Abstract
Coordination of patient care between primary care and oncology care providers is vital to care quality and outcomes across the cancer continuum, yet it is known to be challenging. We conducted a systematic review to evaluate current or new models of care and/or interventions aimed at improving coordination between primary care and oncology care providers for patients with adult breast and/or colorectal cancer. MEDLINE, EMBASE, CINAHL, Cochrane Library Database of Systematic Reviews, and the Centre for Reviews and Dissemination were searched for existing English language studies published between January 2000 and 15 May 2015. Systematic reviews, meta-analyses, randomised controlled trials (RCTs) and non-randomised studies were included if they evaluated a specific model/intervention that was designed to improve care coordination between primary care and oncology care providers, for any stage of the cancer continuum, for patients with adult breast and/or colorectal cancer. Two reviewers extracted data and assessed risk of bias. Twenty-two studies (5 systematic reviews, 6 RCTs and 11 non-randomised studies) were included and varied with respect to the targeted phase of the cancer continuum, type of model or intervention tested, and outcome measures. The majority of studies showed no statistically significant changes in any patient, provider or system outcomes. Owing to conceptual and methodological limitations in this field, the review is unable to provide specific conclusions about the most effective or preferred model/intervention to improve care coordination. Imprecise results that lack generalisability and definitiveness provide limited evidence to base the development of future interventions and policies.
Trial registration number
CRD42015025006.
Keywords: cancer care, primary care, coordination of care, oncology, continuity of care
Introduction
Cancer is the leading cause of death in Canada1 and primary care is the first and most frequent point of contact for patients with cancer within the healthcare system. Although cancer care forms a modest (∼10%) workload component for primary care providers,2 the intricacy and urgency of patients’ care needs are unique and can be complex. These needs include unintended chronic and late-occurring complications of cancer and its treatment, possible oversight of post-treatment surveillance regimens and other multiple concurrent chronic conditions, including those that place patients at higher risk of the adverse effects from cancer treatments.3
The coordination of patient care between primary care and oncology care providers is vital to improve the quality and outcomes of care across the cancer continuum;4 however, this coordination of care has been very challenging.2 5 6 For example, the poor adherence to recommended cancer-specific surveillance regimens and preventative services may be influenced by the ambiguity regarding providers’ roles and diffusion of responsibility, suboptimal collaboration between care providers and increased volume of patients with cancer.7–9 Initiatives to improve care coordination, and evaluations of shared models of care, have been studied; however, a synthesis of this knowledge is required to understand the tactics that can best optimise this goal. To this end, the purpose of this systematic review is to evaluate models of care and interventions designed to improve coordination of care between primary care and oncology care providers for adult patients with breast and/or colorectal cancer. Choice of patient group was restricted to these two diagnoses because of the high prevalence of these diseases,10 and to align with the mandate of the Canadian Team to Improve Community-Based Cancer Care along the Continuum (CanIMPACT) programme of research.
Methods
Overview
This project is part of a larger research programme called CanIMPACT, which aims to improve coordination of care along the cancer care continuum between primary care provider and cancer specialist communities.11
Protocol and registration
The systematic review has been conducted and reported using the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement guidelines.12 Details of the protocol for this systematic review were registered on PROSPERO.13
Search strategy
MEDLINE, EMBASE, CINAHL, Cochrane Library Database of Systematic Reviews and the Centre for Reviews and Dissemination were searched for existing English language studies published between January 2000 and November 2014. The Cochrane Central Register of Controlled Trials was searched for ongoing studies. The full original search strategy can be found in the online supplementary material. Reference lists of relevant systematic reviews were manually searched to identify eligible studies. The search was updated in May 2015 to include articles published between November 2014 and 15 May 2015.
esmoopen-2016-000077supp.pdf (131.7KB, pdf)
Eligibility criteria
Eligibility criteria were defined a priori and included the following elements:
Interventions
Included studies evaluated a specific model of care or intervention (1) designed to improve care coordination between primary care and oncology care providers, AND (2) for any stage of the cancer continuum, AND (3) for adult breast and/or colorectal cancer patients. A model of care/intervention was conceptualised as a programme or project that is intended to improve some aspect of cancer care coordination, delivery, organisation or patient care. Examples of ‘interventions’ are the implementation of case management and primary care-led follow-up.
Study designs
Systematic reviews, meta-analyses, randomised controlled trials (RCTs) and non-randomised studies, evaluating the effectiveness of a model of care or intervention on patient, provider or system outcomes, were included. Retrospective and descriptive studies, unpublished data, abstracts and conference proceedings were excluded.
Participants
The model of care or intervention being evaluated had to include both primary care providers (eg, family physicians, nurse practitioners, family practice nurses, community pharmacists and physiotherapists) and oncology care providers (eg, medical/radiation oncologists, general/family practitioners in oncology, oncology specialists, generalist surgeons and advanced practice or specialist nurses). The participants involved in the evaluation could include members of the healthcare provider group and/or patients who were treated under the model of care being evaluated.
Comparators/controls
For RCTs and non-randomised studies, the comparator group could receive another model of care intervention, standard/usual care or no intervention.
Types of outcome measures
Study eligibility was not dependent on reported outcomes; patient, provider and system outcome measures at all time points were included. Patient outcomes, such as survival, quality of life and chronic adverse effects, were prioritised.
Data extraction
Literature search results were uploaded to, and deduplicated in, EndNote X7 reference management software. Titles and abstracts, followed by full texts of records meeting the initial screening criteria, were retrieved and examined independently by two reviewers (research assistants). Disagreements related to screening were resolved through discussion to reach consensus.
One research assistant extracted data from the included studies using a pilot-tested form, and a second research assistant verified the extracted data through a formal audit process to reduce errors and bias. Disagreements were resolved by consensus. The following data were extracted from each article: (1) study design; (2) setting; (3) risk of bias assessment (more information below); (4) characteristics of participating providers; (5) characteristics of participating patients; (6) model of care or intervention characteristics (including purpose, description and implementation); (7) outcome measures; and (8) results.
Risk of bias assessment
The two reviewers independently assessed the risk of bias for each included study. Disagreements were resolved by consensus. The Assessing Methodological Quality of Systematic Reviews (AMSTAR) Checklist14 was used to assess systematic reviews and Cochrane Collaboration tools15 16 were used to assess randomised and non-randomised studies.
