Factors influencing physicians’ decision to conduct cardiovascular risk assessments among cancer patients: A Systematic Review

doi:10.21203/rs.3.rs-2979487/v1

Download PDF

Research Article

Factors influencing physicians’ decision to conduct cardiovascular risk assessments among cancer patients: A Systematic Review

https://doi.org/10.21203/rs.3.rs-2979487/v1

This work is licensed under a CC BY 4.0 License

Version 1

posted

You are reading this latest preprint version

Background

Improved cancer survivorship has led to untoward effects of developing cardiovascular complications, mainly due to exposure to cardiotoxic cancer therapy. Cardiovascular screening can provide substantial benefits to patient care and outcomes, but successful implementation is challenging. This systematic review consolidates factors from existing literature and explores its relationships to highlight key domains that need to be addressed to implement these risk assessment programs in clinical practice.

Methods

We searched PubMed, EMBASE, CINAHL, Web of Science and PsycINFO using search terms focused specifically on factors influencing the implementation of cardiovascular risk assessment among the cancer population. Two reviewers completed independently in study selection, data extraction, and quality assessment. To get meaningful insight of the findings, we thematically matched those factors into the domain of the Tailored Implementation for Chronic Diseases (TICD) framework and inductively identified its relationships.

Results

Twelve studies met the inclusion criteria. Identified factors were grouped into six domains, of which the top three included factors related to individual health professionals, which were cited in 83% of studies, incentives and resources (75% of the studies), and professional interactions in 58% of studies. Within the domain of individual health professional, we include factors concerning cognitions and attitudes, knowledge and skills, and professional behaviour. The domain of incentives and resources highlighted the needs for availability of necessary resources, continuing education system, assistance for clinicians and financial-related issues. Communication influence, team and referral processes were found to be the main barriers in the domain of professional interaction. Bi-directional associations were evident between these domains, which were categorised into macro and micro levels for better interpretation.

Conclusion

This review identified key factors that could be leveraged to improve cardiovascular assessment reach and appeal. Future intervention efforts should first be targeted at the level of healthcare professionals, who are the key drivers of the entire process.

cardio-oncology

cardiovascular

cancer

systematic review

risk assessment

This review provides novel insights into the associations between factors influencing physicians’ decision making for cardiovascular risk assessment, with postulated synergistic interactions of identified domains at the macro and micro levels.
Our inductive-deductive synthesis using TICD framework showed that factors influencing physicians to conduct cardiovascular risk assessment revolved around the domains of individual health professional factors, incentives and resources and professional interactions.
For a successful implementation of cardiovascular risk assessment program, a targeted approach to behavioural change of relevant stakeholders involved in the work process is crucial.

In recent years, a growing body of evidence reveals an unavoidable association between cancer and cardiovascular (CV) disease[1, 2]. From the point of diagnosis, cancer patients are generally at elevated medium to long-term risk of developing one or more cardiovascular disease outcomes compared to the general population. In a population-based study conducted in the United States, overall cancer survivors were 2–6 times more likely to die from CV disease than cancer itself[1]. The patterns of risk substantially vary by cancer site for specific CV disease; for example, a more than 50% increased risk of heart failure or cardiomyopathy was observed in survivors of haematological, oesophageal, lung, kidney, and ovarian cancers[3]. This deleterious impact of CV health among cancer survivors is expected to be more pronounced, considering that advances in cancer treatments have improved patient survival in this modern era[4].

The increased CV risk among cancer patients could be biologically explained by shared pathogenesis between these two diseases such as oxidative stress, aging factor, and shared risk factors (i.e., tobacco and alcohol consumption, obesity, physical inactivity)[5]. Furthermore, exposures from cardiotoxic anticancer therapies such as conventional chemotherapeutic agents (anthracyclines-based) and monoclonal antibodies (trastuzumab) aggravate the risk[6–8]. Cancer therapy-related cardiac dysfunction (CTRCD) usually occurs in the first year after cancer diagnosis, while the risks remain elevated throughout the follow-up time [1]. For this reason, the goals of developing the cardio-oncology discipline came with two main intentions: 1) to provide the best cancer therapies available with minimal impact on CV health and; 2) to conduct CV surveillance throughout the spectrum of cancer therapies [9].

Despite recognition of these complications, incorporation of cardiovascular risk assessment as part of routine clinical practice remains a challenge. Several expert societies have released monitoring and management approaches for patients undergoing potentially cardiotoxic anticancer therapy but its implementation may not be straightforward, given that it is an emerging field [10–13]. Koop et al reported that although almost one third of breast cancer patients received high risk cardiotoxic treatments, cardiac surveillance or risk assessment was rarely performed. The main cardiac care provided was ECG at 52.0% whereas echocardiography was only in 17.7%, and measurement of Troponin and NT-proBNP in 5.1 and 5.8%, respectively. There was also an observed substantial variation of practice between different hospital types and between individual hospitals[14].

To date, reasons for the lack of translation of these guidelines into clinical practice have been explored via isolated, small studies looking into practices related to management of CTRCD [15–18]. Among the reasons quoted include definitions of cardiovascular toxicity, appropriate duration for cardiovascular follow-up, and shared decision making between oncologists and cardiologists regarding anti-cancer drugs[19]. Nonetheless, there has yet to be an effort to consolidate this information systematically. In fact, many of the identified factors could potentially circulate around the same underlying problems, albeit in an unstructured manner.

As such, our review aimed to summarise available evidence on factors influencing physicians’ decision to conduct cardiovascular risk assessments among cancer patients and to assess the inter-relationship between these factors. We employed the domains of the Tailored Implementation for Chronic Diseases (TICD) framework to systematically categorize these factors[20]. With this approach, we hope to synthesize important attributes that can be utilized to guide the implementation of cardiovascular risk assessment programs for cancer patients in clinical practice.

Study registration

This review protocol was registered in PROSPERO International prospective register of systematic reviews (26.05.2022, registration: CRD42022335451). The study was exempted from institutional ethics approval as it did not involve any human subjects. The reporting for this systematic review follows the Meta-analysis of Observational Studies in Epidemiology (MOOSE) guidelines (Additional file 1).

Eligibility criteria

A study was eligible for inclusion if it (1) was in English language and published from 1st January 2012 to 30th June 2022, (2) involved adult cancer patients 18 years old and above and, (3) included factors influencing physicians’ decision to conduct cardiovascular risk assessment for cancer patients. Definition of cardiovascular risk assessment was adopted from the Cardio-Oncology Study Group of the Heart Failure Association of the European Society, which defines it as ‘the cardiovascular assessment occurring prior to the initiation of cancer treatment’[21]. Conference abstracts, study protocols and non-peer reviewed published reports were excluded as those contained negligible information. The primary outcome evaluated in this review was compilation of factors influencing physicians’ decision to conduct cardiovascular risk assessment among cancer patients. Any factors, either barriers or facilitators were considered in this review and they did not need to be the primary outcome of interest of a study to be considered for inclusion.

