https://orcid.org/0000-0002-7037-4708
Figures
Abstract
Background
The burden of cancer is large in Australia, and rates of cancer Clinical Practice Guideline (CPG) adherence is suboptimal across various cancers.
Methods
The objective of this study is to characterise clinician-perceived barriers and facilitators to cancer CPG adherence in Australia. Semi-structured interviews were conducted to collect data from 33 oncology-focused clinicians (surgeons, radiation oncologists, medical oncologists and haematologists). Clinicians were recruited in 2019 and 2020 through purposive and snowball sampling from 7 hospitals across Sydney, Australia, and interviewed either face-to-face in hospitals or by phone. Audio recordings were transcribed verbatim, and qualitative thematic analysis of the interview data was undertaken. Human research ethics committee approval and governance approval was granted (2019/ETH11722, #52019568810127).
Results
Five broad themes and subthemes of key barriers and facilitators to cancer treatment CPG adherence were identified: Theme 1: CPG content; Theme 2: Individual clinician and patient factors; Theme 3: Access to, awareness of and availability of CPGs; Theme 4: Organisational and cultural factors; and Theme 5: Development and implementation factors. The most frequently reported barriers to adherence were CPGs not catering for patient complexities, being slow to be updated, patient treatment preferences, geographical challenges for patients who travel large distances to access cancer services and limited funding of CPG recommended drugs. The most frequently reported facilitators to adherence were easy accessibility, peer review, multidisciplinary engagement or MDT attendance, and transparent CPG development by trusted, multidisciplinary experts. CPGs provide a reassuring framework for clinicians to check their treatment plans against. Clinicians want cancer CPGs to be frequently updated utilising a wiki-like process, and easily accessible online via a comprehensive database, coordinated by a well-trusted development body.
Conclusion
Future implementation strategies of cancer CPGs in Australia should be tailored to consider these context-specific barriers and facilitators, taking into account both the content of CPGs and the communication of that content. The establishment of a centralised, comprehensive, online database, with living wiki-style cancer CPGs, coordinated by a well-funded development body, along with incorporation of recommendations into point-of-care decision support would potentially address many of the issues identified.
Citation: Bierbaum M, Rapport F, Arnolda G, Delaney GP, Liauw W, Olver I, et al. (2022) Clinical practice guideline adherence in oncology: A qualitative study of insights from clinicians in Australia. PLoS ONE 17(12): e0279116. https://doi.org/10.1371/journal.pone.0279116
Editor: Anna Ugalde, Deakin University, AUSTRALIA
Received: March 21, 2022; Accepted: November 30, 2022; Published: December 16, 2022
Copyright: © 2022 Bierbaum et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the manuscript and the tables. Additional qualitative data cannot be made public because it describes participant experiences which are not de-identifiable and consent for release was not provided by study participants. The South West Sydney Local Health District Human Research Ethics Committee (HREC) provides oversight for the data collected, and by policy requires any use of this data to be directly approved by the HREC. For these reasons, data may only be made available upon request made to the Corresponding Author and the South West Sydney Local Health District HREC. Please direct data requests to the following non-author email at: SWSLHD-Ethics@health.nsw.gov.au.
Funding: MB is supported by an Australian government Research Training Program Scholarship stipend associated with the Australian Institute of Health Innovation, Macquarie University (ID:9100002). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. https://www.dese.gov.au/research-block-grants/research-training-program.
Competing interests: The authors have declared that no competing interests exist.
List of abbreviations: CPG, Clinical Practice Guidelines; COREQ, Consolidated Criteria for Reporting Qualitative Studies checklist; GP, General Practitioner; GRT, Guideline Recommended Treatment; H, Haematologists; i, interview number; LHD, Local Health District; MO, Medical Oncologists; NSLHD, North Sydney LHD; NSW, New South Wales, Australia; PBS, Pharmaceutical Benefits Scheme; RO, Radiation Oncologists; S, Surgeons; SES LHD, South-Eastern Sydney LHD; SWS LHD, South-Western Sydney; TA, Thematic Analys; TGA, Therapeutic Goods Administration; WSLHD, Western Sydney LHD; VMOs, Visiting Medical Officers
Background
The burden of cancer is large in Australia, with the number of new cases (excluding non-melanoma skin cancer) estimated to reach 150,782 in 2021[1] (population of 26 million people[2]). Clinical Practice Guidelines (CPGs) are designed to support clinical decision-making, based on the best evidence, reduce unwarranted clinical variation [3], minimise healthcare expenditure and improve care [4], however non-adherence to CPGs may be justifiable in various circumstances. Emerging literature in Australia indicates that cancer CPG adherence is associated with improved patient outcomes, resulting in increased survival rates [5,6]. However, across the Australian health system, less than 60% of care has been estimated to be adherent to CPGs [7].
Sub-optimal rates of adherence to cancer Guideline-Recommended Treatment (GRT) specifically, have been identified in Australia, across a variety of cancer streams [8,9]. For example, GRT was received by: just over half of the patients with cervical cancer in NSW (2005–2011) [10]; two-thirds of patients in SA (2000–2010) with stage C colon cancer, and nearly half of stage B and C rectal cancer patients [5]; two-thirds of selected patients in NSW (2006–2011) with Non-Small Cell Lung Cancer (NSCLC) [11,12]; and only one-third of patients in NSW with melanoma (2006–2007) [13]. Rates of GRT have been found to be underutilised across a variety of cancers in Australia [8] and internationally [14–21].
Factors that enhance CPG adherence
Dissemination strategies that enhance adherence to CPGs include: face-to-face [22–25] and web-based educational workshops [26], educational outreach programs [27–29], printed materials [22], computerised reminders [22,27] (particularly point-of-care decision support) [30,31], and support by local opinion leaders [32], particularly when used in combination [27]. Adapting CPGs to local contexts can also improve the acceptability of CPGs for the user [3]. Modern dissemination of CPGs has shifted to electronic formats [26], with CPGs now available on multiple platforms, including hand-held devices, wiki-based CPGs [33], and electronic decision-tools at the point-of-care [26]. Compared to printed formats, electronic formats potentially increase accessibility, enabling quicker updates with feedback, while nudging clinicians towards adhering to GRTs, such as appropriate antibiotic use and hand hygiene [34].
Clinician attitudes towards cancer CPGs
A recent systematic review [35] identified that globally, clinicians are generally positive about cancer-specific CPGs, however negative attitudes, and barriers to adherence, persist. Key barriers include concerns about: recency of evidence, cookbook medicine, the need to account for patient complexities, weak evidence, and side-effects associated with GRT, as well as patient treatment preferences, poor accessibility to CPGs, ingrained clinical practice habits and concerns that GRT will increase costs of healthcare [35].
The review also identified key factors that facilitated adherence to GRT including: adapting CPGs to local needs, endorsement from medical colleges and colleagues, educational sessions, MDT meetings, and access to the recommended medicines, as well as clinician agreement with CPGs [35]. CPGs were considered useful, convenient sources of information, and educational tools that support treatment decision making, assist clinicians in litigation issues, and were generally perceived to enhance patient care [35].
Effective Implementation of CPGs needs to take into account local requirements and characteristics of the health system [36]. Considering the range of adherence rates in Australia, it is important to develop our understanding of clinician attitudes towards cancer CPGs. The aim of this study was to examine in-depth, clinician attitudes towards and perceived barriers and facilitators to cancer CPG adherence, to inform implementation strategies for cancer CPGs in the future [37].
