key: cord-0760538-pqdob5l9
authors: Yen, Muh-Yong; Yen, Yung-Feng; Chen, Shey-Ying; Lee, Ting-I.; Huang, Guan-Han; Chan, Ta-Chien; Tung, Tsung-Hua; Hsu, Le-Yin; Chiu, Tai-Yuan; Hsueh, Po-Ren; King, Chwan-Chuen
title: Learning from the past: Taiwan's responses to COVID-19 versus SARS
date: 2021-06-05
journal: Int J Infect Dis
DOI: 10.1016/j.ijid.2021.06.002
sha: 8dac6619be69bd674ddb7e3ce8e610cf36466de2
doc_id: 760538
cord_uid: pqdob5l9

Objectives This study evaluated the effectiveness of two major citizens’ mobilized intervention strategies - facemasks and alcohol-based hand hygiene and their changes from the 2003 SARS outbreak to the 2020 COVID-19 pandemic (pdmCOVID-19). Methods We surveyed 2,328 Taiwanese from July 29 to August 6, 2020, assessing demographics, information sources, and practice of preventive behaviors from the 2003 SARS or 2009 pandemic influenza H1N1 (2009pdmH1N1) era to the current pdmCOVID-19 as well as post-survey intention to continue preventive practices. Logistic regression was employed to identify characteristics associated with close adherence to preventive behavior practices in 2020. Results About 70.2% of participants adhered closely to recommended preventive behavior practices. Compared with 2003SARS/2009pdmH1N1, there was a significant increase in the use of facemasks during pdmCOVID-19 (66.6% vs. 99.2% [indoors], p < 0.001) and the use of on-person alcohol-based hand sanitizer (AHS) (44.2% vs. 65.4%, p < 0.001) or 98.4% (hand sanitation at entry of buildings, p < 0.001) during the pdmCOVID-19. Multivariable logistic regression revealed four characteristics significantly associated with continuance of close adherence to recommend preventive behavior practices in 2020: being female (adjusted odds ratio [aOR], 1.72), receipt of government COVID-19-prevention information (aOR, 1.52), recruitment of the study subjects from primary care clinics (aOR, 1.43), and previous use of AHS during the 2003SARS/2009pdmH1N1 (AOR, 1.37). Conclusions With Taiwan’s concerted efforts of government leadership, healthcare providers’ risk communication, and public cooperation, we rapidly brought the COVID-19 pandemic under control. We advocate the importance of high coverage of population-based preventive behaviors in population-dense areas with increasing dominant fast-spreading SARS-CoV-2 variants.

The 2019 pandemic of has had an immense impact on global health, medical care, and the world economy (Cutler, 2020) . It is crucial to search for reasons why certain areas such as Taiwan have successfully prevented and controlled this threat to help fighting SARS-CoV-2 more efficiently on a global scale.

Taiwan has had close cultural and economic exchanges with China and should be one of the most at-risk areas for large-scale outbreaks of COVID-19. From January 1 to February 29, 2020, Taiwan had a total of 45 cases (including 20 imported and 25 indigenous cases) during the crisis time when several cities in China encountering lock down (Taiwan CDC, 2020 a ). Yet in defiance of the predictions, Taiwan's actual scales had thus far been minimal and well controlled (Wang and Ellis, 2020) . Many scholars attribute Taiwan's effective responses to their past experiences with the 2003 SARS outbreaks, and the 2009 pandemic influenza H1N1 (2009pdmH1N1), the use of big data to enhance surveillance and contact tracing, effective communication, and early deployment of strict border controls Chung et al, 2020; Huang et al, 2020; Lai et al. 2020 Wang et al., 2020 Yen et al, 2020; ) . However, there were three major leaks, each of them having infected persons who were initially not required to undergo quarantine ( Figure 1 During the 2003 SARS outbreak, Taiwan had suffered from heavy loss of healthcare workers (HCWs) Yen et al., 2021) . The specific aims of this study were: (1) to identify the preventive behaviors during the 2003 SARS or the 2009 pdmH1N1, (2) to investigate the role of wearing facemasks and practicing alcohol-based hand hygiene (AHH) as part of the Taiwanese participants' preventive behaviors in 2020pdmCOVID-19, and (3) to search for characteristics associated with persistently practicing these preventive behaviors from the 2003 SARS/2009 pdmH1N1 era to the 2020 challenge of COVID-19. We hope our findings can help in combating COVID-19 pandemic more efficiently.