Search strategy

Searches were performed on five electronic databases: PubMed, EMBASE, CINAHL, Web of Science and PsycINFO. The search strategy included keywords and medical subject headings (MESH) terms as shown in Additional File 2. Reference lists of included articles were also searched for relevant papers.

Study selection process

All searches were transferred into a semi-automatic citation screening software (Abstrackr) to conduct screening by study title and abstracts[22]. Two reviewers (HST and SS) conducted articles screening independently. Pilot test was performed on the first ten articles to ensure validity and consistency of the screening process. Articles were rejected if they failed to meet the inclusion criteria, as determined from the title, or abstract of the study. When an abstract cannot be rejected with certainty, the full texts of these potentially eligible studies were retrieved and independently assessed for eligibility. All reasons for exclusion will be documented and listed. Non-accessible articles were excluded. Disagreements were resolved via discussion and subsequently, opinion from a third reviewer (WYH) if disagreement persists. A similar process was carried out for the full text eligibility of the articles.

Risk of bias assessment

Risk of bias assessment was conducted by HST and SS. The methodological quality of the included studies was evaluated using tools appropriate for each study design. The Joanna Briggs Institute (JBI) Critical Appraisal Checklist was used to assess qualitative study and opinion papers. The Mixed Methods Appraisal Tool (MMAT) was utilized to assess quantitative descriptive papers.

Data extraction and synthesis

A standardized data extraction form was developed for this review, which included bibliographic details, population, objectives, study methods and findings. Similarly, two reviewers independently extracted the data and resolved any discrepancies; if necessary, with help from WYH. Data synthesis was accomplished in a few stages: (1) directly extracting identified factors from the included studies, (2) deriving codes that reflected key concepts highlighted in the factors, (3) thematically matching these codes into the categories of TICD framework, (4) systematically summarising domains in the framework, while entering illustrative quotes to reflect the specific factors. To enhance interpretation of the findings, the review team identified the inter-relation of those domains through an iterative inductive approach from the extracted data and categorized them into macro and micro levels to lay out potential avenues to shape intervention and implementation strategies.

Tailored Implementation in Chronic Disease framework (TICD)

TICD framework was developed to identify determinants that could guide and design appropriate implementation strategies, particularly related to healthcare professional practice. It encompasses 57 potential determinants of practice grouped in seven domains: guideline factors, individual health professional factors, patient factors, professional interactions, incentives and resources, capacity for organisational change, and social, political, and legal factors. This framework is well-established and has been widely applied to understand the pivotal determinants for implementation of interventions against different diseases[23–25].

The final search consisted of 11,488 unique studies that met the inclusion criteria after removing duplicates. Four additional articles were obtained by citation searching. Out of these, 11,438 studies were excluded based on title and abstract. Fifty studies were then subsequently screened in full-text after removing four articles with no full access. Thirty-eight studies were removed after assessing their eligibility, due to following reasons: no factors indicated (n = 30), population not matched (n = 4) and factors related to strategies to set up cardio-oncology programs rather than the CV assessment itself (n = 4). Twelve studies were included in the final synthesis (Fig. 1).

Characteristics of included studies

Studies were predominantly survey-based/quantitative research with a cross-sectional design (n = 8), followed by opinion articles (n = 3) and qualitative research (n = 1). Most studies were conducted in the Western population where cardio-oncology has gained significant attention, such as United States (n = 5), France (n = 2), the Netherlands(n = 2), and one each from Nigeria, Italy, and Canada. The study population was diverse across all papers, with a mixture of cardiologist, oncologist, cancer epidemiologist, nurses, and CV fellowship program directors. Characteristics of the included studies were summarized in Table 1.

Table 1

Characteristics of included studies
Author, publication year, country	Type of study	Population involved	Aims	Sample size	TICD domains cited in the studies
Canale ML et al., 2021, Italy	Quantitative descriptive	regional Associazione Nazionale Medici Cardiologi Ospedalieri (ANMCO) presidents, regional cardio oncology delegates (identified by the presidents), and the referral cardiologists of each CO service across Italy	to characterize the activity of cardio-oncology (CO) services across Italy; to explore their network of cancer treating physicians, general practitioners, and out-of-hospital cardiologists; and to analyse their educational needs.	96 centres	Professional interactions, Incentives and resources
Jovenaux, L. et al., 2017, France	Quantitative descriptive	French medical oncologists working in teaching and non-teaching hospitals, cancer centres and private healthcare facilities in France (data from the French National Medical Council)	to determine the current practices of oncologists regarding cardiovascular toxicity related to anthracyclines, trastuzumab and angiogenic inhibitors and to gather their opinions on the development of cardio-oncology programs	303	Individual health professional factors
Koop, Y. et al., 2022, Netherlands	Quantitative descriptive	Cardiologists, medical oncologists, haematologists, and radiation oncologists	to evaluate current perspectives on cardio-oncology and to assess needs, ultimately to determine an agenda for improvements in current practice	190	Individual health professional factors
Peng J. et al., 2019, Canada	Quantitative descriptive	HCPs included cardiologists, oncologists, and others such as general internists, cardio-oncologists, paediatric oncologists, radiation oncologists, cardiac rehabilitation therapists, nurse practitioners, research students, and pharmacists	to assess clinicians’ understanding of cardio-oncology, opinions towards current practice, and approach to diagnosing and managing cancer therapy related cardiac dysfunction (CTRCD)	160	Individual health professional factors, incentives and resources
I. Mahé et al., 2017, France	Quantitative descriptive	French Society for Vascular Medicine (SFMV) and the Association for Supportive Care in Oncology (AFSOS) members	to assess the awareness of treatment guidelines and the management of patients with CAT in daily clinical practice	401	Individual health professional factors
Ana Barac et al., 2015, US	Quantitative descriptive	adult and paediatric Cardiology Division Chiefs and CV Fellowship Program Training Directors	to summarize the key current aspects of interdisciplinary cardio-oncology clinical care delivery and education in the United States and outline how these data provide a platform for future development of the field	444	Incentives and resources, individual health professional factors
K. Albert et al., 2021, USA	Quantitative descriptive	nurse practitioners and physician assistants (advanced practice providers [APPs]), and medical doctors (MDs) who work in three outpatient hematology medical oncology clinics were approached	to determine whether sharing of evidence-based literature heightened oncology provider knowledge of CTx and changed practice behaviors such that they aligned more closely with evidence-based American Society of Clinical Oncology (ASCO) and National Comprehensive Cancer Network (NCCN)recommendations	12	Incentives and resources, capacity for organisational change, individual health professional factors
D. Sadler et al., 2020, USA	Quantitative descriptive	cardiologists and oncologists in Florida	to determine current levels of awareness and to identify opportunities to enhance and expand education and address knowledge gaps for both specialist groups	303	Individual health professional factors, professional interactions, incentives and resources, capacity for organizational change
Koop, Y. et al., 2021, Netherlands	Qualitative	oncologists (N = 6), a cancer epidemiologist (N = 1), and oncology nurse practitioners (N = 5)	to qualitatively explore the perceptions of oncology professionals regarding cardiac surveillance in breast cancer patients and, more specifically, the influencing factors of delivering cardiac surveillance.	12	Incentives and resources, Guideline factors, Individual health professional factors, professional interactions, patient factors
Anakwue, R. et al., 2020, Nigeria	case report & review	NA	to discuss peculiar challenges in the management of cytotoxic-induced heart failure in Nigeria	NA	Incentives and resources, professional interactions
Tochi M. Okwuosa et al., 2018, US	Review	NA	discuss some of the challenges being tackled by small- to moderate-sized and some larger academic centres, particularly the cancer centres without National Cancer Institute designation	NA	Capacity for organizational change, incentives and resources, guideline factors, professional interactions, individual health professional factors
Tolulope A. Agunbiade et al., 2019, USA	Review	NA	discuss the development of a cardio-oncology program in a health care organization with a focus on the different needs and perspectives of multidisciplinary team members including cardiovascular and oncology specialists as well as health care administrators	NA	Incentives and resources, professional interactions, individual health professional factors, capacity for organisational change

