Chen, MI

Earnest, A

Lew, TW

Loo, S

Tai, DY

Tan Tock Seng Hospital SARS ICU Group

English

LSHTM Research Online

Goh, DL; Lee, BW; Chia, KS; Heng, BH; Chen, M; Ma, S; Tan,CC (2004) Secondary household transmission of SARS, Singapore.Emerging infectious diseases, 10 (2). pp. 232-4. ISSN 1080-6040Downloaded from: http://researchonline.lshtm.ac.uk/8667/Usage GuidelinesPlease refer to usage guidelines at http://researchonline.lshtm.ac.uk/policies.html or alterna-tively contact researchonline@lshtm.ac.uk.Available under license: Creative Commons Attribution Non-commercial No Derivativeshttp://creativecommons.org/licenses/by-nc-nd/2.5/Secondary household transmission of severe acuterespiratory syndrome (SARS) was studied in 114 house-holds involving 417 contacts. The attack rate was low(6.2%). Occupation of the index case was the factor thatmost influenced household transmission (adjusted hazardratio for healthcare workers 0.157; 95% confidence interval0.042 to 0.588). Severe acute respiratory syndrome (SARS) is an emerg-ing infectious disease caused by the SARS-associatedcoronavirus (SARS-CoV) (1). Attack rates are >50% inhospitals (2). A similar trend was seen in Singapore, withSARS spreading to five hospitals and two SpecialtyCentres within 8 weeks (3). This rapid rate of transmissioncaused a national health alert and resulted in large amountsof manpower and resources being deployed.On the other hand, transmission within the householdwas less efficient. We, therefore, examined the attack rateand the factors influencing secondary transmission ofSARS in Singapore households. Data on probable SARScases were collected by Singapore’s Ministry of HealthEpidemiology Unit, Singapore. The case definition ofprobable SARS was in accordance with the World HealthOrganization (WHO) (4). Probable SARS cases that were also a household indexwere identified by using the definition that follow. Ahousehold was defined as a residential place with a uniqueaddress. A household index was a person with probableSARS and the first person to introduce SARS into thehousehold. A household contact was defined as a personliving in the same household as the household index. Demographic and clinical data were collected. For thehousehold index, the following information was collected:age, sex, if the household index was a healthcare worker(defined as a person who works in a healthcare setting),number of days spent at home after onset of symptoms,and number of contacts in household. For household con-tacts, the following information was collected: age, sex, ifthe contact was a healthcare worker, and if the contact wasa family member. The week of the SARS outbreak inSingapore was also evaluated to see if there was a timetrend in the risk for transmission. All household contacts were followed prospectively for(1) clinical symptoms until 20 days after the last contactwith the household index, and (2) evidence of positivePCR (polymerase chain reaction) or serologic test forSARS-CoV (according to criteria set by WHO). Secondaryhousehold transmission was said to have occurred if thehousehold contact fulfilled the case definition of probableSARS (4). Households were excluded if the household index livedalone, the household index did not spend time at homeafter onset of symptoms, if the period of household  expo-sure to the index was not clearly defined (e.g., not isolatedpromptly upon hospital admission), or more than oneindex lived in the household (shown through contact trac-ing or onset <2 days after SARS developed in the first per-son in the household).Statistical tests (Mann-Whitney, chi-square and Fisherexact test) were used to test for associations when appro-priate. The Cox regression model was used to evaluate theinfluence of demographic and clinical factors on second-ary household transmission. All analyses were performedwith SPSS version 11.5.There were 205 probable SARS cases in Singapore dur-ing the period between February 24 and April 29, 2003.These 205 probable SARS cases resided in 163 house-holds. Atotal of 114 households fulfilled the inclusion andexclusion criteria. Forty-nine households were excluded(12 because the index lived alone, 20 because the house-hold index did not spend time at home after onset of symp-toms, 10 because the period of household exposure to theindex was not clearly defined, 7 because more than oneindex patient was in that household). Seventy-two of the114 household indexes (63.2%) were healthcare workers.Secondary Household Transmissionof SARS, SingaporeDenise Li-Meng Goh,* Bee Wah Lee,* Kee Seng Chia,* Bee Hoon Heng,† Mark Chen,‡ Stefan Ma,§ and Chorh Chuan Tan§232 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 10, No. 2, February 2004EMERGENCE OF SARS*National University of Singapore, Singapore; †NationalHealthcare Group, Singapore; ‡Tan Tock Seng Hospital,Singapore; and §Ministry of Health, Singapore Ten were doctors, 37 were nurses, 4 were nursing students,and 21 were paramedical staff. From these 114 households, 417 household contactswere identified and followed