We found 10 case–control studies which examined the effectiveness of different protective measures, including handwashing, against SARS. Four of these were published in Chinese. Six studies investigated the effect of personal protective equipment as precautionary measures against SARS infection but did not cover handwashing practices (Le et al. 2004; Ho et al. 2003; Fan et al. 2004; Loeb et al. 2004; Park et al. 2004; Chia et al. 2005). One study excluded hand hygiene because accurate assessment was difficult (Chen et al. 2005). In a retrospective study in a hospital designated to receive SARS patients in Shenzhen City, Guangdong, China, self-reported compliance with handwashing practices among the health care workers (HCWs) who had contacts with SARS patients was 100% (n = 72) and no nosocomial infections were reported (Luo et al. 2004).
Effectiveness of handwashing as a protective measure against severe acute respiratory syndrome
Of the 10 epidemiological studies found of the effectiveness of handwashing and other protective measures against SARS infection, one was performed in Singapore (Teleman et al. 2004), two in Guangdong province (Yin et al. 2004; Zou et al. 2004), two in Guangzhou, the provincial capital of Guangdong (Gao et al. 2003; Lin et al. 2003), one in Hanoi (Nishiura et al. 2005), three in Hong Kong (Seto et al. 2003; Lau et al. 2004a,c) and one in Beijing (Wu et al. 2004). All 10 were case–control studies, of which nine showed that handwashing was a protective factor when comparing infected cases and uninfected controls in univariate analysis (Table 1).
Table 1. Results of epidemiological studies of handwashing as a protective measure against SARS infection
|Singapore (Teleman et al. 2004)||Wash hands consistently after contacting each patient||36 HCWs||50 HCWs||0.06 (0.007–0.5)||0.03||0.07 (0.008–0.66)||0.02|
|Guangdong 1 (Yin et al. 2004)||Handwashing and disinfecting||77 HCWs||180 HCWs||0.49 (0.28–0.85)||<0.05||NS||NS|
|Guangdong 2 (Zou et al. 2004)||Sterilizing hands after every contact with SARS patients||152 HCWs||1493 HCWs||0.64||<0.01||0.24 (0.063–0.92)||<0.001|
|Presence of non-contact handwashing equipment in the office|| || ||0.46||<0.01||0.15 (0.025–0.86)||<0.001|
|Guangzhou 1 (Gao et al. 2003)||Disinfect and wash hands every time||22 HCWs||64 HCWs||0.11 (0.01–0.90)||0.034||N/A||N/A|
|Guangzhou 2 (Lin et al. 2003)||Wash hands and disinfect||118 HCWs||308 HCWs||Not available§||<0.05||NS||NS|
|Hanoi (Nishiura et al. 2005)||Stage 1: wash hands before contacts with a patient||25 (22 HCWs, two administrative staff and one patient's relative)||90 (48 HCWs, 11 administrative staff and 41 patients’ relatives)||1.0 (0.4–2.3)||0.94||NS||NS|
|Wash hands after contacts with a patient|| || ||1.1 (0.5–2.8)||0.77||NS||NS|
|Stages 2 & 3: wash hands before contacts with a patient||4 HCWs (doctors and nurses only)¶||26 HCWs (doctors and nurses only)¶||NC||1.00||N/A||N/A|
|Wash hands after contacts with a patient|| || ||NC||1.00||N/A||N/A|
|Hong Kong 1 (Seto et al. 2003)||Wash hands during patient care (‘yes’ and ‘most of the time’)||13 HCWs||241 HCWs||0.2(0.053–1.0)||0.047||NS||NS|
|Hong Kong 2 (Lau et al. 2004a)||Handwashing after contact with SARS patients‡||72 HCWs||144 HCWs (matched)||0.21 (0–2.63) †||0.22||N/A||N/A|
|Handwashing after contact with patients in general‡|| || ||1.00 (0.05–50.00) †||1.00||N/A||N/A|
|Handwashing when there was no patient contact‡|| || ||0.16 (0.03–0.61) †||0.004||NS||NS|
|Hong Kong 3 (Lau et al. 2004c)||Wash hands >10 times a day||330 with undefined source of infection||660 matched controls drawn from random telephone survey||0.44 (0.31–0.63) †||<0.005||0.58 (0.38–0.87)†||0.008|
