Literature DB >> 31242185

Clinical pattern of antibiotic overuse and misuse in primary healthcare hospitals in the southwest of China.

Yue Chang1,2, Sarunyou Chusri3,4, Rassamee Sangthong2, Edward McNeil2, Jiaqi Hu1, Wei Du1, Duan Li1, Xingying Fan1, Hanni Zhou1, Virasakdi Chongsuvivatwong2, Lei Tang1.   

Abstract

PURPOSE: Overuse and misuse of antibiotics are the primary risk factors for antibiotics resistance. Inadequate professional competence of primary care physicians might exacerbate these problems in China. This retrospective study aims to document the clinical pattern of antibiotics use and its overuse and misuse rates in rural primary care institutions and to evaluate the association between antibiotics use and characteristics of physicians and their patients.
METHODS: Medical records from 16 primary care hospitals in rural areas of Guizhou province, China were obtained from the Health Information System in 2018. Classification of unnecessary use, incorrect spectrum of antibiotic, escalated use of extended spectrum and combined antibiotics use was based on the Guiding Principle of Clinical Use of Antibiotics (2015, China) and guidelines from the US Centers for Disease Control and Prevention. Generalized Estimating Equations were employed to determine predictive factors for inappropriate antibiotics use.
RESULTS: A total of 74,648 antibiotics prescriptions were retrieved. Uncomplicated respiratory infection was the most common disease accounting for 58.6% of all prescriptions. The main antibiotic group used was penicillins (51.5%) followed by cephalosporins and macrolides (14% each). Of 57,009 patient visits, only 8.7% of the antibiotic prescriptions were appropriate. Combined use, escalated use of extended spectrum antibiotics, incorrect spectrum and unnecessary antibiotics use was found in 7.8%, 1.9%, 4.3% and 77.3% of patient visits, respectively, of which 28.7% were given intravenously. Antibiotics misuse was significantly more likely among newly employed physicians with lower levels of professional education. Adult patients and those who had public insurance had a higher risk of being prescribed unnecessary antibiotics.
CONCLUSION: Overuse of antibiotics for uncomplicated respiratory infection and use of cephalosporins, macrolides and injection antibiotics in primary care are the major problems of clinical practice in rural areas of Guizhou.

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Year:  2019        PMID: 31242185      PMCID: PMC6594576          DOI: 10.1371/journal.pone.0214779

Source DB:  PubMed          Journal:  PLoS One        ISSN: 1932-6203            Impact factor:   3.240


Introduction

Antibiotics resistance is a growing global public health issue [1]. Between 2000 and 2010 global antibiotics consumption grew by more than 50% based on data from 71 countries, including China [2]. Excessive consumption of antibiotics mainly leads to the development of antibiotics resistance. China consumes the second largest amount of antibiotics in the world [3, 4] with a prescription rate twice that recommended by the World Health Organization (WHO) [5] and rural areas have higher rates than urban areas [6]. In this regard, the Chinese government has introduced a number of regulations in the last decade, but it has not played a significant role in rural areas [7]. The majority of people in southwest China live in rural areas where primary care physicians usually provide the health services [8]. Most physicians there have non-degree training yet are allowed to prescribe antibiotics in the national list due to personnel shortages. Previous studies reported a high irrational antibiotics prescription use among primary care physicians [7, 9]. In addition, studies performed in Italy and Germany exploring the patterns of antibiotic prescriptions among primary care physicians found that the rate of inappropriate antibiotic use was high [10-12]. Strengthening the knowledge and practice of rational use of antibiotics among primary care physicians is one way to reduce antibiotic resistance. Thus, we need to understand how antibiotics are unnecessarily used, for example prescribed with incorrect choices for particular diseases, escalated (for example prescribing more expensive and broad spectrum antibiotics when cheaper and more specific antibiotics can give the same result) and used intravenously. The aim of this study was to document the clinical patterns of antibiotics prescriptions in a rural primary care setting where physicians are mostly non-degree trained. The secondary objective was to determine the association between antibiotics use and various characteristics of patients and physicians.

Materials and methods

Ethical approval: This research was approved by the Institutional Review Board of Prince of Songkhla University, Thailand (REC: 60-285-18-5). Ethics committees approved the consent procedure. All participants provided their written informed consent to participate in this study.

