Volume 22, Issue 5 pp. 978-986

Review

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Factors reported to influence fear of recurrence in cancer patients: a systematic review

Jade V. Crist,

Jade V. Crist

Department of Psychology, King's College London, London, UK

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Elizabeth A. Grunfeld,

Corresponding Author

Elizabeth A. Grunfeld

School of Psychology, University of Birmingham, Birmingham, UK

Correspondence to: School of Psychology, University of Birmingham, Birmingham, UK B15 2TT. E-mail: [email protected]Search for more papers by this author

Jade V. Crist,

Jade V. Crist

Department of Psychology, King's College London, London, UK

Search for more papers by this author

Elizabeth A. Grunfeld,

Corresponding Author

Elizabeth A. Grunfeld

School of Psychology, University of Birmingham, Birmingham, UK

Correspondence to: School of Psychology, University of Birmingham, Birmingham, UK B15 2TT. E-mail: [email protected]Search for more papers by this author

First published: 03 June 2012

https://doi.org/10.1002/pon.3114

Citations: 324

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Abstract

Objective

Fear of cancer recurrence (FCR) is a significant psychological problem for cancer survivors. Some survivors experience FCR, which is both persistent and highly distressing. The aim of this systematic review was to identify the key factors associated with fear of recurrence among cancer patients.

Methods

A comprehensive literature search using keywords was performed with three databases, followed by an organic search to identify additional relevant articles. Included studies had a quantitative methodology presenting empirical findings focussed on adult cancer patients. A methodological quality assessment was performed for each study, and the strength of evidence was defined by the consistency of results.

Results

Forty-three studies met the inclusion criteria and are presented in this review. The most consistent predictor of elevated FCR was younger age. There was strong evidence for an association between physical symptoms and fear of cancer recurrence. Additional factors moderately associated with increased FCR included treatment type, low optimism, family stressors and fewer significant others. Inconsistent evidence was found for socio-demographic factors.

Conclusions

Fear of cancer recurrence is a complex issue influenced by a multitude of factors, including demographic, clinical and psychological factors. However, some studies have reported contradictory evidence, and FCR has been measured using a range of scales, which can hamper comparison across studies. Further research is needed to clarify inconsistencies in the current published research. Copyright © 2012 John Wiley & Sons, Ltd.

Introduction

Advances in the early detection and treatment of cancer have resulted in improved survival rates and an increasing cohort of cancer survivors 1. Most patients do well following treatment; however, some cancer survivors experience negative emotional outcomes 2. Anxiety and depression are more common among cancer patients than among the general population with prevalence rates of up to 65% reported 3. A significant emotional difficulty facing cancer survivors is fear regarding disease recurrence or spread 4. This is termed fear of cancer recurrence (FCR) 5 and is defined as the fear or worry that cancer will return, progress or metastasise 5, 6. FCR is prevalent with estimates of between 22% and 99% of cancer survivors experiencing FCR 5 and is considered one of the most distressing consequences of cancer 5. FCR can be long term and may predict poorer quality-of-life outcomes up to 6 years post-diagnosis 7.

A diagnosis of cancer, regardless of the patient's gender or age, brings psychological sequelae, including feelings of vulnerability, a sense of loss and concern for the future 7, 8. Therefore, FCR can be considered a normal and rational response to the threat of recurrence following cancer. However, in some cases, FCR may perpetuate dysfunctional behaviours including avoidance behaviour, hypervigilance for symptoms of recurrence 7 and an inability to plan for the future 9. In extreme cases, FCR has been associated with the development of anxiety disorders, post-traumatic stress symptoms and depression 5, 10-12. Therefore, identifying patients who are at greater risk of experiencing FCR may improve patient management and inform interventions to reduce FCR. This review aimed to identify factors associated with FCR in cancer survivors.

Method

Three methods were used to identify relevant studies: a keyword search, a backward search and a forwards (citation) search (Figure 1). Literature searches were performed using three electronic databases: Medline (1948–August 2011), PsychINFO (1806–August 2011) and EMBASE (1980–August 2011). The search terms were cancer, cancer patients, oncology, cancer survivors, fear of progression, fear of recurrence, fear* about recurrence, concern* about recurrence. Terms relating to cancer were then combined using OR, as were terms relating to FCR. A further search was performed using the AND function. Duplicates were excluded. A backwards organic search was then performed, which involved hand searching the reference lists of included articles. A forwards (citation) search was then conducted.

