Early response to the emergence of influenza A(H7N9) virus in humans in China: the central role of prompt information sharing and public communication
Sirenda Vong a, Michael O’Leary a & Zijian Feng b
a. World Health Organization Office in China, 401 Dongwai Diplomatic Office Building, 23 Dongzhimenwai Dajie, Chaoyang District, Beijing 100600, China.
b. Chinese Centre for Disease Control and Prevention, Beijing, China.
Correspondence to Sirenda Vong (e-mail: firstname.lastname@example.org).
(Submitted: 11 June 2013 – Revised version received: 22 November 2013 – Accepted: 25 November 2013 – Published online: 16 December 2013.)
Bulletin of the World Health Organization 2014;92:303-308. doi: http://dx.doi.org/10.2471/BLT.13.125989
Severe acute respiratory syndrome is a zoonotic viral infection that probably first occurred, in late 2002, in the south of China’s Guangdong province.1 Although the syndrome eventually spread to more than 30 countries – with more than 8000 probable cases and more than 800 deaths reported worldwide – most of the probable cases occurred in mainland China.2
In March 2003, the World Health Organization (WHO) issued a global alert and travel advisory following the identification of clusters of cases of “severe atypical pneumonia” in hospitals in Guangdong and the Hong Kong Special Administrative Region in China and Hanoi in Viet Nam.2 By April 2003, a coronavirus had been identified as the infectious agent responsible for this pneumonia and the pneumonia itself had been called severe acute respiratory syndrome (SARS).3
The early stages of the SARS epidemic went largely unnoticed. Many clinicians were unaware of the epidemic threat posed by the “atypical pneumonia”; cases went undetected because of poor surveillance and an inadequate network of clinical laboratories, and poor information transfer meant that the epidemic had gained considerable strength before it was recognized.4 China’s delayed detection of the outbreak and – in particular – its poor level of communication during the response to the emergency probably led to many avoidable cases of SARS and damaged China’s economy and reputation.
Heavy criticism of China’s response in the early stages of the SARS outbreak led to huge investments in public health by the Chinese government. There has been substantial investment in public health infrastructure, such as new buildings, improvements in Internet connectivity and the purchase of technically advanced equipment. The government has also supported the development of the national Centre for Disease Control and Prevention (China CDC) and the provincial and county-level Centres for Disease Control and Prevention. China CDC has remodelled its surveillance of infectious diseases5 – with an emphasis on severe respiratory diseases and the development of a national influenza surveillance network. The Chinese health authorities have initiated training programmes in field epidemiology – at the national, provincial and municipality levels – and strengthened emergency preparedness and response capacity. The detailed investments that the Chinese government has made to improve the surveillance and control of “high-priority” infectious diseases have been well documented.6
The aims of China’s post-SARS investments in public health were to improve disease surveillance and make the country’s response to future disease outbreaks both swift and effective. To see if these aims had been achieved, we investigated China’s early response to the emergence of avian influenza A(H7N9) virus in humans during April 2013. We compared the chronology of A(H7N9)-related events and responses with the level of A(H7N9)-related public attention. The latter variable was evaluated using Sina Weibo (SINA Corp., Shanghai, China), which is the largest social media network in China. Sina Weibo – which offers services similar to those of Twitter (Twitter Inc., San Francisco, United States of America) but in Chinese – is used by more than 30% of Chinese Internet users. In December 2012, Sina Weibo had more than 500 million registered users and dealt with about 100 million new messages each day.7 For our study, we searched Sina Weibo daily – during the outbreak – for new A(H7N9)-related postings, by using the Chinese words for “H7N9” and “bird flu” as the search terms.