Quality of included studies

All 12 studies were deemed to be of high quality, except for an unclear risk of nonresponse bias for descriptive quantitative studies (survey-based) as it was not reported in the included papers. Additional file 3 provides a detailed assessment of the risk of bias for all included studies.

Identified factors

Using the TICD framework, the identified factors were categorised into six domains: guideline factors, individual health professional factors, patient factors, professional interactions, incentives and resources and capacity for organizational change. The top three cited domains were individual health professional factors (83% of the studies), incentives and resources (75% of the studies), and professional interactions (58% of the studies). We summarized relevant illustrative codes in Table 2 based on its determinants and domains and narratively presented the main findings according to the domains as below. Figure 2 shows the relation between domains and its key determinants at different level of approaches.

Table 2

Identified domains and quotes from included studies
Domains	Determinants	Illustrative quotes taken from articles
Individual health professional factors	(i) Knowledge and skills	• Domain knowledge/Awareness and familiarity with the recommendation/skills needed to adhere: “35% oncologists adopted method for managing cardiovascular toxicity based on guidelines from expert oncology societies, none was aware of recommendations from expert cardiology societies” “38% of oncologists were unaware of the existence of early screening methods for left ventricular dysfunction”[16] “21 cardiologists (31.8%), 43 radiation oncologists (65.2%), and 35 haematologists or medical oncologists (60.3%) stated either they were unaware of the definition in their hospital or there was no clear definition”[27] “Most professionals were not convinced that increased cardiac monitoring can prevent CTRCD or improve quality of life. Those in favor of cardiac monitoring mentioned their colleagues’ lack of knowledge on the topic as a barrier”[15] “The National Cancer Research Institute recommends interruption of trastuzumab if the LVEF decreases to < 45% and reinitiation of treatment when the LVEF recovers to > 49%. This evidence-based answer was selected by 44.0% of cardiologists and 43.8% of oncologists”[26] “Less than half of specialists (43.9%) were aware of AFSOS treatment guidelines whereas a majority of them (74.3%) considered that other guidelines had an influence on the decision for an anticoagulant treatment. This included French guidelines (42.4%), International guidelines (26.4%) or academic references (17.7%)” [28] “In most cases, the focus for care of the typical oncology patient is the cancer, while other not-so-active disease processes—particularly those involving prevention—recede to the background” [29] “Many programs reported having no formal training in cardio-oncology (43%), with some institutions offering exposure during regular clinical rotations (43%), and a small number including lectures in cardio-oncology as part of the Core Curriculum (11%)” [29] • Knowledge about own practice: “For anthracyclines, management was inconsistent for asymptomatic patients with an LVEF between 40 and 50% and relatively consistent in all other cases. For trastuzumab, the management was inconsistent for all cases unless for asymptomatic patients with an LVEF between 40% and 50%”[16]
	(ii) Cognitions & attitudes	• Agreement with the recommendation/Attitudes towards guidelines in general “Only twelve (18.2%) cardiologists, one (1.7%) haematologist, no medical oncologists, and two (3%) radiation oncologists agreed to treat asymptomatic LVEF decline during trastuzumab treatment with appropriate cardiac medications and monitor LVEF during follow-up”[27] “Most professionals did not feel the need to change current practice regarding cardiac surveillance despite the increasing awareness” [15] “Though the majority of all professionals deviated from current recommendations and would continue capecitabine treatment. A total of 26 professionals (13.7%) of which 20 were cardiologist would continue capecitabine combined with a calcium channel blocker”[27] “62.1% cardiologists were aware of the ESC cardio-oncology position paper and 22.7% of the multimodality imaging consensus statement of the European and American imaging associations, and 54.5% use these guidelines in current practice”[27] “Different perception on the value of cardio-oncology clinics or when cardiologists should be involved in caring for cancer patients: 55.8% cardiologist felt they should monitor cardiotoxicity even in the absence of symptoms - only 12.5% oncologists agreed. 50.0% of oncologists felt that cardiologists should be involved only when patients developed cardiotoxicity. Only 6.5% of cardiologists selected this answer” [26] • Emotions and personal feeling: “64% of oncologists believed that with regard to the cardiovascular toxicity of cancer therapies, the level of knowledge of the cardiologists with whom they worked could be improved, and 26% believed that this knowledge was insufficient”[16] “perception of oncologists that cardiology waiting lists are usually long prevented them from referring their patients for cardiac screening because they feared this would significantly delay cancer treatment” [15] “In contrast, only 8.2% of oncologists strongly agreed that cardiologists were knowledgeable about cardiotoxicity and were comfortable treating these complications”[26] • Expected outcome “All professionals were aware of the cardiotoxic effects of anthracycline- and trastuzumab based regimens. They all clarified that their delivery of cardiac surveillance was mainly driven by their sense of (or lack of) urgency; they did not perform any form of cardiac surveillance mostly because they did not recognize the advantages” [15] “Some oncologists disclosed that cardiac monitoring in cancer patients was not a priority for cardiologists because of anticipated poor cancer prognosis” [15] “88.3% cardiologists believed that access to cardioonco services would significantly improve cancer patients' prognosis - only 45.8% oncologists shared this opinion” [26] “Cardiologists felt strongly that access to cardio-oncology clinics would improve prognosis for cancer patients; oncologists were less convinced”[26] • Self-efficacy “Several cardiologists strongly agreed they were knowledgeable about cardiotoxic complications from cancer therapy (48.8%; n = 42) and were comfortable treating these complications (41.0%; n = 35). Very few (2.1%) oncologists strongly agreed that they were comfortable treating cardiovascular complications of cancer therapy” [26] “a difference in risk tolerance for cardiotoxicity between specialties. In the setting of metastatic cancer, more cardiologists (36.7%) accepted a higher risk of cardiotoxicity (5–10% risk) compared to oncologists (20.0%)” [26]
	(iii) Professional behaviour	• Nature of the behaviour “The assumed low incidence of cardiac events in their patient population was the main cause and played a key role in the professionals’ clinical decision making. Oncologists indicated that they rarely treated BC patients with CTRCD; therefore, they perceived the occurrence of (adverse) cardiac events during cancer treatment as rare” [15] • Capacity to plan change “Overwhelmed with administrative and clinical responsibilities, Challenging to balance responsibilities” [30]
Professional interactions	(i) Communication and influence	“66.6% of general hospitals and 44% cancer centers did not share information on patients with territorial cardiologists in a planned way”[17] “Poor collaboration between oncologists and cardiologists in doing proper assessment of cardiotoxicity and managing appropriately all cardiovascular events resulting from therapy with cytotoxic agents” [31] “This last issue usually requires reliance on cardio oncology ancillary staff, and keeping open the lines of communication with the oncologists, advanced practice providers, and other cardio oncology health care providers” [29] “Interestingly, fewer than one-half of respondents felt that there was optimal cooperation between their specialties” [47]
