Historical Perspective: Lessons from SARS-CoV-1

It will likely take years for us to truly learn the lessons from severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the virus that causes COVID-19. For so many of us in the infectious diseases field, a pandemic occurring was always a matter of when, not if; but, having one occur in your lifetime is nonetheless surprising and heartbreaking.

We have learned a lot already—not only about this novel disease, but about dealing with and responding to a pandemic means for the United States and globally. Even the challenges of pinpointing the origin of COVID-19 have shed light on how polarizing and politicized a pandemic can become.

When we consider lessons learned, however, SARS-CoV-2 can aid us in a variety of categories. These include testing, policy, vaccine development and deployment, nonpharmaceutical interventions, transmission dynamics, quarantine and isolation guidance, communication, global partnerships, and more. Moreover, this isn’t our first time dealing with a novel coronavirus. In late 2002 we experienced SARS-CoV-1 and then in 2012 we had the Middle East respiratory syndrome coronavirus (MERS-CoV).

Prior to COVID-19, I spent a few years examining these 2 novel coronavirus outbreaks in relation to infection prevention and public health response. In every outbreak, we know there will be challenges—in communication, rapid testing for and identification of a potential novel disease, frustrations around quarantine, and increased potential for transmission in higher-risk environments such as health care and households. We also must ensure that cross-functional partnerships are working effectively. But despite the lessons learned, we often don’t see the importance of using this hard-earned knowledge to build a more agile response to help break the cycle of neglect and using evidence from previous outbreaks to gauge future events.

This is the first of a 2-part miniseries on the historical perspective from our experience with severe coronaviruses. The first part focuses on SARS-CoV-1 and the second will discuss MERS-CoV. I should note that no “lookback” is perfect: Data and accounts may conflict, not all information is perfect, but hopefully this review will provide some insight to help us look at COVID-19 through a new lens and prepare for the next novel coronavirus more effectively.

LESSONS FROM SARS-COV-1

The first case of SARS, which would be identified retrospectively, occurred in November 2002 in the Guangdong province of China. It would become the first known case resulting from a novel coronavirus that caused an international outbreak across 2 dozen countries in North America, South America, Europe, and Asia before its transmission was halted in July 2003. Between November 2002 and February 2003, SARS spread throughout Guangdong. There were reports of a “strange contagious disease” that was inducing panic and a run on medicine, but alerts were not sent to the World Health Organization (WHO) until things began to spiral out of control. Chinese health officials underreported the number of cases during their initial disclosure, but eventually reported nearly 800 cases shortly after their first account to the WHO.¹ The agency was not notified until February 2003, and although the outbreak started in Guangdong, our concern in this article is with the Canadian portion.

The Toronto, Canada, SARS outbreak represented a pivotal moment in public health and outbreaks in the 21st century. The spread of the disease from China through a single person via air travel and then its rapid transmission within hospitals underscores the ability of novel diseases to spread, especially via super-spreader events. Control measures for the disease proved problematic even though mass quarantine and inconsistent infection control recommendations were enforced. The Toronto outbreak developed in 2 phases: Phase 1 occurred across 4 hospitals and included patients, health care workers, and visitors, whereas phase 2 involved health care workers and visitors at a single hospital.

The SARS outbreak, especially as it concerns the cases in Toronto, underscores the ramifications of poor infection control practices and the role of hospitals as amplifiers of disease transmission during an outbreak. Researchers have found that 72% of cases in Toronto and 22% of cases in Hong Kong were a result of nosocomial transmission,² which varied during each phase of the outbreak. Svoboda et al noted such differences in nosocomial transmission in Toronto; the percentage of patients exposed while in a hospital ward rose from 17% in phase 1 to 88% in phase 2.

Throughout the literature, there are indications of several trends that facilitated the spread of SARS. Lack of diagnostic testing, response to a novel disease, recommendations for and adherence to personal protective equipment (PPE), and management of visitors were all challenges that hospitals and those involved with the public health response experienced during the outbreak. Infection control failures that facilitated the spread of the disease included limited information, delayed isolation, flawed adherence to PPE requirements, and administrative responses that fueled confusion.

LACK OF INFORMATION

Perhaps one of the most challenging aspects regarding control of the outbreak was the novelty of the disease. Because SARS presented as an atypical severe pneumonia, which does not require isolation precautions beyond a mask, initial identification and isolation implementation was less likely. McDonald et al point to the nonspecific SARS symptoms and lack of rapid diagnostic tests as problematic during the outbreak. Sound familiar?

