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SUPPLEMENT ARTICLE China’s Heath Care System and Avian Influenza Preparedness Joan A. Kaufman AIDS Public Policy Project, John F. Kennedy School of Government, Harvard University, Cambridge, and Heller School for Social Policy and Management, Brandeis University, Waltham, Massachusetts The severe acute respiratory syndrome crisis exposed serious deficiencies in China’s public health system and willingness to report outbreaks of threats to public health. Consequently, China may be one of the weak links in global preparedness for avian influenza. China’s rural health care system has been weakened by 20 years of privatization and fiscal decentralization. China plays a huge role in the global poultry industry, with a poultry population of 14 billion birds, 70%–80% of which are reared in backyard conditions. Although surveillance has been strengthened, obstacles to the timely reporting of disease outbreaks still exist. The weakened health care system prevents many sick people from seeking care at a health care facility, where reporting would originate. Inadequate compensation to farmers for culled birds leads to nonreporting, and local officials may be complicit if they suspect that reporting might lead to economic losses for their communities. At the local level, China’s crisis-management ability and multisectoral coordination are weak. The poor quality of infection control in many rural facilities is a serious and well-documented problem. However, traditions of community political mobilization suggest that the potential for providing rural citizens with public health information is possible when mandated from the central government. Addressing these issues now and working on capacity issues, authority structures, accountability, and local reporting and control structures will benefit the control of a potential avian influenza outbreak, as well as inevitable outbreaks of other emerging infectious diseases in China’s Pearl River Delta or in other densely populated locations of animal husbandry in China. The threat of an avian influenza pandemic is the next chapter in a story that began with the severe acute respiratory syndrome (SARS) epidemic. The common thread of both epidemics would be their likely origin in China. With SARS, the Chinese government went from being a global pariah for its initial failure to alert the world about the outbreak, which resulted in a worldwide epidemic, to being a global hero for successful containment. However, China’s lack of trans- Potential conflicts of interest: none reported. Presented in part: Harvard University Asian Flus and Avian Influenza Workshop, Cambridge, Massachusetts, 8–10 December 2006. Financial support: supplement sponsorship is detailed in the Acknowledgments. Reprints or correspondence: Dr. Joan A. Kaufman, AIDS Public Policy Project, John F. Kennedy School of Government, Harvard University, 79 JFK St., Cambridge, MA 02138 ([email protected] or [email protected]). The Journal of Infectious Diseases 2008; 197:S7–13 2008 by the Infectious Diseases Society of America. All rights reserved. 0022-1899/2008/19704S1-0003$15.00 DOI: 10.1086/524990 parency at the outset of the SARS epidemic was troubling, and there is no guarantee that it would not happen again. Even before the global SARS epidemic in 2003, the threat of emerging infectious diseases already had the world’s attention. In 2003, the Institute of Medicine of the US National Academy of Sciences issued a report, Microbial Threats to Health, that noted that, “in the highly interconnected and readily traversed ‘global village’ of our time, one nation’s problems soon become every nation’s problems” [1, p. 1]. The rapid global response to the SARS epidemic was impressive and, fortunately, succeeded in averting a worse outcome. This response was possible because post–September 11 investments in global health-information systems, surveillance, and rapid-response planning paid off. Strategies for infection control, as well as therapeutic information, were quickly shared worldwide. The good news is that these already-effective global infrastruc- Avian Influenza and China’s Health System • JID 2008:197 (Suppl 1) • S7 tures have been strengthened further since the SARS epidemic and are being deployed to prepare for and control an outbreak of avian influenza. Opinions differ about the reality of the threat of an avian influenza pandemic. Human deaths have been confirmed in 12 countries, including some countries outside Asia, but the number of cases of avian influenza in humans is still small, even though the mortality rate is high, at 150%. No clusters of cases in humans in any country have been documented conclusively as being caused by human-to-human transmission. Past influenza pandemics, such as that caused by the influenza A(H1N1) virus in 1918–1919, resulted in large numbers of deaths, which were likely caused by a combination of virus virulence and other factors not yet fully understood. One factor leading to the high mortality rate was the unavailability of antibiotics at that time [2], which resulted in deaths from secondary bacterial infections after acute viral illness [3]. Some public health professionals suggest that the number of deaths during a similar epidemic today would be unlikely to be so high, although the widespread use of antibiotics in poultry in southern China and other parts of Asia may contribute to antibiotic resistance. China may be one of the weak links in global preparedness for 2 main reasons: it lacks transparency in acknowledging outbreaks, and its health