An analysis of antibiotic prescribing practices for enteric bacterial infections within FoodNet Canada sentinel sites

Dougherty, Brendan; Finley, Rita; Marshall, Barbara; Dumoulin, Danielle; Pavletic, Amy; Dow, Joanne; Hluchy, Tara; Asplin, Rod; Stone, Jason

doi:10.1093/jac/dkz525

Abstract

Objectives

Understanding the current state of antibiotic treatment guidelines and prescribing practices for bacterial enteric infections is critical to inform antibiotic stewardship initiatives. This study aims to add to the current understanding through three objectives: (i) to identify and summarize published treatment guidelines for bacterial enteric infections; (ii) to describe observed antibiotic prescribing practices for bacterial enteric infections across three sentinel sites in Canada; and (iii) to assess concordance between observed antibiotic prescribing and treatment guidelines.

Methods

An environmental scan of treatment guidelines for bacterial enteric infections was conducted and recommendations were collated. A descriptive analysis of cases of bacterial enteric illnesses captured in FoodNet Canada’s sentinel site surveillance system between 2010 and 2018 was performed. Antibiotic-use data were self-reported by cases via an enhanced questionnaire.

Results

Ten treatment guidelines were identified in the environmental scan. There was substantial variation between guidelines for both when to prescribe antibiotics and which antibiotics were recommended. Of the 5877 cases of laboratory-confirmed bacterial enteric illness in the three sites, 49% of cases reported having received an antibiotic prescription. Of particular significance was the finding that 21% of verotoxigenic Escherichia coli cases received a prescription. Of the 17 antibiotics recommended in the guidelines, 14 were used in practice. In addition to these, 18 other antibiotics not included in any of the guidelines reviewed were also prescribed.

Conclusions

Our study suggests that a substantial proportion of enteric bacterial infections in Canada are prescribed antibiotics. These findings highlight the need to standardize treatment guidelines for enteric illnesses and could be used to inform future stewardship programme development.

Introduction

Inappropriate antibiotic treatment can have significant adverse health impacts for cases of bacterial enteric infections, such as increasing the risk of haemolytic uraemic syndrome in cases of verotoxigenic Escherichia coli (VTEC), prolonging faecal shedding in cases of non-typhoidal Salmonella and developing antibiotic-associated diarrhoea.¹^,² Excessive use of antibiotics has also been identified as a leading cause for the development and emergence of antibiotic-resistant bacteria.³ It is generally acknowledged that to mitigate the harms associated with inappropriate antibiotic use, antibiotic stewardship interventions must be implemented to measure and improve the appropriate use of antibiotics.⁴ In order to inform the development of effective stewardship interventions, it is imperative that the present state of antibiotic prescribing behaviour be understood.

Bacterial enteric infections are a significant burden of illness in Canada, resulting in approximately 18.28 cases per 1000 people of domestically acquired infections every year.⁵ The current status of antibiotic prescribing practices is poorly understood in Canada. A cross-sectional study conducted in Québec between 2007 and 2008 found that 10% of cases with acute gastrointestinal illness received an antibiotic prescription.⁶ The Public Health Agency of Canada’s Human Antimicrobial Use Report, using data from the Canadian Disease and Therapeutic Index, reported that 5.27% of diagnoses of ‘disease of the gastrointestinal system’ in 2014 had an antimicrobial recommended.⁷ Unfortunately, these data capture enteric illnesses caused by bacteria, viruses and parasites, and lack specificity on the pathogen causing disease, preventing a detailed understanding of prescribing patterns.

To assist healthcare practitioners in making prescribing decisions that are aligned with the best evidence, clinical guidelines have been developed by various organizations. These guidelines have been shown to influence antibiotic prescribing practices as they provide recommendations on circumstances for which antibiotic treatment is suggested as well as which specific antibiotics would be optimal.⁸ It is therefore essential to understand what the clinical guidelines used by Canadian healthcare practitioners recommend for treating bacterial enteric infections, as it provides context for observed prescribing practices.

In our three-part study, we aimed to address the gaps in knowledge surrounding antibiotic use in bacterial enteric illnesses. Part one: an environmental scan was conducted of treatment guidelines used by Canadian healthcare practitioners for bacterial enteric illnesses. Part two: data from the Public Health Agency of Canada’s FoodNet Canada surveillance system were analysed to describe the current state of antibiotic prescribing practices for laboratory-confirmed cases of bacterial enteric illness. Part three: the types of antibiotics recommended in treatment guidelines were compared and contrasted with those observed in the FoodNet Canada cases.

Methods

Environmental scan of practice guidelines

Practice guidelines for treating enteric illnesses were identified using the following search strategies: (i) MEDLINE and PubMed (search conducted in May 2016) were used to search for guidelines utilizing a combination of the MeSH term ‘diarrhea’ (exploded) and publication types ‘practice guideline’ or ‘guideline’; (ii) the National Guideline Clearinghouse (closed in 2018 from loss of funding) and Guideline International Network were searched using the terms ‘diarrhea’ and ‘gastroenteritis’; (iii) personal communications with practising healthcare practitioners and infectious disease specialists in Canada were used to identify guidelines that are commonly used in private practice; and (iv) additional guidelines were identified by manually searching the reference lists of other guidelines.

Guidelines were included in the environmental scan if they were published in English between the years 1990 and 2016 and provided evidence-informed therapeutic recommendations for the treatment of infectious intestinal diseases. This time frame was selected as it was felt by the authors to encapsulate the period when the majority of guidelines used by practising physicians would have been published, with guidelines published prior to 1990 being considerably out of date and those published after 2016 being unlikely to have had rapid uptake. If there were two guidelines published on behalf of the same organization, the most recent version was included.

Once guidelines were identified, the following descriptive characteristics were retrieved: the name of the authors/editors/organizations publishing the guideline; year of guideline publication; and the type of patient the guideline was targeted towards (e.g. adult or paediatric). Following this, recommendations for antibiotic treatment were extracted and collated at both the broad infectious diarrhoea level (empirical treatment/traveller’s diarrhoea) and the pathogen-specific level for five bacterial pathogens: Campylobacter spp., Salmonella spp., VTEC, Shigella spp. and Yersinia enterocolitica. Specifically, the data that were extracted included: when antibiotic use was recommended; which specific antibiotics were recommended; and any noted stipulations for these recommendations. To examine trends in when antibiotic use was recommended for various pathogens and guidelines, the recommendations were categorized into one of five categories: antibiotic use is not recommended; antibiotic use is not recommended unless…; antibiotic use is recommended if…; antibiotic use is recommended; and antibiotic-use recommendations not stated.

