Delays in communicating emergency information to the public has been a persistent problem in China. It was addressed by national legislation to encourage openness and some progress has been made especially on human-human epidemics. The lesson had to be relearned with SARS since veterinary epidemics and animal-human secrecy continued to some degree even after some progress had been made in communicating epidemics among humans.
Chinese journalists at the time pointed to a cover-up by officials who were simultaneously trying to address the problem locally while trying to prevent news of the problem from spreading. This may be because that they don’t want their county to become known as a pariah and the problems that can bring them in trade with neighboring areas as a panic spreads.
China made important reforms in the communication of emergency information to the public since the 1990s rural Henan Province HIV epidemic cover-ups and the 2003 SARS crises. There remain problems however public health professionals and international organizations have noticed sharp improvements in the speed and communication of information about epidemic outbreaks since that time.
I drafted this report when I was TDY at US Consulate Chengdu in 2005. A colleague at Embassy Beijing Ag section suggested WHO Geneva [or perhaps another UN agency there interested in veterinary matters, don’t remember] would be interested, so I got permission to release my report at the time back in September 2005 and then shared it with Geneva.
Sources: The report is based on a visit to Danshan, a small town in the affected area, talking with people there, reading official notices posted at the Danshan market at the time, mainland Chinese and Hong Kong press, and a report on a national conference on the epidemic published on the website of the Guangdong Provincial CDC. Photos from my September 2005 to the township of Danshan in the affected area follow the report.
Here is a short study of the June – August 2005 Sichuan Province pig –
human Pig Steptococcus Suis epidemic.
A Word document with photos from a visit to Danshan that gives some
context is attached. Also attached are some important primary sources —
a collection of official and media reports I collected into a 40 page
Chinese language Word document and a 70 page Powerpoint presentation by
Guangdong Province epidemiologists based on an urgent early August 2005
PRC national experts meeting on the Sichuan human – pig epidemic.
The basic picture that emerges is a slow response on the local level and
a fast response on the provincial and national levels. It took some time
for local physicians to realize that there was an epidemic underway.
Gathering together and analyzing all the different data from complex
perhaps puzzling cases and eliminating many possible hypotheses to
determine that the patient has an epidemic illness takes time so I am
not certain how much of the early part of the delay was avoidable.
The second part of the local delay seems to have been caused by reluctance
of local officials to tell provincial officials that they had a problem.
For example, the Yanjiang district authorities waited one week after
beginning an aggressive campaign of sanitary disposal of pigs and
checking on pig health in the countryside before informing the Sichuan
Province Food and Livestock Bureau. Poverty and regulations that put the
burden for disposing of pigs that died of illness on peasants seem to be
part of the problem. Peasants in the area where the S. Suis epidemic
broke out earn an average annual cash income of 2500 RMB (US 375 per
year). Losing a pig is a great economic blow to these peasants. The
temptation to sell the carcass of a pig that died of illness is great.
Raising pigs and ducks are the mainstays of the local economy in this
part of Sichuan. Just the kind of place that epidemiologists warn could
be the starting point of a new epidemic. Many millions of peasants live
in close proximity to their several pigs and other livestock, increasing
the chances for transmission of old illnesses or new emerging illnesses
between humans and livestock. Most of the pigs sold in Sichuan seem to
be raised by peasants in small scale farms with perhaps three to ten
pigs, although there are a few large scale operations where several
hundred pigs are raised on a farm.
Some statements that have appeared in the PRC media quoting local
officials to the effect that the peasants need to understand science
better and learn raise the pigs in healthier conditions are not wrong
but still have a “let them eat cake” flavor to them. Closer attention to
the economic and other interests of the peasants will help reduce the
chances of new diseases emerging and intervening more effectively at an
early stage to prevent new diseases from spreading. The regulation
mentioned above that makes peasants pay for the sanitary burial of pigs
that die of illness — this is a big disincentive to reporting of animal
Severe problems of local government finance, poor
communication between veterinarians and public health, and the
uncooperative relationship between local officials and peasants (to put
it mildly) in many regions are systemic problems that complicate
response to epidemics at the local and regional levels. These serious
local problems hinder epidemic response (and the severity of these
problems varies very greatly from place to place, but are generally
worse in poorer areas) despite all the determination of the PRC central
and provincial governments to improve its response to epidemics.
