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ORIGINAL CONTRIBUTION

Evaluation of Control Measures Implemented


in the Severe Acute Respiratory Syndrome
Outbreak in Beijing, 2003
Xinghuo Pang, MD Context Beijing, China, experienced the world’s largest outbreak of severe acute res-
Zonghan Zhu, MD piratory syndrome (SARS) beginning in March 2003, with the outbreak resolving rap-
idly, within 6 weeks of its peak in late April. Little is known about the control mea-
Fujie Xu, MD, PhD
sures implemented during this outbreak.
Jiyong Guo, MD, MS Objective To describe and evaluate the measures undertaken to control the SARS
Xiaohong Gong, MD outbreak.
Donglei Liu, MS Design, Setting, and Participants Data were reviewed from standardized sur-
veillance forms from SARS cases (2521 probable cases) and their close contacts ob-
Zejun Liu, MD
served in Beijing between March 5, 2003, and May 29, 2003. Procedures imple-
Daniel P. Chin, MD mented by health authorities were investigated through review of official documents
Daniel R. Feikin, MD, MSPH and discussions with public health officials.
Main Outcome Measures Timeline of major control measures; number of cases

B
EIJING, CHINA, EXPERIENCED THE and quarantined close contacts and attack rates, with changes in infection control mea-
largest outbreak of severe acute sures, management, and triage of suspected cases; and time lag between illness onset
respiratory syndrome (SARS) in and hospitalization with information dissemination.
the world with a total of 2521 Results Health care worker training in use of personal protective equipment and man-
reported probable cases.1-3 The out- agement of patients with SARS and establishing fever clinics and designated SARS wards
break began March 5, 2003, with the im- in hospitals predated the steepest decline in cases. During the outbreak, 30178 per-
portation of several cases among trav- sons were quarantined. Among 2195 quarantined close contacts in 5 districts, the at-
elers from other SARS-affected areas,4-7 tack rate was 6.3% (95% confidence interval [CI], 5.3%-7.3%), with a range of 15.4%
and soon accelerated as multiple SARS (95% CI, 11.5%-19.2%) among spouses to 0.36% (95% CI, 0%-0.77%) among work
cases occurred in health care facilities, and school contacts. The attack rate among quarantined household members in-
creased with age from 5.0% (95% CI, 0%-10.5%) in children younger than 10 years
peaking in late April when more than
to 27.6% (95% CI, 18.2%-37.0%) in adults aged 60 to 69 years. Among almost 14
100 new patients with SARS were being million people screened for fever at the airport, train stations, and roadside check-
hospitalized daily.3,4 During the first points, only 12 were found to have probable SARS. The national and municipal gov-
week of May, the number of new cases ernments held 13 press conferences about SARS. The time lag between illness onset
dropped steeply and then declined and hospitalization decreased from a median of 5 to 6 days on or before April 20, 2003,
steadily during the next few weeks, with the day the outbreak was announced to the public, to 2 days after April 20 (P⬍.001).
the onset of the last probable case on Conclusions The rapid resolution of the SARS outbreak was multifactorial, involv-
May 29, 2003. The World Health Orga- ing improvements in management and triage in hospitals and communities of pa-
nization removed Beijing from its list of tients with suspected SARS and the dissemination of information to health care work-
areas with recent local transmission and ers and the public.
lifted its travel advisory on June 24, JAMA. 2003;290:3215-3221 www.jama.com
2003.8 The onset of the last case oc-
curred only 6 weeks after the peak of the Author Affiliations: Beijing Center for Disease Pre- (Drs Xu and Feikin).
outbreak. In this report, we summarize vention and Control (Drs Pang, Gong, and Z. Liu, Corresponding Author and Reprints: Daniel R. Feikin,
and Mr D. Liu), Beijing Municipal Health Bureau MD, MSPH, Respiratory Diseases Branch, Division of
(Drs Zhu and Guo), and World Health Organiza- Bacterial and Mycotic Diseases, National Center for
See also pp 3222, 3229, and 3251 tion, China Office (Drs Xu, Chin, and Feikin), Infectious Diseases, Centers for Disease Control and
and Patient Page. Beijing, People’s Republic of China; and US Centers Prevention, 1600 Clifton Rd, Mailstop C23, Atlanta,
for Disease Control and Prevention, Atlanta, Ga GA 30333 (e-mail: drf0@cdc.gov).