Data synthesis
The results were summarised in tables according to study design and a systematic narrative synthesis was conducted for each type of study. A meta-analysis was not possible due to heterogeneity in the outcome measures used in the studies.
Results
Results of the search
The original search generated 5064 references. An additional 703 were identified through the search update, resulting in a total of 5767 articles; 130 full-text articles were assessed for eligibility. Twenty-two articles met the eligibility criteria and were included in this review. A PRISMA flow chart outlining the study selection process and reasons for exclusions is found in figure 1.
Details of included studies
Five systematic reviews,17–21 six RCTs22–27 and 11 non-randomised studies28–38 comprised the review. The six RCTs and 11 non-randomised studies were not already included in the five systematic reviews. The findings from each type of study are discussed below.
Systematic reviews
The number of studies included in the five systematic reviews17–21 ranged from 19 to 51. The types of study designs, the number of studies included, the model(s) of care evaluated and the outcomes measured varied across the systematic reviews, making comparisons difficult. None of the reviews specifically focused on breast cancer or colorectal cancer, but did include these patient groups. Three of the five systematic reviews were considered to be of moderate quality (ie, AMSTAR score of 5-8/11) and two were considered to be of low quality (ie, AMSTAR score of 0-4/11). table 1 provides AMSTAR results and table 2 provides study details and outcomes.
Table 1.
Author | 1. Was an “a priori” design provided? | 2. Was there duplicate study selection and data extraction? | 3. Was a comprehensive literature search performed? | 4. Was the status of publication (i.e., grey literature) used as inclusion criteria? | 5. Was a list of studies (included and excluded) provided? | 6. Were the characteristics of the included studies provided? | 7. Was the scientific quality of the included studies assessed and documented? | 8. Was the scientific quality of the included studies used appropriately in formulating conclusions? | 9. Were the methods used to combine the findings of studies appropriate? | 10. Was the likelihood of publication bias assessed? | 11. Was the conflict of interest included? |
---|---|---|---|---|---|---|---|---|---|---|---|
Aubin et al, 201217 | No | No | Yes | Can't Answer | No | Yes | Yes | No | N/A | N/A | No |
Howell et al, 201218 | No | Yes | Yes | No | No | Yes | Yes | Yes | Can't Answer | Yes | No |
Lamb et al, 201119 | No | No | Yes | Can't Answer | No | No | No | No | Yes | No | No |
Lewis et al, 200920 | Yes | Yes | Yes | Yes | No | Yes | Yes | Yes | No | No | No |
Ouwens et al, 200921 | No | Yes | Yes | Yes | No | Yes | No | No | Yes | No | No |
Note: The “can't answer” option is chosen when the item is relevant but not described by the authors. The “not applicable” option is selected when the item is not relevant (e.g. when a meta-analysis was not attempted by the authors).
Table 2.
Author, search years, number of studies | Purpose of systematic review | Models of care examined and participants | Results | Quality of included studies | Authors’ conclusions and recommendations |
---|---|---|---|---|---|
Aubin et al, 2012, Canada17 Search from database inception to Feb 2009 51 studies (49 RCTs) |
To classify, describe and evaluate the effectiveness of interventions aiming to improve patient, healthcare provider and process outcomes. | Primarily case management, shared care and interdisciplinary teams n=12967 (approximate); Any type of cancer was considered; Only adult patients were considered. |
Based on the median effect size estimates, there were no significant differences found between patients assigned to interventions and those assigned to usual care, in regards to patient health-related outcomes. | All studies were of ‘very low quality’ due to inconsistent results and high heterogeneity among studies.* | Evidence is lacking from the majority of studied outcomes; therefore, no conclusions regarding most effective interventions could be made. Future research should evaluate interventions for which improvement in continuity is the primary objective. |
Howell et al, 2012, Canada18 Search from 1999 to Dec 2000 19 studies (9 RCTs; 10 practice guidelines) |
To determine the optimum organisation and care delivery structure for cancer survivorship services. | Nurse-led and primary care physician-led n=3112; Any type of cancer was considered; Only adult patients were considered. |
Nurse-led and primary care physician models of follow-up care were equivalent for detecting recurrence. Consensus also suggested that cancer survivors may benefit from coordinated transition planning that includes the provision of survivorship care plans as a standardised part of care. | The evidence was rated as low quality, due to non-blinding of participants or outcome assessors, poor reporting of randomisation procedures, and lack of power to detect statistically significant differences between treatment groups.†‡ | Evidence is limited; however, the realignment of models of care should be identified as a health system priority, in order to meet the supportive care and surveillance needs of the survivor population. Further research is required to evaluate the efficacy of models of care in a broader population of cancer survivors with differing needs and risks. |
Lamb et al, 2011, UK19 Search from 1999 to May 2009 37 studies (1 RCT) |
To examine the evidence on clinical, social and technological factors that affect the quality of MDT clinical decision-making. | MDTs n=not available; Any type of cancer was considered; Patients of any age were considered. |
Failure to reach a decision at MDT discussions was found in 27–52% of cases. The majority of team decisions were made by physicians (without the inclusion of nurses) and patient preferences were not discussed. The following factors negatively affected decision-making: time pressure; excessive caseload; low attendance; poor team work; and lack of leadership. Telemedicine is effectively being used in developed countries. | Overall study quality was low to medium. The median quality score for quantitative papers was 9/18 (range 3–15) and for qualitative papers was 13/24 (range 9–14).§ | Team/social factors affect management decisions by cancer MDTs. The following may have a positive impact on team decision-making: allowing adequate time for team members to prepare for MDT meetings; making team and leadership skills training available to team-members; and considering systematic input from nursing personnel. |
Lewis et al, 2009, UK20 Search from database inception to February 2007 21 publications and 10 studies (6 RCTs) |
To compare the effectiveness and cost-effectiveness of nurse-led follow-up of cancer patients, with conventional physician-led follow-up. | Nurse-led and primary care physician-led n=927 (for the review's focal four RCTs); Any type of cancer was considered; Patients of any age were considered. |
There were no statistically significant differences in survival, recurrence or psychological morbidity. Patients with lung cancer were more satisfied with nurse-led telephone follow-up. Patients with breast cancer thought patient-initiated follow-up was convenient. No significant observations regarding cost-effectiveness were made. | Study quality ranged from poor to well-conducted; total quality score for internal validity ranged from 7 (47%) to 13 (87%). The statistical tests used in three studies were poorly-reported.¶ | Patients appeared satisfied with nurse-led follow-up. Patient-initiated or telephone follow-up could be practical alternatives to routine hospital follow-up care; however, more evaluations are required and the duration of follow-up needs to be sufficient to allow for comparison of recurrence rates. |
Ouwens et al, 2009, Netherlands21 Search from Jan 1996 to Oct 2006 33 studies (31 RCTs/ quasi-RCTs) |
To review integrated care interventions and their effects on the quality of cancer care. | Interventions comprising at least one of the three integrated care principles: patient-centeredness; organisation or care; and multidisciplinary care n=not available; Any type of cancer was considered; Only adult patients were considered. |
Effective interventions to improve patient-centeredness were: providing patients with an audiotape of the consultation, and with information, and using decision aids. Effective interventions to improve the organisation of care were follow-up and case management, (particularly by nurses and one-stop clinics). | Only studies that met at least three of the five quality criteria described by the Cochrane Collaboration were included in the review.** | In order to improve integrated care for patients with cancer, a multicomponent intervention programme which focuses on patients, professionals and the organisation of care, is required. It is suggested that interventions found in this review should help to structure a future programme which would be evaluated using rigorous methods and explicit outcome measures linked to the intervention. |
*The GRADE approach was used to assess the quality of the evidence.