	(ii) Team processes	“83% of professionals believed that multidisciplinary collaboration is not necessary nor recommended in the literature” [15] “One of the biggest challenges to overcome is bringing together the various service lines in this multi-disciplinary team to foster effective collaboration and facilitate the nuanced management of these at-risk patients” [48]
	(iii) Referral processes	“Such a balance is often difficult to achieve in the cancer patient suffering from anorexia and gastrointestinal complications of cancer therapy (nausea, vomiting, and even diarrhoea), and requires close collaborations between the onco-cardiologist and the cancer center nutritionist or dietician” [29]
Incentives & resources	(i) Availability of necessary resources	“Uneven distribution of Cardio oncology appears where majority CO team present in cancer centre (56%) but only 20% in a general hospital”[17] “ “Oncologists disclosed a knowledge gap regarding the necessity for cardiac surveillance which is mainly due to a lack of data on long-term benefits and cost effectiveness”[15] “The availability and affordability of less toxic agents and investigative tools such as ECG and echocardiography are a big challenge in developing countries” [31] “..barriers to the development of cardio-oncology clinics were due to limited funding (68.0%) and limited infrastructure (54.0%)”[26] “Although the cardiology nurse is well versed in CVDs and testing, the oncology nurse understands cancer patients and their medical, social, and psychological needs, particularly while undergoing cancer treatment. One is hard pressed to find the ideal nurse that spans both specialties… most institutions that have a cardio-oncology service employ only 1 onco-cardiologist” [29] “EMR embedded reminders to screen would be helpful” [30]
	(ii) Continuing education system	“Vocational training paths still represent an unmet need of cardio oncology staff”[17] “38.0% of all respondents reported that formal training in cardio-oncology was lacking”[26] “The diversity and lack of standardization in training and practice within the pockets of training institutions in cardio oncology throughout the United States, calls for formalized (Accreditation Council for Graduate Medical Education accredited) training in this new subspecialty” [29] “Importantly, 70% of respondents reported that they would be likely to use educational material for their fellows and staff, if those were available. Over one-quarter (27%) of respondents (N = 29) offered additional comments to express needed support in the field of cardio-oncology, specifically the need for educational materials and dedicated meetings (25%), training and curriculum (22%), clinical relevance and growth (19%), and the development of guidelines (13%)” [18]
	(iii) Assistance for clinicians	“All professionals acknowledged the need for practical tools in delivering cardiac surveillance for BC patients. They also underlined the need for clinical protocols and guidelines for cardiac surveillance, with a focus on risk stratification, to distinguish between high- and low-cardiovascular-risk patients and tailor cardiac surveillance accordingly” [15] “Lack of national guidelines …were the most frequently cited barriers to the establishment of a cardio-oncology service” [18]
	(iv) Financial-related	“…there are challenges in the affordability of simple and basic investigative tools such as ECG and echocardiography. The cases cited in this report could barely afford the cost of investigations. The patients were in fact lost to follow-up perhaps due to financial problems” [31] “Even the need for serial echocardiograms in the patient receiving cardiotoxic chemotherapy can sometimes present challenges for coverage. Additionally, Medicare would cover screening tests such as B-type natriuretic peptide and troponin I—with very good data to support their use in screening for cardiomyopathy in patients receiving cardiotoxic chemotherapy—only if there is an associated heart failure diagnosis” [29]
Guideline factors	(i) Accessibility of the recommendation	“All professionals indicated that strict clinical protocols (based on guidelines) for the detection of cardiotoxicity during and after cancer treatment are lacking” [15]
Guideline factors	(ii) Clarity of the recommendation	“As new as this subspecialty is, there are no actual societal guidelines to help standardize clinical practice, despite a few consensus statements” [29]
Patient factors	(i) Patient needs	“Professionals stated that they want to avoid overwhelming their patients with extensive information on possible cardiac side effects before the start of essential or even life-saving cancer treatment” [15]
Patient factors	(ii) Patient beliefs and knowledge	“Professionals also believed that patients are not very concerned about their cardiovascular health when first diagnosed with BC and also not during or after cancer treatment because staying alive is assumed to be considered of higher importance after a cancer diagnosis” [15]
Capacity for organizational change	Mandate, authority and accountability	“This often places the onco-cardiologist in the difficult position of being “stuck in the middle” of the 2 medical sections and divisions, particularly regarding funding of clinical, administrative, and sometimes educational and research-related needs” [29]
Capacity for organizational change	Capable leadership	“Mentorship and training in this field is a challenge that is faced by many cardiologists, oncologists as well as cardiology and oncology fellows given the limited availability of experts in this area” [48]

Micro level

(i) Individual health professional factors

Individual health professional factors were highly cited as a key factor to influence the conduct of cardiovascular risk assessment. There were three main determinants under this domain, which include cognitions and attitudes, knowledge and skills, and professional behaviours. Cognitions and attitudes contributed as barriers where physicians’ agreement with recommendations and attitudes towards guidelines in general were poor. Most professionals did not feel the need to change their current practice regarding cardiac surveillance despite the increasing awareness of its importance [26]. There were also different opinions between the oncologists and the cardiologists on elements to be included in the standard of care for cancer patients. The oncologists disclosed that cardiac monitoring in cancer patients was not a priority because of the anticipated poor cancer survival. On the contrary, the cardiologists believed that access to cardio oncology services would significantly improve cancer patients' prognosis [15, 26]. Disparities in the expected patient outcome between these two main pillars of cardio oncology services were frequently discussed. We also found that emotions and personal feelings hindered the smooth implementation of cardiovascular risk assessments among cancer patients. Some of the oncologists deemed their counterpart cardiologists as less knowledgeable in terms of specific training to cater for their cancer patients[15, 26]. In general, there was a noticeable knowledge gap in the awareness of available guidelines[16, 26–28], cardiovascular investigative tools [16], and the importance of CV disease prevention[29]. The oncologists would mainly adopt the management of cardiovascular toxicity from guidelines developed by oncology societies but with low awareness of recommendations by the cardiology societies[16]. Importantly, the move to introduce changes such as adding CV risk assessment into physicians’ professional practice is another challenge, whereby oncologists perceive the occurrence of (adverse) cardiac events during cancer treatment as rare[15]. Even with the acknowledgement of the importance of this preventive method, their capacity to conduct this screening is difficult as they were often overwhelmed with current clinical and administrative responsibilities[30].