2005: WEST CHINA’S PIG EPIDEMIC: FACT & FICTION
The June – August 2005 pig-human Pig Streptococcus Suis epidemic in an impoverished district of Sichuan province where poor peasants, pigs, chickens and other livestock live in close proximity can help understand response to epidemics in China. There were significant delays in this story. The normal delay caused by the time needed for physicians and local health authorities to make the correct diagnosis, put together case information from various sources and to conclude that an epidemic is underway. There were extraordinary delays as well which may have been caused by local officials wanting to solve the problem themselves and not to tell higher levels about it. A lack of communication between livestock and veterinary experts and public health experts seems to have compounded the delay. The response from the provincial and national health authorities was rapid so the avoidable delays seem to have been at the regional and local levels. One factor hindering reporting may have been the regulation that makes peasants responsible for sanitary burial of their own pigs. Some Chinese language media and official sources for this report are provided in URLs below.
Ground Zero: Rural Sichuan Province
Danshan is a poor township located 20 miles east of Ziyang City, a major regional center 80 miles south of Chengdu. Local residents earn their livings by selling pigs and ducks and by receiving migrant worker remittances. Higher prices for pig feed and declining pork prices since late 2004 have made life harder for Danshan peasants, said one local informant. The one paved road through town is only dimly lit at night. Improvements since 1997 of the main road linking Danshan to Ziyang and the highway from Ziyang to the provincial capital of Chengdu has cut Danshan–Chengdu travel time from five hours to two hours. Many people in their 30s and 40s work away from home, sending money from faraway places like Guangdong and Xinjiang. Bus traffic to the capital is frequent. For example, three buses bound for Chengdu passed one Sunday morning in a single hour. The close proximity of millions of peasants in this region to domestic pigs and ducks, and the much closer links between city and countryside due to better roads and massive worker migration have important implications for the spread of emerging diseases. Sichuan has traditionally been an incubator for new varieties of influenza, so the local government’s sluggish response to the recent pig epidemic and the subsequent cover-up offer important lessons for the future.
Danshan Township is part of the rural Yanjiang section of Ziyang City. Yanjiang has a population of one million people and sends one million pigs to slaughter each year, nearly all of which are raised by peasant families with 3–10 pigs each. The annual cash income of peasants in the Danshan area is about 3000 RMB (USD 375) per year. Rising feed prices, quarantines and falling pork prices due to concerns about unsafe pork have hurt the incomes of local peasants this year. A Danshan resident commented to US Consulate General officer that the centralization of pig slaughtering under government supervision had been effective in containing the outbreak of disease. However, the same individual stated that in general he was skeptical of official information, since officials are interested in preserving appearances rather than in actually addressing problems. Several residents volunteered their view that the local government was very corrupt.
Chronology: First Case to Public Warning
- On June 24, the first case arrived at Ziyang First People’s Hospital . On July 11, the Ziyang City CDC Yanjiang District Office received a message from Ziyang Third People’s Hospital – “Patient admitted with suspected case of viral hemorrhagic fever. Please investigate.” The District office investigated that same day and sends a blood sample to Sichuan Province CDC for testing the next day.
- On July 12, the Yanjiang District CDC received another message from Ziyang Third People’s Hospital. “This hospital has a second patient with a suspected case of viral hemorrhagic fever. Patient is in critical condition. Please investigate immediately.” While the District CDC investigation was underway the patient died. The District CDC learned that the Third People’s Hospital had received four patients with similar symptoms over the previous two weeks. Two had died while one had left the hospital voluntarily, and the fourth had just arrived in the epidemiology ward. All had eaten a dead pig or dead lamb, had a high fever. Initial symptoms were similar to a cold, followed by feeling unwell, coughing, fatigue, shock, low blood pressure and an increase in the white blood cell count….” The Yanjiang District CDC decided that that the human illness was linked to pigs. That same day, July 12, Danshan and Lezhi Township began aggressive checks for sick and dead pigs illness in the surrounding countryside. Dead pigs were ordered to be buried. However, the Ziyang leadership waited another week before notifying the Sichuan Livestock and Food Bureau. According to official reports put out by Yanjiang district and other affected areas, 469 dead pigs and 1 mountain goat had been buried by July 25.