care system is not up to the task of putting in place systems to ensure preparedness or the capability to contain the epidemic if it begins in China’s rural areas. The SARS crisis exposed serious deficiencies in China’s public health system. Consequently, since then, strengthening China’s public health system has topped China’s public policy agenda. The central government and the Chinese Communist Party have made equity and social investments in rural health and education top priorities in their agenda for a harmonious society [4]. The SARS crisis also highlighted the importance of political will and national financial resources in the mobilization of public health action [5]. Are enough resources and political accountability being mustered for avian influenza preparedness? Is China’s government and China’s health system now prepared for controlling avian influenza? What areas of the health system, including transparency in reporting outbreaks, must be strengthened further so that the system is up to the urgent task of preparedness and rapid response? This article provides a critical review of the major health-system and governance challenges facing China’s potential to respond to avian influenza and highlights areas that may need strengthening. BACKGROUND ON CHINA’S HEALTH SYSTEM Over the past 50 years, China has achieved remarkable progress in improving the health of its population. Life expectancy is 170 years, and the major causes of morbidity and mortality are now noninfectious and chronic infectious diseases, rather than acute infectious diseases. China’s basic health infrastrucS8 • JID 2008:197 (Suppl 1) • Kaufman ture, put in place 30 years ago, consists of a 3-tiered medical system in rural areas and corresponding structures in cities. Competent, trained health care personnel staff this infrastructure, and many of them are trained vocationally in 3-year medical colleges or by county health institutions and are certified to provide basic care at the local level. China’s health care system, however, has been seriously weakened by 20 years of relaxed government support and inadequate regulation in the health sector, along with overall fiscal decentralization. China’s primary health care system was held up as a model at the time of the call for “health for all by the year 2000” at the World Health Organization (WHO) conference in Alma-Ata, Kazakhstan, in 1978. However, in 2000, China ranked 188 of 191 countries in terms of fairness in financial contributions to health [6], and, in 2001, 21.6% of poor rural households fell below the poverty line because of medical expenses. In China, the average cost of hospitalization at the township or county level is approximately equal to the per capita annual income of a rural farmer [7]. Health care is provided mainly on a fee-for-service basis at rural health clinics, and most provided health care is curative. China’s problems are less related to infrastructure than to equity and affordability. Huge disparities in health care investment and access exist between urban and rural areas and between the developed eastern coastal part of the country and the more-underdeveloped west. The health care system in rural areas has become a mainly privatized fee-for-service system, with facilities maintained by the government but services and drugs provided for a fee and for profit. Although many urban residents have some health care insurance to defray costs, there was virtually no system of health care insurance in rural areas until recently. Preventive health care services and health-education outreach have been seriously weakened by 20 years of China’s market-oriented economic policies [8]. Health care access in China today is determined by wealth, with debt from a major illness identified as one of the major reasons for poor rural households to drop below the poverty line. In 2005, China’s own State Council published a scathing report that castigated the state of China’s health system, noting that 49% of the population cannot afford to see a doctor when ill and that 30% are not hospitalized when necessary [9]. This report prompted increased funding and attention to deficiencies and inequities in China’s rural health system. The central government and the Communist Party have made equity and social investments in rural health care, as well as education, top priorities in their agenda for a harmonious society [4]. In rural areas, the government is piloting a new system of health care insurance for major medical expenses, but investment in basic disease prevention has yet to follow. For China’s 150 million economic migrants, an increasingly large segment of the population that comprises the urban poor, there is little to no coverage for seeking health care services. These huge numbers of the rural and urban poor who cannot afford to seek care when ill represent a worrisome threat to controlling avian influenza. Although serious efforts are under way to revitalize health care financing and equity in rural areas, the urgent and heavy requirements of avian influenza preparedness cannot wait until these efforts are completed. Any epidemic is likely to take hold in China’s poorer areas, where there is only a limited amount of local financing for health care, which will create shortages of trained staff and quality services, including standard infection-control measures, as a result of chronic underfunding. In addition to institutional constraints on the horizontal collaboration between different programs, especially between different government sectors (e.g., animal husbandry and infectious diseases), there