It was hypothesized that performing certain high-risk procedures, such as nasopharyngeal aspiration, bronchoscopy, endotracheal intubation, airway suction, and cardiopulmonary resuscitation, might increase the rate of SARS-Cov shedding occurring in a SARS patient's respiratory secretions, thereby increasing the risk to HCWs of contracting SARS while performing such procedures [15
]. The results of the present study demonstrate that performing tracheal intubations was highly associated with incidence of SARS among HCWs. Therefore, the results imply that adequate personal protective equipment is required when conducting certain high-risk procedures which may contribute to the presence of infectious droplets in the environment.
It was hypothesized that the primary mode of SARS transmission was via droplets spread through close person-to-person contact [1
], and this was strongly supported by the occurrence of clusters of cases among HCWs caring for SARS patients and family members of SARS patients [16
]. In the present study, we found that avoiding face-to-face contact with SARS patients while caring for them could significantly reduce the probability of HCWs contracting the virus. This may be due to decreased exposure to infected droplets resulting from this practice. This result implies that HCWs could use appropriate personal protective measures (such as avoiding face-to-face contact with SARS patients) to protect themselves from SARS infection while they are caring for patients with SARS.
There is some evidence that longer range airborne transmission may have played a role in the spread of the SARS virus in some settings, such as in the outbreak of SARS in wards with faulty ventilation in the Prince of Wales Hospital of Hong Kong [17
], in the transmission of SARS on an aircraft [18
], and in the community outbreak at Amoy Gardens in Hong Kong [19
]. The results of the present study also indicate that airborne transmission might have been a contributing factor in spread of SARS in 2003. Compared with ventilation through artificial central air-conditioners in the wards, natural ventilation alone and natural ventilation enhanced by an additional electronic exhaust fan at the same time could significantly reduce the risk of HCWs contracting SARS in the wards. In wards with artificial central ventilation, windows were closed which might lead to much lower air flow and much higher viral load in the wards, and HCWs were easily infected with the SARS virus while working in such an environment. By contrast, the windows of wards with natural ventilation and natural ventilation enhanced by an additional electronic exhaust fans were opened, and the air flow and the exchange rate of air in the wards were high, which might greatly decrease the density of the SARS virus in the wards and may also reduce the probability of HCWs contracting the virus.
SARS-Cov may be shed from a SARS patient's respiratory secretion and feces, and the latter may further contaminate objects in the ward. The protective gown, gloves, multilayered cotton mask, and head and foot coverings wore by HCWs may also be contaminated while caring for SARS patients. It has been shown that SARS-Cov may remain viable for considerable periods on a dry surface (up to 24 hours) [16
] and is stable in feces and urine at room temperature for at least 1 to 2 days and 4 days in stool from patients with diarrhea [19
]. Hence, touching surfaces or objects that are contaminated with SARS-CoV may introduce the virus into the mucous membranes of the eye, nose, or possibly the mouth. It is believed that nominally 'clean' areas may be contaminated if an HCW wears a piece of protective clothing contaminated with SARS patients' secretions into the area. For this reason, HCWs must wear two layers of gown, gloves, multilayered cotton mask, head and foot covering in SARS wards and discard the outer layer before entering clean areas, in order to prevent fomite transmission to other areas [20
]. This study proved that wearing two layers of gloves significantly protected HCWs from SARS compared with wearing a single layer of gloves, but we did not find that wearing double layers of gowns, multilayered cotton masks, and head and foot coverings were associated with HCWs being protected from SARS. This might be due to the fact that almost of all the procedures involved in caring for patients were done with the hands; hence gloves were more highly contaminated by SARS patients' secretions.
A small number of severely infected patients or super-spreading patients appeared to play a disproportionate role in the spread of the disease to HCWs. For instance, several clusters of SARS outbreaks in hospitals can be traced to such patients in Hong Kong, Singapore, and Toronto [2
]. It had been hypothesized that these patients might have a relatively depressed immune system with associated high viral loads and may be unduly facilitating transmission of the virus. In the present study, the same index patient led to the two clusters of SARS outbreaks among HCWs in the two affiliated hospitals. Statistical analysis showed that caring for a "Super-spreading Patient" significantly increased the risk of HCWs suffering from SARS. In light of this, a series of stringent infection control measures should be required when HCWs care for patients suspected of being SARS super-spreaders.
Several limitations of the study ought to be mentioned here. First, our investigation was limited to two affiliated hospitals of Sun Yat-sen University. This is not representative of all of the hospitals in which patients with SARS were admitted and cared for in Guangzhou. Therefore, this is a typical case investigation. Second, ventilation in the wards was not objectively assessed for some reason, meaning that we could not exactly evaluate the influence of the ventilation in the wards on the transmission of SARS among HCWs. Third, we could not trace the tree structure of the primary, secondary, and third class cases, which prevented us from clarifying the association of the HCWs infected by SARS with the index case directly or indirectly. Fourth, some factors, such as oxygen therapy and bi-level positive airway pressure ventilation were found to be related to nosocomial infection of SARS in other study [21
], were not included in the present study, which indicated that we missing an opportunity to find some effective measures for protecting HCWs from SARS or to assess their effect. Fifth, in the early stage of SARS epidemic, the diagnosis of SARS was based on the history of epidemiology, signs and symptoms suggested by the Health Ministry of China [12
], not on the directive biomarkers of SARS-CoV or antibodies against SARS-CoV, which might lead to over reporting "SARS" cases or missing identifying inapparent infection or subclinical infection. This might be the reason that 80 of 90 HCWs with "SARS" and 11 of 668 subjects without "SARS" were seropositive. Sixth, some prevention measures were usually employed at the same time in SARS wards, which meant that these measures were highly correlated. In this situation, multivariate statistical analysis might omit some effective measures in the final model due to multicollinearity. Seventh, 10.8% of frontline HCWs who cared for SRAS patients were not included in the present study, which was the reason that the number of HCWs involved in intubation in the present study was less than our previous study [13
], which might cause to underestimate the association of the intubation with the nosocomial infection of SARS. Finally, although we identified several preventive measures which were effective for protecting HCWs from SARS, we could not eliminate the inefficiencies of other adopted measures, due to the fact that we utilized a retrospective rather than an interventional study design.