Even in April 2003, the WHO was scrambling to develop a test as the 3 diagnostic tests that were available were limited in their efficacy. Clinicians had to rely on patients reporting their travel history, previous hospitalization, and/or contact with a probable case as a way of assessing likelihood of SARS infection. Without a rapid diagnostic test, screening visitors and health care workers for relevant exposures or symptoms became critical for isolation, but such efforts rely on vigilance and transparency. Screening can be an effective infection control measure but in the absence of widespread disease activity, assessing visitors and staff for relevant exposure quickly lost its “discriminating ability.”¹

The delay in establishing recommendations for isolation precautions, diagnostic tests, and other infection control measures meant transmission continued unencumbered. Novel diseases, of which SARS is a prime example, inherently pose unique challenges for health care workers and infection prevention and control (IPC) efforts. Moreover, lack of information does little to encourage strict isolation for patients with ambiguous symptoms, and pneumonia isolation guidance that ranged from standard to droplet precautions, which leaves room for interpretation.

Ultimately this meant that health care workers were faced with a stark reality: Any patient entering a health care facility with a fever and respiratory symptoms could have SARS. Once the disease was better understood and knowledge was disseminated, the systemic issues of lackluster infection control adherence became problematic.

DELAYED ISOLATION

The initial registration and screening of patients during triage is the prime opportunity for initiating isolation to prevent the spread of infectious diseases. Delayed isolation of patients is already an issue in nonoutbreak situations; however, during the SARS outbreak it became a source of transmission. An analysis of transmission in Singapore found several examples of delayed isolation, which resulted in the exposure of dozens of people per infected patient. A 3-day isolation delay for 1 patient resulted in 25 cases total, which included 12 health care workers, 4 patients in the same unit, and 8 visitors.¹ In fact, 1 patient of a super-spreader event in Singapore had several comorbidities, which led health care providers to dismiss the possibility of SARS, thus delaying isolation and proper respiratory protection further.

Patients of super-spreader events represent a small group of people who are highly infectious but, as Richard A. Stein PhD, noted, such events have multiple factors that also include changes in airflow dynamics, misdiagnosis, and interhospital transfers.¹ The complexity of the super-spreader phenomenon indicates that both physiological and IPC-health care dynamics aid in the larger range of transmission. Twenty-seven secondary cases resulted from the aforementioned patient not being properly isolated for 8 days.² Unrecognized cases and the nonspecific symptoms of patients with SARS, coupled with subpar infection prevention practices, supported nosocomial transmission and amplification of the disease. Even after the outbreak began, determining if incoming patients were suffering from a novel disease versus a severe pneumonia was challenging. Depending on which organism causes pneumonia, the recommended isolation precautions range from standard to droplet. This ambiguity in a triage environment leaves considerable room for variability in isolation enforcement. Delays in isolation underscore the challenges of responding to a novel disease and the endemic problem of poor adherence to infection control practices. McDonald et al note that in Toronto and Taiwan, patients with unrecognized SARS were the main source of transmission and that eventually, early detection and/or continuous use of PPE was pivotal in slowing disease spread.²

PPE ADHERENCE

In general, much of what we learned regarding SARS-CoV-1 stems from our experiences in health care, as the setting was such a significant source of transmission. We can extrapolate some of these nuances into public health guidance for nonpharmaceutical interventions, especially for essential workers. Once infection control guidance was established (eg, specifics of isolation precautions, PPE, and laboratory practices), the challenge then became ensuring that health care workers adhered to it. The enhanced IPC measures, including the use of PPE, were required by Toronto’s provincial Ministry of Health for hospitals. Adherence to PPE recommendations became a critical component in reducing transmission, as the isolation of patients with SARS was frequently delayed. In both phases of the Toronto outbreak, transmission was facilitated by unrecognized cases of SARS; however, it was the breaches in IPC practices during the second phase that fueled such rapid spread.