(ii)Professional interactions

In this domain, three main determinants that needed attention included: communication and influence, team processes and referral processes. Poor interdisciplinary communication and lack of a proper referral pathway from cancer centre to cardiology centre were cited in several studies[17, 29, 31, 32]. It is also worth highlighting that 83% of professionals in one study believed that long-term multidisciplinary collaboration is not recommended as they perceived occasional consultation with a cardiologist as sufficient[15].

Macro level

(i) Incentives and resources

There were four main relevant determinants in this domain: availability of necessary resources, assistance for clinicians, continuing education system and financial-related. In the context of providing cardio oncology services, some pre-requisite resources for a structured cardiac surveillance were fundamental, such as availability of onco-cardiologist and ancillary staff, facilities, and funding to support its long-term development [15, 17, 29]. Amidst the mentioned requirements, shortages of healthcare personnel and facilities were commonly cited. Under such resource constraints, there was a practical need for risk stratification tools to prioritise high cardiovascular-risk patients, which was not available at the current moment. Formal vocational training in cardio-oncology was also highlighted as an unmet need [17, 26]. Appropriate diagnostic and monitoring tools such as echocardiography were also greatly needed in the provision of CV risk assessment but its availability and affordability especially in developing countries remain a huge issue [15, 18, 31]. Besides, financial-related issues were observed to occur from the patients’ perspective as well, whereby the conduct of CV screening is often not included in their insurance coverage, unless there is a confirmed CV diagnosis [29].

(ii) Capacity for organizational change

In a review related to challenges tackled by cancer centres which deliver cardio-oncology services, there was a lack of accountability between oncology and cardiology disciplines, particularly regarding clinical, administrative, educational, and research-related needs [29]. As this involves interdisciplinary effort, there is also a need for capable leadership to provide mentorship and to facilitate the uptake of screening [30, 32, 33].

(iii) Guideline factors

Despite the availability of a few consensus statements from the fields of oncology and cardiology, there was a lack of standardization in CV risk monitoring at different stages of the cancer treatment plan. CV risk assessment post-cancer therapy was prescribed significantly less often for all therapies compared to pre-cancer therapy[16]. Furthermore, the recommendations for clinical practice were usually limited to older well-known drugs such as anthracyclines[29]. Lesser guidance on the conduct of CV risk assessment were available for newer cancer therapy, especially when accompanied by more intricate underlying conditions in cancer patients. In terms of long-term sustainability, clinicians emphasized the need for clinical protocols and guidelines for cardiac risk stratification, to prioritise high-cardiovascular-risk patients for surveillance accordingly[15].

(iv)Patient factors

This domain was less addressed in the included studies but in one qualitative study, the healthcare providers expressed their reluctance to conduct CV risk assessment on their patients because they intended to avoid overwhelming their patients with extensive information pertaining to cardiac side effects of cancer treatment. Also, they believed that patients were not very concerned about their CV health throughout their cancer journey[15].

Inter-relationship between domains

Considering the above identified macro and micro level factors, we identified the inter-relationship between those domains (Fig. 2). At macro level, we consolidated issues pertaining to external context as a supportive backbone of cardiovascular risk assessment practice. Those four domains highlighted challenges in terms of capacity for organizational change, incentives and resources, guideline, and patient factors. Some domains are more closely interrelated, as illustrated in Fig. 2 where facilitators from one domains influence challenge from another domain through certain determinants. The cyclical associations were postulated, whereby organizational change could impact on the execution of guidelines and the allocation of resources, and both domains in turn are dependent on the magnitude of the patient’s needs. The financial resources needed on the ground level are not only limited to facilities and screening equipment, but also to reimburse patients to undergo CV risk assessment under an appropriate healthcare finance scheme [29, 34]. To establish a feasible and relevant guideline on cardiovascular risk assessment among cancer patients in one setting, having a concrete proof of value to introduce cardiovascular risk assessment as part of the routine care in the guidelines is crucial [34]. This value is conceptualised as patients’ needs, which are hardly measured as physicians mainly focus on cancer care and many patients are not aware of cardiac side effects of their therapy [15].

Domains related to individual health professional factors and professional interactions highlighted challenges at the micro level. Although these factors revolve around personal level, they are inter-related to the domains at macro level, particularly relying on the latter to create a conducive practising environment. Under the domain of individual health professional factors, we identified that cognitions and attitudes, specifically their agreement towards guidelines, personal emotions, expected outcome from performing cardiovascular assessment and self-efficacy (self-perceived competence) were the significant barriers to overcome. These determinants also cut across the domain of professional interactions, as the resulting behaviours will influence how likely they will engage the other disciplines for collaboration.

This systematic review highlights two main messages to clinicians and policy-makers who intend to improve the conduct of CV risk assessment among cancer patients, in parallel with strategizing a successful implementation of cardio-oncology services in their respective settings. First, the evidence showed that factors influencing physicians to conduct cardiovascular risk assessment were similar across different countries with the main ones being categorised into the domains of individual health professional factors, incentives and resources and professional interactions, although the magnitude of these factors may differ. Second, the identified domains are inter-related and they work synergistically for a successful cardiovascular risk assessment practice.