Descriptive analysis of antibiotic prescriptions for bacterial enteric illnesses

FoodNet Canada is a passive sentinel site surveillance system coordinated by the Public Health Agency of Canada (PHAC), in collaboration with provincial and local health authorities, which supports activities for reducing the burden of enteric illnesses in Canada. During the study period, FoodNet Canada had three sentinel sites across Canada: Fraser Health Authority in British Columbia since April 2010 (population 470 334); Alberta Health Services Calgary and Central Zones in Alberta since June 2014 (population 1 009 193); and the Middlesex-London Health Unit in Ontario since August 2014 (population 455 526).

The passive surveillance system is based on case presentation to healthcare practitioners in which a stool specimen is requested and then submitted to a hospital or private medical laboratory for testing for enteric pathogens. Positive isolation of a pathogen is reported directly to the healthcare practitioner and the local public health authority. The local public health authority then administers an enhanced standardized questionnaire for enteric diseases to the cases with positive isolation of a bacterial pathogen. The questionnaire collects information regarding demographic characteristics, symptomology and possible risk factors, which is subsequently cleaned and analysed by the FoodNet Canada team for surveillance purposes. The questionnaire used the following queries to inquire about antibiotic use: ‘Were you prescribed any antibiotics for your illness?’; and ‘If yes, what type of antibiotic (name) was prescribed?’.

The analysis was restricted to the five bacterial enteric pathogens most commonly reported to FoodNet Canada: Campylobacter spp., Salmonella spp., VTEC, Shigella spp. and Y. enterocolitica. Cases lost to follow-up, as determined by the sentinel sites, were excluded from the analysis. Cases that did not answer the question on antibiotic use or stated they did not recall whether they were prescribed an antibiotic were also removed from the analysis. The proportion of cases prescribed an antibiotic and an overall proportion was tabulated for each pathogen. Descriptive analysis was also conducted to identify all types and proportions of antibiotics prescribed and to explore whether the types of antibiotics prescribed differed between pathogens. If cases did not report or could not recall the antibiotic they were prescribed, they were removed from this analysis on antibiotic type.

All descriptive analysis was conducted using SAS 9.3 (SAS Institute Inc., USA) and all figures were generated using Microsoft Excel (Microsoft Corporation, USA).

Guideline concordance

To investigate concordance between the observed antibiotic prescriptions and treatment guidelines, the antibiotic information reported by individual cases was cross-referenced with the pathogen-specific list of recommended antibiotics as identified through the environmental scan. The primary analysis was conducted to examine the proportion of cases that were prescribed various antibiotics. A secondary analysis examined the proportion of antibiotics prescribed that were in concordance with the pathogen-specific list of recommended antibiotics. The denominators for these proportions differ slightly as some cases were prescribed multiple antibiotics.

Results

Environmental scan of practice guidelines

The environmental scan identified a total of 10 practice guidelines published between 2001 and 2016 that met the inclusion criteria (see Table S1, available as Supplementary data at JAC Online).^9–18 The majority of guidelines were designed for all types of patients (n = 6), while others were for specific populations: children (n = 2), adults (n = 1) and adult inpatients (n = 1).

As shown in Table 1, positions on when antibiotic treatment was recommended differed substantially between guidelines and pathogens. Only recommendations for VTEC were consistent across all guidelines (with two abstaining from providing recommendations). The guidelines stated that antibiotic use is not recommended when VTEC was confirmed or suspected, with many of them citing research that attributes antibiotic use to increased risk of haemolytic uraemic syndrome among VTEC cases.²

Table 1.

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Frequency of antibiotic-use recommendations observed in reviewed guidelines by pathogen

	Campylobacter	Salmonella	Shigella	Yersinia	VTEC	Empirical treatment/ traveller’s diarrhoea
Antibiotic use is not recommended	0	0	0	0	8¹⁰^,^12–18	0
Antibiotic use is not recommended unless…	4¹⁰^,¹⁴^,¹⁵^,¹⁸	7¹⁰^,^12–16^,¹⁸	4¹⁰^,¹⁴^,¹⁶^,¹⁸	3¹⁰^,¹²^,¹⁴	0	1¹³
Antibiotic use is recommended if…	2¹¹^,¹⁷	2¹¹^,¹⁷	1¹⁵	4¹³^,^15–17	0	5^9–12^,¹⁴
Antibiotic use is recommended	3¹²^,¹³^,¹⁶	0	4^11–13^,¹⁷	0	0	3^16–18
Antibiotic-use recommendations not stated	1⁹	1⁹	1⁹	2⁹^,¹¹	2⁹^,¹¹	1¹⁵

	Campylobacter	Salmonella	Shigella	Yersinia	VTEC	Empirical treatment/ traveller’s diarrhoea
Antibiotic use is not recommended	0	0	0	0	8¹⁰^,^12–18	0
Antibiotic use is not recommended unless…	4¹⁰^,¹⁴^,¹⁵^,¹⁸	7¹⁰^,^12–16^,¹⁸	4¹⁰^,¹⁴^,¹⁶^,¹⁸	3¹⁰^,¹²^,¹⁴	0	1¹³
Antibiotic use is recommended if…	2¹¹^,¹⁷	2¹¹^,¹⁷	1¹⁵	4¹³^,^15–17	0	5^9–12^,¹⁴
Antibiotic use is recommended	3¹²^,¹³^,¹⁶	0	4^11–13^,¹⁷	0	0	3^16–18
Antibiotic-use recommendations not stated	1⁹	1⁹	1⁹	2⁹^,¹¹	2⁹^,¹¹	1¹⁵

Table 1.

