Identifying components of care coordination for primary brain tumor: A scoping review

Abstract

For people with primary brain tumors (PBT) and their carers, care coordination (CC) offers comprehensive, timely, person-centered care. This review aimed to systematically scope the breadth of literature relevant to approaches to CC for PBT. Four databases were searched (PubMed, PsycINFO, EMBASE, and CINAHL) for empirical research, and gray literature was searched for doctoral theses, clinical guidelines, and education resources for healthcare professionals (HCPs) related to the concept/model of CC in neuro-oncology. Data were systematically evaluated and synthesized following PRISMA-SCR guidelines. From 1163 screened abstracts, 30 eligible reports were reviewed (13 addressed CC interventions, 9 narrative reports, 5 describing CC/navigator positions, and 3 clinical guidelines). Most reports described nurse-led models of care within single tertiary care centers in metropolitan settings: a single HCP acting as primary contact, educator, and liaison, screening patient/carer distress and providing referrals as key components of CC. Clinical guidelines emphasize healthcare system navigation and access to medical care in CC. A CC approach overseeing the whole PBT trajectory was lacking. Facilitators of CC included availability of HCP dedicated to CC; HCPs’ competency in relationship-based and communication skills; and improved access to resources. System-level and resource barriers to CC were identified. Knowledge about CC is largely based on descriptions of nurse-led models of PBT care. Further research is required to refine the framework of CC reflecting factors of known importance in PBT care, and identify training and support needs of HCPs who may play a pivotal role in current models of neuro-oncology CC.

Key Points.

• Coordinated brain tumor care and tailored psychosocial support are essential.

• Current approaches focus on navigating specialist care and nurse/coordinator-led models.

• Care coordination is poorly defined and not reflective of unique challenges in neuro-oncology.

Primary brain tumors (PBTs) refer to a heterogeneous group of benign and malignant tumors originating in the brain. Malignant PBTs constitute ~1.3% of all cancers diagnosed in the United States and 1.5% in Australia.^1,2 Adult glioblastoma (GBM; WHO grade IV) is the most common malignant PBT diagnosis and the most aggressive.³ PBT 5-year survival rates are variable, ranging from 6.6% (GBM) to over 90% (lower-grade gliomas), with a mean rate of 35.6% for all malignant PBT.^4,5 People with PBT and their carers experience a significant level of distress due to perceptions of PBT as terminal cancer affecting a vital, irreplaceable organ. Long-term disability and eventual tumor progression or recurrence with further functional decline are common in PBT, including lower-grade gliomas, contributing to the devastating impact of PBT on individuals and families.^6–8 Many people with PBT experience a range of symptoms including persistent physical (eg, weakness or impaired coordination), cognitive, emotional and behavioral (eg, agitation, depression, anxiety, or sleep disturbances), or neurological complaints (eg, seizures, vision, or hearing problems) some of which may be irreversible.^9–11 In addition, the diagnosis of PBT comes as a surprise for many people, both young and old, followed by rapid transition into neurosurgery and cancer treatment.¹² The impact of PBT may be exacerbated for young people as persistent physical and cognitive impairments often lead to unemployment and financial instability.¹² The unique set of challenges along the PBT disease trajectory results in high unmet needs for support and information and poorer health-related quality of life.^13,14

Due to high symptom burden and diverse functional impairments, individually tailored support and coordinated care are essential to assist people with PBT and their carers/families navigating the disease, healthcare system, treatment, symptoms and side-effects, personality and behavior changes, survivorship, and/or end-of-life care. For carers/families, access to bereavement support may also be required.¹⁵ Effective and high-quality coordination of care is critical throughout the disease trajectory, to ensure individuals with PBT receive timely and appropriate services and care without “falling through the cracks” in the system.¹⁶ It has been argued that effective care coordination (CC) can lead to improved continuity of care, provision of systematic, cost-effective, and connected care, and a reduction in barriers to timely access to appropriate health services for those with PBT.¹⁷ Similarly, CC interventions have been shown to improve patient-reported health outcomes and quality of end-of-life care and lead to appropriate healthcare utilization across cancer populations in the United States.¹⁸

For this review, the term care coordination is defined as a comprehensive approach to achieving continuity and consistency of multidisciplinary healthcare through clear communication, linkages, and collaborative integrated care planning to ensure a systematic and timely delivery of care according to the medical and psychosocial needs of individual patients.^17–19 Key activities related to CC include organizing care, conducting psychosocial assessment, systematic monitoring of symptoms and unmet needs, and providing referrals, information, and individualized treatment plans that consider both individual and family needs and preferences.²⁰ Care coordinators for PBT were introduced in the last 10–15 years in Australia, largely informed by a general cancer care coordinator framework¹⁹ or nurse-led care models widely adopted in breast cancer.^21,22 Cancer care coordinators act as lead healthcare professional (HCP) overseeing patient navigation, education, coordination, and survivorship care.^22,23 With this approach, a considerable proportion of people with PBT do not receive coordinated and continuous care due to their tumor type and geographical location, especially when transitioning to outpatient care or a different care team.

More recently, telehealth-based strategies to improve access to information and supportive care for Australian people with PBT and their carers have been reported.^24–26 Although these interventions did not directly aim to improve CC for people with PBT, they provide important insight into components of models of continuous, coordinated, and person-centered care for people with high-grade gliomas (HGGs) and their carers. Therefore, assimilating evidence from a broader literature examining interventions and/or models of CC and supportive care for PBT globally was warranted to develop an evidence-based framework of optimal CC for people with PBT and improve access to continuous care in Australia.

This review aimed to systematically scope and examine evidence and clinical resources relevant to the conceptualization and practice of CC for people with PBT and their carers. We specifically focused on identifying: (1) components within the current practice of CC across healthcare settings and tumor types; (2) interventions or strategies to improve CC and its effectiveness; (3) tools or core approaches used to evaluate the effectiveness of CC; and (4) facilitators or barriers to implementation of optimal CC for people with PBT.

