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Non-prescription sale of antibiotics and service quality in community pharmacies in Guangzhou, China: A simulated client method

  • Lishan Kuang,

    Roles Data curation, Formal analysis, Methodology, Writing – original draft, Writing – review & editing

    Affiliation Department of Health Statistics, School of Medicine, Jinan University, Guangzhou, Guangdong, P.R. China

  • Yizhuo Liu,

    Roles Data curation, Formal analysis, Investigation, Writing – original draft

    Affiliation School of Pharmacy, Jinan University, Guangzhou, Guangdong, P.R. China

  • Wei Wei,

    Roles Formal analysis, Writing – review & editing

    Affiliation Department of Health Statistics, School of Medicine, Jinan University, Guangzhou, Guangdong, P.R. China

  • Xueqing Song,

    Roles Data curation, Investigation

    Affiliation School of Pharmacy, Jinan University, Guangzhou, Guangdong, P.R. China

  • Xiaoqian Li,

    Roles Data curation, Investigation, Methodology

    Affiliation School of Pharmacy, Jinan University, Guangzhou, Guangdong, P.R. China

  • Qiqi Liu,

    Roles Data curation, Investigation

    Affiliation School of Pharmacy, Jinan University, Guangzhou, Guangdong, P.R. China

  • Weimin Hong,

    Roles Data curation, Investigation

    Affiliation School of Pharmacy, Jinan University, Guangzhou, Guangdong, P.R. China

  • Qian Liu,

    Roles Data curation, Investigation

    Affiliation School of Pharmacy, Jinan University, Guangzhou, Guangdong, P.R. China

  • Jingwei Li,

    Roles Data curation, Investigation

    Affiliation School of Pharmacy, Jinan University, Guangzhou, Guangdong, P.R. China

  • Zhongwei Chen,

    Roles Data curation, Investigation

    Affiliation School of Pharmacy, Jinan University, Guangzhou, Guangdong, P.R. China

  • Yu Fang ,

    Roles Conceptualization, Methodology, Supervision, Writing – review & editing

    xiasujian@162.com (SX); yufang@mail.xjtu.edu.cn (YF)

    Affiliation School of Pharmacy, Xi’an Jiaotong University, Xi’an, Shaanxi, P.R. China

  • Sujian Xia

    Roles Funding acquisition, Methodology, Project administration, Resources, Supervision, Writing – original draft

    xiasujian@162.com (SX); yufang@mail.xjtu.edu.cn (YF)

    Affiliation Department of Health Statistics, School of Medicine, Jinan University, Guangzhou, Guangdong, P.R. China

Abstract

Objective

To measure the situation of the non-prescription sale of antibiotics and the service quality of community pharmacies in Guangzhou, China.

Methods

A simulated client method was conducted to estimate the non-prescription sale of antibiotics and service quality based on scenarios about adult acute upper respiratory tract infection in 2019. A total of 595 community pharmacies from 11 districts were investigated in Guangzhou, China. We used binary logistic regression to evaluate the factors associated with the non-prescription sale of antibiotics.

Results

The proportion of non-prescription dispensing of antibiotics was 63.1% in Guangzhou, China, with a higher incidence of antibiotic dispensing without prescription in outer districts (69.3%). Cephalosporin (44.1%) and Amoxicillin (39.0%) were sold more often than other antibiotics. Chain pharmacies had better performance on the prescription sale of antibiotics and service quality. Traditional Chinese medicine was commonly recommended by pharmacy staff.

Conclusion

Since the non-prescription sale of antibiotics is prevalent in Guangzhou, effective solutions should be determined. Strengthened public awareness and regulatory system innovation are needed.

Introduction

Antibiotics are the most commonly prescribed medicines in the world [1]. Between 2000 and 2015, Global dispensing of antibiotics increased by 65% [2]. China was one of the leading consumers among low- and middle-income countries, where antibiotic consumption increased by 79% between 2000 and 2015 [2]. Due to the large sales of antibiotics, the issue of antibiotic resistance has drawn global attention because it can affect not only health but also the economy [3].

A prescription is a medical document issued by a licensed doctor to certify a patient’s medication [4]. The non-prescription sale of antibiotics reduces barriers to obtaining an antibiotic for patients, which may increase the sales of antibiotics. The global prevalence of the non-prescription sale of antibiotics urgently requires solutions, especially in developing countries [5]. As early as 2003, the National Medical Products Administration of China clearly stated that antibiotics that are not over-the-counter medicines must be sold with prescriptions issued by licensed physicians in all community pharmacies nationwide [6]. In 2016, the Chinese government proposed that all community pharmacies across the country dispense antibacterial drugs based on prescriptions by 2020 [7]. In Tanzania, the percentage (92.3%) of retailers dispensing antibiotics without a prescription was high and the description of drug side effects was limited [8]. Most respondents in Nigeria bought antibiotics to self-treat cold and cough [9]. A report from Zambia showed that most customers acquired antibiotics without a prescription in community pharmacies, which is similar to the findings from the Kingdom of Saudi Arabia [10, 11]. In India, among those patients who consumed antibiotics for the treatment of upper respiratory tract infections, only 7% of them have been prescribed a prescription from a licensed doctor [12]. The non-prescription sale of antibiotics grew rapidly in Hungary even though antibiotics can only be obtained by prescription [13]. A meta-analysis published in 2019 estimated the proportion of the non-prescription sale of antibiotics in community pharmacies worldwide [14]. In Asia, 65% of antibiotics were sold without a prescription in community pharmacies [14]. More than a half of pharmacy staff sold antibiotics without a prescription in surveyed areas of China [14].

