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- Wolters Kluwer Health
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- Copyright © 2022 The Author(s). Published by Wolters Kluwer Health, Inc.
- ISSN
- 0959-8278
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- 1473-5709
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- 10.1097/cej.0000000000000755
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Abstract
540 Review article Referring high-risk individuals for lung cancer screening: A systematic review of interventions with healthcare professionals a a,b Mohamad M. Saab , Michelle O’Driscoll , Laura J. Sahm, a a a Patricia Leahy-Warren , Brendan Noonan , Serena FitzGerald , a a c a Caroline Kilty , Maria O’Malley , Noreen Lyons and Josephine Hegarty Objective This systematic review described the effect numbers of Lung-RADS 2 results (i.e. benign nodules with of interventions aimed at helping Healthcare Professionals a very low likelihood to becoming malignant). An increase refer high-risk individuals for lung cancer screening. in Healthcare Professionals’ knowledge and awareness of Primary outcomes included: lung cancer detection, lung cancer screening was achieved using group-based screening for lung cancer, lung cancer treatments received learning compared to lecture-based education delivery. and lung cancer mortality. Healthcare professionals’ Conclusions The effectiveness of Nurse navigation is knowledge and awareness of lung cancer screening evident, as are the benefits of adequate training, shared served as secondary outcomes. decision-making, as well as a structured, clear and well- Methods Experimental studies published between understood referral processes supported by the use of January 2016 and 2021 were included. The search was electronic system-incorporated prompts. European Journal conducted in MEDLINE, CINAHL, ERIC, PsycARTICLES, of Cancer Prevention 31: 540–550 Copyright © 2022 The PsycInfo and Psychology and Behavioral Sciences Author(s). Published by Wolters Kluwer Health, Inc. Collection. The quality of the included studies was European Journal of Cancer Prevention 2022, 31:540–550 assessed using the Mixed Methods Appraisal Tool and Keywords: decision making, lung neoplasms, mass screening, referral and the level of evidence was assessed using the Scottish consultation, systematic review Intercollegiate Guidelines Network grading system. a b Catherine McAuley School of Nursing and Midwifery, School of Pharmacy, University College Cork and Rapid Access Lung Clinic, Cork University Results Nine studies were included. Nurse navigation, Hospital, Cork, Ireland electronic prompts for lung cancer screening and shared Correspondence to Mohamad M. Saab, PhD, RN, Catherine McAuley School of decision-making helped improve patient outcomes. Nursing and Midwifery, Brookfield Health Sciences Complex, University College Specialist screenings yielded more significant incidental Cork, College Road, T12 AK54, Cork, Ireland findings and a higher percentage of Lung-RADS 1 results Tel: +353 21 4901518; e-mail: msaab@ucc.ie (i.e. no nodules/definitely benign nodules), while Primary Received 30 October 2021 Accepted 15 January 2022 Care Physician screenings were associated with higher Introduction contrast to the increase in survival rates for most cancers, Lung cancer (LC) is the leading cause of cancer inci- LC is typically diagnosed at advanced stages with 5-year dence and mortality in men and women globally, with 2.1 survival rates of 10–20% in most countries (Sung et al., million new cases (11.6% of the total cancer cases) and 2021). The 5-year relative survival rate for LC differs sig- 1.8 million deaths (18.4% of the total cancer deaths) in nificantly by stage at diagnosis and LC type. For instance, 2018 (Bray et al., 2018). It is estimated that, by 2040, the in the United States, the 5-year relative survival rate for number of people diagnosed with LC and who die from it localised non–small cell LC between 2010 and 2016 was will increase to 3.63 and 3.01 million respectively (WHO 63%. This decreased to 35% for regional spread and 7% International Agency for Research on Cancer, 2020). for distant metastasis. As for small cell LC, the 5-year More than half of LC cases (53%) are diagnosed among relative survival rate was 27% for localised LC. This men and women aged 55–74 years (Torre et al., 2016). In decreased to 16% for regional spread and 3% for distant metastasis (National Cancer Institute, 2020). Supplemental Digital Content is available for this article. Direct URL citations LC screening using low dose computed tomography appear in the printed text and are provided in the HTML and PDF versions of this article on the journal's website (www.eurjcancerprev.com). (LDCT) is associated with early detection and reduced LC mortality in a number of countries including the USA This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial-No Derivatives License 4.0 (CCBY- (National Lung Screening Trial Research Team, 2011; NC-ND), where it is permissible to download and share the work provided it is Wu and Raz, 2016), Germany (Becker et al., 2020), Italy properly cited. The work cannot be changed in any way or used commercially (Pastorino et al., 2019), the Netherlands and Belgium (de without permission from the journal. 