Materials and Methods

A systematic scoping review was conducted to address the research aims given the heterogeneous literature identified.²⁷ This scoping review followed the reporting guideline of Preferred Reporting Items for Systematic Reviews and Meta-Analyses extension for Scoping Reviews (PRISMA-ScR) Checklist.²⁸ The original review aims were formulated based on the patient, intervention, comparison, outcome (PICO) framework and subsequently integrated into the population, concept, and context (PCC) framework following Joanna Briggs Institute (JBI) methodological guidance for the conduct of scoping reviews.^29,30 Online database searches on International Prospective Register of Systematic Reviews (PROSPERO) and Open Science Framework (OSF) using key search terms of brain tumor/tumour and care coordination yielded no recent or ongoing reviews registered prior to April 2023. The protocol for this review was registered prospectively on OSF on April 18, 2023 (https://osf.io/p8xgv).

Eligibility Criteria

Types of evidence

Both journal articles and gray literature published in English to June 21, 2024 (date of last search) were included to explore the breadth of existing evidence. Gray literature was limited to clinical resources, practice guidelines, and reports by HCP organizations, education materials for HCP, or doctoral dissertations. Eligible empirical study designs included cross-sectional, cohort, descriptive, observational, pilot, feasibility, pre-post intervention studies, randomized controlled trials (RCTs), case studies, case reports, or qualitative studies.

Population

The population of interest was adults (≥18 years) with PBT and/or family/carers.

Concept (Intervention and Outcomes)

Intervention, descriptive, and/or implementation studies entailing development, description, evaluation, or implementation of CC for people with PBT and their carers were considered. Interventions targeted one or more activities related to CC; for example, improving continuity of care, psychosocial care, care transitions, case management, interdisciplinary communication and care planning/pathways (eg, transmission of patient information and referral pathways), follow-up care plans, or symptom monitoring and management processes. Research studies not directly targeting CC were included only if they discussed useful inferences to components and facilitators of CC; identified gaps in current care and services; and inferred strategies to improve aspects of CC. There was no single evaluation tool for cancer CC, and outcome measures for a range of strategies used to achieve CC were included (see Supplementary Materials).

Context (Comparators and Settings)

Elements of CC were compared across healthcare system contexts, such as elements of CC in Australia versus other countries; metropolitan versus regional or rural settings; benign tumor, lower-grade, versus HGGs; and between modes of contact or communication. When examining an intervention, the control was defined as usual or standard care in the relevant health system within the time and clinical context of the study, or as specified in the study, including baseline or pre-intervention outcomes in a pre-post design.

Search Strategy

Four databases (PubMed, PsycINFO, EMBASE, and CINAHL) were searched for published articles (see Supplementary Materials for search terms). Theses and dissertations were searched in ProQuest Dissertations & Theses Global and Trove National Library of Australia. Hand-searching was carried out for reports and practice guidelines, potentially eligible studies from systematic reviews, meta-analyses, and reference lists of relevant studies.

Pilot database searches using the pre-specified search terms were performed by 2 researchers (M.S.J. and S.H.) on PubMed to ensure consistent search results and to maximize the number of studies identified. Amendments to search terms were made accordingly and documented.

Selection Process

Search records were imported into the systematic review software (Covidence³¹) with duplicates removed. Two reviewers (M.S.J. and S.H.) independently reviewed potential relevance of all titles and abstracts and developed an agreed list of relevant articles, full-text copies of which were then retrieved. Four reviewers (M.S.J., S.H., H.B., and T.C.) independently assessed full-text copies for inclusion. Reviewers met to confirm included and excluded studies, and disagreements were resolved by team discussion.

Data Extraction and Synthesis

A data extraction template was developed prior to data collection based on consensus among researchers (Table 1). Data were independently extracted by authors (M.S.J, S.H., H.B., and T.C.) who met to review data collected and revise the template as needed. Based on the definition and key activities of CC in healthcare literature, we examined CC as it related to content and implementation of a model of CC. Specifically, we aimed to identify (1) components within the current practice of CC across healthcare settings and tumor types. We extracted data for the general concept/approach to CC within PBT care, where reported; main focus/objectives of CC; care recipient (ie, patient, carer, or dyad); who oversees CC; timing of care/CC; care planning; and components of CC models (or duties/activities if a report described the position of a care coordinator) including assessment, referral, information provision, and/or other support related to CC. Identified components were grouped based on the nature of CC roles/activities and examined on the extent to which they appeared across different models of CC and/or whether they constituted main components of a given model/approach to CC using content analysis. Components were compared across healthcare settings, geographical locations, and tumor subtypes to identify core components applicable across settings and tumor types. We also specifically aimed to scope (2) available interventions or strategies to improve CC, and (3) how the effectiveness of CC was evaluated. Research studies reporting an intervention of CC were identified and grouped by main approach to CC, and data related to CC were extracted as listed above. Where outcomes of a model/intervention of CC were reported, data for report category, type of outcome, outcome measure/assessment tool, timepoint, and findings related to the effectiveness of CC were extracted and examined. In terms of CC implementation, data were extracted for practical/logistical considerations, resources, healthcare staff training, limitations of current practice, facilitators, and barriers to implementation of a given model of CC. The data were analyzed qualitatively using content analysis and synthesized using a systematic, narrative review approach.

Table 1.

Data Extraction Template

Variable	Data extracted
Participants/populations	Patients (age), caregivers, and healthcare professionals
Study design Type of report	The key features of the study
Diagnosis	Primary brain tumors (clinical diagnosis, point in disease trajectory, and prior/current/planned treatment)
Clinical setting or level of care	Primary, secondary, tertiary, etc., type of care (private or public)
Number of participants	The number of potential participants approached, participated, and followed up
Intervention	Full description; stated theoretical/conceptual basis; aims; training strategies used; how/by whom delivered; duration and timing
Control/comparator	Usual care; wait-list; between group comparison; pre-post
Outcome measures	Outcome measures and timing of outcome assessment
Results	Study findings Outcomes of a care coordination intervention or model
Care coordination	Information on a model/practice of care coordination 1) Factors to consider—Concept/approaches a. Focus b. Objectives c. Care recipient (target) d. Personnel e. Timing and care planning f. Content (components; eg, assessment and referrals) 2)Factors to consider—Implementation a. Practical and logistical factors b. Resources/training required c. Facilitators d. Barriers 3)Existing models a. Description b. Target/timing in brain tumor trajectory c. Essential features d. Advantages/effectiveness (+ methods to assess this) e. Areas for improvement

Critical Appraisal of Included Reports

Two reviewers (H.B. and T.C.) independently assessed methodological rigor of included reports using the JBI critical appraisal checklists.^32,33 Research studies were assessed using the JBI criteria for case reports, RCTs, quasi-experimental, qualitative, cohort, and cross-sectional studies. Studies were assessed with the checklist most relevant to their design, with each criterion being scored as: met; not met; unclear; or not applicable. We applied the JBI criteria for policies/consensus guidelines to clinical guidelines, and criteria for narratives or expert opinions to descriptive reports and narrative pieces, using the same scoring metric. Scoring disagreements were resolved through discussion.

