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Changes in Chinese Policies to Promote the Rational Use of Antibiotics

Changes in Chinese Policies to Promote the Rational Use of Antibiotics Health in Action Changes in Chinese Policies to Promote the Rational Use of Antibiotics Yonghong Xiao*, Jing Zhang, Beiwen Zheng, Lina Zhao, Sujuan Li, Lanjuan Li* Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou, China Antimicrobial resistance (AMR) is a serious Summary Points public health challenge and containment of AMR is a global priority. On World Health Microbial resistance to antimicrobial agents (antimicrobial resistance, AMR) is a Day in April 2011, the World Health serious public health challenge, and containment of AMR is an urgent priority, Organization appealed to all member coun- both in China and worldwide. tries to ‘‘combat drug resistance: no action The main cause of AMR is the irrational use of antimicrobial agents, in today, no cure tomorrow’’ [1]. The imple- healthcare and veterinary settings and by the general public. Actions taken by mentation of new Chinese policies over the the Chinese health administrative authorities in the past 10 years have been past 2 years for the rational use of antimi- largely unsuccessful, likely because of the lack of mandatory regulations. crobials and AMR containment is a prom- In 2011, coupled with new healthcare reforms, the Chinese Ministry of Health ising response to this appeal. N changed strategy and launched a special campaign to promote the rational use of antimicrobials in healthcare settings. This mainly consisted of establishing The Causes of Increasing mandatory management strategies, such as target setting, taskforce organiza- Antimicrobial Resistance in tion, and the development of audit and inspection systems. China The special campaign had notable achievements, with decreased antibiotic sales and a reduced percentage of prescriptions for antimicrobials for both The prevalence of AMR is relatively hospitalized patients and outpatients. high in China; the morbidity and mortal- A number of issues still need to be addressed to ensure further improvements ity from infections caused by multidrug- in AMR containment. These include the unregulated use of antibiotics in animal resistant or pan-drug-resistant pathogens husbandry, over-the-counter purchases of antibiotics, and elimination of are higher in China than in other economic incentives for drug sales. countries [2]. Data reported by the Chinese Ministry of Health (MOH) Na- tional Antimicrobial Resistance Investiga- for disease therapy, infection prevention, sation provided to healthcare institutions tion Net (Mohnarin) indicates that AMR is and animal growth promotion are com- for drug sales. The Chinese healthcare rising steadily. The prevalence of methi- mon phenomena in healthcare settings system consists of a government-led system cillin-resistant Staphylococcus aureus (MRSA), and veterinary practice. The percentage of with characteristics of free market financ- extended-spectrum b-lactamase-produc- prescriptions containing antibiotics in ru- ing and lower service pricing. The gov- ing Escherichia coli, imipenem-resistant ral clinics of western China was around ernment’s contribution to hospital budgets Pseudomonas aeruginosa, and imipenem-resis- 50%, which is higher than in developed is less than 20% of hospital expenditure. tant Acinetobacter baumannii—the so-called countries such as the US and Sweden [5]. Healthcare institutions can receive finan- ‘‘superbugs’’ in nosocomial infections— Another important cause of the irrational cial compensation by selling healthcare was 50.5%, 71.2%, 23.4%, and 56.8% use of antibiotics is the financial compen- services and drugs. The government’s in 2010, respectively (Figure 1). The overall prevalence of erythromycin-resis- tant Streptococcus pneumonia and ciprofloxa- Citation: Xiao Y, Zhang J, Zheng B, Zhao L, Li S, et al. (2013) Changes in Chinese Policies to Promote the cin-resistant E. coli was 94.7% and 65.7% Rational Use of Antibiotics. PLoS Med 10(11): e1001556. doi:10.1371/journal.pmed.1001556 in community settings, respectively [3,4]. Published November 19, 2013 Irrational use of antimicrobial agents is Copyright:  2013 Xiao et al. This is an open-access article distributed under the terms of the Creative the main cause of increased AMR. In Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, China, antibiotics are considered to be a provided the original author and source are credited. panacea by the general public and some Funding: YX is supported by the Research Special Fund for Public Welfare Industry of Health, Ministry of healthcare practitioners. Over-the-counter Health of China (201002021). The funders had no role in the analysis, decision to publish, or preparation of the manuscript. purchase and over-reliance on antibiotics Competing Interests: The authors have declared that no competing interests exist. Abbreviations: AMR, antimicrobial resistance; MOH, Ministry of Health; Mohcas, Chinese Ministry of Health The Health in Action section is a forum for Center for Antibacterial Surveillance; Mohnarin, Chinese Ministry of Health National Antimicrobial Resistance individuals or organizations to highlight