Details are in the caption following the image — **Figure 1**
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Overview of search strategy

Inclusion criteria were as follows: (i) adult cancer patients with any tumour type; (ii) any stage of disease; (iii) being written in English; (iv) quantitative methodology; (v) presentation of empirical findings (i.e. not a review); and (vi) report of data on factors associated with FCR. Studies were excluded if they were published as a conference abstract or a case study. For each study, the following information was obtained: author, year of publication and demographic information (sample size, age, ethnicity, cancer type, measure of FCR, main findings).

Methodological quality assessment

Each article underwent quality assessment from a checklist of 11 items adapted from an established quality assessment tool 13. This process was undertaken independently by two researchers, a comparison was made and only minor differences emerged, which were resolved through consensus. The broad nature of the quality assessment allowed a range of methodologies to be assessed. Studies were scored depending on how fully they met each criterion (Table 1): 2—fully meeting the criterion; 1—partially meeting criteria; 0—not meeting the criteria. If a criterion was not applicable, then it was excluded from the score calculation. A total sum score was calculated by summing the number of ‘yes’ responses then multiplying this by 2 and adding this to the number of ‘partials’. The total possible sum was calculated as 22 minus 2 times the number of ‘n/a’. Finally, a summary score was calculated (total sum/total possible sum), reflecting the overall methodological quality. Studies were categorised as high quality (score of 17 or above), moderate quality (11 to 16) or low quality (10 or less).