Liu reported that it was unknown which antibiotics are dispensed most often without a prescription [5]. We found that Chang et al. [15] performed research on the state of non-prescription sales of antibiotics and trends in six provinces of China, which should be commended. However, the popularity of non-prescription sales of antibiotics in community pharmacies in southern China is still not known. As the province with the largest population in China, Guangdong Province has over 50,000 pharmacies [16, 17]. As the capital of Guangdong Province, there are 6,021 community pharmacies in Guangzhou city [18]. The status of the non-prescription sale of antibiotics in Guangzhou city should be given close consideration. In addition, respiratory diseases are one of the leading causes of death in Chinese urban residents [16]. Moreover, treatments of adult upper respiratory tract infections are commonly associated with the misuse of antibiotics by household self-medication [9, 12]. Chang et al. [15] also mention that the effect of pharmaceutical chains on service quality needs to be studied further. With the advancement of the Internet, pharmacy internet services are very efficient at some times, such as the period when people are required to maintain social distance to prevent the epidemic of COVID-19 [19].

In our study, investigators simulate patients with upper respiratory tract infections to inquire into the non-prescription sale of antibiotics and the service quality at community pharmacies in Guangzhou city. We explore the differences between urban and rural areas by comparing non-prescription sale of antibiotics of the main districts and the outer districts. The research results can provide a basis for the Guangzhou government to formulate regulations on promoting the prescription-based sale of antibiotics in community pharmacies. Moreover, we explore the current status and influencing factors of the service quality, including network services of community pharmacies in Guangzhou. Compared to sole-proprietor pharmacies, chain pharmacies may have more funds and a better employee training system. We expect that the chain pharmacies would perform better than sole-proprietor pharmacies in terms of service quality. Therefore, we compare the service quality of sole-proprietor pharmacies and chain pharmacies in this study.

Method

Study design

The simulated client method included investigators trained strictly in accordance with planned procedures to survey the service site as ordinary customers to simulate a real-world experience. In 2019, we conducted the simulated client method on 595 community pharmacies located in 11 districts in Guangzhou city, which is the capital of Guangdong Province. The sample size is approximately 10% of all pharmacies in Guangzhou city. The distribution of surveyed pharmacies is consistent with the distribution of the resident populations in each district. Please refer to S1 Appendix for the sample composition. Convenience sampling was done at each district. Since the government office are usually located in the center of community, we investigated pharmacies that are near the government office in each street of the district. During pre-survey, 50 pharmacies were randomly selected for investigator training and record sheet modifications. Eight pharmacy students from Jinan University conducted the investigation while simulating adult upper respiratory tract infections after three standard training sessions. Three levels of demand were used to obtain the antibiotic [15]: The pharmacy staff recommended antibiotics actively to the simulated client after the simulated client describes his/her symptoms (level 1); the antibiotic was sold when the simulated client asked for antibiotics (level 2); the antibiotic was sold when the simulated client asked for amoxicillin or cephalosporin (level 3). Please refer to S2 Appendix for the investigation process. The name and specific address of the pharmacy under investigation was not be recorded. Instead, a serial number was assigned to the record sheet.

Study variables

The record sheet that was modified based on published studies consisted of four parts [15] (S3 Appendix). First, characteristics of pharmacies were recorded including pharmacy scale, pharmacy type, pharmacist license, prescription drug sign, prescription drug counter, is the pharmacist on duty, whether to provide online services and whether it is a medical insurance designated pharmacy and so on. Second, characteristics of the reception staff observed during investigation were also recorded, including gender, age and whether the reception staff was a licensed pharmacist. Third, the non-prescription sale of antibiotics by investigated pharmacies and the category of antibiotics sold without acquiring prescription was recorded. Finally, the service quality of community pharmacies was recorded. In this part, we recorded whether or not reception staff asked about a history of drug allergy during the non-prescription sale of antibiotics, whether or not patients were asked about other drugs being taken, and whether or not patients were advised to see a doctor, given advice regarding medication or prevention, or given recommendations for medicines other than antibiotics. Furthermore, service time, whether or not service was provided online, and any specific advice given by staff, including the specific name of non-antibiotic medicines recommended by staff, were recorded.