Results

Database searches yielded 1332 titles for published articles and the manual search an additional 51 records including published articles, clinical guidelines and reports, and gray literature. After removing duplicate reports, 1163 abstracts were screened, of which 137 were selected for full-text review for eligibility. Full texts were retrieved for 134 records. For 2 journal articles reporting data from mixed cancer samples, corresponding authors were contacted to request data relating to adult PBT sub-samples but subsequently excluded due to a lack of response. We included a total of 30 reports in our review. The study selection process and reasons for exclusion are shown in Figure 1.

Figure 1.

Study selection process.

Results of quality assessment of 29 studies assessed with the JBI checklists are shown in Table 2. The online educational module (Report 25)³⁴ was not applicable for risk of bias assessment using the JBI criteria. We identified a wide range of research methodologies for research studies, including one RCT of a nurse-led intervention.²⁶ Most research studies and descriptive reports demonstrated sound methodological rigor overall (4 met all relevant criteria). Clinical guidelines were developed by well-established organizations/research groups and key stakeholders with expertise in neuro-oncology (details about processes of evidence-based development were available for 2/3 clinical guidelines). There was an elevated risk of bias for one report (Report 30)³⁵ describing challenges for people with brain tumors (BT) presenting to the emergency department. We report summary findings of this study in Supplementary Table S1 denoting the sampling issue, however excluded it from data synthesis for identifying components/outcomes of CC.

Table 2.

JBI Quality Checklist Scores for Included Reports

Characteristics of Included Reports

Report category

Table 3 details the study characteristics of the 30 included reports. Of these, 22 published articles of research studies were categorized into intervention studies (n = 13) targeting development or implementation of coordinated care as pre-defined by the eligibility criteria, or descriptive reports (n = 9) if the study focused on describing participant reported outcomes or clinical data. Notably, descriptive reports had indirect relevance to coordination of care, as these studies aimed to identify gaps in current care and services and infer strategies to improve certain parts of CC.

Table 3.

Study Characteristics (n = 30)

Study characteristics	N	%
Report type
Research study—Intervention	13	43
Research study—Descriptive	9	30
Position description	5	17
Clinical guideline/government report	3	10
Country
Australia	13	43
USA	12	40
Europe (incl. UK)	5	17
Year of publicationa
2019–2023	17	57
2013–2018	8	27
<2012	5	17
Level of care
Tertiary	18	60
Secondary	4	13
Secondary and tertiary	3	10
All levels	2	7
Not reported	3	10
Clinical setting
Metropolitan	19	63
Regional/rural	0	0
Mixed	3	10
All health settings	3	10
Not reported/applicable	5	17
Population of interest
Brain cancer	17	57
High-grade gliomas (HGG)	9	30
Caregivers of people with brain cancer	1	3
Caregivers of people with HGG	3	10

^aYear last reviewed for clinical or healthcare professional training material.

Four reports and one online learning module for HCPs (position descriptions, n = 5) described position development (varying position titles, including neuro-oncology care coordinator, or clinical nurse coordinator) in a specific clinical context and clinical duties, and activities allocated to a designated HCP. In addition, we identified 3 clinical guidelines which partially discussed components of care with some relevance to CC.

Table 4 summarizes the study sample, key findings, and relevance to CC of intervention studies, and Supplementary Table S1 reports summary findings of included reports in the other report categories.

Table 4.

Findings of Intervention Studies (n = 13)

