Pang X, Zhu Z, Xu F, Guo J, Gong X, Liu D, Liu Z, Chin DP, Feikin DR. Evaluation of Control Measures Implemented in the Severe Acute Respiratory Syndrome Outbreak in Beijing, 2003. JAMA. 2003;290(24):3215-3221. doi:10.1001/jama.290.24.3215
Author Affiliations: Beijing Center for Disease Prevention and Control (Drs Pang, Gong, and Z. Liu, and Mr D. Liu), Beijing Municipal Health Bureau (Drs Zhu and Guo), and World Health Organization, China Office (Drs Xu, Chin, and Feikin), Beijing, People's Republic of China; and US Centers for Disease Control and Prevention, Atlanta, Ga (Drs Xu and Feikin).
Context Beijing, China, experienced the world's largest outbreak of severe acute
respiratory syndrome (SARS) beginning in March 2003, with the outbreak resolving
rapidly, within 6 weeks of its peak in late April. Little is known about the
control measures implemented during this outbreak.
Objective To describe and evaluate the measures undertaken to control the SARS
Design, Setting, and Participants Data were reviewed from standardized surveillance forms from SARS cases
(2521 probable cases) and their close contacts observed in Beijing between
March 5, 2003, and May 29, 2003. Procedures implemented by health authorities
were investigated through review of official documents and discussions with
public health officials.
Main Outcome Measures Timeline of major control measures; number of cases and quarantined
close contacts and attack rates, with changes in infection control measures,
management, and triage of suspected cases; and time lag between illness onset
and hospitalization with information dissemination.
Results Health care worker training in use of personal protective equipment
and management of patients with SARS and establishing fever clinics and designated
SARS wards in hospitals predated the steepest decline in cases. During the
outbreak, 30 178 persons were quarantined. Among 2195 quarantined close
contacts in 5 districts, the attack rate was 6.3% (95% confidence interval
[CI], 5.3%-7.3%), with a range of 15.4% (95% CI, 11.5%-19.2%) among spouses
to 0.36% (95% CI, 0%-0.77%) among work and school contacts. The attack rate
among quarantined household members increased with age from 5.0% (95% CI,
0%-10.5%) in children younger than 10 years to 27.6% (95% CI, 18.2%-37.0%)
in adults aged 60 to 69 years. Among almost 14 million people screened for
fever at the airport, train stations, and roadside checkpoints, only 12 were
found to have probable SARS. The national and municipal governments held 13
press conferences about SARS. The time lag between illness onset and hospitalization
decreased from a median of 5 to 6 days on or before April 20, 2003, the day
the outbreak was announced to the public, to 2 days after April 20 (P<.001).
Conclusions The rapid resolution of the SARS outbreak was multifactorial, involving
improvements in management and triage in hospitals and communities of patients
with suspected SARS and the dissemination of information to health care workers
and the public.
Beijing, China, experienced the largest outbreak of severe acute respiratory
syndrome (SARS) in the world with a total of 2521 reported probable cases.1- 3 The outbreak began March
5, 2003, with the importation of several cases among travelers from other
SARS-affected areas,4- 7 and
soon accelerated as multiple SARS cases occurred in health care facilities,
peaking in late April when more than 100 new patients with SARS were being
hospitalized daily.3,4 During
the first week of May, the number of new cases dropped steeply and then declined
steadily during the next few weeks, with the onset of the last probable case
on May 29, 2003. The World Health Organization removed Beijing from its list
of areas with recent local transmission and lifted its travel advisory on
June 24, 2003.8 The onset of the last case
occurred only 6 weeks after the peak of the outbreak. In this report, we summarize
the control measures taken to rapidly repress the outbreak in Beijing and
evaluate the effectiveness of some of these measures.
