Healthcare Providers’ Accounts of Influences of Antibiotic-Related Reforms on their Behavior with Respect to the Use of Antibiotics for Children: A Qualitative Study in China

Tingting Zhang*, Hilary Graham and Piran CL White

York, YO10 5NG, UK, Tel: +44(0)1904 322999; Fax: +44 (0)1904 322998; Email:

tz746@york.ac.uk antibiotic use.

analysis.

system that influence their antibiotic-related behavior.

Abbreviations: ABR: Antibiotic Resistance; OTC: Over-The-Counter; EDL: Essential Drug List; ZMU: Zero Mark-Up; CHIs: Community Health Institutions; GPs: General Practitioners; AST: Antimicrobial Sustainability Test; HICs: High Income Countries; LMICs: Low and Middle-Income Countries

Introduction

China has been seriously affected by antibiotic resistance (ABR) [1], which is driven by its high rates of antibiotic use [2, 3, 4]. Paediatric use of antibiotics by healthcare providers (hereafter ‘providers’) is recognized to be a particular challenge, with evidence of high pediatric prescription rates for child patients using hospital outpatient clinics and primary healthcare [5, 6, 7, 8], as well as a widespread purchase of over-the-counter (OTC) antibiotics for children accessed from retail pharmacies [9], which is officially forbidden [10]. The Chinese government’s concern about the inappropriate use of antibiotics resulted in the Ministry of Health, now the National Health and Family Planning Commission, initiating a set of antibiotic-related reforms from 2011 [11, 12]. These reforms mainly included the introduction of a three-year strategy -‘National Special Campaign of the Clinical Use of Antibiotics’ – to promote appropriate use of antibiotics from 2011 to 2013 [11]. One of key features of this strategy is the requirement that physicians adhere to guidelines regarding the prescribing of antibiotics; this should follow a careful check of patients’ clinical presentation and laboratory test results [13]. The strategy has been underwritten by the ‘Administrative Regulations for the Clinical Use of Antibiotics’, the strictest regulation in China so far in terms of antibiotic use [11, 12]. The 2011 reform built on wider healthcare reforms introduced in 2009, which included policies removing financial incentives from drug prescriptions and designed also to promote the appropriate use of antibiotics [14, 15, 16]. Specifically, the government sought to increase access to safe and cost-effective medicines and, at the same time, reduce over-prescribing and use of expensive drugs [17]. The key measures to achieve these goals were the introduction of the Essential Drug List (EDL), supported by the zero mark-up (ZMU) policy. Reducing the high cost of prescription drugs was one of the five priorities of the 2009 reforms relating to prescription drugs [15, 18], and the ZMU policy achieved this by removing the profit margin from drugs sold to prescribers. The EDL is a list of medicines that are most effective and safe, and can be equitably accessed by the public at reasonable price [19]. The latest version, the National Essential Drug List (2012 edition), consists of three parts, including chemical and biological medicines, Chinese traditional formulated drugs, and traditional Chinese cut crude herbs; across these three groups, there are 43 types of antimicrobials [19]. The first stage of the implementation of the EDL and ZMU is at the primary level with the final goal of expanding these policies to the hospitals [18]. To date, the EDL and ZMU policies requiring all national essential drugs to be stocked and dispensed with zero mark-up (no mark-up between wholesale and retail price), have been widely implemented in primary care institutions [14, 20]. These policies also encourage hospitals to make the procurement and provision of national essential drugs a priority and ensure that a minimum of the drugs used by hospitals are from the EDL. In addition, the ZMU policy was scheduled to be implemented in all urban public hospitals by 2017 [14, 21, 22]. Other parts of the 2009 reform, such as expanding the health insurance coverage, have also impacted on providers’ antibiotic-related behavior [15, 16]. Understanding the influence of reform son providers’ behavior with respect to pediatric use of antibiotics is of great importance. However, although studies have suggested that the high rates of antibiotic use declined in China’s hospitals after the 2011 reform [23, 24, 25], there is little evidence on the reforms’ influences on providers’ antibiotic-related behavior, particularly the pediatric use of antibiotics [26, 27, 28, 29]. Qualitative methods, which generate detailed data for our study, are increasingly used to capture provider perspectives and the perceived influences on their behavior [30, 31]. However, only one qualitative study [29] conducted in a rural setting was located via our search of English-language (MEDLINE Ovid) and Chinese (Chinese National Knowledge Infrastructure) databases. The marked differences in socio-economic development across China – particularly differences in healthcare resources and health-related policies – mean rural-based studies may not capture influences on providers’ behavior in urban settings [32]. In addition, the study of Zhang et al. did not focus on the influence of the reforms, but explored more general factors related to village doctors’ antibiotic-prescribing decisions for children under 15 years old with upper respiratory tract infections [29]. Our qualitative study builds on the limited evidence. It explores providers’ perceptions of antibiotic-related reforms’ influences on their behavior with respect to antibiotic use for children in a city with a profile typical of mainland China.

