Factors Influencing Primary Care Practitioners’ Cancer Screening Recommendations for Older Adults: a Systematic Review

Background Primary care practitioners (PCPs) play a key role in cancer screening decisions for older adults (≥ 65 years), but recommendations vary by cancer type and jurisdiction. Purpose To examine the factors influencing PCPs’ recommendations for breast, cervical, prostate, and colorectal cancer screening for older adults. Data Sources MEDLINE, Pre-Medline, EMBASE, PsycINFO, and CINAHL, searched from 1 January 2000 to July 2021, and citation searching in July 2022. Study Selection Assessed factors influencing PCPs’ breast, prostate, colorectal, or cervical cancer screening decisions for older adults’ (defined either as ≥ 65 years or < 10-year life expectancy). Data Extraction Two authors independently conducted data extraction and quality appraisal. Decisions were crosschecked and discussed where necessary. Data Synthesis From 1926 records, 30 studies met inclusion criteria. Twenty were quantitative, nine were qualitative, and one used a mixed method design. Twenty-nine were conducted in the USA, and one in the UK. Factors were synthesized into six categories: patient demographic characteristics, patient health characteristics, patient and clinician psycho-social factors, clinician characteristics, and health system factors. Patient preference was most reported as influential across both quantitative and qualitative studies. Age, health status, and life expectancy were also commonly influential, but PCPs held nuanced views about life expectancy. Weighing benefits/harms was also commonly reported with variation across cancer screening types. Other factors included patient screening history, clinician attitudes/personal experiences, patient/provider relationship, guidelines, reminders, and time. Limitations We could not conduct a meta-analysis due to variability in study designs and measurement. The vast majority of included studies were conducted in the USA. Conclusions Although PCPs play a role in individualizing cancer screening for older adults, multi-level interventions are needed to improve these decisions. Decision support should continue to be developed and implemented to support informed choice for older adults and assist PCPs to consistently provide evidence-based recommendations. Registration PROSPERO CRD42021268219. Funding Source NHMRC APP1113532. Supplementary Information The online version contains supplementary material available at 10.1007/s11606-023-08213-4.


INTRODUCTION
Deciding whether it is worthwhile to advise older adults (aged ≥ 65 years) to continue or stop cancer screening is not straightforward for primary care practitioners (PCPs).At a population level, there is evidence that the benefit/harm trade-off of cancer screening becomes less favorable in older adults.The decision also becomes increasingly complex given competing mortality risks, increasing risks of harm from the screening cascade (follow-up testing, false positive results) and harms from overdiagnosis. 1 Moreover, the chance of benefiting at an individual level does not depend on age, but rather the life expectancy and health status of a person, suggesting screening decisions should be individualized. 2ancer screening recommendations for older adults vary by jurisdiction and cancer type.Many countries implement national breast, bowel, and cervical screening programs that target participation up to a certain age (e.g., 75 years), but it is unclear what role PCPs play in decision-making beyond these ages.In the USA, both researchers and guidelines from the U.S. Preventive Services Task Force have increasingly advocated for individualized screening decisions based on patient health, comorbidities, and prior screening history, [1][2][3][4] Published online May 4, 2023   38(13): -2998 3020

REVIEWS
in which PCPs play a key role.For example, many guidelines recommend against screening older adults with less than 10 years' life expectancy. 1 However, many older adults with limited life expectancy continue to screen 5 and have limited knowledge of the potential harms of doing so. 6nderstanding more about the evidence on the factors that influence PCPs' decisions about continuing or stopping cancer screening in older adults is needed to inform the design of interventions to individualize screening for older adults and to identify areas for further research in this area.The aim of this systematic review was to examine the factors influencing PCPs' recommendations for breast, cervical, prostate, and colorectal cancer screening for older adults.[9]

Protocol and Registration
The protocol for this review was registered with PROSPERO (CRD42021268219) and reporting is guided by the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) checklist. 10

Search Strategy
A comprehensive search strategy previously developed in consultation with an academic librarian to explore patientreported factors associated with older adults' cancer screening decision-making 11 was adapted by adding terms related to PCPs (see Supplementary Table I).Searches were conducted in Medline, Pre-Medline, EMBASE, PsycINFO, and CINAHL on 16th July 2021.After removing duplicates, two researchers (JS, RD) independently screened titles and abstracts for inclusion/exclusion using an eligibility checklist and disagreements were resolved via discussion.A backward citation search and forward citation search were conducted once decisions were finalized (14th July 2022).

Inclusion Criteria
Studies were included if they: a. Empirically assessed clinician-reported factors influencing primary care practitioners' (PCPs) recommendations for cancer screening for older adults, defined as either (1)  adults who are aged ≥ 65 years or (2) adults with limited (< 10-year) life expectancy.b.Included PCPs (e.g., general practitioners, family medicine practitioners, primary care internists, primary care nurse practitioners, physician assistants) providing care to older adults or a sub-group of older adults.
Studies were excluded if they: a. Analyzed factors associated with retrospective screening, or assessed decision-making regarding diagnostic or surveillance tests; or b.Were reviews, editorials, commentaries, research letters, intervention studies or protocols.