Beijing, capital of the People's Republic of China, has approximately
13.6 million people.9 The municipal health
system, which includes 466 nonmilitary hospitals and 85 000 health care
workers, is overseen by the Beijing Municipal Health Bureau, which reports
to the China Ministry of Health (MOH). Disease reporting, epidemic investigations,
and contact tracing are the responsibility of the section of the Beijing Municipal
Health Bureau called the Beijing Center for Disease Prevention and Control
(BCDC). Within the BCDC are 18 district Centers for Disease Prevention and
Control (DCDC), which are affiliated with community health centers.
Probable and suspect SARS case definitions were disseminated by the
MOH. Only probable cases were included in this study because all suspect cases
were ultimately excluded or reclassified as probable based on review of an
expert panel as part of the Beijing joint SARS leading group. The definition
of a probable SARS case changed slightly during the course of the outbreak
but always included clinical and epidemiological components. After May 3,
2003, probable cases were defined as meeting 1 of the 3 following categories:
close contact with a patient with SARS and symptoms and signs of febrile respiratory
illness and chest radiograph changes; visiting or residing in an area with
recent local transmission of SARS and symptoms and signs of febrile respiratory
illness and chest radiograph changes and lack of response to antibiotics;
or visiting or residing in an area with recent local transmission of SARS
and symptoms and signs of febrile respiratory illness and chest radiograph
changes and normal or decreased white blood cell count.4 Laboratory
testing for coronavirus was not part of the case definition.
Beijing municipal government guidelines defined close contacts of patients
with SARS as individuals who stayed in the same room as a patient with SARS
at home, work, or school; who directly contacted a patient with SARS by visiting,
caring for, transporting, or sharing an elevator; who were health care workers
in contact with a patient with SARS without wearing full personal protective
equipment (PPE); or who had other exposures to a patient with SARS deemed
risky by public health personnel (ie, contact with bodily secretions) in a
period from 3 to 14 days before the case's onset of symptoms (varied during
different phases of outbreak) to the time of last contact.
Descriptive data of control measures were obtained through review of
official documents and discussions with officials in the Beijing municipal
health bureau and the BCDC. Data on the number of probable SARS cases were
obtained from a standardized case report form issued by the MOH, which was
required to be completed and sent to the DCDC by the physician who first diagnosed
the SARS case. Public health personnel performed weekly onsite audits of hospitals
to ensure complete reporting of all SARS cases. Because date of onset was
missing for many cases, the reported date of hospitalization, which was missing
in only 3.5% of cases, was used to create the epidemic curve.
Summaries of the number of fever clinic visits were compiled by the
hospitals where the clinics were located and sent daily to both the DCDC and
BCDC. The number of people placed in quarantine was tracked by the DCDC and
reported daily to the BCDC.
Databases on close contacts from 5 districts (Changping, Chongwen, Dongcheng,
Shijingshan, and Xicheng) with the most complete records were merged for the
analysis of outcomes of quarantined close contacts. Information on close contacts
of SARS cases was obtained from a standardized data collection form issued
by the MOH. For each new SARS case, DCDC staff would interview the patient
in the hospital about their potential close contacts. Staff from the DCDC
or community health centers would find the close contacts, enforce quarantine,
and complete the close contact data collection forms, which were maintained
in a database at the DCDC. Close contacts who were already symptomatic when
contacted were not included in the quarantine database. Although close contacts
of suspect SARS cases were managed similarly to those of probable cases, they
were excluded in our analysis.
Databases at the BCDC and DCDCs were maintained in Microsoft Excel version
2002 (Microsoft Corporation, Redmond, Wash). Data analyses used SPSS version
11.0 (SPSS Inc, Chicago, Ill) and EPI Info version 6.02 (Centers for Disease
Control and Prevention, Atlanta, Ga). The χ2 test was used
to compare proportions and the Kruskal-Wallis test to compare median values.
The χ2 test for trend was used to compare attack rates by age.
The normal theory method for binomial parameters was used to calculate 95%
confidence intervals around attack rates. P<.05
was considered significant.
From March 5, 2003, to May 29, 2003, 2521 probable cases of SARS were
reported in Beijing (Figure 1).