Cognitions and attitudes, coupled with the capacity of the clinicians to exert change (given the time and resources) underlie the fundamental issue of poor cardiovascular screening uptake. At this current moment, there is a clear disjuncture between oncology and cardiology disciplines, particularly in recognition of the advantages of conducting CV screening at different stages of the cancer journey, the definitions and risk tolerance of cardiotoxicity [26, 35]. Interestingly, in a survey by the Florida Chapter of the American College of Cardiology (FCACC) and the Florida American Society of Clinical Oncology (FLASCO), more than half of the oncologists rated their knowledge of cardio-oncology as above average but only one- seventh were comfortable treating those patients[33]. This signifies that having knowledge alone is insufficient to take clinical actions on those patients in need. The initiative to start this preventive clinical practice requires a wheel of behavioural change among the physicians. At the same time, pathways in cardio-oncology services for cancer patients could be complicated and treatment decisions require established knowledge of both diseases. More often, oncologists and cardiologists prefer to refer to the guidelines recommended by their own expert societies rather than those developed by other disciplines. One such example was reported in a survey where only 12.5–25% of cardiologists used or were aware about the recommendations of the European Society of Medical Oncology (ESMO) and American Society of Clinical Oncology (ASCO) in comparison to 62–78% following the ESC/Ukrainian Cardiology guidelines [36]. This discrepancy in knowledge results in heterogeneity and inconsistencies across different drug therapies and disciplines[37]. Logically, improving communication and team processes could alleviate the issue, but underlying negative presumptions about their counterpart’s capability and lack of trust will need to be tackled first.

Incentives and resources can provide immediate help to physicians wanting to conduct cardiovascular assessment. However, the privilege of having structured vocational training and investigative tools could be a struggle in most developing countries. The practical allocation of such resources would largely depend on the magnitude/burden of the disease, which is still limited in the area of cardio oncology now. While acknowledging that resource constraint is a long-standing issue, we found that barriers within contextual factors could be mitigated by capacity change in an organization. The influence of such institutional support was particularly evident in review papers that described challenges in setting up cardio-oncology services[38, 39]. In thematic analysis of other studies, system-level challenges related to long-term care coordination for cancer survivors with chronic conditions have also been addressed similarly. In particular, leadership awareness and acknowledgement of the need for care coordination play a role in improving patient’s access[40]. Nonetheless, the imposition of such practice through a hierarchical organization mechanism could backfire, as the local health system may have distinct challenges to face, such as those barriers stipulated at the micro level[41]. Thus, a more refined approach incorporating shared leadership and understanding of the causal chain may lead to an effective transition from oncology care to long-term inter-organisational collaboration[42, 43]. Putting this together, creating an ecosystem to improve access to cardiovascular screening involves domains that are interacting intricately and any intervention forward will need to be carefully planned[44].

Strengths and weaknesses of this study

This review provides novel insights into the associations between factors influencing physicians’ decision making of cardiovascular risk assessment, with each domain having a possible influence on the others. This was made possible via the conduct of inductive analyses along with deductive analyses of categorising the identified factors into domains. By aggregating the factors systematically and assessing the interrelationship between these domains, we hope that it will provide a guide to plan for relevant interventions in improving CV risk assessment among cancer patients, which could be tailored to the local context where possible. Rigorous search strategy across extensive databases has also been applied in this review, with little chance that relevant information was missed.

We acknowledge that this review comes with some limitations. Papers written in languages other than English were excluded, and most studies were conducted in developed countries. It is unsurprising as this new endeavour of cardio-oncology is growing more rapidly in these parts of the world. In the absence of sufficient information from the developing countries, we believe that the summarized evidence here would remain beneficial to be considered in the plans to develop the cardio-oncology discipline and improve the uptake of CV risk assessment across the resource-poor settings.

Study implications and future directions

Through this review that looks at factors in different contexts, we managed to draw a coherent framework related to facilitating the implementation of cardiovascular risk assessment for both clinicians and organizations. What stood out the most among these factors is the domain related to individual health professionals, who are expectedly the key drivers of this cardiovascular risk assessment process. Future directions could focus on practical mechanisms to impart behavioural change among them such as providing continuous updates on the burden of cardiovascular disease among cancer patients. However, shifting behaviour in a complex dynamic system like a hospital may take longer than expected and more ongoing effort is needed to sustain the modifications[45]. We shed new light on the dynamics of the external contributing factors that could facilitate the work process. The findings here could be potentially brought forward to further discussion in local settings, for example, forming the basis of multi-criterion decision analysis to design the most promising interventional program. Ideally, advocacy efforts in this area need to be supplemented by mechanisms to improve access to care customised by the capability of the institutions. Based on the current scenario, those emerging cardio-oncology programs remain confined to larger and academic-based institutions in developed countries. Huge efforts are still needed in resource-limited settings, to ascertain who is best to lead and how to develop a sustainable cardio-oncology program. Therefore, future directions should explore practical ways of sharing the responsibility of long-term care for this cancer population that can be reproduced in a variety of different settings. Task shifting to general practitioners (GPs), instead of limiting this role to oncologists or cardiologists who have been overloaded with current work, could be a possible alternative to mitigate the resource issue. This pathway has been practised in England, whereby approximately half of GPs reported often providing care to people living beyond cancer for treatment-related side effects [46]. However, this successful transition from curative to long-term survivorship care is underpinned by sharing leadership with patient-family, oncology, and primary care teams. The coordinated care involves fluid distribution of responsibilities among the multiple team members. Parallelly, this shared leadership can help to overcome at least three types of barriers impeding the quality and safety of transition to survivorship: attitudes, knowledge, and professional organizational boundaries[42]. While the effectiveness of such intervention is beyond the scope of this review, we hope that the analysis of the interrelationship between domains here might lead to more sustainable interventions in the future.

In conclusion, we have identified factors influencing physicians’ decision to conduct cardiovascular screening among cancer patients from different aspects. Our findings suggest that the integration of such assessment into clinical practice lies heavily in the acceptance of the healthcare professionals. While progressive efforts to improve public access to such programs are ongoing, a more targeted approach to behavioural change of relevant stakeholders could be a promising start.

Ethical Approval: Ethical approval for this study was waived.

Consent for publication: We have obtained permission from the Director General of Health Malaysia to publish this article. All authors agreed on the publication.

Availability of data and materials: The datasets used and/or analysed during the current study is available upon request.
Conflicts of interests: The authors declare that they have no conflicts of interests.

Funding: There was no involvement of funding in this study.

Contributors:

All authors (HST, SS, MT, WYH) were involved in conceptualizing the review. HST, SS, WYH: refining the search terms defining the inclusion/exclusion criteria. HST carried out preliminary database searches. Two authors (HST, SS) screened the articles that met the inclusion criteria and conducted data extraction and quality review. HST wrote the first draft of the manuscript. All authors made significant contributions to subsequent drafts and approved the final manuscript.

Acknowledgements: We would like to thank the Director General of Health Malaysia for his permission to publish this article.