According to McDonald et al, “the second phase resulted from unknown transmission of SARS-CoV-1 among hospitalized patients during a period when healthcare workers were being instructed to wear personal protective equipment, including gowns, gloves, and masks.”² Following the first phase of SARS in Toronto, PPE and isolation precaution practices were relaxed, which amplified the spread and led to the second phase. Following this realization and acknowledging the realities of infection control adherence and high rates of nosocomial cases, hospitals and public health officials worked to reduce transmission within health care. In Singapore, many hospitals opted to have all health care workers wear N95 masks, gowns, and gloves at all times.³ Unfortunately, differing opinions on respiratory protection requirements reportedly affected adherence globally.

Similar to the questions surrounding IPC practices during the Ebola virus disease cluster in Dallas, there were debates during the SARS outbreak regarding respiratory protection.³ Some questioned whether surgical masks were enough, or N95 masks sufficient, or even whether higher levels of protection such as powered air-purifying respirators were necessary. Many hospitals required staff to wear PPE throughout their shift or for long periods of time. Training was also required for support services such as environmental, dietary, and others who might come into contact with the patient. Intense focus on PPE and isolation precautions is exhausting for staff, which is likely why there was a relaxation of requirements.

Low notes that “as recommended by provincial SARS-CoV-1-control directives, all hospitals discontinued SARS-CoV-1 expanded precautions (ie, routine contact precautions with use of an N95 or equivalent respirator) for non-SARS-CoV-1 patients without respiratory symptoms in all hospital areas other than the emergency department and the ICUs [intensive care units].”³ This provincial change to infection control practices also allowed staff to cease wearing masks throughout the hospitals and cease maintaining social distancing, meaning that nonoutbreak IPC practices were resumed.

As we have been seeing with the cyclical nature of relaxing restrictions and a novel disease, this led to a tricky situation for health care workers. This decision coincided with WHO removing Toronto from the list of areas with recent SARS transmission and was likely encouraged by the exhaustive hospital efforts that strained supplies and personnel. McDonald et al, among others, also pointed to the relaxation of IPC recommendations and guidelines as a trigger for the second phase of the outbreak in Toronto. Deployment of IPC guidance, specifically for PPE, for a novel agent during an outbreak already presents a challenge to the public health response. However, systemic issues with health care worker adherence compound such struggles. Ensuring adherence with PPE over long periods of time is taxing not only for the staff, but also for those in charge of disseminating information. Additionally, as highlighted by the outbreak’s second phase, relaxing vigilance came with a heavy cost.

HOSPITAL ADMINISTRATIVE RESPONSE

Organizational hospital response during the SARS outbreak was critical in reducing disease transmission. Hospital responses ranged from new policies to environmental controls that focused on supplies and availability of negative-pressure patient rooms. Environmental control measures and logistical changes were ultimately utilized by several hospitals around the world to manage the influx of potentially infectious patients. Toronto officials established SARS wards by recommissioning existing care facilities or establishing specific SARS units. At the peak of phase 2, they initiated Code Orange, a government emergency response plan that meant hospitals suspended nonessential services. The limitation of hospital services severely impacts revenue and is not a decision made lightly. Hospitals also limited the number of visitors permitted and implemented screening for them. They opted to allow visitors for patients in SARS units, yet many required both screening and utilization of PPE; other hospitals required visitors to wear surgical masks even if they were visiting patients in other (non-SARS) units.

In other countries there were also cases of hospitals opting to implement a no-visitor policy, such as Tan Tock Seng Hospital in Singapore. Lastly, there was also the practice of screening staff for symptoms. Some hospitals, like Tan Tock Seng, opted to follow a strict regime of temperature monitoring for staff as a mechanism for early identification of illness. Outside the challenges surrounding early recognition and PPE use, hospital practices varied during the outbreak, but many chose to isolate patients with potential or confirmed SARS and implement visitor restrictions to help reduce the risk of nosocomial transmission.

From an infection control standpoint, SARS posed a unique problem for hospitals as it was a novel disease presenting with nonspecific symptoms. This was something we experienced again with COVID-19, made even worse with the level of presymptomatic and asymptomatic transmission.

Transmitted through droplet- and aerosol-generating procedures, SARS-CoV-1 easily spread throughout health care facilities. The role of hospitals in the outbreak, especially in Toronto, underscores not only their ability to amplify disease during outbreaks, but also the importance of infection control practices when implemented. Analysis by Webb et al revealed that in simulations, both hospital infection control and quarantine measures were critical in containing the SARS epidemic. Moreover, their mathematical simulations show that the “combination of moderate quarantine but strict hospital infection control procedures was the key to the containment of SARS-CoV-1 in the greater Toronto area.”⁴ According to their analysis, increasing quarantine did not result in significant hospitalization volume, whereas a lack of strict hospital control procedures increased the outbreak duration by more than 100 days. Adherence to infection control practices had a significant role in the SARS outbreak, whether it was relaxed practices triggering a second phase or strict adherence helping halt the outbreak.