their Investigation Net; MRSA, methicillin-resistant Staphylococcus aureus. innovative approaches to a particular health prob- * E-mail: xiao-yonghong@163.com (YX); ljli@zju.edu.cn (LL) lem. Provenance: Not commissioned; externally peer reviewed. PLOS Medicine | www.plosmedicine.org 1 November 2013 | Volume 10 | Issue 11 | e1001556 Figure 1. Overall trends in prevalence of major antimi- crobial-resistant bacteria in Chinese tertiary hospitals in 2000–2011. The majority of the data were adapted from Mohnarin results, which mostly represent situations involving nosocomial infections in tertiary hospitals. The numbers in circles describe the chronology of major administrative interventions taken by the Chinese Ministry of Health. indicates the issue of ‘‘temporary rules for pharmaceutical affairs in healthcare institutions’’ (2002); indicates the issue of ‘‘guidance for the clinical use of antimicrobials’’ (2004); indicates the issue of ‘‘regulations for management of nosocomial infections’ (2006); indicates the issue of recommendations for enhancing the prevention and control of multidrug resistant bacterial infections (2008); and indicates the special campaign initiated in 2011. MRSA, methicillin-resistant Staphylococcus aureus; ESBL (+) EC, extend- ed-spectrum b-lactamase-producing Escherichia coli; CPR-REC, ciprofloxacin-resistant E. coli; IMI-R PA, imipenem-resistant Pseudomonas aeruginosa; IMI-R AB, imipenem-resistant Acine- tobacter baumannii. doi:10.1371/journal.pmed.1001556.g001 acquiescence to the situation has stimu- However, due to strained resources, violate rational use policies. According lated, and to some extent encouraged, insufficient enforcement, absence of su- to the protocol, all hospitals should have excessive examinations, unnecessary treat- pervision and inspection, and inefficient an antibiotic administrative group chaired ment, and overuse of medicines by routine implementation plans, these policies and by the president, formulary restrictions healthcare services. Drug sales constitute strategies were not successful. Indeed, are to be enforced, prescribers have accre- about half of institutional income and during the past decade, antimicrobials dited prescription rights for different most of the profit, with more than 25% antibiotic classes determined by their have remained the most prescribed insti- being sales of antimicrobial agents [6]. tutional medicine, and AMR has contin- positional titles, and antibiotic procure- At the same time, the overuse of antimi- ued to increase, in some cases dramatically ment should be restricted to 50 or 35 crobial agents in animal husbandry and agents in secondary and tertiary hospitals, (for example, imipenem-resistant Acineto- farming has contributed to the occurrence bacter baumannii) (Figure 1) [3,11,12]. respectively. Meanwhile, targets for anti- and spread of antibiotic-resistant microbes biotic prescription are set at less than 60% in the environment [7,8]. and 20% of all prescriptions for hospital- Changes in Policy to Promote ized patients and outpatients, respectively; the Rational Use of Antibiotics prophylactic use of antibiotics in clean The Limited Effect of Professional In 2009, a new round of healthcare operations should be lowered to 30% of Strategies for the Rational Use of reforms was initiated in China with patients and reduced to less than 24 hours’ Antibiotics the ultimate target of eradicating the duration; and antibiotic utilization in To control AMR, the Chinese health ‘‘difficulty and high price of seeing a hospitalized patients should be less than administrative authorities have taken a doctor,’’ and to achieve basic medical 40 daily defined doses per 100 patient series of actions over the past 10 years, security for everyone by 2020. The gover- days. All the indicators are linked to hos- including the development of technical nment increased healthcare spending pital quality evaluation procedures and the specifications and policies. These included and promoted healthcare insurance cov- allocation of future medical resources. the issue of guidance about antibiotic use erage for urban and rural residents. Furthermore, adherence to these protocols and infection control. Mohnarin and the The aim was for the medical establish- are to be considered when appointing or Chinese MOH Center for Antibacterial ment to gradually regain its public service dismissing hospital presidents. Surveillance (Mohcas) were established in role. All these reforms contributed to To enact these protocols, the Chinese 2006. Hospitals were required to set up a policies promoting sustainable progress MOH and local health administration drug therapeutics committee to facilitate the towards the rational use of antimicrobials signed an administrative target responsibil- rational use of drugs, and medical practi- [13]. ity agreement with major hospital author- tioners were required to prescribe antibiot- In 2011, coupled with healthcare re- ities. The Chinese MOH also held several ics in a rational manner. Furthermore, forms, the Chinese MOH adjusted the national medical education programs each nosocomial infection control measures were reliance on the professional strategies year and conducted twice yearly inspec- emphasized, such