Local setting and relevant changes
On 31 March 2013, China’s National Health and Family Planning Commission notified WHO of three human infections with A(H7N9): two in the city of Shanghai and one in Anhui province. By 7 November 2013, 139 confirmed cases of human infection with A(H7N9) – including 45 fatal cases – had been reported in mainland China – in 10 provinces and two municipalities.8 Although the animal reservoir of A(H7N9) infection involved in this outbreak has yet to be confirmed, it is probably poultry and most transmission to humans probably occurs in markets selling live poultry. The Chinese Ministry of Agriculture has already tested more than 1.2 million birds and other animals – from more than 69 000 different sites – for A(H7N9). By 9 December 2013, only 68 non-human samples had been found positive for the virus. The 68 positive samples – which were all collected in markets selling live poultry – came from poultry, a pigeon or feathers, bird faeces, cages or other “environmental” sources within the market.9
Although the investigation of more than 3000 close contacts of the confirmed cases has not revealed any evidence of sustained human-to-human transmission of the A(H7N9) virus, there is evidence of some human-to-human transmission among at least three family clusters.10–12 China’s National Health and Family Planning Commission and WHO remain concerned about the threat posed by the A(H7N9) virus because it is an avian virus that seems to have recently infected humans, causes serious disease in humans and has genetic characteristics that indicate that it has enhanced capacity for mammalian infection.13,14 It remains unclear, however, if A(H7N9) is common in poultry. It has been difficult to detect the virus in poultry or other birds because the virus causes little avian pathogenicity – and may therefore spread undetected within and between flocks of birds.
As with A(H5N1),15 new sporadic cases and small clusters of human infection with A(H7N9) infection are likely to continue. WHO remains alert to any changes in the behaviour of the A(H7N9) virus in humans and poultry and the resistance of the virus to antiviral drugs will be carefully monitored. More or larger clusters of human cases – or evidence of sustained human-to-human transmission – could indicate that the virus is acquiring qualities compatible with pandemic potential.
The 2013 outbreak of human infection with A(H7N9) appears to have begun when a family cluster of three cases of severe pneumonia – which was recognized as abnormal by astute clinicians – triggered an alert to the Shanghai Centre for Disease Control and Prevention on 26 February 2013.13 The influenza A virus found in the cluster did not match any known subtype. Within 4 weeks of the cluster being reported, staff at the China CDC – the WHO Collaborating Centre for Reference and Research on Influenza (WHO CCRRI) in Beijing – had discovered that the virus belonged to a novel strain: A(H7N9). This viral strain was identified much more quickly than SARS coronavirus or A(H5N1), which took about 5 and 3 months to identify, respectively.4,16 The viral genomic sequences from the first three known human cases of A(H7N9) infection were published, via the Global Initiative on Sharing Avian Influenza Data, on 31 March 2013. On the following day, the National Health and Family Planning Commission enhanced surveillance of pneumonia of unknown etiology and influenza-like illnesses across China. Two days later, molecular diagnostic kits were distributed to the National Veterinary Services, the laboratories in provincial Centres for Disease Control and Prevention and clinical pathology laboratories in major hospitals. By 3 April 2013 – just 4 days after WHO had been notified of this family cluster – the relevant guidelines regarding infection control, clinical management and surveillance had been updated and the updated guidelines had been issued. On the same day, the national government established a taskforce – for the control of A(H7N9) – that included representatives from 16 ministries and was led by the National Health and Family Planning Commission. Staff at the Shanghai Centre for Disease Control and Prevention quickly identified markets that sold live poultry to be the main locations of human infection with A(H7N9). On 6 April 2013, the city’s mayor ordered all such markets in Shanghai to be closed. Isolates of the virus were sent to other WHO CCRRIs on 10 April 2013. This sharing led to the investigation of viral mutations and the development of new probes and primers for use in diagnostic tests. As the number of cases continued to increase, China CDC conducted a series of rapid risk assessments to address the likelihood of sustained human-to-human transmission and further cases of human infection. Although these initial assessments were disseminated to all of China’s Centres for Disease Control and Prevention – and were generally similar to the risk assessments that were made, independently, by WHO – they were not released publicly.
By the second week of April 2013, the China CDC was regularly sharing data – on the human infections with A(H7N9) – with WHO’s Regional Office for the Western Pacific, WHO’s headquarters in Geneva and other members of the Global Outbreak Alert and Response Network. New cases of human infection and the type and collection site of each A(H7N9)-positive animal sample were promptly reported on official websites. This allowed members of the public to follow the epidemic situation. There was an initial delay in the collection and sharing of the detailed information needed to evaluate the risks of human-to-human transmission accurately and determine the underlying medical conditions of patients with symptomatic A(H7N9) infections. Nonetheless, the first detailed virological and epidemiological results of investigations on the outbreak were published in scientific journals in mid-April 2013.11,13
To improve clinical management of severely ill patients and to plan for appropriate research, WHO facilitated discussion between key Chinese clinicians and international experts on influenza. WHO and China’s National Health and Family Planning Commission jointly coordinated a mission by internationally-recognized influenza experts, who visited Beijing and Shanghai from 19 to 25 April 2013 to assess the A(H7N9) situation.17 The main aims of this mission were to provide expert opinions on the level of the A(H7N9) threat and encourage investigators to close any relevant gaps in our critical knowledge and understanding.