Sturgeon KM, Deng L, Bluethmann SM, Zhou S, Trifiletti DM, Jiang C, et al. A population-based study of cardiovascular disease mortality risk in US cancer patients. Eur Heart J. 2019;40:3889–97.
Schoormans D, Vissers PAJ, van Herk-Sukel MPP, Denollet J, Pedersen SS, Dalton SO, et al. Incidence of cardiovascular disease up to 13 year after cancer diagnosis: A matched cohort study among 32 757 cancer survivors. Cancer Med. 2018;7:4952–63.
Strongman H, Gadd S, Matthews A, Mansfield KE, Stanway S, Lyon AR, et al. Medium and long-term risks of specific cardiovascular diseases in survivors of 20 adult cancers: a population-based cohort study using multiple linked UK electronic health records databases. Lancet (London, England). 2019;394:1041–54.
C A, Tomohiro, Carlo V di, Harewood R, Matz M, Bonaventura A. Concord-3. Lancet. 2018;391:1023–75.
Koene RJ, Prizment AE, Blaes A, Konety SH. Shared Risk Factors in Cardiovascular Disease and Cancer. Circulation. United States; 2016;133:1104–14.
Bohdan M, Kowalczys A, Mickiewicz A, Gruchała M, Lewicka E. Cancer Therapy-Related Cardiovascular Complications in Clinical Practice: Current Perspectives. J Clin Med [Internet]. 2021;10:1647. Available from: https://www.mdpi.com/2077-0383/10/8/1647
Angsutararux P, Luanpitpong S, Issaragrisil S. Chemotherapy-Induced Cardiotoxicity: Overview of the Roles of Oxidative Stress. Oxid Med Cell Longev. 2015;2015:795602.
Cardinale D, Colombo A, Lamantia G, Colombo N, Civelli M, De Giacomi G, et al. Anthracycline-induced cardiomyopathy: clinical relevance and response to pharmacologic therapy. J Am Coll Cardiol. United States; 2010;55:213–20.
de Wall C, Bauersachs J, Berliner D. Cardiooncology-dealing with modern drug treatment, long-term complications, and cancer survivorship. Clin Exp Metastasis. 2021;38:361–71.
Curigliano G, Lenihan D, Fradley M, Ganatra S, Barac A, Blaes A, et al. Management of cardiac disease in cancer patients throughout oncological treatment: ESMO consensus recommendations. Ann Oncol. 2020;31:171–90.
Armenian SH, Lacchetti C, Barac A, Carver J, Constine LS, Denduluri N, et al. Prevention and Monitoring of Cardiac Dysfunction in Survivors of Adult Cancers: American Society of Clinical Oncology Clinical Practice Guideline. J Clin Oncol Off J Am Soc Clin Oncol. United States; 2017;35:893–911.
Zamorano JL, Lancellotti P, Rodriguez Muñoz D, Aboyans V, Asteggiano R, Galderisi M, et al. 2016 ESC Position Paper on cancer treatments and cardiovascular toxicity developed under the auspices of the ESC Committee for Practice Guidelines: The Task Force for cancer treatments and cardiovascular toxicity of the European Society of Cardiology (ES. Eur J Heart Fail. England; 2017;19:9–42.
Plana JC, Galderisi M, Barac A, Ewer MS, Ky B, Scherrer-Crosbie M, et al. Expert consensus for multimodality imaging evaluation of adult patients during and after cancer therapy: a report from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr Off Publ Am Soc Echocardiogr. United States; 2014;27:911–39.
Koop Y, El Messaoudi S, Vermeulen H, Maas AHEM, Atsma F. Healthcare utilization and hospital variation in cardiac surveillance during breast cancer treatment: A nationwide prospective study in 5000 Dutch breast cancer patients. Cardio-Oncology. Cardio-Oncology; 2020;6:1–9.
Koop Y, Dobbe L, Maas AHEM, van Spronsen DJ, Atsma F, El Messaoudi S, et al. Oncology professionals’ perspectives towards cardiac surveillance in breast cancer patients with high cardiotoxicity risk: A qualitative study. PLoS One [Internet]. 2021;16:1–13. Available from: http://dx.doi.org/10.1371/journal.pone.0249067
Jovenaux L, Cautela J, Resseguier N, Pibarot M, Taouqi M, Orabona M, et al. Practices in management of cancer treatment-related cardiovascular toxicity: A cardio-oncology survey. Int J Cardiol. Netherlands; 2017;241:387–92.
Canale ML, Turazza F, Lestuzzi C, Parrini I, Camerini A, Russo G, et al. Portrait of Italian Cardio-Oncology: Results of a Nationwide Associazione Nazionale Medici Cardiologi Ospedalieri (ANMCO) Survey. Front Cardiovasc Med. 2021;8:677544.
Barac A, Murtagh G, Carver JR, Chen MH, Freeman AM, Herrmann J, et al. Cardiovascular Health of Patients With Cancer and Cancer Survivors: A Roadmap to the Next Level. J Am Coll Cardiol. 2015;65:2739–46.
Cautela J, Lalevée N, Ammar C, Ederhy S, Peyrol M, Debourdeau P, et al. Management and research in cancer treatment-related cardiovascular toxicity: Challenges and perspectives. Int J Cardiol. Netherlands; 2016;224:366–75.
Wensing M, Huntink E, Van Lieshout J, Godycki-Cwirko M, Kowalczyk A, Jag̈er C, et al. Tailored implementation of evidence-based practice for patients with chronic diseases. PLoS One. 2014;9:1–8.
Lyon AR, Dent S, Stanway S, Earl H, Brezden-Masley C, Cohen-Solal A, Tocchetti CG, Moslehi JJ, Groarke JD, Bergler-Klein J, Khoo V, Tan LL, Anker MS, von Haehling S, Maack C, Pudil R, Barac A, Thavendiranathan P, Ky B, Neilan TG, Belenkov Y, Rosen SD, Iak LD. Baseline cardiovascular risk assessment in cancer patients scheduled to receive cardiotoxic cancer therapies: a position statement and new risk assessment tools from the Cardio-Oncology Study Group of the Heart Failure Association of the European Society . Eur J Hear Fail. 2020;22:1945–60.
Byron C. Wallace, Kevin Small, Carla E. Brodley, Joseph Lau and Thomas A. Trikalinos. Byron C. Wallace, Kevin Small, Carla E. Brodley JL and TAT. Deploying an interactive machine learning system in an evidence-based practice center: abstrackr. ACM Int Heal Informatics Symp. 2012. p. 819–24.
Jager C, Freund T, Steinhauser J, Aakhus E, Flottorp S, Godycki-Cwirko M, et al. Tailored Implementation for Chronic Diseases (TICD): A protocol for process evaluation in cluster randomized controlled trials in five European countries. Trials. 2014;15:1–6.
Skolarus LE, Neshewat GM, Evans L, Green M, Rehman N, Landis-Lewis Z, et al. Understanding determinants of acute stroke thrombolysis using the tailored implementation for chronic diseases framework: A qualitative study. BMC Health Serv Res. BMC Health Services Research; 2019;19:1–9.
Haverhals LM, Magid KH, Kononowech J. Applying the Tailored Implementation in Chronic Diseases Framework to Inform Implementation of the Preferences Elicited and Respected for Seriously Ill Veterans Through Enhanced Decision-Making Program in the United States Veterans Health Administration. Front Heal Serv. 2022;