Statistical analysis

It is reported that the proportion of non-prescription sales of antibiotics is higher in rural areas [20]. Outer districts have a larger rural population than main districts. For that reason, we compared the results of main districts and outer districts. Univariate analyses were conducted to compare characteristics of pharmacies, characteristics of reception staff, the non-prescription sale of antibiotic, the category of antibiotics sold and the service quality of community pharmacies between the main district and the outer district. We performed multivariate, binary logistic regressions to evaluate the factors associated with the non-prescription sale of antibiotics in the main and outer districts adjusted for the age and gender of reception staff [15]. Differences in service quality between sole-proprietor pharmacies and chain pharmacies were also analyzed. Chi-squared tests were used to compare categorical variables between two groups. Additionally, we compared the percentage of medication or prevention advice provided from staff and medicines other than antibiotics recommended by staff between the main districts and outer districts. A p-value of < 0.05 was considered significant. Pairwise deletion method, which is considered effective when only a small part of data are missing, was used to handle missing data [21].

This study was approved by the Institutional Review Board of the First Affiliated Hospital of Jinan University. We used the simulated client method, as the study cannot be performed if the investigators’ identity is disclosed to the pharmacy staff. Since it is an observational and minimal-risk study, consent from pharmacies was waived under the policy of the IRB.

Results

Characteristics of pharmacies and reception staff

Table 1 shows the characteristics of pharmacies and reception staff. The total pharmacies surveyed numbered 595, consisting of 406 pharmacies from the main districts and 189 pharmacies from the outer districts. Among all pharmacies, over 70% of pharmacies were considered medium in scale. No significant difference was found between the main districts and the outer districts. Compared to the outer districts, the main districts had more chain pharmacies (p = 0.002). Almost 90% of pharmacies both in the main districts and the outer districts had signed a medical insurance agreement with the Medical Insurance Agency. In other words, the cost of the applicant buying medicines in these pharmacies was partly covered by medical insurance. The great majority of pharmacies had a pharmacist license, a sign of prescription drug and a prescription drug counter. Only approximately one-third of pharmacies had a pharmacist on duty. In terms of the characteristics of reception staff, few reception staff were registered pharmacist. The gender of most of reception staff was female. More than half were between 30 and 50 years old. Relative to the outer districts, the reception staff were younger in the main districts (p <0.001).

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Table 1. The characteristics of community pharmacies and reception staff.

https://doi.org/10.1371/journal.pone.0243555.t001

Non-prescription sale of antibiotics

The non-prescription sale of antibiotics in Guangzhou is summarized in Table 2. A total of 375/595 (63.1%) interactions resulted in the non-prescription sale of antibiotics. Significant differences were found in the non-prescription sale of antibiotics between the main districts and the outer districts. Pharmacies in outer districts were more likely to distribute antibiotics without requiring a prescription. A total of 72 (12.1%) pharmacies sold antibiotics under demand level 1. A total of 127 (21.4%) pharmacies sold antibiotics under demand level 2. Cephalosporin and Amoxicillin were most often sold when reception staff sold antibiotics actively (level 1) and investigators asked for an antibiotic during interactions of the non-prescription sale of antibiotics (level 2). The category of antibiotics sold without prescription was not significantly different between the main districts and the outer districts.

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Table 2. Non-prescription sale of antibiotics in Guangzhou.

https://doi.org/10.1371/journal.pone.0243555.t002

Univariate analysis and multiple logistic regression analysis

Table 3 shows that a univariate logistical analysis was used to ascertain the relationship between the non-prescription sale of antibiotics and characteristics of pharmacies and reception staff. Among those characteristics, pharmacy scale and pharmacy type were significantly associated with the non-prescription sale of antibiotics for pharmacies located in the main districts. Medium (p = 0.0369) and small (p = 0.0365) pharmacies were more inclined to dispense antibiotics without a prescription than large pharmacies. Additionally, sole-proprietor pharmacies had a greater proportion of non-prescription sales of antibiotics than chain pharmacies. We calculated the adjusted OR by adjusting for gender and the age of reception staff (S4 Appendix). The multiple regression model showed that pharmacy scale was related to the non-prescription sale of antibiotics for pharmacies located in the main districts (p<0.05). No association between the non-prescription sale of antibiotics and the characteristics of pharmacies and reception staff in outer districts was observed.

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Table 3. The relationship between the non-prescription sale of antibiotics and the characteristics of pharmacies and reception staff in Guangzhou.

https://doi.org/10.1371/journal.pone.0243555.t003

Service quality

First, we compared the service quality of pharmacies between the main districts and the outer districts, as shown in Table 4. Suggestions about medication or prevention were given in 47.3% and 48.7% of interactions when the non-prescription sale of antibiotics happened in the main districts and the outer districts, respectively (Fig 1). Reception staff of pharmacies in the main districts tended to offer advice about lifestyle. Comparatively, suggestions on the dosage of drugs were more recommended in the outer districts. A majority of reception staff recommended drugs other than antibiotics (Fig 2). Among those interactions, the most popular category of drugs was traditional Chinese medicine. No significant differences between the main and outer districts were observed in whether or not the staff asked about a history of drug allergies, whether or not suggestions about medications or preventions were given, whether or not a list of current medications was solicited, whether or not it was suggested to go to the doctor and whether or not online services were provided (p>0.05).