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Frequency of antibiotic-use recommendations observed in reviewed guidelines by pathogen

	Campylobacter	Salmonella	Shigella	Yersinia	VTEC	Empirical treatment/ traveller’s diarrhoea
Antibiotic use is not recommended	0	0	0	0	8¹⁰^,^12–18	0
Antibiotic use is not recommended unless…	4¹⁰^,¹⁴^,¹⁵^,¹⁸	7¹⁰^,^12–16^,¹⁸	4¹⁰^,¹⁴^,¹⁶^,¹⁸	3¹⁰^,¹²^,¹⁴	0	1¹³
Antibiotic use is recommended if…	2¹¹^,¹⁷	2¹¹^,¹⁷	1¹⁵	4¹³^,^15–17	0	5^9–12^,¹⁴
Antibiotic use is recommended	3¹²^,¹³^,¹⁶	0	4^11–13^,¹⁷	0	0	3^16–18
Antibiotic-use recommendations not stated	1⁹	1⁹	1⁹	2⁹^,¹¹	2⁹^,¹¹	1¹⁵

	Campylobacter	Salmonella	Shigella	Yersinia	VTEC	Empirical treatment/ traveller’s diarrhoea
Antibiotic use is not recommended	0	0	0	0	8¹⁰^,^12–18	0
Antibiotic use is not recommended unless…	4¹⁰^,¹⁴^,¹⁵^,¹⁸	7¹⁰^,^12–16^,¹⁸	4¹⁰^,¹⁴^,¹⁶^,¹⁸	3¹⁰^,¹²^,¹⁴	0	1¹³
Antibiotic use is recommended if…	2¹¹^,¹⁷	2¹¹^,¹⁷	1¹⁵	4¹³^,^15–17	0	5^9–12^,¹⁴
Antibiotic use is recommended	3¹²^,¹³^,¹⁶	0	4^11–13^,¹⁷	0	0	3^16–18
Antibiotic-use recommendations not stated	1⁹	1⁹	1⁹	2⁹^,¹¹	2⁹^,¹¹	1¹⁵

There were notable variations in the guideline recommendations for the remaining pathogens, with many of these including caveats as to when a case would benefit from antibiotic use. These caveats varied by pathogen and by guideline, but several were repeatedly mentioned: invasive infection/bacteraemia, the patient being of extreme age (both young and old), the patient being immunocompromised, the illness lasting longer than a week and the presence of fever, bloody diarrhoea or generally severe symptoms.

The type of antibiotic recommended by the guidelines was also found to vary by pathogen and guideline. In total, there were 36 different antibiotic type–pathogen combinations recommended in the reviewed guidelines. These antibiotic type–pathogen combinations were not consistent between the guidelines. The only antibiotic type–pathogen combination for which there was a consensus amongst the reviewed guidelines was for the use of ciprofloxacin to treat Salmonella, Shigella and empirical treatment/traveller’s diarrhoea. A listing of the antibiotics recommended for each pathogen and the frequency at which these were observed can be found in Table 2.

Table 2.

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Frequency of antibiotic-type recommendations observed in reviewed guidelines by pathogen^a

	Campylobacter (n = 8)	Salmonella (n = 7)	Shigella (n = 8)	Yersinia (n = 6)	Empirical treatment/ traveller’s diarrhoea (n = 8)
Ciprofloxacin^b	5^10–13^,¹⁵	7¹⁰^,^12–17	8^10–17	5¹⁰^,¹²^,¹⁴^,¹⁵^,¹⁷	8^9–12^,¹⁴^,^16–18
Trimethoprim/sulfamethoxazole	0	5¹⁰^,^14–17	6^12–17	6¹⁰^,¹²^,^14–17	3¹⁰^,¹²^,¹⁴
Azithromycin	6^10–13^,¹⁶^,¹⁷	4¹⁰^,¹²^,¹³^,¹⁶	5¹⁰^,^12–14^,¹⁶	1¹⁰	5⁹^,¹⁰^,¹²^,¹⁶^,¹⁸
Ceftriaxone	0	6¹⁰^,^12–14^,¹⁶^,¹⁷	6^10–14^,¹⁶	0	1¹⁰
Levofloxacin^b	0	0	3¹²^,¹⁴^,¹⁵	0	5⁹^,¹⁰^,¹²^,¹⁴^,¹⁶
Doxycycline^b	3¹²^,¹³^,¹⁵	0	0	4^14–17	0
Erythromycin	5¹⁰^,¹²^,^14–16	0	0	0	0
Ampicillin	0	2¹⁵^,¹⁶	3¹³^,¹⁵^,¹⁶	0	0
Cefixime	0	1¹²	3¹⁰^,¹³^,¹⁶	0	1¹⁰
Norfloxacin^b	0	0	0	0	4⁹^,¹⁰^,¹⁴^,¹⁶
Ofloxacin^b	0	0	0	0	3⁹^,¹⁴^,¹⁶
Aminoglycosides	0	0	0	3^14–16	0
Chloramphenicol	0	2¹²^,¹⁵	0	1¹⁶	0
Nalidixic acid^b	0	0	2¹³^,¹⁴	0	0
Amoxicillin	0	1¹⁶	0	0	0
Pivmecillinam	0	0	1¹¹	0	0
Rifaximin	0	0	0	0	1¹⁸
No specific drugs recommended	1⁹	2⁹^,¹¹	1⁹	3⁹^,¹¹^,¹³	2¹³^,¹⁵

	Campylobacter (n = 8)	Salmonella (n = 7)	Shigella (n = 8)	Yersinia (n = 6)	Empirical treatment/ traveller’s diarrhoea (n = 8)
Ciprofloxacin^b	5^10–13^,¹⁵	7¹⁰^,^12–17	8^10–17	5¹⁰^,¹²^,¹⁴^,¹⁵^,¹⁷	8^9–12^,¹⁴^,^16–18
Trimethoprim/sulfamethoxazole	0	5¹⁰^,^14–17	6^12–17	6¹⁰^,¹²^,^14–17	3¹⁰^,¹²^,¹⁴
Azithromycin	6^10–13^,¹⁶^,¹⁷	4¹⁰^,¹²^,¹³^,¹⁶	5¹⁰^,^12–14^,¹⁶	1¹⁰	5⁹^,¹⁰^,¹²^,¹⁶^,¹⁸
Ceftriaxone	0	6¹⁰^,^12–14^,¹⁶^,¹⁷	6^10–14^,¹⁶	0	1¹⁰
Levofloxacin^b	0	0	3¹²^,¹⁴^,¹⁵	0	5⁹^,¹⁰^,¹²^,¹⁴^,¹⁶
Doxycycline^b	3¹²^,¹³^,¹⁵	0	0	4^14–17	0
Erythromycin	5¹⁰^,¹²^,^14–16	0	0	0	0
Ampicillin	0	2¹⁵^,¹⁶	3¹³^,¹⁵^,¹⁶	0	0
Cefixime	0	1¹²	3¹⁰^,¹³^,¹⁶	0	1¹⁰
Norfloxacin^b	0	0	0	0	4⁹^,¹⁰^,¹⁴^,¹⁶
Ofloxacin^b	0	0	0	0	3⁹^,¹⁴^,¹⁶
Aminoglycosides	0	0	0	3^14–16	0
Chloramphenicol	0	2¹²^,¹⁵	0	1¹⁶	0
Nalidixic acid^b	0	0	2¹³^,¹⁴	0	0
Amoxicillin	0	1¹⁶	0	0	0
Pivmecillinam	0	0	1¹¹	0	0
Rifaximin	0	0	0	0	1¹⁸
No specific drugs recommended	1⁹	2⁹^,¹¹	1⁹	3⁹^,¹¹^,¹³	2¹³^,¹⁵