Study setting

Out of 1,399 township public hospitals in Guizhou rural areas, 132 use the same health information system (HIS) developed by the Department of Public Health. Those that had more than three outpatient physicians were eligible for the study. Out of the 84 eligible hospitals, we randomly selected 31 to participate in the study.

Data retrieval process

Only data from outpatient units were retrieved. Demographic characteristics of the patients, and education and work experiences of the physicians, were obtained from the Personnel Management Department. All patients prescribed antibiotics during February to August, 2018 were included in the analysis. The primary diagnoses of all diseases except for tuberculosis (since the treatment options are fixed and standardized), were grouped into 10 diagnostic categories according to the international classification for diseases version 10 (ICD-10) code [13]. Antibiotics were classified, based on the 2018 National Catalogue of Clinical Application of Antibacterial Drugs, into seven groups: penicillins, cephalosporins, macrolides, quinolones, lincosamides, nitroimidazoles, and aminoglycosides [14]. We focused on systemic antimicrobials excluding topical antimicrobial prescriptions such as ophthalmic ointments and skin creams.

Categorization of appropriateness of antibiotic use

We used the National Health Commission of China for Guiding Principle of Clinical Use of Antibiotics introduced in 2015 (summarized in S1 File), and antibiotic use guidelines from the US Centers for Disease Control and Prevention (CDC) [15]. Appropriate antibiotic use in primary care settings was classified based on the diagnosis of probable bacterial infection. We categorised antibiotic use into appropriate use and inappropriate use. Inappropriate use was further categorised into four groups: 1) unnecessary use, e.g. prescribing antibiotics for viral infections, 2) incorrect spectrum of antibiotic, e.g. prescribing aminoglycoside for gram positive bacteria, 3) escalated use of extended spectrum antibiotics, e.g. prescribing cephalosporin instead of penicillin, and 4) combined use of antibiotics, defined as use of more than one antibiotic group per patient visit without any indications. In some cases, definitive bacterial culture penicillin (e.g. for acute pharyngitis/tonsillitis) is not available a presumptive narrow spectrum antibiotic, e.g. penicillin was considered as appropriate. Misuse of antibiotics was defined as unnecessary antibiotic use while overuse was defined as any other category of inappropriate antibiotic use.

Data analysis

The units of analysis were both antibiotic prescriptions and patient visits; one physician may prescribe one or more antibiotics to a patient on a given day, but a patient can only visit one doctor per day. Cross-tabulation between the groups of antibiotics and the disease categories by ICD-10 diagnosis code was used to determine the pattern and appropriateness of antibiotics use. Misuse of antibiotic prescriptions was aggregated by antibiotic group. Bivariate cross-tabulations were initially used to identify potential risk factors of inappropriate antibiotic use. In order to account for the correlation of antibiotic prescriptions by the same physician, Generalized Estimating Equations (GEE) were used to determine independent predictors of antibiotic misuse controlling for possible confounding effects by other variables. All p-values were two-sided. R version 3.3.1 was used for all data management and analysis for the database (S1 Table).

Results

A total of 96,509 antibiotic prescriptions among 57,009 patient visits were retrieved from the electronic database during the study period. The ten most common diagnoses among these patients accounted for over 77% of all prescriptions; therefore, we focused on only these ten diagnostic categories in the analysis. Table 1 shows a comparison of the number of antibiotics prescribed for various common diseases stratified by appropriateness of use. Diseases of the respiratory system accounted for about 70% of all antibiotic prescriptions followed by diseases of the digestive system (13.1%) and genitourinary system (5.6%). Inappropriate use of antibiotics was found in 91.8% of the 74,648 prescriptions. The highest rate of inappropriate use was seen for symptoms, signs and abnormal clinical and laboratory finding not elsewhere classified (100%), diseases of the eye and adnexa (99%), and diseases of the skin and subcutaneous tissue (97.4%). Escalated use of extended spectrum antibiotics was common for patients with acute appendicitis (40.8%) and pneumonia, organism unspecified (31.3%). Incorrect spectrum of antibiotic was used frequently among patients with cystitis (45.8%) and other disorders of the urinary system (44.1%) whereas unnecessary use was common to all diseases. The highest rate of appropriate use was found in diseases of pulp and periapical tissues (71.2%), acute pharyngitis (69.7%), and arthritis (67.6%).
Table 1

Distribution of antibiotic prescriptions stratified by clinical diagnosis and appropriateness of use.