Methods
This manuscript reports the findings from an inductive, exploratory qualitative study, and conforms with the S1 Checklist [38]. This study was informed by the interdisciplinary framework developed by Gurses et al [39]. It encompasses the qualitative component of a multiphase sequential mixed-methods study [37,40]. The findings from these interviews will inform the quantitative data collection in the proceeding phase.
Ethics statement
Human research ethics committee approval was attained granted by the South Western Sydney Local Health District Human Research Ethics Committee, and Macquarie University Human Research Ethics Committee (2019/ETH11722, #52019568810127), as well as governance approval at each hospital site.
Recruitment and data collection
Clinicians who met the eligibility criteria (Box 1) and worked in one of 7 major hospitals offering cancer services across South-Western Sydney Local Health District (SWSLHD), South-Eastern Sydney LHD (SESLHD), Western Sydney LHD (WSLHD), and North Sydney LHD (NSLHD) were invited to participate in an interview; these four LHDs contain approximately half of the population of New South Wales (NSW), Australia [41]. As more than a quarter of all cancer services are located in NSW [42], these clinicians are expected to be representative of Australian cancer clinicians. Purposive sampling [43,44] was used to recruit interview participants, with promotional emails sent to targeted clinicians by key hospital contacts; snowball sampling was conducted with interviewees invited to pass study invitations to colleagues [43]. This approach ensured a targeted sample of clinicians from specific disciplines and of varying seniority, but preserved clinician autonomy by allowing self-selection to guide interview participation, in line with Australian ethical guidelines for research [45]. Each person who contacted the research team was sent a participant information sheet and consent form (PICF), which included details about the study aim and design, the qualifications of the interviewer and contact details for the study team. The PICF was signed before an interview commenced. Interviews were conducted between October 2019-January 2020.
The interview topic guide was piloted in interviews with three clinicians. Following analysis of pilot data, no amendments were made (see S1 Appendix). The remaining semi-structured interviews were conducted, and data from all interviews were included in the full analysis. No repeat interviews were conducted.
Interviews were conducted either over-the-phone or face-to-face in hospital, by the lead researcher (MB, BSc, MPH, PhD candidate), an experienced female qualitative researcher. The interviewer had no prior relationship with any interviewee. Interviews were approximately 30 minutes in duration. All participants were offered a gift voucher as a token of appreciation for their participation. All interviews were audio recorded, transcribed verbatim, and deidentified.
Data analysis
An iterative, inductive thematic analysis (TA) [46,47] approach was used to obtain insight into the experiences and perceptions of participating clinicians regarding adherence to cancer CPGs. This allowed patterns to emerge from the data, through re-reading and coding of the transcripts (by MB), establishing a deeper understanding of the data (Steps 1–3 of TA: Data familiarisation, generation of initial codes and theme searching) [48]. Themes were refined (Step 4 of TA: Theme review) [48], while reflexively examining the influence of the authors’ assumptions on data analysis [47], and acknowledging anticipated themes informed by a topical systematic review [35]. Recruitment and data analysis ceased once thematic saturation occurred and no new codes were identified [43]. Analysis was conducted using NVIVO version 12.4.0 [49]. The resulting coding framework was discussed during development (with FR), with iterative adjustments made to the themes and codes following discussion (Step 5 of TA: Theme definition and naming) [48]. This two coder technique enabled the corroboration of the thematic framework and for team consensus to be reached on the coding terminology [44]. The final framework was validated by FR who read and coded 5 interviews to ensure trustworthiness and methodological rigor [50] (see S2 Appendix). All remaining transcripts were then recoded (by MB) using the finalised thematic framework [44]. The frequency with which codes were identified across the interview transcripts, was calculated in order to identify how many clinicians raised each subtheme, giving an indication of whether attitudinal trends existed across disciplines [51].
‘Member checking’ was employed to enhance data credibility and minimise potential misinterpretation of data [44]. Following completion of thematic data analysis, a summary of the preliminary findings was sent to each participant, providing them with an opportunity to verify, reject or clarify researcher thematic interpretation of findings. Checking-back was considered important to minimise the potential for misinterpretation. Any clinician feedback would be returned to the study team for consideration and integrated into the final findings.
Results
Demographics
Thirty-three interviews were completed, including 3 pilot interviews. Most clinicians were aged 40–49 years (33.3%), practiced in SWSLHD (54.5%), and were staff specialists (75.8%). Breast cancer (30.3%) and Haematological cancers (30.3%) were the most common cancers the clinicians worked with. Half of the clinicians (51.5%) reported working in only one cancer stream and nearly half of the clinicians had commenced specialist practice within the preceding decade (2010–2019) (48.5%) (Table 1).
Response rate and member checking
Invitations were sent to 66 clinicians to participate in an interview, and an unknown number by snowballing; 35 clinicians contacted the study team, and of those, 33 clinicians completed the interview. Five clinicians responded to the invitation for member checking and provided confirmatory feedback. This limited feedback was positive and did not substantively change interpretation (5/33). The characteristics of the non-respondents are unknown.
Themes that emerged from the interviews
Five key themes with subthemes were identified during analysis of the interviews: CPG content; Individual clinician and patient factors; Access to, awareness of and availability of CPGs; Organisational and cultural factors; and CPG development and implementation factors (see S2 Appendix). Barriers and facilitators to CPG adherence were identified within each theme, and the proportion of clinicians who contributed to each of the subthemes are presented, according to their medical discipline (see Table 2). Clinicians were assigned a label based on their sequential interview number. Quotes representing each theme and subtheme are presented in Table 3.
Theme 1: CPG content
Subtheme 1.1: Applicability of recommendations to patient population
Barriers.
CPGs not catering for patient complexities such as comorbidities, performance status, age, or the ability to tolerate treatment, was a barrier to CPG adherence raised by many clinicians. When CPGs were not applicable to patients, clinicians made clinical judgements and modified CPG recommendations, tailoring treatment to individual needs, referred to as the art of medicine. It was unclear from the interviews whether these modifications would be considered warranted variation within the scope of the CPG or considered non-adherent.
A third of clinicians reported modifying CPG recommendations when concerned that treatments would not be well tolerated by patients, or when patients were perceived to be able to tolerate more aggressive treatment than the CPG recommends. Such modifications are not necessarily non-adherent, as some CPGs include recommendations for modifications for certain patient groups. When these modifications are made, they are often justified and approved through peer review or in MDT meetings, recorded in electronic patient records, and in letters back to General Practitioners (GPs) and patients. One common justification for modifications, was that the evidence underpinning CPGs was gathered from clinical trials comprised of patient cohorts who are generally healthier and younger than patients being seen by clinicians, reducing the applicability of the CPGs.
Facilitators.
Locally adapted or Australian CPGs provide context-specific information and were seen to be more likely adhered to. CPGs reflective of peer-accepted practice were considered useful as were CPGs that provide options to modify recommendations for specific patient populations.
Half of the clinicians commented that CPG adherence was a good measure of quality of care, indicating where practice variation lies, and possible reasons for variation, so long as the guideline was up-to-date, noting that a lack of adherence must be interpreted carefully. Many clinicians found that CPGs create a coherent framework within which to discuss patients, and this is particularly useful for decision making around complex cases, for unfamiliar clinical scenarios, less common cancers, or for new treatments. CPGs also provide reassurance for junior clinicians, and for busy clinicians working with a cancer with which they are less familiar.
CPGs help clinicians reach consensus in borderline cases, particularly when there is debate over the order of treatment modality. They provide a reassuring framework for clinicians to check their treatment plans against, and are generally seen as helpful, educational tools, that reduce clinical variation and improve patient care.
Subtheme 1.2: Degree of evidence and level of agreement with evidence underpinning CPGs
Barriers.