Study ID	Research context	Intervention	Outcome measures	Key findings	Relevance to care coordination
1 - Riblet (2014, USA)	Study design: retrospective cohort study. Sample: people with glioma (n = 98 at baseline; n = 63 at follow-up). Clinical setting: tertiary; metropolitan.	Intervention: changes to improve clinical care pathway. Key changes include: (1) Introducing a standardized template to document that patients were counseled about clinical trials and symptoms of concern. (2) Clinic secretary scheduling independent social worker visits for patients and families. (3) Encouraging clinicians to document clinical outcomes (eg, treatment complications). (4) Aiming to provide pathology results within 5 days. Control/comparator: original clinical care pathway.	Difference between baseline and post-intervention on 12 best practice measures.	There were significant improvements in 5/12 of the best practice measures. The proportion of patients meeting criteria for all 12 measures modestly improved (65% → 76%). However, this change was not statistically significant.	Highly relevant: describes a clinical pathway for glioma patients and ways to improve said pathway.
3 - Miller (2018, USA)	Study design: narrative description. Patient population: primary BTs Clinical setting: tertiary; metropolitan.	Intervention: introduction of a neuro-oncology nurse navigator. Control/comparator: N/A.	Informal feedback, number of patient-navigator interactions and time to start of treatment.	Several signs of effective nurse navigation: (1) Positive informal feedback was received from patients and providers. (2) Increased patient volume and number of patient-navigator encounters. (3) The time between surgery and the start of radiation was reduced.	Highly relevant: describes the successful implementation of a neuro-oncology nurse navigation program.
6 - Zeitouni (2020, USA)	Study design: retrospective cohort study. Sample: people with glioma undergoing unplanned neurosurgery and adjuvant treatment; n = 66 (45 intervention, 21 historical controls). Clinical setting: tertiary; metropolitan.	Intervention: nurse-driven care coordination: included department-wide access to a multidisciplinary follow-up list which aimed to improve communication between inpatient neurosurgeons and outpatient neuro-oncology nurse navigators. Control/comparator: Historical controls	Time from neurosurgery to: (1)Neuro-oncology follow-up. (2)Start of radiation. (3)Start of chemotherapy.	Compared to historical controls, the intervention group was associated with more patients following up with neuro-oncology at 2 weeks (30% vs. 51%), more patients starting radiation within 30 days of neurosurgery (25% vs. 44%) and more patients starting chemotherapy within 30 days of neurosurgery (35% vs. 59%).	Moderately relevant: highlights the importance of care coordination as an essential component to ensure timely follow-up care.
8 - Philip (2019, AUS) & 9 - Philip (2020, AUS) Note. Two reports of the single intervention study	Study design: open-label single-arm pilot study. Sample: newly diagnosed HGG patients/caregivers (n = 32 patients; n = 31 caregivers). Clinical setting: single tertiary metropolitan cancer center (Melbourne, Australia).	Intervention: I-CoPE (Information, Coordination, Preparation and Emotional). A care coordinator delivered intervention consisting of: (1) Staged information. (2) Regular screening for needs. (3) Communication and coordination. (4) Family caregiver engagement. Control/comparator: N/A.	Primary outcomes: feasibility and acceptability Secondary outcomes: (1) Short-term effectiveness of intervention. (2) Severity and content of key patient/caregiver concerns using the distress thermometer and problem checklist.	Feasibility outcomes: intervention had high accrual rates—86% of patients enrolling and 88% completing the study. Ninety-four percent of caregivers also completed the study. Regular screening was manageable and resulted in fewer spontaneous calls from patients/caregivers. However, feasibility was impacted by poor health and/or cognitive deficits among patients. Intervention was associated with lower support and information needs for patients and caregivers. There were no significant changes in QoL. Distress and unmet needs outcomes: 60% of patients and 87% of caregivers reported clinically significant distress at diagnosis. This distress fluctuated over time. Patient concerns were mainly in the spiritual or existential domains. Physical and health-related concerns were minimal at diagnosis but became a greater focus during treatment. Initially, caregiver concerns were focused on practical caring responsibilities and treatment questions. However, over time emotional concerns became more prevalent.	Highly relevant: provides a structured supportive care approach for people with newly diagnosed HGG and their family caregivers which is delivered by care coordinators.
10 - Knowlton (2023, USA)	Study design: descriptive study. Sample: 15 HCPs experienced in treating BTs. Clinical setting: tertiary, metropolitan inpatient rehabilitation center (northeastern USA).	Intervention: care coordination checklist to facilitate communication between MDT members and address patient needs. Control/comparator: N/A.	Clinician feedback on quality improvement survey.	Majority of participants believed that the checklist had positive effects on care delivery, patient experience, and communication between healthcare providers.	Highly relevant: reports on the development of a seemingly effective care coordination checklist for HCPs.
12 - DeSwart (2021, NL)	Study design: prospective cohort study. Sample: 255 patients with suspected neuro-oncological disease (primary or otherwise) (72 intervention; 153 control). Clinical setting: tertiary; metropolitan.	Intervention: digital referrals to a multidisciplinary neuro-oncology triage panel (neurologist, neurosurgeon, and neuroradiologist). Control/comparator: standard referral pathway via fax, mail, email, or telephone consultation.	Primary outcomes: lead times to referral and treatment. Secondary outcomes: cost of information exchange and time investment from HCPs.	The intervention group received significantly faster referrals compared to those in the standard referral pathway (1 vs. 6 days). Estimated costs and time investment were comparable for both groups.	Moderately relevant: demonstrates ways to improve the timely referrals aspects of care coordination.
14 - Nichols (2015, AUS)	Study design: descriptive report and reflection of clinical experience. Patient population: primary BT patients and caregivers. Clinical setting: tertiary; public (Liverpool Hospital, Sydney, Australia).	Intervention: nurse-led BT support group with education program that incorporated a coordinated approach to delivering person-centered care for patients and caregivers. Control/comparator: N/A.	N/A	Activities and interventions that reflect the tenets of the primary healthcare (PHC) framework result in improved outcomes for patients/caregivers (ie, appropriate technology, collaboration, accessibility, health promotion, and public participation). Multidisciplinary collaboration was especially key for sustaining the initiative.	Moderately relevant: demonstrates how to improve care coordination through a nurse-led support group. Support group was informed by the PHC framework, which is frequently referenced in care coordination literature.
17 - Tepper (2003, USA)	Study design: descriptive report. Patient population: primary BT patients and caregivers. Clinical setting: tertiary; metropolitan.	Intervention: transitions Program Model; a program that provides education, counseling services, and psychological support at critical time points across illness trajectory (ie, diagnosis, progression, hospice referral, and bereavement). Control/comparator: N/A.	N/A	N/A—Descriptive report of the steps taken to develop and implement the Transitions Program.	Highly relevant: provides coordinated supportive care protocols for key time points along illness trajectory.
20 - Dionne-Odom (2021, USA)	Study design: retrospective evaluation of a single-center pilot study. Sample: 53 caregivers of people with grade IV glioma. Clinical setting: tertiary; metropolitan (Alabama, USA).	Intervention: FamilyStrong; a nurse-led telehealth support service for caregivers. Includes: (1) Distress screening every month and comprehensive assessment every 3 months. (2) Vetted education materials and/or referrals to supportive services. (3) Assessment, follow-up care, and referrals to bereaved caregivers. Control/comparator: N/A.	Distress thermometer, GAD-2 (for anxiety), PHQ-2 (for depression), reported problems, number of calls, and assessments and actions provided by palliative care nurse.	A total of 277 phone calls were made. Of these, 235 included a distress screening that averaged 11.4 min. More than half of the distress screening indicated instances of moderate to high distress. The most common problems caregivers wanted help with included managing the patient’s health, coordinating care/services, and planning for the future. There were 211 documented actions assisting caregivers based on their distress screening and assessment.	Highly relevant: provides a model of nurse-led telehealth care coordination for caregivers of people with HGG.
26 - Halkett (2023, AUS)	Study design: Phase III RCT. Sample: caregivers of people newly diagnosed (within 2 months) with HGG undergoing chemoradiation; n = 188 (98 intervention, 90 control). Clinical setting: tertiary; public.	Intervention: Care-IS; a nurse-led caregiver-specific intervention that includes: (1)Initial telephone assessment of unmet needs. (2)Tailored hard-copy resource folder. (3)Home visit. (4)Monthly telephone support for up to 12 months. Control/comparator: usual care.	Primary outcomes: distress thermometer and preparedness for caregiving scale. Secondary outcomes: hospital anxiety and depression scale (HADS); Quality of life (CQOL-C); Caregiver Competence Scale; Modified Caregiver Strain Index	Compared to the control group, the intervention group had significantly higher caregiver preparedness at 4 months and at follow-up time points up to 12 months. There were no significant effects on distress or any secondary outcomes (anxiety and depression, quality of life, competence, and strain).	Moderately relevant: intervention to support caregivers that includes core components of care coordination (eg, routine assessment, timely referrals, and resource provision).
27 - Page (2017, USA)	Study design: descriptive report of observations and preliminary findings. Sample: 334 caregivers of people with GBM. (90 newly diagnosed, 198 transitioning, 149 bereaved). Clinical setting: tertiary; metropolitan.	Intervention: caregiver-specific program to provide additional services and address unmet needs. Run by a dedicated team consisting of a medical director, nurse clinician, social worker, and administrative program manager. Included informal screening and needs assessment to guide interactions, referrals and support. Support was offered to 4 caregiver subgroups: (1)Needs assessment and an education packet for new-to-clinic caregivers. (2)Four proactive telephone check-ins, assessment and support for caregivers of newly diagnosed GBM patients. (3)Assessment, support, and referrals for caregivers of high-risk/transitioning patients (either in person or over telephone). (4)Telephone check-ins, assessment, and intervention at 1 and 6 months post-death for bereaved caregivers. Control/comparator: N/A.	Caregivers seen, identified needs and services provided in the first 2 years of the program.	Caregivers of patients in transition reported a higher percentage of needs compared to caregivers of newly diagnosed patients. Caregivers of newly diagnosed and transitioning patients had highest needs around emotional support and advocacy, followed by family dynamics and procuring home services. Overall, caregiver needs and the timing in which individuals desire support varies among caregivers. Repeated outreach increased knowledge of the program and satisfaction with care provided.	Highly relevant: reports on the development of a caregiver-specific program that includes core elements of care coordination (eg, needs assessment, referrals, and tailored support).
29 - Spetz (2008, SE)	Study design: inspired by action research, including practical inquiry, field notes, and interview data. Sample: 16 caregivers of people with HGG. Clinical setting: secondary; metropolitan.	Intervention: specialist nurse approached next-of-kin during diagnosis, gave them her number, and told them that they could use her as a point of contact and resource when they wanted. Caregivers were given the option of who initiated contact (ie, them or the nurse). Control/comparator: N/A.	Field notes about how next-of-kin used specialist nurse throughout disease. After the patient’s death, bereaved caregivers were interviewed to give feedback on the specialist nurse’s function.	Contact related to the patient was the focus of contact in the early stages of the disease. However, as the disease progressed, contact increasingly focused on personal concerns and needs. Initially, the specialized nurse was used as an “informational resource”; however, over time the relationship with the specialist nurse became more personal.	Highly relevant: specialist nurse provided coordinated care for caregivers by being a point of contact for practical, emotional, and informational needs.