0959-8278 Copyright © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. DOI: 10.1097/CEJ.0000000000000755 Lung cancer screening referral Saab et al. 541 Koning et al., 2020), among others. In its latest recommen- review aims using a modified version of the Population, dation statement, the US Preventive Services Task Force Intervention, Comparison and Outcomes (PICO) frame- (USPSTF, 2021) recommends annual LC screening with work (Schardt et al., 2007), to include ‘S’ for study design LDCT among ‘adults aged 50–80 years who have a 20 and ‘T’ for timeframe (PICOST). Studies considered pack-year smoking history and currently smoke or have for inclusion met the following criteria: Population: Any quit within the past 15 years’. HCP . Patients were included only when patient outcomes were reported as a result of an intervention targeted Despite the reduced LC mortality, screening uptake towards HCPs; Intervention: any intervention targeted remains suboptimal. A 2010–2015 survey of 2347 eligi- at helping HCPs detect LC early or increase their aware- ble participants found that only 3–4% of all eligible indi- ness or knowledge of any aspect of LC; Comparison: any viduals underwent LC screening (Jemal and Fedewa, comparison(s) (within or between group[s]) pre- and 2017). This was attributed to the relative novelty of postintervention; Outcomes: reported on at least one of LC screening and the recent adoption of screening rec- the review outcomes namely patient outcomes (e.g. LC ommendations (Triplette et al., 2019). This highlights detection, screening for LC, LC treatments received, the importance of raising the public’s awareness of LC and LC mortality) (primary outcome) or HCPs’ knowl- screening. Indeed, a recent systematic review conducted edge/awareness regarding any aspect of LC (secondary by Saab et al. (2021) found that national campaigns outcome); Study design: used any experimental study including the UK-based campaign ‘Be Clear on Cancer’ design; and Timeframe: studies published between were effective in enabling at-risk individuals to seek January 2016 and January 2021. Studies were excluded medical advice regarding LC screening (Ironmonger et if they did not report on patient or HCP outcomes, did al., 2015). This contributed to significant increases in not incorporate a comparator, or used nonexperimental LC screening update and early LC diagnosis. Indeed, designs. The full review eligibility criteria are presented the proportion of non–small cell LC diagnosed at stage I in Table 1. increased from 14.1% to 17.3% (P < 0.001) and decreased from 52.5% to 49% (P < 0.001) for stage IV LC following Search strategy the based ‘Be Clear on Cancer’ campaign (Ironmonger MEDLINE, CINAHL, ERIC, APA PsycARTICLES, et al., 2015). APA PsycInfo and Psychology and Behavioral Sciences Collection were searched on 4 January 2021. Truncation Primary Healthcare Professionals (HCPs) are the stew- was used to enable different forms of a keyword. ards of preventive healthcare, including LC screening. A Keywords were then combined using Boolean operators survey of 1384 USA-based primary care physicians found ‘OR’ and ‘AND’ and the proximity indicator for EBSCO that less than half of participants (47%) were aware that ‘N’. Four search strings relating to interventions, screen- LC screening was recommended by the USPSTF and ing, LC and HCPs were used. The search was limited to only 12% reported having referred at least one patient for studies published in English. The full search terms and LC screening over the past 12 months (Raz et al., 2018). strategies are presented in Table 1. This highlights the need to support primary HCPs and raising their awareness of LC screening, which would Study selection potentially lead to earlier LC referral and subsequent ear- Records identified from the database search were trans- lier diagnosis and improved patient outcomes (de Koning ferred to Covidence, an online software used to produce et al., 2020). Therefore, this systematic review described systematic reviews (The Cochrane Collaboration, 2020). the effect of interventions aimed at helping HCPs refer Titles and abstracts of records were first screened, and high-risk individuals for LC screening. Specifically, this irrelevant records were excluded. The full texts of poten- systematic review focused on the effect of interventions tially eligible records were then sourced and screened. on: Title, abstract and full-text screenings were conducted I. Primary outcomes: Patient outcomes such as LC in pairs. For a screening decision to be made, each record detection, screening for LC, LC treatments received, had to be screened twice by two independent reviewers. and LC mortality. Screening conflicts were resolved by a third independent II. Secondary outcomes: HCPs’ knowledge and aware- reviewer. ness of LC screening. Data extraction and synthesis Methods Data from the included studies were extracted using a stand- Eligibility criteria ardised data extraction table (Saab et al., 2021). The follow- The Preferred Reporting Items for Systematic Reviews ing were extracted for each study: author(s); year; country; and Meta-Analyses (PRISMA) checklist was used to design; theoretical underpinning; sample; setting; relevant report this review (Page et al., 2021). The review eli- outcomes; intervention; procedures; instruments; follow-up gibility criteria were predetermined according to the time(s); and findings. The full data extraction table is 542 European Journal of Cancer Prevention 2022, Vol 31 No 6 Table 1 Systematic review eligibility criteria and associated search terms PICOST frame- work Inclusion criteria Exclusion criteria Search terms Population Healthcare professionals (HCPs) including someone Patients (when patient outcomes were not (Lung* OR pulmo*) N3 (cancer* OR with a navigator role (or patients, only when patient reported as a result of an intervention targeted neoplas* OR malignan* OR tumo* OR outcomes were reported as a result of an interven- towards HCPs). symptom* OR sign*) tion targeted towards HCPs). ‘Health* profession*’ OR ‘health care profession*’ OR HCP* OR ‘health* work*’ OR ‘health care work*’ OR HCW* OR clinician* OR nurs* OR ‘public health nurs*’ OR PHN* OR ‘community nurs*’ OR ‘clinic nurs*’ OR ‘practice nurs*’ OR pharmac* OR chemist* OR doctor* OR physician* OR ‘general practitioner*’ OR GP* OR consultant* Intervention Any intervention, campaign, programme, trial, edu- Studies without an intervention or where inter- Interven* OR program* OR campaign* OR cation, algorithm, decision tree/support or guide ventions were not pertinent to LC. trial* OR experiment* OR educat* OR targeted at helping HCPs detect lung cancer (LC) algorithm* OR ‘decision* tree*’ OR ‘deci- early or increase their awareness or knowledge of sion* support*’ OR guid* any aspect of LC. Comparison Any comparison(s) (within or between group[s]) pre- Studies without a comparator. Not specified post the intervention. Outcomes Primary outcomes: number of referrals for LC, Outcomes relating to diseases other than LC or Refer* OR consult* OR recogni* OR number of consultations for LC, number of