J o u r n a l P r e -p r o o f

To understand Taiwanese behaviors in practicing prevention measures during the 2020 COVID-19 pandemic compared to those observed during the past outbreaks (2003 SARS/2009pdmH1N1), we conducted a retrospective survey to determine the significant characteristics underlying Taiwanese citizens' participation in effectively containing the COVID-19 epidemic. All the laboratory-confirmed SARS-CoV-2 cases documented in Taiwan's Central Epidemic Command Center (CECC) were used to evaluate the effectiveness of the overall prevention and control measures.

Alcohol-based hand disinfection became a standard nosocomial infection control policy in the aftermath of SARS. This policy extended beyond hospitals into broader communities in 2009 pdmH1N1 emphasizing alcohol-based hand sanitizers to increase feasibility, as alcohol can be easily installed at all entrances to buildings, elevators, and other locations.

In 2020 COVID-19, the Taiwanese government developed a slogan to enhance public awareness: "Disinfect your hands before entering a hospital (avoiding fomite contamination in the hospital) to help our country; disinfect your hands when leaving the hospital to protect yourself and your family (avoiding fomite contamination from hospitals)" (Taiwan-CDC, 2020 d ). This message encourages citizens to participate in the national campaign to fight the pandemic.

Mask wearing developed across Asia in reaction to the 2003 SARS outbreak Hsueh et al, 2004) . As SARS-CoV-2 proved to be transmissible via droplets in high viral doses even before symptoms appear . The Taiwanese public had confidence that face masks were effective at blocking respiratory transmission and therefore chose to wear masks. The government guideline is to reinforce citizens to wear facemasks in eight public venues, including healthcare facilities, markets and shopping centers, schools/educational centers, sport contests and exhibition venues, religious places, entertainment sites, when taking public transportations, participating in human-gathering activities, and in areas where appropriate physical distancing (1.5-meter separation indoors, and 1-meter separation outdoors) is not possible (Taiwan-CDC, 2020 e ).

To explore Taiwanese citizens' (including patients') preventive behaviors regarding the wearing of facemasks and practicing AHH in the 2020 COVID-19 pandemic, we administered an anonymous questionnaire to Taiwanese residents from July 29, 2020 to August 6, 2020 through several channels. Among these 2,416 questionnaires with complete answers for each question, 1,646 (68.1%), 265 (11.0%), and 505 (20.9%) were collected from the web system, local clinics, and others (such as e-mail, Facebook, LINE groups, etc.), respectively.

The questionnaire involved three major parts: (1) demographic characteristics (age, gender, and residential areas of Taiwan); (2) sources of information [government agencies (such as the Taiwan CECC), television, newspaper, internet news, social 

To ascertain the characteristics for the persistent adoption of preventive measures from the 2003 SARS/2009 pdmH1N1 era to the present challenge of COVID-19 in 2020, we developed a scoring system as follows: one point for practicing any one of the officially communicated, right prevention behaviors versus zero points for the neglecting to practice any one of the right preventive behaviors. The highest score possible for the 2020 preventive behaviors was five points. Noteworthily, wearing masks outdoors scored zero points according to government risk communication rules; however, wearing masks during mass gatherings outdoors scored one point.

Because many seriously cautious Taiwanese citizens might have still worn facemasks outdoors, they could potentially have scored four points. Therefore, the "highpreventive behavior group" in 2020 (2020-HPBG) was defined as participants who had over four (>4) points (taking at least four correct prevention measures). In J o u r n a l P r e -p r o o f contrast, the "poor-preventive behavior group" (2020-PPBG) was defined as those who had three or fewer (≤3) points.

Both univariable and multivariable analyses were performed to compare the two aforementioned groups. In univariable analysis, means of age in these two groups were compared using the student's t-test. The association between the prevention groups and the categorical variables was examined using either the chi-squared test or To assess the associations of selected characteristics with the 2020 high preventive behaviors group (HPBG with preventive behavior scores >4), univariable and multivariable logistic regression analyses were performed. All variables found to be significant (p<0.10) through univariable analysis were included in multivariable analysis using the SAS program. Subsequently, multivariable analyses for the where the sample size in this study was also quite small. The best model was selected from the candidate models through a stepwise search. The odds ratios (ORs) were calculated from the coefficients of the regression models, and p-values of < 0.05 were regarded as statistically significant. The crude ORs (cORs) and adjusted ORs (aORs) with 95% confidence intervals (CIs) were reported to show the strength and direction of these associations.

All the data analyses were examined as three independent analyses. The logistic regression results from the SAS program version 9.4 were double-checked by two other persons using the R version 4.0.2 (2020-06-22) and SPSS programs version 22 to enhance internal validity.