Quality Appraisal
Two researchers (JS, KG) independently assessed the quality of included studies using the Joanna Briggs Institute critical appraisal tools, which are checklists that can be used to determine the sources of bias in a study's design, conduct, and analysis (Prevalence Studies Checklist for survey studies and Qualitative Research Checklist for interview and focus group studies). 12Different aspects of the methods and reporting of results in included studies were scored individually and then combined to determine an overall assessment of risk of bias (low, moderate, or high).See Supplementary Table II for more details.

Data Extraction and Synthesis
Previous systematic reviews conducted by the research team and their colleagues were used to inform the development of a standardized data extraction template (Supplementary Table III). 11,13After piloting, two authors (JS, KG) independently extracted data and resolved any disagreements through discussion.Disagreements were evident for the categorization of factors, for example, whether fear of what the patient thought was a "patient psychosocial" or "clinician psychosocial" factor.These discrepancies were solved through input of all other co-authors.The data was narratively summarized.JS conducted a preliminary synthesis, which was continually refined throughout the writing process through input from all co-authors.

RESULTS
After removal of duplicates, 1921 titles and abstracts were screened for inclusion or exclusion, and 57 full texts were reviewed, of which 25 met inclusion criteria (Fig. 1).Five additional records were included: one identified in our review on patient-reported factors, 14 three from forward citation searching, [15][16][17] and one from backward citation searching. 18This led to the inclusion of 30 studies (20 quantitative, nine qualitative, and one mixed-methods).
Findings from the included studies are summarized in Figure 2. It highlights the factors reported as influential by three or more quantitative or qualitative studies.Furthermore, findings are narratively synthesized below according to patient demographic and health characteristics, patient psycho-social factors, clinician characteristics, clinician psycho-social factors, and health system factors, with the most commonly reported factor summarized first.Influential factors are only summarized in-text if reported by two or more studies.However, all the findings from the quantitative studies (including effect sizes where available) are shown in Table 2, and for the qualitative studies in Table 3 (quotes in Supplementary Table III) and interactions between factors in Table 4.

Patient Demographic Characteristics
39]41 Quantitative studies using vignettes and linear regression models found greater likelihood of recommending screening to 80-year-olds compared to 90-year-olds; 22 to 75-year-olds compared to 85-year-olds; 34 and to 70-year-olds compared to 85-or 90-year-olds. 14,35However, these studies had moderate 34,35 to high risk of bias 14 and the one study with low risk of bias was conducted in 2006. 22In descriptive and qualitative studies, PCPs reported using specific age cutoffs in deciding whether to screen or not.For example, 67.5% reported that they discontinued prostate screening based on age 38 and "I'll just do 75 for everything." 20

Patient Health Characteristics
Life Expectancy Fifteen studies (four of good quality) found that PCPs considered life expectancy an important factor in screening recommendations, including being less likely to recommend screening for individuals with limited life expectancy as presented in vignettes (< 5 years 23,34,41 or < 2 years 14,24,40 ). 14,17,25,30,31,33,38,39,43In qualitative studies, PCPs determined clearly limited life expectancy by considering comorbidities, frailty, and cognitive decline, but also reported difficulty or uncertainty about these estimations 38 or disagreed with using life expectancy to guide decision-making. 33,38When life expectancy was 5-10 years in vignettes, PCPs were more likely to defer to the patient's preference for colorectal screening. 24,40alth Status, Comorbidities and Functional Status Five quantitative studies, including three of good quality, found that PCPs were less likely to offer screening (or more likely to recommend against 24 ) to those in poor health compared to good health 22,40 or to those with more severe comorbidity. 21,34PCPs also described comorbidity as an important factor in decision-making in six studies (two of good quality) 14,27,31,33,42,43 and one study of poor quality found 68% felt that breast screening should be offered to healthy women regardless of their age. 14Five qualitative studies, including two of good quality, highlighted how PCPs assessed health status globally or based on "gut feeling" (e.g., considering comorbidities, functional status, life expectancy) when making screening recommendations. 14,25,27,30,31One quantitative study of lower quality and one qualitative study of good quality also found functional status and ability to tolerate further tests/treatment were influential. 27,42ncer Risk One quantitative study of low quality 41 and two qualitative studies of moderate quality 30,46 reported that risk due to family or personal history of cancer influenced PCP recommendations for breast and prostate screening.
Screening History Screening history influenced PCPs in two studies whereby history of normal cervical screening reduced likelihood of offering screening to older women (good quality) 22 and longer time since last colonoscopy (> 5 years vs < 5 years) increased likelihood of recommending colonoscopy. 34