patients where data relating to LC cannot be distin- screen* OR counsel* OR advice OR screened for LC, number of patients diagnosed with guished from other diseases/cancers. advis* OR detect* OR find* OR triag* LC, stage of LC at diagnosis, treatments received OR direct* OR manag* OR signpost* OR for LC, and so on. know* OR aware* OR understand* Secondary outcomes: HCPs’ awareness or knowl- edge of any aspect relating to LC. Study design Any experimental design (i.e. randomised controlled Qualitative studies, cross-sectional surveys, edi- Not specified trials, nonrandomised controlled trials and pre-post torials, opinion pieces, theses, dissertations, studies). literature reviews and conference abstracts. Timeframe Studies published between January 2016 and January Studies published before January 2016 Not specified HCPs, healthcare professionals; LC, lung cancer. presented in Supplementary Table S1, Supplemental dig- quality appraisal were conducted by one author and ital content 1, http://links.lww.com/EJCP/A352. cross-checked for correctness by a second author. Data extraction was conducted by one author. Each Results extracted study was cross-checked by a second author Study selection for accuracy. Inaccuracies were resolved by consensus. A Electronic database searching resulted in 3418 records. meta-analysis was not plausible due to heterogeneity in Following deletion of duplicates, 1966 records were study design, outcomes, and outcome measures; instead, screened on the basis of title and abstract and 1885 irrele- a narrative synthesis of study findings was conducted. vant records were excluded. The full texts of the remain- Findings were synthesised then categorised according to ing 81 records were obtained and screened and 72 records the review outcomes. were excluded mainly due to wrong study design (n = 47). Therefore, nine studies were included in this systematic Quality appraisal and level of evidence assessment review. The study selection process is presented in Fig. 1. The Mixed Methods Appraisal Tool was used to appraise the methodological quality of the included randomised Study characteristics controlled trials (RCTs) and non-RCTs (Hong et al., 2018). Quality appraisal was conducted in terms of the Most of the included studies were conducted in the USA appropriateness of recruitment, data collection and data (n = 8) and were non-RCTs (n = 7). None of the included studies reported having a theoretical underpinning. The analysis to the research question. Each item was voted on sample size ranged between 109 (Griffith et al., 2016) a ‘yes’, ‘no’ and ‘cannot tell’ basis. and 1619 (Brenner et al., 2018) participants. Studies were The Scottish Intercollegiate Guidelines Network (2011) mainly conducted either in hospital settings (n = 3) or in grading system was used to assess the level of evidence primary/community care settings (n = 3). for each of the included studies. The eight levels of evi- Nine different interventions were used across the nine dence range between 1++, 1+, 1−, 2++, 2+, 2−, 3, and 4. For instance, a score of 1++ corresponds to high-quality studies, with some studies comparing and using more than one intervention. Examples include group-based learning meta-analyses, systematic reviews of RCTs, or RCTs with versus lecture-based learning (Ortmeyer et al., 2020); LC a very low risk of bias, whereas a score of 4 is assigned screening best practice advisory/Nurse Navigator (Hirsch to expert opinions. Level of evidence assessment and Lung cancer screening referral Saab et al. 543 et al., 2020); lung nodule program (LeMense et al., 2020); data; however, only one study reported accounting for Oncology Nurse navigation (Watson et al., 2020); online confounders (Ortmeyer et al., 2020). case vignettes (Schmidt et al., 2018); patient navigation pro- As for RCTs (n = 2), both had comparable groups at base- gramme (Percac-Lima et al., 2018); shared decision-mak- line, presented complete data outcomes and had partici- ing process (Rennert et al., 2020); software-incorporated pants adhere to the assigned intervention (Percac-Lima et reminder system (Brenner et al., 2018); and streamlined LC al., 2018; Schmidt et al., 2018). However, only Schmidt et al. screening protocol (Griffith et al., 2016). Follow-up times (2018) reported performing appropriate randomisation and and duration of data collection varied widely from 8 months neither of the RCTs reported blinding the outcome assessor. of data (Brenner et al., 2018) to 4-year follow-up (Hirsch et al., 2020), with some studies (n = 4) not reporting on follow-up Five of the studies scored 2+ on the Scottish time (Griffith et al., 2016; Percac-Lima et al., 2018; Schmidt Intercollegiate Guidelines Network (2011) level of evi- et al., 2018, Watson et al., 2020). Outcomes reported in the dence criteria, indicating well-conducted non-RCTs reviewed studies varied. These can be categorised into four with a low risk of confounding or bias and a moderate broad categories, namely (1) Efficiency and levels of LC probability that the relationship is causal (Brenner et al., screening (n = 5); (2) detection of LC (n = 4); (3) engage- 2018; Hirsch et al., 2020; LeMense et al., 2020; Ortmeyer ment with LC early detection and referral (n = 4); and (4) et al., 2020; Watson et al., 2020). One RCT (Schmidt et al., knowledge and awareness of LC and its screening (n = 2). 2018) had a high risk of bias (1−) and one (Percac-Lima et The full study characteristics are presented in Table 2. al., 2018) had a low risk of bias (1+). The remaining two studies (Griffith et al., 2016; Rennert et al., 2020) scored Quality appraisal and level of evidence assessment 2− indicating that they were case-control or cohort stud- All nine studies had clear research questions and used ies with a high risk of confounding or bias and a signif- appropriate data collection methods. All non-RCTs icant risk that the relationship is not causal. The full (n = 7) reported that participants were representative of quality appraisal and level of assessment results are pre- the target population and seemed to administer the inter- sented in Table 3. vention as intended. All but one non-RCT (LeMense et al., 2020) reported using measurements that were appro- Data synthesis priate to both the outcome and the intervention. Five The summary of findings from individual studies is pre- of the non-RCTs seemed to provide complete outcome sented in Table 4. Fig. 1 Study identification, screening and selection process. 