|Hong Kong 3 (continued)||Wash hands >10 times a day||118 whose source of infection remained undefined (likely to be community- acquired)||236 matched controls||N/A||N/A||0.44†||0.008|
|Beijing (Wu et al. 2004)||Always washed hands before eating||94 unlinked, probable SARS patients (not HCWs)||281 matched controls drawn from telephone sequential digit dialling||0.6 (0.3–1.1) †||0.11||NS||NS|
|Always washed hands after using restrooms|| || ||0.5 (0.2–1.2) †||0.10||NS||NS|
|Always washed hands after returning home|| || ||0.3 (0.2–0.7) †||0.003||NS||NS|
Singapore (nosocomial). The Singapore hospital-based case–control study involved 36 cases and 50 controls, who were ‘all HCWs from SARS-affected wards who reported exposure to patients with probable SARS during the same period’ (Teleman et al. 2004) with the controls being uninfected workers from the same wards. Exposure of the controls was established ‘where there was a history of being within close physical proximity (1 m) of a patient subsequently confirmed with SARS. For all patients not subsequently confirmed by serology, controls were excluded from final analysis’. Those controls whose exposure was not established were also excluded. Telephone interviews were conducted, using a closed questionnaire. Among other questions, the interviewees were asked whether they washed their hands consistently after contacting each patient.
Using univariate analysis, handwashing consistently after contacting each patient was protective [crude odds ratio (OR) = 0.06, 95% confidence interval (CI) 0.007–0.5, P = 0.03]. Wearing of N95 masks also conferred protection (OR = 0.1, 95% CI 0.03–0.4, P = 0.001). With logistic regression analysis, the adjusted OR for handwashing was 0.07 (95% CI 0.008–0.66, P = 0.02), while that for wearing N95 masks was 0.1 (95% CI 0.02–0.86, P = 0.04). Thus handwashing after attending each patient reduced the odds of infection 15-fold, after adjustment for the use of masks and other possible confounding factors. In this study, the respondents were not asked whether they used soap to wash their hands.
Guangdong 1 (nosocomial). This Guangdong case–control study (Yin et al. 2004), by the Chinese Centre for Disease Control and Prevention (CDC), Guangdong Provincial CDC and Guangzhou (i.e. Canton) Municipal CDC, involved 77 cases and 180 controls, who were HCWs from 10 hospitals who accessed the isolation wards of SARS patients and participated in direct first aid for severe SARS patients. ‘Handwashing and disinfecting’ gave an OR of 0.49 (95% CI 0.28–0.85), which indicates that it was protective against SARS infection. However, this variable was not included in the final model of stepwise logistic regression as it was not significant. Three protective measures were significant in the regression model: the use of 12-layer masks (OR = 0.78, 95% CI 0.60–0.99), goggles when necessary (OR = 0.20, 95% CI 0.10–0.41) and footwear (OR = 0.58, 95% CI 0.39–0.86). Again, soap was not mentioned in this study and we are not sure how the investigators defined ‘disinfecting’. It could refer to the use of soap, but more probably to the use of disinfectants.
Guangdong 2 (nosocomial)
Another Guangdong case–control study involved 152 cases and 1493 controls, who were HCWs from nine hospitals in the province (seven in Guangzhou city and two in Jiangmen city; Zou et al. 2004). All of them had contacts with confirmed or probable SARS cases. ‘Sterilizing your hands after contact with SARS patients every time’ gave an OR of 0.64 (P < 0.01) in univariate analysis and 0.24 (95% CI 0.063–0.92, P < 0.001) in multivariate analysis. ‘Sterilizing’ might include the application of alcohol-based hand gels. The use of soap was not mentioned but might be included.