©2003 American Medical Association. All rights reserved. (Reprinted) JAMA, December 24/31, 2003—Vol 290, No. 24 3215

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CONTROL MEASURES IMPLEMENTED IN THE SARS OUTBREAK

the control measures taken to rapidly re- Beijing municipal government guide- interview the patient in the hospital
press the outbreak in Beijing and evalu- lines defined close contacts of patients about their potential close contacts. Staff
ate the effectiveness of some of these with SARS as individuals who stayed in from the DCDC or community health
measures. the same room as a patient with SARS centers would find the close contacts,
at home, work, or school; who di- enforce quarantine, and complete the
METHODS rectly contacted a patient with SARS by close contact data collection forms,
Setting and Definitions visiting, caring for, transporting, or which were maintained in a database
Beijing, capital of the People’s Repub- sharing an elevator; who were health at the DCDC. Close contacts who were
lic of China, has approximately 13.6 care workers in contact with a patient already symptomatic when contacted
million people.9 The municipal health with SARS without wearing full per- were not included in the quarantine da-
system, which includes 466 nonmili- sonal protective equipment (PPE); or tabase. Although close contacts of sus-
tary hospitals and 85 000 health care who had other exposures to a patient pect SARS cases were managed simi-
workers, is overseen by the Beijing Mu- with SARS deemed risky by public larly to those of probable cases, they
nicipal Health Bureau, which reports to health personnel (ie, contact with were excluded in our analysis.
the China Ministry of Health (MOH). bodily secretions) in a period from 3 to
Disease reporting, epidemic investiga- 14 days before the case’s onset of symp- Data Analysis
tions, and contact tracing are the re- toms (varied during different phases of Databases at the BCDC and DCDCs
sponsibility of the section of the Bei- outbreak) to the time of last contact. were maintained in Microsoft Excel ver-
jing Municipal Health Bureau called the sion 2002 (Microsoft Corporation, Red-
Beijing Center for Disease Prevention Data Collection mond, Wash). Data analyses used SPSS
and Control (BCDC). Within the BCDC Descriptive data of control measures version 11.0 (SPSS Inc, Chicago, Ill) and
are 18 district Centers for Disease Pre- were obtained through review of offi- EPI Info version 6.02 (Centers for Dis-
vention and Control (DCDC), which cial documents and discussions with of- ease Control and Prevention, Atlanta,
are affiliated with community health ficials in the Beijing municipal health Ga). The ␹2 test was used to compare
centers. bureau and the BCDC. Data on the proportions and the Kruskal-Wallis test
Probable and suspect SARS case defi- number of probable SARS cases were to compare median values. The ␹2 test
nitions were disseminated by the MOH. obtained from a standardized case re- for trend was used to compare attack
Only probable cases were included in port form issued by the MOH, which rates by age. The normal theory method
this study because all suspect cases were was required to be completed and sent for binomial parameters was used to cal-
ultimately excluded or reclassified as to the DCDC by the physician who first culate 95% confidence intervals around
probable based on review of an expert diagnosed the SARS case. Public health attack rates. P⬍.05 was considered sig-
panel as part of the Beijing joint SARS personnel performed weekly onsite au- nificant.
leading group. The definition of a prob- dits of hospitals to ensure complete re-
able SARS case changed slightly dur- porting of all SARS cases. Because date RESULTS
ing the course of the outbreak but of onset was missing for many cases, the Timeline of Outbreak
always included clinical and epidemio- reported date of hospitalization, which and Control Measures
logical components. After May 3, 2003, was missing in only 3.5% of cases, was From March 5, 2003, to May 29, 2003,
probable cases were defined as meet- used to create the epidemic curve. 2521 probable cases of SARS were
ing 1 of the 3 following categories: close Summaries of the number of fever reported in Beijing (FIGURE 1). It is
contact with a patient with SARS and clinic visits were compiled by the hos- unlikely that many patients hospital-
symptoms and signs of febrile respira- pitals where the clinics were located and ized with SARS were not reported
tory illness and chest radiograph sent daily to both the DCDC and BCDC. because reporting SARS cases was
changes; visiting or residing in an area The number of people placed in quar- mandatory and weekly audits of hospi-
with recent local transmission of SARS antine was tracked by the DCDC and talized cases occurred. However, it is
and symptoms and signs of febrile res- reported daily to the BCDC. possible that some SARS cases were
piratory illness and chest radiograph Databases on close contacts from 5 not counted before mid-April when
changes and lack of response to anti- districts (Changping, Chongwen, the extent of the outbreak was fully
biotics; or visiting or residing in an area Dongcheng, Shijingshan, and Xicheng) recognized. Of the 2521 cases, 192
with recent local transmission of SARS with the most complete records were (7.6%) died.2 The median (range) age
and symptoms and signs of febrile res- merged for the analysis of outcomes of of cases was 33 years (1-93 years),
piratory illness and chest radiograph quarantined close contacts. Informa- with less than 1% of cases in children
changes and normal or decreased white tion on close contacts of SARS cases was younger than 10 years, and 51% of
blood cell count.4 Laboratory testing for obtained from a standardized data col- cases were men.4 The outbreak peaked
coronavirus was not part of the case lection form issued by the MOH. For on April 25, when 173 probable SARS
definition. each new SARS case, DCDC staff would cases were hospitalized.
3216 JAMA, December 24/31, 2003—Vol 290, No. 24 (Reprinted) ©2003 American Medical Association. All rights reserved.