DiagnosisTotalAppropriate use, n (%)Inappropriate use, n (%)
Escalated use of extended spectrumIncorrect spectrumUnnecessary use
1. Diseases of the respiratory system51,9874,248 (8.2)126 (0.2)1329 (2.6)46,284 (89.0)
    Upper respiratory tract infection
    Acute tonsillitis4,4232,193 (49.6)0 (0)859 (19.4)1,371 (31.0)
    Acute pharyngitis1,369954 (69.7)0 (0)0 (0)415 (30.3)
    Acute sinusitis33281 (24.4)11 (3.3)56 (16.9)184 (55.4)
    Others34,2800 (0)0 (0)0 (0)34,280 (100)
    Lower respiratory tract infection
    Bronchitis, not specified as acute or chronic1,725887 (51.4)0 (0)333 (19.3)505 (29.3)
    Pneumonia, organism unspecified367133 (36.2)115 (31.3)81 (22.1)38 (10.4)
    Others9,4910 (0)0 (0)0 (0)9,491 (100)
2. Diseases of the digestive system9,795987 (10.1)822 (8.4)1,469 (15.0)6,517 (66.5)
    Gingivitis and periodontal diseases1,776622 (35.0)138 (7.8)0 (0)1,016 (52.2)
    Diseases of pulp and periapical tissues11884 (71.2)0 (0)4 (3.4)30 (25.4)
    Gastritis and duodenitis4,4050 (0)323 (7.3)650 (14.8)3,432 (77.9)
    Cholecystitis511273 (53.4)89 (17.4)82 (16)67 (13.1)
    Acute appendicitis498 (16.3)20 (40.8)0 (0)21 (42.9)
    Other non-infective gastroenteritis and colitis1,7550 (0)252 (14.4)733 (41.8)770 (43.9)
    Others1,1810 (0)0 (0)0 (0)1,181 (100)
3. Diseases of the genitourinary system4,191365 (8.7)537 (32.5)768 (18.3)2,521 (60.2)
    Other female pelvic inflammatory disease13670 (0)273 (20)294 (21.5)800 (58.5)
    Other inflammation of vagina and vulva455284 (62.4)0 (0)0 (0)171 (37.6)
    Cystitis1660 (0)27 (16.3)76 (45.8)63 (38.0)
    Urethritis and urethral syndrome3830 (0)99 (25.8)163 (42.6)121 (31.6)
    Other disorders of urinary system53381 (15.2)138 (25.9)235 (44.1)79 (14.8)
    Others12870 (0)0 (0)0 (0)1,287 (100)
4. Diseases of the musculoskeletal system and connective tissue2,318669 (28.9)77 (3.3)22 (0.9)1,550 (66.9)
    Other arthritis989669 (67.6)77 (7.8)22 (2.2)221 (20.9)
    Others13290 (0)0 (0)0 (0)1,329 (100)
5. Injury, poisoning and certain other consequences of external causes93686 (9.2)11 (1.2)7 (0.7)832 (88.9)
    Other and unspecified injuries of abdomen, lower back and pelvis18086 (47.8)11 (6.1)7 (3.9)76 (42.2)
    Others7560 (0)0 (0)0 (0)756 (100)
6. Diseases of the eye and adnexa1,78618 (1.0)0 (0)0 (0)1,768 (99.0)
    Hordeolum and chalazion14118 (12.8)0 (0)0 (0)123 (87.2)
    Others16450 (0)0 (0)0 (0)1,645 (100)
7. Diseases of the skin and subcutaneous tissue96525 (2.6)14 (1.5)9 (0.9)917 (95.0)
    Cellulitis6525 (38.5)14 (21.5)9 (13.8)17 (26.2)
    Others9000 (0)0 (0)0 (0)900 (100)
8. Diseases of the circulatory system952103 (10.8)0 (0)0 (0)849 (89.2)
    Rheumatic fever without mention of heart involvement174103 (59.2)0 (0)0 (0)71 (40.8)
    Others7780 (0)0 (0)0 (0)778 (100)
9. Certain infectious and parasitic diseases62766 (10.5)30 (4.8)80 (12.8)451 (71.9)
    Other gastroenteritis and colitis of infectious and unspecified origin24666 (26.8)30 (12.2)80 (32.5)70 (28.5)
    Others3810 (0)0 (0)0 (0)381 (100)
10. Symptoms, signs and abnormal clinical and laboratory finding not elsewhere classified1,0910 (0)0 (0)0 (0)1,091 (100)
    Abdominal and pelvic pain + fever of unknown origin + cough + pain in throat and chest + headache1,0910 (0)0 (0)0 (0)1,091 (100)
Total prescriptions74,6486,567 (8.8)1,617 (2.2)3,684 (4.9)62,780 (84.1)
Table 2 summarizes appropriateness of antibiotic use by group. Over a half (51.5%) of the prescribed antibiotics were penicillins. However, 84.4% of penicillins unnecessarily prescribed. The percentage of cephalosporins and macrolides prescribed was about 14% each, of which about 84.7% were unnecessarily prescribed. Quinolones, which should be used mainly as second-line antibiotics, was found in around 6% of all prescriptions, of which 46.2% were incorrect spectrum of antibiotic. Lincosamides, nitroimidazoles, and aminoglycosides were not commonly seen, however almost all were prescribed inappropriately.
Table 2