Clinician Characteristics
Influence on Recommendations In three lower quality studies, clinician age influenced recommendations, such that older PCPs were less likely than younger PCPs to recommend colorectal screening for 85-year-olds 34 but more likely to recommend prostate screening for men ≥ 75 years. 36,37There were mixed findings for the impact of gender and specialty, as two studies (one of good quality) reported no impact for colorectal screening. 22,34However, other studies of lower quality found female PCPs in England were twice as likely to be undecided about breast screening compared to males (who were more likely to recommend against) 14 and family medicine PCPs were more likely to recommend prostate screening for men ≥ 75 years in the USA than medical and radiation oncology specialty providers. 36,37fluence on Inappropriate Recommendations (Based on < 5-Year Life Expectancy or Moderate-Severe Comorbidity Including Non-small cell Lung Cancer or Ischemic Cardiomyopathy with Dyspnea) All studies that assessed influence of clinician characteristics on inappropriate screening recommendations were of good quality.Internal medicine and family medicine doctors were less likely to recommend inappropriate colorectal 21 or breast screening 29 compared to obstetrics and gynecology physicians.Females were more likely to recommend inappropriate colorectal 21 or breast screening 22 than males (but no difference for cervical).

Gender
Females were half as likely as males to choose not to screen compared to being undecided (female vs. male clinician gender, relative risk for not screening vs. undecided 0.52, 95% CI 0.32-0.84,p = 0.008)

Clinician Psycho-social Factors
Attitudes and Perceived Benefits/Harms PCPs considered direct and downstream harms for screening recommendations in four studies, including three of good quality (i.e., overdiagnosis, overtreatment, false positives). 20,25,26,33owever, two qualitative studies (one of good quality) highlighted differences in PCP recognition of screening harms for older adults, whereby some PCPs did not believe overscreening in older adults occurred, felt it was acceptable, or disagreed with how it is defined based on limited life expectancy. 17,33Similarly, a small study found that PCPs recommend inappropriate prostate screening despite knowing that harms may outweigh benefits. 16PCPs were more likely to recommend screening when concerned about missing cancers in three good quality studies, 19,20,26 and when the test was perceived as accurate/effective. 20,31Uncertainty led to higher breast screening rates and recommendations in two more recent studies (one of good quality) 18,26 or deferring to patient preference rather than provide a recommendation in one study from 2008. 40Positive attitudes towards screening were associated with recommending screening in two studies (one of good quality). 23,35PCPs reported decisions about screening based on a gut feeling, not necessarily conscious or deliberate, 27 given there were so many factors to consider. 25cial Factors Three studies (one of good quality) found that PCPs reported inappropriately screening due to difficulty discussing risks and benefits or stopping screening. 14,19,39necdotal experiences with patients 27 or their own social networks 32 also influenced PCP decision-making.Fear of negative patient appraisal and liability concerns led PCPs to continue inappropriate cervical screening 19 or recommend breast screening to older women. 26PCPs also reported patient-PCP relationship as an important factor in three qualitative studies. 25,30,39alth System Factors Guidelines/Recommendations Four studies (two of good quality) reported that guidelines were influential in PCPs' screening recommendations including US Preventive Services Task Force (USPSTF), 29,30,35 American Cancer Society, 30 and American College of Obstetricians and Gynecologists 15 guidelines.However, three qualitative studies highlighted negative views towards guidelines, including concerns of inequality, 14 undermining patient-centered care, 33 and inadequate evidence to support best practice. 30n older studies, PCPs also reported that better guidelines were needed. 39,42In recent studies, PCPs expressed desire for decision support (e.g., patient hand-outs, electronic Using life expectancy to decide when screening should stop Life expectancy: some agreed basing decision to stop on limited life expectancy but others disagreed.Many used < 10 years as threshold Distrust of life expectancy predictions: clinicians were skeptical of prediction tools and felt the existing models may miss important variables (e.g., family history of longevity), and did not account for changes in patient status or medical technology Using life expectancy felt impersonal: Some felt uncomfortable even when they understood the rationale for the guidelines Concern for bias in considering life expectancy: bias in terms of race and cost are introduced when using life expectancy and developing prediction tools Schonberg 2006 39 Explore decision-making about BCa screening in women aged ≥ 80 years Age: three commented that they were less likely to recommend screening to patients as they aged into their late 80 s or 90 s Availability of further tests or treatment: eight noted that the availability of acceptable treatments for elderly women with BCa influenced their screening recommendations Life expectancy: eight described recommending screening to patients they perceived to have adequate life expectancy and not discussing screening or discussing stopping with patients they perceived to have very limited life expectancy Walters 2011 14 Views on extending BCa screening to women ≥ 70 years Life expectancy and fitness: the effect of comorbidity, frailty and cognitive decline were all viewed as important if healthcare professionals were considering whether to recommend continuing screening.It was generally felt that a woman should continue to be screened if she was fit enough to benefit