prospectively. Secondarytransmission occurred in only 14 households (12.3%), giv-ing rise to 26 household cases of probable SARS.Household transmissions occurred within 2–11 days (mean5.3 ± 2.6 days) after the onset of symptoms in the indexcases. Symptoms developed in eight contacts (30%) whileon home quarantine orders. The remaining 18 were notgiven home quarantine orders because they were eitheralready in hospital with SARS or were not identified bycontact tracing. The mean length of stay at home afteronset of symptoms was not statistically different betweenthe home-quarantined group and the group not quarantinedat home (p = 0.09). The secondary household attack rate was thus low(6.2% [95% confidence interval 3.9% to 8.6%]) and con-curs with that reported by Beijing, China (5). In that study,the attack rate was 4.6% in persons who had contact with aprobable SARS case-patient during the symptomatic periodand lived in the same residence (which included some per-sons who visited or cared for a SARS patient). These find-ings are in contrast to the high attack rate seen in the health-care setting (6). One possible explanation for this differenceis the phase of the illness. SARS case-patients in the house-hold tend to be in the early phase of illness whereas SARScase-patients in the healthcare settings tend to be in the laterphase. In addition, coexisting conditions and invasive pro-cedures done within the hospital setting may also influencerisk of transmitting disease (7).The low rate of household transmission suggests thatthe magnitude of a household outbreak would be less thana hospital-based one, which could help allay public fearand panic, a societal concern evident in the recent outbreak(2,7). This knowledge will also enable public health offi-cers to develop a more sensitive and responsive surveil-lance system. As the expected attack rate is known, health-care professionals can be prepared early if the observedattack rate in the households is higher than predicted,allowing rational rather than empirical implementation ofpublic health measures and justify rapid and aggressiveinvestigative and containment measures needed to preventa large outbreak. These considerations are particularlyimportant for countries with limited healthcare and fiscalresources. In Singapore, we learned the usefulness of edu-cating persons on the need and means of doing daily tem-perature monitoring, to have a centralized temperaturerecording database for hospital staff and patients so that acluster of fevers could be spotted early, to evaluate symp-tomatic hospital staff in designated hospital clinics, and totrace contacts by using many resources including thepolice and army. The authorities in Hong Kong did nothave the benefit of this information as little was knownthen about SARS. Perhaps in the future, such knowledgewill help prevent another situation similar to that seen inAmoy Gardens, Hong Kong Special AdministrativeRegion (8).Factors influencing household transmission were alsostudied in the Singapore cohort. Univariate analysis (Table1) showed that household index cases were less likely totransmit SARS to their household contacts if they wereyounger or were healthcare workers. Contacts were morelikely to develop SARS if they were family members ornonhealthcare workers. The Cox regression model (Figureand Table 2) verified two of these four factors, index occu-pation and age. The most consistent and important factor influencinghousehold transmission was whether or not the index casewas a healthcare worker (adjusted hazard ratio 0.157; 95%CI 0.042 to 0.588). This was independent of length ofexposure or demographics. The reason for this finding wasnot evident from the data available. A difference in socialbehavior between healthcare worker and nonhealthcareworker is a possible explanation for this disparity in risksof household transmission. For example, healthcare work-Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 10, No. 2, February 2004 233DISPATCH SARS TRANSMISSIONTable 1. Characteristics of household contacts and index casesa Risk Factor Household  contacts with SARS (n = 26) (mean ± 1 SD) Household  contacts without SARS (n = 391) (mean ± 1 SD)  p value Household  contact       Age (y)  35.3 ± 19.8  30.3 ± 17.4  0.17 Sex (female)  14 (53.8%)  225 (57.5%)  0.71 Healthcare worker  1 (3.8%)  84 (21.5%)  0.04 Family member  24 (92.3%)  269 (68.8%)  0.01 Index case       Age (y)  53.5 ± 16.2  35.4 ± 13.6  <0.001 Sex (female)  20 (76.9%)  290 (74.2%)  0.76 Healthcare worker  4 (15.4%)  273 (69.8%)  <0.001 Days index spent at home after onset of symptoms  5.3 ± 2.5  4.8 ± 2.5  0.43 No. of persons in household  5.0 ± 3.0  4.8 ± 2.4  0.79 aUsing univariate analysis, SARS, severe acute respiratory syndrome. ers may be more acutely aware of the risk of acquiring andtransmitting SARS and may alter hygiene practices athome. In addition, better health and disease preventionknowledge may influence the efficacy of such practices.Qualitative differences in social behavior between health-care worker and nonhealthcare