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Fig 1. Medication or prevention advice given by reception staff in community pharmacies in Guangzhou.

https://doi.org/10.1371/journal.pone.0243555.g001

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Fig 2. The types of non-antibiotic medicines recommended by reception staff in community pharmacies in Guangzhou.

https://doi.org/10.1371/journal.pone.0243555.g002

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Table 4. Differences in the service quality of community pharmacies between the main districts and the outer districts in Guangzhou.

https://doi.org/10.1371/journal.pone.0243555.t004

Second, the results of the service quality of sole-proprietor pharmacies and chain pharmacies are shown in Table 5. We found statistically significant differences in asking for a history of drug allergies or not and in providing online service or not between sole-proprietor pharmacies and chain pharmacies (p<0.05). In the interaction of the non-prescription sale of antibiotics, more reception staff in chain pharmacies asked whether the patient had a drug allergy history. Moreover, the proportion of chain pharmacies that had an online service platform is larger than that for sole-proprietor pharmacies.

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Table 5. Differences of in service quality between sole-proprietor pharmacies and chain pharmacies in Guangzhou.

https://doi.org/10.1371/journal.pone.0243555.t005

Discussion

In our study, more than half of community pharmacies in Guangzhou dispensed antibiotics without a prescription. The proportion of the non-prescription sale of antibiotics in community pharmacies in main districts is significantly less than that in community pharmacies in outer districts. For community pharmacies in main districts, scale and type are influencing factors in the non-prescription sale of antibiotics. On the other hand, we also investigated the service quality of community pharmacies. We found that only a few pharmacies can provide internet services. The service hours of community pharmacies are generally short. Almost all reception staff recommended medicines other than antibiotics to patients. Approximately half of the pharmacy reception staff did not ask customers about their drug allergy history. Compared to the sole-proprietor pharmacies, chain pharmacies have better performance in service quality.

The proportion of the non-prescription sale of antibiotics in Guangzhou, China (63.1%) is equivalent to the pooled estimate globally (62%, 95% CI 53–72) [14]. Additionally, the percentage of Guangzhou is lower than the pooled estimate of South America (78%, 95CI% 72–84) and Africa (74%, 95% CI 62–85) [14]. A survey done in 2019 [15] found that the proportion of non-prescription sales of antibiotics in eastern, central, and western China is 70.1%, which is higher than the proportion in Guangzhou found here. The results present here indicate that pharmacies in the outer districts were more likely to sell antibiotics without a prescription than those in the main districts. We think that the difference between the main districts and outer districts may be due to the following reasons. First, the outer districts have a less developed economy than the main districts [22]. Individuals with poor financial ability are more likely avoid consulting doctors due to considerations of expense and thus choose self-treatment [23]. Second, the number of villages in the outer districts is relatively large [24]. Individuals in rural areas have less knowledge about antibiotics [25]. Moreover, the non-prescription sale of antibiotics is more likely happen in rural than urban areas [20]. Therefore, pharmacies in outer districts may more routinely sell antibiotics without acquiring a prescription.

In keeping with work done in India and other provinces of China, our study shows that factors that affect the non-prescription sale of antibiotics in the main districts are the scale and type of pharmacy [15, 26]. Chain pharmacies located in the main districts are more inclined to sell antibiotics with a prescription from a doctor. Medium and small pharmacies are associated with more non-prescription sales of antibiotics than large pharmacies. Smaller pharmacies and sole-proprietor pharmacies may have relatively little funding. For that reason, staff training may not be carried out effectively in smaller pharmacies. At the same time, factors affecting the non-prescription sale of antibiotics in outer districts was not found. However, the illegal rate of pharmacies in outer districts is higher than that in the main districts. Therefore, the factors that affect the proportion of non-prescription sales of antibiotics by pharmacies in outer districts are not the characteristics of the pharmacies we studied but may be due to other reasons. The specific reasons that affect the proportion of non-prescription sales of antibiotics of the pharmacies in outer districts needs further research.

In our study, when reception staff sold antibiotics actively or investigators asked for an antibiotic, Cephalosporin and Amoxicillin were most often sold. Amoxicillin was also found to be the most commonly non-prescribed antibiotic sold in Zambia [10]. Cephalosporin and Amoxicillin are commonly used drugs to treat infectious diseases in many countries, such as the United States, the Netherlands and France [2729]. Cephalosporin should be used as a reserve drug rather than the first choice for the treatment of infectious diseases. For that reason, the high proportion of non-prescription sales of Cephalosporin should be taken seriously. Additionally, allergic reactions to Amoxicillin and Cephalosporin, which are both beta-lactams, are commonly reported [30]. However, less than half of reception staff asked if the patient had a history of drug allergies when they sold antibiotics without a prescription in our study. Additionally, similar to a study in Tanzania, our work found that side effects of medicines are rarely mentioned [8]. Beta-lactam allergies may cause bronchospasm and even anaphylactic shock in some severe cases [30]. Hence, staff training about medication specification should be strengthened. We believe that the risk of patient antibiotic abuse could be reduced when the allergy history of the patient is known to reception staff.