n = total number of guidelines that provided antibiotic-type recommendations for each pathogen.

a

VTEC not included as all guidelines did not recommend antibiotic use.

b

Guidelines that recommended the broad categories of quinolones, fluoroquinolones and tetracyclines were amalgamated into the frequencies of individual drugs within these categories.

Table 2.

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Frequency of antibiotic-type recommendations observed in reviewed guidelines by pathogen^a

	Campylobacter (n = 8)	Salmonella (n = 7)	Shigella (n = 8)	Yersinia (n = 6)	Empirical treatment/ traveller’s diarrhoea (n = 8)
Ciprofloxacin^b	5^10–13^,¹⁵	7¹⁰^,^12–17	8^10–17	5¹⁰^,¹²^,¹⁴^,¹⁵^,¹⁷	8^9–12^,¹⁴^,^16–18
Trimethoprim/sulfamethoxazole	0	5¹⁰^,^14–17	6^12–17	6¹⁰^,¹²^,^14–17	3¹⁰^,¹²^,¹⁴
Azithromycin	6^10–13^,¹⁶^,¹⁷	4¹⁰^,¹²^,¹³^,¹⁶	5¹⁰^,^12–14^,¹⁶	1¹⁰	5⁹^,¹⁰^,¹²^,¹⁶^,¹⁸
Ceftriaxone	0	6¹⁰^,^12–14^,¹⁶^,¹⁷	6^10–14^,¹⁶	0	1¹⁰
Levofloxacin^b	0	0	3¹²^,¹⁴^,¹⁵	0	5⁹^,¹⁰^,¹²^,¹⁴^,¹⁶
Doxycycline^b	3¹²^,¹³^,¹⁵	0	0	4^14–17	0
Erythromycin	5¹⁰^,¹²^,^14–16	0	0	0	0
Ampicillin	0	2¹⁵^,¹⁶	3¹³^,¹⁵^,¹⁶	0	0
Cefixime	0	1¹²	3¹⁰^,¹³^,¹⁶	0	1¹⁰
Norfloxacin^b	0	0	0	0	4⁹^,¹⁰^,¹⁴^,¹⁶
Ofloxacin^b	0	0	0	0	3⁹^,¹⁴^,¹⁶
Aminoglycosides	0	0	0	3^14–16	0
Chloramphenicol	0	2¹²^,¹⁵	0	1¹⁶	0
Nalidixic acid^b	0	0	2¹³^,¹⁴	0	0
Amoxicillin	0	1¹⁶	0	0	0
Pivmecillinam	0	0	1¹¹	0	0
Rifaximin	0	0	0	0	1¹⁸
No specific drugs recommended	1⁹	2⁹^,¹¹	1⁹	3⁹^,¹¹^,¹³	2¹³^,¹⁵

	Campylobacter (n = 8)	Salmonella (n = 7)	Shigella (n = 8)	Yersinia (n = 6)	Empirical treatment/ traveller’s diarrhoea (n = 8)
Ciprofloxacin^b	5^10–13^,¹⁵	7¹⁰^,^12–17	8^10–17	5¹⁰^,¹²^,¹⁴^,¹⁵^,¹⁷	8^9–12^,¹⁴^,^16–18
Trimethoprim/sulfamethoxazole	0	5¹⁰^,^14–17	6^12–17	6¹⁰^,¹²^,^14–17	3¹⁰^,¹²^,¹⁴
Azithromycin	6^10–13^,¹⁶^,¹⁷	4¹⁰^,¹²^,¹³^,¹⁶	5¹⁰^,^12–14^,¹⁶	1¹⁰	5⁹^,¹⁰^,¹²^,¹⁶^,¹⁸
Ceftriaxone	0	6¹⁰^,^12–14^,¹⁶^,¹⁷	6^10–14^,¹⁶	0	1¹⁰
Levofloxacin^b	0	0	3¹²^,¹⁴^,¹⁵	0	5⁹^,¹⁰^,¹²^,¹⁴^,¹⁶
Doxycycline^b	3¹²^,¹³^,¹⁵	0	0	4^14–17	0
Erythromycin	5¹⁰^,¹²^,^14–16	0	0	0	0
Ampicillin	0	2¹⁵^,¹⁶	3¹³^,¹⁵^,¹⁶	0	0
Cefixime	0	1¹²	3¹⁰^,¹³^,¹⁶	0	1¹⁰
Norfloxacin^b	0	0	0	0	4⁹^,¹⁰^,¹⁴^,¹⁶
Ofloxacin^b	0	0	0	0	3⁹^,¹⁴^,¹⁶
Aminoglycosides	0	0	0	3^14–16	0
Chloramphenicol	0	2¹²^,¹⁵	0	1¹⁶	0
Nalidixic acid^b	0	0	2¹³^,¹⁴	0	0
Amoxicillin	0	1¹⁶	0	0	0
Pivmecillinam	0	0	1¹¹	0	0
Rifaximin	0	0	0	0	1¹⁸
No specific drugs recommended	1⁹	2⁹^,¹¹	1⁹	3⁹^,¹¹^,¹³	2¹³^,¹⁵

n = total number of guidelines that provided antibiotic-type recommendations for each pathogen.

a

VTEC not included as all guidelines did not recommend antibiotic use.

b

Guidelines that recommended the broad categories of quinolones, fluoroquinolones and tetracyclines were amalgamated into the frequencies of individual drugs within these categories.