Physicians in Taiwan must report any suspected case of COVID-19 to the CECC within 24 h (Taiwan CDC, 2020 f ). Laboratory-confirmed cases in Taiwan are defined as SARS-CoV-2-positive results mainly by real-time reverse transcriptase-polymerase chain reaction (RT-PCR) (Wölfel et al., 2020) and partially by serological tests that quantitatively detect SARS-CoV-2 antibodies in human serum, using commercial kits from Elecsys (Roche Labs, Basel, Switzerland) for identifying asymptomatic cases or late reported cases (Long et al., 2020) .

We calculated the overall monthly incidence rates in 2020 and 2003 and also evaluated them by Student's t-test. Additionally, the total numbers of cases in the five 

This study recruited 2,416 subjects to investigate their behaviors in practicing prevention measures during the 2020 COVID-19 pandemic. After excluding 7 persons younger than 18 years old, 7 non-citizens, and 74 participants who reported not having engaged in protective practices such as mask wearing during both the 2003 J o u r n a l P r e -p r o o f outbreak and 2009 pandemic, the remaining 2,328 individuals were used in the data analysis. Their demographic information was as follows: the overall mean and standard deviation (mean ± standard deviation) of age was 48.9 ± 12.1 years (68.6% of older adults aged 40-64 years and only 4.8% of young adults of <25 years); 60.3% of the subjects were female; and 60.6%, 16.8%, 20.5%, and 2.1% of them were living in northern, central, southern, and eastern Taiwan, respectively ( Table 1) .

The proportion of participants wearing facemask significantly increased from 66.6% during the 2003 SARS/2009 H1N1 pandemic to 99.2% (p< 2.2e-16) and 80.9% (p< 2.2e-16) in indoor and outdoor environments, respectively, during the 2020 COVID-19 pandemic (Figure 2A ).

On the other hand, the proportion of participants disinfecting their hands with alcohol-based hand sanitizer (AHS) significantly increased from 44.2% during the 2003 SARS/2009 H1N1 pandemic to 98.4% (disinfecting hands with AHS on entering a commercial building or restaurant, p< 2.2e-16) and 65.4% (carrying AHS, p= 2.695e-05) during the 2020 COVID-19 pandemic ( Figure 2B ).

Approximately 70.2% of the Taiwanese participants belonged to the "maintaining high preventive behavior group in 2020" (2020-HPBG) against COVID-19 (Table 1) .

To understand the characteristics of the participants in this highly self-motivated preventive behavior group (Table 1) , univariable analysis showed that those with high preventive behaviors during the 2020 COVID-19 pandemic were significantly more likely to be: (1) female; (2) those who received COVID-19-prevention information from the Taiwan CECC; and (3) those who had disinfected their hands with AHS during the 2003 SARS/009 H1N1 pandemics (p<0.01). Moreover, the participants reported that they were more likely to maintain such preventive behaviors, even if there were only sporadic or zero indigenous COVID-19 cases. However, those participants who had received COVID-19 prevention information from newspapers (rather than directly from the official CECC source) were less likely to have high preventive behavior against COVID-19.

Multivariable logistic regression was used to identify the independent characteristics associated with high preventive behaviors against COVID-19 in Taiwanese 

The international spread of the 2020 COVID-19 pandemic has caused major disruption throughout the world. SARS-CoV-2 is highly transmissible and makes necessary public participation in prevention and control measures Lai et al, 2020 b ). In light of this, our study has three unique findings which can be applied at a global scale. First, the percentages of participants wearing facemasks and practicing alcohol-based hand hygiene (AHH) showed statistically significant increases from the 2003 SARS outbreak to the 2020 COVID-19 pandemic, suggesting the importance of combining both prevention measures, which can potentially halt transmission of SARS-CoV-2. Second, encouraging the public has been successful in Taiwan because the participants who maintained in the 2020-high-preventionbehavior-group (2020-HPBG) were mostly females, those who had their questionnaires collected from primary care clinics, those acquiring the information from the government CECC, and those who practiced AHH during the 2003 SARS outbreak implying the importance of risk communication. Third, both the percentages of healthcare-facilities-associated CoV infections and the percentages of the CoV infections in HCWs in 2020 were significantly decreased than those in 2003. The percentage of cases with unidentified sources in 2020 also were significantly more reduced than that in 2003. As 99.2% confirmed wearing facemasks indoors and 98.4% reported practicing AHH while entering a building or a restaurant, these results all together indicate that Taiwan's integrated public health approaches involve not only government-public cooperation but also minimize the transmission between healthcare and non-healthcare settings to successfully avoid lock-downs.