Abbreviations: AUS = Australia; BT = brain tumor, DE = Denmark; GBM = glioblastoma multiform; GP = general practitioner; HCP = healthcare professional; HGG = high-grade glioma; MDT = multidisciplinary team; NL = Netherlands; SE = Sweden; UK = United Kingdom; USA = United States of America.

Location and clinical setting

Most included reports were conducted in Australia (n = 13, 43%) and the USA (n = 12, 40%), over the past 5 years (n = 17, 57%). Most were set in secondary or tertiary level care (n = 25, 83%), and within single metropolitan cancer centers (n = 19, 63%). The call for coordinating care across more than one level of care or clinical setting was only evident in a supportive and palliative care framework³⁶ or the “Optimal Care Pathway for people with high-grade glioma (HGG)” by Cancer Council Victoria.¹⁷ No report specifically focused on CC in regional or rural settings was identified. The population of interest included 17 (57%) targeted all brain cancers, 9 (30%) targeted HGG, and 4 (13%) targeted informal carers of people with brain cancer.

Timing of care across PBT trajectory

To examine the clinical coverage and identify gaps in continuity of care, reports were mapped across the 6 phases of the brain tumor disease trajectory, informed by key transition points in a supportive care framework for people with HGG.³⁶Figure 2 illustrates coverage of phases broadly mentioned by each report, with or without specific phase(s) focus, in terms of CC. Most reports mentioned early disease phases from diagnosis, acute treatment to post-treatment follow-up. Seven reports focused on one or more phases in this early period as the key timing of CC for PBT (depicted with darker shades in Figure 2). Many reports (n = 20) mentioned tumor recurrence/progression and end-of-life phases, although fewer (n = 7) considered the bereavement phase within a concept/model of coordinated care. Only 2 clinical guidelines and 2 position descriptions discussed the timing of introducing palliative care. Four reports (1 intervention and 3 descriptive reports) did not mention the timing of care and are not shown in Figure 2.

Figure 2.

Phases of disease trajectory covered by included reports. Note. Reports 4, 14, 15, and 19 did not mention the timing of care; darker colors reflect the focus of the article; ● = point to consider introducing palliative care.

Current Approaches To and Components of CC

Current approaches to CC for PBT emphasize healthcare system navigation and access to medical care through a HCP dedicated to CC.^17,37 For example, CC enables patients “to successfully navigate the complex health system” and “to ensure care is delivered in a systematic, connected and timely way that promotes efficiency and reduces the risk of duplication and over-servicing to meet the medical and personal needs of patients” (“Optimal Care Pathway for people with HGG,” p. 14).¹⁷ The scope and components of CC were frequently equated to roles and activities of a care coordinator (nurse navigator in some reports) in promoting healthcare navigation and care delivery. Objectives of CC reflecting this tendency were similarly observed in many included reports.^23,38–47Figure 3 illustrates these objectives and key components commonly reported.^{23,24,39,42–46,48,49} Other components mentioned in fewer reports included discussion of palliative care, peer support and community groups, availability of clinical trials, participation in research, practical support (eg, transport, accommodation, advance care planning, and financial support), and access to telehealth.^17,45,46

Figure 3.

Objectives and components of care coordination reported for people with primary brain tumors. Note. Superscripted numbers refer to references in the reference list.