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CONTROL MEASURES IMPLEMENTED IN THE SARS OUTBREAK

Emergency Infrastructure care worker cases had already been hos- than entering it, and was assessed by
On April 10, 3565 public health work- pitalized compared with 45% of non– observing the movement of smoke. A
ers were mobilized to assist in the out- health care worker cases (P⬍.001). Be- new 1000-bed SARS hospital was built
break management. On April 17, the ginning on April 18, 62363 health care in 7 days by the Beijing municipal gov-
mayor of Beijing established the Bei- workers received training through in- ernment and completed on May 1, af-
jing joint SARS leading group, which person courses, videotapes, and printed ter which it treated 40% of Beijing’s pa-
operated from an emergency com- materials in the management of pa- tients with probable SARS. No health
mand center in a downtown hotel. At tients with SARS, infection control, and care workers contracted SARS at this
that time, the Beijing government be- the use of PPE. Two or 3 sets of gowns, new hospital. After this hospital’s
gan purchasing emergency supplies gloves, and masks (N95 and/or 12- completion, the designated SARS hos-
both nationally and from abroad. Rel- layer cotton) were required, the outer pitals had a capacity of 6700 beds with
evant local production facilities were di- layer being removed and disposed of af- 3400 (51%) occupied at the height of
rected to shift production toward SARS- ter contact with each patient with SARS. the outbreak.
related supplies. As of June 17, the Goggles were also required.
following number of supplies had been On April 27, all patients with SARS Fever Clinics
distributed: 11092000 surgical masks, started to be placed together on desig- On April 17, 123 fever clinics were set
758 000 gowns, 2 954 000 pairs of nated hospital wards. Hospitals also up in all secondary and tertiary hospi-
latex gloves, 621 000 shoe covers, started to limit visitors at that time. By tals in Beijing. However, because some
1130000 thermometers, and 302 tons May 8, all previously and newly diag- fever clinics were part of emergency de-
of chemical disinfectant (peracetic nosed patients with SARS were hospi- partments or health centers where afe-
acid). In addition, 76 new ambu- talized in 16 hospitals designated ex- brile patients went for medical care,
lances, 79 new radiograph machines, clusively for probable SARS cases and transmission of SARS was suspected to
and 759 mechanical ventilators were 30 hospitals for suspected SARS cases. have occurred in some clinics. On May
acquired. Negative pressure rooms were not avail- 6, the number of fever clinics de-
able in most Beijing hospitals. As rec- creased to 66, all of which were re-
Medical Sector Interventions ommended by Chinese authorities and quired to be separated from other pa-
Of SARS cases, 407 (16%) occurred in the World Health Organization– tient care areas, staffed by trained
health care workers. In 1 hospital, 88 Beijing Joint Expert Team, rooms in personnel wearing full PPE, have indi-
health care workers were infected and designated SARS hospitals were fitted vidual examination rooms with out-
3 other hospitals had more than 20 with air extraction fans on windows or ward-blowing extraction fans, and
health care workers infected. All 4 hos- walls that blew air from the room to the rooms for overnight medical observa-
pitals were closed by May 4. The spread outside, either directly or through air tion. Fever clinic patients included pa-
of SARS virus among health care work- ducts. The primary direction of air- tients with febrile respiratory or influ-
ers occurred more in the early part of flow was from the hospital into the enza-like illnesses sent from community
the outbreak. Before April 25, the peak room and then to the outside, with the physicians and quarantine sites, as well
day of hospitalization, 55% of all health goal of 20% more air leaving the room as self-referrals. All persons who vis-