This study is the first to address the significant role of citizens' willingness to practice AHH and wear facemasks in curbing the spread of SARS-CoV-2. Our multivariable analyses showed that both Taiwanese citizens' past AHH practices and J o u r n a l P r e -p r o o f visiting of healthcare facilities were important in maintaining as high preventive behaviors in 2020. Hand hygiene has long been recommended as an inexpensive protective measure for most respiratory viral infections (Fung and Cairncross, 2006; Kampf, 2018) . AHH has been applied in healthcare settings since 2005 when the WHO started paying more attention to hand hygiene (Pittet and Donaldson, 2005) .

Through the 2009 pdmH1N1 to COVID-19 2020, a series of public health policies have resulted in alcohol dispensers being made available at the entrance sites of hospitals and major buildings, and the 2020 public initiative further consolidated AHH as a cultural norm in Taiwan. Fomite transmission has been mostly ignored in emerging infectious diseases until COVID-19 (Santarpia et al., 2020) . In addition to improving compliance of hand hygiene, wearing facemasks are also helpful in curbing fomite transmission through source control of droplet transmission (Lai et al., 2012; Chin et al., 2020) . Our findings on a high percentage of compliance with AHH together with wearing facemasks has proven effective in reducing community spread, particularly in meetings, co-dining, and other social gatherings (Hamner et al., 2020; Feng et al., 2020) . Future projection on the compliance of prevention behaviors under the three scenarios by univariate logistic regression (Supplementary Table 2 ) also showed that the crude odds ratios (CORs) increased from the Scenario 1 with zero indigenous COVID-19 cases to the Scenario 2 with sporadic COVID-19 cases, and to J o u r n a l P r e -p r o o f Scenario 3 if the COVID-19 pandemic lasts for one to two years. However, facemasks have been a controversial issue in Western countries where many citizens think only infected people have to wear facemasks, and prefer to have personal freedom (Olivera-La Rosa et al., 2020) . The percentage of mask-wearing compliance thus is not sufficiently high to effectively curb viral transmission (Chen and Fang, 2020) .

Although comprehensive data is difficult to obtain, progressively more and more evidence has shown that the wearing of facemasks provides community-wide benefits (Lyu and Wehby, 2020; Chu et al., 2020; Cowling et al., 2020; Eikenberry et al., 2020) . Among those studies with controversies, most had ignored the complementary efficacy of facemasks and AHH, and also overlooked the significance of fomite transmission either when the percentage of wearing facemask was inadequate, or when water and soap for hand hygiene were inaccessible (Pittet et al., 2000; Bundgaard et al., 2020) . Interestingly, the total incidence rate of common respiratory-/contact transmitted viral diseases in Taiwan also showed a tremendous decline in 2020, implying the effectiveness of these preventive behaviors to reduce other infections (Galvin et al., 2020) . (Wilson et al., 2005) and the national hand-hygiene campaign in Germany (Reichardt et al., 2013) , have successfully achieved their intended public health goal. Since Taiwan government officials like our citizens to have high percentage of protection behavior compliance after understanding the dynamics of the 2020 pandemic, the CECC had daily press briefings plus social media risk communication covering the most updated epidemiological data in Taiwan and global trends plus the Chinese translation of the WHO guidelines and the CECC guidelines, using Chinese language for detailed information. We found that those participants who maintained high preventive behaviors in 2020, did not only obtain top-down risk communication from the government CECC and public initiatives, but also acquired the appropriate prevention information and guidance from health professionals in medical care institutions.

from government agencies such as early border controls, hotel quarantine policies, innovative health information technology, integrated with a strong national healthcare insurance infrastructure, and free medical treatment for COVID-19 cases, combined with the facilitating of more efficient contact tracing and monitoring of those in quarantine, have helped for interrupting viral transmission effectively . This was further demonstrated by the absence of domestic SARS-CoV-2positive cases for 253 consecutive days (from April 13 to December 21, 2020). It is time for public health agencies worldwide to make rational recommendations on appropriate use of facemasks to complement other preventive measures (Feng et al., 2020) .

