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Canadian Journal of Public Health = Revue Canadienne de Santé Publique logoLink to Canadian Journal of Public Health = Revue Canadienne de Santé Publique
. 2020 Feb 27;111(4):523–530. doi: 10.17269/s41997-020-00298-2

Increasing paediatric prescribing rates in British Columbian children: cause for concern?

Ariana Saatchi 1, Fawziah Marra 1,✉
PMCID: PMC7438437  PMID: 32109315

Abstract

Objectives

Antibiotic prescribing in paediatric care is highly prevalent, and quite often, children are prescribed for conditions, like upper respiratory tract infections, which are self-limiting and viral in aetiology. The purpose of this study was to identify potential new targets for provincial antimicrobial stewardship efforts.

Methods

Antibiotic prescription data for children were extracted from a provincial prescription database, linked to physician billing data in order to obtain diagnostic information, and then combined with demographic data in order to obtain patient age, sex and geographic location. Prescription rates were calculated, and trends were examined by major anatomical therapeutic chemical (ATC) classification.

Results

Our cohort included an average of 271,134 children per year and 1,767,652 antibiotic prescriptions. Antibiotic utilization increased 4.5% (from 453 to 474 prescriptions per 1000 population). The greatest increases in prescribing were seen in children aged 0–2 years. Increased indication-specific rates of prescribing were observed in children aged 0–2 years, across every category. Although antibiotic use for upper respiratory tract infections decreased, prescribing rates remain as high as 5 times more than other indications.

Conclusion

Past studies have widely illustrated decreasing or static rates of prescribing in British Columbia. However, these results signal a potential problem in the sphere of paediatric antibiotic prescribing, wherein rates have been increasing since 2013. Despite the success of provincial efforts in reducing the use of broad-spectrum penicillins, marked surges in the use of classes like tetracyclines, quinolones and other antibacterials identify a new potential target for provincial stewardship.

Electronic supplementary material

The online version of this article (10.17269/s41997-020-00298-2) contains supplementary material, which is available to authorized users.

Keywords: Antibiotics, Paediatrics, Antimicrobial stewardship, Resistance

Introduction

Since the introduction of penicillin, antibiotics have played a major role in reducing infectious diseases morbidity and mortality, especially in children. To this day, antibiotics are one of the most commonly prescribed medications in the paediatric population (Ferris et al. 1998; Clavenna and Bonati 2009; Sturkenboom et al. 2008). However, the overuse of antibiotics has caused substantial bacterial resistance, resulting in a global public health crisis (Goossens et al. 2005; Chung et al. 2007).

Many studies have evaluated the use of antibiotics for specific indication and have shown that antibiotics are most commonly prescribed for respiratory tract infections, otitis media and urinary tract infections (McCaig et al. 2003; van den Broek d’Obrenan et al. 2014; Holstiege and Garbe 2013; de Bont et al. 2013). Further analyses of these data have shown that antibiotics are commonly used for upper respiratory tract infections, sore throat, acute cough, sinusitis, common cold and acute bronchitis—all of which are predominantly caused by viruses and do not benefit from antibiotic therapy (Gonzales et al. 2001; Grijalva et al. 2009). As an indicator for the quality of primary care physician prescribing, studies can measure the total prescription use of antibiotics for non-bacterial indications.

In the last decade, many guidelines have been introduced by various agencies in North America to help primary care physicians with the prescribing of antibiotics in children, including the judicious treatment of upper respiratory tract infections (Centers for Disease Control and Prevention (CDC) n.d.), streptococcal pharyngitis (Shulman et al. 2012), pneumonia (Bradley et al. 2011), rhinosinusitis (Chow et al. 2012), skin and soft tissue infections (Stevens et al. 2014), otitis media (BC Ministry of Health 2010), asthma (BC Ministry of Health 2015) and urinary tract infections (BC Ministry of Health 2009). In 2005, a provincial education program was launched for both healthcare professionals and the public, to disseminate information regarding the use of antibiotics through social media campaigns, educational programs and the provision of guidelines for physicians (No author n.d.). This population-based study was conducted to evaluate our antibiotic use in British Columbia, Canada. Given that it has been over a decade since the introduction of both the program and prescribing guidelines, the objectives of this study were to evaluate overall antimicrobial usage within primary care for children, identify types of antibiotics being used and determine for which indications prescribing was still commonly occurring.