Table 1. Summary of studies

Study	Study design	Sample size, cancer type(s)	Time since diagnosis	Measures of FCR	Associated with greater FCR		Quality rating
Northouse et al. 18, USA	Cross-sectional	30, breast	Not stated	Fear of Recurrence Questionnaire	Fewer significant others	r = −0.39*	Mod
Northouse et al. 18, USA	Cross-sectional	30, breast	Not stated	Fear of Recurrence Questionnaire	Fewer others understanding concerns	r = −0.40*	Mod
de Haes and Welvaart 23, Netherlands	RCT	41, breast	11 months post-surgery	Fear of Recurrence Checklist 58	Younger age	r = −0.34*	Mod
Bartelink et al. 44, Netherlands	Cross-sectional	172, breast	Not stated	Single item	Mastectomy versus BCT	29% vs 13%*	Mod
de Haes et al. 41, Netherlands	RCT	34, breast	11 months post-surgery	Based on framework by Meyerowitz 58	NA	—	Mod
Lasry and Margolese 39, Canada	RCT	123, breast	3.5 years post-surgery	Fear of Recurrence Index	Multiple surgeries	8.2 vs 6.0**	Mod
Kemeny et al. 45, USA	Prospective	52, breast	18 months post-surgery	Psychosocial reactions to surgery 59	Mastectomy versus BCT	2.0 vs 1.3*	Mod
Lasry et al. 40, Canada	RCT	123, breast	Not stated	Fear of Recurrence Index 39	Chemotherapy	Full results missing*	Mod
Noguchi et al. 42, Japan	Cross-sectional	90, breast	Not stated	Single item	NA	—	Mod
Curran et al. 22, UK	RCT	278, breast	Not stated	Fear of Recurrence Scale 60	Younger age	Full results missing**	High
Burnstein et al. 57, USA	Longitudinal (9-month follow-up)	480, breast	Newly diagnosed	Fear of recurrence 38	Use of psychological therapies	8.17 vs 7.51**	High
Leake et al. 28, Australia	Cross-sectional	202, gynaecological	0–6 years	Functional Living Index 61	Younger age	Mean age 49 vs 54*	High
Stanton et al. 16, USA	Longitudinal (12-month follow-up)	70, breast	Not stated	Fear of Recurrence Questionnaire 18	Younger age	r = −0.36**	High
					Coping (avoidance oriented)	r = −0.33**
					POMS distress	r = 0.60**
					POMS vigour	r = −0.53**
de Haes et al. 43, UK, Netherlands, Greece, S. Africa	RCT	136, breast	Not stated	Single item	NA	—	High
Härtl et al. 25, Germany	Prospective	274, breast	4.2 years	Single item	BCT versus mastectomy	63.9 vs 55.3*	High
Härtl et al. 25, Germany	Prospective	274, breast	4.2 years	Single item	Younger age	<59 years*	High
Humphris et al. 17, UK	Prospective and cross-sectional	87, orofacial	<2 years post-treatment	Single item	Younger age	χ² = 9.31*	High
Humphris et al. 17, UK	Prospective and cross-sectional	100, orofacial	<2 years post-treatment	Single item	Anxiety	χ² = 7.57**	High
Mehta et al. 19, USA	Longitudinal (24-month follow-up)	519, prostate	Not stated	Fear of Recurrence Scale 62	Poorer quality of life	β = −0.23*	Mod
Poulakis et al. 38, Germany	Retrospective	357, renal cell carcinoma	Not stated	Fear of Recurrence Scale 62	Mandatory nephron-sparing surgery	19.19 (CI 17.85 to 20.54)*	High
Poulakis et al. 38, Germany	Retrospective	357, renal cell carcinoma	Not stated	Fear of Recurrence Scale 62	Larger tumour size	r² = 0.8530**	High
Vickberg 6, USA	Cross-sectional	169, breast	3 years	Concerns about Recurrence Scale	BCT versus mastectomy	Mean difference = 9**	High
Vickberg 6, USA	Cross-sectional	169, breast	3 years	Concerns about Recurrence Scale	Younger age	Mean difference = 9**	High
Rabin et al. 36, USA	Longitudinal (4-month follow-up)	69, breast	Not stated	Fear of Recurrence Scale 62	Stage 2 vs 1	F = 5.07**	High
Rabin et al. 36, USA	Longitudinal (4-month follow-up)	69, breast	Not stated	Fear of Recurrence Scale 62	Illness perceptions (timeline)	F = 9.69**	High
Gil et al. 31, USA	Longitudinal (10-month follow-up)	244, breast	6.8 years	Triggers of uncertainty	Hearing about another's cancer	Reported by 82%	High
					New symptoms	88%
					Media Information	63%
					Annual check-up	47%
Humphris and Rogers 55, UK	Longitudinal (12-month follow-up)	87, head/neck	Not stated	Worry of Cancer Scale 59	Smokers/relapsed versus quitters	F = 2.89*	High
Black and White 10, UK	Cross-sectional	36, haematological	Not stated	Fear of Recurrence Questionnaire 18	Low sense of coherence	F = 6.15*	Mod
Black and White 10, UK	Cross-sectional	36, haematological	Not stated	Fear of Recurrence Scale 62	Low sense of coherence	F = 6.15*	Mod
Wade et al. 47, Australia	Longitudinal (12-week follow-up)	44, breast	Not stated	Single item	Denial coping	r = 0.53**	High
					Younger age	r = −0.34*
					Breast cancer symptoms	r = 0.44**
Deimling et al. 32, USA	Cross-sectional	321, breast, colorectal, prostate	10.4 years	Cancer related	Race (African-American)	β = −0.22**	High
				Health worries	Optimism	β = −0.27**
				Scale 63	Symptoms	β = 0.20*
Constanzo et al. 14, USA	Longitudinal (5-month follow-up)	89, breast	Not stated	Concerns about Recurrence Scale 6	Younger age	F = 9.90**	High
					Lower education	F = 7.65**
					Mastectomy	F = 6.45*
Kornblith et al. 24, USA	Longitudinal (12-month follow-up)	252, breast, endometrial	Not stated	Fear of Recurrence Scale 62	Younger age	F = 26.58**	High