Descriptive analysis of antibiotic prescriptions for bacterial enteric illnesses

A total of 7037 cases of laboratory-confirmed Campylobacter spp., Salmonella spp., VTEC, Shigella spp. or Y. enterocolitica cases were reported to PHAC’s FoodNet Canada between 1 January 2010 and 31 December 2018. Of these cases, 707 were lost to follow-up and the antibiotic use of 453 cases was unknown. The remaining 5877 cases were included in the analysis. The overall proportion of cases that received an antibiotic prescription was 49.3%, with the proportion varying by the causative pathogen (Table 3). Overall, 59.6% of Shigella cases received an antibiotic prescription, which was the highest proportion observed amongst the pathogens included. The pathogen with the lowest proportion was VTEC, for which 20.6% of cases received a prescription.

Table 3.

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Total number of cases reported to FoodNet Canada and total number and percentage of cases reporting receiving an antibiotic prescription by causative organism, 2010–18

	Total number of cases reported to FoodNet Canada	Total number of cases reporting receiving an antibiotic prescription (percentage of cases)
Pathogens
Campylobacter	2690	1474 (54.8)
Salmonella	2238	1067 (47.7)
Yersinia	411	167 (40.6)
VTEC	335	69 (20.6)
Shigella	203	121 (59.6)
Total	5877	2898 (49.3)

	Total number of cases reported to FoodNet Canada	Total number of cases reporting receiving an antibiotic prescription (percentage of cases)
Pathogens
Campylobacter	2690	1474 (54.8)
Salmonella	2238	1067 (47.7)
Yersinia	411	167 (40.6)
VTEC	335	69 (20.6)
Shigella	203	121 (59.6)
Total	5877	2898 (49.3)

Table 3.

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Total number of cases reported to FoodNet Canada and total number and percentage of cases reporting receiving an antibiotic prescription by causative organism, 2010–18

	Total number of cases reported to FoodNet Canada	Total number of cases reporting receiving an antibiotic prescription (percentage of cases)
Pathogens
Campylobacter	2690	1474 (54.8)
Salmonella	2238	1067 (47.7)
Yersinia	411	167 (40.6)
VTEC	335	69 (20.6)
Shigella	203	121 (59.6)
Total	5877	2898 (49.3)

	Total number of cases reported to FoodNet Canada	Total number of cases reporting receiving an antibiotic prescription (percentage of cases)
Pathogens
Campylobacter	2690	1474 (54.8)
Salmonella	2238	1067 (47.7)
Yersinia	411	167 (40.6)
VTEC	335	69 (20.6)
Shigella	203	121 (59.6)
Total	5877	2898 (49.3)

A total of 2898 cases (49.3%) reported being prescribed an antibiotic, of which 1856 (64.0%) provided information on the type of antibiotic prescribed. Thirty-five different antibiotics were prescribed to cases included in this analysis, of which the most commonly prescribed was ciprofloxacin, representing 46.2% of all prescriptions, followed by azithromycin (20.5%) and metronidazole (9.9%). One hundred and forty-six cases reported having received multiple antibiotics for treatment. Of these cases, the combination of ciprofloxacin and metronidazole was the most common, with 60 cases receiving this combination.

Guideline concordance

Substantial discordance between the type of antibiotics recommended in the guidelines and those used in practice was observed. Of the 17 types of antibiotics recommended in the guidelines, 14 were used in practice. In addition to these, 18 other antibiotics not included in any of the guidelines reviewed were also prescribed (Table 4).

Table 4.

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Comparison of antibiotics prescribed to cases of enteric illness across FoodNet Canada sentinel sites with antibiotics recommended in clinical treatment guidelines reviewed

	Campylobacter n = 939	Salmonella n = 697	VTEC n = 44	Shigella n = 83	Yersinia n = 93	Empirical treatment/ traveller’s diarrhoea
Ciprofloxacin	● (35.9)	● (56.8)	X (59.1)	● (55.4)	● (55.9)	●
Azithromycin	● (32.5)	● (7.9)	X (13.6)	● (10.8)	X (5.4)	●
Metronidazole	X (8.1)	X (10.3)	X (22.7)	X (15.7)	X (14.0)
Erythromycin	● (17.8)	X (1.4)		X (1.2)	X (1.1)
Trimethoprim/sulfamethoxazole	X (1.1)	● (8.6)	X (2.3)	● (3.6)	● (11.8)	●
Amoxicillin	X (2.0)	● (4.6)	X (2.3)	X (7.2)
Ceftriaxone	X (0.4)	● (7.0)		● (1.2)	●
Clarithromycin	X (3.7)	X (0.3)			X (2.2)
Cefixime	X (0.3)	X (3.0)		● (6.0)
Levofloxacin	● (0.9)	● (1.6)		●	●	●
Sulfamethoxazole	X (0.2)	X (1.9)	X (2.3)		X (3.2)
Nitrofurantoin		X (1.7)	X (2.3)
Ampicillin		● (1.3)		● (2.4)
Vancomycin	X (0.3)	X (0.1)	X (2.3)	X (1.2)	X (5.4)
Tetracyclines^a	● (0.7)	X (0.1)		●	● (6.5)
Piperacillin/tazobactam	X (0.1)	X (0.9)
Clindamycin	X (0.5)	X (0.1)
Penicillin	X (0.1)	X (0.4)		X (2.4)
Cephalexin	X (0.1)	X (0.4)		X (1.2)
Norfloxacin	● (0.1)	● (0.6)		●	●	●
Trimethoprim		X (0.4)
Aminoglycosides^a	X (0.2)				●
Cefotaxime	X (0.1)				X (1.1)
Cefazolin		X (0.1)
Cloxacillin					X (1.1)
Ertapenem		X (0.1)
Flucloxacillin	X (0.1)
Imipenem	X (0.1)
Meropenem		X (0.3)
Moxifloxacin	● (0.1)	●		●	●	●
Ofloxacin	●	●		● (1.2)	●	●
Piperacillin		X (0.1)
Chloramphenicol		●			●
Pivmecillinam				●
Rifaximin						●