as hand hygiene and described above and launched a special tions (every September and December). contact precautions for AMR infections campaign to reorganize the rational use According to the protocols, hospitals that (although compliance is often unsatisfactory of antimicrobials in healthcare settings. fail to meet targets would be downgraded because of heavy staff workloads and large The campaign protocol mainly consists to a lower classification level, and the patient populations). In addition, nation- of establishing mandatory administrative leaders of the institutes involved would wide continuing medical education pro- strategies for the rational use of antimi- grams focusing on rational drug use and be dismissed. Medical staff who seriously crobials, setting targets for antimicrobial violate the regulations could lose their AMR control, were conducted repeatedly. All of the measures were established as part management, organizing task forces, de- accreditation to prescribe antibacterial veloping audit and inspection systems, of a technical support system to promote the agents, have their professional qualification rational use of antibiotics, as recommended and investigating and reassigning respon- revoked, or even be prosecuted if their by the World Health Organization [9,10]. sibility to hospital management staff who actions have serious consequences [14]. PLOS Medicine | www.plosmedicine.org 2 November 2013 | Volume 10 | Issue 11 | e1001556 During the past 2 years in China, these use associated with clean surgical proce- administrative motivation. This ‘‘adminis- policies were enacted with extensive pro- trative antibiotic stewardship’’ regulation is dures also decreased from 95% to 58% of motion of education and increased levels cases, with the duration of use shortened implemented by the Chinese MOH. They may also provide a valuable reference for of supervision. Excellent hospitals were from 5 days to less than 48 hours. For recognized, and failures were criticized in example, antibiotic procurement in Tian- other countries with similar healthcare systems [17]. public. Several hospital presidents were jin City was 200 million RMB Yuan dismissed and some clinicians were pun- lower in 2011 than in 2010, although the ished with economic sanctions. A few numbers of outpatient visits, hospitalized Further Problems for the clinicians also had their prescription rights patients, and operations increased by 1.4 Containment of AMR suspended by health authorities as a result million, 84,000, and 58,000, respectively Although the special campaign launched of severe regulatory violations. A gradual [15]. by the MOH to promote the rational use of return towards the rational use of antimi- To ensure sustainable progress towards antibiotics in healthcare settings has had crobials has begun. According to IMS the rational use of antimicrobial agents in some success, several factors need to be Research data, the percentage of drug healthcare settings, ‘‘administrative regu- considered to establish a long-term and sales (by value) for antimicrobials de- lations for the clinical use of antimicrobi- nationwide framework for sustainable creased to 17% in the fourth quarter of als’’ were issued in China in August 2012, AMR containment in China. Firstly, sev- 2012 from 25% in 2011, with an associ- in which the concept of ‘‘antibiotic stew- eral ministries share regulatory oversight of ated decrease in the volume of antibiotics ardship’’ was integrated into the measures antimicrobial use. The State Food and sold (Figure 2). Data released by the outlined during the special campaign [16]. Drug Administration is responsible for the Chinese MOH indicates that the percent- The legislation considers long-term antibi- registration, production, quality control, age of prescriptions for antimicrobials otic stewardship in Chinese healthcare and distribution of antimicrobials. The decreased from 68% to 58% for hospital- institutions and is expected to change the Ministry of Agriculture is independently ized patients and from 25% to 15% for current situation in which rational antimi- responsible for complete oversight of anti- outpatients. Antimicrobial prophylaxis crobial use simply relies on incidental biotic use in animal feed and veterinary care. The MOH exclusively administers the use of antibiotics in healthcare settings. This power-sharing administrative system has a tendency to dilute direct responsibil- ity. New mechanisms should be explored to provide integrated policies to promote the rational use of antibiotics and AMR containment in related fields. Secondly, medical school curricula and continuing medical education should be improved. At present, most medical students in China do not study the relevance of antibiotic therapy to AMR. Thirdly, public education should be provided to ensure that the general public are aware of the risks associated with AMR, which will likely help to reduce over-the-counter sales and self-medication of antibiotics. Finally, and critically, the government should widen the healthcare reforms and provide financial guarantees to medical institutions to ensure that economic incentives from drug sales are eliminated. This will return healthcare institutions to a