Kornblith et al. 24, USA	Longitudinal (12-month follow-up)	252, breast, endometrial	Not stated	Fear of Recurrence Scale 62	Breast cancer	F = 17.48*	High
Mellon et al. 30, USA	Secondary analysis	123, breast, colon, uterine, prostate	3.4 years	Fear of Recurrence Questionnaire	Concurrent family stressors	r = 0.31**	High
					Less positive meaning of illness	r = −0.43**
					Co-morbidities	r = 0.35**
					Somatic concerns	r = 0.19*
Steele et al. 34, UK	Cross-sectional	100, colorectal	Not stated	Single item	Young children	50% vs 22%*	High
Steele et al. 34, UK	Cross-sectional	100, colorectal	Not stated	Single item	Concern about results	Full results missing**	High
Bellizi et al. 21, USA	Longitudinal (12-month follow-up)	730, prostate	Not stated	Fear of Cancer Recurrence Scale 62	Poorer mental quality of life	t = 3.74**	High
Bellizi et al. 21, USA	Longitudinal (12-month follow-up)	730, prostate	Not stated	Fear of Cancer Recurrence Scale 62	Reduction in FCR post-treatment	Full results missing**	High
Hart et al. 9, USA	Longitudinal (18-month follow-up)	333, prostate	Not stated	Fear of Cancer Recurrence Scale 62	Less treatment satisfaction	r = −0.32**	High
					Poorer mental quality of life	r = −0.43**
					Poorer physical quality of life	r = −0.30**
Llewellyn et al. 7, UK	Prospective	82, head/neck	Newly diagnosed	Single item	Perceptions of severe consequences	r = 0.39**	High
					Stronger emotional representations	r = 0.38**
					Denial coping	r = 0.29*
					Positive reframing coping	r = 0.33*
					Use of religion coping	r = 0.29*
					Planning coping	r = 0.41**
					Lower optimism	r = −0.40**
					Greater anxiety	r = 0.50**
van den Beuken-van Everdingen et al. 12, Netherlands	Prospective	136, breast	Not stated	Concerns about Recurrence Scale 6	Pain	β = 0.28**	High
					Younger age	β = −0.2*1
					Poorer quality of life
					Physical functioning	r = −0.22**
					Social functioning	r = −0.39**
					Role limitations	r = −0.24**
					Mental health	r = −0.57**
					Vitality	r = −0.38**
					General health	r = −0.27**
Bergman et al. 33, USA	Prospective	476, prostate	Not stated	Memorial Anxiety Scale 64	Unpartnered patients	Parameter estimate 5.79*	High
Hodges and Humphris 20, UK	Prospective	101, head/neck	Newly diagnosed	Worry of Cancer Scale 59	Distress	β = 0.22**	High
Mehnert et al. 15, Germany	Cross-sectional	1083, breast	3.9 years	Fear of Progression Questionnaire 65	Married/divorced	η = 0.02**	High
					Unemployed	η = 0.03**
					Younger age	r = −0.17**
					Children	d = 0.14*
					Disease progression/ recurrence
					Chemotherapy	η = 0.01**
					Perceived impairments	η = 0.02**
					Depressive coping	η = 0.10**
					Active problem-oriented coping
					Intrusion coping	β = 1.80**
					Avoidance coping	β = 0.55**
					Hyperarousal coping	β = 0.62**
						β =0.69**
						β = 0.45**
Simard and Savard 56, Canada	Cross-sectional	227, breast	4.9 years	Concerns about Recurrence Scale 6	Women	r = 0.31**	High
		246, prostate	4.9 years	Fear of Recurrence Questionnaire 18	Younger age	r = −0.31**
		49, lung	3.8 years		Chemotherapy	r = 0.26**
		78, colorectal	4.2 years		Radiotherapy	r = 0.12**
					Surgery	r = 0.10**
					Cancer progression	r = 0.14**
Skaali et al. 29, Norway	Cross-sectional	1336, testicular	11.4 years	Single item	Younger age	OR 1.51**	High
					Neuroticism	OR 1.24**
					Intrusion	OR 1.18**
					Avoidance	OR 1.04**
McGinty et al. 27, USA	Cross-sectional	155, breast	6–24 months post-treatment	Modified Cancer Worry Scale 35	Younger age	β = −0.16*	High
					Stage of disease	β = 0.14*
					High threat appraisal	β = 0.61**
					Perceived vulnerability	β = 0.58**
Rogers et al. 35, UK	Cross-sectional	123, head and neck (cohort 1)	Not stated	Fear of Recurrence Questionnaire 18	Low mood about cancer	69%*	Mod
		68, head and neck (cohort 2)			Anxious about cancer	67%**
		68, head and neck (cohort 2)			Poorer quality of life	35%*
Rosmolen et al. 46, Netherlands	Cross-sectional	95, Barrett's neoplasia	Not stated	Worry of Cancer Scale 59	Oesophagus-preserving treatment	Mean difference = 10**	High
Shim et al. 37, South Korea	Case–control	112, breast, gastrointestinal, lung, other	14.5 months	Fear of Progression Questionnaire 4	Recurrence	F = 5.76**	High
Shim et al. 37, South Korea	Case–control	112, breast, gastrointestinal, lung, other	14.5 months	Fear of Progression Questionnaire 4	Dissatisfaction with treatment	r = −0.26**	High
Simard et al. 5, Canada	Cross-sectional	977, breast	3.3– 4.3 years	Fear of Cancer Recurrence Inventory 1	Intrusive thoughts	OR = 28.6*	High
		92, lung			No prostate cancer	Full results missing*
		727, prostate
		188, colorectal
Janz et al. 26, USA	Cross-sectional	1837, breast	Not stated	Worry of Cancer Scale 59	Ethnicity	β = 0.86**	High
					Younger age	β = −0.34**
					Employed	β = 0.12*
					Pain	β = 0.48**
					Fatigue	β = 0.39**
					Radiotherapy	β = 0.29**