Distribution of antibiotic prescriptions stratified by antibiotic group and appropriateness of use.

Antibiotic groupTotalAppropriate use, n(%)Inappropriate use, n (%)
Escalated use of extended spectrumIncorrect spectrumUnnecessary use
Penicillins38,462 (51.5)5,981 (15.6)0 (0)0 (0)32,481 (84.4)
Cephalosporins10,757 (14.4)0 (0)1,641 (15.3)0 (0)9,116 (84.7)
Macrolides10,574 (14.2)355 (3.4)0 (0)1,318 (12.5)8,901 (84.2)
Quinolones4,693 (6.3)0 (0)0 (0)2,168 (46.2)2,525 (53.8)
Lincosamides4,732 (6.3)0 (0)0 (0)0 (0)4,732 (100)
Nitroimidazoles3,687 (4.9)288 (7.8)0 (0)0 (0)3,399 (92.2)
Aminoglycosides1,743 (2.3)0 (0)0 (0)198 (11.4)1,545 (88.6)
Total74,6486,297 (8.4)1,641 (2.2)3,684 (4.9)63,026 (84.5)
Table 3 compares the distribution of appropriateness of antibiotics use by physicians’ and patients’ characteristics. In the second column, “combined use” refers to physicians prescribing more than one group of antibiotic for the same patient in the same visit. The percentage of appropriate antibiotics use was reduced from that shown in Table 1 because two or more antibiotics prescribed to the same patient on the same day was considered as one visit. The percentage of each prescription type was thus appropriate use (8.7%), combined use (7.8%), escalated use of extended spectrum (1.9%), incorrect spectrum (4.3%) and unnecessary use (77.3%).
Table 3

Factors associated with inappropriate use of antibiotics on bivariate analysis.