Figure 1. Epidemic Curve for Beijing SARS Outbreak and Timeline of Major Control Measures From March 5 to May 29, 2003

22 Universities and 2610 Schools Closed (Apr 24) Libraries, Bars, Theaters Closed (Apr 26)

Fever Checks at Airports Begin (Apr 22) Start to Group Patients With SARS in
Quarantine of Close Contacts (Apr 21) Designated Wards (Apr 27)
200
Outbreak Announced Publicly by New 1000-Bed SARS Hospital
Government (Apr 20) Opens (May 1)
150
No. of Probable Cases

HCW Training in PPE and Management of MOH Infection Control


Patients With SARS (Apr 18) Guidelines (May 4)

100 Joint SARS Group Formed, Fever Clinics 66 Designated Fever


Open (Apr 17) Clinics (May 6)

SARS Made Reportable (Apr 10) All Patients With SARS


50 Contact Tracing Begins (Apr 9) in Designated Hospitals
(May 8)

0
Mar 7 Mar 14 Mar 21 Mar 28 Apr 4 Apr 11 Apr 18 Apr 25 May 2 May 9 May 16 May 23 May 30

Date of Hospitalization

SARS indicates severe acute respiratory syndrome; HCW, health care worker; PPE, personal protective equipment; MOH, China Ministry of Health.

©2003 American Medical Association. All rights reserved. (Reprinted) JAMA, December 24/31, 2003—Vol 290, No. 24 3217

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CONTROL MEASURES IMPLEMENTED IN THE SARS OUTBREAK

at more than 11000 people (FIGURE 2).


Figure 2. Persons Quarantined for SARS in Beijing From March 27 to June 23, 2003
Several instances of mass quarantine
1800 12 000 were instituted, including 4 hospitals
No. of Persons Starting Quarantine
(2643 people), 2 universities (517