Progressive increase in breast cancer risk with older age
Cognitive impairment: most would not recommend screening for older women with significant cognitive impairment who would be unable to give informed consent should they need treatment, due to the marginal benefits

Study (author, year) Outcome details Results
Patient psycho-social Austin 2021 17 Experiences discussing BCa screening with older patients, influence of guidelines, overscreening perceptions Patient autonomy: several reported that an in-person visit was not required for older women to obtain a referral for BCa screening and that they could call the provider's office and speak with a nurse who can generate an order or have the referral signed off by another provider who is unfamiliar with the patient's history Lewis 2009 25 CRC screening decisions using two vignettes of 78-year-old women in fair and poor health Patient personality: whether a patient had previously been aggressive about screening or were proactive about screening Patient-provider relationship: no quote available Family support: Another aspect was opinions of family members about screening Patient autonomy: PCPs reported a patient in fair health had a highly autonomous role.
Many emphasized their role was to provide information to help the patient understand options Oshima 2021 30 BCa screening practice patterns with older women including discussions about stopping Patient preference: all strongly valued a patient's desire for continued screening as rationale for continuing.While most older women were perceived as eager to stop, PCPs also acknowledged that patients' personal experiences with screening influenced the degree to which they felt invested in BCa screening Patient satisfaction: four mentioned their recommendations were influenced by knowing that performance evaluations depend on patient satisfaction, e.g., Press Ganey scores.This led to reluctance to recommend an alternative if a patient had a strong preference for continued screening Patient post-screening preference: seven emphasized the importance of knowing how invested women were in the outcomes following screening Patient-provider relationship: strong relationships gave PCPs more insight into patient preferences, increased patient trust of PCP recommendations, and helped PCPs more easily personalize discussions and recommendations Park 2021 31 PCP perceptions of CRC screening test options Patient choice: patient preference was a strong influence on the choice of screening tests.
Stool tests were considered alternatives when patients refused colonoscopy Rowe 2021 16 PCP explanations for overuse of PCa screening in men ≥ 75 years Patient preference: PCPs were aware and knowledgeable of guidelines, but many deferred to patient preference when deciding whether to order a test.Another recognized that PSA screening in older men probably should not be ordered but felt some were still insistent or expectant Schoenborn 2020a 27 Decisions for 2-3 patients: at least 1 who had screened in previous year and 1 who had not Patient request: most would give in to the patients' request for screening even if they otherwise would have stopped screening Anecdotes about family and friends

Schoenborn
2020b 33 Using life expectancy to decide when screening should stop Patient choice: PCPs generally felt that patients should be able to make the ultimate decision as long they were informed about the benefits and risks, even if that meant choosing screening when they had limited life expectancy Schonberg 2006 39 Explore decision-making about BCa screening in women aged ≥ 80 years Patient preference: if patients had a preference about screening PCPs followed the patient's preference Patient-provider relationship: six described that a longstanding doctor-patient relationship and patient trust can facilitate these discussions Walters 2011 14 Views on extending BCa screening to women ≥ 70 years Patient choice: "Quite a lot of elderly patients ask if they can come back for screening when it ceases." Clinician psycho-social Austin 2021 17 Experiences discussing BCa screening with older patients, influence of guidelines, overscreening perceptions Benefits vs. harms: a few described how other PCPs believe that the benefits of screening outweigh the potential harms of not screening Past experiences: PCP colleague's decisions to continue screening indefinitely may be due to past experiences; no quote available Avoid confusion: PCP colleague's decisions to continue screening indefinitely may be due to avoid confusion among older women; no quote available Fear of malpractice: PCP colleague's decisions to continue screening indefinitely may be due to fear of malpractice Enns 2021 20 BCa, PCa and CRC screening decisions in patients with limited life expectancy and in general Accuracy and efficacy of test: some felt more strongly about continuing colonoscopy due to being a more reliable way of finding/preventing advanced cancer Minimising direct harm: others would forego colonoscopies in a patient while continuing PSA or BCa screening Downstream harms: clinicians considered downstream harms even when the upfront harm is low such as for PSA test Negative consequences of late-stage cancers: Others focused on the negative consequences of late-stage cancers when prioritizing different screenings Cancers that are easier to treat: one PCP would continue BCa screening in a patient while stopping other screenings because cancers detected by mammogram require treatments that are less risky and invasive than those used to treat other cancers