	Campylobacter n = 939	Salmonella n = 697	VTEC n = 44	Shigella n = 83	Yersinia n = 93	Empirical treatment/ traveller’s diarrhoea
Ciprofloxacin	● (35.9)	● (56.8)	X (59.1)	● (55.4)	● (55.9)	●
Azithromycin	● (32.5)	● (7.9)	X (13.6)	● (10.8)	X (5.4)	●
Metronidazole	X (8.1)	X (10.3)	X (22.7)	X (15.7)	X (14.0)
Erythromycin	● (17.8)	X (1.4)		X (1.2)	X (1.1)
Trimethoprim/sulfamethoxazole	X (1.1)	● (8.6)	X (2.3)	● (3.6)	● (11.8)	●
Amoxicillin	X (2.0)	● (4.6)	X (2.3)	X (7.2)
Ceftriaxone	X (0.4)	● (7.0)		● (1.2)	●
Clarithromycin	X (3.7)	X (0.3)			X (2.2)
Cefixime	X (0.3)	X (3.0)		● (6.0)
Levofloxacin	● (0.9)	● (1.6)		●	●	●
Sulfamethoxazole	X (0.2)	X (1.9)	X (2.3)		X (3.2)
Nitrofurantoin		X (1.7)	X (2.3)
Ampicillin		● (1.3)		● (2.4)
Vancomycin	X (0.3)	X (0.1)	X (2.3)	X (1.2)	X (5.4)
Tetracyclines^a	● (0.7)	X (0.1)		●	● (6.5)
Piperacillin/tazobactam	X (0.1)	X (0.9)
Clindamycin	X (0.5)	X (0.1)
Penicillin	X (0.1)	X (0.4)		X (2.4)
Cephalexin	X (0.1)	X (0.4)		X (1.2)
Norfloxacin	● (0.1)	● (0.6)		●	●	●
Trimethoprim		X (0.4)
Aminoglycosides^a	X (0.2)				●
Cefotaxime	X (0.1)				X (1.1)
Cefazolin		X (0.1)
Cloxacillin					X (1.1)
Ertapenem		X (0.1)
Flucloxacillin	X (0.1)
Imipenem	X (0.1)
Meropenem		X (0.3)
Moxifloxacin	● (0.1)	●		●	●	●
Ofloxacin	●	●		● (1.2)	●	●
Piperacillin		X (0.1)
Chloramphenicol		●			●
Pivmecillinam				●
Rifaximin						●

n = number of cases.

Numbers in parentheses show the proportion of cases that received a prescription for each antibiotic.

●

, antibiotic was recommended in guidelines for that specific pathogen.

X, antibiotic was not recommended in guidelines for that specific pathogen.

a

Individual drugs were amalgamated into these drug categories.

Table 4.

Open in new tab

Comparison of antibiotics prescribed to cases of enteric illness across FoodNet Canada sentinel sites with antibiotics recommended in clinical treatment guidelines reviewed

	Campylobacter n = 939	Salmonella n = 697	VTEC n = 44	Shigella n = 83	Yersinia n = 93	Empirical treatment/ traveller’s diarrhoea
Ciprofloxacin	● (35.9)	● (56.8)	X (59.1)	● (55.4)	● (55.9)	●
Azithromycin	● (32.5)	● (7.9)	X (13.6)	● (10.8)	X (5.4)	●
Metronidazole	X (8.1)	X (10.3)	X (22.7)	X (15.7)	X (14.0)
Erythromycin	● (17.8)	X (1.4)		X (1.2)	X (1.1)
Trimethoprim/sulfamethoxazole	X (1.1)	● (8.6)	X (2.3)	● (3.6)	● (11.8)	●
Amoxicillin	X (2.0)	● (4.6)	X (2.3)	X (7.2)
Ceftriaxone	X (0.4)	● (7.0)		● (1.2)	●
Clarithromycin	X (3.7)	X (0.3)			X (2.2)
Cefixime	X (0.3)	X (3.0)		● (6.0)
Levofloxacin	● (0.9)	● (1.6)		●	●	●
Sulfamethoxazole	X (0.2)	X (1.9)	X (2.3)		X (3.2)
Nitrofurantoin		X (1.7)	X (2.3)
Ampicillin		● (1.3)		● (2.4)
Vancomycin	X (0.3)	X (0.1)	X (2.3)	X (1.2)	X (5.4)
Tetracyclines^a	● (0.7)	X (0.1)		●	● (6.5)
Piperacillin/tazobactam	X (0.1)	X (0.9)
Clindamycin	X (0.5)	X (0.1)
Penicillin	X (0.1)	X (0.4)		X (2.4)
Cephalexin	X (0.1)	X (0.4)		X (1.2)
Norfloxacin	● (0.1)	● (0.6)		●	●	●
Trimethoprim		X (0.4)
Aminoglycosides^a	X (0.2)				●
Cefotaxime	X (0.1)				X (1.1)
Cefazolin		X (0.1)
Cloxacillin					X (1.1)
Ertapenem		X (0.1)
Flucloxacillin	X (0.1)
Imipenem	X (0.1)
Meropenem		X (0.3)
Moxifloxacin	● (0.1)	●		●	●	●
Ofloxacin	●	●		● (1.2)	●	●
Piperacillin		X (0.1)
Chloramphenicol		●			●
Pivmecillinam				●
Rifaximin						●

	Campylobacter n = 939	Salmonella n = 697	VTEC n = 44	Shigella n = 83	Yersinia n = 93	Empirical treatment/ traveller’s diarrhoea
Ciprofloxacin	● (35.9)	● (56.8)	X (59.1)	● (55.4)	● (55.9)	●
Azithromycin	● (32.5)	● (7.9)	X (13.6)	● (10.8)	X (5.4)	●
Metronidazole	X (8.1)	X (10.3)	X (22.7)	X (15.7)	X (14.0)
Erythromycin	● (17.8)	X (1.4)		X (1.2)	X (1.1)
Trimethoprim/sulfamethoxazole	X (1.1)	● (8.6)	X (2.3)	● (3.6)	● (11.8)	●
Amoxicillin	X (2.0)	● (4.6)	X (2.3)	X (7.2)
Ceftriaxone	X (0.4)	● (7.0)		● (1.2)	●
Clarithromycin	X (3.7)	X (0.3)			X (2.2)
Cefixime	X (0.3)	X (3.0)		● (6.0)
Levofloxacin	● (0.9)	● (1.6)		●	●	●
Sulfamethoxazole	X (0.2)	X (1.9)	X (2.3)		X (3.2)
Nitrofurantoin		X (1.7)	X (2.3)
Ampicillin		● (1.3)		● (2.4)
Vancomycin	X (0.3)	X (0.1)	X (2.3)	X (1.2)	X (5.4)
Tetracyclines^a	● (0.7)	X (0.1)		●	● (6.5)
Piperacillin/tazobactam	X (0.1)	X (0.9)
Clindamycin	X (0.5)	X (0.1)
Penicillin	X (0.1)	X (0.4)		X (2.4)
Cephalexin	X (0.1)	X (0.4)		X (1.2)
Norfloxacin	● (0.1)	● (0.6)		●	●	●
Trimethoprim		X (0.4)
Aminoglycosides^a	X (0.2)				●
Cefotaxime	X (0.1)				X (1.1)
Cefazolin		X (0.1)
Cloxacillin					X (1.1)
Ertapenem		X (0.1)
Flucloxacillin	X (0.1)
Imipenem	X (0.1)
Meropenem		X (0.3)
Moxifloxacin	● (0.1)	●		●	●	●
Ofloxacin	●	●		● (1.2)	●	●
Piperacillin		X (0.1)
Chloramphenicol		●			●
Pivmecillinam				●
Rifaximin						●