Total Persons Under Quarantine


1600
Persons Starting Quarantine

Total No. of Persons Under Quarantine 10 000


1400 students), and 7 construction sites
1200 8000 (1434 workers).
1000 In the 5 districts in which close con-
6000
800 tact data were further analyzed (total
600 4000 population 2.6 million [19% of Bei-
400 jing’s population]), there were 582
2000
200 cases who reported 2195 close con-
0 0 tacts, with a mean 3.8 contacts per
Mar Apr Apr Apr Apr May May May May May Jun Jun Jun Jun case (range, 1-80). Of the 2195 con-
27 3 10 17 24 1 8 15 22 29 5 12 19 23
tacts, 2120 (96.6%) were located,
Date
quarantined, and included in the data-
SARS indicates severe acute respiratory syndrome. base. Of the remaining 75, 38 were not
quarantined, mostly because they were
ited the fever clinics had a physical ex- cluded hotels, universities, and con- exposed before standardized criteria
amination, white blood cell count, and struction work sites. Masks were not for quarantine were enforced, and 37
chest radiograph. required to be worn by quarantined per- had incomplete records. However,
Data became available on fever clin- sons within the quarantine sites. Quar- these 75 cases were included in the
ics after the establishment of the 66 des- antined persons were unable to leave analysis of close contacts because the
ignated clinics on May 6, 2003. Be- the site of quarantine, except for rare relationship with the patient with
tween May 7 and June 9, there were circumstances like funerals, during SARS was often known by report of
65321 fever clinic visits, with an aver- which they were required to wear the case-patients, as was the clinical
age of 1921 visits per day. During this masks. Community health workers and outcome through matching the names
time, 7457 (11%) visits resulted in over- volunteers brought quarantined indi- of the close contacts with the SARS
night medical observation. From May viduals food and other essential sup- case report forms. The overall attack
17, the first day information was avail- plies, paid for mostly by the munici- rate for becoming a probable case
able on outcome of fever clinic visits, pality. Only authorized public health among close contacts was 6.3% (range
to June 9, 47 probable cases were iden- or medical workers could enter the by district, 2.9%-9.7%). The attack
tified in the fever clinics, which were quarantined site and were required to rate was highest among spouses
0.1% of all visits but accounted for 84% wear full PPE. Community commit- (15.4%), other household members
of probable cases hospitalized during tees mobilized neighbors to support (8.8%), and nonhousehold relatives
that period in Beijing. quarantined persons through ges- (11.6%) (TABLE 1). The attack rate
tures, such as giving flowers and com- among work and school contacts was
Quarantine forting letters. When breaches in quar- low (0.36%). Among spouses, other
The DCDC or community health cen- antine were observed, community household members, and nonhouse-
ters were responsible for reaching all re- members could call a SARS hotline to hold relatives (n = 1162), the attack
ported close contacts of patients hos- report the incident. The police could en- rate increased with the age of the close
pitalized with SARS and issuing force quarantine if necessary accord- contact, from 5.0% in children
quarantine orders by telephone within ing to national and municipal regula- younger than 10 years to 27.6% in
1 hour of notification about the case. tions; however, such action was not adults aged 60 to 69 years (TABLE 2).
If unable to reach the close contact, lo- required during the outbreak. All quar- The attack rate decreased from 22.0%
cal police were notified to help find the antined persons were required to moni- among those quarantined during April
individuals. Quarantine for close con- tor their temperatures twice daily. A 1 to April 15 to 1.1% during May 16 to
tacts was enforced for 14 days from the community health worker collected fe- May 31. A total of 42% of close con-
last contact with the patient according ver logs daily. Symptomatic persons tacts were put into quarantine on the
to national guidelines, which were were either sent to a fever clinic or same day and most (74%) were iso-
based on data from the prior SARS out- evaluated by health care staff in mo- lated within 2 days of the day of hospi-
break in Guangdong Province that be- bile SARS evaluation vans. talization of the related case. Among
gan in November 2002. The majority By July 1, a total of 30178 persons 206 close contacts whose last contact
of close contacts were quarantined at (0.22% of the Beijing population) had with a patient with SARS was before
home (60%) with the rest being quar- been quarantined. The number of the patient’s symptom onset, 4 (1.9%)
antined at designated sites, which in- people in quarantine peaked on May 2 developed SARS. For 2 persons, the
3218 JAMA, December 24/31, 2003—Vol 290, No. 24 (Reprinted) ©2003 American Medical Association. All rights reserved.