Study (author, year) Outcome details Results
Lewis 2009 25 CRC screening decisions using two vignettes of 78-year-old women in fair and poor health Gestalt process: it was difficult for PCPs to express how they put all considered factors together to decide whether screening was worthwhile.Some reported that the decision was based on more of gestalt (i.e., a feeling of knowing the patient and their medical problems) and emphasized the importance of a long-term relationship Concern about harm: the major concern was when there was no chance that a patient could benefit and also about causing distress from colonoscopy Influence of screening test on management: physicians considered what they would do with information from a screening test and whether it would change their future management of the patient.If they were unlikely to pursue treatment, they were less likely to recommend screening Difficulty weighing many factors: Some reported that the decision-making process for CRC was difficult due to the sheer number of factors that they had to weigh Oshima 2021 30 BCa screening practice patterns with older women including discussions about stopping Evidence: seven felt there was inadequate evidence to suggest a best practice for BCa screening in women ≥ 75, one felt there was enough evidence to recommend against screening in older women.All reported frequently engaging in shared decision-making on whether to pursue routine BCa screening, however this was particularly important among PCPs who felt that current guidelines were unclear Park 2021 31 PCP perceptions of CRC screening test options in older adults

Familiarity with newer tests
Test effectiveness: some were concerned that stool tests are not as effective as colonoscopy in detecting advanced adenomas Rowe 2021 16 PCP explanations for overuse of PCa screening in men ≥ 75 years Knowledge: PCPs were aware of guideline content, suggesting over testing was not due to a knowledge deficit.General knowledge of guidelines was apparent in the responses to discrete questions.(e.g., 67% agreed that harms of PCa screening outweighed benefits for the average 77-year-old man) Underestimation of harms: few discussed downsides of PCa screening.One mentioned they would, but later discussed not wanting to miss PCa in an older healthy man Resistance to change: many reported the desire to not change management for patients doing well, preferring to maintain the status quo Schoenborn 2020a 27 Decisions for 2-3 patients per PCP: at least 1 who had screened in previous year and 1 who had not Anecdotes: clinicians mentioned various anecdotal experiences involving patients or their personal experiences that were factors in their cancer screening practice

Risks from screening test: no quote available
Gestalt process: for 26/53 patients, their PCP described the decision as not a conscious one or was not able to recall how the decision was made even after medical record review (in patients with and without recent screening).Sometimes after record review, PCPs said they should have made the opposite decision for some Schoenborn 2020b 33 Using life expectancy to decide when screening should stop Non-mortality-related benefits of screening: PCPs mentioned that screening may provide other benefits that make it worthwhile, even if it did not impact the patient's mortality; including quality of life, less extensive treatment, reassurance, and positive changes triggered by knowing a cancer diagnosis Difficulty of applying population-based screening data to individual patients Overscreening perceptions: 18/30 PCPs perceived there was overscreening in older adults.
Others did not believe there was or thought it was acceptable.Others disagreed with how overscreening is defined Schonberg 2006 39 Explore decision-making about BCa screening in women aged ≥ 80 years Not wanting to discuss stopping screening: 9 PCPs described difficulties when discussing stopping screening with women ≥ 80 years; 6 reported it can be uncomfortable Walters 2011 14 Views on extending BCa screening to women ≥ 70 years Difficulty explaining risks vs benefits: several HCPs reported the potential difficulties of explaining the risks vs. benefits of BCa screening to women ≥ 70 years, as well as the controversy regarding the factors to consider in this decision-making process Impact of downsides of screening: overdiagnosis, false positive results and the impact of overtreatment were felt to be more pressing in the older age group Health system Austin 2021 17 Experiences discussing BCa screening with older patients, influence of guidelines, overscreening perceptions Guideline recommendations: all stated that they followed the guideline recommendations for BCa screening released by their respective professional organizations, mainly the USPSTF and American College of Obstetrics and Gynecology.However, providers discussed that providers within their own specialty and/or clinic did not always adhere No within-system consensus: PCPs felt the annual reminder letter from outside their clinic created conflict/confusion around which provider specialty is in charge of BCa screening and made it difficult for them to discuss stopping or reducing screening during an appointment Educational resources + electronic health record: several stated older women and PCPs could receive educational resources about the harms and limited benefits of BCa screening to help facilitate discussions.A couple suggested utilizing the electronic health record to identify women for whom stopping (or reducing frequency of) BCa screening are recommended (e.g., < 10-year life expectancy) and to customize system-generated reminder letters based on individual BCa risk and health status medical record (EMR) notifications with guideline recommendation updates). 30,43her Health System Factors In three studies (one of good quality), PCPs reported limited time to provide justification for a recommendation to stop screening. 19,38,39Clinical reminders 28,35 and EMR alerts 27 influenced recommendations in three studies (two of good quality).In two poorer quality studies, PCPs did not consider stool tests and breast screening for older adults worthwhile due to limited cost-effectiveness and unnecessary burden on the health system 14,31 and costs for the patient was also reason for not recommending screening in two other poorer quality studies. 30,42PCPs quality metrics including scores on how well they are screening patients also led them to encouraging screening up to 70 or 75 years, regardless of other factors. 30,31teraction Between Factors Age One vignette study found that PCPs were less likely to recommend colorectal screening to an 80-year-old with congestive heart failure compared to a healthy patient, but this difference was not evident for patients 65 years old. 21Another study Using life expectancy to decide when screening should stop Guidelines limit access: PCPs were concerned that the guidelines will be implemented in a way that limits patient access and/or undermines patient-centered care Skeptical about guidelines: anticipated regret when new evidence comes out Schonberg 2006 39 Counselling about BCa screening to women aged ≥ 80 years Need better evidence and guidelines: n = 6 Time to provide information: 6 described how difficult it was for patients to understand the risks and 3 reported that this discussion can take a great deal of time Walters 2011 14 Views on extending BCa screening to women ≥ 70 years Equality of access: current system viewed as favoring higher socio-economic groups Cost effectiveness: several strongly believed screening should fully cease when there were marginal benefits to the woman (i.e., not cost effective or efficient and "overburdened" the service) Burden on health system: in a system that was currently struggling to cope, several argued it was not a political imperative to promote availability of BCa screening to older women for fear of being "over burdened."Difficulty of selective screening: having GPs selectively advise screening for older women raised concerns regarding time, capacity and workload issues.Without selectivity, concerns were for harms done to less fit women.With selectivity some commented that this just introduced an additional, unnecessary barrier to access.Although HCPs were aware that there were currently several problems with the current system of voluntary self-referral (access and uptake), there was no consensus about how the system could be improved found that the consideration of health status did not change with increasing age. 34The influence of screening history also depended on age, as 53% of PCPs recommended screening for a 75-year-old who had undergone colonoscopy < 5 years ago, but 23% recommended screening for an 80-year-old with the same screening history. 34Patient request was also more likely to influence prostate and colorectal screening recommendations for 70-year-olds compared to 90-year-olds. 35alth PCPs used average life expectancies of people at that age to guide their colorectal screening decisions for patients in good health, but for patients in poor health, severity of comorbidities and functional status was influential. 24PCPs were also more likely to elicit preferences for a patient in fair health compared to a patient in poor health. 24Reported difficulty estimating life expectancy did not impact whether life expectancy influenced prostate screening decision-making. 38P Characteristics Female PCPs were more likely to recommend prostate screening due to patient anxiety compared to male PCPs 41 and non-black providers were more likely than black providers to report that their patients expected them to continue ordering PSA tests, uncomfortable with the uncertainty of discontinuing screening, and that it takes more time to explain rationale for stopping screening compared to just continuing.38 Family and internal medicine PCPs were more likely to be influenced by USPSTF recommendations than obstetrician-gynecologists who were more likely to be influenced by the American Cancer Society or American College of Obstetricians and Gynecologists guidelines.29