are a number of challenges facing the capacity of China’s health system to respond to avian influenza. DECENTRALIZED AUTHORITY AND ACCOUNTABILITY FOR DISEASE REPORTING China’s Law on Preventing and Treating Infectious Diseases, enacted in September 1989, requires mandatory reporting of many infectious diseases. Between October 2005 and February 2006, China’s Ministry of Agriculture, Ministry of Finance, and State Council published 15 regulations, guidelines, and policies related to avian influenza and disease prevention and control, cost reimbursement during disease control, and financial assistance for poultry production [10]. However, this clear legislation regarding mandatory disease reporting for specified infectious diseases is hampered by a structure of decentralized authority that impedes its realization. China’s ability to respond to emergency disease outbreaks surely will be complicated by decades of political decentralization and by its own governance system, which will be compounded by weakness in the power and authority of the national Ministry of Health. In 1978, China began fiscal decentralization from the national level to the provinces and from the provinces to the counties. The new approach of “every tub on its own bottom” shifted major financing for province-level government operations and services to the provinces themselves and substantially reduced centralized transfers. Unfunded mandates (directives and policies) are set at the level of the central government, but financing depends on local resources, allocation, and priority setting. However, with privatization of the health care system that began in the early 1980s and the focus on economic investment in infrastructure and industry, local governments, especially poor ones, have greatly reduced investment in social sectors. Although the government owns health care facilities, government contributions for health at the local level are scant, and sometimes the only funds provided are for partial salary support, with nothing allocated for public health programs. As a result, the focus of the delivery of health care services in China is almost exclusively on the provision of curative services. User payment as a percentage of health care spending has been rising steadily for 20 years, from 20% to 54% [11]. Moreover, the Ministry of Health is bureaucratically weak, and it is hard for it to mobilize other ministries. This was a major problem during the SARS epidemic, because the Ministry of Health did not have the authority or ability to require direct reporting from lower levels of government or even from military hospitals. Provincial governments have greater control over provincial health bureaus than does the Ministry of Health. The Ministry of Health has limited authority within any particular province outside the Bureau of Heath or its associated Centers for Disease Control. The Ministry of Health may formulate national policies, but these policies serve merely as guidelines or unfunded mandates for the lower levels of government, which must generate and allocate the funding needed to support their implementation. This weakness limits the ability of the Ministry of Health to manage health crises. Moreover, health resources in China are managed by many sectors, and coordination is difficult if not impossible, further complicating any urgent crisis-management situation. For example, in addition to the more-general functions of the Ministry of Health, numerous other ministries and departments are involved in health-related matters. The National Development Research Center controls health infrastructure and financing, the Ministry of Finance controls routine budgets and national programs, the State Food and Drug Administration controls pharmaceuticals, the Ministry of Labor and Social Security deals with basic medical insurance for urban employees, and the Ministry of Civil Affairs handles medical financial assistance to the poor. Provincial control over financing, personnel decision making and allocation, and new initiatives within each province complicate coordination and accountability even more. In 2005, the Minister of Health, Gao Qiang, identified key healthsystem challenges facing China, and the need for a health emergency–response network was at the top of the list. CHINA AS THE INCUBATOR FOR A GLOBAL EPIDEMIC OF AVIAN INFLUENZA Recent events related to the global avian influenza threat included a massive dying off of 16000 wild migratory birds in the Qinghai Lake nature reserve in northwestern China in April 2005. Following this, the number of countries reporting disease outbreaks due to avian influenza A(H5N1) virus increased dramatically through the end of 2006, with 55 countries reporting outbreaks of H5N1 virus infection in wild birds and/or poultry. China has had several confirmed cases of infection in humans; the first 2 were reported in November 2005. It is not surprising that the current culprit in the global avian influenza threat is likely to have originated in China. The H5N1 Avian Influenza and China’s Health System • JID 2008:197 (Suppl 1) • S9 virus was first isolated in China in 2003 from diseased pigs on farms in southern China [12]. This was the first documented infection of pigs by any H5 subtype of avian influenza virus. Historically, densely populated southern China has been a breeding ground for new influenza viruses, because of the large numbers of animals and people living in close proximity; the ubiquity of backyard animal husbandry of pigs, chickens, and ducks; and the presence of live-animal markets. All these factors were