Many clinicians discussed how CPG adherence is limited when the evidence base is still emerging. In this case, when recommendations are expert consensus based, clinicians prefer to rely on their own clinical judgement, which may result in low CPG adherence. Similarly, when patient survival outcomes are good, regardless of the treatment provided, higher practice variation results. Adherence is also limited in areas with rapidly changing evidence, especially when emerging evidence indicates better outcomes for patients than current GRT. A lack of agreement with the interpretation of evidence underpinning the CPG was a barrier to adherence, particularly if the evidence is controversial or various CPGs provide different recommendations.
Subtheme 1.3: Format, ease of use and references to evidence
Barriers.
The format of CPGs was considered important, with some CPGs being difficult to navigate if they are too complex. CPGs that do not include references and justifications for recommendations, or explicitly state whether recommendations are based on evidence or expert opinion, were also poorly regarded.
Facilitators: Important content factors included CPGs having a good lay out, being easy to read and user friendly, being comprehensive, and including multiple treatment options. Inclusion of information on side effects was considered useful for clinicians to reference when making treatment decisions and monitoring patients.
Provision of schedule and dose information provides assurance for clinicians that they are practicing appropriately and accurately, especially if working across multiple cancer streams. Inclusion of patient resources within the CPG was also an important component for CPGs, as they help to increase treatment decision transparency, and aid communication when discussing treatment plans with patients. Inclusion of concise summaries of evidence with references, that highlight the level of evidence that recommendations are based on, and whether the evidence is controversial or consensus based were highly valued.
Subtheme 1.4: How up-to-date CPGs are
Barriers: Most clinicians noted that one of the main barriers to adherence was that CPGs are often outdated. Many also suggested that not receiving notifications regarding CPG updates was a barrier.
Facilitators: CPGs being updated regularly with notifications about CPG updates from colleges, colleagues or CPG developers were considered facilitating factors for adherence.
Subtheme 1.5: Prescriptiveness of CPG recommendations
Barriers: CPG content being too broad and not detailed enough for complex cases, too rigid, not taking account of emerging evidence, or containing conservative recommendations, were considered barriers to adherence. CPGs often have clear treatment options for first-line treatment but were criticised for having less clarity for second and third-line treatment options due to a lack of evidence, leading to practice variation.
Theme 2: Individual clinician and patient factors
Subtheme 2.1: Clinician personality, and the impact of CPGs on autonomy
Barriers: Multiple clinicians highlighted that CPGs are guides, or frameworks, that support decision making, but require clinicians to apply clinical judgement when making clinical decisions, reinforcing that CPG recommendations should not be considered rules to which clinicians should strictly adhere.
Clinicians reported that the personalities or hubris of influential clinicians can act as barriers to adherence, with strong personalities influencing treatment decisions in MDTs. Clinicians suggested that individual clinical equipoise can impede clinician acceptance of new evidence-based treatment options, and many noted that as subject experts they no longer needed to regularly refer to CPGs.
Facilitators: A positive sentiment captured by clinicians (including a registrar), was that CPGs enable junior clinicians to have more autonomy, as it provides them with an independent mechanism to confirm treatment plans.
Subtheme 2.2: Generational and disciplinary differences in perceptions towards CPGs
Barriers: Generational differences in clinician attitudes and use of CPGs was raised, with CPGs being considered less helpful for experienced clinicians, who may be less inclined to refer to CPGs, compared to junior clinicians. Junior clinicians’ practice was also perceived to be influenced by the preferences of senior clinicians, potentially acting as a barrier to adherence.
Clinicians also raised concerns that clinicians can be biased toward their own discipline, or financially incentivised by fee-for-service, to independently complete treatment with patients rather than engage in CPG-adherent multidisciplinary care.
Subtheme 2.3: Litigation concerns
Barriers: Clinicians raised concerns that following guidelines, due to apprehension about litigation for non-adherent practice, could lead to patients not receiving the best practice.
Facilitators. Possible litigation (although rare) was a strong incentive for clinicians to adhere to CPGs, encouraging clinicians to justify and communicate treatment decisions clearly, and providing assurance and medicolegal protection that clinicians are practicing according to the evidence.
Subtheme 2.4: Patient age, comorbidities, preferences and logistics
Barriers.
Clinician concern about patients’ older age, frailty, fitness, performance status, comorbidities, contraindications, and organ impairment, can all act as barriers towards CPG adherence. Clinician concern about toxicity or potential side effects of a treatment were also seen as barriers, including concern about how patient treatment history may affect future treatment tolerability (for example, past radiation on present treatment plans).
Similarly, patient preference, and concern about side effects, toxicity, and treatment tolerability can also impede receipt of CPG adherent care, with some patients rejecting treatment plans based on anecdotal experiences of friends and family receiving treatments. Geographic challenges and the logistics of patients travelling long distances to access treatments also contributes to lower CPG adherence, necessitating alterations to treatment schedules.
Theme 3: Awareness of, access to and availability of CPGs
Barriers
Clinicians commented that CPGs can be hard to access, especially if published in a journal that is not open access, or on a website that requires clinicians to login (as passwords are often forgotten). Poor Wi-Fi access and internet site restrictions in hospitals can limit real time access to CPGs. Several clinicians indicated that there weren’t many (if any) local Australian CPGs available in their field, particularly for rare cancers while often international CPGs were not applicable locally. Clinicians observed that other clinicians’ limited awareness of CPGs or limited knowledge of where to access them acted as barriers to adherence.
Facilitators
Clinicians felt that easy access to guidelines facilitated use and adherence. CPGs that were available electronically or via phone applications (apps) were easier to access, as were those published in open access journals or published in a peer-reviewed, reputable journal, and free to download. Availability of CPGs on websites or apps that required no password was considered a facilitator. Some clinicians expressed a preference for local CPGs, or protocols produced by their hospital departments. Others preferred international CPGs, as they tend to be more frequently updated. All clinicians said they were aware of CPGs in their field, an important facilitator of adherence. It is important, however, to remain cognisant that CPG awareness doesn’t necessarily translate to adherence.
Theme 4: Organisational and cultural factors
Subtheme 4.1: Access to treatments recommended by CPGs, resource availability and clinician time
Barriers.
Limited access to resources such as drugs and technology impacts adherence. In Australia, this occurs when international CPGs recommend drugs that are not approved by the Therapeutic Goods Administration (TGA) or funded by the Pharmaceutical Benefits Scheme (PBS) (Australia’s approval authorities), limiting their availability, and increasing costs. In these situations, clinicians weigh up the cost-benefit of international CPG-adherent treatments. High clinician workload, limited staffing, and lack of clinician time were also regarded as barriers to CPG adherence.
Facilitators
Clinicians explained that when a CPG-recommended drug is not approved or funded in Australia, some access schemes operated by pharmaceutical companies or Local Health Districts, enable patients to receive those drugs. Organisational support and provision of adequate resources were seen to facilitate CPG adherence. The availability of care coordination for scans and treatment, as well as the infrastructure and use of flexible home-based treatment for geographically isolated patients were also seen as facilitating factors.
CPGs were perceived to save clinicians’ time by concisely summarising the evidence and were considered a better alternative than clinicians searching through the literature independently, so long as they are up-to-date. Clinicians suggested that regular meetings to discuss CPGs, protocols, and practices, and the purposeful hospital provision of protected time for clinicians to read, discuss and contribute to CPGs and the literature encouraged CPG adherence.
Subtheme 4.2: A culture of peer or multidisciplinary review of treatment plans
Barriers.