544 European Journal of Cancer Prevention 2022, Vol 31 No 6 Table 2. Characteristics of the studies included in the systematic review United States of America (n = 8) Country Australia (n = 1) Research design Retrospective (n = 3) Uncontrolled pre–post (n = 3) Randomised controlled trial (n = 2) Pre-post and between-group (n = 1) Theoretical underpinning None/not reported (n = 9) Sample size (min–max) 109–1619 Settings Hospital (n = 3) Primary/community care (n = 3) Academic healthcare delivery system (n = 1) Professional organisation (n = 1) Not reported (n = 1) Relevant outcomes Efficiency and levels of lung cancer (LC) screening (n = 5) Detection of LC (n = 4) Engagement with LC early detection and referral (n = 4) Knowledge and awareness of LC and its screening (n = 2) Intervention Group-based learning versus lecture-based learning (n = 1) LC screening best practice advisory/nurse navigator (n = 1) Lung nodule programme (n = 1) Oncology nurse navigation (n = 1) Online case vignettes (n = 1) Patient navigation programme (n = 1) Shared decision-making process (n = 1) Software-incorporated reminder system (n = 1) Streamlined LC screening protocol (n = 1) Follow-up time (min–max) 8 months of data – 4 years follow-up n = 9 unless otherwise indicated. Studies often reported on more than one outcome. n corresponds to the number of times an outcome was measured/reported. n = 4 studies did not report on length of follow-up. LC, lung cancer. Primary outcome: efficiency and levels of lung cancer With regards to levels of screening, Percac-Lima et al. screening (2018) reported that a greater proportion of patients in the Five studies reported on the efficiency and levels of LC intervention group who availed of a patient navigation screening (Griffith et al., 2016; Percac-Lima et al., 2018; programme had any chest CT compared to patients in LeMense et al., 2020; Rennert et al., 2020; Watson et al., the control group who received usual care (31% [n = 124] 2020). A reduction of three days in the time between versus 17.3% [n = 138]; P < 0.001). LC screening CTs LDCT order to scan pre- versus posttest (13.5 ± 16.2 were performed in 94 patients in the intervention group vs. 10.1 ± 13.3 days, respectively) was found when a (23.5%) as compared to 69 in the control group (8.6%; streamlined approach involving a three-way confer- P < 0.001; Percac-Lima et al., 2018). Watson et al. (2020) ence call between patient, navigator and radiographer reported similarly promising findings whereby the use was implemented among 109 participants (Griffith et of hospital CT slots increased from 38% to 65% after al., 2016). LeMense et al. (2020) reported similar initial initiating oncology nurse navigation and provider edu- findings, with a decrease in the average number of days cation. The ordering fidelity of LDCTs also improved to treatment across Year 1 of their incidental lung nod- (P = 0.000), becoming more appropriately aligned to ule management programme (41 days in the phase-in the Centers for Medicaid and Medicare Services and period versus 28 days in last quarter), with a fluctuation the USPSTF guidelines. Rennert et al. (2020) reported thereafter. Watson et al. (2020) found that the time from on the factors associated with lower screening comple- Primary Care Physician referral for LDCT LC screen- tion following participation in shared decision-mak- ing to undergoing LDCT did not significantly decrease ing. These included shared decision-making location as a result of their intervention which examined the (P = 0.02), longer distances to the screening location effect of oncology Nurse Navigation on assisting patients (P = 0.03), referrals from internal medicine clinicians and ensuring optimal LDCT LC screening (P = 0.787). (P = 0.03), from younger clinicians (P = 0.01) and from Moreover, there was no statistically significant difference those with fewer years of experience (P = 0.02; Rennert between the median number of days from order to scan et al., 2020). for the pretest group versus the posttest group (7 days Primary outcome: detection of lung cancer versus 5.5 days respectively; P = 0.2953). However, the Four of the nine included studies reported directly on times from LDCT to provider notification of LDCT and patient outcomes relating to the detection of LC (Percac- subsequent patient notification of LDCT were signif- Lima et al., 2018; Hirsch et al., 2020; LeMense et al., 2020; icantly improved by 2.6 days and 1.5 days respectively (P = 0.000 for both outcomes; Watson et al., 2020). Watson et al., 2020). Hirsch et al. (2020) assessed the impact Lung cancer screening referral Saab et al. 545 Table 3 Quality appraisal and level of evidence assessment Quality appraisal items Study designs Author(s) (year) 1 2 3 4 5 6 7 8 9 10 11 12 Level of evidence Nonrandomised studies Y Y Y Y CT CT Y 2+ Brenner et al. (2017) Griffith et al. (2016) Y Y Y Y Y CT Y 2- Y Y Y Y Y CT Y 2+ Hirsch et al. (2020) LeMense et al. (2020) Y Y Y CT CT CT Y 2+ Y Y Y Y Y Y Y 2+ Ortmeyer et al. (2020) Rennert et al. (2020) Y Y Y Y Y CT Y 2− Y Y Y Y Y CT Y 2+ Watson et al. (2020) Randomised controlled trials Percac-Lima et al. (2018) Y Y CT Y Y CT Y 1+ Schmidt et al. (2018) Y Y Y Y Y CT Y 1− All studies: 1=clear research questions/aims; 2=data collected address research question/aims. Nonrandomised studies: 3=participants representative of target population; 4=measurements appropriate regarding both the outcome and the intervention; 5=complete outcome data; 6=confounders accounted for in the design and analysis; 7=the intervention administered as intended. Randomized controlled trials: 8=randomisation appropriately performed; 9=groups comparable at baseline; 10=there are complete outcome data; 11=outcome asses- sors blinded to the intervention; 12=Participants adhered to the assigned intervention. CT, cannot tell; N, No; Y, Yes. of programmatic structure on provider behaviour and LC four studies (Brenner et al., 2018; Hirsch