Materials and methods

The Ministry of Health in British Columbia houses several healthcare-related databases, which have comprehensive information on the majority of the population that live in BC (population of 4.6 million). The antibiotic information was extracted from BC PharmaNet, a centralized data system that links all pharmacies with every prescription dispensed through community pharmacies. All antimicrobials are recorded in this system except those used for treatment of sexually transmitted infections and HIV. Data were extracted for all children in BC, which was defined as those less than 18 years of age.

We also used the Medical Service Plan (MSP) billing system that records all reimbursement claims submitted by physicians for services provided to British Columbian residents, including diagnostic codes. Antibiotic prescriptions from January 1, 2013 to December 31, 2016 were extracted from PharmaNet and then matched to the MSP billing system using anonymized patient identifiers. A prescription was assigned a diagnostic code using an algorithm that matched the date on which the medication was dispensed, to a practitioner service date within 5 days prior, via an MSP billing claim. If a practitioner service date was associated with more than one diagnostic code, or multiple service dates fell within a single 5-day period of a prescription dispensing date, then a three-tiered hierarchy was applied to link only the most relevant diagnostic code to the prescription (Fleming-Dutra et al. 2016). If multiple codes were present within the same tier, the primary physician code was selected for analysis. Multiple prescriptions per subject were permitted in our analyses. All cells with n < 5 were excluded from subsequent analyses to preserve subject anonymity.

Antibiotics were classified based on the Anatomical Therapeutic Chemical (ATC) classification system developed by the World Health Organization (WHO) (World Health Organization 1996). Consumption rates were calculated as prescriptions per 1000 population per year, using age- and gender-specific denominator estimates for the population from statistics BC (Province of British Columbia n.d.). The MSP diagnostic codes were based on the ninth revision of the International Classification of Diseases developed by WHO, commonly referred to as ICD-9. Several indications were grouped within the classifications of upper respiratory tract infections (URTI), acute otitis media (AOM), urinary tract infections (UTI), lower respiratory tract infections (LRTI) and skin/soft tissue infections (SSTI) (Supplementary material, eTable 1).

We analyzed the data first with respect to overall rate of antibiotic use [J01], then according to use of the seven major classes and clinically relevant antibiotics. For each major class, we also evaluated changes in use by gender, age group (0–2, 3–9, 10–18) and indication. The 5 major health authorities of British Columbia defined the geographic regions within the province, and with respect to the age categories delineated above, these were used in our previous provincial analyses and are in line with provincial reporting on antimicrobial prescribing for BC (No author n.d.; Fleming-Dutra et al. 2016). Annual trends of antibiotic consumption were explored using generalized linear regression models (Poisson, α = 0.05). These analyses were stratified by age and gender; however, standardized rates were not calculated. All analyses were performed using SAS 9.4 and R version 3.3.1.

Results

Overall antibiotic utilization

There were 1,084,536 children in our antibiotic prescription claims database. There were slightly more females than males in the cohort (51%) and the majority of children were in the 3–9-year age group (Table 1). Over 1,767,652 million prescriptions for oral antibiotics were dispensed to children during the 4-year study period, with over 50% being treatment for RTIs and AOM.

Table 1.

Study population characteristics

2013 2014 2015 2016 Overall
N (%) N (%) N (%) N (%) N (%)
Cohort total 261,698 262,027 274,093 286,718 1,084,536
Age group
  0–2 38,004 (14) 51,373 (8) 63,704 (23) 79,331 (27) 232,412 (21)
  3–9 109,289 (41) 94,996 (36) 89,310 (32) 81,877 (28) 375,472 (34)
  10–18 114,405 (43) 115,658 (44) 121,079 (44) 125,510 (43) 476,652 (43)
Gender
  Females 131,116 (50) 132,807 (50) 140,694 (51) 149,028 (52) 553,645 (51)
  Males 130,582 (49) 129,220 (49) 133,398 (48) 137,690 (48) 530,890 (49)
Health authority
  Fraser 109,411 (41) 109,930 (42) 116,077 (42) 123,464 (43) 458,882 (42)
  Vancouver Coastal 47,946 (18) 49,208 (18) 52,362 (19) 55,291 (19) 204,807 (18)
  Vancouver Island 37,663 (14) 38,339 (14) 40,409 (14) 41,564 (14) 157,975 (14)
  Interior 37,555 (14) 36,816 (14) 37,409 (13) 39,336 (13) 151,116 (13)
  Northern 20,480 (7) 21,171 (8) 23,504 (9) 24,208 (8) 89,363 (8)
Total antibiotic prescriptions 434,870 425,675 444,993 462,114 1,767,652
Infectious diagnosis
  Upper respiratory tract 89,807 (20) 128,843 (29) 110,730 (40) 81,011 (28) 410,391 (37)
  Acute otitis media 51,029 (11) 72,308 (17) 61,911 (13) 43,149 (9) 177,368 (16)
  Urinary tract 31,817 (7) 59,103 (14) 52,462 (11) 43,646 (9) 155,211 (14)
  Skin/soft tissue 36,177 (8) 58,611 (14) 44,055 (9) 34,332 (7) 136,998 (12)
  Lower respiratory tract 17,476 (4) 24,419 (6) 19,449 (4) 15,383 (3) 59,251 (5)
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Overall, antibiotic utilization increased 4.6% from 453 to 474 prescriptions per 1000 children per year between 2013 and 2016 (p < 0.05). Sex was not a significant factor across antibiotic prescribing. The age-specific breakdown is shown in Fig. 1 and the highest rate of use for all years was observed in the youngest age group of 0–2 years of age, which increased from 516 to 947 prescriptions per 1000 children per year between 2013 and 2016 (p < 0.05). The age group of 10–18 years also experienced a statistically significant 14% increase over time, while prescribing for the middle-age group decreased by 35% (p < 0.05).