- On July 14, Sichuan Province CDC test results: negative for IgG, IgM hemorrhagic fever antibodies.
- On July 15 12-noon Sichuan Province CDC receives reports from Ziyang CDC of “an unknown infectious disease that has thus far infected five people of who four have died. … Most serious symptoms are poison shock and meningitis. That same day the Sichuan CDC eliminated viral hemorrhagic fever as a possible cause of the illness.
- On July 15, the Sichuan Province CDC sent a fax report to the Ministry of Public Health Disease Control Office.
- On July 16 at 00:45 Ziyang City Yanjiang District CDC made the first report on the disease of unknown origin on the “Outbreak Network” [Tufa Wang] of the Ministry of Health.
- On July 18, the Sichuan Provincial Livestock and Food Bureau takes “immediate action upon being informed by Ziyang City” of an epidemic among pigs. Also on July 18, the PRC Ministry of Health sent seven epidemiologists, lab experts and clinicians to assist. On July 23, an epidemiological study of 55 patients shows that all were affected by S. suis from dead pigs and that they were infected by slaughtering or other direct contact with pigs that had become sick and died.
July 25 Order On Centralized Pig Slaughtering
A July 25, 2005 notice from the Yanjiang regional people’s government of the Ziyang City administrative region ordered strict enforcement of regulations on the illegal slaughter, consumption, transportation of sick or dead livestock and poultry. Compulsory sterilization was ordered for all designated slaughtering points for livestock and poultry as well as for all markets and all transportation vehicles. Management of slaughtering points was to be strengthened and no livestock or poultry that did not pass veterinary inspection was to be admitted for slaughtering. Any meat that entered the marketplaces without a stamp of veterinary inspection was to be disposed of in a safe manner and the violator fined. The regional public security, health, livestock, trade and commerce bureaus were ordered to cooperate closely. People who violated the above rules were to be strictly punished. A local informant told US Consulate General Officer that centralized pig slaughtering was being done. Congenoff sighting of a pig leg on a motorcycle leaving a peasant home made him doubt that farmers completely stopped slaughtering their own pigs.
August 14 Danshan Order On Pig Slaughtering
On August 14, the Danshan Township government listed four slaughtering points for pigs and stressed that these were the only places where pigs could be slaughtered. Violators were to be strictly punished. The health departments were ordered to strengthen their supervision of these four slaughtering points. Organizations and individuals involved in slaughtering pigs as well as buyers of pigs needed to
- Obtain a valid “place of origin epidemic inspection certificate” [chandi jianyi zhengming];
- Understand the epidemic status;
- Check the ear marking on the pig, and
- Get the full name and address of the individual who raised any slaughtered livestock.
Any pig that was sick or dead or did not have an earmark would not be admitted to the slaughtering point. Pigs without ear markings needed a veterinary inspection, quarantine observation for 24 hours or seven days, and a new veterinary inspection. A fee was charged for the additional inspection. Pig meat products that passed inspection were to be stamped with a mark of approval. Any pig meat product not passing inspection or without a stamp was subject to confiscation by the industry and trade administrative departments and would be disposed of safely in accordance with the law. Any costs incurred in disposing of a pig that did not pass inspection were to be paid by the owner of the pig.
The Danshan township order also strictly forbad the slaughtering, processing and sale of meat from pigs that died of an illness. All pigs that died of an illness were ordered disposed of in a safe manner [wuhai chuli]. Any expenses involved were to be borne by the person involved. The order stressed that the economic development office, the livestock station, the trade and industry office, the health bureau and the police stations would work together under the guidance of the government to strengthen enforcement of these regulations. Anyone who interfered with or disrupted the work of the designated pig slaughtering points was to be dealt with severely by public security according to regulations on fines for disrupting public order and the Criminal Law of the PRC.