It is unlikely that many patients hospitalized with SARS were not reported
because reporting SARS cases was mandatory and weekly audits of hospitalized
cases occurred. However, it is possible that some SARS cases were not counted
before mid-April when the extent of the outbreak was fully recognized. Of
the 2521 cases, 192 (7.6%) died.2 The median
(range) age of cases was 33 years (1-93 years), with less than 1% of cases
in children younger than 10 years, and 51% of cases were men.4 The
outbreak peaked on April 25, when 173 probable SARS cases were hospitalized.
On April 10, 3565 public health workers were mobilized to assist in
the outbreak management. On April 17, the mayor of Beijing established the
Beijing joint SARS leading group, which operated from an emergency command
center in a downtown hotel. At that time, the Beijing government began purchasing
emergency supplies both nationally and from abroad. Relevant local production
facilities were directed to shift production toward SARS-related supplies.
As of June 17, the following number of supplies had been distributed: 11 092 000
surgical masks, 758 000 gowns, 2 954 000 pairs of latex gloves,
621 000 shoe covers, 1 130 000 thermometers, and 302 tons of
chemical disinfectant (peracetic acid). In addition, 76 new ambulances, 79
new radiograph machines, and 759 mechanical ventilators were acquired.
Of SARS cases, 407 (16%) occurred in health care workers. In 1 hospital,
88 health care workers were infected and 3 other hospitals had more than 20
health care workers infected. All 4 hospitals were closed by May 4. The spread
of SARS virus among health care workers occurred more in the early part of
the outbreak. Before April 25, the peak day of hospitalization, 55% of all
health care worker cases had already been hospitalized compared with 45% of
non–health care worker cases (P<.001). Beginning
on April 18, 62 363 health care workers received training through in-person
courses, videotapes, and printed materials in the management of patients with
SARS, infection control, and the use of PPE. Two or 3 sets of gowns, gloves,
and masks (N95 and/or 12-layer cotton) were required, the outer layer being
removed and disposed of after contact with each patient with SARS. Goggles
were also required.
On April 27, all patients with SARS started to be placed together on
designated hospital wards. Hospitals also started to limit visitors at that
time. By May 8, all previously and newly diagnosed patients with SARS were
hospitalized in 16 hospitals designated exclusively for probable SARS cases
and 30 hospitals for suspected SARS cases. Negative pressure rooms were not
available in most Beijing hospitals. As recommended by Chinese authorities
and the World Health Organization–Beijing Joint Expert Team, rooms in
designated SARS hospitals were fitted with air extraction fans on windows
or walls that blew air from the room to the outside, either directly or through
air ducts. The primary direction of airflow was from the hospital into the
room and then to the outside, with the goal of 20% more air leaving the room
than entering it, and was assessed by observing the movement of smoke. A new
1000-bed SARS hospital was built in 7 days by the Beijing municipal government
and completed on May 1, after which it treated 40% of Beijing's patients with
probable SARS. No health care workers contracted SARS at this new hospital.
After this hospital's completion, the designated SARS hospitals had a capacity
of 6700 beds with 3400 (51%) occupied at the height of the outbreak.
On April 17, 123 fever clinics were set up in all secondary and tertiary
hospitals in Beijing. However, because some fever clinics were part of emergency
departments or health centers where afebrile patients went for medical care,
transmission of SARS was suspected to have occurred in some clinics. On May
6, the number of fever clinics decreased to 66, all of which were required
to be separated from other patient care areas, staffed by trained personnel
wearing full PPE, have individual examination rooms with outward-blowing extraction
fans, and rooms for overnight medical observation. Fever clinic patients included
patients with febrile respiratory or influenza-like illnesses sent from community
physicians and quarantine sites, as well as self-referrals. All persons who
visited the fever clinics had a physical examination, white blood cell count,
and chest radiograph.