As we observed, traditional Chinese medicine was popular with reception staff in the treatment of adult colds. In recent years, traditional Chinese medicine has shown some effectiveness in the relief of clinical symptoms in the treatment of adult acute respiratory tract infections and some non-infectious diseases [3133]. However, well-designed experiments are needed to further prove the efficacy and safety of traditional Chinese medicine [31].

In addition to non-prescription sales of antibiotics, we analyzed the quality of service in pharmacies. Service times at community pharmacies in Guangzhou were generally less than five minutes. In this short time, reception staff may only ask the main symptoms of a patient. Some situations that needed to be noticed may be ignored, such as a history of drug allergies of patients. Therefore, a lack of information from patients may lead to reception staff making an incorrect decision on medication dispensation. Chain pharmacies have sufficient funds, so the content of employee training may be more abundant. Compared with Sole-proprietor pharmacies, the proportion of employees of chain pharmacies that made recommendations on disease prevention may be greater. Therefore, in the main districts with more chain pharmacies, more staffs advise patients to change their lifestyles to prevent disease or its deterioration. Chain pharmacies have better performance in service quality. The reception staff of chain pharmacies were more likely to ask about the allergy history of the patient, which means that chain pharmacies can provide safer medication services to patients than sole-proprietor pharmacies. Additionally, a greater proportion of chain pharmacies provide online service. Online pharmacies have enormous potential in the future [34]. The global market of online pharmacies was approximately USD 42.3 billion in 2018; this is estimated to expand to USD 107.5 billion in 2025 [35]. According to a study of seven countries, using online health services has resulted in more relaxation than anxiety [36]. As research published in 2016 reported, a quarter of respondents searched for information on a medication online [37]. Online pharmacies can facilitate individuals with reduced mobility and individuals living in remote areas. Moreover, medicine sales data can be quickly and accurately collected from a unified online pharmacy platform. Real-time medicine sales data enable regulators to monitor antibiotic dispensing efficiently. It is feasible to establish a unified pharmacy drug sales platform in China [38]. However, a regulatory system on online pharmacies also needs to be established because it is also possible to sell antibiotics without a prescription online [39, 40].

Some published studies show that a pharmacist’s participation in intervention design, education for dispensing staff, public education campaigns and supervision from government staff are effective in reducing the probability of non-prescription sales of antibiotics [41]. Moreover, interventions should continue to be implemented for a sufficiently long duration [42]. In other words, dispensers and the public should be regularly educated. Government personnel should regularly carry out supervision of the non-prescription sale of antibiotics.

Raising caution with the public and pharmacists regarding the prescription of antibiotics is necessary. In developing countries, the proportion of self-treatment with antibacterial drugs was 38.8% [43]. Research performed in Chinese cities showed that 41.0% of caregivers were not aware that a doctor’s prescription is necessary to buy antibiotics from community pharmacies [44]. Thus, to reduce public demand for antibiotics without a prescription, public education on regulations of prescription drugs should be strengthened. Effective education can be achieved not only through traditional paper media but also through internet media. More diversified ways of disseminating information on the Internet should be considered, such as video, music, and images. More importantly, training on antibiotic medications for pharmacy workers is key to reducing antibiotic abuse. Pharmacists have insufficient knowledge of the efficacy of antibiotics [45]. To update the knowledge of pharmacists in a timely manner, routine testing should be held in addition to the licensed pharmacist qualification examination.

Laws and regulations on antibiotic medication need to be improved and implemented effectively. Poor regulations and a lack of qualified pharmacists were contributing factors for the non-prescription sales of antibiotics in developing countries [46]. Additionally, as reported previously, licensed pharmacists on duty are associated with the prescription sale of antibiotics [15]. According to the regulations, community pharmacies must be equipped with licensed pharmacists [47]. However, in China, the scale of licensed pharmacists is still insufficient [48]. Moreover, no pharmacist is actually on duty in a large number of pharmacies [49]. Fines have proven effective in reducing non-prescription sales of antibiotics [50]. Training more licensed pharmacists and increasing penalties for illegal community pharmacies could be effective methods.