Yanjiang Notice & Official Press On Disease Outbreak
A Yanjiang District government public notice covering the period July 24 – August 23 provided the time of onset and death as well as the symptoms of eighteen pigs that died in Yanjiang District of Ziyang City. The notice also described compensation given to the owners, most of whom reportedly raised only 3–8 pigs. According to the notice, the pigs died the same day their illness was first noticed. Symptoms noted included high temperature, swelling, difficult in breathing, and refusal to eat. Compensation paid to the pig owners ranged from 30 RMB for a small pig up to 300 RMB for a very large pig. By comparison, live pigs were sold for 7 RMB per kilogram and meat from healthy slaughtered pigs sold for about 14 RMB per kilogram in Sichuan Province in mid 2005. Pork prices were not greatly affected by news of the epidemic in Ziyang although slaughterhouse close downs and quarantines imposed on some areas hurt local peasants.
Danshan and the townships abutting it on the east were at the center of the pig illness (S. suis) that spread to people and killed 38 people in Sichuan. The illness spread from sick pigs to people who butchered, handled or ate them. At the height of the outbreak in late July in Danshan township, a Danshan Township Party propaganda official stated that 30 sick or dead pigs a day were buried. This report for just one township, albeit at the center of the epidemic, contrasts sharply with the 18 pigs noted on the Yanjiang District government list for the entire district.
Hong Kong Press On Sale Of Sick And Dead Pigs
According to the Hong Kong press, the sale of sick and dead pigs has been common in the epidemic area for many years. On August 23, the Phoenix TV (Hong Kong) weekly magazine in a cover story on the epidemic quoted a butcher in Ziyang City as saying that the sale of sick and dead pigs was an “open secret”. The butcher estimated that with 5 million pigs slaughtered in the Ziyang region each year, there were at least 50,000 sick or dead pigs each year from Ziyang alone found their way into the meat supply. The meat was popular with peasants and some hard pressed fast food restaurants with thin profit margins because it was cheap. Sick pigs typically sold for 100 RMB and dead pigs for 50 RMB, said the butcher. Several media reports mentioned that pigs were sometimes seized and buried one day by the health authorities, and then dug up and sold the next day.
Stricter enforcement, at least for the time being, of the longstanding regulation against selling sick and dead pigs reflects the magnitude of the problem. During the weeks following widespread knowledge of the epidemic in mid-July, public security officers in Ziyang and other affected areas, according to incomplete statistics, seized 2,000 metric tons of pork from pigs that died of illness and another several metric tons of pork from pigs that was not inspected. These seizures in the atmosphere of a campaign against eating sick or dead pigs, confirm the overall volume of meat sold and how enforcement of regulations was usually very lax.
Hk Magazine Reveals Dead Pigs Not Reported
Peasants reportedly resisted notifying authorities of sick or dead pigs because one pig represented up to several months of cash income. The PRC law requiring the owner of a dead pig to sterilize and bury the diseased animal in two meters of earth further discouraged reporting. One peasant told the Phoenix TV weekly print magazine that he did not report a dead pig after learning that he would have to pay burial costs. Another peasant complained that the Chinese media criticized the peasants severely for eating and selling dead pigs, but “they never think about it from our point of view.” Ziyang City government compensated owners who reported dead pigs and disposed of the dead animals properly. However, Ziyang City officials were reluctant to publicize this decision widely because authorities could not afford the cost of the program over the long term and feared that a lack of central government compensation would cause the region to become a dumping ground for dead pigs.
The newspaper “Dongfang Zaobao” asked on July 26 and July 27 why was there a one month delay between the arrival on June 24 of the first case transmitted to humans at Ziyang’s First People’s Hospital and the revelation in a July 25 official announcement that sickness was caused by butchering or eating sick or dead pigs. The newspaper noted that on July 12, in Danshan Township, Yanjiang District and adjacent Lezhi County, Jianyang City, local officials had begun checking for pigs that had died of illness. The paper noted great secrecy around the hospitals where infected people were admitted. Why, the paper asked, did the local government wait two weeks before announcing that the illness was linked to consumption of sick and dead pigs?
Prc Journalist Criticized Slow Response And Coverup
Journalist Yang Jian, in his long article “Survey on the Strange Illness in Ziyang, Sichuan” [available online entitled Sichuan Ziyang Guaibing Diaocha], agreed with Chongqing media criticism of Sichuan provincial authorities. Yang asserted that the sluggish, poorly coordinated response of local governments to the pig illness and its spread to humans resembled China’s early response to SARS. He concluded that the slow response of local government to the outbreak was a major factor in the spread of the epidemic. The pig epidemic was underway well before the first human case entered the Ziyang hospital on June 24. Why didn’t the veterinary and livestock departments warn of the danger to humans who came in close contact or ate the animals? Some local people asked if the local anti-epidemic stations were only there to collect fees. Yang noted that the epidemic subsided rapidly in late July after strong emergency measures were taken. The delay was costly, he concluded.