et al., 2020; screening outcomes using a retrospective chart review of LeMense et al., 2020; Watson et al., 2020). A smoking 624 patients who underwent LC screening CT between history procedure introduced by Brenner et al. (2017) 2014 and 2018. Of those, 48% were specialist screened increased the level of smoking histories completion and 52% were primary care physician screened. It was from 22% pretest to 47% posttest, with 53% of patients found that Specialist screenings had more significant who needed smoking history completion being incidental findings (P = 0.0008), and a higher percentage addressed during the 12-month study period. Chart of lung-RADS 1 results (i.e. no nodules/definitely benign prompting was found to increase the rate of smoking nodule), while Primary Care Physician screenings were history completion (difference 34%; 95% confidence associated with higher numbers of lung-RADS 2 results interval (CI), 29–39; P < 0.001). Similarly, Watson et (P < 0.05) (i.e. benign nodules with a very low likelihood al. (2020) reported that provider-documented tobacco to becoming malignant) (Hirsch et al., 2020). Comparisons cessation discussions prior to LDCT significantly in RADS scores were also reported by Watson et al. improved (P = 0.000) as a result of their Oncology (2020), who found that patients navigated to LDCT Nurse Navigation intervention. Nurse navigation was by an oncology nurse navigator had significantly higher also key to increasing smoking cessation counselling Lung-RADS scores (P = 0.003). Interestingly, however, to >95% and almost eliminating the screening of inel- education provided to the team by the Oncology Nurse igible patients in the study conducted by Hirsch et al. Navigator did not affect the Lung-RADS scores in the (2020). intervention group. Of note, higher Lung-RADS scores Shared decision-making was reported by several studies indicate a higher probability of malignancy (American to improve clinician engagement with the referral pro- College of Radiology, 2019). cess through increased documentation of the decision LeMense et al. (2020) used a different approach to process itself (Hirsch et al., 2020; Watson et al., 2020), as assessing patient outcomes, investigating the effects of well as documentation of the resulting LC screening CTs an LC screening and incidental nodule management pro- (Brenner et al., 2018). Two studies described the beneficial gramme by retrospectively analysing 1410 CTs. Results implementation of electronic prompts for HCPs to better showed that a proportion of early-stage LC detection engage with the LC referral process (Brenner et al., 2018; increased during the two years after programme imple- Hirsch et al., 2020). For instance, Brenner et al. (2017) mentation, compared to 2012 Medicare baseline data piloted a visit-based reminder into their electronic health (LeMense et al., 2020). A similar programme involving record and found that 27% of clinicians interacted with it. patient navigation by Percac-Lima et al. (2018) found that Training reduced the deferral of the visit-based reminder 20% of patients required follow-up and reported an LC and increased interaction with the other visit-based diagnosis in 2% of the intervention group who received reminder features. After implementing the shared deci- education and follow-up versus 0.5% of the control group sion-making and visit-based reminder, the rate of Centers who received usual care. for Medicaid and Medicare Services-compliant documen- tation for LC screening CTs increased from 0% in quar- Primary outcome: engagement with lung cancer early ter 3, 2015 to 76% in quarter 1, 2016. Similarly, Hirsch et detection and referral al. (2020) developed a best practice advisory prompt to The engagement of HCPs in the processes surrounding alert/trigger when patients should be referred. Increased the early detection and referral of LC was improved in exposure to the LC screening best practice advisory was 546 European Journal of Cancer Prevention 2022, Vol 31 No 6 Table 4. Summary of findings table Author(s) (year) Intervention Findings Brenner et al. Software-incorpo- O1: Rate of completed smoking histories increased from 22% pre-test to 47% posttest. (2017) rated reminder O1: 65% of complete smoking history collection opportunities successfully completed during chart prompting versus 31% system without chart prompting (95% confidence interval (CI), 29–39; P < 0.001) O1: 53% (982/1840) of current and former smokers aged 55–80 years, needing complete smoking history at pre-test were addressed during the 12-month project. O1: Providers interacted with 27% of visit-based reminders (VBRs; 172/644). Training decreased the frequency of deferral (16% pretraining vs. 7% posttraining) and increased interaction with other features of the VBR (11% pretraining vs. 19% posttraining). O1: Seven LC screenings with computed tomography (CT) ordered between quarter 4, 2014 and quarter 3, 2015, of which none included Centers for Medicaid and Medicare Services (CMS)-compliant shared decision making (SDM) documentation. After implementing the SDM template and VBR, the rate of CMS-compliant documentation for LC screening CTs increased to 76% in quarter 1, 2016. Griffith et al. Streamlined LC O1: Time between receipt of low-dose CT (LDCT) order and actual scan reduced by 3 days pretest versus posttest (2016) screening protocol (13.5 ± 16.2 vs. 10.1 ± 13.3 days, respectively). O1: Median number of days from order to scan was 7 for the pre-test group and 5.5 for posttest group (P = 0.2953). Hirsch et al. LC screening best O1: Specialist-screened patients had a higher percentage of Lung-RADS 1 results, while Primary Care Professional (PCP) had (2020) practice advisory/ a higher number of Lung-RADs 2 results (P < 0.05). nurse navigator O1: Specialist screenings had more significant incidental findings (P = 0.0008). O1: Increased exposure to an LC screening best practice advisory associated with increased PCP screening orders (Pearson r = 0.62, P < 0.0001). O1: Nurse navigation increased documentation of SDM and tobacco cessation counselling to >95% and eliminated screening of ineligible patients. LeMense et al. Lung nodule pro- O1: Year 1: 665 nodules evaluated according to American College of Chest Physicians guidelines and entered into the (2020) gramme database as requiring either biopsy or follow-up versus 745 in Year 2. 