NA, no association; BCT, breast-conserving treatment; POMS, Profile of Mood States; RCT, randomised controlled trial; FCR, fear of cancer recurrence; OR, odds ratio; CI, confidence interval.
* p < 0.05;
** p < 0.01.

Overall assessment

The information gathered was synthesised into four evidence levels: (i) strong evidence: consistent findings of an association in the same direction in at least three studies; (ii) moderate evidence: at least two studies reported a significant association in the same direction with one or none in the opposing direction; (iii) inconsistent evidence: inconsistent findings whereby no clear directionality in the findings was apparent ; (iv) weak evidence: only one study available with supporting evidence or studies consistently identified no association.

Results

The search strategy resulted in 420 bibliographic records, reduced to 257 articles following the exclusion of duplicates and to 36 following application of the inclusion criteria. Backwards organic searching identified a further seven articles. The forwards (citation) search did not identify further relevant articles. Forty-three studies were included in the review. The majority of studies were classified as high quality (Table 1), 11 as moderate quality and none as poor quality. Twenty-two studies focussed on breast cancer, five on prostate and testicular cancers, five on head and neck cancer, one on gynaecological cancers, one on haematological cancer, one on colorectal cancer, one on renal cell carcinoma and one on early Barrett's neoplasia. In addition, six studies covered mixed cancer types.

Eleven studies utilised a longitudinal design with follow-up periods ranging from 12 weeks to 18 months and between two and four data collection points. Retention rates between initial and final data collection ranged from 73% to 90%. Eight studies reported that FCR changed minimally over the periods examined 9, 14, 16, 24, 55, 31, 57. However, three studies reported that FCR decreased between the first two time points measured 21, 36, 47.

Demographic factors

Younger age was consistently associated (in 14 studies) with greater FCR. Older patients reported less fear in breast 6, 12, 14-16, 22-27, 47, endometrial 24, orofacial 17, gynaecological 28, testicular 29 and mixed cancer types 56. In contrast, two studies did not find a significant association between age and FCR 7, 18. However, age remains an important predictor of recurrence worry in multivariate models 14.

Contradictory findings were reported for gender, ethnicity and educational status. Llewellyn and colleagues 7 did not identify any noteworthy relationship between gender and FCR. Simard and Savard 56 found that women reported greater FCR than men although this finding did not hold once cancer type was controlled for. In addition, only one study reported that medium educational level was associated with greater FCR 14.

No clear association between ethnicity and FCR emerged 7. Two studies reported that African-American survivors were less fearful than Caucasian survivors 26, 32. Moreover, Janz and colleagues 26 also identified higher levels of worry about recurrence among Latina women.

There was a mixed pattern of findings for marital status. Six studies reported that following multivariate analysis marital status was unrelated to FCR 5, 7, 12, 18, 26, 28. In comparison, Bergman and colleagues 33 found that men with partners reported less fear of recurrence, and a further study reported that being either married or divorced was associated with greater FCR 15.

Concurrent family stressors were predictive of elevated FCR 30. Family resources, including family hardiness and social support, were unrelated to FCR although women who had fewer significant others with whom they could discuss concerns reported greater FCR 18. Mehnert and colleagues 15 found that having children was significantly associated with FCR. In addition, having younger children (under 21) was associated with greater FCR 34.

Cancer and treatment-related factors

None of the studies included in the review found an association between time since diagnosis and severity of self-reported FCR 6, 15, 30, 56. There were some differences in reports of FCR across cancer types. Prostate cancer patients reported lower FCR than patients with breast, colorectal and lung cancer 5. However, greater FCR was observed among breast cancer survivors than among endometrial cancer survivors 24.