DISCUSSION
Our review builds on previous narrative reviews by systematically synthesizing evidence on how patient, clinician, and health system factors influence PCPs' cancer screening decision-making for older adults.Our findings highlight a complex interplay between patient health factors and clinician psycho-social factors in decisionmaking for PCPs, and the role of older adults' screening preferences.US-based research dominates the evidence base, highlighting the need for further research to understand factors influencing PCPs' decision-making for cancer screening in older adults in non-US countries, including those with national screening programs.
Prior research has posited frameworks for individualizing cancer screening decisions for older adults that consider patient, clinician, and health system factors, 2,47 and has summarized the evidence and guidelines for cancer screening in older adults. 5,48Breslau and colleagues developed the Individualized Decisions for Screening (IDS) framework in 2016, providing a guide for the conceptualization, measurement, and implementation of multilevel interventions to improve the quality of older adult's screening decisions through consideration of patient, clinician, and health system influences. 2Our review provides an up-to-date summary of how PCP decision-making may or may not align with this framework for individualized decision-making.
Regarding patient factors, our review highlights older adults' preferences particularly influence PCPs' decisionmaking, emphasizing the importance of continued efforts to develop and implement tools to support informed choice for screening.Although the gold standard may be that PCPs provide information about the benefits and harms of screening, additional approaches may be helpful such as directly targeting information to older adults, perhaps even before the notion of no longer screening becomes relevant, as previously suggested by Schonberg and colleagues for breast screening. 49Older adults have long heard persuasive screening messaging and some have strong positive attitudes towards screening that may outweigh the influence of factors such as limited life expectancy or a clinician's recommendation. 50They may need time to consider tailored information, clarify values, and have ongoing conversations with their doctor and family if desired.Researchers have examined how patient decision aids can improve the quality of cancer screening decisions for older adults and reduce overscreening.For example, Schonberg and colleagues developed a decision aid for women aged ≥ 75 years in the USA, which led to more informed screening decisions and a 9% reduction in the number of women choosing to be screened. 51In countries with national screening programs, it may also be useful for information to be provided from screening programs to communicate to individuals before they reach the upper age when screening is no longer recommended.However, further research on the impacts of providing such information outside of US contexts is needed.
Our review also highlighted clinician-level barriers to achieving individualized screening decisions for older adults.Contrary to Breslau and colleagues' suggested framework, 2 some PCPs may not make conscious, deliberate screening decisions, may only consider health status in a general sense and life expectancy to varied degrees when making recommendations, and have fears around recommending stopping screening.Other contributors to this challenge are the influence of PCP attitudes and anecdotal experiences on their decision-making, the importance of age-based guidelines, and differences in how they perceive harms such as overscreening.These findings were particularly highlighted in qualitative studies.Continued efforts to develop and implement patient-level interventions such as patient decision aids must also be accompanied by further efforts to support PCPs to provide evidence-based, tailored recommendations to stop screening when it is relevant to do so.
Recommendations to stop screening that incorporate health status ("other health issues should take priority") may be more acceptable to older adults than recommendations that incorporate life expectancy ("you may not life long enough to benefit"). 52,53However, in our experimental scenario-based study, recommendations incorporating life expectancy resulted in reduced intention to screen compared to recommendations incorporating health status. 6Specific scripts and strategies co-designed with patients and PCPs to discuss stopping screening in various clinical scenarios have also been developed in the USA, including a briefer statement about stopping, a longer script highlighting reasons for stopping, and a shared decision-making script to support discussion about the benefits and harms, 54 which could be adapted for use in countries with national screening programs.Further research is needed to test communication strategies that are acceptable to PCPs and effectively support older adults to have a realistic understanding of the benefits and harms of cancer screening, especially for those with strong positive attitudes towards screening.
System-level factors such as time, age-based guidelines, and clinical reminders and electronic medical record alerts are also important influences on PCP recommendations and may form barriers to individualized decision-making.In the USA, it is essential that existing systems are leveraged to better align with the goal of individualized screening decisions.Suggestions include training for PCPs in the use of decision aids, professional organizations expressing support for the use of decision aids, incorporating use of decision aids and life expectancy estimation into electronic medical record alerts, 46,51 and pre-clinical visits for PCPs to understand patient preferences and understanding ahead of a discussion.In non-US contexts, further research is needed to understand whether and how individualized decisions for cancer screening in older people can be achieved in the context of national screening programs.The design of organized screening programs is likely an important influence on decision-making about cancer screening, for both younger and older adults.