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CONTROL MEASURES IMPLEMENTED IN THE SARS OUTBREAK

last reported contact was 1 day before ners educated and motivated the pub- formation dissemination is suggested by
the patient’s onset of symptoms. For lic to protect themselves and fight the observation that the time lag be-
the other 2, the last contact was 5 days together to control SARS. Beijing tele- tween symptom onset and hospitaliza-
before the patient’s symptom onset; vision ran daily 2-hour educational pro- tion decreased significantly during
however, both contacts occurred in a grams about SARS. The BCDC started the outbreak from a median of 5 to 6
hospital where the patient was being an informational 24-hour SARS hot- days before the outbreak was made
treated for an illness before contract- line on April 8. At its peak, the hotline public on April 20 to 2 days afterward
ing SARS, so that the transmission of received 11 000 calls per day. In (TABLE 4).
SARS might have been from other hos- addition, the Beijing municipal health
pitalized patients with SARS. bureau conducted 6672 SARS semi- COMMENT
nars in the communities and distrib- The SARS outbreak in Beijing was no-
Closing of Facilities uted 8 280 000 copies of educational table for its acceleration, magnitude,
On April 26, all sites of public enter- materials ranging from pamphlets to and rapid resolution. There are sev-
tainment (theaters, bars, libraries, and compact disks. The importance of in- eral likely reasons for the size of the out-
indoor sports facilities) were closed. By
the time these places began opening Table 1. Distribution of Relationship Between SARS Cases and Quarantined Close Contacts
again during the second week in June, and Attack Rates for Probable SARS Among Close Contacts, 5 Districts in Beijing
3500 public places had been closed. Res- No. (%) of All Attack Rate, %
taurants were never ordered to close, al- Relationship to SARS Case Quarantined Contacts (95% Confidence Interval)
though patronage was much reduced Work or school 830 (37.8) 0.36 (0-0.77)
during the height of the outbreak. Of the Household member (nonspouse) 635 (28.9) 8.8 (6.6-11.0)
68 universities in Beijing, 22 (32%) can- Spouse 338 (15.4) 15.4 (11.5-19.2)
celled classes. All public elementary, Nonhousehold relative 189 (8.6) 11.6 (7.1-16.2)
middle, and high schools (n=2610) were Friend 40 (1.8) 10.0 (0.70-19.3)
closed on April 24, not reopening again Health care worker* 30 (1.4) 0 (0-12)†
in some cases until early July. In addi- Other/unknown 133 (6.1) 0.75 (0-2.2)
tion, universities, construction sites, and Total 2195 (100) 6.3 (5.3-7.3)
prisons stopped the entry of all visitors Abbreviation: SARS, severe acute respiratory syndrome.
*Includes those exposed in small, community, nondesignated SARS hospitals or student clinics and not deemed to
and many residential communities and have been wearing complete personal protective equipment.
†Exact method used to calculate 95% confidence interval.
business places screened visitors for fe-
ver at entry.
Table 2. Attack Rate for Probable SARS Among Quarantined Family Members by Age,
Transit Site Surveillance 5 Districts in Beijing*
In late April, fever checks were insti- Total No. in No. of Probable Attack Rate, %
Age, y Quarantine SARS Cases (95% Confidence Interval)†
tuted at the Beijing airport, major train 0-9 60 3 5.0 (0-10.5)
stations, and all 71 roads connecting 10-19 158 8 5.1 (1.6-8.5)
Beijing to other areas. Infrared ther- 20-29 220 11 5.0 (2.1-7.9)
mometers were used to screen passen- 30-39 149 17 11.4 (6.3-16.5)
gers, followed up by axillary thermom- 40-49 268 34 12.7 (8.7-16.7)
eters on those found to be febrile on 50-59 137 24 17.5 (11.2-23.9)
screening. As of June 30, of almost 14 60-69 87 24 27.6 (18.2-37.0)
million people screened at these sites, 70-79 83 9 10.8 (4.2-17.5)
only 12 probable cases of SARS were Total 1162 130 11.2 (9.4-13.0)
identified (TABLE 3). Abbreviation: SARS, severe acute respiratory syndrome.
*Quarantined family members included spouses, other household members, and nonhousehold relatives.
†P⬍.001 for increasing attack rate by age (␹2 for trend).
Information Dissemination
The scope of the Beijing outbreak was
announced in a press conference given Table 3. Summary of Screening for SARS at Points of Transit as of June 30, 2003, Beijing
by the executive vice-minister of health No. of People No. (%) No. (%) With
Transit Site Screened for Fever Febrile Probable SARS
on April 20. Subsequently, the MOH Airport
participated in 4 press conferences International passengers 275 600 496 (0.2) 0
about SARS and the Beijing municipal Domestic passengers 952 200 1449 (0.2) 10 (0.001)
government had 9 press conferences. Train stations 5 246 100 2575 (0.05) 2 (⬍0.001)
Many billboards, bus advertisements, Roads 7 365 600 577 (0.008) 0
and traditional red neighborhood ban- Abbreviation: SARS, severe acute respiratory syndrome.