n = number of cases.

Numbers in parentheses show the proportion of cases that received a prescription for each antibiotic.

●

, antibiotic was recommended in guidelines for that specific pathogen.

X, antibiotic was not recommended in guidelines for that specific pathogen.

a

Individual drugs were amalgamated into these drug categories.

A total of 1999 antibiotic prescriptions with data on the type of antibiotic prescribed were reported by cases. The overall proportion of prescriptions that were in concordance with the pathogen-specific list of recommended antibiotics was 78.0%. This proportion varied by pathogen, with the lowest concordance being observed in VTEC prescriptions at 0.0% and the highest for Campylobacter at 82.8% (Table 5). When VTEC cases were excluded, as no agent is guideline concordant for this pathogen, the proportion of prescriptions that were in concordance was 79.9%.

Table 5.

Open in new tab

Number of antibiotic prescriptions reported by cases and number and percentage of prescriptions that were in concordance with the pathogen-specific list of recommended antibiotics

	Number of antibiotic prescriptions reported by cases^a	Number of prescriptions that were in concordance with the pathogen-specific list of recommended antibiotics (percentage of prescriptions)
Pathogens
Campylobacter	991	821 (82.8)
Salmonella	770	607 (78.8)
Yersinia	100	65 (65.0)
VTEC	47	0 (0.0)
Shigella	91	67 (73.6)
Total	1999	1560 (78.0)

	Number of antibiotic prescriptions reported by cases^a	Number of prescriptions that were in concordance with the pathogen-specific list of recommended antibiotics (percentage of prescriptions)
Pathogens
Campylobacter	991	821 (82.8)
Salmonella	770	607 (78.8)
Yersinia	100	65 (65.0)
VTEC	47	0 (0.0)
Shigella	91	67 (73.6)
Total	1999	1560 (78.0)

a

Only includes those that included the type of antibiotic prescribed.

Table 5.

Open in new tab

Number of antibiotic prescriptions reported by cases and number and percentage of prescriptions that were in concordance with the pathogen-specific list of recommended antibiotics

	Number of antibiotic prescriptions reported by cases^a	Number of prescriptions that were in concordance with the pathogen-specific list of recommended antibiotics (percentage of prescriptions)
Pathogens
Campylobacter	991	821 (82.8)
Salmonella	770	607 (78.8)
Yersinia	100	65 (65.0)
VTEC	47	0 (0.0)
Shigella	91	67 (73.6)
Total	1999	1560 (78.0)

	Number of antibiotic prescriptions reported by cases^a	Number of prescriptions that were in concordance with the pathogen-specific list of recommended antibiotics (percentage of prescriptions)
Pathogens
Campylobacter	991	821 (82.8)
Salmonella	770	607 (78.8)
Yersinia	100	65 (65.0)
VTEC	47	0 (0.0)
Shigella	91	67 (73.6)
Total	1999	1560 (78.0)

a

Only includes those that included the type of antibiotic prescribed.

Discussion

Results from the environmental scan of treatment guidelines for bacterial enteric illnesses found a substantial variation on when guidelines recommend antibiotics be used and which antibiotics should be recommended. Our study describes antibiotic prescribing trends observed from 5877 laboratory-confirmed cases of bacterial enteric illness reported to a surveillance system, 49% of whom received an antibiotic prescription.

Our study had several notable limitations. First, despite searching several databases and sources, the environmental scan of treatment guidelines was unlikely to have captured all relevant guidelines. Older guidelines not listed in these online databases, guidelines used by clinical decision support resources and guidelines published in languages other than English would have been missed in the environmental scan. It is also unknown how frequently Canadian physicians use these older guidelines. A significant limitation of this study is that the data used for determining trends of antibiotic use were self-reported, which makes it subject to recall bias. It is also important to note that the current data provide only a snapshot of cases’ antibiotic use and not of the full clinical treatment chain (i.e. healthcare practitioner visit up to being reported to national surveillance). As a result, important temporal aspects, such as the timeline of the antibiotic prescription, could not be assessed. Information on whether the antibiotic was prescribed before or after the culture results was known would provide further insight into prescribing practices. An additional limitation is the lack of information on comorbidities, allergies or other key factors that would influence a healthcare practitioner’s decision to prescribe antibiotics or the particular type of antibiotic. This prevented case-by-case evaluation from determining whether the antibiotic prescribed was needed and whether the type of antibiotic was appropriate, limiting the analysis to descriptive statistics. Additionally, one of the criteria for determining whether treatment was necessary was the severity of the disease. This study was unable to examine this criterion as there was no consistent definition of severity used by the guidelines. An array of factors used in various combinations were used by guidelines to indicate the severity of disease, including the presence of bloody diarrhoea and/or fever, hospitalization, bacteraemia and frequency of diarrhoea. Not only does the absence of a universal definition of severity prevent this study from effectively exploring the effect of severity on antibiotic prescribing, it may also cause a disparity in how healthcare practitioners view severity and subsequently how they prescribe antibiotics.

It is important to recognize that the cases included in this study represent only individuals who sought medical attention and for whom a clinical specimen was requested, submitted and confirmed by a laboratory as containing a pathogen. A study by Thomas et al.⁵ estimated that for every laboratory-confirmed Campylobacter case captured by surveillance, there were approximately 26 other Campylobacter cases in the community going undiagnosed or unreported. Due to this, the findings of our study should not be extrapolated out to represent all enteric bacterial cases in the community or all cases that seek medical attention. Further research is needed to understand antibiotic prescribing practices for all cases of enteric bacterial infections that receive medical attention.