Our study has some limitations. First, although uniform training for investigators was conducted, differences between simulated customers may still exist. The symptoms simulated by different investigators may vary. Second, we sampled pharmacies according to the distribution of the number of permanent residents and implemented convenience sampling in each district in Guangzhou city. Pharmacies investigated by simulated customers may be more inclined to comply with regulations because those pharmacies are geographically close to the local government position. In other words, the proportion of the non-prescription sale of antibiotics in our study may be underestimated. Third, the sample size of this study is approximately 10% of all pharmacies in Guangzhou city. The data for the total number of pharmacies in Guangzhou comes from a study published in 2011. As the population increases, the total number of pharmacies in Guangzhou may increase during the intervening years. Therefore, the actual sample size of this study may be smaller than mentioned above. The representativeness of the sample may be overestimated. Fourth, as an observational study, this study cannot explore the effect of interventions on the non-prescription sale of antibiotics in Guangzhou city. Fifth, according to the above research results, the factors affecting the non-prescription sale of antibiotics in outer districts have not been found. Further research can explore the impact of other factors (such as different diseases, knowledge, attitude and perception of pharmacy staff) on the non-prescription sale of antibiotics in outer districts [51, 52]. Last, three levels of demand were used to obtain the antibiotics in our study. The customer made a request to buy antibiotics in level 2 and level 3, which may make pharmacies more inclined to sell antibiotics without prescription.

Conclusion

Our findings fill a data gap regarding the non-prescription sale of antibiotics in Guangzhou, China. Non-prescription sales of antibiotics in Guangzhou were less severe than in other regions studied in China but were still prevalent. Cephalosporin and Amoxicillin were sold more often than other antibiotics. The frequent use of Cephalosporin and Amoxicillin should be paid close attention. Drug side effects were rarely described clearly. A higher incidence of antibiotic dispensation without a prescription was observed in outer districts. Chain pharmacies had better performances on the prescription sale of antibiotics and service quality, including inquiring about the allergy history of the patient and providing online service. Traditional Chinese medicine was commonly recommended by pharmacy staff. Public awareness and pharmacist training should be strengthened.

Supporting information

S4 Appendix. The relationship between the non-prescription sale of antibiotics and the characteristics of pharmacies and reception staff in Guangzhou.

https://doi.org/10.1371/journal.pone.0243555.s004

(DOCX)