Several reports highlighted the role of CC in screening for distress to facilitate referral to appropriate care and responding to unmet needs. Individuals with HGG were reported to experience higher levels of distress on the Distress Thermometer (DT) than those with lower-grade or benign PBTs.⁵⁰ A neuro-oncology nurse/care coordinator administering the DT would refer these individuals to relevant allied health or support services (eg, psychologist review).^24,50 In addition, the patient’s unmet information, communication, and supportive needs changed throughout the disease trajectory.^51,52

CC Across Healthcare Settings and Tumor Types

Care coordination was mostly described in secondary (inpatient) or tertiary settings, focused on diagnosis, surgery, and acute treatment phases, making it difficult to compare and comment on components of CC across healthcare settings and levels. The “Optimal Care Pathway for people with HGG”¹⁷ presents several different models of survivorship care in the post-treatment phase, including a model of shared care between specialists and primary care practitioners where appropriate. However, reports describing the current approach to CC in primary/community care and regional/rural settings were lacking overall. A UK qualitative survey of people diagnosed with PBT (n = 84) highlighted gaps in coordination of care and current care standards of primary care (general practice) not meeting people’s expectations.⁵³ These gaps included difficulty receiving timely, accurate diagnosis and follow-up assessment and post-treatment care, lack of prompt referrals and supportive responses from their general practitioner (GP; ie, primary care physician), and poorly coordinated communication between hospitals and GPs about test results, care plans, and symptom management.⁵³ Patients raised the lack of family member or carer involvement in their primary care and reported rehabilitation challenges and feeling alone.⁵³

Care coordination limited to the secondary or tertiary care levels was similarly observed across reports from the Unites States, Australia, and European countries. Unique to the US health system, but relevant to private or mixed systems in other countries, was the importance of identifying patient’s insurance status and discussing insurance needs early in a care coordinator’s communication with the patient to improve postoperative care.⁴¹ This finding may not generalize readily to other non-private healthcare systems.

No systematic patterns or differences were identified when comparing approaches to CC across BT subtypes. Most studies with mixed PBT samples including benign and malignant tumors reported the diagnosis as part of sample characteristics (2 studies^42,54 included a subsample of patients with brain metastases). None conducted subgroup analyses regarding how the CC approach in a given clinical setting varied according to BT diagnosis.

Interventions and Approaches to Neuro-Oncology CC

Research studies involving interventions pertaining to CC depicted 3 main approaches: (1) care coordinator-led models; (2) development and implementation of a clinical pathway or care program; or (3) resources to aid CC activities or processes.

Nurse-led or care coordinator-led interventions/programs

Similar to clinical guidelines and position descriptions, which emphasized the role of a dedicated HCP in coordination of care, most research studies involving CC interventions for PBT described a care coordinator as the lead HCP operating within tertiary cancer centers. Most HCPs in this role were oncology nurses. The target of nurse-led interventions and components of CC differed between models depending on outcomes of interest.

Two US observational studies described nurse navigator-led models of multidisciplinary neuro-oncology care, with a strong focus on outcomes related to healthcare navigation (assisting triage, access to specialists, and coordination of referrals and appointments) and access to timely care (indicated by shorter lead time and increased uptake of follow-up and patient-navigator encounters).^41,43 Other nurse/care coordinator-led models situated CC as a core process in providing patient and carer support. One Australian study⁵⁵ described long-term implementation of a BT peer support group led by a senior neuro-oncology nurse. In addition to CC activities related to identification of patient needs, multidisciplinary collaboration in the abovementioned models, the authors reported educational sessions and peer networking events for patients and carers promoted post-discharge support, patient well-being outside the hospital, and system-level support for BT patients.⁵⁵ However, no formal, systematic evaluation was conducted to assess these outcomes. More recently, a structured supportive care approach was evaluated in a pilot study (n = 32 patients and n = 31 carers) demonstrating high levels of feasibility and acceptability for people with newly diagnosed HGG and their family carers (I-CoPE).²⁴ This model comprised 4 intervention components delivered by care coordinators: (1) staged information; (2) regular screening for needs; (3) communication and coordination; and (4) carer engagement. The model centered on cancer care coordinators’ tasks of relationship forming and communication, provision of accessible and relevant information, distress screening, responding to changing needs of patients and carers, and supportive counseling.^24,52 In both models, coordination was narrowly inferred as nurse/coordinator activities relevant to clinical care to support transitions and facilitate communication between patients and treating teams, treatment planning, and follow-up.

Carer Interventions

Among nurse-led interventions, 3 studies^26,38,56 targeted family carers of individuals with PBT and similarly used elements of CC within their models of carer education and support. In an observational US study, a highly experienced, oncology specialist nurse played the role of resource and communication channel for family members of a person with HGG.³⁸ The nurse provided information and emotional support to family members, supporting clinicians and families to address questions and dissatisfaction with aspects of patient care.³⁸ More recently, 2 carer interventions used a telehealth support service for family carers of individuals newly diagnosed with a HGG (FamilyStrong⁵⁶ US & Care-IS²⁶ Australia). In both interventions, oncology and/or palliative care trained nurses established rapport with carers and followed their caring journey from diagnosis (up to 12 months in Care-IS and into bereavement in FamilyStrong). Regular and systematic monitoring of distress and carer needs constituted a core component in both interventions, which guided delivery of appropriate information/recommendations and referrals to support services. These interventions focused on supporting carers in managing the patient’s health condition and symptoms and coordinating care/services when carer distress was identified. Only the Care-IS program was assessed in a RCT (n = 188), demonstrating improvement in carer preparedness to care but not carer distress or quality of life compared to controls.²⁶ The efficacy of FamilyStrong was assessed retrospectively by analyzing the volume and type of CC activities for carers; pre-post carer-reported outcomes were not reported.⁵⁶ In both reports, data on whether recommendations or referrals were actioned by carers was lacking.

Clinical pathway or program

Another approach to CC was through implementation of a care pathway/program enabling provider or system-level interventions to improve quality and delivery of care. We identified one clinical pathway for glioma in acute care⁴⁶ and another for people with malignant PBT and carers aimed at improving psychosocial care at 5 transition points (diagnosis, progression, hospice referral, post-hospice referral, and post-death).⁴⁸ These clinical pathways identified CC activities required for cancer stages according to established protocols and standards of care for all patients. Some system-level interventions included development of patient and carer education materials; standardized templates for documenting patient-reported issues and clinical outcomes; increased social worker involvement; and use of outcome measures to monitor process and quality of care. Reports were descriptive and lacked data to determine the effectiveness of these clinical pathways.