not-for-profit status and aid professional standards [9,12,18,19]. Author Contributions Analyzed the data: YX JZ BZ LL. Wrote the first draft of the manuscript: YX. Contributed to the writing of the manuscript: YX JZ BZ LZ SL LL. ICMJE criteria for authorship read and met: YX JZ BZ LZ SL LL. Agree with manuscript results and conclusions: YX JZ BZ LZ SL LL. Figure 2. Quarterly sales volume and the proportion of antimicrobial agents sold in 2010–2012 in China. (A) The sales value of all drugs (blue bars) or antimicrobial agents (pink References bars) in millions (M) of US dollars (USD) and the proportion of antimicrobial agents sold (green line). (B) The sales volume of all antimicrobial agents in minimal packaging units (green bars) and 1. World Health Organization (April 2011) World the percentage of fluoroquinolones (blue line) or cephalosporin sales (red line). Data were Health Day-7. Available: http://wwwwhoint/ adapted from IMS Research. world-health-day/2011/en/indexhtml Accessed doi:10.1371/journal.pmed.1001556.g002 10 March 2013. PLOS Medicine | www.plosmedicine.org 3 November 2013 | Volume 10 | Issue 11 | e1001556 2. Yezli S, Li H (2012) Antibiotic resistance amongst resistance genes in Chinese swine farms. Proc 14. China MoH (2011) Protocol for special campaign healthcare-associated pathogens in China. Natl Acad Sci U S A 110: 3435–3440. of antibiotic administrative in healthcare institu- Int J Antimicrob Agents 40: 389–397. 9. Xiao YH (2012) Building technical support tions. Ministry of Health, May 8, 2011Beijing. 3. Xiao YH, Giske CG, Wei ZQ, Shen P, Heddini system for antibiotic rational use. Chin J Pract 15. China MoH (10 March 2013) Available: http:// A, et al. (2011) Epidemiology and characteristics Intern Med 32: 973–976. www.moh.gov.cn/mohbgt/s3582/201205/ of antimicrobial resistance in China. Drug Resist 10. World Health Organization (2002) Promoting 54651.shtml. News Conference on May 8, 2012. Updat 14: 236–250. rational useofmedicines:corecomponents. 16. Dellit TH, Owens RC, McGowan JE, Gerding 4. Xiao YH, Shen P, Wei ZQ, Chen YB, Kong HS, Policy Perspectives on Medicines No 5 2002 DN, Weinstein RA, et al. (2007) Infectious et al. (2012) Mohnarin report of 2011 : monitor- Geneva. Available: http://apps.who.int/ Diseases Society of America and the Society for ing of bacterial resistance in China. Chinese medicinedocs/en/d/Jh3011e/. Accessed 05 Healthcare Epidemiology of America guidelines Journal of Nosocomiology (Zhonghua Yi Yuan May, 2013. for developing an institutional program to Gan Ran Xue Za Zhi) 22: 4946–4952. 11. Xu J, Sun Z, Li Y, Zhou Q (2013) Surveillance and enhance antimicrobial stewardship. Clin Infect 5. Dong L, Yan H, Wang D (2008) Antibiotic correlation of antibiotic consumption and resis- Dis 44: 159–177. prescribing patterns in village health clinics across tance of Acinetobacter baumannii complex in a tertiary 17. Xiao Y, Li L (2013) Legislation of clinical antibiotic 10 provinces of Western China. J Antimicrob care hospital in northeast China, 2003–2011. use in China. Lancet Infect Dis 13: 189–191. Chemother 62: 410–415. Int J Environ Res Public Health 10: 1462–1473. 18. Guardabassi L, Larsen J, Weese J, Butaye P, 6. Reynolds L, McKee M (2009) Factors influencing 12. Wang H, Li N, Zhu H, Xu S, Lu H, et al. (2013) Battisti A, et al. (2013) Public health impact and antibiotic prescribing in China: an exploratory Prescription pattern and its influencing factors in antimicrobial selection of meticillin-resistant analysis. Health Policy 90: 32–36. Chinese county hospitals: a retrospective cross- staphylococciinanimals.Journal of Global 7. Tang S, Meng Q, Chen L, Bekedam H, Evans T, sectional study. PLoS One 8: e63225. Antimicrobial Resistance 1: 55–62. et al. (2008) Tackling the challenges to health doi:10.1371/journal.pone.0063225 19. Khachatourians GG (1998) Agricultural use of equity in China. Lancet 372: 1493–1501. 13. Yip WC-M, Hsiao WC, Chen W, Hu S, Ma J, et al. antibiotics and the evolution and transfer of 8. Zhu YG, Johnson TA, Su JQ, Qiao M, Guo GX, (2012) Early appraisal of China’s huge and complex antibiotic-resistant bacteria. Can Med Assoc J et al. (2013) Diverse and abundant antibiotic health-care reforms. Lancet 379: 833–842. 159: 1129–1136. PLOS Medicine | www.plosmedicine.org 4 November 2013 | Volume 10 | Issue 11 | e1001556 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png PLoS Medicine Public Library of Science (PLoS) Journal

Changes in Chinese Policies to Promote the Rational Use of Antibiotics

PLoS Medicine , Volume 10 (11) – Nov 19, 2013

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Copyright: © 2013 Xiao et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: YX is supported by the Research Special Fund for Public Welfare Industry of Health, Ministry of Health of China (201002021). The funders had no role in the analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. Abbreviations: AMR, antimicrobial resistance; MOH, Ministry of Health; Mohcas, Chinese Ministry of Health Center for Antibacterial Surveillance; Mohnarin, Chinese Ministry of Health National Antimicrobial Resistance Investigation Net; MRSA, methicillin-resistant Staphylococcus aureus Provenance: Not commissioned; externally peer reviewed.