Data became available on fever clinics after the establishment of the
66 designated clinics on May 6, 2003. Between May 7 and June 9, there were
65 321 fever clinic visits, with an average of 1921 visits per day. During
this time, 7457 (11%) visits resulted in overnight medical observation. From
May 17, the first day information was available on outcome of fever clinic
visits, to June 9, 47 probable cases were identified in the fever clinics,
which were 0.1% of all visits but accounted for 84% of probable cases hospitalized
during that period in Beijing.
The DCDC or community health centers were responsible for reaching all
reported close contacts of patients hospitalized with SARS and issuing quarantine
orders by telephone within 1 hour of notification about the case. If unable
to reach the close contact, local police were notified to help find the individuals.
Quarantine for close contacts was enforced for 14 days from the last contact
with the patient according to national guidelines, which were based on data
from the prior SARS outbreak in Guangdong Province that began in November
2002. The majority of close contacts were quarantined at home (60%) with the
rest being quarantined at designated sites, which included hotels, universities,
and construction work sites. Masks were not required to be worn by quarantined
persons within the quarantine sites. Quarantined persons were unable to leave
the site of quarantine, except for rare circumstances like funerals, during
which they were required to wear masks. Community health workers and volunteers
brought quarantined individuals food and other essential supplies, paid for
mostly by the municipality. Only authorized public health or medical workers
could enter the quarantined site and were required to wear full PPE. Community
committees mobilized neighbors to support quarantined persons through gestures,
such as giving flowers and comforting letters. When breaches in quarantine
were observed, community members could call a SARS hotline to report the incident.
The police could enforce quarantine if necessary according to national and
municipal regulations; however, such action was not required during the outbreak.
All quarantined persons were required to monitor their temperatures twice
daily. A community health worker collected fever logs daily. Symptomatic persons
were either sent to a fever clinic or evaluated by health care staff in mobile
SARS evaluation vans.
By July 1, a total of 30 178 persons (0.22% of the Beijing population)
had been quarantined. The number of people in quarantine peaked on May 2 at
more than 11 000 people (Figure 2).
Several instances of mass quarantine were instituted, including 4 hospitals
(2643 people), 2 universities (517 students), and 7 construction sites (1434
In the 5 districts in which close contact data were further analyzed
(total population 2.6 million [19% of Beijing's population]), there were 582
cases who reported 2195 close contacts, with a mean 3.8 contacts per case
(range, 1-80). Of the 2195 contacts, 2120 (96.6%) were located, quarantined,
and included in the database. Of the remaining 75, 38 were not quarantined,
mostly because they were exposed before standardized criteria for quarantine
were enforced, and 37 had incomplete records. However, these 75 cases were
included in the analysis of close contacts because the relationship with the
patient with SARS was often known by report of the case-patients, as was the
clinical outcome through matching the names of the close contacts with the
SARS case report forms. The overall attack rate for becoming a probable case
among close contacts was 6.3% (range by district, 2.9%-9.7%). The attack rate
was highest among spouses (15.4%), other household members (8.8%), and nonhousehold
relatives (11.6%) (Table 1). The
attack rate among work and school contacts was low (0.36%). Among spouses,
other household members, and nonhousehold relatives (n = 1162), the attack
rate increased with the age of the close contact, from 5.0% in children younger
than 10 years to 27.6% in adults aged 60 to 69 years (Table 2). The attack rate decreased from 22.0% among those quarantined
during April 1 to April 15 to 1.1% during May 16 to May 31. A total of 42%
of close contacts were put into quarantine on the same day and most (74%)
were isolated within 2 days of the day of hospitalization of the related case.
Among 206 close contacts whose last contact with a patient with SARS was before
the patient's symptom onset, 4 (1.9%) developed SARS. For 2 persons, the last
reported contact was 1 day before the patient's onset of symptoms. For the
other 2, the last contact was 5 days before the patient's symptom onset; however,
both contacts occurred in a hospital where the patient was being treated for
an illness before contracting SARS, so that the transmission of SARS might
have been from other hospitalized patients with SARS.