The presence of non-contact handwashing equipment in the office gave an OR of 0.46 (P < 0.01) in univariate analysis and 0.15 (95% CI 0.025–0.86, P < 0.001) in multivariate analysis. The authors of the paper suggested that traditional water taps should be replaced by automatic or paddle taps to avoid transmission via fomites. However, it had been reported that although introducing an automated sink in intensive care units might lead to a significant improvement in the quality of handwashing among HCWs, it might also reduce handwashing frequency because of the additional time involved (Larson et al. 1991; Naikoba & Hayward 2001).
Guangzhou 1 (nosocomial)
This small case–control study was conducted in Guangzhou city, the provincial capital of Guangdong, in one of the first hospitals in the province to receive SARS patients (Gao et al. 2003). The hospital received its first case (a severely ill SARS patient from another place in Guangdong province) on 22 December 2002. The first case of nosocomial infection of a HCW in the hospital was on 13 January 2003, while the last was on 23 April. Altogether 25 HCWs (11 physicians, 12 nurses and two other staff members) were infected.
The study involved 22 cases and 64 controls. They were all HCWs. It was found that ‘disinfecting and washing hands every time’ was protective with an OR of 0.11 (95% CI 0.01–0.90, P < 0.034) in univariate analysis. Multivariate analysis was not performed. The term ‘disinfecting’ might imply that alcohol-based hand gels were used. The use of soap was not mentioned but might be included.
Guangzhou 2 (nosocomial). This study included nine hospitals in Guangzhou city which received a relatively large cohort of patients and thus were representative of the scenario in the city (Lin et al. 2003). The case–control analysis section of the study involved 426 HCWs who had participated in treating SARS patients in seven of the nine hospitals. 118 were cases and 308 were controls. It was found that ‘washing hands and disinfecting’ was among the 11 protective factors in univariate analysis. The exact OR of each factor was not published, but the range of OR of these 11 protective factors was 0.160–0.698 (all P < 0.05). However, ‘washing hands and disinfecting’ was found to be non-significant in multivariate analysis. As noted before, ‘disinfecting’ might include the application of alcohol-based hand gels. The use of soap was not mentioned but might be included.
Hanoi (nosocomial). This case–control study was performed in Hanoi French Hospital (HFH) where the first SARS case in Viet Nam was hospitalized (Nishiura et al. 2005). The outbreak in HFH consisted of three stages: Stage 1, from admission of the index case to the onset of secondary cases; Stage 2, from the suspicion of nosocomial spread to closure of the hospital; and Stage 3, from strict isolation to local eradication.
The study involved 29 cases (out of 38 laboratory-confirmed SARS cases) and 98 controls in total. Of the 29 cases, 28 were HFH employees (26 HCWs and two receptionist and administrative staff) and one was a patient's relative. The other nine SARS patients who did not participate were either dead because of SARS and/or respiratory failure (five or 13.2%), refusing to participate (one or 2.6%) or had been relocated (three or 7.9%). Controls were selected among ‘those thought to have had contact with confirmed cases inside the hospital based on contact investigations’, provided that they were Vietnamese, aged more than 20 years and had given their written consent. Among the controls, 57 were HFH employees (46 HCWs and 11 receptionists and administrative staff members) while 41 were relatives of patients.
Univariate analysis of precautionary measures taken by 25 cases and 90 controls in Stage 1 found no association between handwashing, whether before or after contact with a patient and being infected, with ORs of 1.0 (95% CI 0.4–2.3) and 1.1 (95% CI 0.5–2.8) respectively (Table 1).
Analysis in Stages 2 and 3 was limited to doctors and nurses who had probable contact in these stages and whose incubation period was within 95% CI of having occurred after the beginning of Stage 2 (four cases and 26 controls). It is not possible to find any association as all the four SARS cases and 25 of the 26 controls claimed that they washed their hands before and after having contact with a patient. This study did not mention whether the participants washed their hands with soap.