†The AGREE II instrument was used to assess the quality of the practice guidelines.
‡The SIGN guideline development handbook was used to assess the quality of the randomised controlled trials.
§Included studies were assessed against a quality score. Quantitative papers were scored out of a total of 18, and qualitative papers out of 24 (more detail included in online supplementary material of the original review).
¶A modified Downs and Black checklist was used to assess the quality of the evidence.
**Five methodological criteria described by the Cochrane Collaboration (ie, completeness of follow-up, reliability of outcomes, protection against contamination, baseline measurement and concealment of allocation) were used to assess the quality of the evidence.
MDT, multidisciplinary care team; RCTs, randomised controlled trials.
Overall, the reviews did not support any one model or intervention over another to improve continuity and/or coordination of care. This was due to heterogeneity of outcomes, lack of clinical-centred or person-centred outcomes, and the overall low quality of the studies. The most definitive conclusion that emerged from the existing reviews was from Howell et al,18 who found that primary care and nurse-led models of care are equivalent in post-surgical colorectal cancer populations and following adjuvant treatment for breast cancer. These results are similar to earlier conclusions by Lewis et al,20 who demonstrated no statistically significant difference in survivorship, recurrence of cancer or psychological morbidity between physician-led and nurse-led follow-up care. All systematic reviews concluded that better quality investigations are warranted.
Randomised controlled studies
Six RCTs were included in the review, one each from Canada,23 Australia,24 the UK25 and the USA,26 and two from Denmark.22 27 Studies were designed for all cancers,22 haematological, breast, ovarian and colorectal cancers,24 breast, colorectal and lung cancers,25 26 breast cancer only23 and colorectal cancer only.27 Two RCTs examined interventions that targeted transition from diagnosis through to treatment,26 27 one study targeted only treatment,24 two studies targeted transition from treatment through to survivorship22 25 and one study targeted survivorship specifically.23 The types of model designs or interventions included case management,22 24 25 27 nurse navigation26 and the dissemination of survivorship care plans.23 Outcomes assessed in the studies also varied. All six RCTs examined patient outcomes, including satisfaction with care,22 23 27 self-advocacy,25 dropout,25 quality of life,23 26 patient experience,23 26 cancer-related distress,23 anxiety/depression and empowerment24 and adverse effects of treatment.24 Four studies examined provider outcomes, such as satisfaction with care provided,22 24 27 and system outcomes, such as number of patient visits with a general practitioner and/or oncologist23 27 and costs after diagnosis.26 The key issues regarding study bias were lack of blinding of participants and personnel, and selective reporting of outcomes. table 3 provides a Cochrane risk of bias table and table 4 describes study details and outcomes. Overall, there were no significant changes reported in any of the measured outcomes.
Table 3.
Random sequence generation (selection bias) | Allocation concealment (selection bias) | Blinding of participants and personnel (performance bias) | Blinding of outcome assessment (detection bias) | Incomplete outcome data (attrition bias) | Selective reporting (reporting bias) | Other bias | |
---|---|---|---|---|---|---|---|
Bergholdt et al, 201322 | + | - | - | + | ? | - | ? |
Grunfeld et al, 201123 | + | + | + | + | + | + | + |
Johnson et al, 201524 | + | ? | - | ? | + | + | + |
King et al, 200925 | + | + | + | ? | - | ? | + |
Wagner et al, 201426 | + | + | - | + | + | - | + |
Wulff et al, 201327 | + | + | - | + | + | - | + |
Table 4.