61.5% were incidental, 15.2% were symptomatic and 12.6% were identified through screening. O1: 182 patients underwent a diagnostic intervention in Year 1, and 169 in Year 2, 121 received a cancer diagnosis in Year 1 (18.2% of all nodules) and 86 (11.5%) in Year 2. O1: Diagnosis occurred at 26.4% Stage 1, 9.1% Stage 2, 26.4% Stage 3, 38% Stage 4. O1: Relative proportion of early-stage LC detection increased during the 2 years post-test compared to 2012 Medicare baseline data. O1: Average days to treatment over 2 years decreased across Year 1, from 41 days in the phase-in period to 36 days in the first quarter and 28 days in last quarter. Increase to 42 and 43 days observed in the fourth quarter of 2017 through the first quarter of 2018, dropping to 30 days in the second quarter, and rising again to 52 days in the third quarter of Year 2. Ortmeyer et al. Group-based O2: Residents and Faculty participating in GBL demonstrated greater total knowledge compared with residents and Faculty (2020) learning (GBL) participating in the lecture format. (79 ± 17% vs. 66 ± 20%; P < 0.01). vs lecture-based learning Patient navigation Percac-Lima et O1: Greater proportion of patients in the intervention group (IG) had any chest CT compared to patients in the control group programme al. (2018) (CG; 31% [124] vs. 17.3% [138], P < 0.001). O1: LC screening CTs were performed in 94 IG patients (23.5%) vs. 69 CG (8.6%, P < 0.001). O1: 20% of screened patients required follow-up. O1: LC was diagnosed in 8 IG (2%) and 4 CG (0.5%) patients. Rennert et al. Shared deci- O1: n = 152 (88.8%) completed LDCT screening. SDM site (P = 0.02), longer distances to the screening site (P = 0.03), refer- (2020) sion-making rals from internal medicine clinicians (P = 0.03), and referrals from younger clinicians (P = 0.01) and from those with fewer years of experience (P = 0.02) were significantly associated with a lower likelihood of screening completion. Schmidt et al. Online case O2: Providing the correct answers had no systematic effect on doctors’ answers. Reduction in the number of deaths due to (2018) vignettes screening was overestimated six-fold (95% CI, 4–8) compared with the actual data. CG participants (solution withheld) esti- mated the number of preventable deaths through screening to be 17 (12–24) out of 1000 patients. In the IG, the estimated number was 13 (9–20) out of 1000 patients. Correct answer was three preventable deaths. O2: Prevalence of LC, estimated incidence of positive screening results and positive predictive value were not different between the two groups (P values of 0.2, 0.19 and 0.28, respectively). O2: Estimated specificity was higher in IG and thus closer to the actual value of 98%, compared with the CG (P = 0.0120). O2: The false-negative rate was estimated to be lower in the IG when compared to CG (P = 0.0150) and, therefore, was further from the actual value. O2: Participants specified a mean of 1.9 (95% CI, 1.7–2.1) risks of LC screening. The three most mentioned risks were radia- tion exposure, complications associated with biopsies and negative psychological effects of a positive screening result. Watson et al. Oncology nurse navi- O1: Hospital CT slot use rate increased from 38% to 65%. (2020) gation (ONN) O1: No statistically significant decrease in the time from PCP referral for LDCT LC screening to LDCT (P = 0.787); however, the times from LDCT to provider notification of LDCT results and subsequent patient notification of LDCT results were signifi- cantly improved by 2.6 and 1.5 days, respectively (P = 0.000). O1: Intervention did not affect Lung-RADS scores. Patients navigated to LDCT by the ONN had significantly higher Lung-RADS scores (P = 0.003). O1: Documentation of SDM conversations continued throughout the intervention (P = 0.174). O1: Provider-documented tobacco cessation discussions prior to LDCT significantly improved (P = 0.000). This also resulted in increased LDCT ordering fidelity (P = 0.000), that is, more aligned with CMS and the United States Preventive Services Task Force guidelines. Findings presented according to the review objectives: O1, clinical outcomes; O2, knowledge/awareness. CG, control group; CI, confidence interval; CMS, Centers for Medicaid and Medicare Services; CT, computed tomography; IG, intervention group; LC, lung cancer; LDCT, low dose computer tomography; O, objective; ONN, oncology nurse navigation; PCP, primary care physician; SDM, shared decision-making; VBR, visit-based reminder. Lung cancer screening referral Saab et al. 547 associated with increased primary care physician screen- interventions to improve screening levels and increase ing orders (Pearson r = 0.62; P < 0.0001). screening efficiency was documented across several stud- ies (Griffith et al., 2016; Percac-Lima et al., 2018; LeMense Secondary outcome: knowledge and awareness of et al., 2020; Rennert et al., 2020; Watson et al., 2020). lung cancer screening Nurse navigation, electronic prompts relating to LC HCPs’ knowledge and awareness of LC were inves- screening, and shared decision-making emerged as key tigated in two studies, using group-based versus lec- approaches to improve patient outcomes. The role of the ture-based learning (Ortmeyer et al., 2020) and online Nurse navigator is to act as the primary point of contact case vignettes with and without correct answers provided during the patient journey through educating and sup- (Schmidt et al., 2018). porting patients and liaising between the patient and Using pre-post and between-group intervention analysis other Healthcare Providers (Haase et al., 2020). Nurse across 709 participants, Ortmeyer et al. (2020) reported navigation provides person-centred care and is becoming greater resident and faculty knowledge post-group-based integral in the provision of high-quality cancer care and learning compared to lecture formats of LC screening detection, particularly in the more vulnerable and disad- education delivery (79 ± 17% versus 66 ± 20%, P < 0.01). vantaged LC cohorts (Shusted et al., 2019). Nurse nav- Schmidt et