Propaganda Department Control Of Sichuan Media
Chinese journalists trying to investigate the outbreak were blocked or even expelled from the area by the Ziyang City Propaganda Department. Yang learned that during the outbreak, Zheng Xiaoxing, Deputy Director of the Sichuan Province Party Committee Propaganda Department and its News Department, worked personally with Ziyang City Party Secretary Zhong Mian to maintain tight supervision of news and strict control over journalists. The Sichuan Communist Party Propaganda Department notified all Sichuan media that only Xinhua and Sichuan Daily were cleared to write stories about the Ziyang epidemic. Yang attended a July 25 Ziyang meeting between propaganda officials and media led to a partial relaxation of that order.
Sichuan provincial media were given permission to do interviews, but other media remained forbidden to report. The central government’s Xinhua new agency reporter was allowed to do interviews only if accompanied by the Ziyang City propaganda department chief. On July 27, Ziyang City officials, angry at critical Shanghai and Chongqing media reports, declared many journalists persona non grata in the region. The journalists were threatened with an official escort out of the region if they did not leave voluntarily. Reporters visiting the First People’s Hospital of Ziyang, where peasants lay sick with S. suis, were told to report to the Ziyang City Propaganda Department to get permission for an interview. Yang wrote that, under those conditions in Ziyang, Chinese journalists had to work like secret agents.
Yang Jian reported that 18 days elapsed between the arrival of the first patient at the First People’s Hospital in Ziyang City on June 24 and the notification to the Ziyang City Center for Disease Control on July 11. On July 15, Sichuan Provincial Health Department experts went to Ziyang. Experts from the PRC Ministry of Public Health and the Ministry of Agriculture followed on July 18 and July 19. On July 20, the Ministry of Health gave the illness the temporary name “Ziyang Toxic Shock Syndrome”. On July 25, the Ministry of Health and the Ministry of Agriculture decided that the illness was due to contagion to humans from pigs of S. suis. Right up until the official announcement on July 25, local officials in Ziyang and other affected areas continued to contradict media reports that there was a mysterious illness in Sichuan connected to an epidemic among pigs. The officials maintained that there was no epidemic and pork from their area was completely safe to eat.
PRC National Conference On Sichuan Pig-To-Human Epidemic
A 70-page Guangdong Province Center for Disease Control Central Laboratory informal Powerpoint presentation on the Sichuan pig–human epidemic based on an early August PRC national conference on the epidemic was found online. The title of the presentation, found at http://www.cdcp.org.cn/zsjz/zhu/zhu3.ppt is translated as “Epidemiology of Human Infection of Pig Streptococcus Suis and Its Prevention and Control”. According to the report, S. suis is commonly found in 50% of all pigs and in all slaughtered pigs, but causes illness in only 5% of cases, especially when pigs are in crowded conditions with poor ventilation or mixed with pigs from other areas. A 1998 outbreak killed 14 of 25 infected people. Thirteen of the 16 who developed toxic shock syndrome died, while only one of the 9 who got meningitis died.
Similar 1998 Outbreak In Jiangsu Killed Fourteen
According to an August 10 China Newsweekly [Zhongguo Xinwen Zhoukan] report, the 1998 outbreak occurred July 2–August 8, 1998 in Jiangsu Province and killed 14 of 25 people diagnosed. A joint study of this outbreak by the Nanjing Military District Military Medicine Research Institute and the Jiangsu Province Epidemic Prevention station in a report published in November 2001 issue of the Third Military Medical University Journal concluded that this outbreak was also caused by S. suis. This report created a sensation during the Sichuan outbreak since none of the epidemiologists or veterinarians in Sichuan had heard of it. One Chinese researcher who was closely involved with the 1998 Jiangsu outbreak commented to China Newsweekly “China’s disease control departments only concern themselves with human illnesses and are under the Ministry of Health. Monitoring of veterinary diseases falls under the Ministry of Agriculture. This is very little communication between the two systems. The problem we face now is that more and more illnesses afflict both people and animals.”
