key: cord-0914094-qhtvewxw
authors: Zhou, Lei; Wu, Zunyou; Li, Zhongjie; Zhang, Yanping; McGoogan, Jennifer M; Li, Qun; Dong, Xiaoping; Ren, Ruiqi; Feng, Luzhao; Qi, Xiaopeng; Xi, Jingjing; Cui, Ying; Tan, Wenjie; Shi, Guoqing; Wu, Guizhen; Xu, Wenbo; Wang, Xiaoqi; Ma, Jiaqi; Su, Xuemei; Feng, Zijian; Gao, George F
title: 100 Days of COVID-19 Prevention and Control in China
date: 2020-06-05
journal: Clin Infect Dis
DOI: 10.1093/cid/ciaa725
sha: 892366441d413a46cd28b3044b078dbe9176fd41
doc_id: 914094
cord_uid: qhtvewxw

The epidemic of novel coronavirus diseases was first reported in China in late December 2019 and has been brought under control after some two months in China. However, it has become a global pandemic and the number of cases and deaths continues to increase outside of China. We describe the emergence of the pandemic, detail the first 100 days of China’s response as a Phase 1 Containment followed by Phase 2 Containment strategy, and briefly highlight areas of focus for the future. Specific, simple, and pragmatic strategies used in China for risk assessment, prioritization, and deployment of resources are described. Details of implementation, at different risk levels, of the traditional public health interventions are shared. Involvement of society in mounting a whole country response and challenges experienced with logistics and supply chains are described. Finally, the methods China is employing to cautiously re-start social life and economic activity are outlined.

A cluster of cases of pneumonia of unknown etiology raised concerns in Wuhan, China in late December 2019 [1] , and on March 11, 2020 , what is now known as coronavirus disease 2019 was declared a global pandemic by the World Health Organization (WHO) [2, 3] .

Worldwide, >5.7 million cases and >357 thousand deaths have been reported [4] , far-reaching economic impacts are being felt, and geopolitical repercussions loom [5] . In this article, we describe the emergence of the pandemic, detail the first 100 days of China's response as a Phase 1 Containment followed by Phase 2 Containment strategy, and briefly highlight some areas of focus for the future.

The Hubei health authority reported a cluster of pneumonia to Chinese Center for Disease Control and Prevention (China CDC) on December 30, 2019 [1] , which triggered the dispatch of a rapid response team from Beijing. Initial clinical investigation ruled out major known pathogens including influenza, avian influenza, adenovirus, severe acute respiratory syndrome coronavirus (SARS-CoV), and Middle East respiratory coronavirus (MERS-CoV) while early epidemiological investigation pointed to an unknown animal source at Huanan Seafood Wholesale Market. On January 1, 2020, the market was closed, and scientists raced to discover the pathogen [6] [7] [8] . A task force for virus identification was established across several institutes in China. In early January, Chinese scientists identified a novel virus, specifically a β-coronavirus related to known bat coronaviruses and to SARS-CoV and MERS-CoV [9] [10] [11] [12] . The identity of the novel coronavirus was announced on January 7, with a clear virus morphology under electron microscopy, and whole gene sequences were shared on January 10 [8], kicking off two parallel workstreams-characterization of the virus and development of diagnostics.

Characterization of the viral genome by Chinese scientists over the ensuing week revealed it encoded 27 proteins and confirmed it is more similar to SARS-like bat coronaviruses than to other human coronaviruses [13, 14] . Notably, the most divergent portion of the genome is in an area that interacts with host cell receptors [13] . However, an analysis of >100 sequences indicated that as of mid-February very little mutation of the virus had yet occurred [8] . The 

On January 20, China's National Infectious Diseases Law was revised to include COVID-19 as a Class B notifiable disease and its Frontier Health and Quarantine Law was amended to support the response. These actions coincided with the start of widespread testing and greatly enhanced collection and use of data. COVID-19 data are collected in 4 complementary information systems that were already operational prior to this outbreak and used for routine management of other infectious diseases ( Table 1 ) [15] [16] [17] . Thus, health and public health personnel immediately began using them to collect data on COVID-19.

[Insert Table 1 here.]