al. (2018) sent a survey consisting of seven igation was a feature of six studies (Griffith et al., 2016; online cases to members of the Australian Society of Percac-Lima et al., 2018; Hirsch et al., 2020; Rennert et Pulmonology and received 556 responses. Half of the par- al., 2020; Watson et al., 2020; LeMense et al., 2020), with ticipants were provided with the statistical information improved system efficiency and LC detection demon- required to answer correctly, while the other half had to strated (Griffith et al., 2016; Percac-Lima et al., 2018; rely on previous knowledge or estimates. No statistically Hirsch et al., 2020). Evidence from the international lit- significant differences were demonstrated in answers erature has shown that Nurse Navigators successfully relating to prevalence of LC, estimated incidence of establish relationships with the patient and facilitate the positive screening results and positive predictive values planning and aligning of care in complex chronic diseases between the two groups (P = 0.2, 0.19 and 0.28, respec- (Coyne et al., 2020). In a recent study by Čačala et al. tively). Specificity was higher in the intervention group (2021), Nurse Navigators significantly improved chemo- (P = 0.0120) and closer to the actual value, while the therapy medication adherence and therapeutic surgi- false-negative rate was lower in the intervention group cal interventions for patients with breast cancer, with (P = 0.0150) and further from the actual value. Regardless primary chemotherapy not completed in 40.2% of the of the information provided to participants, there was a nonnavigator group versus 13.5% of the Navigator group six-fold overestimation of the effect of LC screening (P < 0.001). Similarly, Seoane et al. (2020) found that (95% CI, 4–8), and participants were able to name a mean nurse navigation via telephone for nonscreening colo- of 1.9 risks of LC screening (95% CI, 1.7–2.1). noscopy improved attendance, with nonattendance rates lower in the intervention, both in the intention-to-treat analysis (intervention group 8.4% versus control group Discussion 14.3%, P < 0.001) and in the per-protocol analysis (4.4% This systematic review identified and described inter - versus 14.3%, P < 0.001). Seoane et al. (2020) also found ventions aimed at helping HCPs recognise and refer that nurse navigation improved protocol compliance high-risk individuals with symptoms indicative of LC (P = 0.001) as well as having a large economic impact (i.e. along the appropriate healthcare pathway. Results from net benefit of €55 600/year) after the intervention. This is the included studies demonstrated improvements in in line with findings from the current systematic review HCPs’ engagement in processes linked to the early detec- whereby Percac-Lima et al. (2018) reported an increase in tion of LC such as taking smoking histories (Brenner et the proportion of patients who availed of a chest CT in al., 2018) and engaging in smoking cessation discussions the intervention group with Nurse navigation, compared (Watson et al., 2020). Moreover, HCPs were more likely to the control group who received usual care. to implement the recommended consultation processes with patients (Hirsch et al., 2020). An increase in HCPs’ Shared decision-making is defined by the National knowledge and awareness of LC screening was generated Institute for Health and Care Excellence (2021) as HCPs using group-based learning compared to lecture-based and patients working together, placing people at the cen- education delivery (Ortmeyer et al., 2020), while online tre of decisions about their own treatment and care. The provision of information did not affect how well HCPs reported benefits of shared decision-making include: all were able to answer case vignettes relating to LC screen- parties understanding what is important in terms of out- ing (Schmidt et al., 2018). comes, supporting and empowering informed decisions about patients’ own care, and tailoring treatments to Improved detection of LC with higher reported lung- individual needs (National Institute for Health and Care RADS scores emerged from the findings (Hirsch et al., Excellence, 2021). 2020; Watson et al., 2020), and the successful use of 548 European Journal of Cancer Prevention 2022, Vol 31 No 6 The current systematic review demonstrated the benefits This review highlighted the importance of educating of shared decision-making in relation to LC screening, HCPs around LC screening, its benefit-risk ratio and with Brenner et al. (2017) showing that after implement- the resulting patient outcomes. Ortmeyer et al. (2020) ing the shared decision-making template with visit-based explored potential ways to deliver education about LC reminder systems, the rate of Centers for Medicaid and screening and found that participants in the group-based Medicare Services-compliant documentation for LC learning arm demonstrated greater total knowledge of LC screening CTs increased. Rennert et al. (2020) similarly screening in comparison to participants in lecture-based reported that being part of a shared decision-making site/ learning arm. These findings are in line with other edu- location had a significant positive impact on LC screen- cational interventions (Aebersold et al., 2021; Smit et al., ing levels. 