An analysis by Loufty et al of hospital preparedness in relation to SARS-CoV-1 in Toronto hit on a point that was rarely addressed in the literature—infection control staffing. They note that at North York General Hospital in Toronto, which was hit the hardest in the outbreak, there were only 2 infection preventionists (IPs), and the hospital was ultimately forced to recruit additional IPs to establish the necessary IPC infrastructure.⁴ The existing IP staffing ratio for Canadian hospitals is reportedly 3 IPs per 500 beds, although Quebec has a 1:133 ratio mandate. Loufty et al also point to the Delphi project, which recommends a ratio of 0.8 to 1.0 IPs for every 100 beds.⁵ These staffing ratios are similar to those in the United States. During the outbreak, however, additional staffing was critical for daily rounding on the SARS units and for education, policy organization and modification, and addressing issues in real time. In efforts to ensure consistent levels of IPC practice, they also established a review system to monitor adherence to infection control measures, answer questions, and conduct surveillance for fever and symptoms within the hospital units.

Recommendations from Loufty et al included adequate IPC staffing, sustained training and standards for IPC practices, and provision of authority for the team to work effectively. In fact, this distribution of authority over IPC efforts was underscored in their analysis as it was critical for the IPC program to maintain a certain degree of authority over the issues. The limited IPC staffing and resources that are endemic throughout health care are especially obvious during public health emergencies such as the SARS outbreak.

Overall, the challenges and failures that occurred during the outbreak in 2003 are representative not only of the systemic infection control failures within health care, but of the operational challenges of biothreat response at an administrative level. Beyond the challenges of operationalizing a response to the outbreak, substantial financial strain also was associated with the novel disease.

FINANCIAL IMPLICATIONS AND QUARANTINE

The economic burden from the spread of SARS-CoV-1 to 29 countries fell across multiple sectors. From tourism to retail sales, the financial toll was felt well beyond the walls of hospitals and public health programs.

For example, the export of goods in 2003 year over year in Toronto went from 7.1% in January to –7.8% in August, whereas in Hong Kong it went from 26.7% in January to 7.0% in August.⁴ The SARS outbreak is reported to have cost the Asian economies $11 to $18 billion, with an estimated loss of 0.5% to 2% of total output.⁵ The WHO reported that apart from the direct costs to the health care and public health systems, there were costs related to quarantine efforts enacted across schools, hospitals, and even borders. International travel to the affected areas dropped by 50% to 70% and hotel occupancy fell by 60%.⁶ Some estimates put the cost of SARS-CoV-1 at $2.2 billion in China and $1.7 billion in Hong Kong, which were the hardest-hit countries in Asia. In Toronto, it is estimated that the outbreak cost the city roughly $1 billion.

What about quarantine? Much of the world experienced this for the first time with COVID-19. But for many individuals responding to and living in areas that had been affected by SARS-CoV-1, it wasn’t their first time dealing with large-scale quarantine efforts during a novel coronavirus disease outbreak. The application of large-scale quarantine was a particularly unique feature of the SARS outbreak. In Toronto, 30,000 individuals were quarantined, whereas only 1282 were quarantined in Hong Kong and 4090 in Shanghai-a substantial difference considering the vast variation in population (3 million in Toronto, 7 million in Hong Kong, and 18 million in Shanghai).⁷ Taiwan also quarantined roughly 131,132 individuals of their population of 22 million. Interestingly, of all those quarantined in Toronto, only 27 required formal orders under the Health Protection and Promotion Act.⁸

As Jacobs noted, Toronto had a surprisingly extensive application of quarantine efforts during the outbreak.⁷ These efforts were initiated by Canadian health officials on March 30, 2003, with hundreds of employees of York Central Hospital being asked to quarantine themselves.⁹ Public health authorities instructed asymptomatic contacts of patients with SARS to stay home under quarantine for 10 days ( from the last known date of exposure), which also included sleeping separately, using separate personal items (eating utensils, towels, etc), and wearing a mask when near household members.¹⁰

