A systematic mixed studies review of fear of cancer recurrence in families and caregivers of adults diagnosed with cancer

Abstract

Purpose

Fear of cancer recurrence (FCR) may be equally prevalent, persistent and burdensome in cancer caregivers as in survivors. This systematic review evaluated FCR prevalence, severity, correlates, course, impact and interventions in cancer caregivers.

Methods

Electronic databases were searched from 1997 to May 2021. Two reviewers identified eligible peer-reviewed qualitative or quantitative studies on FCR in adult caregivers or family members of adult cancer survivors. The risk of bias was assessed using the Cochrane Risk of Bias tools for randomised and non-randomised studies and the Mixed-Methods Appraisal Tool. A narrative synthesis and thematic synthesis occurred on quantitative and qualitative studies, respectively.

Results

Of 2418 papers identified, 70 reports (59 peer-reviewed articles, 11 postgraduate theses) from 63 studies were included. Approximately 50% of caregivers experienced FCR. Younger caregivers and those caring for survivors with worse FCR or overall health reported higher FCR. Most studies found caregivers’ FCR levels were equal to or greater than survivors’. Caregivers’ FCR was persistently elevated but peaked approaching survivor follow-up appointments. Caregivers’ FCR was associated with poorer quality of life in caregivers and survivors. Three studies found couple-based FCR interventions were acceptable, but had limited efficacy.

Conclusions

FCR in caregivers is prevalent, persistent and burdensome. Younger caregivers of survivors with worse overall health or FCR are at the greatest risk. Further research on identifying and treating caregivers’ FCR is required.

Implications for Cancer Survivors

Caregiver and survivor FCR are similarly impactful and appear interrelated. Addressing FCR may improve outcomes for both cancer caregivers and survivors.