Study Context and Methods

In China, hospitals are the cornerstone of the healthcare system [33]. While the primary care system, including community health institutions (CHIs) in urban areas, is weak, it is growing rapidly [14, 32, 34]. The CHIs can be further divided into community health centers and smaller community health stations. Most hospitals and CHIs have their own pharmacies and these hospital pharmacies still dominate China’s pharmaceutical sales [14]. However, in recent years, retail pharmacies have become a rapidly growing sector, with an average 20% growth in annual pharmaceutical sales from 1978 to 2009 [9]. Retail pharmacies are expected to be staffed by pharmacists who are present during opening hours to provide pharmaceutical services [35]; however, it is not always the case and other staff, such as sales staff, can sell prescribed drugs in retail pharmacies [9, 36, 37]. Our qualitative study included providers in these different sectors. For the hospital sector, we included pediatricians working in outpatient departments along with hospital pharmacists; for the primary care sector, we included general practitioners (GPs) and community pharmacists working in CHIs; and for the retail pharmacy sector, we included retail pharmacists and sales staff working in retail pharmacies. Our study, using semi-structured interviews, was piloted and conducted with providers in Taiyuan city, a medium-sized city in China with average wealth and health expenditure [38, 39]. In line with other qualitative studies conducted in Asian countries with Confucian- based cultures [40, 41], both the study sites and participants of our study were enrolled via personal connections and social networks. This method, which has been confirmed by pilot work, was adapted to the cultural context of China, where the anonymous and formal methods associated with surveys based on random samples can reduce the study validity, for example through study participants giving what they perceive to socially approved answers (social desirability bias) [42]. The study sites were accessed through senior-level staff, and in total three hospitals, six CHIs and five retail pharmacies were successfully enrolled. One potential study site (a CHI) refused. Study participants were then introduced by the senior-level staff, with additional participants suggested by those already recruited to the study.

Results

The antibiotic-related reforms were noted by most participants as an influence on their antibiotic-related behavior. These influences clustered into broad themes, including a) provider facilities (discussed by 23 providers), b) financial considerations (16) c) the influence of other healthcare institutions (16).

Discussion

As far as we are aware, this is the first city-based qualitative study in China exploring providers’ perceptions of the influences of the 2009 and 2011 reforms on their antibiotic-related behavior. Similar to other qualitative studies [45, 46, 47], our study has limitations related to its small sample size. Additionally, it is cross-sectional and therefore cannot compare providers’ views pre and post reforms, but relies on comparisons that providers made about practices prior to and following the reforms. However, its qualitative design provides insight into provider perspectives. The research team has an interdisciplinary background with one female Chinese researcher and two UK researchers (male and female) from different research areas. This facilitated the validity of the study through data interpretation by researcher familiar with Chinese cultural values, who, additionally, was able to clarify any language or culture- related ambiguities; moreover, the use of personal contact recruitment methods reduced potential social desirability bias in a Confusion-based country [48]. As the important role of laboratory-based blood tests in making antibiotic-prescribing decisions was highlighted in the three-year strategy, most providers in our study noted provider facilities as an influence on their antibiotic-related behavior. However, they also pointed to concerns about the lack of diagnostic facilities which made it difficult to adhere to these policies and could work against their appropriate use of antibiotics, concerns which were particularly evident at primary care level. This fits with findings from the qualitative study of Zhang et al. conducted after the reforms, which indicated a lack of diagnostic tests in village clinics of rural China and its influences on doctors’ inappropriate antibiotic- related behavior [29]. Moreover, the limitations of quality-assured diagnostic facilities at primary care level have been reported by a nationwide survey in China [49]; this problem was also highlighted as a challenge among low and middle-income countries (LMICs) resulting in delayed or inaccurate diagnosis and therefore ineffective treatment, which related to gaps, such as basic equipment and laboratory supplies [50]. Our study identified that financial considerations were another factor influencing providers’ use of antibiotics. However, only a few participants pointed to the influence of finance-related policies (the EDL and ZMU policies), even though this set of policies is one of five priorities of 2009 reform [33]. Moreover, a key aim of this set of policies is to reduce financial incentives from prescribing unnecessary drugs at primary care level, with the expectation that the policies will be implemented in other healthcare institutions, such as tertiary hospitals [49, 51]. However, providers’ accounts suggested that financial considerations in different healthcare institutions were not in line with the policies’ focus, with evidence that making profits from antibiotic prescriptions was still regarded as a factor related to the use of antibiotics in CHIs. These findings are similar to studies undertaken in various provinces in China, which noted that the EDL and ZMU policies had no effect on the inappropriate use of antibiotics among primary care institutions [52, 53, 54], even in the period after the introduction of 2011 reform [51, 55, 56]. In the studies of high income countries (HICs), the high workload and limited time have been identified as factors that influenced providers’ antibiotic-related behavior for children in primary care [57, 58]. These factors were also noted by providers in our study; however, they appeared to combine in different ways among providers working in different parts of China’s healthcare system, pointing to the interactions between different healthcare institutions. Along with previous findings related to provider facilities and financial considerations, our study further identified the structure of China’s current healthcare system as an overarching factor shaping the reforms’ influences on providers’ use of antibiotics for children. The overutilization of hospitals for all forms of healthcare provision is a long-standing problem in China; even after the 2009 healthcare reform, hospitals remain the main healthcare provider [32], with higher levels of trust and resources than primary care institutions [14, 49, 59]. High patient demand and the resulting pressure on the hospital pediatricians evident in our study required them to maintain high levels of patient throughput, a factor that appeared to increase pressures on them to prescribe antibiotics.

