POLICY REVIEW

Public Health Interventions and

SARS Spread, 2003
David M. Bell* and World Health Organization Working Group on Prevention
of International and Community Transmission of SARS1

The 2003 outbreak of severe acute respiratory syn- persons with fever at international borders and in public
drome (SARS) was contained largely through traditional places. After the outbreaks, WHO sought information to
public health interventions, such as finding and isolating help assess the effectiveness of interventions in preventing
case-patients, quarantining close contacts, and enhanced the transmission of SARS in the community and interna-
infection control. The independent effectiveness of meas-
tionally. Of particular interest was information on the
ures to “increase social distance” and wearing masks in
public places requires further evaluation. Limited data exist effectiveness of thermal scanning of travelers.
on the effectiveness of providing health information to trav-
elers. Entry screening of travelers through health declara- Methods
tions or thermal scanning at international borders had little Information was obtained by reviewing scientific liter-
documented effect on detecting SARS cases; exit screen- ature and surveying members of an informal WHO work-
ing appeared slightly more effective. The value of border ing group about preventing community and international
screening in deterring travel by ill persons and in building transmission of SARS. Members were surveyed with stan-
public confidence remains unquantified. Interventions to dardized questionnaires regarding measures taken in their
control global epidemics should be based on expert advice
countries and evaluation studies known to them.
from the World Health Organization and national authori-
ties. In the case of SARS, interventions at a country’s bor-
1The members of the World Health Organization (WHO) Working
ders should not detract from efforts to identify and isolate
Group are as follows: Ximena Aguilera, Ministerio de Salud,
infected persons within the country, monitor or quarantine
Santiago Chile; Roy Anderson, Imperial College London, United
their contacts, and strengthen infection control in health-
Kingdom; Dounia Bitar, Institut de Veille Sanitaire, Paris France;
care settings. Martin Cetron (with Pattie Simone), Centers for Disease Control
and Prevention, Atlanta, Georgia, USA; Chew Suok Kai (with
Benjamin K.W. Koh), Ministry of Health, Singapore; Clete
he 2003 outbreak of severe acute respiratory syndrome
T (SARS) is a modern example of containing a global
epidemic through traditional or nonmedical public health
DiGiovanni, Jr., Defense Threat Reduction Agency, Fort Belvoir,
Virginia, USA; Arlene King, Health Canada, Ottawa, Canada; Cindy
K-L Lai (with P.L. Ma), Department of Health, Hong Kong Special
interventions. The interventions included finding and iso- Administrative Region, China; Angus Nicoll (with Jane Leese),
lating case-patients; quarantining contacts; measures to Communicable Disease Surveillance Centre, London, United
Kingdom; Sonja Olsen, International Emerging Infections Program,
“increase social distance,” such as canceling mass gather- Nonthaburi, Thailand; Alice Sarradet, Direction Generale de la
ings and closing schools; recommending that the public Sante, Paris, France; Mingchang Song, General Administration of
augment personal hygiene and wear masks; and limiting Quality Supervision, Inspection and Quarantine, (AQSIQ), Beijing,
the spread of infection by domestic and international trav- China; Ron St. John (with Susan Courage), Health Canada,
elers, by issuing travel advisories and screening travelers Ottawa, Canada; Robert Steffen (with Leonie Prasad), University of
Zurich, Switzerland; Ih-Jen Su (with S.K. Lai), Taiwan Center for
at borders. Some measures were implemented pursuant to Disease Control, Taipei, Taiwan, China; WHO Staff in the
recommendations of the World Health Organization Department of Communicable Diseases Surveillance and
(WHO); others were implemented by governments on Response (CSR): Julie Hall, Beijing, China; Emmanuel
their own initiative. A novel technology, infrared scanning, Jesuthasan, Angela Merianos, Cathy Roth, Max Hardiman,
was used extensively in some countries to try to identify Geneva, Switzerland; Hitoshi Oshitani, Western Pacific Regional
Office, Manila, Philippines; and group facilitator: David Bell, WHO
(CSR) Geneva, Switzerland, and Centers for Disease Control and
*World Health Organization, Geneva, Switzerland Prevention, Atlanta, Georgia, USA.