©2003 American Medical Association. All rights reserved. (Reprinted) JAMA, December 24/31, 2003—Vol 290, No. 24 3219

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CONTROL MEASURES IMPLEMENTED IN THE SARS OUTBREAK

cluded in our analysis, whereas in the


Table 4. Lag Time Between Onset of Symptoms and Hospitalization of Probable SARS Cases,
Beijing Taiwan analysis contacts of both prob-
No. of Lag Time, Median able and suspected cases were in-
Date of Onset, 2003 SARS Cases (Interquartile Range), d* cluded. Who should be quarantined
March 5 to April 9 (SARS becomes reportable) 146 6 (0-14) during a SARS outbreak likely de-
April 10 to April 20 (SARS announced publicly) 476 5 (2-7) pends on several factors, such as re-
April 21 to May 6 (designated fever clinics) 1046 2 (1-4) source availability, ability to mobilize
May 7 to June 15 192 2 (1-3) public health personnel, and societal ac-
Abbreviation: SARS, severe acute respiratory syndrome. ceptability. Public health departments
*P⬍.001 comparing median times (Kruskal-Wallis test).
must weigh these factors in setting quar-
antine guidelines. For example, in
break: multiple imported cases, lack of earlier decrease in hospital-based in- smaller outbreaks or when resources are
knowledge about hospital spread, lack fections was likely because of control limited, public health authorities might
of awareness about proper PPE, de- measures implemented in general hos- consider active but nonquarantined sur-
lays in hospitalizing patients with symp- pitals, such as the use of PPE and group- veillance in lower-risk settings, such as
toms, the population density of Bei- ing of patients with SARS on certain workplaces and schools, and among
jing, and a failure to communicate the wards, because by May 8 the outbreak those whose contact with patients with
problem to hospitals and the public was already waning. In addition, the es- SARS was only during the asymptom-
early enough. With these initial disad- tablishment of designated fever clin- atic incubation phase.
vantages, the prompt resolution of the ics identified the majority of new cases In retrospect, several control mea-
Beijing outbreak was surprising and im- (84%) late in the outbreak. The earlier sures undertaken by the Beijing mu-
pressive. Beijing rapidly implemented implementation of dedicated fever clin- nicipality seemed to have less direct im-
multiple measures to control the SARS ics, separated from general medical care pact in resolving the outbreak; however,
outbreak. areas, might have stemmed some of the this was not known at the time of their
Similar to other SARS-affected areas, transmission earlier in the outbreak. implementation in the face of an accel-
a large part of the Beijing outbreak oc- Rigorous quarantine measures in erating outbreak of an unknown dis-
curred in hospitals.10-13 This was par- Beijing were possible through both ease. The screening at points of trans-
ticularly true early on as suggested by community-based and governmental portation required a large amount of
the number of health care workers in- involvement. Some categories of quar- human and financial resources to main-
fected. Part of the reason for the de- antined close contacts, such as family tain but identified very few cases of
crease in cases among health care work- members, had much higher attack rates SARS. Such measures, however, might
ers was likely the emphasis on training than others, such as school and work- have prevented SARS cases indirectly
and guidelines on infection control and place contacts. The high attack rate by persuading symptomatic people to
use of PPE after April 18. The effec- among family members might par- stay home. Moreover, these check-
tiveness of these interventions is high- tially reflect contact with patients with points assured the local as well as in-
lighted by the fact that no health care SARS not just at home but at the hos- ternational community that proactive
workers contracted SARS at the new pital while visiting their ill relatives. El- steps were being made toward control-
1000-bed SARS hospital that opened derly close contacts had significantly ling the outbreak. Second, the closing
May 1. In addition to health care work- higher attack rates than did children, of the public schools for more than a
ers, many patients without SARS and although it is unclear if this is because month likely had a minimal effect on
visitors to the hospital were likely in- of differences in the type of contact with the prevention of SARS because of the
fected by patients with SARS, as ob- the case, susceptibility to SARS, or the low attack rate among schoolmates and
served in other outbreaks.10,12 The in- likelihood of developing symptoms af- the rarity of pediatric SARS in Beijing,
stitution of improved triage, limitation ter infection. The attack rate among as observed in other SARS-affected
of visitors, and designated SARS wards quarantined persons was significantly sites.4,9,11,16,17 However, the closing of
likely led to a decrease in such in- higher in Beijing than in Taiwan, where schools may have contributed to the
hospital exposures. The hospitals des- among 50139 quarantined close con- widespread self-quarantine that oc-
ignated to SARS began to be estab- tacts the attack rate, even for family curred in Beijing in early May, when the
lished in late April and by May 8, all members of patients with SARS, was less streets were virtually empty.
patients with SARS were hospitalized than 1%.14,15 The reasons for this dif- Besides these specific control mea-
in such hospitals. Designated hospi- ference might be because of differ- sures, a general increase in the aware-
tals had the advantage of ensuring ences in the case definitions of SARS, ness about SARS played an important
proper infection control practices, uni- the higher incidence of SARS in Bei- role in controlling the outbreak. Early
directional airflow rooms, and proper jing, and the fact that only close con- in the outbreak before information
patient triage and flow. However, the tacts of probable SARS cases were in- about the number of patients with SARS
3220 JAMA, December 24/31, 2003—Vol 290, No. 24 (Reprinted) ©2003 American Medical Association. All rights reserved.

