysis patients in the Regional Municipality of Durham east of the city may have become infected and spread the disease to others, but this was proven to not be the case. Because the symptoms are so general, the health care system has had a difficult time identifying these cases up front. Three or four cases remained hospitalized across the UHN system in late June. Nurses at Mt Sinai Hospital have charged in the press that the provincial directive for all staff to wear protective clothing in some instances was ignored, perhaps exposing infants, new mothers, and health care workers to the disease. Canadian officials have called for an investigation into how the epidemic was handled, and there have been charges that the health care delivery system was stretched much too thin. Tourism in Toronto is still nonexistent. A fur dealer’s convention set for late May was canceled and moved to Copenhagen.

Nonetheless, adverse events can have silver linings, and the SARS outbreak in Toronto is no different. Andrew Holt says some of the silver linings were purely serendipitouslike the installation of DR equipment and a PACS (picture archiving and communications system) upgrade that were able to proceed quickly because of the reduced patient load. More than that, there was what Holt calls “a breakdown of the silos” where teams from various departments were thrown together to handle the emergency. This, he says, has resulted in a collaborative spirit institution-wide that was not there before. Paul agrees, “Health people were concerned, and even when their colleagues were going down with symptoms, they still stuck at it. That is a hard thing to do when your colleagues are becoming sick.”

Other silver linings may come slowly and be on a larger scale. Bret says the SARS outbreak has given impetus to a desire to move away from hospital-based care and more into the ambulatory care arena, such as has been done in the United States. Paul suggests that cleanliness protocols put in place for the outbreak may become permanent. Holt agrees, saying, “Your whole approach now is dictated as much by infection control as it was by radiation safety. We are obsessed with both now.”

But the biggest silver lining may come from what Holt calls SARS: a “pre-test.” The next epidemic will hit with lines of attack already in place. “We will come out of this stronger,” he says. “This is the era we’re moving into, and the next time we’ll respond more quickly.”

In an age of monkeypox and mad cow disease, it does seem likely that a new test will come.

George Wiley is a contributing writer for Decisions in Axis Imaging News.