From the first recognition of the outbreak, WHO participated – with China’s National Health and Family Planning Commission – in national risk assessments and press conferences. Some outbreak-related events appeared related to increases or decreases in the daily numbers of A(H7N9)-related messages posted on Sina Weibo. The first main surge in the number of cases reported daily – on 4 April 2013 – and the report of the first case to be identified in Beijing – on 13 April 2013 – were followed by dramatic rises in the number of A(H7N9)-related postings. In contrast, a press conference on 8 April 2013 – presented jointly by WHO and the National Health and Family Planning Commission – and a public announcement on 17 April 2013 – on the WHO’s experts’ mission to China – each appeared to be associated with a subsequent fall in the daily number of such postings (Fig. 1).
Fig. 1. Events during emergence of A(H7N9) virus as human pathogen and numbers of related postings on social media network, China, 2013
The main lessons learnt are summarized in Box 1. China’s prompt communication and collaboration with WHO in assessing and responding to human infections with the novel influenza A(H7N9) virus were the result of sound preparedness and close and continuing international collaboration. Above all, China’s apparently effective response to the A(H7N9) outbreak in 2013 should be perceived both as one of the major returns on the investment that China has made in public health since the SARS epidemic in 2003 and as a useful – if still not optimal – model for responses to similar outbreaks in the future. The International Health Regulations that were formulated in 2005 – partly in response to the emergence of SARS – have helped catalyse a standardized international framework in which WHO provides a system to enable prompt information sharing.
Box 1. Summary of main lessons learnt
- Countries should invest in preparedness to respond to emerging and existing disease threats by strengthening the relevant infrastructures, surveillance systems and response capacity.
- Risk assessments should be released publicly and should not jeopardize authors’ plans to publish in scientific journals.
- Coordination between public health and veterinary services would be stronger during an emergency if these services had already undertaken joint preparedness planning.
Epidemics caused by emerging infectious diseases often generate substantial public concern. By publicly communicating about the risks – from the early stages of a possible epidemic – health authorities can help to build trust in governments, public health workers and the public. The public needs to have prompt access to appropriate public health information.
The use of Sina Weibo and similar social networks to monitor public interest in a health threat – or any other health topic – and also, perhaps, to disseminate health education merits further research. In our study, certain major events during the outbreak were associated with major increases in A(H7N9)-related postings but some more formal announcements about the outbreak appeared to reduce public interest. It seems possible that the formal announcements simply reduced public concern about the outbreak.
Risk assessment is a systematic process that can be used to assess the level of threat and facilitate the selection of the most appropriate interventions in an often-complex situation. Such assessment often helps to identify gaps in our critical knowledge and weaknesses in the relevant infrastructure. It may also help to identify the better strategies for closing the knowledge gaps and strengthening infrastructures. As the A(H7N9) virus emerged as a public health emergency of international concern, the public health community and the threatened public expected to be kept informed of all of the relevant data. The findings of national risk assessments should therefore be rapidly released publicly and – in due course –published in full in scientific journals. Journal editors should be willing to publish articles based on data that – for public benefit – have already been released to the public in summary form.
China’s prompt response to the emergence of the A(H7N9) virus as a human pathogen – which spanned multiple governmental departments and ministries at national, provincial and municipal level – was mainly the result of strong leadership in a critical situation. We believe that strong and well integrated coordination between veterinary and public health services can be best sustained by joint preparedness planning and the creation of joint response systems – as already promoted by international health organizations under the “One Health” approach.18
- Parashar UD, Anderson LJ. Severe respiratory syndrome: review and lessons of the 2003 outbreak Int J Epidemiol 2004; 33: 628-34 http://dx.doi.org/10.1126/science.279.5349.393 pmid: 9430591.
- WHO issues global alert about cases of atypical pneumonia: cases of severe respiratory illness may spread to hospital staff [Internet]. Geneva: World Health Organization; 2003. Available from: http://www.who.int/csr/sars/archive/en/ [accessed 9 December 2013].