CharacteristicAppropriate useInappropriate use, n (%)Crude OR(95% CI)TotalN (%)
Frequency (%)Combined useEscalated use of extended spectrumIncorrect spectrumUnnecessary use
Total4,966 (8.7)4,463 (7.8)1,071 (1.9)2,436 (4.3)44,073 (77.3)57,009
Physician characteristics
    Sex
Female2376 (10.6)1,565 (7.0)482 (2.1)1184 (5.3)16,821 (75.0)Ref22,428 (39.3)
Male2590 (7.5)2,898 (8.4)589 (1.7)1252 (3.6)27,252 (78.8)1.46 (1.38, 1.55)34,581 (60.7)
    Age group (years)
25–311925 (8.8)1,779 (8.1)506 (2.3)779 (3.5)16,995 (77.3)Ref21,984 (38.6)
32–381345 (7.4)1,466 (8.1)353 (2)660 (3.6)14,266 (78.9)1.19 (1.11, 1.29)18,090 (31.7)
39–751696 (10.0)1,218 (7.2)212 (1.3)997 (5.9)12,812 (75.7)0.86 (0.8, 0.92)16,935 (29.7)
    Education
College2082 (9.9)1,676 (7.9)564 (2.7)716 (3.4)16,064 (76.1)Ref21,102 (37.0)
Junior college2278 (8.5)1,923 (7.2)356 (1.3)1405 (5.2)20,812 (77.7)1.18 1.11, 1.25)26,774 (47.0)
Technical secondary school606 (6.6)864 (9.5)151 (1.7)315 (3.4)7,197 (78.8)1.54 (1.40, 1.69)9,133 (16.0)
    Work duration (years)
≤51485 (9.5)1,373 (8.8)242 (1.5)488 (3.1)12,098 (77.1)Ref15,686 (27.5)
6–101624 (9.6)812 (4.8)533 (3.2)660 (3.9)13,285 (78.5)0.98 (0.91, 1.06)16,914 (30.0)
11–20924 (6.3)1,435 (9.7)194 (1.3)606 (4.1)11615 (78.6)1.57 (1.44, 1.71)14,774 (25.9)
21–30411 (6.7)547 (9.0)73 (1.2)518 (8.5)4548 (74.6)1.45 (1.29, 1.62)6,097 (10.7)
≥31522 (14.8)296 (8.4)29 (0.8)164 (4.6)2,527 (71.4)0.60 (0.54, 0.67)3,538 (6.2)
    Professional title
Resident physician4,001 (8.7)3,523 (7.7)845 (1.8)1757 (3.8)35,623 (77.9)Ref45,749 (80.2)
Attending physician830 (9.4)881 (9.9)218 (2.5)584 (6.6)6,349 (71.6)0.93 (0.86, 1.00)8,862 (15.5)
Associate chief physician135 (5.6)59 (2.5)8 (0.3)95 (4)2,101 (87.6)1.61 (1.35, 1.93)2,398 (4.3)
Patient characteristics
    Sex
Female2,604 (8.5)2,454 (8.0)703 (2.3)1395 (4.5)23,579 (76.7)Ref30,735 (53.9)
Male2,362 (9.0)2,009 (7.6)368 (1.4)1041 (4)20,494 (78.0)0.94 (0.88, 0.99)26,274 (46.1)
    Age group (years)
≤5947 (10.6)675 (7.5)41 (0.5)416 (4.6)6,881 (76.8)Ref8,960 (15.7)
5–171,234 (12.8)765 (7.9)88 (0.9)274 (2.8)7,271 (75.5)0.80 0.73, 0.88)9,632 (16.8)
18–491,472 (7.7)1,222 (6.4)501 (2.6)916 (4.8)14,962 (78.4)1.41 (1.30, 1.54)19,073 (33.5)
50–64706 (6.5)966 (8.9)263 (2.4)473 (4.4)8,404 (77.7)1.69 (1.53, 1.88)10,812 (19.0)
≥65607 (7.1)835 (9.8)178 (2.1)357 (4.2)6,555 (76.8)1.54 (1.39 1.72)8,532 (15.0)
Antibiotic route
Injection911 (5.6)1,796 (11.0)749 (4.6)393 (2.4)12,492 (76.4)Ref16,341 (28.7)
Oral4,055 (10.0)2,667 (6.6)322 (0.8)2043 (5)31,581 (77.7)0.53 (0.49, 0.57)40,668 (71.3)
Payment source
Out-of-pocket614 (10.2)487 (8.1)132 (2.2)404 (6.7)4,410 (72.9)Ref6,047 (10.6)
New rural cooperative- medical care system4,352 (8.5)3,976 (7.8)939 (1.8)2032 (4)39,663 (77.8)1.21 (1.11, 1.32)50,962 (89.4)

OR: Odds ratio, CI: Confidence interval, Ref: Reference group

OR: Odds ratio, CI: Confidence interval, Ref: Reference group The crude odds ratios indicate the strengths of the association between inappropriate use and physicians’ and patients’ characteristics. Male physicians were more likely to prescribe antibiotics inappropriately as were those aged 32–38 years (compared to those aged less than 32 years), those who had not completed a college degree, worked for 11–30 years (compared to those who had worked for less than 5 years), and were associate chief physicians (compared to resident physicians). Patients who were female, aged 18 years or more (compared to those aged ≤5 years), received antibiotics intravenously and received financial assistance from an insurance scheme were more likely to be prescribed antibiotics inappropriately. Table 4 shows factors associated with inappropriate antibiotic use on multivariate analysis. On the physician's side, being male, aged less than 32 years, having a lower level of education, and being an associate chief physician were associated with a higher likelihood of inappropriate antibiotic use. Increasing work duration did not equate to a higher odds of inappropriate antibiotic use. However, compared to newly employed physicians, those who had a work experience duration of more than 5 years were more likely to prescribe antibiotics inappropriately. Antibiotics prescribed intravenously were more likely to be inappropriate. On the patient's side, younger patients (age≤17 years) were more likely to get appropriate prescription. Finally, patients who received financial assistance from an insurance scheme were more likely to be prescribed antibiotics inappropriately.
Table 4

Factors predicting inappropriate use of antibiotics on multivariate analysis.