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Abstract

Health in Action Changes in Chinese Policies to Promote the Rational Use of Antibiotics Yonghong Xiao*, Jing Zhang, Beiwen Zheng, Lina Zhao, Sujuan Li, Lanjuan Li* Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou, China Antimicrobial resistance (AMR) is a serious Summary Points public health challenge and containment of AMR is a global priority. On World Health Microbial resistance to antimicrobial agents (antimicrobial resistance, AMR) is a Day in April 2011, the World Health serious public health challenge, and containment of AMR is an urgent priority, Organization appealed to all member coun- both in China and worldwide. tries to ‘‘combat drug resistance: no action The main cause of AMR is the irrational use of antimicrobial agents, in today, no cure tomorrow’’ [1]. The imple- healthcare and veterinary settings and by the general public. Actions taken by mentation of new Chinese policies over the the Chinese health administrative authorities in the past 10 years have been past 2 years for the rational use of antimi- largely unsuccessful, likely because of the lack of mandatory regulations. crobials and AMR containment is a prom- In 2011, coupled with new healthcare reforms, the Chinese Ministry of Health ising response to this appeal. N changed strategy and launched a special campaign to promote the rational use of antimicrobials in healthcare settings. This mainly consisted of establishing The Causes of Increasing mandatory management strategies, such as target setting, taskforce organiza- Antimicrobial Resistance in tion, and the development of audit and inspection systems. China The special campaign had notable achievements, with decreased antibiotic sales and a reduced percentage of prescriptions for antimicrobials for both The prevalence of AMR is relatively hospitalized patients and outpatients. high in China; the morbidity and mortal- A number of issues still need to be addressed to ensure further improvements ity from infections caused by multidrug- in AMR containment. These include the unregulated use of antibiotics in animal resistant or pan-drug-resistant pathogens husbandry, over-the-counter purchases of antibiotics, and elimination of are higher in China than in other economic incentives for drug sales. countries [2]. Data reported by the Chinese Ministry of Health (MOH) Na- tional Antimicrobial Resistance Investiga- for disease therapy, infection prevention, sation provided to healthcare institutions tion Net (Mohnarin) indicates that AMR is and animal growth promotion are com- for drug sales. The Chinese healthcare rising steadily. The prevalence of methi- mon phenomena in healthcare settings system consists of a government-led system cillin-resistant Staphylococcus aureus (MRSA), and veterinary practice. The percentage of with characteristics of free market financ- extended-spectrum b-lactamase-produc- prescriptions containing antibiotics in ru- ing and lower service pricing. The gov- ing Escherichia coli, imipenem-resistant ral clinics of western China was around ernment’s contribution to hospital budgets Pseudomonas aeruginosa, and imipenem-resis- 50%, which is higher than in developed is less than 20% of hospital expenditure. tant Acinetobacter baumannii—the so-called countries such as the US and Sweden [5]. Healthcare institutions can receive finan- ‘‘superbugs’’ in nosocomial infections— Another important cause of the irrational cial compensation by selling healthcare was 50.5%, 71.2%, 23.4%, and 56.8% use of antibiotics is the financial compen- services and drugs. The government’s in 2010, respectively (Figure 1). The overall prevalence of erythromycin-resis- tant Streptococcus pneumonia and ciprofloxa- Citation: Xiao Y, Zhang J, Zheng B, Zhao L, Li S, et al. (2013) Changes in Chinese Policies to Promote the cin-resistant E. coli was 94.7% and 65.7% Rational Use of Antibiotics. PLoS Med 10(11): e1001556. doi:10.1371/journal.pmed.1001556 in community settings, respectively [3,4]. Published November 19, 2013 Irrational use of antimicrobial agents is Copyright:  2013 Xiao et al. This is an open-access article distributed under the terms of the Creative the main cause of increased AMR. In Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, China, antibiotics are considered to be a provided the original author and source are credited. panacea by the general public and some Funding: YX is supported by the Research Special Fund for Public Welfare Industry of Health, Ministry of healthcare practitioners. Over-the-counter Health of China (201002021). The funders had no role in the analysis, decision to publish, or preparation of the manuscript. purchase and over-reliance on antibiotics Competing Interests: The authors