Fig. 1.

Fig. 1

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Age-stratified antibiotic utilization in children within British Columbia, 2013 to 2016

Class- and drug-specific antibiotic utilization

An evaluation of antibiotic classes shows that between 2013 and 2016, usage increased for each class overall. Figure 2 shows the details for consumption, by class, between 2013 and 2016. The use of all antibiotic classes increased in our study population of children 18 years of age, and younger, with the class of other antibacterials (J01X) having the greatest increase (109%), followed by quinolones (J01M), which doubled in use (Supplementary material, eTable 2). Nitrofurantoin (104%) drove the increase in the J01X class, while the lesser-utilized metronidazole also saw a significant increase of 92% over time (Supplementary material, eFig. 1).

Fig. 2.

Fig. 2

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Use of various antibiotics across major antibiotic classes in British Columbian children, 2013 to 2016

Penicillin (J01C) use increased 23.5% over the study period and was consistently dispensed at rates far and above all other classes (Fig. 2). Usage across most individual penicillin antibiotics was steady; however, the increase can be attributed to elevated rates of prescribing penicillin V oral, which increased 22% over the study period (Supplementary material, eFig. 2). By 2016, overall penicillin use increased from 841 to 1040 prescriptions per 1000 children per year with children between 0 and 2 years of age experiencing the greatest increase (Supplementary material, eTable 2).

The class of macrolides, lincosamides and streptogramins increased 2% over the study period. Although the overall prescribing rate changed only marginally, the landscape of drugs within the class shifted. Erythromycin and clarithromycin significantly decreased in use by 14% and 34%, respectively, while azithromycin and clindamycin saw parallel, increasing rates of prescribing at 14% and 38%, over the study period (Supplementary material, eFig. 3).

All remaining classes of antibiotics experienced slight increases over time, with the exception of tetracyclines (J01A), which increased 30%. By 2016, 55 tetracycline prescriptions were dispensed per 1000 children, in comparison with the 42 dispensed in 2013. The remaining major classes were less variable over time, with lower prescribing rates, as trimethoprim/sulfamethoxazole and cephalosporins increased 12% and 6%, respectively throughout the study period (Fig. 2).

When evaluating the class- and drug-specific data according to the various age groups, we see similar usage patterns as the overall group (Supplementary material, eTable 2). In 2016, the class of beta-lactams penicillins has the highest use, followed by macrolides and cephalosporins. There is much less use of trimethoprim/sulfamethoxazole across all age groups and minimal use of tetracyclines and fluoroquinolones, although as age increases, their usage does as well (Supplementary material, eTable 2). Nitrofurantoin was primarily used for older children, aged 10–18 years. Between 2013 and 2016, the greatest increase in antibiotic use occurred in children 0–2 years of age, with the class of beta-lactams, penicillins increasing by 95% (647 prescriptions per 1000 children), macrolides by 62% (149 prescriptions per 1000 children), cephalosporins by 53% (98 prescriptions per 1000 children) and trimethoprim/sulfamethoxazole by 95% (41 prescriptions per 1000 children) (Supplementary material, eTable 2).

The decrease in prescribing for children 3–9 years of age was driven by lower rates of prescribing in the classes of penicillin, cephalosporin, trimethoprim/sulfamethoxazole and macrolides (Supplementary material eTable 2). Overall, prescribing for this age category decreased 35.5% during the study period. Slight variations in prescribing were observed when evaluating the trends according to the five provincial, geographic areas or health authorities. Percentage change in prescription rates was lowest in the more remote geographic areas (i.e., Northern Health Authority and Vancouver Island) in comparison with more populated, urban regions.