Study author | Participants (n), type of cancer, stage of cancer care continuum | Description of study | Results |
---|---|---|---|
Bergholdt et al, 2013, Denmark22 | n=955 patients (baseline); 612 patients (6-month follow-up); 506 patients (14-month follow-up); 776 GPs (14-month follow-up) Any type of cancer was considered; Treatment into survivorship |
Intervention: (CM) Assessment of patient needs; results shared with patients’ GPs, who were then encouraged to contact patients to facilitate rehabilitation Control: Standard care Data collection methods: Self-administered questionnaires Outcome(s) measured: Patients’ satisfaction with their GPs (in general) and with GP support, and GPs’ satisfaction with their contribution to their patients’ well-being |
No statistically significant effects of the intervention were observed. Subgroup analysis of breast cancer patients showed a statistically significant improvement of satisfaction with their GP, in regards to ‘information and support’ and ‘the organisation of care’. |
Grunfeld et al, 2011, Canada23 | n=407 patients (baseline); 332 patients (3-month follow-up); 318 patients (6-month follow-up); 299 (12-month follow-up) Breast; Survivorship |
Intervention: (SCPs) Supplement to standard care; all routine follow-up care transferred to patients’ PCPs, and SCPs sent to patients and their PCPs Control: Enhanced standard care (ie, all routine follow-up care transferred to patients' PCPs) Data collection methods: Self-administered questionnaires and collection of health services records Outcome(s) measured: Patients’ level of cancer-related distress, quality of life, patient satisfaction, continuity of care, and health services outcomes (ie, patient transfer to PCP, oncologist visits, and awareness of which care provider is primarily responsible for follow-up care). |
No statistically significant effects of the intervention were observed on any outcome measure, at any time point. Nine intervention and five control patients were not transferred to the PCP for follow-up due to recurrence/other reasons. After transfer to PCP, 16 control patients and 15 intervention patients visited an oncologist. Overall, over 89% of patients correctly identified their PCP as being the primary provider of follow-up care; at 12 months, significantly more intervention group patients were able to do so. |
Johnson et al, 2015, Australia24 | n=88 patients; 55 PCPs; 5 cancer specialists Haematological, breast, ovarian and colorectal cancers; Treatment |
Intervention: (CM) Shared care model, incorporating the use of patient-held records and dissemination of PCP educational resources packages Control: Standard care Data collection methods: Self-administered questionnaires and symptom diary completion Outcome(s) measured: Patients’ level of anxiety, depression, empowerment, adverse effects of treatment and patients’, PCPs' and cancer specialists’ perceptions of the shared care model |
No statistically significant differences in patients’ levels of anxiety, depression, empowerment or adverse effects of treatment were observed. No differences were detected in perceptions of care between PCPs and patients in the intervention and control groups. The majority (88%) of PCPs found the patient health records to be useful and the majority of their comments were positive. One of five cancer specialists thought the patient health record was useful and all five had concerns about the shared care model. |
King et al, 2009, UK25 | n=93 patients (baseline); 61 patients (6-month follow-up) Breast, colorectal and lung; Treatment into survivorship |
Intervention: (CM) (a) Patients completed continuity assessment; (b) Patients completed aforementioned assessment; results shared with clinical nurse specialists, who were encouraged to address patients’ needs Control: Standard care Data collection methods: Self-administered questionnaires Outcome(s) measured: Patients’ experienced continuity of care |
No statistically significant differences in patients’ experienced continuity of care; some trends were observed. For example, participants in the intervention trial arms expressed less unmet needs for care than participants allocated to the control group. |
Wagner et al, 2014, USA26 | n=251 patients (baseline); 242 patients (4-month follow-up); 229 patients (12-month follow-up) Breast, colorectal and lung; Diagnosis into treatment |
Intervention: (Nurse navigation) Four months of nurse navigation support Control: Enhanced standard care (ie, receipt of more tailored patient education) Data collection methods: Telephone-administered questionnaires and automated administrative data Outcome(s) measured: Quality of life, patient experience with care, healthcare costs |
There were no statistically significant differences between intervention and control groups in quality of life scores. Nurse navigator patients reported a significantly higher extent to which care actively involves patients, and reported significantly fewer problems with care (especially regarding psychosocial care, care coordination, and information). Furthermore, there were no statistically significant differences (by cancer type and intervention group) in the median cumulative costs of care, calculated from 3 months before the date of diagnosis through to 1 year postdiagnosis. |
Wulff et al, 2013, Denmark27 | n=280 GPs (baseline); 228 GPs (30 weeks) Colorectal; Primarily diagnosis into treatment |
Intervention: (Hospital-based CM) Supplement to standard care, involving assessment of patient needs, patient outreach and informing GPs of patients’ overall health status Control: Standard care Data collection methods: Self-administered questionnaires and Danish National Health Service Register Outcome(s) measured: GPs’ evaluation of the intervention, and amount of contact between patients and GPs during daytime hours and out-of-hours services |
The use of CM was associated with a significant tendency towards more positive evaluations (particularly relating to psychological effects of the cancer, social effects of the cancer and information given to the patient by the specialists). Additionally, significantly fewer CM GPs than non-CM GPs reported having contacted the hospital regarding their patients’ care. CM did not affect the number of patient contacts with their GPs during daytime hours, but CM patients showed a tendency towards more contacts to out-of-hours GP services than non-CM patients. |
The recorded number of participants in the second column of the table represents the number that completed the study at each time point.
CM, case management; GP, general practitioner; PCP, primary care provider; RCT, randomised controlled trial; SCP, survivorship care plan.
Non-randomised studies
Eleven non-randomised studies examining models of care/interventions to improve care coordination between primary care and oncology care providers were eligible for inclusion in the review.28–38 The countries of origin of these studies included three each from the USA30 31 37 and the UK,28 32 35 two each from Canada27 36 and Australia,29 38 and one from New Zealand.36 The types of cancer targeted in the studies included breast only (n=4),29 30 34 38 colorectal only (n=4),28 33 35 36 either breast or colorectal (n=2)31 37 and breast, colorectal and other (n=1).32 The majority of studies piloted interventions for patients in the transition from treatment to survivorship (n=8),31–38 with only one intervention focused on diagnosis28 and two focused on the transition from diagnosis through to treatment.29 30 Intervention strategies included the use of nurse navigators (n=3),29 35 36 treatment or survivorship care plans (n=3),30 31 37 referral letters/forms (n=1),28 transfer into survivorship assessments (n=1)38 and shared care/creation of multidisciplinary teams (n=1).32 Two studies reported interventions that comprised a number of strategies from those previously listed.33 34 The outcomes assessed in the studies ranged from patient outcomes (eg, perceptions of quality of care,30 satisfaction with care,30–33 35 37 quality of life,35 psychological morbidity34), to provider outcomes (eg, satisfaction with care32 35) to system outcomes (eg, wait times,29 number of tests requested or appointments,36 patient referrals28 38 and cost savings35). Eight studies were judged to be of serious risk of bias and three were judged to be of moderate risk of bias. table 5 provides A Cochrane Risk of Bias Assessment Tool: for Non-Randomized Studies of Interventions (ACROBAT-NRSI) results and table 6 describes the study details and outcomes. All of the non-randomised studies presented inconclusive results.
Table 5.