CharacteristicAdjusted OR (95% CI)P value
PhysiciansSex: ref = Female
    Male1.65 (1.54, 1.78)< 0.001
Age: ref = 25–31 years (years)
    32–380.58 (0.53, 0.64)< 0.001
    39–750.30 (0.27, 0.35)< 0.001
Education: ref = College
    Junior college1.30 (1.21, 1.39)< 0.001
    Technical secondary school1.60 (1.42, 1.80)< 0.001
Work duration: ref = ≤ 5 (years)
    6–101.36 (1.25, 1.48)< 0.001
    11–203.14 (2.78, 3.54)< 0.001
    21–303.80 (3.20, 4.53)< 0.001
    ≥ 311.54 (1.29, 1.83)< 0.001
Professional title: ref = Resident physician
    Attending physician0.97 (0.87, 1.08)0.60
    Associate chief physician1.99 (1.62, 2.43)< 0.001
PatientSex: ref = Female
    Male0.98 (0.92, 1.04)0.46
Age: ref. < 5 (years)
    5–170.76 (0.69, 0.83)< 0.001
    18–491.25 (1.14, 1.36)< 0.001
    50–641.36 (1.22, 1.50)< 0.001
    ≥ 651.20 (1.08, 1.34)< 0.001
Route: ref = Injection
    Oral0.49 (0.45, 0.53)< 0.001
Payment source: ref = Out-of-pocket
    New rural cooperative medical care system1.18 (1.08, 1.30)< 0.001

OR: Odds ratio, CI: Confidence interval

OR: Odds ratio, CI: Confidence interval

Discussion

This study showed five patterns of antibiotic use, namely: 1) appropriate use, 2) unnecessary use, 3) escalated use of extended spectrum antibiotics, 4) incorrect spectrum of antibiotics, and 5) combined antibiotic use. More than 90% of antibiotic prescriptions were inappropriately prescribed. Respiratory infection was the most common disease linked with antibiotic prescriptions. While penicillins were the most commonly prescribed antibiotic, cephalosporins and macrolides were more inappropriately prescribed, particularly due to escalation and incorrect spectrum of antibiotic. These antibiotics could have been de-escalated to penicillins. The background education of these primary care physicians was generally below college level. A physician's low level of education and senior position were significantly associated with inappropriate antibiotic prescription. Antibiotic misuse was also associated with injection route as well as adult patients and those who had insurance. In general, uncomplicated respiratory infections are mostly caused by viruses, which cannot be treated with antibiotics [15]. Unnecessary use of antibiotics to treat such infections has been reported in many countries such as Italy (67%), Norway (11%), USA (42%), Qatari (45%), Canada (84%) and China (71%) [10, 16–20]. In our study, unnecessary antibiotic use accounted for 77% of the prescriptions. Misuse and overuse of antibiotics could increase the duration of the disease and associated costs and increase resistance to infections as well as increase the risk of adverse drug reactions [21]. Therefore, it is important to identify antibiotic patterns as they vary by different factors such as the medical education system of a country. As much as 29% of antibiotics used in this study was administered by injection. Overuse of injections was also seen other countries such as Vietnam, India, and Korea [22-24]. This practice is rarely needed in primary care as most infections can be controlled with oral antibiotics [25]. Injection of drugs is complicated by serious adverse drug reaction and diseases complications such as local infections, bleeding, and nerve injury [24, 26]. There are many guidelines and punitive measures in China that guide physicians on how to use antibiotics, but there are no such guidelines as how physicians should talk to patients and families about whether antibiotics are needed or not, and discuss possible harms [21]. Most of the antibiotic prescriptions in this study were made by resident physicians with a below college level of education, and this was associated with antibiotic overuse and misuse. Based on this evidence, refresher courses on antibiotic prescribing for primary care physicians are necessary [7, 9]. The training should emphasize avoidance of incorrect and unnecessary use, narrow-spectrum antibiotics use, and when to prescribe injection antibiotics. Furthermore, there are no measures to teach patients how to use antibiotics and manage symptoms of non-bacterial infections. Patient’s attitude, education level and expectations play a key role in inappropriate antibiotic prescribing by physicians in outpatient settings. Patients who are misled by the efficacy of antibiotics were prescribed antibiotics more frequently than those who were not expecting them [27]. Patients need to be given more information concerning antibiotics use. Easy-to-understand health education materials can help empower patients and consequently change inappropriate antibiotic prescribing practices by physicians [27, 28]. Studies from Italy and the UK have shown that the Internet and social media can be an effective way for relevant government departments and medical institutions to disseminate the right principles of antibiotic use to patients [29, 30]. Our study has several limitations. Firstly, the results of our study cannot be generalized to hospitals with fewer outpatient physicians and to hospitals outside of our study setting. Secondly, the whole analysis of this study was based on data keyed in by the primary physicians. While the antibiotic information is very accurate, that on disease classification might be less so. Accurate diagnosis is a prerequisite of appropriate selection of antibiotic. Data on appropriateness of antibiotic choice in this study must therefore be interpreted with caution. Thirdly, the time frame of the survey is limited, diseases and medications in different seasons will vary, which is not covered in this study.