On April 26, all sites of public entertainment (theaters, bars, libraries,
and indoor sports facilities) were closed. By the time these places began
opening again during the second week in June, 3500 public places had been
closed. Restaurants were never ordered to close, although patronage was much
reduced during the height of the outbreak. Of the 68 universities in Beijing,
22 (32%) cancelled classes. All public elementary, middle, and high schools
(n = 2610) were closed on April 24, not reopening again in some cases until
early July. In addition, universities, construction sites, and prisons stopped
the entry of all visitors and many residential communities and business places
screened visitors for fever at entry.
In late April, fever checks were instituted at the Beijing airport,
major train stations, and all 71 roads connecting Beijing to other areas.
Infrared thermometers were used to screen passengers, followed up by axillary
thermometers on those found to be febrile on screening. As of June 30, of
almost 14 million people screened at these sites, only 12 probable cases of
SARS were identified (Table 3).
The scope of the Beijing outbreak was announced in a press conference
given by the executive vice-minister of health on April 20. Subsequently,
the MOH participated in 4 press conferences about SARS and the Beijing municipal
government had 9 press conferences. Many billboards, bus advertisements, and
traditional red neighborhood banners educated and motivated the public to
protect themselves and fight together to control SARS. Beijing television
ran daily 2-hour educational programs about SARS. The BCDC started an informational
24-hour SARS hotline on April 8. At its peak, the hotline received 11 000
calls per day. In addition, the Beijing municipal health bureau conducted
6672 SARS seminars in the communities and distributed 8 280 000
copies of educational materials ranging from pamphlets to compact disks. The
importance of information dissemination is suggested by the observation that
the time lag between symptom onset and hospitalization decreased significantly
during the outbreak from a median of 5 to 6 days before the outbreak was made
public on April 20 to 2 days afterward (Table 4).
The SARS outbreak in Beijing was notable for its acceleration, magnitude,
and rapid resolution. There are several likely reasons for the size of the
outbreak: multiple imported cases, lack of knowledge about hospital spread,
lack of awareness about proper PPE, delays in hospitalizing patients with
symptoms, the population density of Beijing, and a failure to communicate
the problem to hospitals and the public early enough. With these initial disadvantages,
the prompt resolution of the Beijing outbreak was surprising and impressive.
Beijing rapidly implemented multiple measures to control the SARS outbreak.
Similar to other SARS-affected areas, a large part of the Beijing outbreak
occurred in hospitals.10- 13 This
was particularly true early on as suggested by the number of health care workers
infected. Part of the reason for the decrease in cases among health care workers
was likely the emphasis on training and guidelines on infection control and
use of PPE after April 18. The effectiveness of these interventions is highlighted
by the fact that no health care workers contracted SARS at the new 1000-bed
SARS hospital that opened May 1. In addition to health care workers, many
patients without SARS and visitors to the hospital were likely infected by
patients with SARS, as observed in other outbreaks.10,12 The
institution of improved triage, limitation of visitors, and designated SARS
wards likely led to a decrease in such in-hospital exposures. The hospitals
designated to SARS began to be established in late April and by May 8, all
patients with SARS were hospitalized in such hospitals. Designated hospitals
had the advantage of ensuring proper infection control practices, unidirectional
airflow rooms, and proper patient triage and flow. However, the earlier decrease
in hospital-based infections was likely because of control measures implemented
in general hospitals, such as the use of PPE and grouping of patients with
SARS on certain wards, because by May 8 the outbreak was already waning. In
addition, the establishment of designated fever clinics identified the majority
of new cases (84%) late in the outbreak. The earlier implementation of dedicated
fever clinics, separated from general medical care areas, might have stemmed
some of the transmission earlier in the outbreak.