Five studies reported that cancer stage was not associated with FCR 6, 12, 18, 19, 26. In contrast, two studies 27, 36 reported that breast cancer patients with stage I diagnosis reported less FCR than patients with stage II. Moreover, patients with cancer recurrence or progression reported greater FCR in comparison with controls 37.

Mixed evidence emerged for an association between treatment type and FCR. Skaali and colleagues 29 reported that treatment type for prostate and testicular cancer was not a significant predictor. However, five studies reported that chemotherapy was related to greater FCR among breast cancer survivors 14, 15, 38, 39, although this was not upheld in multivariate analyses. In a further multivariate analysis with a breast cancer sample, radiation therapy was predictive of greater worry 26. Four studies found no relationship between treatment type and FCR 18, 28, 30, 35 among a range of cancer types. However, the relationship between treatment type and FCR was reported to be influenced by treatment satisfaction 9 and symptom control 26.

Mixed evidence emerged for an association between type of surgery and FCR. Eight studies reported no difference between mastectomy and breast-conserving therapy 6, 22, 23, 40-43. However, two studies 6, 25 reported that patients undergoing breast-conserving therapy reported greater FCR than mastectomy patients. Conversely, three studies reported greater FCR among mastectomy patients compared with those receiving breast-conserving therapy 14, 44, 45. The discrepancy may partly be explained by the differing methodologies used and by the single treatment centre focus of most studies, whereby there may have been different surgical approaches or information provision.

Patients who underwent compulsory nephron-sparing surgery for renal cell carcinoma were significantly more fearful of cancer recurrence than those who underwent radical nephrectomy or elective nephron-sparing surgery 38. In addition, one study reported that preserving the oesophagus using endoscopic therapy in early Barrett's neoplasia resulted in greater reported FCR 46.

Psychological factors and coping responses

Mixed evidence emerged for the association between psychological factors and FCR. One study identified the association between personality, in particular neuroticism, and FCR 29. Furthermore, an association was found between low mood or psychological distress (including anxiety and depression) and FCR 7, 16, 17, 20, 35, although the directionality of such a relationship was not apparent. Finally, two studies also identified an association between intrusive thoughts and FCR 5, 29.

Two studies 7, 32 reported that lower optimism was associated with greater FCR, and optimism was the strongest predictor of FCR following treatment (excluding baseline FCR) 7. The same study identified that illness perceptions, including perceptions of more severe consequences and stronger emotional representations, were associated with FCR. In addition, conceptualising cancer as a chronic illness was associated with greater FCR 36. Furthermore, greater perceived physical impairments 15 and appraising cancer as having less positive meaning 30 was associated with greater FCR. McGinty and colleagues 27 reported a correlation between risk perceptions of breast cancer (vulnerability and severity) and greater FCR.

Low self-esteem, denial coping and avoidance-orientated coping were predictors of future FCR 16, 29, 47. In addition, both depressive coping and active problem-oriented coping were associated with greater FCR 15.

Quality-of-life domains were associated with FCR in five of the studies. In four studies, there was an observed association between poorer physical and mental-health-related quality of life and FCR 9, 12, 19, 35. In one study, there was an association between mental-health-related quality of life only and FCR 21.

Factors triggering FCR

One study reported that hearing of another's diagnosis, exposure to media information or an annual check-up influenced reports of FCR 31. In addition, experiencing new or ongoing side effects or symptoms (especially pain) was associated with reports of greater FCR 12, 26, 29, 30, 32. Furthermore, Humphris and Rogers 47 identified a weak relationship between FCR and smoking behaviour.

Discussion

This review aimed to identify factors associated with FCR in cancer patients. Strong evidence emerged for a relationship between FCR and younger age, coping responses, poorer quality of life and cues (new symptoms, pain and follow-up appointments). Moderate evidence was found for beliefs (e.g. perceptions of vulnerability) and demographic factors (ethnicity, having younger children). Finally, inconclusive or weak evidence was found for cancer-related factors (cancer type, stage, treatment type), socio-demographic factors (gender, education, employment) and social resources (family resources/stressors, significant others). Findings from the majority of studies suggest that FCR remains fairly stable over time. However, most studies reporting on changes in FCR examined the concept post-treatment and over relatively short follow-up periods. Further longitudinal evidence would improve the assessment of the stability of the FCR profile over the survivorship trajectory. This review found evidence of an association between baseline FCR and later FCR, which would suggest that if FCR is initially high, it is likely to remain elevated. Actual cancer recurrence or progression was also associated with FCR 37; however, causality cannot be inferred from these studies given the cross-sectional designs utilised.