2021) and a systematic review (Zaher and Ratnapalan, 2012) which reported that group-based learning is a Of note, benefits of shared decision-making are recog- promising method for continuing professional develop- nised in the screening for other cancer types. For exam- ment among HPCs and an effective means to increase ple, the USPSTF recommend shared decision-making and retain knowledge and potentially enhance inter-pro- between patients and their healthcare providers as the fessional learning. optimal method for determining whether and how often The incorporation of electronic prompts into clinical sys- to screen for breast cancer using mammography, espe- tems is an approach utilized to facilitate clinician deci- cially in average-risk women (Schrager et al., 2020). In sion-making and encourage intervention uptake across keeping with LC, a systematic review by Saab et al. (2021) many contexts. Brenner et al. (2017) demonstrated that found that shared decision-making regarding LC screen- 27% of clinicians interacted with electronic health record ing using video- and web-based decision aids helped prompts relating to LC screening. Training was an impor- dissipate LC screening decisional conflicts and enabled tant factor in adequate engagement. This result is com- participants to make an informed decision about whether parable to findings from the wider health literature. For to undergo LC screening (Lau et al., 2015; Mazzone et al., instance, Minian et al. (2021) showed that the addition 2017; Housten et al., 2018). of an electronic prompt positively influenced the pro- Another key finding from the current review relates to portion of practitioners delivering a brief intervention the potential impact that Specialist Care can have on relating to alcohol use, with 19/23 practitioners acknowl- LC outcomes as compared to Primary Care (Hirsch et edging the value of adding a validated screening tool to al., 2020). It was found that specialist-screened patients the baseline questionnaire. Participants did advise, how- had a higher percentage of lung-RADS 1 results, while ever, that organisational and sociocultural factors need Primary Care Professionals had a higher number of to be included as part of an electronic prompt design to Lung-RADS 2 results, indicating a lower probability increase its diagnostic value and reduce redundant alerts of malignancy among specialist-screened patients. It (Minian et al., 2021). Similarly, QT drug-drug interactions was also found that primary care physicians were more (i.e. prolongation of the QT interval in the heartbeat as likely to screen patients yet, specialist screenings a side effect of some drugs) were flagged in a study by had more significant incidental findings (Hirsch et Berger et al. (2021). It was found that a clinical decision al., 2020). This is echoed in a study which found that support tool led to an increase in pharmacist interven- a nationally representative sample of Primary Care tion for QT drug–drug interactions from 35.7% before Physicians frequently ordered LC screening tests and 43% after the implementation of the clinical decision for asymptomatic patients, even though expert and support tool (Berger et al., 2021). Specialist groups did not recommend it (Klabunde et al., 2012). Similarly, findings relating to skin cancer Limitations detection showed that while there were long waiting Some limitations are worthy of note. Study selection bias times for screening from a dermatologist versus other could have occurred since only studies that answered physicians (31.1 versus 15.7 days, P < 0.001), exam- the review questions were included, the search did not ination of each body area was more frequently per- include records from the grey literature, and the review formed by dermatologists versus other physicians (e.g. was limited to studies published within a five-year upper body, 96.6% versus 91.7%, P < 0.001), respec- timeframe. In addition, it was not possible to conduct a tively, and written information was more frequently meta-analysis, provide a hierarchy of evidence or rank provided (47.8% versus 34.8%, P < 0.001) (Görig studies by statistical significance due to significant heter - et al., 2021). Cost emerged as an accessibility issue, ogeneity in outcomes, outcome measures, study designs, however, with patients with statutory insurance pay- and interventions. ing more frequently for dermatologist screening than other physicians (24.7% versus 17.1%, P = 0.012; Görig Conclusion et al., 2021). This finding may be transferrable to the This review has shown the importance of interventions context of LC screening. targeted at HCPs to navigate patients appropriately Lung cancer screening referral Saab et al. 549 Bou Akl I, K Zgheib N, Matar M, Mukherji D, Bardus M, Nasr R. (2021). Primary through LC referral, diagnosis and treatment processes, care and pulmonary physicians’ knowledge and practice concerning screen- as well as ensuring that HCPs’ knowledge and aware- ing for lung cancer in Lebanon, a middle-income country. Cancer Med ness of different aspects of LC is optimal to facilitate 10:2877–2884. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. (2018). Global early detection. The effectiveness of Nurse navigation is cancer statistics 2018: GLOBOCAN estimates of incidence and mortality evident, as are the benefits of adequate training, shared worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68:394–424. decision-making and a structured, clear and well-under- Brenner AT, Cubillos L, Birchard K, Doyle-Burr C, Eick J, Henderson L, et al. (2018). Improving the implementation of lung cancer screening guidelines at stood referral process supported by the use of electronic an academic primary care practice. J Healthc Qual 40:27–35. system-incorporated prompts. However, despite the Byrne AL, Harvey C, Baldwin A. (2021). Nurse navigators and person-centred documented benefits of nurse navigation, implemen- care; delivered but not valued? Nurs Inq 28:e12402. Čačala SR, Farrow H, Makhanya S, Couch DG, Joffe M, Stopforth L. (2021). The tation remains a challenge since patient-centred care is value of navigators in breast cancer management in a south African hospital. frequently impeded by the rigid, siloed structure of the World J Surg 45:1316–1322. health services, and this is an ongoing hurdle to overcome Coyne E, Carlini J, Doherty T, Harlow W, Mitchell ML, Grealish L. (2020). Partnership between Nurse Navigators and adult persons living with complex (Byrne et al., 2021). Notwithstanding this, the importance chronic disease-An exploratory study. J Clin Nurs 29:2918–2926. of careful patient navigation and oversight in achieving de Koning HJ, van der Aalst CM, de Jong PA, Scholten ET, Nackaerts K, patient outcomes needs to be considered and empha- Heuvelmans MA, et al. (2020). Reduced lung-cancer mortality with volume CT screening in a randomized trial. N Engl J Med 382:503–513. sised in future studies. Görig T, Schneider S, Breitbart EW, Diehl K. (2021). 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European Journal of Cancer Prevention – Wolters Kluwer Health
Published: Nov 5, 2022