Limited access to peer review or multidisciplinary review of treatment plans for private practicing clinicians and rural and regionally practicing clinicians, and poor multidisciplinary engagement or poor MDT attendance, were seen to contribute to lower CPG adherence. Clinicians noted that peer review occurs less frequently for common cancers.
Facilitators.
Multidisciplinary engagement or MDT attendance, and a culture of valuing multidisciplinary care was seen to facilitate CPG adherence reinforcing how important peer review of treatment decisions was. CPG-focused clinician training was seen to produce clinicians more inclined to adhere to CPGs.
Clinical leadership that encourages CPG adherence, a culture of error reporting, and documenting treatment decisions facilitate adherence. Several clinicians commented that peer expectation to adhere to CPGs was an influential factor, as was fear of looking negligent if non-adherent. Good relationships between multidisciplinary teams, teamwork and timely peer support were also seen as important facilitating factors.
Subtheme 4.3: Referral pathways
Barriers.
Incomplete patient referral pathways were flagged as a potential barrier to CPG adherent care, particularly if patients receive treatment (such as surgery) prior to MDT presentation, potentially preventing multi-modality GRT from being delivered in the recommended sequence. Similarly, a lack of awareness by GPs (and patients) of the importance of multidisciplinary review was considered a barrier, as it can limit referrals to multidisciplinary clinicians.
Theme 5: Development and implementation factors
Subtheme 5.1: Development, adaptations, and review of CPGs by an expert development committee
Barriers.
When CPGs are perceived to be biased toward a particular modality of treatment, by development committee or individual member agendas (with biased weighting of evidence), or by pharmaceutical company influence on the development committee, this was a barrier to adherence. Clinicians also acknowledged that the development, updating, and maintenance of CPGs was seen as a slow and difficult process.
Subtheme 5.2: CPG dissemination and implementation strategies
Barriers.
Several clinicians felt that audits of adherence rates do not accurately reflect the reasons for modifying CPGs, or take individual patient needs into account, highlighting that low CPG adherence may reflect a poor-quality CPG.
Facilitators.
Endorsement of CPGs, and education sessions provided by trusted and well-known organisations such as tumour groups were seen to increase clinician awareness and adherence. Similarly, effective marketing and distribution, publication in high quality journals, and discussion at conferences increase awareness and facilitate adherence. Several clinicians commented that clinical audits, and incorporation of CPGs into point-of-care electronic decision tools nudge clinicians towards adhering to CPGs.
Subtheme 5.3: Future CPG development and implementation improvements
CPG development should involve broader clinician input, with wider consultation outside of the working group. Junior clinician involvement in the development process was suggested with the incentive of CPG authorship, as was continuing professional development points, or financial incentives.
Adapting international CPGs to local Australian needs was recommended. This could be coordinated by a nationally resourced, centralised, and trusted CPG development body with access to good infrastructure, for quick and efficient CPG development. Development of a comprehensive centralised online cancer CPG database was proposed, that incorporates a dynamic and living wiki-style process of updating provisional CPGs, an extension of the already well-respected CCA Wiki platform, and the online Australian eviQ protocol database. Clinicians could register to receive automatic alerts about CPG updates.
CPG development should incorporate more real-world data (such as registry data) to bridge gaps in CPGs where clinical trial evidence is lacking, and to support consensus-based recommendations. Clinicians suggested that future CPGs should include treatment sequencing algorithms (e.g., decision trees and flow charts).
Frequency analysis
The frequency analysis highlighted that the most commonly reported barriers to cancer CPG adherence were when CPGs do not cater for patient complexities (25/33), were slow to be updated (23/33), or underpinned by rapidly changing evidence (19/33). Patient treatment preferences (21/33), as well as clinician concern about patients’ older age, performance status, comorbidities, and contraindications (13/33), limited availability of CPG recommended drugs (19/33), and limited access to peer review or multidisciplinary review of treatment plans (15/33) were also frequently reported barriers.
The most commonly reported facilitators to cancer CPG adherence were the perspective that CPGs provide a reassuring framework for clinicians to check their treatment plans against (24/33). Multidisciplinary engagement, or MDT attendance (24/33), easy access to guidelines (19/33), and possible litigation (18/33) were commonly reported facilitators of adherence, as were transparent CPG development by trusted and respected experts (16/33), regular CPG updates (16/33), and peer review of treatment decisions (15/33). The provision of a concise summary of evidence that includes justifications and reference to the clinical trials underpinning recommendations (15/33) was also frequently reported.
Broader clinician consultation and input, with international collaboration to develop CPGs (16/33) and a nationally resourced, centralised CPG development body with access to good infrastructure (12/33) were also common recommendations for future improvements. No disciplinary trends in attitudes were identified, and the themes were present during interviews with MOs, ROs, Haematologists and Surgeons.
Discussion
The study examined clinician attitudes towards and determinants (perceived barriers and facilitators) of cancer CPG adherence, with the intention of informing future implementation strategies for cancer CPGs. A range of barriers and facilitators to cancer CPG adherence were identified from this study, some of which appear to be unique to the Australian context when compared to a recent systematic review of international barriers and facilitators[35]. While noting these factors, it is important to remain cognisant of the plethora of valid reasons to make warranted variations from CPG recommendations including: patient preference; the non-applicability of recommendations to complex patients; and CPGs underpinned by weak evidence or consensus.
Lack of applicability of CPGs was seen to result from CPGs not catering for patient complexities, a universal CPG adherence issue [52], as CPGs are often underpinned by evidence from clinical trials comprised of patients who are unrepresentative of real-world populations. Instead, trial cohorts are often restricted to a subset of fitter patients, with lower risk profiles, often excluding patients based on age, organ function and lack of comorbidities [53–55]. Patient age [10,11,56–58] and comorbidities [56,58–62] are factors independently associated with cancer CPG non-adherence. This observation reflects the challenges in developing CPGs, with the work-as-done (CPG adoption and utilisation) being vastly different from the work-as-imagined by the CPG development group [63]. These issues could be addressed with greater utilisation of evidence reflective of real-world patients, including observational studies [64], to guide CPG development. In addition, incentives are needed to encourage broader eligibility criteria in industry-financed randomised trials, and to promote and facilitate post-marketing trials for patient groups not covered by industry-funded trials, in part to confirm important clinical conclusions arrived at by observational research.
Guidelines are designed to standardise practice [3], and improve care [4], but the complexity of oncological treatment decisions necessitates flexibility and reflexivity by the clinician to deliver patient-centred care [65]. Cancer care is becoming increasingly more complex, translating into lengthy and multifaceted CPGs being developed, potentially influencing adherence [66]. Concern about the evidence underpinning CPGs is considerable, with a recent Australian study indicating that 18% of CPG recommendations across a variety of conditions are based on level 1 evidence, while 19% were consensus-based [67]. This links to concerns about CPGs being biased [68]. Explicit CPG declaration of committee member medical discipline and biases, and industry funding [68,69] may help to overcome these concerns.
Limited availability of Australian CPGs was discussed as a barrier to CPG adherence, specifically, when international CPGs don’t apply to the Australian context. This was reported as a significant issue when CPG-recommended drugs aren’t approved by the TGA or publicly funded by the PBS in Australia, restricting access to and affordability of GRTs. Prescription of off-label anticancer medication (drugs not approved by the TGA for particular clinical scenarios) is high in Australia, with up to 85% of cancer patients receiving off-label medication, many underfunded by the PBS [70].