For carers, the UCSF Neuro-Oncology Gordon Murray Caregiver Program⁵⁷ demonstrated successful implementation of a care system for family carers of people with PBT within a tertiary cancer care setting. This program was designed to be carer-centric and specific, unlike other carer support interventions aimed at helping carers to support patients. It involved a multidisciplinary HCP team, dedicated consultation rooms for carers, and documentation of carer information within the patient medical record.⁵⁷ They identified 4 subgroups of carers with varying levels and types of support needs (eg, a group of carers of people newly diagnosed with GBM), for tailored care pathways consisting of ongoing needs assessment, referral, information, and support.⁵⁷ Regular contact and support provision was shared among the program team members, such as a neuro-oncology nurse, social worker, and program coordinator.⁵⁷ While generalizability of this model may depend on resources available and the model remains to be evaluated, it presents an example of a structured care model with key elements of CC.

Resources to aid CC

Two studies examined feasibility and potential benefits of resources to aid CC.^42,54 A cohort study in the Netherlands showed a neuro-oncology triage panel with a digital referral platform led to more efficient patient data transfer and shorter time from scan to referral to a specialist, compared to the conventional referral pathway.⁵⁴ Another study used a CC checklist for all PBT patients in an inpatient rehabilitation setting to improve communication between multidisciplinary team members and facilitate post-rehabilitation care and follow-up.⁴² The authors reported positive feedback from HCPs, but did not report data on checklist feasibility or effectiveness.⁴² Overall, both resources were developed to improve CC either during pre-diagnosis and referral or within a single postoperative rehabilitation care team, rather than as a model of CC across phases and settings when people with PBT start to engage in neuro-oncology care.

Tools or Core Principles Used to Evaluate the Effectiveness of CC

Most reports described an intervention, and there was a large variability in outcomes used to assess feasibility and preliminary effectiveness. Common outcomes included:

1. Clinical outcomes and healthcare use (eg, accurate diagnosis, hospital admission, complications, toxicity, end-of-life care use, and cost associated with care).^46,54,56

2. Timely care and follow-up (e.g., lead time to referral and/or treatment, percentage of people followed-up).^41,43,46,54

3. Volume and type of nurse/coordinator activities and support provided.^24,38,43

4. Subjective evaluation of a program/intervention by patients, carers, or healthcare providers.^24,38,39,51

5. Patient/carer unmet needs for information and support, quality of life, or emotional preparedness.^24,26,51

Overall, the studies reported a positive impact of various approaches to providing coordinated neuro-oncology care. There was no agreed set of indicators of effective CC. None of the studies provided a theoretical or empirical basis for evaluating the effectiveness of CC.

Facilitators and Barriers to Implementation of Optimal CC

We found facilitators of optimal CC were largely linked to a nurse/care coordinator-led model of CC. One of the most discussed facilitators was the availability of healthcare staff dedicated to CC, to provide regular screening and timely referral to interventions for rapidly changing symptoms and functional declines in people with PBT. Healthcare professionals’ creativity, leadership, competency in relationship-based (eg, rapport-building), and communication skills were key facilitators. Providing HCPs with opportunities to upskill and practice in settings suitable for using their skills would facilitate ongoing implementation of CC. Similarly, instrumental support for HCPs were potential facilitators, such as having clear pathways for referral to specialist and allied health services; improved access to resources to facilitate interdisciplinary communication and referrals; attendance at multidisciplinary team (MDT) meetings; and better access to tools, interventions, or checklists. Lastly, many discussed the importance of recognizing the role of carers in neuro-oncology CC and the wide-ranging psychosocial impacts on people with PBT and their families.

However, system-level barriers were identified, as implementation of a model or intervention required increased staff or workload for a dedicated CC role. These barriers included funding instability and limited access to CC staff outside hospital care. Limited resources and capacity for staff training and staff turnover may hinder systematic use of a developed checklist or care pathway. Also, the conventional neuro-oncology care structure and electronic medical record systems present a challenge for documenting and tracking carer unmet needs, information, referrals, and support provided. Lack of clear communication constituted another major barrier to connected and streamlined care across transitions of care between hospital and primary care, specialist teams, and multidisciplinary team members.

Discussion

This review identified current and novel approaches to CC for people with PBT. Overall, the lack of consensus on a framework of CC in neuro-oncology has led to variable concepts and objectives of CC, regarding what a model of CC should aim to achieve. Hence, a range of components and activities of CC for people with PBT were identified. Based on the clinical guidelines and evidence we reviewed, CC has mostly been adopted as an approach to healthcare system navigation and improved access to medical (ie, specialist) care and support services, especially during the acute treatment phase of PBT. As illustrated in Figure 3, most components of CC are directly related to activities/duties of a HCP dedicated to CC; being a channel of communication, source of information, and rendering timely referrals, to assist people with PBT and their carers to navigate multidisciplinary specialist care and support services. Coordination tasks identified, such as ordering and organizing tests, results, and appointments, and use of checklists to track coordination primarily aimed to achieve this goal. This is consistent with the definition of CC in healthcare more broadly⁵⁸; CC equates to clear communication between individuals and HCPs involved in their care to enable a shared understanding of care needs, care plans, and steps needed for appropriately and timely care delivery.

Notably, many of these components have been previously identified in general cancer care nurse models across the domains of professional role, education, coordination of care, and communication.⁵⁹ Current knowledge about CC based on most reports reviewed did not reflect factors of known importance in neuro-oncology care. For example, neurosurgery, neurological symptoms, functional impairment, cognitive issues, and varying distress levels are additional CC concerns for people with PBT, emphasizing regular screening and timely referral to services, as well as tailoring individual patient care.³⁶ These PBT symptoms are highly debilitating, impairing the ability of individuals with PBT to navigate healthcare and maintain quality of life during survivorship when unaddressed as part of CC.⁹ Involving carers facilitated implementation of CC in neuro-oncology, with several studies proposing a model of support for carers to address carers unmet needs and distress.^26,56,57 However, no systematic attempt has been made to determine unique features of PBT experience and adapt definitions and frameworks of CC to suit this population. In addition, a range of outcomes has assessed effectiveness of an approach/intervention at multiple levels ranging from patient to system-level, reflecting difficulty in defining indicators of effective CC for quality benchmarking.¹⁹ Further research is warranted to establish consensus on the framework and components of CC unique to PBT based on consumer and professional stakeholder feedback and establish indicators of effective CC. To progress this work, we have devised a preliminary list of components of CC for people with PBT to initiate discussion among stakeholders (see Supplementary Materials).