have declared that no competing interests exist. Abbreviations: AMR, antimicrobial resistance; MOH, Ministry of Health; Mohcas, Chinese Ministry of Health The Health in Action section is a forum for Center for Antibacterial Surveillance; Mohnarin, Chinese Ministry of Health National Antimicrobial Resistance individuals or organizations to highlight their Investigation Net; MRSA, methicillin-resistant Staphylococcus aureus. innovative approaches to a particular health prob- * E-mail: xiao-yonghong@163.com (YX); ljli@zju.edu.cn (LL) lem. Provenance: Not commissioned; externally peer reviewed. PLOS Medicine | www.plosmedicine.org 1 November 2013 | Volume 10 | Issue 11 | e1001556 Figure 1. Overall trends in prevalence of major antimi- crobial-resistant bacteria in Chinese tertiary hospitals in 2000–2011. The majority of the data were adapted from Mohnarin results, which mostly represent situations involving nosocomial infections in tertiary hospitals. The numbers in circles describe the chronology of major administrative interventions taken by the Chinese Ministry of Health. indicates the issue of ‘‘temporary rules for pharmaceutical affairs in healthcare institutions’’ (2002); indicates the issue of ‘‘guidance for the clinical use of antimicrobials’’ (2004); indicates the issue of ‘‘regulations for management of nosocomial infections’ (2006); indicates the issue of recommendations for enhancing the prevention and control of multidrug resistant bacterial infections (2008); and indicates the special campaign initiated in 2011. MRSA, methicillin-resistant Staphylococcus aureus; ESBL (+) EC, extend- ed-spectrum b-lactamase-producing Escherichia coli; CPR-REC, ciprofloxacin-resistant E. coli; IMI-R PA, imipenem-resistant Pseudomonas aeruginosa; IMI-R AB, imipenem-resistant Acine- tobacter baumannii. doi:10.1371/journal.pmed.1001556.g001 acquiescence to the situation has stimu- However, due to strained resources, violate rational use policies. According lated, and to some extent encouraged, insufficient enforcement, absence of su- to the protocol, all hospitals should have excessive examinations, unnecessary treat- pervision and inspection, and inefficient an antibiotic administrative group chaired ment, and overuse of medicines by routine implementation plans, these policies and by the president, formulary restrictions healthcare services. Drug sales constitute strategies were not successful. Indeed, are to be enforced, prescribers have accre- about half of institutional income and during the past decade, antimicrobials dited prescription rights for different most of the profit, with more than 25% antibiotic classes determined by their have remained the most prescribed insti- being sales of antimicrobial agents [6]. tutional medicine, and AMR has contin- positional titles, and antibiotic procure- At the same time, the overuse of antimi- ued to increase, in some cases dramatically ment should be restricted to 50 or 35 crobial agents in animal husbandry and agents in secondary and tertiary hospitals, (for example, imipenem-resistant Acineto- farming has contributed to the occurrence bacter baumannii) (Figure 1) [3,11,12]. respectively. Meanwhile, targets for anti- and spread of antibiotic-resistant microbes biotic prescription are set at less than 60% in the environment [7,8]. and 20% of all prescriptions for hospital- Changes in Policy to Promote ized patients and outpatients, respectively; the Rational Use of Antibiotics prophylactic use of antibiotics in clean The Limited Effect of Professional In 2009, a new round of healthcare operations should be lowered to 30% of Strategies for the Rational Use of reforms was initiated in China with patients and reduced to less than 24 hours’ Antibiotics the ultimate target of eradicating the duration; and antibiotic utilization in To control AMR, the Chinese health ‘‘difficulty and high price of seeing a hospitalized patients should be less than administrative authorities have taken a doctor,’’ and to achieve basic medical 40 daily defined doses per 100 patient series of actions over the past 10 years, security for everyone by 2020. The gover- days. All the indicators are linked to hos- including the development of technical nment increased healthcare spending pital quality evaluation procedures and the specifications and policies. These included and promoted healthcare insurance cov- allocation of future medical resources. the issue of guidance about antibiotic use erage for urban and rural residents. Furthermore, adherence to these protocols and infection control. Mohnarin and the The aim was for the medical establish- are to be considered when appointing or Chinese MOH Center for Antibacterial ment to gradually regain its public service dismissing hospital presidents. Surveillance (Mohcas) were established in role. All these reforms contributed to To enact these protocols, the Chinese 2006. Hospitals were required to set up a policies promoting sustainable progress MOH and local health administration drug therapeutics committee to facilitate the towards the rational use of antimicrobials signed an administrative target responsibil- rational use of drugs, and medical practi- [13]. ity agreement with major hospital author- tioners were required to prescribe antibiot- In 2011, coupled with healthcare re- ities. The Chinese MOH also held several ics in a rational manner. Furthermore, forms, the Chinese MOH adjusted the national medical education programs each nosocomial infection control measures were reliance on the professional strategies year and conducted twice yearly inspec- emphasized, such as hand hygiene and described above and launched a special tions (every September and December). contact precautions for AMR infections campaign to reorganize the rational use According to the protocols, hospitals that (although compliance is often unsatisfactory of antimicrobials in healthcare settings. fail to meet targets would be downgraded because of heavy staff workloads and large The campaign protocol mainly consists to a lower classification level, and the patient populations). In addition, nation- of establishing mandatory administrative leaders of the institutes involved would wide continuing medical education pro- strategies for the rational use of antimi- grams focusing on rational drug use and be dismissed. Medical staff who seriously crobials, setting targets for antimicrobial violate the regulations could lose their AMR control, were conducted repeatedly. All of the measures were established as part management, organizing task forces, de- accreditation to prescribe antibacterial veloping audit and inspection systems, of a technical support system to promote the agents, have their professional qualification rational use of antibiotics, as recommended and investigating and reassigning respon- revoked, or even be prosecuted if their by the World Health Organization [9,10]. sibility to hospital management staff who actions have serious consequences [14]. PLOS Medicine | www.plosmedicine.org 2 November 2013 | Volume 10 | Issue 11 | e1001556 During the past 2 years in China, these use associated with clean surgical proce- administrative motivation. This ‘‘adminis- policies were enacted with extensive pro- trative antibiotic stewardship’’ regulation is dures also decreased from 95% to 58% of motion of education and increased levels cases, with the duration of use shortened implemented by the Chinese MOH. They may also provide a valuable reference for of supervision. Excellent hospitals were from 5 days to less than 48 hours. For recognized, and failures were criticized in example, antibiotic procurement in Tian- other countries with similar healthcare systems [17]. public. Several hospital presidents were jin City was 200 million RMB Yuan dismissed and some clinicians were pun- lower in 2011 than in 2010, although the ished with economic sanctions. A few numbers of outpatient visits, hospitalized Further Problems for the clinicians also had their prescription rights patients, and operations increased by 1.4 Containment of AMR suspended by health authorities as a result million, 84,000, and 58,000, respectively Although the special campaign launched of severe regulatory violations. A gradual [15]. by the MOH to promote the rational use of return towards the rational use of antimi- To ensure sustainable progress towards antibiotics in healthcare settings has had crobials has begun. According to IMS the rational use of antimicrobial agents in some success, several factors need to be Research data, the percentage of drug healthcare settings, ‘‘administrative regu- considered to establish a long-term and sales (by value) for antimicrobials de- lations for the clinical use of antimicrobi- nationwide framework for sustainable creased to 17% in the fourth quarter of als’’ were issued in China in August 2012, AMR containment in China. Firstly, sev- 2012 from 25% in 2011, with an associ- in which the concept of ‘‘antibiotic stew- eral ministries share regulatory oversight of ated decrease in the volume of antibiotics ardship’’ was integrated into the measures antimicrobial use. The State Food and sold (Figure 2). Data released by the outlined during the special campaign [16]. Drug Administration is responsible for the Chinese MOH indicates that the percent- The legislation considers long-term antibi- registration, production, quality control, age of prescriptions for antimicrobials otic stewardship in Chinese healthcare and distribution of antimicrobials. The decreased from 68% to 58% for