Unfortunately, the attempt to halt the spread of the disease through quarantine efforts also triggered another negative externality-thousands of Toronto residents quarantined in their homes, unable to work, with many reporting fear and stress. Blendon et al assessed public surveys during this time and found that although there was little disease spread in the general population, the outbreak had a considerable psychological impact. Additionally, public health efforts to educate residents were of mixed success, and communication failures were prevalent.¹¹ The burden of implementing quarantine by public health authorities should also be considered during the evaluation of response efficacy. Toronto Public Health reportedly investigated 2132 potential cases, identified 23,103 contacts of patients with SARS as requiring quarantine, and logged 316,615 calls on the SARS-CoV-1 hotline.¹²

Given that transmission of SARS mostly occurred in hospitals and households, quarantine efforts involving hospitalized patients could be quite cumbersome. For every case of SARS, public health authorities expected to quarantine up to 100 contacts and investigate 8 possible cases. Schabas noted that for quarantine to be useful-an unproven intervention, especially when dealing with a novel disease-the following 3 criteria should be met:

• Individuals likely to be incubating the disease must be efficiently and effectively identified,
• individuals must adhere to the conditions of quarantine, and
• the infectious disease in question must be transmissible in its presymptomatic or early symptomatic stages.¹³

Schabas reported that quarantine in the Toronto SARS outbreak failed to meet all 3 criteria. He emphasized that it was carried out on a massive scale, was neither effective nor efficient, and ultimately isolated 25 times more individuals than required, which was repeatedly questioned during the outbreak.

From quarantine to identifying and responding to a novel coronavirus with nonspecific symptoms, many of these challenges of the SARS outbreak hit close to home when we consider those of COVID-19. Each outbreak has its own particular features and this review touched upon just a fraction of what occurred, but we will continue to repeat the same mistakes if we cannot work outside the rigid box we have made for ourselves and if we persist with an intermittent attention to pandemic response.

References

1. Richard A. Stein, “Super-Spreaders in Infectious Diseases,” International Journal of Infectious Diseases 15, no. 8 (August 1, 2011): e510–13, https://doi.org/10.1016/j.ijid.2010.06.020.

2. Tomislav Svoboda et al., “Public Health Measures to Control the Spread of the Severe Acute Respiratory Syndrome during the Outbreak in Toronto,” New England Journal of Medicine 350, no. 23 (June 3, 2004): 2352–61, https://doi.org/10.1056/NEJMoa032111.

3. McDonald LC, Simor AE, Su IJ, et al. SARS in healthcare facilities, Toronto and Taiwan. Emerg Infect Dis. 2004;10(5):777-781. doi:10.3201/eid1005.030791

4. Malik Peiris et al, Severe Acute Respiratory Syndrome (John Wiley & Sons, 2008). P. 224.

5. General Accounting Office, “EMERGING INFECTIOUS DISEASES: Asian SARS-CoV-1 Outbreak Challenged International and National Responses,” Report to the Chairman, Subcommittee on Asia and the Pacific, Committee on International Relations, House of Representatives, April 2004, https://www.gao.gov/new.items/d04564.pdf.

6. “WHO | Chapter 5: SARS-CoV-1: Lessons from a New Disease,” WHO, accessed June 27, 2018, http://www.who.int/whr/2003/chapter5/en/index4.html.

7. Jacobs, “Rights and Quarantine During the SARS-CoV-1 Global Health Crisis.”

8. Government of Ontario, “The SARS-CoV-1 Commission Interim Report.”

9. “WHO | Update 95 - SARS-CoV-1: Chronology of a Serial Killer,” WHO, accessed June 28, 2018, http://www.who.int/csr/don/2003_07_04/en/.

10. Svoboda et al, “Public Health Measures to Control the Spread of the Severe Acute Respiratory Syndrome during the Outbreak in Toronto.”

11. Blendon et al, “The Public’s Response to Severe Acute Respiratory Syndrome in Toronto and the United States.”

12. Svoboda et al, “Public Health Measures to Control the Spread of the Severe Acute Respiratory Syndrome during the Outbreak in Toronto.”

13. Richard Schabas, “Severe Acute Respiratory Syndrome: Did Quarantine Help?,” The Canadian Journal of Infectious Diseases & Medical Microbiology 15, no. 4 (2004): 204.