Our review highlights several gaps in the literature on CC for people with PBT. Overall, a model of CC and/or interventions targeting CC across the whole PBT trajectory is absent. In particular, palliative, end of life, and/or bereavement care were not always included in models/discussions of CC, despite PBT being associated with high morbidity and mortality. Screening and addressing unmet needs and distress in post-treatment phase and across transitions of care can be difficult, without a care pathway and protocol for regular contact, as shown by several nurse-led models of care. In addition, CC is largely accessed through hospital or tertiary cancer centers, and there is limited understanding of access and practice in rural/regional settings. Lack of resources and systems to facilitate communication and connect care across sectors (eg, hospital to community care) is a recognized major barrier.¹⁶ Also, with the general lack of quality evidence for PBT CC, the applicability/tailoring of CC approaches to other priority populations remains unanswered, such as those with Indigenous, culturally and linguistically diverse backgrounds, adolescent and young adults, or elderly populations who may have additional psychosocial needs. Further work is needed to develop and implement a model of streamlined, optimal CC encompassing the PBT trajectory, sectors, and populations.

Importantly, current approaches to CC for PBT demonstrate a reliance on HCP availability for CC, usually nursing or allied health staff in hospitals or tertiary cancer centers. Consequently, CC is predominantly operationalized as the role of one designated HCP, not a shared multidisciplinary team. Availability of these HCPs impacts the implementation of CC, yet evidence is lacking to evaluate the impact, nature, and caseload of work and support available for HCPs delivering CC and sustainability of current practice. A range of advanced skills are needed; not only clinical and oncological knowledge and skills to accurately identify patient/carer issues and link them to appropriate care but also creativity, leadership, interpersonal, communication, and organization skills. These skills appear pivotal in achieving optimal coordination in current PBT care models. A HCP dedicated to CC builds knowledge and relationships with patients, their carers, and multidisciplinary team members, and coordinates different parts of PBT care. This is similar to the concept of relational coordination, where quality of relationships reinforces, and is strengthened by frequent, timely, accurate, problem-solving communication, and individuals and HCPs coordinate care through shared goals and knowledge, and mutual respect (role awareness).^60,61 In this CC approach, resources can facilitate CC, including staff hiring, training, shared accountability, and reward structures, further supported by structures enhancing communication, including established work protocols, systems for information exchange, and regular MDT meetings.⁶⁰ These have been similarly proposed as facilitators of CC implementation in our findings. Better understanding of existing training and resources for HCPs and identifying their support needs is warranted, given their pivotal role in existing models of CC for PBT.

We note several limitations to our review. First, CC components identified are based on the included reports relevant to CC for people with PBT only. Thus, some elements found in the broader CC literature in health may be missing in this review.⁶¹ Second, several reports described a newly appointed position of neuro-oncology nurse navigator/coordinator. It is difficult to examine the long-term impact and sustainability of the role in a real-world clinical setting and how roles evolve. Also, we were unable to examine the effectiveness of interventions/models of CC due to large heterogeneity in reported outcomes. We note one additional study⁶² on healthcare utilization and cost implications of brain cancer care coordinators was published post data synthesis and not included in our review. Evidence for interventions targeting CC in neuro-oncology is limited, with only one RCT examining a nurse-led carer support program.²⁶ We used nurse as a part of search terms which possibly biased search results. Much of the available evidence was obtained from research studies not directly targeting CC but describing elements of CC as components of their care model/framework. To overcome the paucity of evidence directly related to neuro-oncology CC and provide an informative summary of current knowledge, we extended our inclusion criteria to descriptive reports not specifically related to CC, if they discussed useful inferences to components and facilitators of CC. To our knowledge, this is the first systematic scoping review to assimilate existing empirical evidence and clinical guidelines to form an evidence base for developing a framework of optimal CC for people affected by PBT.

Conclusion

We synthesized a broad scope of literature relevant to CC for people with PBT, identifying key components of CC models; interventions and their effectiveness; and facilitators and barriers to implementation of optimal CC in neuro-oncology. Clinical guidelines and CC models emphasize healthcare system navigation and access to medical care. Knowledge about CC for PBT is largely based on descriptions of nurse-led models of care. Components of CC equated to duties and activities of a HCP dedicated to CC, mostly within tertiary care settings and aimed at providing a channel of communication and timely care responsive to patient needs. This approach heavily relies on HCP availability and their neuro-oncology specialized knowledge and competency in organization, relationship-based, and communication skills. Previous research used CC as a process underlying a model of care/support, and interventions targeting CC across the whole PBT trajectory are scarce. There is a significant gap in the literature depicting continuity of care across transitions and sectors for PBT care. Research is required to refine the framework of CC for people with PBT and identify training and support needs of HCPs who may play a pivotal role in current models of CC.

Supplementary material

Supplementary material is available online at Neuro-Oncology Practice (https://academic.oup.com/nop/).

Funding

This study forms part of Brain Cancer Rehabilitation, Assessment, Intervention of Survivor Needs (BRAINS), a program funded by the Australian Government Department of Health and Aged Care Medical Research Future Fund, 2019 Brain Cancer Survivorship Grant (ID: MRFBC000016). U.M.S.-D. was funded by an Early Career Fellowship from the Cancer Institute of New South Wales, Australia (Cancer Institute NSW [ID: 2020/ECF1163]).

Conflict of interest statement

None declared.

Authorship statement

Conception and protocol development: all authors. Literature search and data extraction: M.S.J., H.B., S.H., and T.C. Data synthesis and interpretation: M.S.J., H.B., S.H., T.C., J.M.S., and H.M.D. Initial draft preparation: M.S.J., H.B., S.H., and H.M.D. Draft review and editing: all authors. All authors have read and approved the final version of the manuscript.