1900 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 10, No. 11, November 2004
 Public Health Interventions and SARS

Preventing transmission in healthcare settings was not

addressed but had a major impact on preventing the trans-
mission of SARS into the community and internationally
(1,2).

Results

Local and National Interventions

Identifying Patients and Quarantining Contacts

Ascertaining and isolating case-patients, combined
with rapid identification and management of contacts, Figure. Severe acute respiratory syndrome cases in Singapore,
were highly effective in interrupting transmission in sev- February 25–May 5, 2003. Number of primary cases (gray) by
time from symptom onset to isolation, number of secondary cases
eral countries (1–6).2 For example, a study in Singapore
infected by such cases (black), and mean number of secondary
demonstrated a correlation between rapidly isolating cases per primary case. Reprinted with permission from Lipsitch
patients after onset of symptoms and a decreased number M, Cohen T, Cooper B, Robins JM, Ma S, James L, et al. Science
of secondary cases among their contacts (4) (Figure). 2003;300:1966–70. Copyright 2003 by the American Association
Contacts in these countries were placed in various forms for the Advancement of Science. http://www.sciencemag.org
of quarantine or, less commonly, monitored for symptoms
without confinement and isolated if and when symptoms toms. In several countries, quarantine was legally mandat-
emerged. The location of quarantine was usually at home ed and monitored by neighborhood support groups, police
but was sometimes at a designated residential facility and other workers, or video cameras in homes. In other
(e.g., for travelers, persons who did not wish to remain at areas, compliance was “requested,” but court orders were
home for fear of exposing their families, homeless per- issued for a small percentage of noncompliant persons.
sons, and noncompliant persons). In some cases, quaran- Reports indicate that SARS was diagnosed in 0.22% of
tined persons were allowed to leave the quarantine site quarantined contacts in China-Taiwan, 2.7% in China-
with the permission of local health authorities if they wore Hong Kong Special Administrative Region (SAR), and
masks and did not use public transportation or visit 3.8%–6.3% in China-Beijing. These different rates were
crowded public places. In at least one area, these restric- partly due to different criteria for placing persons in quar-
tions were applied to essential workers and termed “work antine. Contacts at highest risk (aside from healthcare
quarantine.” workers with certain unprotected patient care exposures)
Several respondents emphasized that the modern con- had been exposed to ill family members (6,9–11).
cept of quarantine differs greatly from quarantine in past Quarantine led to financial and psychosocial stresses,
centuries. Quarantine is most acceptable and arguably risk communication, compensation, and workforce
most effective when protecting the health and rights of staffing issues for persons, families, employers, and gov-
quarantined persons is emphasized. In previous centuries, ernments. Legal appeals and defiance of quarantine orders
sick and exposed persons were often locked up together were rare (2,6,8–13).
and received limited medical care. Moreover, quarantine The optimal management of contacts, stratified accord-
was sometimes applied in an arbitrary and discriminatory ing to risk of becoming ill, remains under discussion in
fashion, targeting lower socioeconomic classes and racial several countries, e.g., whether confinement is always
minorities. The modern concept emphasizes science-based needed or close monitoring of health status without con-
interventions with attention to the medical, material, and finement would suffice. Reports from Canada indicate that
mental health needs of quarantined persons and protecting the insidious onset of symptoms sometimes posed chal-
fundamental human rights. Exposed persons who are not lenges for clinicians and public health officials. “Timely
sick should be separated from symptomatic patients, mon- diagnosis and isolation of cases were sometimes hindered
itored for the minimum time necessary (e.g., one maxi- by delays in patient recognition of symptoms, obtaining
mum incubation period), and provided appropriate medical medical evaluation, and/or physician recognition of the
care at the first sign of illness during the monitoring peri- significance of symptoms, which occasionally waxed and
od. Quarantine may be applied to individual persons, to waned early in illness” (A. McGeer and D. Low, Mount
small groups, or, in extreme cases, to entire neighborhoods Sinai Hospital Toronto, pers. comm.). “In Toronto, some
or other geographic districts (“cordon sanitaire”) (7,8).
In the SARS epidemic, persons under quarantine were 2The term “isolation” is applied to ill persons; “quarantine” is
mostly confined at home and actively monitored for symp- applied to persons who have been exposed but are not ill.

Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 10, No. 11, November 2004 1901
POLICY REVIEW

healthcare workers continued to work without recognizing tires, and pedestrian walking zones. Little information
that they were ill, perhaps confusing their symptoms with exists on the effectiveness of disinfectant use in reducing
fatigue, despite daily screening and repeated messages not community or hospital transmission. In Hong Kong, disin-
to come to work if ill. This resulted in transmission to fecting living quarters thoroughly (not otherwise defined
patients and staff” (B. Henry, Toronto Public Health, pers. and reported retrospectively by telephone) appeared to be
comm.). protective (16).

Measures To Decrease Time from Symptom Measures for International Travel

Onset to Isolation of Patients
Public campaigns to accelerate reporting and evaluat- Travel Advisories
ing symptomatic patients appeared to decrease the interval Travel advisories (e.g., advice to postpone nonessential
between onset of symptoms and isolation of ill patients in travel) were issued by WHO and various governments. Air
several areas (3,4). Novel interventions included urging travel to areas affected by the advisories decreased dramat-
the entire population of affected areas to measure their ically during the epidemic (M.A. Hinayon and D. Gamper,
temperature at least once daily, fever telephone hotlines Airports Council International, communication to WHO),
(14), and fever evaluation clinics with appropriate infec- although the impact of advisories compared with other
tion control measures. Thermal scanning in public places sources of information to travelers, such as news media
was implemented in several areas where community trans- reports of SARS cases, is difficult to assess.
mission was suspected. Data on the effectiveness of this
practice are not available, but in Beijing thermal screening Measures for International Borders
was not an efficient way to detect cases among intercity Passive and active methods were used to provide infor-
travelers (5). mation and screen entering and exiting travelers. These
methods included signs, videos, public address announce-
Measures To Increase Social Distance ments, distributing health alert notices, administering ques-
Measures to increase social distance, e.g., canceling tionnaires to assess symptoms and possible exposure, visual
mass gatherings; closing schools, theaters, and public inspection to detect symptoms, and thermal scanning.
facilities; and requiring masks for all persons using public Few data exist on the relative effectiveness of methods
transport, working in restaurants, or entering hospitals, of providing information to travelers. Available data on the
were implemented in areas where extensive unlinked com- effectiveness of screening and other measures directed to
munity transmission of SARS coronavirus (SARS-CoV) travelers are sometimes difficult to interpret because they
was suspected. Many persons in these areas also chose to may not distinguish between entry and exit screening,
wear masks outside their homes. These measures were specify how many entering travelers were from affected
often applied simultaneously with other measures, includ- countries, distinguish the epidemic period from subse-
ing enhanced contact tracing, which makes their independ- quent, or include the number of SARS cases detected.
ent effectiveness difficult to assess. However the
simultaneous introduction of a variety of measures was Health Alert Notices to Entering Travelers
temporally associated with dramatic declines in new Combined data from Canada, China (mainland, Hong
SARS cases. A case-control study in Beijing found that Kong SAR, and Taiwan), France, Singapore, Switzerland,
wearing a mask more frequently in public places may have Thailand, and the United States indicate that approximately
been associated with increasing protection (15). Another 31 million travelers entering these countries received health
case-control study in China-Hong Kong found that using a alert notices. Of these, approximately 1.8 million were
mask “frequently” in public places, washing one’s hands reported as arriving from affected areas; this estimate is
>10 times per day, and “disinfecting living quarters thor- likely low given the difficulties in tracking travelers and the
oughly” appeared to be protective (16). The types of masks fact that many airline passengers change planes en route.
used were not specified. With the exception of the Amoy Inadequate data exist to evaluate the effect of distribution of
Gardens cluster in which SARS-CoV was apparently most of these notices. China-mainland reported distribut-
transmitted through accidentally produced aerosols of ing 450,000 notices and detecting four SARS cases that
sewage (17), SARS transmission in the community from may have been linked to the notices (M. Song, China Dept
aerosols or in social settings appeared to be rare. of Health and Quarantine Supervision and Management,
communication to WHO). Thailand printed l million
Disinfection notices; as a result 113 cases of illness (108 at airports, l at
In some areas, disinfectants were applied inside the a seaport, and 4 at land crossings) were detected. Twenty-
homes and vehicles of persons with SARS, ambulance four cases were suspected or probable SARS: all of which