Author | Overall risk of bias | Confounding | Selection of participants | Measurement of interventions | Departures from intended interventions | Missing data | Measurement of outcomes | Selection of the reported result |
---|---|---|---|---|---|---|---|---|
Aljarabah et al, 200928 | Serious | Serious | Serious | Serious | Low | Low | Low | Low |
Baliski et al, 201429 | Moderate | Moderate | Low | Low | Low | Low | Low | Low |
Blinder et al, 201330 | Serious | Serious | Serious | Moderate | Low | Serious | Moderate | Moderate |
Dulko et al, 201331 | Serious | Serious | Moderate | Moderate | Low | NI | Moderate | Low |
Hall et al, 201132 | Serious | Serious | Serious | Low | Low | Moderate | Low | Low |
Jefford et al, 201133 | Serious | Serious | Moderate | Low | Low | Low | Moderate | Moderate |
Jiwa et al, 201334 | Serious | Serious | Serious | Moderate | Low | Low | Low | Low |
Knowles et al, 200735 | Serious | Serious | Moderate | Low | Low | Low | Low | Low |
McFarlane et al, 201136 | Moderate | Low | Moderate | Low | Low | Low | Moderate | Low |
Sprague et al, 201337 | Serious | Serious | Serious | Moderate | Low | Moderate | Serious | Low |
Vanhuyse et al, 200738 | Moderate | Moderate | Moderate | Low | Moderate | Low | Low | Low |
Table 6.
Study author (type of study) | Participants (n), type of cancer, stage of cancer care continuum | Description of study | Results |
---|---|---|---|
Aljarabah et al, 2009, UK28 (Prospective) |
n=3 clinical consultants (receiving GPs’ referral letters for 217 patients) Colorectal; Diagnosis |
Intervention: (Referral letters) Clinical consultants’ assessment of the reliability of GPs’ referral letters for allowing patients to proceed ‘straight-to-test’ Control: None Data collection methods: Prospective collection of clinical consultants' recommendations for diagnostic test referrals based on both GP letter and postpatient consultation Outcome(s) measured: Consultants’ diagnostic test referrals |
The diagnostic tests that were recommended by clinical consultants having only read GPs’ referral letters differed from those that they would have recommended having performed an in-person clinical consultation for 31% of patients. Therefore, suspected patients with colorectal cancer should be seen in a clinic by an expert before proceeding to testing. |
Baliski et al, 2014, Canada29 (Cohort) |
n=97 current patients (and 100 patients from previous years) Breast; Diagnosis into treatment |
Intervention: (Nurse navigation) Implementation of a nurse navigation programme Control: None Data collection methods: Prospective records database, and wait time records from BC Cancer Agency Sindi Ahluwalia Hawkins Centre for the Southern Interior and Kelowna General Hospital (from previous years) Primary outcome(s): Surgical wait times |
Wait times for surgery decreased with the introduction of the programme (median of 59 vs 48 days); however, this decrease was not statistically significant. The need for MRI was found to significantly influence wait times by delaying surgery. |
Blinder et al, 2013, USA30 (Prospective) |
n=174 patients (completed at least one survey) Breast; Diagnosis into treatment |
Intervention: (TPSs) Seven oncology practices from the ASCO membership were instructed to offer all patients TPSs and to discuss them with the patients. Patients receiving chemotherapy received the plan and summary documents separately (at the beginning and end of treatment, respectively). All other patients received a single integrated TPS. Control: None Data collection methods: Telephone surveys Outcome(s) measured: Quality of care, coordination of care and patient satisfaction |
Of all patients who recalled receiving TPSs, 94% believed that the documents improved patient–physician communication (quality of care) and 82% believed that they improved communication between physicians (coordination of care). Participants expressed high satisfaction with TPSs. Of patients who still had their documents, 97% said they were useful (patient satisfaction). |
Dulko et al, 2013, USA31 (Descriptive) |
n=17 APPs, 39 PCPs and 58 patients participated Breast and colorectal; Survivorship |
Intervention: (SCPs) Evaluating the process of SCP completion and assessing the barriers to SCP creation and implementation Control: None Data collection methods: Self-administered questionnaires and telephone interviews Outcome(s) measured: Usefulness and barriers to SCP development, challenges to development and implementation of SCPs, and patient perceptions of the SCP visit |
Fifty-eight per cent of PCPs identified inadequate knowledge of cancer survivor issues as a barrier to SCP implementation and 64% identified limited access to patients as a barrier to providing follow-up care. The primary barrier to SCP completion, identified by APPs, was the time required to prepare a SCP (the average time needed was 53.9 min). More than half of the patients surveyed did not know what to expect from their SPC visit; 64% of patients seen within 6 months of diagnosis (and 55% of patients seen at 7–12 months after diagnosis) agreed that the SCP was given to them at an appropriate time. |
Hall et al, 2011, UK32 (Cross-sectional) |
n=23 patients and 5 GPs participated Breast, colorectal, gastrointenstinal, prostate and melanoma; Survivorship |
Intervention: (Shared follow-up care) Assessment of opinions regarding shared-care and conducting a shared-care modelling exercise Control: none Data collection methods: Telephone or in-person interviews and shared follow-up modelling exercise Outcome(s) measured: Opinions regarding shared follow-up care |
Most patients and GPs had a positive outlook on shared follow-up care. Patients perceived the benefits of shared follow-up care to be improved access, convenience, travel time and continuity of care; they agreed that GPs who provide shared care should be specially trained and that shared-care must be supported by secondary care. GPs emphasised the importance of maintaining their clinical skills and receiving strong administrative support. |
Jefford et al, 2011, Australia33 (Prospective) |
n=10 patients (baseline); 8 patients* Colorectal; Survivorship |
Intervention: (Nurse-led care) Implementation of nurse-led post-treatment intervention Control: None Data collection methods: Self-administered questionnaires, and in-person and telephone interviews Outcome(s) measured: Patient satisfaction |
Overall, patients considered the nurse-led intervention to be appropriate, relevant, and useful. All participants agreed that nurse-led treatment sessions addressed their concerns and clarified information, and that the phone calls were informative, reassuring and allowed for continued contact with the hospital (which was deemed important). |
Jiwa et al, 2013, Australia34 (Prospective) |
n=21 patients (baseline); 19 patients* Breast; Survivorship |
Intervention: (Cancer care coordination) Evaluation of the benefits of therapeutic action delivered to patients by GPs (therapeutic action was based on the recommendations of a primary care-led multidisciplinary team, who had received the patient's needs assessment) Control: None Data collection methods: Self-administered questionnaires and telephone conversations Outcome(s) measured: Physical and psychological patient outcomes |
Questionnaire responses showed no statistically significant difference in physical or psychological patient outcomes. However, the majority of participants (11/17 women who had visited their GPs) reported that their condition had improved as a result of the primary care-led intervention. |
Knowles et al, 2007, UK35 (Prospective) |
n=80 patients (baseline); 60 patients* Colorectal; Survivorship |