S. Suis Kills Quickly
According to the Guangdong Province CDC Powerpoint presentation, as of July 31, of the 181 human cases reported, 57% (103) were from Ziyang City, 23% (42) from Neijiangzhan, and 11% (20 cases) from Chengdu City. Of the 181 cases, 179 involved contact with a dead pig and two with a dead sheep. Exposures included butchering, washing, transporting and eating dead pigs. No evidence of human-to-human transmission. Period from exposure to illness onset varied from two hours to 14.5 days, with the median of 2.4 days. Seventy-one case of S. suis were diagnosed by the end of July. Twenty of these patients developed toxic shock of which 17 (85%) died. Forty-five of these patients developed meningitis of whom 1 (2%) died. For patients who later died, the period from exposure to onset of symptoms ranged from six hours to 8.7 days with a median of 1.5 days. The illness developed quickly. Of the 34 patients who had died as of July 31, the shortest time between onset of symptoms and death was 8 hours, the longest 11 days with a median of 22.5 hours. All the dead were peasants, 85% male, between 36 and 78 years of age with the median age of 53 years.
The Guangdong CDC Central Laboratory Powerpoint presentation noted that preventing the shipment of pigs that died of disease into Guangdong Province was difficult since Guangdong imported 20 million pigs annually from other provinces.
— Strengthen collaboration between the health and agricultural departments at each level
— Monitor livestock for S. suis infections
— Establish a joint system for controlling diseases that afflict both humans and livestock
Sichuan Province Livestock Bureau July 27 Report
The Sichuan Province Livestock and Food Bureau on July 26 issued an official notice (original text of this notice and two urgent orders from this Bureau are archived with Chinese sources at bottom of Chengdu OSIS site URL cited above) on the S. suis outbreak. To summarize the notice, unusually high mortality in pigs had occurred since late June in Ziyang City. Once they received a report, the Sichuan Province Livestock and Food Bureau and the Sichuan Province Animal Epidemic Prevention Central Station made an emergency survey and ordered urgent control measures to be taken. The animal epidemic is chiefly in the Yanjiang District of Ziyang City, Jianyang City, Lezhi County and Zizhong County of Neijiang City. As of July 25, 73 villages and 43 townships had reported 469 dead pigs. The pigs were from 300 different peasants who raised them in relatively poor conditions. There were no sick pigs reported from large or medium sized pig farms. Pig to pig transmission was very low. In the great majority of cases, a sick pig did not transmit the disease to other pigs.
According to the notice, a Ministry of Agriculture PCR test having eliminated other types of bacteria or disease, a preliminary conclusion of pig S. suis was made. When the epidemic occurred, [Note:on July 23] Sichuan Governor Zhang Zhongwei personally called a meeting of high level provincial leaders and leaders from the areas affected. The province immediately allocated RMB 3 million for anti pig epidemic work. Livestock and Food Bureau urgent notice No. 70 [Note: no date specified. End note] called for a report from all affected areas of the number of dead livestock and daily reports beginning July 25. One million copies of epidemic prevention information were printed and the public was urged not to not to privately slaughter, buy, sell, transport or eat dead livestock. Affected areas were quarantined. The quarantine lasts until 21 days after the last sick pig died. Twenty-four temporary quarantine stations were established in Ziyang City and 26 in Neijiang City.
A press release from the Sichuan Provincial Livestock and Food Bureau dated August 4 states that the Livestock and Food Bureau immediately sent experts and took urgent epidemic control measures on July 18 upon being informed by the Ziyang City authorities that there was an abnormally high rate of deaths among pigs in the region. Thus Ziyang City region which, according to Chinese media interviews with local officials, started urgent pig epidemic control measures on July 12 but waited nearly a week to inform the provincial livestock and food officials. According to the same press release, local officials had by August 2 already checked on the health of 4 million pigs, 68% of the total in the area. Three thousand veterinary and medical personnel sent throughout the area to supervise the sanitary disposal of dead pigs.
Photos from September 2005 Visit to Danshan, Ziyang, Sichuan Province