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CONTROL MEASURES IMPLEMENTED IN THE SARS OUTBREAK

in the city was disseminated, the out- tine was evaluated might have led to impact in curbing the outbreak. The les-
break amplified because of underrecog- SARS attack rates that were falsely el- sons learned from controlling this out-
nition and mismanagement of pa- evated. The 5 districts selected to evalu- break can hopefully serve to inform fu-
tients with SARS in both the hospitals ate contact tracing and quarantine might ture responses to SARS, if it were to
and the community. The control of the not have been representative of all of Bei- reemerge in Beijing or elsewhere.
outbreak followed improvements in jing. Three districts were urban and 2 Author Contributions: Drs Xu and Feikin had full ac-
communication and awareness among suburban, which might have overrepre- cess to all the data in the study and take responsibil-
health care workers, public health per- sented urban Beijing because of the 18 ity for the integrity of the data and the accuracy of
the data analysis.
sonnel, and the general public, as sug- districts in Beijing, 8 are urban and 10 Study concept and design: Pang, Zhu, Xu, Guo, Z. Liu,
gested by the decrease in the time be- suburban. Attack rates tended to be Chin, Feikin.
Acquisition of data: Pang, Gong, D. Liu.
tween illness onset and hospitalization higher in urban districts because of the Analysis and interpretation of data: Pang, Xu, Gong,
as the outbreak progressed. presence of more hospitals and a greater D. Liu, Feikin.
Drafting of the manuscript: Pang, Zhu, Xu, Feikin.
Our analysis had several limitations. density of people. Critical revision of the manuscript for important in-
Because of the simultaneous and over- The multiple control measures tellectual content: Pang, Zhu, Guo, Gong, D. Liu, Z.
lapping implementation of multiple con- implemented in Beijing likely led to the Liu, Chin.
Statistical expertise: Xu, D. Liu.
trol measures, it was difficult to pin- rapid resolution of the SARS out- Administrative, technical, or material support: Zhu,
point which one or several interventions break. Improvements in infection con- Guo, Z. Liu, Chin.
Study supervision: Zhu, Guo, Feikin.
were the most effective. Evaluation of the trol practices, use of PPE, grouping of Funding/Support: The SARS control measures imple-
control measures was further compli- patients with SARS in the hospital, es- mented in Beijing were funded by the Beijing munici-
pal government. The Beijing municipal health bu-
cated by the lag of at least an incubation tablishment of designated fever clin- reau, Beijing Center for Disease Prevention and Control,
period between implementation and ics, quarantine of high-risk close con- the World Health Organization, and the US Centers
effect. Laboratory testing for SARS coro- tacts, and improved public information for Disease Control and Prevention provided finan-
cial support for the participation of their respective staff
navirus infection was not widely avail- and awareness of SARS likely played im- in this study. No additional funding for this study was
able during the outbreak in Beijing and portant roles in controlling the out- obtained.
Acknowledgment: We thank all the health care work-
was not part of the SARS case defini- break. Some interventions, in retro- ers, public health personnel, government officials, and
tion; therefore, circulation of other agents spect, such as quarantine of low-risk citizens of Beijing who contributed to the effort to con-
trol the SARS outbreak in Beijing. We also thank Anne
causing febrile respiratory illness in 1 or contacts and fever checks at transpor- Schuchat, MD, Weigong Zhou, MD, and C.K. Lee, MD,
more of the districts in which quaran- tation sites, seemed to have less direct for their early input on this article.

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