Intervention: (Nurse-led follow-up care) Assessment of the feasibility of a nurse-led follow-up programme over the course of 1 year Control: None Data collection methods: Access database, patients’ case notes, self-administered questionnaires Outcome(s) measured: Adherence to follow-up protocol; detection of recurrence; quality of life; patient and clinician satisfaction; cost savings analysis |
Over the course of 1 year, nurse adherence to protocol was strict and resulted in recurrence being detected in 10 patients. Furthermore, patients’ quality of life significantly improved throughout the study period. The programme was acceptable to both patients and care providers, and the presence of nurses provided an added benefit of streamlining services and reducing the burden on outpatient resources. The assumed cost savings over a 3-year follow-up period (supposing a steady rate of 220 new patients annually) was estimated to be £28 030. |
McFarlane et al, 2012, New Zealand36 (Prospective) |
n=950 patients, tracked for 7 years Colorectal; Survivorship |
Intervention: (Nurse-led follow-up care) Documentation of the results of a nurse-led follow-up clinic over the course of 7 years Control: None Data collection methods: Patient details recorded prospectively in a database Outcome(s) measured: Patient health outcomes and process outcomes |
Over the course of 7 years, 368 patients were discharged, 474 remained actively involved in the programme and 108 died. Of those who were discharged, 73% returned to the care of their GP, free of disease. Twenty patients were identified as having disease recurrence and 93 as having distant metastatic disease; of these, 65 were referred to palliative care and 28 had surgery. Overall, the clinic's detection rates of recurrent or metastatic disease were comparable to surgical consultant follow-up. |
Sprague et al, 2013, USA37 (Cross-sectional) |
n=78 patients (baseline); 58 patients* Breast and colorectal; Survivorship |
Intervention: (SCPs) Evaluation of patient satisfaction with SCPs Control: None Data collection methods: Telephone interviews Outcome(s) measured: Patient satisfaction |
Ninety-one per cent of patients agreed that the SCP they received was useful, easy to understand, and that the length was appropriate. Nineteen per cent stated that they would need help in using the plan. The majority agreed that the SCP was very or critically important to understanding survivorship issues; however, only about half of all patients felt that the SCP helped them to understand the individual roles of, and the collaborative relationship between, PCPs and oncologists. |
Vanhuyse et al, 2007, Canada38 (Cross-sectional) |
n=193 patients, tracked over the course of 4 months Breast; Survivorship |
Intervention: (Transfer of follow-up care) Prospective programme of planned patient transfer to a PCP for follow-up Control: None Data collection methods: Patient details recorded prospectively in a database Outcome(s) measured: Number of patients for whom transfer back to a PCP for follow-up care was feasible |
Transfer was deemed suitable for 43% of all patients assessed for transfer. This strategy of safely assessing follow-up patients for transfer to primary care may help in allowing oncologists to focus on primarily caring for newly diagnosed and advanced-stage patients. |
*Number of patients who completed the study.
APP, advanced practice professional; ASCO, American Society of Clinical Oncology; BC, British Columbia; GP, general practitioner; PCP, primary care provider; SCP, survivorship care plan; TPS, treatment plan and summary.
Discussion
This review evaluated models or intervention aimed at improving coordination of care between primary care and oncology care providers, for patients with breast and/or colorectal cancer. The 22 included studies varied with respect to type of model (most incorporating nurse navigation25–27 29 33 35 36) or intervention (most incorporating survivorship care plans23 31 33 34 37) evaluated. Many different outcome measures were used and assessed the impact at provider, patient and system levels. The conceptual and methodological limitations with the studies make it challenging to provide specific conclusions about the model or intervention tactic that would lead to changes in patient, provider and system outcomes.
Two conceptual issues with the research until now became evident when conducting the review. First, the majority of the reviewed studies provide little rationale for the selection of the model or intervention being tested, with tactics being chosen by investigator preference rather than by a systematic process of building from previous research.39 40 Second, the evaluation of the model or intervention is often a secondary consideration, not the primary objective, of the investigation. As a result, the implementation of the model or intervention was infrequently monitored, making it difficult to decipher whether the results were attributable to the model or intervention. For example, in two studies, the results of patient needs interviews/assessments were provided to primary care providers who were encouraged to participate in patient care, but their involvement was neither enforced nor documented.22 25 Consequently, there is a haphazard progression in inquiry such that the field is not advancing in logical sequence as might have been seen more often in clinical investigations (eg, evaluation of new chemotherapy agents). Researchers and practitioners in this field are encouraged to pursue inquiries based on theoretical41 42 and evidence-based rationale to build on previously published work.43 Planning for monitoring of implementation would further our knowledge of the effectiveness and feasibility of selected models or interventions in practice.
This synthesis of research also pointed to a number of methodological concerns in this field. With only six RCTs meeting eligibility criteria,22–27 it is evident that non-experimental pilot and feasibility studies are dominating the field. However, the included studies are of low to moderate quality; common methodological flaws include small sample sizes and inadequate statistical power,24 25 a lack of baseline data collected to examine changes over time,22 25 26 and a lack of clarity about the statistical significance of the results and their importance from a clinical and health system perspective.25 Moreover, very few studies investigated any one model or intervention type, making it challenging for a body of knowledge to be accumulated. Compounding this issue is when studies do investigate the same model design or intervention type, yet study authors use different nomenclature. For example, the concept of ‘nurse navigation’ in Wagner et al26 is referred to as ‘case management’ in two other RCTs,25 27 although the model appears to be essentially identical. Even when several studies investigate similar intervention types, an array of provider, patient and system outcomes are assessed, and the quality of the measurement of these varied outcomes is often questionable. By way of illustration, patients’ needs/satisfaction with care is best defined by how it is experienced by patients;23–25 however, studies often examine practitioners’ evaluation of care and extrapolate the outcome as patient satisfaction.27 Similar methodological flaws and the heterogeneity in outcome measures were noted in the included systematic reviews.17–21
The primary potential limitation of this systematic review was that all relevant literature may not have been captured and/or reported. For example, a number of terms (eg, ‘care coordination’, ‘continuity of care’ and ‘care integration’) exist for similar concepts in this field, and are often interchangeable. To mitigate this limitation, we used a rigorous, systematic methodology12 and our search strategy included a number of search terms encompassing the variety in nomenclature (see online supplementary material).