1902 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 10, No. 11, November 2004
 Public Health Interventions and SARS

were detected at airports (S. Warintrawat, Ministry of Taiwan), and Singapore indicate that no cases of SARS
Public Health, Thailand, communication to WHO). were detected among >7 million people who underwent
thermal scanning at exit (Table 3) (S. Courage, Health
Entry Screening Canada, S.K. Lai, China-Taiwan Center for Disease
Preliminary data from a worldwide survey indicate that Control; P.L. Ma, Hong Kong SAR China Dept of Health;
among 72 patients with imported probable or confirmed and B.K.W. Koh, Singapore Ministry of Health, communi-
SARS cases, 30 (42%) had onset of symptoms before or on cations to WHO). In some areas, “stop lists” were used at
the same day as entry into the country and symptoms borders to prevent persons on isolation or quarantine lists
developed in 42 patients (58%) after entry (J. Jones, from exiting. Anecdotes suggest that exit screening may
United Kingdom Health Protection Agency, communica- have helped dissuade ill persons from traveling by air but
tion to WHO). SARS was diagnosed in a small percentage may have been more successful in dissuading local resi-
of persons who completed entry health declaration ques- dents from traveling abroad than in dissuading ill travelers
tionnaires in affected areas during the SARS epidemic. from attempting to return home.
(Table 1).
Results combined from Canada, China (including the Transmission on Commercial Aircraft
mainland and Hong Kong SAR), and Singapore indicate Five commercial international flights were associated
that no cases of SARS were detected by thermal scanning with transmission of SARS from patients with sympto-
among >35 million international travelers scanned at entry matic probable cases to passengers and crew (1).
during the SARS epidemic (Table 2; data for China-Hong Notification of exposed passengers and studies of transmis-
Kong SAR include travelers arriving from China-main- sion risk were greatly hampered by difficulties in identify-
land). Temperature screening of 13,839,500 travelers ing and tracing passenger contacts (19–23). In the most
entering or leaving Beijing by air, train, or automobile comprehensive investigation, involving three flights with
identified 5,097 patients with fever, of whom 12 had prob- extensive passenger tracing and laboratory confirmation of
able SARS. These 12 included 10 of 952,200 domestic air- index and secondary cases, a wide range of risk was noted
line passengers and 2 of 5,246,100 train passengers. None (Table 4). For flight 2, in which the secondary attack rate
of 275,600 international travelers who underwent temper- was 18.3%, the risk of infection was increased for persons
ature screening had SARS (5). seated close to the index patient, but most passengers who
In China-Taiwan, incoming travelers from affected became infected were seated farther away, even though
areas were quarantined; probable or suspected SARS was their individual risk was lower (19). In another study, one
diagnosed in 21 (0.03%) of 80,813. None of these 21 was person with SARS, who had difficulty breathing but was
detected by thermal scanning when they entered China- not coughing, infected two other passengers. One of these
Taiwan (9) (S.K. Lai, China-Taiwan Center for Disease sat in the row in front of the index patient but the other pas-
Control, pers. comm.). senger sat four rows, plus a passageway, behind and on the
opposite side of the plane (20). On nine flights arriving in
Exit Screening Singapore, the incidence of transmission from passengers
After WHO recommended exit screening on March 27, with SARS who had respiratory symptoms was estimated
2003 (18), no additional cases from airline travel were at 1 in 156 persons (21). A fourth study found no transmis-
documented from countries with screening. Combined sion to passengers seated near a patient who took multiple
data from China (Hong Kong SAR and Taiwan) indicate flights (22). In comparison, an influenzalike illness devel-
that among 1.8 million people who completed health ques- oped within 3 days in 72% of passengers in a plane contain-
tionnaires at exit, 1 probable case of SARS was detected. ing a person with symptomatic influenza and grounded for
Combined data from Canada, China (Hong Kong SAR and 3 hours without ventilation (24). The risk for transmission

Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 10, No. 11, November 2004 1903
POLICY REVIEW

of tuberculosis during a long flight was also increased the most cost-effective ways to accomplish this are uncer-
among, but not limited to, passengers seated close to a tain. The difficulties in identifying and tracing passengers
highly infectious index patient (25). exposed on aircraft highlight the need for public health
authorities to have a mechanism for rapid access to passen-
Discussion ger contact information. In the case of SARS, the data on
SARS-CoV was contained in human populations in border screening indicate that if resources are limited,
2003 largely by aggressive use of traditional public health interventions at a country’s international borders should
interventions (case finding and isolation, quarantine of not detract from efforts to identify and isolate infected per-
close contacts, and enhanced infection control measures in sons within the country, monitor and quarantine their close
settings where care was provided to persons with SARS, contacts appropriately, and strengthen infection control in
especially in healthcare facilities and homes). These meas- healthcare settings.
ures also contained a smaller SARS outbreak in 2004 that In retrospect, although SARS-CoV was transmitted pri-
originated from a laboratory-acquired infection (26). marily through the respiratory droplet route, certain epi-
Measures to decrease the interval between onset of symp- demiologic parameters facilitated its containment through
toms and isolation were effective in containing communi- public health interventions . Presymptomatic transmission
ty transmission. The independent effectiveness of general was not observed. Infectivity in most patients was low at
community measures to increase social distance (in addi- onset of illness and seemed to peak during week 2 of ill-
tion to contact tracing and quarantine) and improve ness in association with maximal respiratory symptoms,
hygiene and wearing masks in public places requires fur- when patients were often in the hospital. Virus transmis-
ther evaluation. sion was primarily by respiratory droplets, with little natu-
Limited information exists on the relative effectiveness ral airborne dissemination but some environmental spread.
of methods of providing information on SARS (or other With some important exceptions (Hotel M and Amoy
illnesses) to travelers. For inbound travelers who may have Gardens in Hong Kong), transmission occurred primarily
been exposed to SARS, such information should include in healthcare or household settings, with close person-to-
what to do if symptoms develop and the need to inform person contact. Cases among children were uncommon,
healthcare workers who provide care for them in advance and children did not seem to be involved in transmission.
to take appropriate precautions. Entry screening of travel- Although the reproductive number for SARS (R0, the aver-
ers by using health declarations or thermal scanning at age number of new cases resulting from a single infection
international borders had little documented impact in in a susceptible community) was approximately 2–4, con-
detecting SARS cases. Exit screening appeared only tact tracing was facilitated by its relatively long serial
slightly more effective; however, the possible value of interval (time between onset of symptoms in successive
these interventions in deterring travel by ill persons and patients in a chain of transmission: mean 8–10 days) and
building public and business confidence was not assessed. incubation period (median 4–5 days). Most infections did
Preventing passengers with SARS from boarding aircraft not lead to further transmission, although a small number
would likely have reduced transmission of infection, but of “super-spreading” events occurred in which single

1904 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 10, No. 11, November 2004
 Public Health Interventions and SARS

Disease Control and Prevention. He is a consultant to the World

Health Organization on the control of SARS and influenza.

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1906 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 10, No. 11, November 2004