This study identified a perceived difference in CPG adherence between clinicians practicing in rural and metropolitan areas. Rural and remote Australian cancer services face unique logistical challenges (e.g. treating remote patients who travel hours to access services), contributing to disparities and inequalities in healthcare for a quarter of the Australian population who live outside of major cities [71]. Rural cancer patients have significantly higher mortality [72,73] and a lower likelihood of receiving GRT [12,73]. The lower survival rates are attributed in part to large distances travelled by patients, delayed diagnosis and treatment times [74], and an undersupply of oncology specialists and treatment services [72,75] necessitating patients to travel to metropolitan centres for treatment [76–78]. Modification of these patients’ cancer care, as a result of these geographical challenges, may impact CPG adherence. Telemedicine is one strategy that aims to reduce these disparities [79], as well as shared care between oncologists and General Practitioners (GPs) [75].
These issues are compounded by limited access to peer review or multidisciplinary collaboration for rural clinicians. Attendance or engagement with MDTs [80] and peer review of treatment decisions increases CPG adherence [81] and is associated with improved patient survival rates [61,82]. This teamwork, along with good collegial relationships, a culture of valuing multidisciplinary care, and peer expectation to be adherent were also perceived facilitators for CPG adherence.
MDTs often facilitate referral of patients for multidisciplinary treatment [83]. Failure to refer patients to consult with clinicians from multiple disciplines, however, was a perceived barrier to CPG adherence that limits the opportunity for patients to receive multimodality GRT in the recommended sequence. GPs often refer patients to surgeons within their existing networks [84], potentially due to limited awareness of the importance of multidisciplinary review by GPs and patients. Lack of familiarity with other treatment modalities [85] and concerns about treatment side effects can also limit referrals for radiation oncology [86,87]. Treatment patterns have been found to vary widely for prostate cancer patients in Australia, for example, depending on whether patients were referred to a radiation oncologist (RO) as well as a surgeon [88] with fewer than 14% consulting with an RO prior to surgery [89]. Addressing these referral issues requires a systems-level focus, to define and promote optimal referral pathways, rather than relying on individual GPs to appropriately refer patients to multidisciplinary care, as they typically see relatively few new cancer diagnoses each year. CCA Optimal Care Pathway documents provide support for GPs to navigate the patient journey, and often recommend referral to MDTs [90], while clinicians who attend MDTs are listed on CanRefer, an online directory of oncology specialists in NSW [91]. However, more evidence is needed to understand referral patterns in Australia and associated barriers.
Perceived difference in CPG adherence between junior and senior clinicians was identified as an issue across multiple health conditions [92,93]. Differences across cancer disciplines were also discussed, with a disciplinary bias perceived to prevent some clinicians from engaging in multidisciplinary care, potentially influenced by a fee-for-service model within some Australian cancer care services. These observations highlighting clinical hierarchies and tribalism are unlikely to reflect differences between individuals, and instead represent the broader impact of the clinical culture of hospitals on clinician behaviour [94].
Implications for research and clinical practice
Future development and implementation of cancer CPGs in Australia should utilise the facilitators of CPG adherence identified in this study. CPGs need to be frequently updated, easily accessible, provide treatment modification options, and include a concise summary of evidence with justifications referencing the evidence. Strategies should incorporate audit and feedback strategies [27,95,96], along with education-based strategies, reminders regarding CPG updates [97], and incorporation of CPG recommendations into real-time point-of-care decision support [98]. Effective implementation strategies need to consider both the CPG content and communication of that content [99].
The establishment of a centralised, trusted, and well-funded CPG development body, akin to CCA, to produced CPGs in a transparent and systematic manner is recommended. In addition, the development of an online CPG database is recommended, that provides a comprehensive range of cancer CPGs either locally developed or adapted from international CPGs. These CPGs can be frequently updated through the use of a wiki-like process, extending the existing and well-regarded CCA wiki-platform, which enables ongoing consultation, review of the literature, and automatic updates of content [33]. As clinicians report difficulties with time, it is important that protected non-clinical time be allocated to allow clinicians to participate in the crucial work of CPG development and update.
Strengths and limitations
Strengths of this study include the use of multiple coders, member checking and triangulation of data from participants from different disciplines and hospitals across Sydney, Australia. While it is acknowledged that member checking can be perceived as a limitation, in this instance, responding participants confirmed the thematic interpretation, and provided no conflicting comments [44]. Limitations of this study include participant self-selection bias, potentially recruiting respondents who feel particularly positively or negatively towards guidelines. The characteristics of the invited non-respondents are unknown, potentially introducing bias. The member checking process was delayed due to restricted access to hospital staff as a result of COVID-19 and was conducted in March 2021. No response rate was calculated due to the snowball element of recruitment. Similarly, the sample was limited to four disciplines of clinicians who treat cancer patients, potentially excluding the views of other clinicians involved in the patient pathway, such as clinicians who provide supportive care, palliative care, or GPs who help patients navigate their cancer journey. The cohort of participants were also typically staff specialists, from SWSLHD in the first 10 years of their career, who likely work with complex cases that are typically poorly addressed by CPGs. Only one Fellow and one Registrar participated in the study, resulting in limited observations from those groups of clinicians. Only clinicians working in NSW were interviewed, and no clinicians who work exclusively in private practice or in rural centres were included.
Conclusion
This study has identified perceived barriers and facilitators specific to cancer CPG adherence that contribute to variation from cancer-CPG recommendations across a variety of cancer streams in Australia. This research will guide the implementation of future cancer CPGs, by informing strategies that target these factors, to enhance implementation of high-quality evidence into practice.
Supporting information
S1 Checklist. COREQ (COnsolidated criteria for REporting Qualitative research) checklist.
https://doi.org/10.1371/journal.pone.0279116.s001
(PDF)
S1 Appendix. Appendix A: Interview topic guide.
https://doi.org/10.1371/journal.pone.0279116.s002
(DOCX)
References
- 1.
Australian Institute of Health and Welfare. Cancer in Australia 2021. Canberra: AIHW; 2021.
- 2.
Australian Bureau of Statistics. Population clock Canberra: ABS; 2022. Available from: https://www.abs.gov.au/.