Compared to the hospitals, China’s primary care system is weak and faces multiple challenges, including underutilization by the public and under-resourcing [14, 49]. Studies note that patients were not switching from hospitals to primary care system after the first few years of 2009 reform [14]. Consistent with this picture, providers in our study who worked at CHIs did not report the workload pressures described by the hospital pediatricians. Moreover, despite increased government subsidies at primary care level since the 2009 reforms, staff in the CHIs is still facing problems of low incomes compared with hospitals [49], which meant that, in our study, financial concerns were more evident in CHI-based providers’ antibiotic-prescribing decisions. In addition, although the importance of the EDL and ZMU policies was underlined by 2009 reform, there is no national pharmaceutical policy framework in China, which has been found to undermine their enforcement [14]. These problems in the healthcare system as a whole have made it difficult for China to realize the aims of 2009 and 2011 reforms. The retail pharmacies are a relatively independent sector in China’s healthcare system, which are supervised by China Food and Drug Administration and were not the focus of the antibiotic-related reforms [32]. Similar to studies investigating the antibiotic distribution in China’s retail pharmacies [9, 36, 60], we found that antibiotics were inappropriately used in retail pharmacies due to poor enforcement of regulations and financial incentives. In addition, while our data are derived from a small-scale study, they suggest that the more regulated use of antibiotics in hospitals and CHIs as a consequence of the reforms has had some perverse effects. In particular, it may have resulted in retail pharmacies, with poorer enforcement of antibiotic-related regulations, becoming a more significant source of unnecessary antibiotics. For example, consumers could purchase unnecessary antibiotics prescribed by doctors from the retail pharmacies, or, as none of retailers in our study mentioned the need for a prescription, they could get over-the-counter antibiotics from retail pharmacies when doctors refused their antibiotic demands. This points to the importance of interactions between healthcare institutions with, in this instance, policies to promote appropriate antibiotic use having the effect of transferring the inappropriate use of antibiotics from institutions which have introduced more stringent enforcement systems to those with poor enforcement.

Conclusion and Implications

Our study adds important evidence on providers’ perceptions of the reforms’ influences on their behavior with respect to the use of antibiotics for children. Undertaken five years after the most recent antibiotic- related reform, the 2011 reform, this study has highlighted provider facilities, financial considerations and other influences from healthcare institutions as being important determinants of antibiotic prescribing behavior for children. Our study points to the importance of strengthening the relatively weaker parts of China’s healthcare system. Strengthening the primary care sector through an increase of government investment and subsidy is in line with the Chinese government’s emphasis on primary care as a key aspect of its national plan [61]. Because of the lack of effective antibiotic-related regulations on the retail pharmacies, further polices and reforms focusing on the retail pharmacy sector are also clearly required. Additionally, antibiotic-related policies and reforms should take the China’s current healthcare system as a whole into consideration, which was identified as an overarching factor shaping the reforms’ influences on providers’ pediatric use of antibiotics.

Acknowledgements

We wish to thank all participants of the interviews who contributed to this study and senior staff in study sites for their support. All authors contributed to the study design, analysis and report writing. Tingting Zhang is supported by a doctoral fellowship funded by the University of York (UK). The fellowship is linked to the Health of Populations and Ecosystems (HOPE) project funded by the Economic and Social Research Council [Grant Number ES/L003015/1]. The authors have no conflicts of interest to disclose.