References

  1. 1. Van Boeckel TP, Gandra S, Ashok A, Caudron Q, Grenfell BT, Levin SA, et al. Global antibiotic consumption 2000 to 2010: an analysis of national pharmaceutical sales data. Lancet Infect Dis. 2014;14: 742–750. pmid:25022435
  2. 2. Klein EY, Van Boeckel TP, Martinez EM, Pant S, Gandra S, Levin SA, et al. Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc Natl Acad Sci U S A. 2018;115: E3463–E3470. pmid:29581252
  3. 3. Laxminarayan R, Duse A, Wattal C, Zaidi AKM, Wertheim HFL, Sumpradit N, et al. Antibiotic resistance—the need for global solutions. Lancet Infect Dis. 2013;13: 1057–1098. pmid:24252483
  4. 4. Ministry of Health of the People's Republic of China. Prescription management.2006 [cited 29 February 2020]. Available from: http://www.nhc.gov.cn/yzygj/s3572/200602/dd4277bbf3784ff589b9f12b6a0422ab.shtml
  5. 5. Liu J. Tackling the global non-prescription use of antibiotics. Lancet Infect Dis. 2020;20: 169–170. pmid:32006505
  6. 6. National Medical Products Administration. The supervision of antibacterial drug sales in community pharmacies should be strengthened and rational drug use should be promoted.2003[cited 22 July 2020]. Available from:http://www.sda.gov.cn/cmsweb/webportal/W945325/A38046820.htm
  7. 7. National Health and Family Plan Commission of China, National Development and Reform Commission of China, Ministry of Education of China, et al. National action plan for the containment of antibacterial resistance (2016–2020). 2016[cited 22 July 2020]. Available from: http://www.gov.cn/xinwen/2016–08/25/content_5102348.htm
  8. 8. Horumpende PG, Sonda TB, van Zwetselaar M, Antony ML, Tenu FF, Mwanziva CE, et al. Prescription and non-prescription antibiotic dispensing practices in part I and part II pharmacies in Moshi municipality, Kilimanjaro region in Tanzania: a simulated clients approach. PLos One. 2018;13: e0207465. pmid:30462700
  9. 9. Badger-Emeka LI, Emeka PM, Okosi M. Evaluation of the extent and reasons for increased non-prescription antibiotics use in a University town, Nsukka Nigeria. Int J Health Sci. 2018;12: 11–17.
  10. 10. Kalungia AC, Burger J, Godman B, Costa JD, Simuwelu C. Non-prescription sale and dispensing of antibiotics in community pharmacies in Zambia. Expert Rev Anti Infect Ther. 2016;14: 1215–1223. pmid:27548801
  11. 11. Khan TM, Ibrahim Y. A qualitative exploration of the non-prescription sale of drugs and incidence of adverse events in community pharmacy settings in the Eastern province of the kingdom of Saudi Arabia. Eur J Hosp Pharm Sci Pract. 2013;20: 26–31.
  12. 12. Bhanwra S. A study of non-prescription usage of antibiotics in the upper respiratory tract infections in the urban population. J Pharmacol Pharmacother. 2013;4: 62–64. pmid:23662028
  13. 13. Matuz M, Benko R, Doro P, Hajdu E, Soos G. Non-prescription antibiotic use in Hungary. Pharm World Sci. 2007;29: 695–698. pmid:17530434
  14. 14. Auta A, Hadi MA, Oga E, Adewuyi EO, Abdu-Aguye SN, Adeloye D, et al. Global access to antibiotics without prescription in community pharmacies: a systematic review and meta-analysis. J Infect. 2019;78: 8–18. pmid:29981773
  15. 15. Chang J, Xu S, Zhu S, Li Z, Yu J, Zhang Y, et al. Assessment of non-prescription antibiotic dispensing at community pharmacies in China with simulated clients: a mixed cross-sectional and longitudinal study. Lancet Infect Dis. 2019;19: 1345–1354. pmid:31588042
  16. 16. National Bureau of Statistics. China Statistical Yearbook. 2019 [cited 29 February 2020]. Available from: http://www.stats.gov.cn/tjsj/ndsj/2019/indexch.htm.
  17. 17. Li Z, Zhou Y, Xie G, Zhang T, Zhang Q, Ban L. Study on the employment of licensed pharmacists in retail pharmacies in Qinghai, Yunnan, Sichuan and Guangdong Provinces. China Pharm. 2019;07: 1320–1322+1343.
  18. 18. Wu H-X. Investigation of the development situation of Guangzhou drug retail market. China Pharm. 2011;22: 862–864.
  19. 19. Morawska L, Cao J. Airborne transmission of SARS-CoV-2: the world should face the reality. Environ Int. 2020;139: 105730. pmid:32294574
  20. 20. Zapata-Cachafeiro M, Pineiro-Lamas M, Guinovart MC, Lopez-Vazquez P, Vazquez-Lago JM, Figueiras A. Magnitude and determinants of antibiotic dispensing without prescription in Spain: a simulated patient study. J Antimicrob Chemother. 2019;74: 511–514. pmid:30395222
  21. 21. Schafer JL, Graham JW. Missing data: our view of the state of the art. Psychol Methods. 2002;7: 147–177. pmid:12090408
  22. 22. Zhongyan L. The research on regional comprehensive economic strength of Guangzhou. Master, Jinan University. 2011.
  23. 23. Alhomoud F, Aljamea Z, Almahasnah R, Alkhalifah K, Basalelah L, Alhomoud FK. Self-medication and self-prescription with antibiotics in the Middle East-do they really happen? A systematic review of the prevalence, possible reasons, and outcomes. Int J Infect Dis. 2017;57: 3–12. pmid:28111172
  24. 24. Guangzhou Statistics Bureau. Population size and distriution of Guangzhou in 2018. 2019 [cited 29 February 2020]. Available from: http://tjj.gz.gov.cn/tjgb/qtgb/content/post_2788687.html
  25. 25. Farkas M, Ivce DG, Stojanovic S, Mavrinac M, Micovic V, Andrasevic AT. Parental knowledge and awareness linked to antibiotic use and resistance: comparison of urban and rural population in Croatia. Microb Drug Resist. 2019;25: 1430–1436. pmid:31314687
  26. 26. Miller R, Goodman C. Do chain pharmacies perform better than independent pharmacies? Evidence from a standardised patient study of the management of childhood diarrhoea and suspected tuberculosis in urban India. BMJ Glob Health. 2017;2: e000457 pmid:29018588