- 3. Harrison MB, Légaré F, Graham ID, Fervers B. Adapting clinical practice guidelines to local context and assessing barriers to their use. Canadian Medical Association Journal. 2010;182(2):E78–E84. pmid:19969563
- 4. Pronovost P. Enhancing physicians’ use of clinical guidelines. JAMA. 2013;310(23):2501–2. pmid:24310916
- 5. Adelson P, Fusco K, Karapetis C, Wattchow D, Joshi R, Price T, et al. Use of guideline‐recommended adjuvant therapies and survival outcomes for people with colorectal cancer at tertiary referral hospitals in South Australia. Journal of Evaluation in Clinical Practice. 2018;24(1):135–44. pmid:28474459
- 6. Hanna T, Shafiq J, Delaney G, Vinod S, Thompson S, Barton M. The population benefit of evidence-based radiotherapy: 5-year local control and overall survival benefits. J Radiotherapy Oncology. 2018;126(2):191–7. pmid:29229506
- 7. Braithwaite J, Hibbert PD, Jaffe A, White L, Cowell CT, Harris MF, et al. Quality of health care for children in Australia, 2012–2013. JAMA. 2018;319(11):1113–24. pmid:29558552
- 8. Delaney G, Jacob S, Featherstone C, Barton M. The role of radiotherapy in cancer treatment: estimating optimal utilization from a review of evidence‐based clinical guidelines. Cancer: Interdisciplinary International Journal of the American Cancer Society. 2005;104(6):1129–37. pmid:16080176
- 9. Kang Y-J, O’Connell DL, Tan J, Lew J-B, Demers A, Lotocki R, et al. Optimal uptake rates for initial treatments for cervical cancer in concordance with guidelines in Australia and Canada: Results from two large cancer facilities. J Cancer Epidemiology. 2015;39(4):600–11. pmid:26004990
- 10. Chiew KL, Chong S, Duggan KJ, Kaadan N, Vinod SK. Assessing guideline adherence and patient outcomes in cervical cancer. Asia‐pacific Journal of Clinical Oncology. 2017;13(5):e373–e80. pmid:27726297
- 11. Duggan KJ, Descallar J, Vinod SK. Application of guideline recommended treatment in routine clinical practice: a population-based study of stage I–IIIB non-small cell lung cancer. Clinical Oncology. 2016;28(10):639–47. pmid:27211609
- 12. Vinod SK, O’Connell DL, Simonella L, Delaney GP, Boyer M, Peters M, et al. Gaps in optimal care for lung cancer. Journal of Thoracic Oncology. 2008;3(8):871–9. pmid:18670305
- 13. Varey AH, Madronio CM, Cust AE, Goumas C, Mann GJ, Armstrong BK, et al. Poor adherence to national clinical management guidelines: a population-based, cross-sectional study of the surgical management of melanoma in New South Wales, Australia. Annals of Surgical Oncology. 2017;24(8):2080–8. pmid:28547563
- 14. Ng W, Jacob S, Delaney G, Do V, Barton M, practice. Estimation of an optimal chemotherapy utilisation rate for upper gastrointestinal cancers: setting an evidence-based benchmark for the best-quality cancer care. J Gastroenterology Research. 2015. pmid:25883645
- 15. Chagpar R, Xing Y, Chiang Y-J, Feig BW, Chang GJ, You YN, et al. Adherence to stage-specific treatment guidelines for patients with colon cancer. Journal of Clinical Oncology. 2012;30(9):972. pmid:22355049
- 16. Eldin NS, Yasui Y, Scarfe A, Winget M. Adherence to treatment guidelines in stage II/III rectal cancer in Alberta, Canada. J Clinical Oncology. 2012;24(1):e9–e17. pmid:21802914
- 17. Gagliardi G, Pucciarelli S, Asteria C, Infantino A, Romano G, Cola B, et al. A nationwide audit of the use of radiotherapy for rectal cancer in Italy. J Techniques in Coloproctology. 2010;14(3):229–35. pmid:20632061
- 18. Dronkers EA, Mes SW, Wieringa MH, van der Schroeff MP, de Jong RJB. Noncompliance to guidelines in head and neck cancer treatment; associated factors for both patient and physician. J BMC cancer. 2015;15(1):1–10. https://doi.org/10.1186/s12885-015-1523-3.
- 19. Fong A, Ng W, Barton MB, Delaney GP. Estimation of an evidence-based benchmark for the optimal endocrine therapy utilization rate in breast cancer. The Breast. 2010;19(5):345–9. pmid:20223666
- 20. Fong A, Shafiq J, Saunders C, Thompson A, Tyldesley S, Olivotto IA, et al. A comparison of systemic breast cancer therapy utilization in Canada (British Columbia), Scotland (Dundee), and Australia (Western Australia) with models of “optimal” therapy. The Breast. 2012;21(4):562–9. pmid:22297168
- 21. Fong A, Shafiq J, Saunders C, Thompson AM, Tyldesley S, Olivotto IA, et al. A comparison of surgical and radiotherapy breast cancer therapy utilization in Canada (British Columbia), Scotland (Dundee), and Australia (Western Australia) with models of “optimal” therapy. The Breast. 2012;21(4):570–7. pmid:22425535
- 22. Flodgren G, Hall AM, Goulding L, Eccles MP, Grimshaw JM, Leng GC, et al. Tools developed and disseminated by guideline producers to promote the uptake of their guidelines. J Cochrane Database of Systematic Reviews. 2016;(8). pmid:27546228
- 23. Giguère A, Zomahoun HTV, Carmichael P-H, Uwizeye CB, Légaré F, Grimshaw JM, et al. Printed educational materials: effects on professional practice and healthcare outcomes. J Cochrane Database of Systematic Reviews. 2020;(8). https://doi.org/10.1002/14651858.CD004398.pub4.
- 24. Grimshaw JM, Eccles MP, Lavis JN, Hill SJ, Squires JE. Knowledge translation of research findings. Implementation science. 2012;7(1):1–17. pmid:22651257
- 25. Forsetlund L, Bjørndal A, Rashidian A, Jamtvedt G, O’Brien MA, Wolf FM, et al. Continuing education meetings and workshops: effects on professional practice and health care outcomes. J Cochrane Database of Systematic Reviews. 2009;(2). pmid:19370580
- 26. De Angelis G, Davies B, King J, McEwan J, Cavallo S, Loew L, et al. Information and communication technologies for the dissemination of clinical practice guidelines to health professionals: a systematic review. JMIR Medical Education. 2016;2(2):e6288. pmid:27903488
- 27. Fretheim A, Oxman AD, Håvelsrud K, Treweek S, Kristoffersen DT, Bjørndal A. Rational prescribing in primary care (RaPP): a cluster randomized trial of a tailored intervention. PLoS Medicine. 2006;3(6):e134. pmid:16737346
- 28. O’Brien MA, Rogers S, Jamtvedt G, Oxman AD, Odgaard‐Jensen J, Kristoffersen DT, et al. Educational outreach visits: effects on professional practice and health care outcomes. Cochrane Database of Systematic Reviews. 2007;(4). pmid:17943742
- 29. Olver I, von Dincklage J, Nicholson J, Shaw T. Improving uptake of wiki‐based guidelines with Qstream education. Medical Education. 2016;50(5):590–1. pmid:27072480
- 30. Shojania KG, Jennings A, Mayhew A, Ramsay CR, Eccles MP, Grimshaw J. The effects of on‐screen, point of care computer reminders on processes and outcomes of care. J Cochrane database of Systematic Reviews. 2009;(3). https://doi.org/10.1002/14651858.CD001096.pub2.
- 31. Gill JM, Mainous AG, Koopman RJ, Player MS, Everett CJ, Chen YX, et al. Impact of EHR-based clinical decision support on adherence to guidelines for patients on NSAIDs: a randomized controlled trial. The Annals of Family Medicine. 2011;9(1):22–30. pmid:21242557
- 32. Flodgren G, O’Brien MA, Parmelli E, Grimshaw JM. Local opinion leaders: effects on professional practice and healthcare outcomes. J Cochrane Database of Systematic Reviews. 2019;(6). pmid:31232458
- 33. Neuhaus S, Thomas D, Desai J, Vuletich C, Von Dincklage J, Olver I. Wiki-based clinical practice guidelines for the management of adult onset sarcoma: a new paradigm in sarcoma evidence. Sarcoma. 2015;2015. pmid:25784832
- 34. Lamprell K, Tran Y, Arnolda G, Braithwaite J. Nudging clinicians: a systematic scoping review of the literature. Journal of Evaluation in Clinical Practice. 2021;27(1):175–92. pmid:32342613
- 35. Bierbaum M, Rapport F, Arnolda G, Nic Giolla Easpaig B, Lamprell K, Hutchinson K, et al. Clinicians’ attitudes and perceived barriers and facilitators to cancer treatment clinical practice guideline adherence: a systematic review of qualitative and quantitative literature. Implementation Science. 2020;15:1–24. https://doi.org/10.1186/s13012-020-00991-3.
- 36. Wang Z, Norris SL, Bero L. The advantages and limitations of guideline adaptation frameworks. Implementation Science. 2018;13(1):1–13. https://doi.org/10.1186/s13012-018-0763-4.