- Peiris JS, Lai ST, Poon LL, Guan Y, Yam LY, Lim W, et al., SARS study group, et al. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 2003; 361: 1319-25 http://dx.doi.org/10.1016/S0140-6736(03)13077-2 pmid: 12711465.
- Feng D, de Vlas SJ, Fang LQ, Han XN, Zhao WJ, Sheng S, et al., et al. The SARS epidemic in mainland China: bringing together all epidemiological data. Trop Med Int Health 2009; 14: 4-13 http://dx.doi.org/10.1111/j.1365-3156.2008.02145.x pmid: 19508441.
- Yang W, Li Z, Lan Y, Wang J, Ma J, Jin L, et al., et al. A nationwide web-based automated system for outbreak early detection and rapid response in China. Western Pac Surveill Response J 2011; 2: 10-5 pmid: 23908878.
- Wang L, Wang Y, Jin S, Wu Z, Chin DP, Koplan JP, et al., et al. Emergence and control of infectious diseases in China. Lancet 2008; 372: 1598-605 http://dx.doi.org/10.1016/S0140-6736(08)61365-3 pmid: 18930534.
- Ong J. China’s Sina Weibo grew 73% in 2012, passing 500 million registered accounts [Internet]. Amsterdam: The Next Web; 2013. Available from: http://thenextweb.com/asia/2013/02/21/chinas-sina-weibo-grew-73-in-2012-passing-500-million-registered-accounts [accessed 22 September 2013].
- Human infection with influenza A(H7N9) virus in China – update [Internet]. Geneva: World Health Organization; 2013. Available from: http://www.who.int/csr/don/2013_11_06/en/index.html [accessed 9 December 2013].
- Updates on national surveillance of A(H7N9) influenza virus in animals [Internet]. Beijing: Ministry of Agriculture; 2013. Available from: http://www.moa.gov.cn/zwllm/zwdt/201305/t20130523_3471497.htm [accessed 9 December 2013]. Chinese.
- Rudge JW, Coker R. Human to human transmission of H7N9. BMJ 2013; 347: f4730 http://dx.doi.org/10.1136/bmj.f4730 pmid: 23920349.
- Li Q, Zhou L, Zhou M, Chen Z, Li F, Wu H, et al., et al. Preliminary report: epidemiology of the avian influenza A (H7N9) outbreak in China. N Engl J Med 2013130424140638006 http://dx.doi.org/10.1056/NEJMoa1304617 pmid: 23614499.
- Qi X, Qian YH, Bao CJ, Guo XL, Cui LB, Tang FY, et al., et al. Probable person to person transmission of novel avian influenza A (H7N9) virus in eastern China, 2013: epidemiological investigation. BMJ 2013; 347: f4752 http://dx.doi.org/10.1136/bmj.f4752 pmid: 23920350.
- Gao R, Cao B, Hu Y, Feng Z, Wang D, Hu W, et al., et al. Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med 2013; 368: 1888-97 http://dx.doi.org/10.1056/NEJMoa1304459 pmid: 23577628.
- Chen Y, Liang W, Yang S, Wu N, Gao H, Sheng J, et al., et al. Human infections with the emerging avian influenza A H7N9 virus from wet market poultry: clinical analysis and characterisation of viral genome. Lancet 2013; 381: 1916-25 http://dx.doi.org/10.1016/S0140-6736(13)60903-4 pmid: 23623390.
- Risk assessment summary for H5N1 [Internet]. Geneva: World Health Organization; 2013. Available from: http://www.who.int/influenza/human_animal_interface/HAI_Risk_Assessment/en/index.html [accessed 9 December 2013].
- Subbarao K, Klimov A, Katz J, Regnery H, Lim W, Hall H, et al., et al. Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. Science 1998; 279: 393-6 http://dx.doi.org/10.1126/science.279.5349.393 pmid: 9430591.
- China–WHO joint mission on human infection with avian influenza A(H7N9) virus. 18–24 April 2013. Manila: World Health Organization; 2013. [Internet]. Available from: http://www.who.int/influenza/human_animal_interface/influenza_h7n9/ChinaH7N9JointMissionReport2013.pdf [accessed 26 May 2013].
- One Health Initiative will unite human and veterinary medicine [Internet]. One Health Initiative; 2013. Available from: http://www.onehealthinitiative.com [accessed 30 September 2013].