worker should be investi-gated, as this knowledge may be useful in containingfuture SARS outbreaks.The risk for household transmission was also lower ifthe index case was younger. This finding may correlatewith milder disease seen in younger persons and lowerinfectivity. The week of the outbreak did not significantlyinfluence the model, indicating the lack of a time trend inhousehold transmission. In conclusion, this study is the first to characterize sec-ondary household transmission of SARS. We have shownthat the attack rate is low and the most significant factorinfluencing household transmission was the occupation ofthe index case. The results of this study challenge some ofthe current concepts about SARS. Given that the studynumbers are not large, a multicenter analysis of the pastSARS cases would be helpful in verifying these findings. AcknowledgementsWe thank the clinical and healthcare workers in Singapore,in particular the Tan Tock Seng Hospital, for their dedication andprofessionalism in the fight against SARS. Dr. Denise Goh is a pediatrician and geneticist at theNational University of Singapore and the National UniversityHospital, Singapore. Her interests are in childhood diseases.References1. Ksiazek TG, Erdman D, Goldsmith CS, Zaki SR, Peret T, Emery S, etal. A novel coronavirus associated with severe acute respiratory syn-drome. N Engl J Med 2003;348:1953.2. World Health Organization. Outbreak news—severe acute respirato-ry syndrome (SARS). Wkly Epidemiol Rec 2003;78:81.3. Hsu L-Y, Lee C-C, Green JA, Ang B, Paton NI, Lee L, et al. Severeacute respiratory syndrome (SARS) in Singapore: clinical features ofindex patient and initial contacts. Emerg Infect Dis 2003;9:713–7.  4. Lingappa JR, McDonald C, Parashar U, Simone P, Anderson L.SARS emergence from uncertainty. Emerg Infect Dis2004;10:167–70.5. Efficiency of quarantine during an epidemic of severe acute respira-tory syndrome—Beijing, China, 2003. MMWR Morb Mortal WklyRep 2003;52:1037.6. World Health Organization. Outbreak news—severe acute respirato-ry syndrome (SARS). Wkly Epidemiol Rec 2003;78:81.7. Lee N, Hui D, Wu A, Chan P, Cameron P, Joynt GM, et al. A majoroutbreak of severe acute respiratory syndrome in Hong Kong. N EnglJ Med 2003;348:1986.8. H.K.S.A.R.C. Department of Health. Outbreak of Severe AcuteRespiratory Syndrome (SARS) at Amoy Gardens, Kowloon Bay,Hong Kong. Main Findings of the Investigation; 2003. Address for correspondence: Denise Li-Meng Goh, Dept of Paediatrics,National University of Singapore, 5 Lower Kent Ridge Road, S 119074,Singapore; fax:(65)-6779-7486; email: paegohlm@nus.edu.sg 234 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 10, No. 2, February 2004EMERGENCE OF SARSFigure. Survival analysis for secondary household transmission(Cox regression model). Household contacts were more likely toget SARS if the index was older or a nonhealthcare worker.Hazard ratios of risk factors analyzed are tabulated in Table 2. The-2log likelihood for this analysis was 253.77. HH, household;HCW, healthcare worker; NHCW, nonhealthcare worker.Table 2. Hazard ratios of risk factors analyzeda Independent risk factor  Hazard ratio (95% CI)  p value Household contact     Age (yrs)  1.013 (0.992 to 1.034)  0.222 Sex (female)  1.232 (0.542 to 2.796)  0.619 Healthcare worker  1.692 (0.137 to 20.926)  0.682 Family member  1.936 (0.372 to 10.076)  0.432 Household index     Age (y)  1.055 (1.015 to 1.097)  0.007 Sex (female)  1.274 (0.451 to 3.595)  0.648 Healthcare worker  0.157 (0.042 to 0.588)  0.006 Days index spent at home after onset of symptoms 0.942 (0.794 to 1.117)  0.493 No. of persons in household   1.060 (0.899 to 1.249)  0.490 Week of outbreak  1.019 (0.733 to 1.417)  0.911 a Using Cox Regression Model; CI, confidence interval. Use of trade names is for identification only and does not implyendorsement by the Public Health Service or by the U.S.Department of Health and Human Services.All material published in Emerging Infectious Diseases is in thepublic domain and may be used and reprinted without special per-mission; proper citation, however, is appreciated.

A major outbreak of severe acute respiratory syndrome in Hong Kong.

A novel coronavirus associated with severe acute respiratory syndrome.

Department of Health. Outbreak of Severe Acute Respiratory Syndrome (SARS) at Amoy Gardens, Kowloon Bay, Hong Kong. Main Findings of the Investigation;

Efficiency of quarantine during an epidemic of severe acute respiratory syndrome—Beijing,

Organization. Outbreak news—severe acute respiratory syndrome (SARS). Wkly Epidemiol Rec

SARS emergence from uncertainty. Emerg Infect Dis

Severe acute respiratory syndrome (SARS) in Singapore: clinical features of index patient and initial contacts. Emerg Infect Dis

Clinical features and predictors for mortality in a designated national SARS ICU in Singapore.

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Clinical features and predictors for mortality in a designated national SARS ICU in Singapore.

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