Limitations
The studies included in our review are limited due to the focus of the literature on the US context, therefore lacking generalizability to other international contexts.Some included studies were also vignette-based, meaning it is difficult to understand whether the factors would have a similar impact in clinical settings.Our review itself was limited as it was not possible to conduct a meta-analysis using any of the quantitative data due to the variability in study designs, measurement, and operationalization of decision-making and influencing factors in the included studies.Extracted data was synthesized narratively, as understanding the relative magnitude of effect sizes for influencing factors was not the aim of this study.This narrative approach allowed for the variation and heterogeneity across studies to be captured, building on the existing narrative reviews on this topic.Strengths of this review were having two independent reviewers conduct screening, data extraction and quality appraisal, and searching studies from grey literature (e.g., theses).

Conclusion
There are a wide range of patient, clinician, and health system factors that influence PCPs decisions and recommendations for cancer screening in older adults.Decision support should continue to be developed and implemented to support informed choice for older adults and assist PCPs to consistently provide evidence-based recommendations, alongside system changes in electronic medical records, professional organizations, and clinician training.Our findings also highlight the importance of supporting informed choice for younger adults who are beginning to screen, so this information does not become difficult for clinicians to communicate to patients when the benefit/risk trade-off becomes less favorable.Further research is also needed in non-US contexts, especially where national screening programs are implemented, to understand the role of PCPs in older adults' cancer screening decisions.

Figure 1
Figure 1 Flow diagram of included studies.

Figure 2
Figure 2 Individual studies reporting influence of factors on PCPs' recommendations about cancer screening for older adults; further displacement from the center indicates a greater number of individual studies reporting factor as influential; range = 0-9; factors were only included if reported by ≥ 3 studies (across qualitative and quantitative).