Despite these limitations, our study provides much-needed information on the current state of antibiotic prescribing practices for bacterial enteric illnesses. The environmental scan of treatment guidelines found that apart from recommendations for VTEC, there was no consensus of when or which antibiotics were recommended for bacterial enteric illnesses. The observed variance in treatment recommendations is a concern as it is higher than one would expect if all guidelines were basing their recommendations on the same evidence. It is possible that the heterogeneity in guideline recommendations could be explained by differences in the scope of the guidelines (adult/paediatric or inpatient/outpatient) or other factors such as the year the guidelines were published. Recognizing that there is substantial variation in treatment guidelines provides valuable context to understanding antibiotic prescribing practices.

Our analysis of the 5877 cases of laboratory-confirmed enteric bacterial infections reported across three Canadian sentinel sites offers a unique glimpse into prescribing practices. Observing that 49% of our cases were prescribed an antibiotic sets a benchmark that future prescribing rates can be compared with. Previous Canadian studies have investigated antibiotic prescribing more broadly among cases of acute gastrointestinal illness or diseases of the gastrointestinal system. Observed rates of antibiotic prescribing among these studies ranged from 6% to 10%, which are substantially lower than what was observed in our study.⁶^,⁷ The large difference observed could be due to different case definitions used for case inclusion as these studies defined cases as anyone that suffered diarrhoea in the previous 3–7 days, which would include cases that did not seek medical attention and cases infected by bacterial, viral or parasitic organisms. Similar rates have been observed in previous studies conducted elsewhere in the world. A 2017 study conducted in Spain of children with culture-confirmed cases of bacterial gastroenteritis reported that 33% of cases received an antibiotic prescription.¹⁹ Another study by Sasaki et al.²⁰ (2018) found that 73% of hospitalized cases of infectious diarrhoea received an antibiotic prescription. These high rates of antibiotic use are of substantial concern as it has been shown that high consumption of antibiotics is strongly associated with the development of antibiotic-resistant bacteria.²¹

The case-level detail of our data also allowed us to explore the pathogen-specific rates of antibiotic prescribing. A remarkable finding was that 21% of VTEC cases reported having received an antibiotic prescription, seeing as antibiotic treatment has been shown to increase the risk of developing haemolytic uraemic syndrome in cases of VTEC.²^,²² It is suspected that the majority of the 69 VTEC cases that received an antibiotic prescription were treated empirically. Empirical treatment of enteric infections is reasonable under some circumstances (such as treating patients who are immunocompromised or are severely ill) and is often necessary for time-sensitive treatment as cultures can take up to 48 h.²³^,²⁴ However, the use of antibiotics for treating VTEC cases represents a potential risk if treating empirically, as their use can lead to the development of haemolytic uraemic syndrome.¹^,²

Considerable differences in the antibiotic types used in practice and those recommended within the reviewed guidelines were also observed in our data (self-reported by cases). Of the 60 drug–pathogen combinations reported in the data, only 18 were recommended in the guidelines reviewed. It is important to note that the majority of these non-guideline combinations were rare, only being observed once or twice in the data. Metronidazole is the major exception to this. It was prescribed for treating illnesses associated with all five pathogens and was the third most commonly prescribed antibiotic, but was not indicated in any reviewed guideline (neither pathogen-specific nor empirical treatment/traveller’s diarrhoea). The Sanford Guide (2015) states metronidazole can be used to treat giardiasis, amoebiasis, mild Clostridioides difficile infections and (when combined with another antibacterial) contamination of the peritoneal cavity with bowel flora.¹² The high use of metronidazole observed in our study is indicative of empirical treatment being common practice for acute gastrointestinal illnesses and may be either an indication of healthcare practitioners’ concerns regarding community-acquired C. difficile infections or of a parasitic infection being suspected.

The findings from this study highlight the need to develop future antibiotic stewardship initiatives that target bacterial enteric illnesses in addition to improving current guidelines for treating these infections. Future studies are needed to better understand the decision to prescribe antibiotics by healthcare practitioners, such as determining which attributes of cases make them more or less likely to be prescribed antibiotics. Studies that investigate antibiotic prescribing practices for all cases of gastrointestinal diseases are needed, as this study could only describe laboratory-confirmed cases of bacterial enteric infections that were reported and captured through an existing enhanced surveillance system. Additionally, the results of this study may encourage healthcare practitioners to reflect on their own prescribing practices critically.

Acknowledgements

Preliminary results from this study were presented at the 2017 and 2018 annual conferences of the Association of Medical Microbiology and Infectious Disease (Abstract SP25 and Abstract SP58, respectively).

We would like to thank Dr John Conly, Dr Fawziah Lalji, Dr David Patrick and Dr Lynora Saxinger for providing medical advice to better analyse and interpret the findings of this work. We would also like to acknowledge Dr Frank Pollari for initiating this line of research and all the public health inspectors and public health nurses in the sentinel sites that follow up with cases and collect the questionnaire data.

Transparency declarations

None to declare.

Funding

The Public Health Agency of Canada supported this research.

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Article Contents

An analysis of antibiotic prescribing practices for enteric bacterial infections within FoodNet Canada sentinel sites

Abstract

Introduction

Methods

Environmental scan of practice guidelines

Descriptive analysis of antibiotic prescriptions for bacterial enteric illnesses

Guideline concordance

Results

Environmental scan of practice guidelines

Descriptive analysis of antibiotic prescriptions for bacterial enteric illnesses

Guideline concordance

Discussion

Acknowledgements

Transparency declarations

Funding

References

Supplementary data

Citations

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Article Contents

An analysis of antibiotic prescribing practices for enteric bacterial infections within FoodNet Canada sentinel sites Free

Abstract

Introduction

Methods

Environmental scan of practice guidelines

Descriptive analysis of antibiotic prescriptions for bacterial enteric illnesses

Guideline concordance

Results

Environmental scan of practice guidelines

Descriptive analysis of antibiotic prescriptions for bacterial enteric illnesses

Guideline concordance

Discussion

Acknowledgements

Transparency declarations

Funding

References

Supplementary data

Citations

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An analysis of antibiotic prescribing practices for enteric bacterial infections within FoodNet Canada sentinel sites