- 37. Bierbaum M, Braithwaite J, Arnolda G, Delaney GP, Liauw W, Kefford R, et al. Clinicians’ attitudes to oncology clinical practice guidelines and the barriers and facilitators to adherence: a mixed methods study protocol. BMJ Open. 2020;10(3):e035448. pmid:32205377
- 38. Tong A, Sainsbury P, Craig J. Consolidated criteria for reporting qualitative research (COREQ): a 32-item checklist for interviews and focus groups. International Journal for Quality in Health Care. 2007;19(6):349–57. pmid:17872937
- 39. Gurses AP, Marsteller JA, Ozok AA, Xiao Y, Owens S, Pronovost PJ. Using an interdisciplinary approach to identify factors that affect clinicians’ compliance with evidence-based guidelines. Critical Care Medicine. 2010;38:S282–S91. pmid:20647785
- 40. Fetters MD, Curry LA, Creswell JW. Achieving integration in mixed methods designs—principles and practices. Health Services Research. 2013;48(6pt2):2134–56. pmid:24279835
- 41.
NSW Department of Planning Industry and Environment. 2016 New South Wales State and Local Government Area Population Projections. In: Department of Planning Industry and Environment, editor. Sydney, NSW2016.
- 42. Hunter J, Smith C, Delaney GP, Templeman K, Grant S, Ussher JM. Coverage of cancer services in Australia and providers’ views on service gaps: findings from a national cross-sectional survey. BMC Cancer. 2019;19(1):1–11. https://doi.org/10.1186/s12885-019-5649-6.
- 43. Teddlie C YF. Mixed methods sampling: A typology with examples. Journal of Mixed Methods Research. 2007;1(1):77–100. https://doi.org/10.1177/1558689806292430.
- 44. Barbour RS. Checklists for improving rigour in qualitative research: a case of the tail wagging the dog? BMJ. 2001;322(7294):1115–7. pmid:11337448
- 45.
The National Health and Medical Research Council. National Statement on Ethical Conduct in Human Research In: Commonwealth of Australia, editor. Canberra 2007 (Updated 2018).
- 46.
Braun V, Clarke V. Successful qualitative research: A practical guide for beginners. London, UK: Sage; 2013.
- 47. Srivastava P, Hopwood N. A practical iterative framework for qualitative data analysis. International Journal of Qualitative Methods. 2009;8(1):76–84. https://doi.org/10.1177/160940690900800107.
- 48. Braun V, Clarke V. Using thematic analysis in psychology. Qualitative research in psychology. 2006;3(2):77–101. https://doi.org/10.1191/1478088706qp063oa.
- 49.
QSR International Pty Ltd. NVIVO version 12. 2020.
- 50. O’Brien BC, Harris IB, Beckman TJ, Reed DA, Cook DA. Standards for reporting qualitative research: a synthesis of recommendations. Academic Medicine. 2014;89(9):1245–51. pmid:24979285
- 51.
Joffe H, Yardley L. Content and thematic analysis. In: Marks D, Yardley L, editors. Research methods for clinical health psychology. 56: SAGE Publications; 2004. p. 56–68.
- 52. Djulbegovic B, Guyatt GH. Progress in evidence-based medicine: a quarter century on. The Lancet. 2017;390(10092):415–23. pmid:28215660
- 53. Tang M, Pearson S-A, Schaffer AL, Lewis CR, John T, Simes RJ, et al. Are clinical trial eligibility criteria representative of older patients with lung cancer? A population-based data linkage study. Journal of Geriatric Oncology. 2021. pmid:34119452
- 54. Hamaker ME, Stauder R, van Munster BC. Exclusion of older patients from ongoing clinical trials for hematological malignancies: an evaluation of the National Institutes of Health Clinical Trial Registry. The Oncologist. 2014;19(10):1069. pmid:25170014
- 55. Kennedy-Martin T, Curtis S, Faries D, Robinson S, Johnston J. A literature review on the representativeness of randomized controlled trial samples and implications for the external validity of trial results. Trials. 2015;16(1):1–14. pmid:26530985
- 56. Vinod SK, Sidhom MA, Gabriel GS, Lee MT, Delaney GP. Why do some lung cancer patients receive no anticancer treatment? Journal of Thoracic Oncology. 2010;5(7):1025–32. pmid:20453689
- 57. Young JM, Leong DC, Armstrong K, O’Connell D, Armstrong BK, Spigelman AD, et al. Concordance with national guidelines for colorectal cancer care in New South Wales: a population‐based patterns of care study. MJA. 2007;186(6):292–5. pmid:17371209
- 58. Wah W, Stirling RG, Ahern S, Earnest A. Association between Receipt of Guideline-Concordant Lung Cancer Treatment and Individual-and Area-Level Factors: A Spatio-Temporal Analysis. Cancer Epidemiology Prevention Biomarkers. 2020;29(12):2669–79. pmid:32948632
- 59. Shekelle P, Woolf S, Grimshaw JM, Schünemann HJ, Eccles MP. Developing clinical practice guidelines: reviewing, reporting, and publishing guidelines; updating guidelines; and the emerging issues of enhancing guideline implementability and accounting for comorbid conditions in guideline development. Implementation Science. 2012;7(1):1–7. https://doi.org/10.1186/1748-5908-7-62.
- 60. Beckmann KR, Bennett A, Young GP, Roder DM. Treatment patterns among colorectal cancer patients in South Australia: a demonstration of the utility of population‐based data linkage. Journal of Evaluation in Clinical Practice. 2014;20(4):467–77. pmid:24851796
- 61. Boxer MM, Duggan KJ, Descallar J, Vinod SK. Do patients discussed at a lung cancer multidisciplinary team meeting receive guideline‐recommended treatment? Asia‐Pacific Journal of Clinical Oncology. 2016;12(1):52–60. pmid:26481765
- 62. Whop LJ, Bernardes CM, Kondalsamy‐Chennakesavan S, Darshan D, Chetty N, Moore SP, et al. Indigenous Australians with non–small cell lung cancer or cervical cancer receive suboptimal treatment. Asia‐Pacific Journal of Clinical Oncology. 2017;13(5):e224–e31. pmid:26997361
- 63. Braithwaite J, Wears RL, Hollnagel E. Resilient health care: turning patient safety on its head. International Journal for Quality in Health Care. 2015;27(5):418–20. pmid:26294709
- 64. Visvanathan K, Levit LA, Raghavan D, Hudis CA, Wong S, Dueck A, et al. Untapped potential of observational research to inform clinical decision making: American Society of Clinical Oncology research statement. Journal of Clinical Oncology. 2017;35(16):1845–54. pmid:28358653
- 65. Iedema R, safety. Creating safety by strengthening clinicians’ capacity for reflexivity. BMJ Quality. 2011;20(Suppl 1):i83–i6. http://dx.doi.org/10.1136/bmjqs.2010.046714.
- 66. Kann BH, Johnson SB, Aerts HJ, Mak RH, Nguyen PL. Changes in length and complexity of clinical practice guidelines in oncology, 1996–2019. JAMA Network Open. 2020;3(3):e200841–e. pmid:32167566
- 67. Venus C, Jamrozik E. Evidence‐poor medicine: just how evidence‐based are Australian clinical practice guidelines? Internal Medicine Journal. 2020;50(1):30–7. pmid:31943616
- 68. Shaneyfelt TM, Centor RM. Reassessment of clinical practice guidelines: go gently into that good night. JAMA. 2009;301(8):868–9. pmid:19244197
- 69.
National Health and Medical Research Council. Guidelines for Guidelines Handbook: NHMRC; 2022. Available from: www.nhmrc.gov.au/guidelinesforguidelines.