From September to November 2020, a near synchronous resurgence of SARS-CoV-2 cases across US, Europe and Asia. Undoubtedly, the resumption of daily activities and gatherings with asymptomatic or pre-symptomatic people accounted for as much as 40 to 60% of total cases (He et al., 2020) . This might have initiated a series of transmission chains and then quickly increased R0 reaching above the threshold of community saturation, overwhelmingly threatening the healthcare system (Yen et al., 2021) , provoking the vicious circle of community-hospital-community and sprouting the second wave of the pandemic. Importantly, most appropriate public health measures, nonetheless, have not yet stopped the transmission efficiently J o u r n a l P r e -p r o o f (Tirachini et al., 2020) . Using population-based prevention measures, public initiatives on wearing facemasks and hand-hygiene disinfection can interrupt the viral transmission early in the Susceptible-Exposed-Infectious-Removed (SEIR) dynamic model (Faranda and Alberti, 2020) . In other words, citizens' preventive behavior is the most cost-effective way to combat disease spread before a safe and effective vaccine is globally available. Our study indicates that the policies governing universal mask usage must achieve a high coverage of the population, requiring coupling with AHH through effective government-civilian cooperation to improve public compliance, particularly in males until awareness is established at a community level (Abate et al., 2020) . Certainly, such a coverage rate must be even higher in areas dominant with the fast-spreading SARS-CoV-2 variants (Lauring and Hodcroft, 2021) . This study has four major limitations. First, this was a retrospective survey, and several important explanatory variables leading to preventive behaviors, were not collected in order to obtain more participants willing to complete the questionnaire.

Second, our study population was recruited via the web system, clinics or social media, which may have resulted in some social desirability bias, recall bias, and/or sampling bias. Nonetheless, our finding is supported by another study showing over 70% of the targeted general population in Taiwan wearing facemasks (Chen et al., J o u r n a l P r e -p r o o f 2020). Third, this study cannot differentiate the combined effect of wearing facemasks and hand-hygiene disinfection versus each one separately. We also cannot exclude the other preventive/control measures such as early border controls. Fourth, we only had limited rather than nationwide seroepidemiological data on the infection rate of SARS-CoV-2 among HCWs to evaluate the infection control at healthcare facilities (Tseng WP et al., 2021) .

In conclusion, our results confirm that Taiwan's integrated intervention strategies, including wearing of facemasks, practicing AHH, and implementing enhanced traffic control bundles in healthcare facilities have increased the effectiveness of the preventive measures and thus protecting HCWs during the COVID-19 pandemic responses (Yen et al., 2021) . Furthermore, early border controls with contact tracing and quarantine measures, government leadership, transparency, widespread risk communication on preventive behaviors, all together have successfully assisted Taiwan in avoiding lockdowns (Greenhalgh et al., 2020; Godlee, 2020) . Given the likelihood of additional waves following reopening plus the appearance of the fastspreading SARS-CoV-2 variants in many countries (Lauring and Hodcroft, 2021) , we recommend our strategies could be adopted internationally and modified to fit into the social/cultural context of other countries to effectively control the COVID-19 pandemic before mass vaccination worldwide is finally achieved.

This study was approved by the Institutional Review Board of Taipei City Hospital (TCH) (no. TCHIRB-10907007-E) on 26 July 2020. Questionnaires and data were fully anonymized to protect participants' privacy, and only aggregated data were used for further analyses and statistical tests.

All the data for this study will be available upon request to the corresponding authors.

This study was supported by grants from the Department of Health, Taipei The bottom parts involve the four major public health policies, which are shown as "B" for border control, with "T" representing policies related to traffic control bundle or enhanced TCB (TCB or eTCB), "M" indicating mask-related policies, and "A" for alcohol-based hand hygiene. All the numbers are based on the order of calendar dates from when the policy started to be implemented (Taiwan Ministry Health and Welfare, 2020). The top three arrow-shaped text boxes represent the three major leaks (see details in the Introduction section). The overall public health prevention measures involve three tiers: 1 st tire with border control, J o u r n a l P r e -p r o o f Table 1 Characteristics of study subjects with high and poor preventive behaviors against SARS-CoV-2 infection Table 2 Crude and adjusted odds ratios (ORs) for the characteristics associated with the high preventive behaviors group against SARS-CoV-2. 

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Age, years (mean ± SD)

Present preventive behaviors Wearing masks indoors or while taking mass transportation 2309 (99.2) 679 (97.8)

Future preventive behaviors Maintaining the COVID-19 preventive behaviors when no indigenous SARS-CoV-2 cases are laboratory-confirmed

AHS, alcohol-based hand sanitizer; HPBG, high prevention behavior group; PPBG, poor prevention behavior group

AHS, alcohol-based hand sanitizer

We would like to sincerely thank medical and public health professionals in Taiwan