The WHO China Country Team in Beijing was first informed of the outbreak on December 31 [4] . On January 3, top government officials, including the highest-level leaders and epidemiologists within National Health Commission (NHC) and China CDC, began regularly sharing information with WHO leaders and technical staff. At that time, there were 44 known cases [3] . The WHO China Country Team made its first field visit to Wuhan on January 20-21. China also sent delegations to WHO on January 22-23 and 30 to share information and discuss the outbreak and response [18, 19] . To promote dissemination of information (and limit misinformation and infodemic development [20] ) within China, officials focused on being transparent and thorough, targeting messages to intended audiences, and using suitable media channels. Starting on January 21, official epidemic information has been released daily to the public by NHC [21] , and starting January 27, the Joint Prevention and Control Mechanism of the State Council (JPCMSC) has held a daily press conference. Early evaluations have suggested that these communications were reaching citizens. For example, a survey of ~7,000 Hubei residents conducted on January 27 to February 1 found 90% had the necessary COVID-19 knowledge [22] . 

The availability of test kits, the rapid scale up of testing and reporting, and the deployment of case finding and contact tracing teams enabled crucial epidemiological advancements, first with small case series [23] [24] [25] [26] , and then larger ones [1, 6, 27, 28] . Together with studies targeting specific epidemiological questions [28] [29] [30] [31] [32] [33] , this research yielded several critical findings: 1) despite broad age distribution, elderly people were most vulnerable, 2) while ~80% of cases were mild, higher case fatality rate was associated with underlying health conditions and severe or critical illness, 3) humanto-human transmission was occurring within close contacts causing infection among health workers and in households, 4) mean incubation period was 5 days, infectious period began before symptom onset, and asymptomatic cases existed, and 5) basic reproductive number (R 0 ) was >2 [1, 6, [23] [24] [25] [26] [27] [28] [29] [30] [31] [32] [33] .

Rapid geographic spread was occurring and by January 20, >600 counties in 30 provinces were reporting cases. On February 11, ~1,400 counties in all 31 provinces had cases [1] . However, the epidemiological curve of daily numbers of confirmed cases at the national level indicated that China's epidemic peaked in late January (Figure 1 ) [1, 6] , and an overall steady decline in domestically acquired cases was observable from January 26 through March 10.

[Insert Figure 1 here.]

The first cases found outside China were reported by Thailand on January 13, Japan on January 15, and the Republic of Korea on January 20 [4] . By January 31, ~9,800 cases had been confirmed, 106 of which were outside of China, mostly in Western Pacific and Southeast Asia region countries.

However, 12 cases were found in Europe (including 2 in Italy), and 9 cases were reported in North America (6 in the United States) [4] . Just 1 month later, on February 29, there were ~85,000 cases globally, and although 93% were in China, the rate of new infections had slowed dramatically ( 

China met the challenge of COVID-19 by essentially mobilizing "everything." Taking what has been described as a "whole-of-government, whole-of-society approach," the Phase 1 Containment strategy was launched on January 15, 2020. The Central Committee and the State Council triggered a national emergency response posture and established the JPCMSC [33] . The JPCMSC is composed of 9 task forces covering 32 departments and charged with leading inter-agency and cross-sector coordination and communication for the COVID-19 response. On January 21, the JPCMSC was elevated to a national institutional arrangement with NHC as the coordinator of 32 cooperating departments. Top officials lead the task forces with clear duties and divisions of labor. Beginning on January 25, the JPCMSC issued many notices, technical guidelines, and work plans on prevention and control, scientific research, delivery of equipment and supplies, interpretation of policies, and responses to public concerns. A supervisory team was stationed in Wuhan on January 27, and in all provinces on February 3. By January 29, all provinces had declared public health emergencies and launched local Phase 1 Containment strategies [34] .

As the quantity and quality of information improved and as it bettered understanding of the epidemic, Chinese officials were newly able to conduct risk assessments and set priorities, resulting in the socalled "4 Lines" (Figure 2A) and "4 Levels" (Figure 2B ). These simple dictates set out a pragmatic strategy for containment that was easy to understand and easy to communicate. They guided allocation of resources and public health assets to prevent, detect, isolate, treat, and report cases and to trace and quarantine contacts.

[Insert Figure 2 here.]