Appendices

Appendix 1

Methodology of included studies

ID	Author (year)	Theoretical framework	Study design	Study setting	N caregivers	Type of cancer of care recipient	Sampling strategy	Data collection method
1	Alleyne & Gutt (2008) [21]	Neuman’s systems model	Qualitative	Peer support group	5	Prostate	Purposive	Semi-structured interviews
2	Balfe et al. (2016) [69]	NR	Cross-sectional	NR	197	Head and neck	NR	Questionnaire
3	Bamgboje-Ayodele et al. (2021) [39]	Yardley’s person-based approach	Mixed methods	Support organisations	89	Breast	Convenience	Survey Interview
4	Boehmer et al. (2016) [53]	NR	Cross-sectional	Community-based	167	Breast	Non-probability	Telephone survey
5	Braun et al. (2021) [62]	Actor-partner interdependence model	Cross-sectional	Cancer centre	52	Brain	NR	Survey
6	Butow et al. (2014) [70]	NR	Longitudinal	Treatment centres Cancer registries	99	Ovarian	NR	Questionnaire
7	Catania et al. (2019) [93]	Interpretive phenomenological approach	Qualitative	NR	8	Breast	NR	Interview
8	Cavers (2010) [89]	Grounded theory	Qualitative	Hospital	24	Glioma	Purposive	Semi-structured interviews
9	Chien et al. (2018) [76]	NR	Longitudinal	Medical centre	48	Prostate	Purposive	Questionnaire
10	Christie & Meyerowitz (2011) [54]	NR	Longitudinal	Hospital	153	Breast	Convenience	Questionnaire
11	Clavarino et al. (2002) [71]	NR	Mixed methods	Clinic Patient’s residence	19	Mixed	Purposive	Questionnaire and structured interview
12	Cohee et al. (2017) [30]	Social cognitive processing theory	Cross-sectional	University Cancer institute	222	Breast	Purposive	Questionnaire
13	Dempster et al. (2011) [31]	Self-regulatory model	Cross-sectional	Support group database	382	Oesophageal	Convenience	Questionnaire
14	Dockery (2016) [22]	Social constructionist	Qualitative	Skype	5	Breast	Purposive Convenience	Interview
15	Ellis (1998) [55]	Emotional approach coping Demand/withdraw interaction	Longitudinal	Medical facilities	30	Prostate	NR	Questionnaire
16	Gerhardt et al. (2020) [87]	NR	Qualitative	Home	10	Pancreative, duodenum, bile duct	Convenience	Interview
17	Girgis et al. (2013) [72]	Lazarus and Folkman’s stress and coping	Longitudinal	Participant homes	547	Mixed	NR	Survey
18	Graham et al. (2015) [32]	Leventhal’s common sense model	Longitudinal	Participant homes	171	Oesophageal	NR	Questionnaire
19	Haj Mohammad et al. (2015) [73]	NR	Cross-sectional	Medical centre	47	Oesophageal	NR	Questionnaire
20	Haun et al. (2014) [68]	NR	Cross-sectional	Medical centre	54	Lung	NR	Questionnaire
21	Heinrichs et al. (2012) [49]	Cognitive behavioural theory	Randomised controlled study	Hospital	72	Breast	NR	Questionnaire
22	Hodges & Humphris (2009) [6]	NR	Longitudinal	Multi-centre	101	Head and neck	NR	Survey
23	Hodgkinson et al. (2007) [35]	NR	Cross-sectional	Hospital	212	Mixed	NR	Questionnaire
24	Hodgkinson et al. (2007) [36]	NR	Cross-sectional	Hospital	154	Mixed	NR	Questionnaire
25	Hodgkinson et al. (2007) [105]	NR	Qualitative	Database	8	Mixed	Convenience	Semi-structured interviews
26	Hu et al. (2020) [52]	Family survivorship model	Cross-sectional	Cancer centre	127	Multiple myeloma	Convenience	Questionnaire
27	Ihrig et al. (2018) [28]	NR	Cross-sectional	Participant home	83	Prostate	NR	Survey
28	O'Callaghan et al. (2014) [94]	NR	Qualitative	Cancer centre	14	Prostate	Purposive	Semi-structured interviews
29	Janz et al. (2016) [81]	Modified stress and appraisal framework	Cross-sectional	Cancer registry	510	Breast	NR	Survey
30	Keesing et al. (2019) [95]	NR	Mixed methods	Community	8	Breast	Purposive	Interview
31	Kim et al. (2012) [80]	NR	Cross-sectional	Cancer registry	455	Mixed	NR	Survey
32	la Cour et al. (2016) [86]	Narrative theory Social practice theory	Qualitative	Medieval castle	10	Mixed	NR	Interview
33	Lethborg et al. (2003) [92]	Systems theory	Qualitative	Participant homes	8	Breast	Purposive	Interview
34	Lin et al. (2016) [42]	NR	Cross-sectional	Hospital	250	Head and neck	Convenience	Questionnaire
35	Lin et al. (2018) [43]	NR	Cross-sectional	Medical centre	300	Head and neck	Convenience	Questionnaire
36	Maguire (2017) [74]	Common sense model	Qualitative	Hospital	180	Head and neck	Purposive	Interview
37A	Matthews (2003) [63]	NR	Cross-sectional	Hospital cancer registries Online network	135	Mixed	Convenience	Questionnaire
37B	Matthews et al. (2003) [65]	NR	Cross-sectional	Hospital cancer registries Online network	135	Mixed	Convenience	Questionnaire
38	McCorry et al. (2009) [88]	Wainwright, Donovan Kacadas, Cramer and Blazeby (2007)	Qualitative	Oesophageal patients’ association	10	Oesophageal	Purposive	Focus group
39	McManus (2017) [44]	Actor-partner independence model	Longitudinal	Community cancer centre	71	Breast	NR	Daily diary Accelerometer
40A	Mellon et al. (2007) [4]	Family stress coping framework	Cross-sectional	Participant home Other selected by the family	123	Mixed	Stratified random	Questionnaire
40B	Mellon & Northouse (2001) [84]	Family survivorship model	Cross-sectional	Participant home	123	Mixed	Stratified random	Questionnaire
40C	Mellon et al. (2006) [56]	Family survivorship model	Cross-sectional	Participant home	123	Mixed	Stratified random	Questionnaire
40D	Mellon & Northouse (1999) [57]	Resiliency model	Mixed methods	Cancer institute	123	Mixed	Stratified random	Survey Interview
41	Muldbücker et al. (2021) [51]	NR	Cross-sectional	Participant home	188	Mixed	NR	Questionnaire
42	Nidhi & Basavareddy (2020) [66]	NR	Cross-sectional	Hospital	148	NR	Random	Questionnaire
43	Northouse et al. (1999) [82]	Stress and coping model	Cross-sectional	Oncology clinics	30	Colorectal	Convenience	Interview
44	Northouse et al. (2002) [85]	Family stress coping framework	Randomised controlled study	Participant home	73	Breast	Stratified random	Questionnaire
45	Perndorfer et al. (2019) [45]	The relationship intimacy model	Longitudinal	Participant home	69	Breast	NR	Daily diary
46	Persson et al. (2004) [106]	NR	Qualitative	Outpatient clinic	9	Colorectal	NR	Focus group
47	Ponto (2009) [58]	Resiliency model	Cross-sectional	Cancer organisation	32	Ovarian	Snowball	Survey
48	Ream et al. (2021) [107]	BR	Qualitative	Hospital, telephone, private homes, carers’ workplace	25	Mixed	Purposive	Interview
49	Rowley-Green & Meyerowitz (2003) [59]	NR	Longitudinal	Medical centre	171	Breast	NR	Questionnaire
50	Shands et al. (2006) [108]	NR	Qualitative	Home intervention	29	Breast	Consecutive	Tape recording of the intervention session
51A	Soriano et al. (2021) [34]	Social-cognitive processing model	Longitudinal	Participant home	79	Breast	NR	Survey
51B	Soriano et al. (2019) [47]	Cancer anxiety theories	Longitudinal	Participant homes	58	Breast	NR	Daily diary Survey
51C	Soriano et al. (2018) [33]	Social-cognitive processing model	Study 1: cross-sectional Study 2: longitudinal	Participant homes	Study 1: 46 Study 2: 72	Breast	NR	Study 1: survey Study 2: daily diary
51D	Soriano et al. (2018) [46]	NR	Longitudinal	Participant homes	57	Breast	NR	Survey
52	Szczesny (2015) [27]	Generalised mediation framework	Longitudinal	Cancer centre	44	Breast	NR	Diary Survey
53	Takeuchi et al. (2020) [23]	NR	Longitudinal	Participant homes	813	Mixed	Snowball	Questionnaires
54	Tan et al. (2020) [90]	NR	Qualitative	Online	78	Ovarian	NR	Open-ended survey
55	Turner et al. (2013) [37]	NR	Cross-sectional	Cancer registry	257	Mixed	NR	Survey
56	van de Wal et al. (2017) [40]	NR	Cross-sectional	Hospital database	168	Prostate	NR	Survey
57	Vivar (2007) [91]	Grounded theory	Qualitative	Hospital	14	Mixed	Purposive	Interview
58	Walker (1997) [60]	NR	Cross-sectional	Support group Treatment centre Hospital	58	Breast	NR	Survey
59	Wu et al. (2019) [78]	Social cognitive theory Common sense model	Longitudinal	Participant home	62	Prostate	NR	Questionnaire
60	Xu et al. (2019) [79]	Cognitive behavioural model of FCR Intimacy process model	Longitudinal	Participant home	54	Breast	NR	Questionnaire Daily diary
61	Yeo et al. (2004) [109]	NR	Cross-sectional	NR	23	Breast	NR	Questionnaire
62	Zhang et al. (2014) [77]	NR	Cross-sectional	Hospital	1468	Breast	NR	Questionnaire
63	Zimmermann et al. (2011) [50]	NR	Cross-sectional	Rehabilitation clinic	119	Breast	NR	Survey