Diagnosis-specific antibiotic use

Throughout the study period, URTI was the most common category of diagnoses linked to antibiotic prescriptions (ranging from 297 to 43 prescriptions per 1000 population per year). Usage within this category was driven by prescriptions for acute RTI unspecified (2016: 37.3 prescriptions per 1000 population per year) and acute bronchitis (2016: 20.2 prescriptions per 1000 population per year) (Supplementary material, eTable 3).

The second most common indication for prescribing antibiotics was AOM (2016: 44.2 prescriptions per 1000 population per year) followed by SSTI (35.2 prescriptions per 1000 population per year). Rate of antibiotic use for UTI and LRTI was similar with 16.3 and 15.8 prescriptions per 1000 population per year, respectively, in 2016. Between 2013 and 2016, the use of antibiotics across all categories was either stagnant, or decreasing steadily for all indications except influenza, which increased by 14.5%, and urinary tract infections, wherein prescribing increased between 10% and 45% per indication, by 2016 (Fig. 3).

Fig. 3.

Fig. 3

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Indications for use of antibiotics according to major diagnostic criteria, 2013 to 2016

When evaluating antibiotic usage by age, URTI and AOM are the two most common indications for prescribing antibiotics in all age groups except for the oldest group of children aged 10–18 years, wherein prescribing for urinary tract infections was more common than otitis media. UTI was the only indication category wherein females were more likely to receive a prescription; all other categories had no significant difference between the sexes. For the youngest age strata, there was a significant increase in the use of antibiotics for AOM and URTI over time. However, in 2014, there was a distinct spike in prescribing across all ages and indications. Overall, we identified a positive association between young age and antibiotic prescribing; these age-stratified trends are further delineated in eTable 4 of the online supplement.

Discussion

During our 4-year study, almost 2 million prescriptions for antibiotics were dispensed to children under the age of 18. Over half of all antibiotics prescribed were for respiratory tract infections and acute otitis media. From 2013 to 2016, prescribing increased by roughly 4% across all age strata and was more pronounced in the youngest group of 0 to 2 years of age (84%). By 2016, children aged 0–2 years were prescribed at rates 2.3 and 2.6 times higher, respectively, than those between the ages of 10–18 and 3–9 years. As our database included just over one million children, the number of prescriptions suggests that some individuals received multiple antibiotics, either through repeat clinician visits or multiple antibiotics per visit. Despite an overall decreasing trend, we still found that the majority of the antibiotics were prescribed for URTI which is self-limiting, with viral aetiology and does not require antibiotic use. Prescribing for URTI was driven by acute bronchitis and acute RTI unspecified. These two indications were common for all age groups except the oldest cohort aged 10–18 years, wherein UTIs were a more common indication.

The use of metronidazole highlights the importance of ongoing surveillance efforts as this medication increased in use by 92% over the study period, despite not being a recommended first-line agent, or efficacious, for many of the indications included in our analyses. Most of these prescriptions were attributed to broad diagnostic profiles including “other symptoms involving abdomen and pelvis” and “symptoms involving digestive system”, with a significant proportion tied to appendicitis. This example emphasizes the importance of examining the quality of prescriptions issued, in tandem with indication.

Our findings are comparable with a United Kingdom study that showed a 4% increase in the prescribing of antibiotics by general practitioners, between 2010 and 2013 (Public Health England 2015). Williams et al. analyzed data originally collected in the DUTY study: a longitudinal, prospective cohort UK study (Downing et al. 2012) and concluded that, for children aged below 5 years, paediatric prescribing was suboptimal in UK primary care (Williams et al. 2018). Moreover, the proportion of children receiving the recommended first-line agent (65.1%) was below the national standard of 80%, as put forth by the ESAC-Net. Specific indications (i.e., tonsillitis) were noted to receive prescriptions at rates exceeding optimal levels, while more general diagnoses (i.e., URTIs) were within recommended prescribing limits. Although antibiotic use for upper respiratory tract infections decreased by 11% over this study period, these diagnoses continue to be prescribed for at rates 2–5 times higher than other conditions. A key disparity between this study and the conclusions put forth by Williams et al. is tied to the nature of the data reviewed. The provincial administrative health data utilized by this study are not collected for research purposes whereas Williams et al. analyzed prescribing in an unblinded research environment.