hospital- institutions and is expected to change the Ministry of Agriculture is independently ized patients and from 25% to 15% for current situation in which rational antimi- responsible for complete oversight of anti- outpatients. Antimicrobial prophylaxis crobial use simply relies on incidental biotic use in animal feed and veterinary care. The MOH exclusively administers the use of antibiotics in healthcare settings. This power-sharing administrative system has a tendency to dilute direct responsibil- ity. New mechanisms should be explored to provide integrated policies to promote the rational use of antibiotics and AMR containment in related fields. Secondly, medical school curricula and continuing medical education should be improved. At present, most medical students in China do not study the relevance of antibiotic therapy to AMR. Thirdly, public education should be provided to ensure that the general public are aware of the risks associated with AMR, which will likely help to reduce over-the-counter sales and self-medication of antibiotics. Finally, and critically, the government should widen the healthcare reforms and provide financial guarantees to medical institutions to ensure that economic incentives from drug sales are eliminated. This will return healthcare institutions to a not-for-profit status and aid professional standards [9,12,18,19]. Author Contributions Analyzed the data: YX JZ BZ LL. Wrote the first draft of the manuscript: YX. Contributed to the writing of the manuscript: YX JZ BZ LZ SL LL. ICMJE criteria for authorship read and met: YX JZ BZ LZ SL LL. Agree with manuscript results and conclusions: YX JZ BZ LZ SL LL. Figure 2. Quarterly sales volume and the proportion of antimicrobial agents sold in 2010–2012 in China. (A) The sales value of all drugs (blue bars) or antimicrobial agents (pink References bars) in millions (M) of US dollars (USD) and the proportion of antimicrobial agents sold (green line). (B) The sales volume of all antimicrobial agents in minimal packaging units (green bars) and 1. World Health Organization (April 2011) World the percentage of fluoroquinolones (blue line) or cephalosporin sales (red line). Data were Health Day-7. Available: http://wwwwhoint/ adapted from IMS Research. world-health-day/2011/en/indexhtml Accessed doi:10.1371/journal.pmed.1001556.g002 10 March 2013. PLOS Medicine | www.plosmedicine.org 3 November 2013 | Volume 10 | Issue 11 | e1001556 2. Yezli S, Li H (2012) Antibiotic resistance amongst resistance genes in Chinese swine farms. Proc 14. China MoH (2011) Protocol for special campaign healthcare-associated pathogens in China. Natl Acad Sci U S A 110: 3435–3440. of antibiotic administrative in healthcare institu- Int J Antimicrob Agents 40: 389–397. 9. Xiao YH (2012) Building technical support tions. Ministry of Health, May 8, 2011Beijing. 3. Xiao YH, Giske CG, Wei ZQ, Shen P, Heddini system for antibiotic rational use. Chin J Pract 15. China MoH (10 March 2013) Available: http:// A, et al. 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Dong L, Yan H, Wang D (2008) Antibiotic correlation of antibiotic consumption and resis- Dis 44: 159–177. prescribing patterns in village health clinics across tance of Acinetobacter baumannii complex in a tertiary 17. Xiao Y, Li L (2013) Legislation of clinical antibiotic 10 provinces of Western China. J Antimicrob care hospital in northeast China, 2003–2011. use in China. Lancet Infect Dis 13: 189–191. Chemother 62: 410–415. Int J Environ Res Public Health 10: 1462–1473. 18. Guardabassi L, Larsen J, Weese J, Butaye P, 6. Reynolds L, McKee M (2009) Factors influencing 12. Wang H, Li N, Zhu H, Xu S, Lu H, et al. (2013) Battisti A, et al. (2013) Public health impact and antibiotic prescribing in China: an exploratory Prescription pattern and its influencing factors in antimicrobial selection of meticillin-resistant analysis. Health Policy 90: 32–36. Chinese county hospitals: a retrospective cross- staphylococciinanimals.Journal of Global 7. Tang S, Meng Q, Chen L, Bekedam H, Evans T, sectional study. PLoS One 8: e63225. Antimicrobial Resistance 1: 55–62. et al. (2008) Tackling the challenges to health doi:10.1371/journal.pone.0063225 19. Khachatourians GG (1998) Agricultural use of equity in China. Lancet 372: 1493–1501. 13. Yip WC-M, Hsiao WC, Chen W, Hu S, Ma J, et al. antibiotics and the evolution and transfer of 8. Zhu YG, Johnson TA, Su JQ, Qiao M, Guo GX, (2012) Early appraisal of China’s huge and complex antibiotic-resistant bacteria. Can Med Assoc J et al. (2013) Diverse and abundant antibiotic health-care reforms. Lancet 379: 833–842. 159: 1129–1136. PLOS Medicine | www.plosmedicine.org 4 November 2013 | Volume 10 | Issue 11 | e1001556

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