Without safe and effective treatments or a proven vaccine, China had to rely solely on traditional, non-pharmacological (public health) interventions (NPIs). Controlling sources of infection, blocking transmission, and protecting susceptible populations were crucial. China's public health sector was given a mission summed up by the "4 Earlies" (Figure 2C ). Like the 4 Lines and the 4 Levels, these simple objectives set out a pragmatic strategy that was easy to disseminate and comprehend, and that could guide personnel and resource allocation. The 4 Earlies (ie, early detection, reporting, isolation/quarantine, and treatment) were implemented quickly and thoroughly with initial focus on Wuhan, that was expanded according to the 4 Lines and 4 Levels. The 4 Earlies generated a lot of information ( Table 1) , which improved the evidence base for strategic decision making and treatment and prevention protocols. Early detection took the form of active testing campaigns, which found A c c e p t e d M a n u s c r i p t 7 25,645 confirmed cases, 144,992 suspected cases, and 14,870 close contacts in Wuhan, and passive surveillance, which found 913 confirmed cases, 710,000 close contacts, and 658,000 people seeking entry nationwide. Early reporting drove the interval from illness onset to case reporting down to 4 days from 11 in Wuhan and to 4 days from 8 nationwide (January versus February). Early isolation and quarantine drove the interval from illness onset to isolation down to 4 days from 8 in Wuhan and 2 days from 6 nationwide.

National treatment and prevention protocols were developed, and by March 31, they had been revised many times to incorporate new evidence. For example, when many suspected cases in Wuhan and Hubei could not immediately be confirmed because of insufficient testing capacity, diagnostic criteria were changed to create an additional case category and facilitate faster isolation and treatment in hospitals. Once the testing backlog was cleared, case definitions were returned to their original forms.

Other examples include broadening travel history criteria, detailing clinical manifestations of mild cases, and integrating serological testing. Also, when asymptomatic and pre-symptomatic cases were discovered [31] , new case definitions were added, and when viral shedding was found before symptoms, contact tracing methods were updated.

To support the Phase 1 Containment strategy, the Chinese government called upon its 1.4 billion citizens to participate and society helped in the "5 Reliable Forces"-sub-district staff, community grid staff, medical staff, police and other security staff, and staffing a variety of other activities.

Citizens assisted with COVID-19 screening, controlling movement of people and goods, supervising critical activities, and helping with education and communication. Society was also mobilized to improve personal hygiene, support environmental disinfection, and comply with new community containment and social distancing rules. All citizens were asked to comply with 3 major personal hygiene and infection protection measures-hand washing, respiratory etiquette, and mask wearing [35] . For persons with occupational exposure risks, such as health, transportation, and food service workers, N95 masks were recommended.

Chinese authorities began to move toward community containment on January 15, when the first cases of COVID-19 were found outside of Wuhan. This included moderate movement restrictions and partial closure of major public venues, restricting travelers with fever leaving from airports and railway stations. Then, on January 23, Wuhan was subjected to a "lockdown" (or cordon sanitaire).

Fifteen other Hubei cities followed over January 24-26, putting ~60 million citizens into community containment. Movement was strictly controlled into and out of these cities and forbidden within the cities without special permission. This measure was complimented by nationwide social distancing measures. The New Year holiday, planned for January 25-31, was mandatorily extended to February A c c e p t e d M a n u s c r i p t 8 10 and all public gatherings were cancelled, postponed, or reduced; businesses, schools, entertainment venues, and restaurants were closed; most manufacturing was stopped; and mass transit was curtailed.

Lessons from the SARS outbreak in 2003 [36, 37] , and the H1N1 pandemic in 2009 38] , taught China the value of evaluating response effectiveness, finding problems early, and decisively, rapidly, fully implementing response plans. So, it was immediately apparent that critical bottlenecks and supply challenges needed to be resolved. For example, Wuhan's hospitals were forecasted to run out of beds in early February, just as thousands of patients were being diagnosed each day. So, on February 5, the first 3 "Fangcang" shelter hospitals opened. Over the next few weeks, 13 more of these large temporary field hospitals were built to handle the surge of new patients. This approach facilitated the hospitalization and isolation of all diagnosed COVID-19 patients and avoided problems with home isolation-exposure of family members and lack of monitoring [39] . The surge also quickly depleted equipment and supplies. So, ventilators, oxygen, medicines, and personal protective equipment were shipped in from around the nation and manufacturing was ramped up. Also, >40,000 health workers were brought into Hubei from other provinces. All were provided daily transportation, food, and accommodation. Finally, when concerns emerged about food and supplies for citizens in lockdown, these items along with a monetary allowance, surgical masks, hand sanitizer, and thermometers were provided.