Rigorous quarantine measures in Beijing were possible through both community-based
and governmental involvement. Some categories of quarantined close contacts,
such as family members, had much higher attack rates than others, such as
school and workplace contacts. The high attack rate among family members might
partially reflect contact with patients with SARS not just at home but at
the hospital while visiting their ill relatives. Elderly close contacts had
significantly higher attack rates than did children, although it is unclear
if this is because of differences in the type of contact with the case, susceptibility
to SARS, or the likelihood of developing symptoms after infection. The attack
rate among quarantined persons was significantly higher in Beijing than in
Taiwan, where among 50 139 quarantined close contacts the attack rate,
even for family members of patients with SARS, was less than 1%.14,15 The
reasons for this difference might be because of differences in the case definitions
of SARS, the higher incidence of SARS in Beijing, and the fact that only close
contacts of probable SARS cases were included in our analysis, whereas in
the Taiwan analysis contacts of both probable and suspected cases were included.
Who should be quarantined during a SARS outbreak likely depends on several
factors, such as resource availability, ability to mobilize public health
personnel, and societal acceptability. Public health departments must weigh
these factors in setting quarantine guidelines. For example, in smaller outbreaks
or when resources are limited, public health authorities might consider active
but nonquarantined surveillance in lower-risk settings, such as workplaces
and schools, and among those whose contact with patients with SARS was only
during the asymptomatic incubation phase.
In retrospect, several control measures undertaken by the Beijing municipality
seemed to have less direct impact in resolving the outbreak; however, this
was not known at the time of their implementation in the face of an accelerating
outbreak of an unknown disease. The screening at points of transportation
required a large amount of human and financial resources to maintain but identified
very few cases of SARS. Such measures, however, might have prevented SARS
cases indirectly by persuading symptomatic people to stay home. Moreover,
these checkpoints assured the local as well as international community that
proactive steps were being made toward controlling the outbreak. Second, the
closing of the public schools for more than a month likely had a minimal effect
on the prevention of SARS because of the low attack rate among schoolmates
and the rarity of pediatric SARS in Beijing, as observed in other SARS-affected
the closing of schools may have contributed to the widespread self-quarantine
that occurred in Beijing in early May, when the streets were virtually empty.
Besides these specific control measures, a general increase in the awareness
about SARS played an important role in controlling the outbreak. Early in
the outbreak before information about the number of patients with SARS in
the city was disseminated, the outbreak amplified because of underrecognition
and mismanagement of patients with SARS in both the hospitals and the community.
The control of the outbreak followed improvements in communication and awareness
among health care workers, public health personnel, and the general public,
as suggested by the decrease in the time between illness onset and hospitalization
as the outbreak progressed.
Our analysis had several limitations. Because of the simultaneous and
overlapping implementation of multiple control measures, it was difficult
to pinpoint which one or several interventions were the most effective. Evaluation
of the control measures was further complicated by the lag of at least an
incubation period between implementation and effect. Laboratory testing for
SARS coronavirus infection was not widely available during the outbreak in
Beijing and was not part of the SARS case definition; therefore, circulation
of other agents causing febrile respiratory illness in 1 or more of the districts
in which quarantine was evaluated might have led to SARS attack rates that
were falsely elevated. The 5 districts selected to evaluate contact tracing
and quarantine might not have been representative of all of Beijing. Three
districts were urban and 2 suburban, which might have overrepresented urban
Beijing because of the 18 districts in Beijing, 8 are urban and 10 suburban.
Attack rates tended to be higher in urban districts because of the presence
of more hospitals and a greater density of people.
The multiple control measures implemented in Beijing likely led to the
rapid resolution of the SARS outbreak. Improvements in infection control practices,
use of PPE, grouping of patients with SARS in the hospital, establishment
of designated fever clinics, quarantine of high-risk close contacts, and improved
public information and awareness of SARS likely played important roles in
controlling the outbreak. Some interventions, in retrospect, such as quarantine
of low-risk contacts and fever checks at transportation sites, seemed to have
less direct impact in curbing the outbreak. The lessons learned from controlling
this outbreak can hopefully serve to inform future responses to SARS, if it
were to reemerge in Beijing or elsewhere.