The factor most consistently associated with FCR was younger age. Younger survivors may perceive their cancer as more unexpected 6 and report higher levels of anxiety and depression in general 48, 49. Moreover, two studies reported that survivors with young children experienced greater FCR 15, 34. Parents may be concerned about a child's emotional and behavioural adaptation to a parental diagnosis of cancer 50, and both parent and child may have significant fears about how the child would cope without the parent 51. Survivors of cancer who have children may benefit from a family-orientated psychological intervention that accounts for the emotional concerns of both the survivor and their children 52.

The review found strong evidence for an association between physical symptoms and elevated FCR 30, as survivors may attribute unrelated symptoms to cancer recurrence. Experimental evidence suggests that somatic cues, such as the occurrence of symptoms, trigger beliefs about vulnerability and thereby elicit cancer worry 53. Research thus far suggests that socio-demographic and disease-related factors do not contribute significantly to FCR 7. Inconsistencies emerged regarding the role of education in FCR. Highly educated patients may have a greater understanding of the implications of a diagnosis of cancer, whereas a low level of education may impact on the information that is provided 26. Finally, ethnicity may be important, with a growing body of research suggesting that African-American women report lower levels of FCR than Caucasian women 27.

Inconsistencies existed with regard to type of breast cancer surgery. The scarring that follows mastectomy may remind patients of their cancer 22, 39, and evidence suggests that breast cancer survivors would benefit from improved information provision and management of expectations with regard to breast reconstruction 66, 67. Conversely, patients undergoing a lumpectomy may experience greater FCR than mastectomy patients as they fear the cancer has not been fully removed 54. Conservative treatments such as endoscopic therapy for oesophageal cancer 55 and nephron-sparing surgery for renal carcinoma 38 are associated with FCR, which may relate to beliefs about whether the cancer has been fully removed.

A range of psychological factors were found to be associated with FCR. There was some evidence for an association between FCR and other forms of psychological distress (i.e. depression) although the designs of the studies did not allow for consideration of the directionality of such relationships. In addition, there was evidence that FCR is associated with poorer mental-health-related quality of life. Further studies examining the development of FCR and its relationship to other aspects of psychological distress (i.e. depression) would contribute to the understanding of the trajectory of FCR and inform the development of interventions targeting FCR and other components of psychological distress. Such interventions to date have focussed on reducing fear of recurrence, targeting illness perceptions and inappropriate checking behaviour using a form of cognitive behavioural therapy 68 or reducing psychological distress in general among survivors using a group intervention 69.

Family factors (including family stressors and social support) 30 and gender appeared unrelated to FCR although this may reflect that few studies have examined these factors to date. The majority of studies were conducted with female cancer patients (gynaecological and breast cancers); therefore, the role of gender requires further exploration employing larger samples of mixed-gender cancer types.

The primary studies presented in this review had a range of limitations that need to be considered. The majority of the studies recruited homogenous samples in that participants were mostly White, well-educated and married. In addition, a number of the studies acknowledged the small samples sizes recruited and in some cases the low initial response rates for recruitment into the studies. Although reported response rates varied, the majority of studies reported little about non-responders. Given that more distressed individuals would be less likely to respond, then the prevalence of FCR may be underestimated in these studies. Additionally, FCR was assessed using a variety of measures, making it difficult to compare across studies. Some measures relied on a single item, which could be considered less reliable and more likely to increase the error variance in the sample. Furthermore, the measures used were not appropriate to determine if the observed levels of FCR were of clinical significance. The acquisition of such information would be useful to inform the development of interventions aimed at reducing FCR.

The designs of the studies reported in this review varied. Cross-sectional studies do not allow for changes in FCR over time to be observed and may be prone to recall bias on some of the measures used. Eleven studies utilised longitudinal designs, and although the attrition rates across time points were generally low, these designs incorporated relatively short follow-up periods. This would limit the assessment of the stability of the FCR profile over the survivorship trajectory. Furthermore, the designs utilised did not allow for the assessment of pre-treatment levels of distress or the identification of factors associated with the development of FCR. Such information would help the targeting and timing of interventions to reduce FCR among cancer survivors.