Peng J, Rushton M, Johnson C, Brezden-Masley C, Sulpher J, Chiu MG, et al. An international survey of healthcare providers’ knowledge of cardiac complications of cancer treatments. Cardio-oncology (London, England). 2019;5:12.
Koop Y, Teske AJ, Wanders I, Meijer H, Kaanders JHAMH, Manintveld OC, et al. Future steps in cardio-oncology-a national multidisciplinary survey among healthcare professionals in the Netherlands. J Cancer Surviv. United States; 2022;
Mahé I, Scotté F, Rey J-B, Elalamy I, Lamblin A, Mayeur D, et al. Prevention and treatment of cancer-associated thrombosis in France: A national survey among vascular disease and supportive care specialists. J Med Vasc. France; 2017;42:255–62.
Okwuosa TM, Prabhu N, Patel H, Kuzel T, Venugopal P, Williams KA, et al. The Cardiologist and the Cancer Patient: Challenges to Cardio-Oncology (or Onco-Cardiology) and Call to Action. J Am Coll Cardiol. United States; 2018;72:228–32.
Albert K, Pollard D, Klemp J, Kondapalli L, Tuffield D. Assessment of Oncology Provider Knowledge and Cardiovascular Screening Practices: A Call for Heightened Screening. J Adv Pract Oncol. 2021;12:795–807.
Anakwue R. Cytotoxic-induced heart failure among breast cancer patients in Nigeria: A call to prevent today’s cancer patients from being tomorrow’s cardiac patients. Ann Afr Med. 2020;19:1–7.
Agunbiade TA, Ottaviano Y, Goswami D, Ruiz G, Barac A. Targeting Barriers of Systems of Care in a Growing Multi-disciplinary Field. Curr Oncol Rep. United States; 2019;21:36.
Sadler D, Fradley MG, Ismail-Khan R, Raez L, Bhandare D, Elson L, et al. Florida Inter-Specialty Collaborative Project to Improve Cardio-Oncology Awareness and Identify Existing Knowledge Gaps. JACC CardioOncology [Internet]. Elsevier; 2020;2:535–8. Available from: https://doi.org/10.1016/j.jaccao.2020.06.009
Adusumalli S, Alvarez-Cardona J, Khatana SM, Mitchell JD, Blaes AH, Casselli SJ, et al. Clinical Practice and Research in Cardio-Oncology: Finding the “Rosetta Stone” for Establishing Program Excellence in Cardio-oncology. J Cardiovasc Transl Res. United States; 2020;13:495–505.
Sulpher J, Mathur S, Lenihan D, Johnson C, Turek M, Law A, et al. An International Survey of Health Care Providers Involved in the Management of Cancer Patients Exposed to Cardiotoxic Therapy. J Oncol. 2015;2015:391848.
Kozhukhov S, Dovganych N. Cardio-Oncology Educational Program: National Survey as the First Step to Start. Front Cardiovasc Med. 2021;8:697240.
Hedayati E, Papakonstantinou A, Månsson-Broberg A, Bergh J, Hubbert L, Altena R. Approaches to management of cardiovascular morbidity in adult cancer patients - cross-sectional survey among cardio-oncology experts. Cardio-oncology (London, England). 2020;6:16.
Okwuosa TM, Barac A. Burgeoning Cardio-Oncology Programs: Challenges and Opportunities for Early Career Cardiologists/Faculty Directors. J Am Coll Cardiol. United States; 2015;66:1193–7.
Lancellotti P, Suter TM, López-Fernández T, Galderisi M, Lyon AR, Van Der Meer P, et al. Cardio-oncology services: Rationale, organization, and implementatio: A report from the ESC Cardio-Oncology council. Eur Heart J. 2019;40:1756–63.
Balasubramanian BA, Higashi RT, Rodriguez SA, Sadeghi N, Santini NO, Lee SC. Thematic Analysis of Challenges of Care Coordination for Underinsured and Uninsured Cancer Survivors with Chronic Conditions. JAMA Netw Open. 2021;4:1–11.
Tremblay D, Touati N, Usher SE, Cournoyer J. Dimensions of Proximity: An Actionable Framework to Better Understand Integrated Practices in Cancer Networks. Int J Integr Care. 2022;22:1–14.
Tremblay D, Latreille J, Bilodeau K, Samson A, Roy L, L’Italien MF, et al. Improving the transition from oncology to primary care teams: A case for shared leadership. J Oncol Pract. 2016;12:1012–9.
Aunger JA, Millar R, Rafferty AM, Mannion R, Greenhalgh J, Faulks D, et al. How, when, and why do inter-organisational collaborations in healthcare work? A realist evaluation. PLoS One [Internet]. 2022;17:1–29. Available from: http://dx.doi.org/10.1371/journal.pone.0266899
Canale ML, Lestuzzi C, Bisceglia I, Vallerio P, Parrini I. Cardio-oncology organization patterns in Italy: One size does not fit all. J Cardiovasc Med. 2018;19:229–33.
Levi CR, Attia JA, D’Este C, Ryan AE, Henskens F, Kerr E, et al. Cluster-Randomized Trial of Thrombolysis Implementation Support in Metropolitan and Regional Australian Stroke Centers: Lessons for Individual and Systems Behavior Change. J Am Heart Assoc. 2020;9.
Walter FM, Usher-Smith JA, Yadlapalli S, Watson E. Caring for people living with, and beyond, cancer: an online survey of GPs in England. Br J Gen Pract J R Coll Gen Pract. 2015;65:e761-8.
Sadler D, Fradley MG, Ismail-Khan R, Raez L, Bhandare D, Elson L, et al. Florida Inter-Specialty Collaborative Project to Improve Cardio-Oncology Awareness and Identify Existing Knowledge Gaps. JACC. CardioOncology. 2020. p. 535–8.
Agunbiade TA, Ottaviano Y, Goswami D, Ruiz G, Barac A. Targeting Barriers of Systems of Care in a Growing Multi-disciplinary Field. Curr Oncol Rep. Current Oncology Reports; 2019;21.

Download PDF

Version 1

posted

You are reading this latest preprint version

Factors influencing physicians’ decision to conduct cardiovascular risk assessments among cancer patients: A Systematic Review

Status:

Version 1

Abstract

Background

Methods

Results

Conclusion

Figures

Contributions to the literature

Introduction

Methods

Study registration

Eligibility criteria

Search strategy

Study selection process

Risk of bias assessment

Data extraction and synthesis

Tailored Implementation in Chronic Disease framework (TICD)

Results

Characteristics of included studies

Quality of included studies

Identified factors

(i) Individual health professional factors

(ii)Professional interactions

(i) Incentives and resources

(ii) Capacity for organizational change

(iii) Guideline factors

(iv)Patient factors

Discussion

Strengths and weaknesses of this study

Study implications and future directions

Conclusion

Declarations

References

Supplementary Files

Status:

Version 1