Conclusion

Overuse of antibiotics for uncomplicated respiratory infections, use of cephalosporins, macrolides and injection antibiotics in primary care are the major problems of clinical practice in the study areas.

Summary of National Health Commission of China for Guiding Principle of Clinical Use of Antibiotics introduced in 2015 related to this study.

(DOCX) Click here for additional data file.

Database of antibiotic prescriptions.

(XLSX) Click here for additional data file.
  24 in total

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2.  Internet and social media use for antibiotic-related information seeking: Findings from a survey among adult population in Italy.

Authors:  Rossella Zucco; Francesco Lavano; Rosa Anfosso; Aida Bianco; Claudia Pileggi; Maria Pavia
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3.  Antimicrobial prescribing patterns in a large tertiary hospital in Shanghai, China.

Authors:  Yuan-Yuan Wang; Ping Du; Fang Huang; Dong-Jie Li; Jun Gu; Fu-Ming Shen; Yuan-Ying Jiang
Journal:  Int J Antimicrob Agents       Date:  2016-10-14       Impact factor: 5.283

4.  Retrospective survey of the efficacy of mandatory implementation of the Essential Medicine Policy in the primary healthcare setting in China: failure to promote the rational use of antibiotics in clinics.

Authors:  Yonghong Xiao; Jin Wang; Ping Shen; Beiwen Zheng; Yingdong Zheng; Lanjuan Li
Journal:  Int J Antimicrob Agents       Date:  2016-07-28       Impact factor: 5.283

5.  Use and prescription of antibiotics in primary health care settings in China.

Authors:  Jin Wang; Pan Wang; Xinghe Wang; Yingdong Zheng; Yonghong Xiao
Journal:  JAMA Intern Med       Date:  2014-12       Impact factor: 21.873

Review 6.  Worldwide pattern of antibiotic prescription in endodontic infections.

Authors:  Juan José Segura-Egea; Jenifer Martín-González; María Del Carmen Jiménez-Sánchez; Isabel Crespo-Gallardo; Juan José Saúco-Márquez; Eugenio Velasco-Ortega
Journal:  Int Dent J       Date:  2017-04-17       Impact factor: 2.607

7.  Factors affecting the prescribing patterns of antibiotics and injections.

Authors:  Kyung-Hyun Choi; Sang-Min Park; Ju-Hyun Lee; Soonman Kwon
Journal:  J Korean Med Sci       Date:  2012-01-27       Impact factor: 2.153

8.  Antibiotic prescriptions for outpatient acute rhinosinusitis in Canada, 2007-2013.

Authors:  Prateek Sharma; Rita Finley; Scott Weese; Shiona Glass-Kaastra; Warren McIsaac
Journal:  PLoS One       Date:  2017-07-27       Impact factor: 3.240

9.  Consumption of antibiotics in Chinese public general tertiary hospitals (2011-2014): Trends, pattern changes and regional differences.

Authors:  Xiaoyuan Qu; Chang Yin; Xihong Sun; Shusheng Huang; Chaofan Li; Panpan Dong; Xiufang Lu; Zhuo Zhang; Aitian Yin
Journal:  PLoS One       Date:  2018-05-03       Impact factor: 3.240

10.  Online health information and public knowledge, attitudes, and behaviours regarding antibiotics in the UK: Multiple regression analysis of Wellcome Monitor and Eurobarometer Data.