implicated in the SARS outbreak of 2003. However, other factors also are at play in the current avian influenza threat. China plays a large role in the global poultry industry and, according to the WHO, has a poultry population of 14 billion at any one point in time, 70%–80% of which is reared in backyard conditions [13]. Individual poultry farmers have little incentive to report sick birds. AVIAN INFLUENZA PREPAREDNESS AND THE REQUIREMENTS FOR AN EFFECTIVE RESPONSE The WHO has taken a lead role in defining the steps that will be required for the prevention of an avian influenza epidemic and has been working with countries to put in place systems to ensure early identification and containment. These steps include (1) recognizing the possible event of an avian influenza outbreak through detection of clusters of cases, investigation of suspected clusters, and reporting of early signals to the scientific community for comparative studies of virus isolates and in-depth investigation of sources of reservoirs of the virus; (2) verifying an outbreak event and then making an assessment of that event and putting in place immediate infection-control measures; and (3) containing the outbreak event through a rapid response that entails active case finding and contact tracing and the administration of antiviral drugs. If necessary, exceptional measures such as quarantine, the wider prophylactic administration of drugs, and social distancing measures such as staying home from work and home schooling should be used. Ideally, all countries should put in place systems to successfully implement these steps. To do this, however, countries must invest in building the institutional and operational capacity to reach rural areas, where an outbreak is likely to begin. In addition, there is a need to create multisectoral, integrated authority and control systems that can be activated if an outbreak is detected or an epidemic begins. Prior to an outbreak, however, there is a critical need for the institutional and operational capacity to implement educational outreach aimed at prevention and containment, through a focus on birds and poultry-industry practices, to minimize the opportunity for the avian influenza virus to mutate into a type that can easily infect humans (T. Kane, personal communication). The widespread mobilization of people (esS10 • JID 2008:197 (Suppl 1) • Kaufman pecially rural farmers) is needed to reduce practices that increase the odds of an epidemic and to prepare the population for what to do if an outbreak or epidemic occurs. CHINA’S AVIAN INFLUENZA PREPAREDNESS: KEY ISSUES Full surveillance, timely reporting, and transparency in reporting avian influenza cases in birds and humans are very important. Containment and effective quarantine and culling after a reported outbreak also are essential. In addition, the need for communication about basic hygiene practices for humans and for the poultry and animals in their care are key prevention measures. Is China up to the task? China’s surveillance system has been strengthened during the post-SARS era, which is perhaps one of the biggest lessons learned from that mishandled epidemic. Both the US Centers for Disease Control and Prevention and the WHO’s Beijing office have been working closely with the Chinese Ministry of Health and Centers for Disease Control during the post-SARS era to strengthen and computerize routine disease reporting of many infectious diseases, in accordance with China’s newly strengthened Law and Regulations on Infectious Disease Reporting. By mid-2005, all 2800 counties in China had direct Internet connections to a Ministry of Agriculture monitoring system, and 93% of county or higher-level hospitals and 43% of township hospitals had direct connections to the diseasereporting system of China’s Centers for Disease Control [10]. The WHO is working with China to develop an integrated surveillance system, to strengthen laboratory diagnostic capacity, and to create a reporting system that will allow epidemiological, clinical, and laboratory information from both human and animal surveillance, the environment, and other sectors to be analyzed and shared with decision makers in all sectors. The WHO and China also are working on strengthening early response to an outbreak event and on fostering better collaboration between the animal sector and the health sector and are working with health institutions on the surveillance and control of facility-acquired infections. China’s capacity to accomplish these goals with its current infrastructure is high. The communications infrastructure and the designated personnel exist throughout the 3-tiered medical system, down to the county level. China’s laboratory and science infrastructure, pharmaceutical research, and biotech sector are strong. Owing to the political will that resulted from the acknowledgement of failures in the timely reporting of SARS cases, there now exists a strong mandate, as well as financial support, for a strong diseasesurveillance infrastructure for avian influenza. However, the challenges for surveillance are great, and a number of factors might interfere with the verification of disease events in both birds and humans. Farmers and government officials have economic reasons for not reporting suspected avian influenza outbreaks in an area. If the government does not properly compensate farmers for culled birds, farmers may hide the birds. The weakened and privatized health care system prevents many sick people from seeking care at a health care facility, where reporting would originate (i.e., at the township