  27. 27. Cars O, Mölstad S, Melander A. Variation in antibiotic use in the European Union. Lancet. 2001;357: 1851–1853. pmid:11410197
  28. 28. Ong DSY, Kuyvenhoven MM, van Dijk L, Verheij TJM. Antibiotics for respiratory, ear and urinary tract disorders and consistency among GPS. J Antimicrob Chemother. 2008;62: 587–592. pmid:18544602
  29. 29. McCaig LF, Hughes JM. Trends in antimicrobial drug prescribing among office-based physicians in the United States. JAMA. 1995;273: 214–219. pmid:7807660
  30. 30. Viola M, Quaratino D, Gaeta F, Valluzzi RL, Caruso C, Rumi G, et al. Allergic reactions to antibiotics, mainly betalactams: facts and controversies. Eur Ann Allergy Clin Immunol. 2005;37: 223–229. pmid:16156401
  31. 31. Hu XY, Wu RH, Logue M, Blondel C, Lai LYW, Stuart B, et al. Andrographis paniculata (Chuan Xin Lian) for symptomatic relief of acute respiratory tract infections in adults and children: a systematic review and meta-analysis. PLos One. 2017;12: 30.
  32. 32. Pang B, Li Q-W, Qin Y-L, Dong G-T, Feng S, Wang J, et al. Traditional chinese medicine for diabetic retinopathy: a systematic review and meta-analysis. Medicine. 2020;99: e19102. pmid:32049817
  33. 33. Yu Y, Zhang G, Han T, Huang H. Efficacy and safety of oral traditional Chinese patent medicine in treatment of liver stagnation and spleen deficiency of depression: a protocol for systematic review. Medicine. 2020;99: e19142. pmid:32049837
  34. 34. Chen YK, Chiu FR, Chang YC. Implementing green supply chain management for online pharmacies through a VADD inventory model. Int J Environ Res Public Health. 2019;16: 18 pmid:31766175
  35. 35. Globe Newswire. Global E-Pharmacy Market will Reach USD 107.53 Billion By 2025: Zion Market Research. 2019 [cited 18 June 2019]. Available from: https://www.globenewswire.com/news-release/2019/06/18/1870266/0/en/Global-E-Pharmacy-Market-Will-Reach-USD-107-53-Billion-By-2025-Zion-Market-Research.html/.
  36. 36. Andreassen HK, Bujnowska-Fedak MM, Chronaki CE, Dumitru RC, Pudule I, Santana S, et al. European citizens' use of E-health services: a study of seven countries. BMC Public Health. 2007;7: 53. pmid:17425798
  37. 37. Lombardo S, Cosentino M. Internet use for searching information on medicines and disease: a community pharmacy-based survey among adult pharmacy customers. Interact J Med Res. 2016;5: 24–30. pmid:27417304
  38. 38. Meng L, Wu Z. Exploration on establishment of unified electronic trading platform of online pharmacies in China. China Pharm. 2012;23: 1245–1248.
  39. 39. Cicero TJ, Ellis MS. Health outcomes in patients using no-prescription online pharmacies to purchase prescription drugs. J Med Internet Res. 2012;14: 347–359. pmid:23220405
  40. 40. Chen J, Jiang K, Liu Y. The problems and measures of supervision of standardized management of the online pharmacies in China. Chin Pharm J. 2015;50: 1643–1647.
  41. 41. Wirtz VJ, Herrera-Patino JJ, Santa-Ana-Tellez Y, Dreser A, Elseviers M, Stichele RHV. Analysing policy interventions to prohibit over-the-counter antibiotic sales in four Latin American countries. Trop Med Int Health. 2013;18: 665–673. pmid:23551290
  42. 42. Jacobs TG, Robertson J, van den Ham HA, Iwamoto K, Bak Pedersen H, Mantel-Teeuwisse AK. Assessing the impact of law enforcement to reduce over-the-counter (OTC) sales of antibiotics in low- and middle-income countries; a systematic literature review. BMC Health Serv Res. 2019;19: 536. pmid:31366363
  43. 43. Ocan M, Obuku EA, Bwanga F, Akena D, Richard S, Ogwal-Okeng J, et al. Household antimicrobial self-medication: a systematic review and meta-analysis of the burden, risk factors and outcomes in developing countries. BMC Public Health. 2015;15: 742. pmid:26231758
  44. 44. Chang J, Lv B, Zhu S, Yu J, Zhang Y, Ye D, et al. Non-prescription use of antibiotics among children in urban China: a cross-sectional survey of knowledge, attitudes, and practices. Expert Rev Anti Infect Ther. 2018;16: 163–172. pmid:29310469
  45. 45. Hoxha I, Malaj A, Kraja B, Bino S, Oluka M, Markovic-Pekovic V, et al. Are pharmacists' good knowledge and awareness on antibiotics taken for granted? The situation in Albania and future implications across countries. J Glob Antimicrob Resist. 2018;13: 240–245. pmid:29414723
  46. 46. Sakeena MHF, Bennett AA, McLachlan AJ. Non-prescription sales of antimicrobial agents at community pharmacies in developing countries: a systematic review. Int J Antimicrob Agents. 2018;52: 771–782. pmid:30312654
  47. 47. Chinese National Medical Prosucts Asministration. Regulations on the professional qualification system of licensed pharmacist and implementation measures. 2019 [cited 29 February 2020]. Available from: http://www.nmpa.gov.cn/WS04/CL2196/335795.html.
  48. 48. Huang H, Li G, Liu S. Thinking on the role orientation of licensed pharmacists in China. China Pharm. 2014;25: 2398–2400.
  49. 49. Zhen K. Analysis on the problem of "license registration" of licensed pharmacists. China Food & Drug Administration Magazine. 2019;4: 102–104.
  50. 50. Alrasheedy AA, Alsalloum MA, Almuqbil FA, Almuzaini MA, Aba Alkhayl BS, Albishri AS, et al. The impact of law enforcement on dispensing antibiotics without prescription: a multi-methods study from Saudi Arabia. Expert Rev Anti Infect Ther. 2020;18: 87–97. pmid:31834825
  51. 51. Koji EM, Gebretekle GB, Tekle TA. Practice of over-the-counter dispensary of antibiotics for childhood illnesses in Addis Ababa, Ethiopia: a simulated patient encounter study. Antimicrob Resist Infect Control. 2019;8: 119. pmid:31346460
  52. 52. Machowska A, Lundborg CS. Drivers of irrational use of antibiotics in Europe. Int J Environ Res Public Health. 2018;16: 27. pmid:30583571