Hong Kong 1 (nosocomial). The case–control study performed by the University of Hong Kong, also hospital-based, involved 13 cases and 241 controls using self-completed questionnaires (Seto et al. 2003). Both the cases and controls were HCWs ‘with documented exposures to 11 index patients with SARS during patient care…. They were listed on the current roster in the clinical regions providing care for index patients with SARS’. Only those who affirmed that they had cared for the named index patients were interviewed. Among other questions, they were asked whether they washed their hands during patient care (options available: yes, most of the time or no). Univariate analysis showed that handwashing (‘Yes’ and ‘most of the time’ were grouped together) was protective (OR = 0.2, 95% CI 0.053–1.0, P = 0.047). However, logistic regression (with forward stepwise selection) of the use of masks, gowns, gloves and handwashing showed that only use of masks was significant while the other measures were not. The authors concluded that in hospital, handwashing adds no significant protection to the mask, which seems to be essential for protection. In this study, the respondents were not asked whether they used soap to wash their hands.
Hong Kong 2 (nosocomial). This was a 1:2 matched case–control study of 72 cases and 144 controls (Lau et al. 2004a). Both groups were hospital workers who had been working in wards with SARS inpatients, some of which also included non-SARS patients. Controls were recruited by asking the cases to nominate ‘two colleagues who had been working in the same job position, in the same ward and in proximity with the case–patient before he became ill’ (Lau et al. 2004a).
In the questionnaire, three questions were asked about the frequency of handwashing after making contact with (1) SARS patients, (2) patients in general and (3) when there was no patient contact. The four possible answers to each question were grouped into two categories for analysis: inconsistently (‘never’ or ‘occasionally’) and consistently (‘most of the time’ and ‘all of the time’).
Most cases and controls reported that they consistently washed their hands after direct contact with SARS patients and patients in general, so these two factors are not significant in the univariate analysis (P = 0.22 and P = 1.00 respectively, Table 1). On the other hand, washing hands consistently when there was ‘no patient contact’ was found to be a statistically significant protective factor (matched OR = 0.16, 95% CI 0.03–0.61) in the univariate analysis. However, it was not statistically significant in the multivariate analysis.
Inconsistent handwashing when there was ‘no patient contact’ was one of the seven factors identified in the unadjusted analysis as significantly associated with a risk of SARS infection. The other six were (1) inconsistent use of at least one type of personal protection equipment when having contact with SARS patients or (2) with ‘patients in general’ or (3) when there was ‘no patient contact’, (4) SARS infection control training <2 h, (5) the respondent reported not understanding SARS infection control procedures and (6) at least one item of personal protection equipment was perceived to be in inadequate supply in the three settings. The authors constructed an indicator variable by counting how many of the above factors applied to each individual. It was found that the risk increased greatly with the number of factors (OR = 44.2 for three or more problems, P < 0.0001) (Lau et al. 2004a).
Hong Kong 3 (community acquired). This 1:2 matched case–control study performed by the Chinese University of Hong Kong was different from the eight above. It was a telephone survey of households of ‘all probable SARS patients whose cases were reported to the Department of Health on or before May 16, 2003 (n = 1690)’ (Lau et al. 2004c). Of the 1690 probable cases, 140 patients (8.2%) did not have a correct telephone number, 163 (9.6%) could not be contacted after at least five attempts, 163 (9.6%) refused to participate and 10 (0.6%) were either not in Hong Kong or could not communicate in English or Chinese. The remaining 1214 patients (72%) from 996 households were interviewed. Apart from 22 with incomplete questionnaires, the data for 1192 of these 1214 patients were analysed. A total of 727 patients fell into one or more of the following four categories: (1) probable cases of secondary or tertiary household transmission, (2) hospital workers, (3) residents in the Amoy Gardens or (4) inpatients who had been hospitalized for diseases other than SARS and kept on wards with SARS patients. Another 118 patients were in contact with a SARS patient within a 10-day period before onset of fever. The source of infection of the remaining 347 (29.1% of 1192) was undefined. Excluding 17 patients who were below 16 years of age, 330 SARS patients aged 16 years or above became the cases of the case–control study. Two controls per case, matched for age and sex, were drawn by a random telephone survey.