Table 2 Summary of Quantitative Studies Examining Factors Influencing Primary Care Practitioners' Cancer Screening Recommenda- tions Study (author, year) Outcome and analysis details Variable Results
6% of family medicine practitioners and 2% of urologists 71-75 years: 9.3% of family medicine practitioners, 16% of internists, 10% of oncologists, and 14.5% of urologists 76-80 years: 21% of family medicine practitioners, 27.5% of internists, 38% of oncologists, and 41.6% of urologists 80 + years: 64.7% of family medicine practitioners, 52.8% of internists, 48% of oncologists, and 39.5% of urologists Preferred not to stop: 4% of family medicine practitioners, 3.4% of internists, 3.4% of oncologists, and 2% of urologists Pollack 2012 Means/proportions (%), test statistic (odds ratios [OR], relative risks [RR]), 95% confidence intervals (CIs; unless otherwise specified), p-values38 Attitudes and beliefs about PCa screening; descriptive Age 32.5% did not have an age at which they typically stop recommending PSA screening For 67.5% who discontinued screening based on patient age, 26.8% at 70 years, 52.4% at 75 years, and 20.7% at > 80 years Ruff 2005 41 Self-reported tendency to screen for PCa; descriptive Age 49 (28.0%) and 67 (38.3%) providers thought age of > 75 years and 80 years respectively substantially decreased their tendency to screen for PCa Race African American race somewhat or significantly increased tendency for screening for 148 (84.6%) practitioners Age Screening should only be offered to age range where it was cost effective (63%, 87/138).Patient age had greatest influence in discrete choice experiment.Clinicians 17 × more likely to not screen (compared to undecided) woman > 85 vs < 70 (p < 0.001) Comorbidity Physicians were less likely to recommend any screening among patients with unresectable non-small cell lung cancer (34%) than among those who were healthy (96% vs. 34%, p < 0.001) or had congestive heart failure (89% vs. 34%, p < 0.001), across all age groups

Table 2
(continued) PCP primary care practitioner, HCP healthcare professional, CRC colorectal cancer, PCa prostate cancer, PSA prostate-specific antigen, BCa breast cancer, USPSTF United States Preventive Services Taskforce

Table 3 Summary of Qualitative Studies Examining Factors Influencing Primary Care Practitioners' Cancer Screening Recommenda- tions Study (author, year) Outcome details Results
Health status: all PCPs reported that a patient's health status affected how they approached recommendations Life expectancy: Some (n = 5) assessed health status and 10-year life expectancy by considering comorbid conditions (e.g., renal failure, heart failure, coronary artery disease, metastatic cancer, neurologic degenerative processes).Several (n = 4) were uncertain in accurately estimating prognosis Functional status: used to decide whether or not to discuss screening Risk of breast cancer: PCPs were more likely to bring up BCa screening if there was personal/family history, or other relevant risk factors, e.g., obesity PCPs reported resorting to stool tests in older patients who would be too high risk for a colonoscopy Functional status: PCPs considered burdens of getting to the screening facility (e.g., mobility and/or transportation challenges) Life expectancy: some stopped all screening in patients with clearly limited life expectancy.

Table 3
33ontinued) seven followed USPSTF recommendations for BCa screening in daily practice, beginning discussions at age 40, with an increased emphasis on routine screening every 1-2 years from age 50-75 Financial costs: five did not consider financial costs when discussing BCa screening, due partly to difficulty determining cost given healthcare pricing opacity, but one did Institutional quality metrics: not reported as consideration in recommendations.Two mentioned that metrics did not apply for patients ≥ 75 years Decision support tools: six indicated a patient-facing handout outlining the current guidelines surrounding BCa screening along with considerations for patients would be helpful.PCPs voiced awareness of clinical recommendations to avoid overuse in older adults.When asking how one might approach PSA testing in an older man, one PCP commented: "I'd just tell him the guidelines and see what his response was."EMR alerts: associated with less deliberate decisions.Screened patients: often ordered from routine process or triggered by alerts (BCa and CRC screenings for patients < 75).Patients not screened: absence of alerts, screening not being mentioned, reliance on alerts Specialists: PCPs reported less control over decisions when patients saw a specialist Schoenborn 2020b33

Table 4 Summary of Studies That Examined Interactions Between Factors Influencing Primary Care Practitioners' Cancer Screening Recommendations
electronic medical record, PCP primary care practitioner, HCP healthcare professional, CRC colorectal cancer, PCa prostate cancer, PSA prostate-specific antigen, BCa breast cancer; USPSTF United States Preventive Services Taskforce See Supplementary Table III for quotes, except where stated that no quote is available Poor health: some would bring up screening, but others would only discuss it if the patient asked."Bringing it up is the reasonable thing, but then you have to be very, very honest with them and you have to say look it here's a situation what are you going to really do if they tell you there's there and we have to do something about it?Do you really want to know that?" OR would be thinking about other issues "[I] Wouldn't even think about it."

Table 4
(continued) 47%) were more likely to find USPSTF guidelines extremely influential than OBG (25%) (p ≤ .001for both comparisons) OBG were more likely to describe American Cancer Society (p = 0.07) and American College of Obstetricians and Gynaecologists (p ≤ 0.001) guidelines very influential on their practice compared to FP and IM PCP primary care practitioner, CRC colorectal cancer, PCa prostate cancer, BCa breast cancer, FOBT fecal-occult blood testing, USPSTF United States Preventive Services Taskforce