A recent study conducted by Zetts et al. found that children below the age of 2 years were prescribed for at elevated rates when compared with other age categories (Zetts et al. 2018). In their analysis of paediatric prescribing, defined as those individuals below 19 years of age, the study authors determined 29% of the total prescriptions to be unnecessary. In our classification of URTI, all included indications are not currently recommended antibiotics by current Canadian guidelines. As the most prescribed for category of indications, this inappropriate use of medications is a cause for concern. A study by Hersh et al., conducted in the United States among paediatric ambulatory care prescribing, found that respiratory conditions accounted for more than 70% of visits in which antibiotics were prescribed (Hersh et al. 2011). Of the visits where antibiotics were prescribed, 23% were for respiratory conditions for which antibiotics are not clearly indicated, accounting for more than 10 million visits annually.

Throughout our study period, penicillins were the most prescribed in comparison with all other major classes. In their study, De Bie et al. also identify that penicillins, specifically amoxicillin, are dispensed at the highest rates to European children (Bie et al. 2016). Furthermore, a narrow spectrum of antibacterials was identified to comprise over 90% of all antibiotics dispensed. These most common antibiotics were comparable with our own findings regarding prescription prevalence, with amoxicillin dispensed at the highest rates, followed by the second-generation macrolides and then cephalosporins.

The similarities identified in paediatric prescribing trends across various geographic regions, and nations, delineate important targets for antibiotic stewardship. As the program initiated across British Columbia in 2005 emphasized a strong focus on upper respiratory tract infections, avoiding unnecessary prescribing, and a return to first-line antibiotics, the presence of similar international trends affirm the ongoing issue of rational prescribing. In their 2013 report, Fleming-Dutra et al. found that in the USA, family practitioners are almost twice as likely to prescribe to young children (Fleming-Dutra et al. 2018). As children are high risk and a vulnerable group, elevated prescribing of antibiotics within this population has been documented to be indicative of broader inappropriate prescribing patterns. In comparison with paediatricians, family practitioners, nurse practitioners and physician assistants were all more likely to prescribe to children (Fleming-Dutra et al. 2018). The elevated use of antibiotics for URTI and AOM in British Columbian children indicates that further action is necessary to promote the judicious use of antibiotics.

On a national scale, antimicrobial stewardship has been an increasing concern throughout recent decades. In 2014, the Canadian Paediatric Society described effective stewardship as an interplay of art, science and common sense while, that same year, Choosing Wisely Canada™ was launched to advocate for increased stewardship and to disseminate prescribing/diagnostic toolkits in order to facilitate change (Le Saux 2014; Levine 2017). As 92% of antibiotics are used in the community, increased stewardship within primary care is paramount (Public Health Agency of Canada 2017). This study adds to the current scientific literature regarding antibiotic use, in order to establish more targeted interventions.

Our study has limitations inherent to all retrospective studies using administrative data. In order to obtain information regarding the type of antibiotics used for the various diagnoses, we linked two datasets together—the PharmaNet database containing dispensing information and the Physician billing database, which held diagnostic codes. As pharmacists do not currently have prescribing authority in British Columbia, unlinked records (14%) can be attributed to other prescribing professions such as dentists or nurse practitioners. These records were subsequently excluded from our analyses and thus, we could have underestimated prevalence rates. Similarly, as the nature of the datasets precludes nested analyses (i.e., prescriptions per child, per family unit, per clinic and so on), our standard error may have been biased as a result. Furthermore, as only dispensing data are accessible, levels of compliance to prescribed antibiotics are unknown.

Future directions for this research will build on the baseline presented and incorporate comorbidity, allergy, physician/patient characteristics and lab data in order to elucidate a more in-depth scope of prescribing in British Columbia. As the urgency surrounding antimicrobial resistance and the preservation of antibiotic efficacy grows, this study offers an integral first review of paediatric antibiotic utilization in British Columbia.

Conclusions

Antibiotic stewardship has garnered a positive change with respect to paediatric prescribing practices in British Columbian children, and past studies have illustrated decreasing or static rates of antibiotic prescribing in British Columbia. However, we have identified a 4.5% increase in paediatric antibiotic prescribing since 2013. Although it appears that provincial efforts have been successful in reducing the use of broad-spectrum penicillins, our study suggests that a new message is required—to decrease the use of azithromycin and clarithromycin as first-line agents and preserve their use for exceptional circumstances wherein penicillins are not appropriate. Furthermore, this study found a decrease in prescribing over time across all indications although antibiotic use continues to be a concern for upper respiratory tract infections in paediatric care. These diagnoses generally do not require antibiotics, and inappropriate prescribing remains a major factor underlying antimicrobial resistance.

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Conflict of interest

The authors declare that they have no conflict of interest.

Footnotes

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