Conclusion
Overall, researchers, clinicians and administrators are left with imprecise results that lack both generalisability as well as definitiveness, providing limited data to build better interventions. Therefore, the development of provincial or national policies based on a strong evidence base remains unlikely. The most robust conclusion that can be made from this systematic review is that there has been little progress in this field. The ageing population, combined with an overall greater life expectancy for those living with cancer, will lead to an increased burden on the healthcare system. The Canadian healthcare system can neither afford nor has the human resource capacity to continue with business as usual. Ongoing demands will be placed on primary care and oncology care providers, without adequate evidence to direct the most suitable model designs (for the most appropriate patients and contexts), and without enough support to optimise the collaboration between these healthcare providers. High quality and adequately powered prospective experimental designs in this field are required to optimise patient experience, provider satisfaction and system performance.
Acknowledgments
The authors would like to thank: Julie Makarski and Tricia Waldron for their support with study planning and design; Kate Kerkvliet, Keneisha Gardiner and Heather Kilgour for assistance with acquisition of data, and data entry and analysis; and Sharon Matthias, Margaret Tompson and Richard Wassersug for providing the patient perspective to the project.
Footnotes
Contributors: JRT, MCB and MV conceived the design of the study, led the implementation, as well as the drafting and modification of this paper. All authors contributed to the analysis and interpretation of the data, reviewed drafts and provided important intellectual contributions during the revisions, and approved of this final draft. All authors can attest to the accuracy and integrity of the work.
Funding: The CanIMPACT project is funded by the Canadian Institutes of Health Research (reference number: 128272).
Competing interests: None declared.
Provenance and peer review: Not commissioned; externally peer reviewed.
References
- 1.2014. Leading causes of death, by sex: CANSIM Table 102-0561. http://www.statcan.gc.ca/tables-tableaux/sum-som/l01/cst01/hlth36a-eng.htm.
- 2.Manuel DG, Maaten S, Thiruchelvam D et al. . Primary care in the healthcare system. In: Jaakkimainen L, Upshir REG, Klein-Geltink JE et al.. eds Primary care in Ontario: ICES Atlas. Toronto: Institute for Evaluative Sciences, 2006:2–14. [Google Scholar]
- 3.Hewitt M, Greenfield S, Stovall E. From cancer patient to cancer survivor: lost in translation. Washington: The National Academies Press, 2006. [Google Scholar]
- 4.Haggerty JL. Ordering the chaos for patients with multimorbidity. BMJ 2012;345:e5915 10.1136/bmj.e5915 [DOI] [PubMed] [Google Scholar]
- 5.Grunfeld E, Earle CC. The interface between primary and oncology specialty care: treatment through survivorship. J Natl Cancer Inst Monographs 2010;2010:25–30. 10.1093/jncimonographs/lgq002 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Taplin SH, Rodgers AB. Toward improving the quality of cancer care: addressing the interfaces of primary and oncology-related subspecialty care. J Natl Cancer Inst Monographs 2010;2010:3–10. 10.1093/jncimonographs/lgq006 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Grunfeld E, Moineddin R, Gunraj N et al. . Cancer screening practices of cancer survivors: population-based, longitudinal study. Can Fam Physician 2012;58:980–6. [PMC free article] [PubMed] [Google Scholar]
- 8.Hodgson DC, Grunfeld E, Gunraj N et al. . A population-based study of follow-up care for Hodgkin lymphoma survivors: opportunities to improve surveillance for relapse and late effects. Cancer 2010;116:3417–25. 10.1002/cncr.25053 [DOI] [PubMed] [Google Scholar]
- 9.Sisler JJ, Seo B, Katz A et al. . Concordance with ASCO guidelines for surveillance after colorectal cancer treatment: a population-based analysis. J Oncol Pract 2012;8:69–79. 10.1200/JOP.2011.000396 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10. Canadian Cancer Society, Statistics Canada, Public Health Agency of Canada, Provincial/Territorial Cancer Registries. Canadian Cancer Statistics 2015. https://www.cancer.ca/~/media/cancer.ca/CW/cancer%20information/cancer%20101/Canadian%20cancer%20statistics/Canadian-Cancer-Statistics-2015-EN.pdf.
- 11. CanIMPACT: The Canadian Team to Improve Community-Based Cancer Care along the Continuum. http://canimpact.utoronto.ca/ [PMC free article] [PubMed]
- 12.Liberati A, Altman DG, Tetzlaff J et al. . The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ 2009;339:b2700 10.1136/bmj.b2700 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Tomasone J, Vukmirovic M, Makarski J et al. . Interventions to improve care coordination between community-based primary healthcare providers and cancer specialists: a systematic review. PROSPERO 2015: CRD42015025006. http://www.crd.york.ac.uk/PROSPERO/display_record.asp?ID=CRD42015025006
- 14.Shea BJ, Grimshaw JM, Wells GA et al. . Development of AMSTAR: a measurement tool to assess the methodological quality of systematic reviews. BMC Med Res Methodol 2007;7:10 10.1186/1471-2288-7-10 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Higgins JPT, Altman DG, Gøtzche PC et al. . The Cochrane Collaboration's tool for assessing risk of bias in randomised trials. BMJ 2011;343:d5928 10.1136/bmj.d5928 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Sterne JAC, Higgins JPT, Reeves BC, on behalf of the developing group for ACROBAT-NRSI. A cochrane risk of bias assessment tool: for non-randomized studies of interventions (ACROBAT-NRSI), Version 1.0.0 2014. http://www.riskofbias.info
- 17.Aubin M, Giguère A, Martin M et al. . Interventions to improve continuity of care in the follow-up of patients with cancer. Cochrane Database Syst Rev 2012;(7):CD007672 10.1002/14651858.CD007672.pub2 [DOI] [PubMed] [Google Scholar]
- 18.Howell D, Hack TF, Oliver TK et al. . Models of care for post-treatment follow-up of adult cancer survivors: a systematic review and quality appraisal of the evidence. J Cancer Surviv 2012;6:359–71. 10.1007/s11764-012-0232-z [DOI] [PubMed] [Google Scholar]