By February 17, China was 23 days beyond the peak of its epidemic curve (Figure 1 ) and numbers of daily new cases had fallen below 800. Yet, the nation was still in danger. Asymptomatic infection was poorly understood, much of the nation remained unexposed and susceptible, and the durability of immunity was unknown. Hence, rather than stop the response, it was revised to better target current conditions and new objectives. This new Phase 2 Containment strategy aimed to avoid a resurgence in local cases (ie, a so-called second wave), prevent importation of cases (which had been increasing since the first imported case was reported on January 30), and facilitate the restart of work and life. (Figure 2A) . In high-risk areas (Level 4), it required strong emphasis on prevention of local and imported cases using strict control measures, recognizing that these areas will only gradually recover. In medium-risk areas (Level 3 or Level 2), prevention of local and imported cases should remain a high priority, but orderly return-to-work activities should begin as soon as possible. Finally, in low-risk areas (Level 1), guidance was for prevention of case importation only.

Full resumption of work and production was immediately encouraged (Figure 2B) . Several additional notices, guidelines, and technical documents have been issued since, all aimed at supporting safe return to work for China's citizens.

To shift out of social distancing and community containment, leaders called for an extremely high degree of public health readiness to handle new cases. Therefore, the 4 Earlies ( Figure 2C ) were strongly emphasized. Testing was dramatically expanded again, this time with serological testing to complement nucleic acid testing. National testing program scale up to drive early detection promoted the second of the 4 Earlies, early reporting. However, reporting in Phase 2 Containment has taken on a larger role-while case reporting is still paramount, reporting negative results has become important too. To facilitate the careful loosening of strict movement controls, all citizens now carry electronic "health codes" on their mobile devices-a red, yellow, green system of QR codes that denotes their personal COVID-19 risk thereby dictating the degree to which they can move about and return to A c c e p t e d M a n u s c r i p t 10 work. Health code color changes based upon testing frequency and results, proximity to people with different colored health codes, and responses to daily risk surveys. Another way that movement restrictions and return-to-work efforts are facilitated is through a "point-to-point" labor cooperation mechanism. Combining public health protections with employer-provided information, migrant workers are now safely returning to work using a new cross-regional, non-stop chartered car (railway and highway) transport mode. This door-to-door service limits exposures, provides testing, and facilitates rapid tracking and contact tracing should an outbreak occur.

The first imported COVID-19 case was reported on January 30. By mid-February, occasional cases were being detected among travelers entering from abroad (Figure 1) . The rapidly expanding pandemic put increasing pressure on China's borders and a marked rise in infections detected at entry points has been observed since March 1. Although daily total cases found at border crossings and customs and immigration installations has yet to exceed 75, these figures are worrisome for their potential to spark a new outbreak. All travelers entering China are required to be quarantined under the supervision of security forces at their own expense in designated facilities or immediately deported. Emphasis has been placed on entrants to Beijing (Line 2) and more recently the remote northeast border shared with the Russian Federation. On March 28, China also suspended entry by foreign nationals holding visas or residence permits.

During the first 100 days of COVID-19 in China, the nation experienced a skyrocketing outbreak, but quickly initiated a layered, targeted, tailored, and pragmatic response strategy that has brought the epidemic under control. Much has been learned yet many unknowns make the future uncertain, especially our understanding of the virology of this coronavirus. Prevalence of asymptomatic infection and its contribution to transmission; pathogenesis of disease, optimal supportive care, and means of reducing mortality; and development and durability of immunity all require extensive further study. No therapeutics are yet proven safe and effective, and vaccines are still at least 1 year away. All these areas must be the focus of our future. Furthermore, retrospective analysis of the global response to this pandemic must foster international cooperation in joint pandemic preparedness for the future. 

The authors declare no conflicts of interest. Level 3, mid-high-risk counties, had clusters of cases. Level 4, high-risk counties, had ongoing community transmission. Goals for each of these levels were additive. For example, in Level 3, midhigh risk areas, the goal was not only to stop local transmission, but also to prevent local transmission and strictly prevent importation.

[C] The 4 Earlies were public health mission areas-early case detection, early case reporting, early case isolation and contact quarantine, and early supportive care. *Surveillance networks highlighted here are supplements to information systems detailed in Table 1 .

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