Univariate analysis showed that cases were less likely than controls to have washed their hands more than 10 times a day (18.4% vs. 33.7%, OR = 0.44, 95% CI 0.31–0.63, P < 0.005). Multivariate analysis gave an adjusted OR of 0.58 (95% CI 0.38–0.87) and P-value of 0.008. The other protective factors included in the regression model were: using a mask frequently in public places (adjusted OR = 0.27, P < 0.001) and disinfecting the living quarters thoroughly (adjusted OR = 0.41, P < 0.001). The significant risk factors included in the regression model were (1) having visited mainland China (OR = 1.95, P = 0.020), (2) having visited Amoy Gardens where a cluster of cases had occurred (OR = 7.63, P < 0.001), (3) having visited the Prince of Wales Hospital (OR = 7.07, P < 0.001) and (4) having visited other hospitals and clinics (OR = 3.70, P < 0.001).
The study authors then moved on to a second round of analysis, in which they excluded the 212 cases ‘who may have contracted SARS after visiting Amoy Gardens, the Prince of Wales Hospital, other hospitals or an affected country, including mainland China, Singapore and Taiwan’ and their matched controls (Lau et al. 2004c). The remaining 118 cases were considered likely to have acquired SARS through unknown sources of transmission in the community. Once again, univariate and multivariate conditional logistic regression analyses gave similar results. The adjusted OR for washing hands more than 10 times a day was 0.44 and the P-value was 0.008. Wearing a mask in public places (adjusted OR = 0.36, P < 0.001) and disinfecting the living quarters thoroughly (adjusted OR = 0.36, P < 0.001) were also protective. The respondents were not asked whether they used soap to wash their hands.
Beijing (community acquired). This 1:3 matched case–control study examined the risk factors for SARS among those without known contact with SARS patients (Wu et al. 2004). A total of 94 unlinked, probable SARS patients were compared with 281 community-based controls matched for sex and age group. Patients who met the ‘probable case definition and reported no close contact with any known, probable or suspected SARS patients’ were eligible for enrolment. Patients who were HCWs were excluded from the study.
Three controls were selected for each case by sequence digit dialling, by adding to or subtracting from the last digit of the case–patient's home telephone number by one digit in an alternating sequence until three controls were enrolled, matched by age group and sex. As telephone number prefixes are geographically clustered in Beijing, this strategy was intended to provide neighbourhood matching.
Of a total of 1091 probable SARS case–patients without a history of contact with other SARS patients, 373 were called from the master list until 100 were successfully interviewed. The refusal rate was about 50% among patients who could be reached. Six matched sets were excluded; four cases were reclassified as HCWs after interview and controls in the other two sets were below 14 years of age.
In the univariate analysis, it was found that having ‘always washed hands after returning home’ was a protective factor, with a matched OR of 0.3 (95% CI 0.2–0.7, P = 0.003). However, it was not significant in the multivariate analysis. Having ‘always washed hands before eating’ (matched OR = 0.6, 95% CI 0.3–1.1, P = 0.11) and having ‘always washed hands after using restrooms’ (matched OR = 0.5, 95% CI 0.2–1.2, P = 0.10) were protective yet statistically insignificant in the univariate analysis.
The authors mentioned the possible limitations of this study, including recall bias (interviewed late in the Beijing epidemic), low participation rate raising the possibility of selection bias, unknown representativeness of the control population from the telephone survey and the insufficient number of samples for serological tests.