- 19.Lamb BW, Brown KF, Nagpal K et al. . Quality of care management decisions by multidisciplinary cancer teams: a systematic review. Ann Surg Oncol 2011;18:2116–25. 10.1245/s10434-011-1675-6 [DOI] [PubMed] [Google Scholar]
- 20.Lewis R, Neal RD, Williams NH et al. . Nurse-led vs. conventional physician-led follow-up for patients with cancer: systematic review. J Adv Nurs 2009;65:706–23. 10.1111/j.1365-2648.2008.04927.x [DOI] [PubMed] [Google Scholar]
- 21.Ouwens M, Hulscher M, Hermens R et al. . Implementation of integrated care for patients with cancer: a systematic review of interventions and effects. Int J Qual Healthcare 2009;21:137–44. 10.1093/intqhc/mzn061 [DOI] [PubMed] [Google Scholar]
- 22.Bergholdt SH, Hansen DG, Larsen PV et al. . A randomised controlled trial to improve the role of the general practitioner in cancer rehabilitation: effect on patients’ satisfaction with their general practitioners. BMJ Open 2013;3:pii: e002726. 10.1136/bmjopen-2013-002726 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Grunfeld E, Julian JA, Pond G et al. . Evaluating survivorship care plans: results of a randomized, clinical trial of patients with breast cancer. J Clin Oncol 2011;29:4755–62. 10.1200/JCO.2011.36.8373 [DOI] [PubMed] [Google Scholar]
- 24.Johnson CE, Saunders CM, Phillips M et al. . Randomized controlled trial of shared care for patients with cancer involving general practitioners and cancer specialists. J Oncol Pract 2015;11:349–55. 10.1200/JOP.2014.001569 [DOI] [PubMed] [Google Scholar]
- 25.King M, Jones L, McCarthy O et al. . Development and pilot evaluation of a complex intervention to improve experienced continuity of care in patients with cancer. Br J Cancer 2009;100:274–80. 10.1038/sj.bjc.6604836 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Wagner EH, Ludman EJ, Aiello Bowles EJ et al. . Nurse navigators in early cancer care: a randomized, controlled trial. J Clin Oncol 2014;32:12–8. 10.1200/JCO.2013.51.7359 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Wulff CN, Vedsted P, Søndergaard J. A randomized controlled trial of hospital-based case management in cancer care: a general practitioner perspective. Fam Pract 2013;30:5–13. 10.1093/fampra/cms050 [DOI] [PubMed] [Google Scholar]
- 28.Aljarabah MM, Borley NR, Goodman AJ et al. . Referral letters for 2-week wait suspected colorectal cancer do not allow a ‘straight-to-test’ pathway. Ann R Coll Surg Engl 2009;91:106–9. 10.1308/003588409X359114 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Baliski C, McGahan CE, Liberto CM et al. . Influence of nurse navigation on wait times for breast cancer care in a Canadian regional cancer center. Am J Surg 2014;207:686–91. 10.1016/j.amjsurg.2014.01.002 [DOI] [PubMed] [Google Scholar]
- 30.Blinder VS, Norris VW, Peacock NW et al. . Patient perspectives on breast cancer treatment plan and summary documents in community oncology care: a pilot program. Cancer 2013;119:164–72. 10.1002/cncr.27856 [DOI] [PubMed] [Google Scholar]
- 31.Dulko D, Pace CM, Dittus KL et al. . Barriers and facilitators to implementing cancer survivorship care plans. Oncol Nurs Forum 2013;40:575–80. 10.1188/13.ONF.575-580 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Hall SJ, Samuel LM, Murchie P. Toward shared care for people with cancer: developing the model with patients and GPs. Fam Pract 2011;28:554–64. 10.1093/fampra/cmr012 [DOI] [PubMed] [Google Scholar]
- 33.Jefford M, Lotfi-Jam K, Baravelli C et al. . Development and pilot testing of a nurse-led posttreatment support package for bowel cancer survivors. Cancer Nurs 2011;34:E1–10. 10.1097/NCC.0b013e3181f22f02 [DOI] [PubMed] [Google Scholar]
- 34.Jiwa M, Longman G, Sriram D et al. . Cancer care coordinator: promoting multidisciplinary care—a pilot study in Australian general practice. Collegian 2013;20:67–73. 10.1016/j.colegn.2012.03.007 [DOI] [PubMed] [Google Scholar]
- 35.Knowles G, Sherwood L, Dunlop MG et al. . Developing and piloting a nurse-led model of follow-up in the multidisciplinary management of colorectal cancer. Eur J Oncol Nurs 2007;11:212–23. 10.1016/j.ejon.2006.10.007 [DOI] [PubMed] [Google Scholar]
- 36.McFarlane K, Dixon L, Wakeman CJ et al. . The process and outcomes of a nurse-led colorectal cancer follow-up clinic. Colorectal Dis 2012;14:e245–249. 10.1111/j.1463-1318.2011.02923.x [DOI] [PubMed] [Google Scholar]
- 37.Sprague BL, Dittus KL, Pace CM et al. . Patient satisfaction with breast and colorectal cancer survivorship care plans. Clin J Oncol Nurs 2013;17:266–72. 10.1188/13.CJON.17-03AP [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38.Vanhuyse M, Bedard PL, Sheiner J et al. . Transfer of follow-up care to family physicians for early-stage breast cancer. Clin Oncol (R Coll Radiol) 2007;19:172–6. 10.1016/j.clon.2007.01.115 [DOI] [PubMed] [Google Scholar]
- 39.Craig P, Dieppe P, Macintyre S et al. . Developing and evaluating complex interventions: the new Medical Research Council guidance. BMJ 2008;337:a1655 10.1136/bmj.a1655 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Moore GF, Audrey S, Barker M et al. . Process evaluation of complex interventions: Medical Research Council guidance. BMJ 2015;350:h1258 10.1136/bmj.h1258 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41.Cane J, O'Conner D, Michie S. Validation of the theoretical domains framework for use in behaviour change and implemention research. Implement Sci 2012;7:37 10.1186/1748-5908-7-37 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 42.Damschroder LJ, Aron DC, Keith RE et al. . Fostering implementation of health services research findings into practice: a consolidated framework for advancing implementation science. Implement Sci 2009;4:50 10.1186/1748-5908-4-50 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 43.Clark AM. What are the components of complex interventions in healthcare? Theorizing approaches to parts, powers and the whole intervention. Soc Sci Med 2013;93:185–93. 10.1016/j.socscimed.2012.03.035 [DOI] [PubMed] [Google Scholar]
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Supplementary Materials
esmoopen-2016-000077supp.pdf (131.7KB, pdf)