level). Moreover, local officials, who control the work of the sectors under their jurisdiction, may hide cases of disease if they suspect that reporting might result in economic losses for their communities. Many suspect that unreported deaths of fowl have occurred on a large scale in many places in China, because similar events among poultry have occurred across China’s borders, in Hong Kong, Vietnam, and other neighboring countries, with no plausible explanation other than an origin in China [14]. Moreover, China is still poorly prepared for a rapid response to an outbreak event. Its crisis-management capability and ability to coordinate different agencies, such as the Ministry of Agriculture and the Ministry of Health, is weak, especially at the local level. During the SARS epidemic, the Ministry of Health was unable to put in place the needed interventions at either the national or local level. To support the recently strengthened response to AIDS, a new State Council Working Committee on AIDS was created to manage the needed multisectoral collaborations [15], but no such similar agency exists for a potential outbreak of a communicable disease. The weakness of the health sector in mobilizing other sectors must be addressed and an emergency-response agency and plan formulated, to avoid the problems that occurred during the early response to SARS. For example, an obvious failure in response to SARS occurred when millions of migrants fled Beijing because they feared being unreasonably quarantined without concern for their personal rights. Fortunately, this mass exodus did not result in a widespread rural epidemic, owing to a combination of luck and strong, albeit belated, local action [5]. Rural communities in China quickly built local infectious-disease hospitals modeled after the SARS hospital that was built in Beijing. Staff was seconded from all health institutions in the county, and training in infection-control measures, including quarantine and reporting procedures, was provided. These hospitals still exist in rural communities in China and would likely be mobilized during another infectious disease emergency. In the event of a much more contagious influenza epidemic, stronger measures to ensure quarantine and social distancing would be needed. Other significant concerns are the limited potential for proper case management and shortcomings in infection-control practices in hospitals. By some estimates, 170% of the health care visits in China that do occur (many individuals do not seek care at all) occur at village-level clinics. These clinics are staffed by village-level rural doctors and doctors of traditional medicine. Although they are certified to practice and capable of dealing with common illnesses and first aid, these doctors may not be capable of recognizing and dealing with the early symptoms of avian influenza during an epidemic. However, as a step in the right direction, rural doctors now are required to report, by telephone, to township health centers all cases of suspicious pneumonia or serious influenza. Infection-control measures in many rural facilities leave much to be desired, and facility-acquired infection is a serious and well-documented problem in China. The capacity for outreach to and mobilization of the population threatens to be a major limitation of any effort at avian influenza preparedness. China’s outreach system for public health information has been seriously weakened by the privatization of the rural health care system, which has driven service providers to focus on income-earning curative care. As a result, the capacity for health education (in terms of human resources and responsible institutions) has been seriously weakened. However, a tradition of community political mobilization suggests that the potential for reaching rural citizens with public health information exists when mandated from the central government. China’s ability to mobilize its population has been an enduring feature of its single-party system of governance for the past 50 years. Early patriotic health campaigns were responsible for important public health achievements during the “barefoot doctor” era (i.e., the 1960s and 1970s, until the end of the Cultural Revolution). The patriotic health campaign was resurrected during the SARS epidemic, and its success in mobilizing and reaching the public with critical prevention information was impressive. In the event of an avian influenza outbreak, it could be used to reach rural citizens with communications about behavior change and hygiene. An important question is why it is not already being used to its fullest extent to deal with the repeated outbreaks of epidemics among poultry, to reach out to the rural population to communicate the necessary hygiene measures mentioned above and, thus, minimize the potential of infection in humans? In this area, China’s preparedness for avian influenza could easily be strengthened. Another area of concern is China’s veterinary surveillance and its ability to control its widespread live-animal markets or to apply restrictions and controls to its backyard poultry- and duck-raising industries. A matter of some concern is the fact that, in parts of Asia, mammals that were thought to not be susceptible to H5N1 virus infection have developed disease (WHO, unpublished data) [12]. Live-animal markets were implicated in the emergence of the SARS epidemic, when the civet cat, which is sold in live-animal markets in southern China, was identified as the likely source of the mutated human SARSassociated virus. Many of the live-animal markets were shut