Authors:  Alistair Anderson
Journal:  PLoS One       Date:  2018-10-24       Impact factor: 3.240

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  14 in total

Review 1.  Gain and loss of antibiotic resistant genes in multidrug resistant bacteria: One Health perspective.

Authors:  Misung Kim; Jaeeun Park; Mingyeong Kang; Jihye Yang; Woojun Park
Journal:  J Microbiol       Date:  2021-04-20       Impact factor: 3.422

2.  Two Important Issues in Subacute Thyroiditis Management: Delayed Diagnosis and Inappropriate Use of Antibiotics.

Authors:  Hayri Bostan; Muhammed Erkam Sencar; Murat Calapkulu; Sema Hepsen; Hakan Duger; Ilknur Ozturk Unsal; Mustafa Ozbek; Erman Cakal
Journal:  Eur Thyroid J       Date:  2021-03-18

3.  Discovering interrelated natural mutations of efflux pump KmrA from Klebsiella pneumoniae that confer increased multidrug resistance.

Authors:  Ying Li; Xizhen Ge
Journal:  Protein Sci       Date:  2022-06       Impact factor: 6.993

4.  Impacts of Antibiotic Residues in the Environment on Bacterial Resistance and Human Health in Eastern China: An Interdisciplinary Mixed-Methods Study Protocol.

Authors:  Shenghan Cai; Na Wang; Like Xu; Fei Yan; Qingwu Jiang; Xinping Zhao; Wei Wang; Hexing Wang; Lufang Jiang; Wenjuan Cong; Samuel K Sheppard; Jason Weeks; Barbara Kasprzyk-Hordern; Chaowei Fu; Helen Lambert
Journal:  Int J Environ Res Public Health       Date:  2022-07-02       Impact factor: 4.614

5.  Effect of unifaceted and multifaceted interventions on antibiotic prescription control for respiratory diseases: A systematic review of randomized controlled trials.

Authors:  Yue Chang; Zhezhe Cui; Xun He; Xunrong Zhou; Hanni Zhou; Xingying Fan; Wenju Wang; Guanghong Yang
Journal:  Medicine (Baltimore)       Date:  2022-10-14       Impact factor: 1.817

6.  Clinical diagnosis and treatment of common respiratory tract infections in relation to microbiological profiles in rural health facilities in China: implications for antibiotic stewardship.

Authors:  Xingrong Shen; Jilu Shen; Yaping Pan; Jing Cheng; Jing Chai; Karen Bowker; Alasdair MacGowan; Isabel Oliver; Helen Lambert; Debing Wang
Journal:  BMC Fam Pract       Date:  2021-05-06       Impact factor: 2.497

7.  Impact of multicenter unified enhanced environmental cleaning and disinfection measures on nosocomial infections among patients in intensive care units.

Authors:  Jing Huang; Can Cui; Shuli Zhou; Ming Chen; Hao Wu; Ronghua Jin; Xinyue Chen
Journal:  J Int Med Res       Date:  2020-08       Impact factor: 1.671

8.  The contribution of Pseudomonas aeruginosa infection to clinical outcomes in bronchiectasis: a prospective cohort study.

Authors:  Rongchun Wang; Shuizi Ding; Cheng Lei; Danhui Yang; Hong Luo
Journal:  Ann Med       Date:  2021-12       Impact factor: 4.709

9.  Cationic π-Conjugated Polyelectrolyte Shows Antimicrobial Activity by Causing Lipid Loss and Lowering Elastic Modulus of Bacteria.

Authors:  Ehsan Zamani; Tyler J Johnson; Shyambo Chatterjee; Cheryl Immethun; Anandakumar Sarella; Rajib Saha; Shudipto Konika Dishari
Journal:  ACS Appl Mater Interfaces       Date:  2020-10-22       Impact factor: 9.229

Review 10.  Emerging macrolide resistance in Bordetella pertussis in mainland China: Findings and warning from the global pertussis initiative.

Authors:  Ye Feng; Cheng-Hsun Chiu; Ulrich Heininger; Daniela Flavia Hozbor; Tina Quanbee Tan; Carl-Heinz Wirsing von König
Journal:  Lancet Reg Health West Pac       Date:  2021-02-05
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