1. NR not reported

Appendix 2. Risk of bias assessment

Appraisal of non-randomised controlled studies (RoBANS) (n = 49)

Appraisal	Low risk, N (%)	High risk/unclear, N (%)
Selection of participants	27 (55)	22 (45)
Confounding variables	36 (73)	13 (27)
Measurement of exposure	27 (55)	22 (45)
Incomplete outcome data	35 (71)	14 (29)
Selective outcome reporting	42 (86)	7 (14)

1. Soriano et al. [33] reported findings from two separate studies they conducted, hence the additional study

Appraisal of qualitative and mixed-methods studies (MMAT) (n = 20)

Appraisal	Yes, N (%)	No/unclear, N (%)
Qualitative (n = 20)
Are the sources of qualitative data relevant to address the research question/objective?	20 (100)	–
Is the process for analysing qualitative data relevant to address the research question/objective?	20 (100)	–
Is appropriate consideration given to how findings relate to the context?	13 (65)	7 (35)
Is appropriate consideration given to how findings relate to researchers’ influence?	6 (30)	13 (65)
Quantitative (non-randomised) (n = 1)
Are participants (organisations) recruited in a way that minimises selection bias?	1 (100)	–
Are measurements appropriate (clear origin, or validity known, or standard instrument, and absence of contamination between groups) regarding the exposure/intervention and outcomes?	1 (100)	–
In the groups being compared, are the participants comparable, or do researchers take into account (control for) the difference between these groups?	NA	–
Are there complete outcome data, and, when applicable, an acceptable response rate, or an acceptable follow-up rate for cohort studies?	–	1 (100)
Quantitative (descriptive) (n = 2)
Is the sampling strategy relevant to address the quantitative research question?	2 (100)	–
Is the sample representative of the population under study?	2 (100)	–
Are measurements appropriate (clear origin, or validity known, or standard instrument?)	2 (100)	–
Is there an acceptable response rate?	2 (100)	–
Mixed methods (n = 3)
Is the mixed-methods research design relevant to address the research questions?	3 (100)	–
Is the integration of qualitative and quantitative data relevant to address the research question?	3 (100)	–
Is appropriate consideration given to the limitations associated with this integration?	2 (67)	1 (33)

1. NA not applicable

Appraisal of randomised controlled studies (Cochrane Collaboration) (n = 2)

Appraisal	Low, N (%)	High/unclear, N (%)
Selection bias
Random sequence generation	1 (50)	1 (50)
Allocation concealment	1 (50)	1 (50)
Performance bias
Blinding of participants and personnel	–	2 (100)
Detection bias
Blinding of outcome assessment	1 (50)	1 (50)
Attrition bias
Incomplete outcome data	1 (50)	1 (50)
Reporting bias
Selective reporting	1 (50)	1 (50)