down in the immediate aftermath of the SARS epidemic, but many have reopened or operate behind closed doors, catering to traditions for food preparation and to traditional health Avian Influenza and China’s Health System • JID 2008:197 (Suppl 1) • S11 beliefs about the consumption of certain foods. How these markets are monitored is far from clear, and the possibility of animal-to-human transmission of infection remains high. A recent analysis pointed to direct and indirect factors that facilitate the spread of avian influenza virus and discussed 8 highrisk farming practices related to poultry and farm animals, 5 unsafe poultry-transport practices, and 11 high-risk practices at “wet” markets (i.e., live-animal markets) that are common in China, Vietnam, and other Asian countries. Complicating veterinary infection-control measures is the fact that the Chinese government has chosen chicken immunization, rather than restrictions on backyard poultry- and duck-raising that would minimize the possibility of wild fowl infecting poultry and duck flocks. After confirmation of a human case of H5N1 virus infection in Anhui Province, the provincial government decreed that all backyard poultry must be kept in cages, but this localized response was neither sufficient to deal with the problem nor easy to enforce. It is difficult to ensure the implementation and monitoring of restrictions to prevent the intermingling of these 2 populations in China’s backyard ponds. Moreover, there are questions about the effectiveness of the vaccination of poultry. China has vaccinated 120% of its chickens [13], and many suspect that infection control through poultry vaccination is only mildly successful and may be leading to the selection of more-virulent viruses. A recent article in the Proceedings of the National Academy of Sciences of the United States (PNAS) [16] suggested that a more dangerous “Fujian-like” variant of the H5N1 virus had been strengthened as a result of poultry vaccination (a response noted that 95% of domestic birds had been vaccinated [17]). The Chinese government vehemently denied this suggestion [18], but doubt remains. The WHO noted that its ability to assess the accuracy of the PNAS report had been hampered by China’s refusal to share avian influenza virus samples with the international scientific community, which uses such samples for the development of human avian influenza vaccines [17]. China’s resistance to sharing information and virus samples with Hong Kong and the United States impedes efforts to document the mutations occurring in the virus in cases of infection in both birds and humans. China claimed that such virus samples had been misused previously but agreed to share 20 virus samples from 2004 and 2005 with the WHO, to support its claim that no new strain of H5N1 virus had emerged in southern China [17]. CONCLUSION If an avian influenza pandemic among humans were to emerge, its likely source would be China. The good news is that China has a reasonably good health infrastructure and a demonstrated ability to mobilize for action, given the political authority of its single-party system of governance, as proved by its quick S12 • JID 2008:197 (Suppl 1) • Kaufman turnaround during the SARS epidemic. However, China’s crisis-management procedures for epidemic threats currently are very weak, its authority structures are unclear and potentially dysfunctional, and it is difficult, if not impossible, for the Ministry of Health to exercise local control, as a result of decentralized financing and authority. Moreover, China has a long history of and an incentive system that leads to the concealment of sensitive and negative information, by lower levels of government from higher levels, which does not bode well for the timely reporting and containment of disease outbreaks among poultry and humans. Many incentives exist for concealment, but the main incentive is a supervision and promotion system based on the achievement of targets and an expectation of negative consequences for the reporting of bad news. The example of the response to SARS shows that these problems can be overcome with an infusion of strong political will. However, given the worldwide importance of preventing avian influenza viruses from mutating to adapt to human hosts, this political will should be mobilized now, not after an epidemic begins, since preparedness can help prevent the virus reassortment that happens in the type of backyard-farming conditions present in rural China today. Moreover, it is essential that Chinese scientists and officials exhibit greater transparency in sharing virus information, so that global efforts to develop influenza vaccines are as efficient and effective as possible. Addressing these issues now and working on issues related to institutional and operational capacity; authority structures; accountability; and more local surveillance, reporting, and infection-control structures will benefit the response to not only a potential avian influenza outbreak but also the inevitable future outbreak of another emerging infectious disease that will be likely to originate in China’s Pearl River Delta or in other densely populated locations of animal husbandry in China. Acknowledgments The Harvard University Asian Flus and Avian Influenza Workshop was hosted by the Harvard University Department of Anthropology, Harvard School of Public Health, and Harvard Asia Center and was supported by the National Science Foundation, Harvard Asia Center, and the Michael Crichton Fund. Supplement sponsorship. 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