- 70. Mellor JD, Bensted KE, Chan PL. Off label and unlicensed prescribing in a specialist oncology center in Australia. Asia‐Pacific Journal of Clinical Oncology. 2009;5(4):242–6. https://doi.org/10.1111/j.1743-7563.2009.01239.x.
- 71.
Australian Institute of Health and Welfare. Rural and remote health Canberra 2020. Available from: https://www.aihw.gov.au/reports/australias-health/rural-and-remote-health.
- 72. George M, Ngo P, Prawira A. Rural oncology: overcoming the tyranny of distance for improved cancer care. Journal of Oncology Practice. 2014;10(3):e146–e9. pmid:24667293
- 73. Craft PS, Buckingham JM, Dahlstrom JE, Beckmann KR, Zhang Y, Stuart-Harris R, et al. Variation in the management of early breast cancer in rural and metropolitan centres: implications for the organisation of rural cancer services. The Breast. 2010;19(5):396–401. pmid:20452216
- 74. Venchiarutti RL, Clark JR, Palme CE, Shakespare TP, Hill J, Tahir ARM, et al. Influence of remoteness of residence on timeliness of diagnosis and treatment of oral cavity and oropharynx cancer: a retrospective cohort study. Journal of Medical Imaging Radiation Oncology. 2020;64(2):261–70. pmid:32037663
- 75. Fox P, Boyce A. Cancer health inequality persists in regional and remote Australia. MJA. 2014;201(8):445–6. pmid:25332023
- 76. Bierbaum M, Plueckhahn T, Roth F, McNamara C, Ramsey I, Corsini N. Challenges to uptake of cancer education resources by rural Aboriginal Health Workers: the Cancer Healing Messages flipchart experience. Rural and Remote Health. 2017;17:4199. pmid:29262688
- 77. Gordon LG, Ferguson M, Chambers SK, Dunn J, editors. Fuel, beds, meals and meds: out-of-pocket expenses for patients with cancer in rural Queensland. Cancer Forum; 2009.
- 78. Gabriel G, Barton M, Delaney GP. The effect of travel distance on radiotherapy utilization in NSW and ACT. J Radiotherapy Oncology. 2015;117(2):386–9. pmid:26243679
- 79. Sabesan S, Larkins S, Evans R, Varma S, Andrews A, Beuttner P, et al. Telemedicine for rural cancer care in North Queensland: bringing cancer care home. Australian Journal of Rural Health. 2012;20(5):259–64. pmid:22998200
- 80. Prabhu Das I, Baker M, Altice C, Castro KM, Brandys B, Mitchell SA. Outcomes of multidisciplinary treatment planning in US cancer care settings. Cancer. 2018;124(18):3656–67. pmid:30216477
- 81. Gebhardt BJ, Heron DE, Beriwal S. A peer review process as part of the implementation of clinical pathways in radiation oncology: Does it improve compliance? Practical Radiation Oncology. 2017;7(5):332–8. pmid:28284760
- 82. Wright F, De Vito C, Langer B, Hunter A. Multidisciplinary cancer conferences: a systematic review and development of practice standards. European Journal of Cancer. 2007;43(6):1002–10. pmid:17329094
- 83. Rao K, Manya K, Azad A, Lawrentschuk N, Bolton D, Davis ID, et al. Uro-oncology multidisciplinary meetings at an Australian tertiary referral centre–impact on clinical decision-making and implications for patient inclusion. BJU International. 2014;114(Suppl 1):50–4. pmid:25070295
- 84. Pascoe SW, Veitch C, Crossland LJ, Beilby JJ, Spigelman A, Stubbs J, et al. Patients’ experiences of referral for colorectal cancer. BMC Family Practice. 2013;14(1):1–8. pmid:23972115
- 85. Leech M, Katz MS, Kazmierska J, McCrossin J, Turner S. Empowering patients in decision‐making in radiation oncology–can we do better? Molecular Oncology. 2020;14(7):1442–60. pmid:32198967
- 86. Sundaresan P, King MT, Stockler MR, Costa DS, Milross CG. Barriers to radiotherapy utilisation in New South Wales Australia: Health professionals’ perceptions of impacting factors. Journal of Medical Imaging Radiation Oncology. 2015;59(4):535–41. pmid:26076378
- 87. Morris L, Gorayski P, Turner S. Targeting general practitioners: prospective outcomes of a national education program in radiation oncology. Journal of Medical Imaging Radiation Oncology. 2018;62(2):270–5. pmid:29080296
- 88. Egger S, Smith DP, Brown B, Kneebone AB, Dominello A, Brooks AJ, et al. Urologists’ referral and radiation oncologists’ treatment patterns regarding high‐risk prostate cancer patients receiving radiotherapy within 6 months after radical prostatectomy: A prospective cohort analysis. Journal of Medical Imaging Radiation Oncology. 2020;64(1):134–43. pmid:31793211
- 89. Yap ML, O’Connell DL, Goldsbury DE, Weber MF, Smith DP, Barton MB. Patterns of care for men with prostate cancer: the 45 and Up Study. MJA. 2021;214(6):271–8. pmid:33665811
- 90. Malalasekera A, Dhillon HM, Shunmugasundaram C, Blinman PL, Kao SC, Vardy JL. Why do delays to diagnosis and treatment of lung cancer occur? A mixed methods study of insights from Australian clinicians. Asia‐Pacific Journal of Clinical Oncology. 2021;17(2):e77–e86. pmid:32298539
- 91. Cancer Institute NSW. Canrefer: Find cancer specialists and hospitals across NSW and ACT 2022. Available from: www.canrefer.org.au.
- 92. McKinlay JB, Link CL, Freund KM, Marceau LD, O’Donnell AB, Lutfey K. Sources of variation in physician adherence with clinical guidelines: results from a factorial experiment. Journal of General Internal Medicine. 2007;22(3):289–96. pmid:17356957
- 93. Hoorn C, Crijns H, Dierick-van Daele A, Dekker L. Review on factors influencing physician guideline adherence in cardiology. J Cardiology in Review. 2019;27(2):80–6. pmid:29634492
- 94. Braithwaite J, Clay-Williams R, Vecellio E, Marks D, Hooper T, Westbrook M, et al. The basis of clinical tribalism, hierarchy and stereotyping: a laboratory-controlled teamwork experiment. BMJ open. 2016;6(7):e012467. pmid:27473955
- 95. Hysong SJ, Best RG, Pugh JA. Audit and feedback and clinical practice guideline adherence: making feedback actionable. Implementation science. 2006;1(1):1–10. pmid:16722539
- 96. Ivers N, Jamtvedt G, Flottorp S, Young JM, Odgaard‐Jensen J, French SD, et al. Audit and feedback: effects on professional practice and healthcare outcomes. Cochrane Database of Systematic Reviews. 2012;(6). pmid:22696318
- 97. Tomasone JR, Kauffeldt KD, Chaudhary R, Brouwers MC. Effectiveness of guideline dissemination and implementation strategies on health care professionals’ behaviour and patient outcomes in the cancer care context: a systematic review. Implementation Science. 2020;15:1–18. https://doi.org/10.1186/s13012-020-0971-6.
- 98. Garcia-Vidal C, Sanjuan G, Puerta-Alcalde P, Moreno-García E, Soriano A. Artificial intelligence to support clinical decision-making processes. J eBioMedicine. 2019;46:27–9. pmid:31303500
- 99. Kastner M, Bhattacharyya O, Hayden L, Makarski J, Estey E, Durocher L, et al. Guideline uptake is influenced by six implementability domains for creating and communicating guidelines: a realist review. Journal of Clinical Epidemiology. 2015;68(5):498–509. pmid:25684154