The review demonstrates that FCR is a common response to a cancer diagnosis and the associated treatments. The current literature in this field does not allow one to determine the factors contributing to the development of FCR or to determine the stability of FCR over the survivorship trajectory. Further research is necessary to identify the key predictors of FCR among cancer survivors to identify at-risk groups and key factors to be targeted in an intervention. This review highlights the importance of managing the physical and emotional consequences of cancer; however, further research is necessary to target interventions and to determine the timing of such interventions to reduce FCR among cancer survivors and support patients at risk of FCR 31. This review provides a first step towards meeting this aim.

References

1 Rowland J, Aziz N, Tesauro G, Feuer E. The changing face of cancer survivorship. Semin Oncol Nurs 2001; 17: 236–240.
10.1053/sonu.2001.27912
CAS PubMed Google Scholar
2 Aziz NM. Late effects of cancer treatments. In Cancer Survivorship: Today and Tomorrow, PA Ganz (ed.). Springer: New York, 2007.
Google Scholar
3 Jadoon NA, Munir W, Shahzad MA, Choudhry ZS. Assessment of depression and anxiety in adult cancer outpatients: a cross-sectional study. BMC Cancer 2010; 10: 594.
10.1186/1471-2407-10-594
PubMed Web of Science® Google Scholar
4 Herschbach P, Book K, Dinkel A, et al. Evaluation of two group therapies to reduce fear of progression in cancer patients. Support Care Cancer 2010; 18: 471–479.
10.1007/s00520-009-0696-1
PubMed Web of Science® Google Scholar
5 Simard S, Savard S, Ivers H. Fear of cancer recurrence: specific profiles and nature of intrusive thoughts. J Cancer Surviv 2010; 4: 361–371.
10.1007/s11764-010-0136-8
PubMed Web of Science® Google Scholar
6 Vickberg SMJ. The Concerns About Recurrence Scales (CARS): a systematic measure of women's fears about the possibility of breast cancer recurrence. Ann Behav Med 2003; 25: 16–24.
10.1207/S15324796ABM2501_03
PubMed Web of Science® Google Scholar
7 Llewellyn CD, Weinman J, McGurk M, Humphris G. Can we predict which head and neck cancer survivors develop fears of recurrence? J Psychosom Res 2008; 65: 525–532.
10.1016/j.jpsychores.2008.03.014
PubMed Web of Science® Google Scholar
8 Heyman EN, Rosner TT. Prostate cancer: an intimate view from patients and wives. Urol Nurs 1996; 16: 37–44.
CAS PubMed Google Scholar
9 Hart SL, Latini DM, Cowan JE, et al. Fear of recurrence, treatment satisfaction and quality of life after radical prostatectomy for prostate cancer. Support Care Cancer 2008; 16: 161–169.
10.1007/s00520-007-0296-x
PubMed Web of Science® Google Scholar
10 Black EK, White CA. Fear of recurrence, sense of coherence and posttraumatic stress disorder in haematological cancer survivors. Psycho-Oncology 2005; 14: 510–515.
10.1002/pon.894
PubMed Web of Science® Google Scholar
11 Montel S. Fear of recurrence: a case report of a woman breast cancer survivor with GAD treated successfully by CBT. Clin Psychol Psychother 2010; 17: 346–353.
10.1002/cpp.682
PubMed Web of Science® Google Scholar
12 Van den Beuken-van Everdingen MHJ, Peters ML, de Rijke JM, Schouten HC, van Kleef M, Patign J. Concerns of former breast cancer patients about disease recurrence: a validation and prevalence study. Psycho-Oncology 2008; 17: 1137–1145.
10.1002/pon.1340
PubMed Web of Science® Google Scholar
13 Kmet LM, Lee RC, Cook LS. Standard quality assessment criteria for evaluating primary research papers from a variety of fields. AHFMR, HTA Initiative 2004; 13: 1–21.
Google Scholar
14 Constanzo ES, Lutgendorf SK, Mattes ML, et al. Adjusting to life after treatment: distress and quality of life following treatment for breast cancer. Br J Cancer 2007; 97: 1625–1631.
10.1038/sj.bjc.6604091
PubMed Web of Science® Google Scholar
15 Mehnert A, Berg P, Henrich G, Herschbach P. Fear of cancer progression and cancer related intrusive cognitions in breast cancer patients. Psycho-Oncology 2009; 18: 1273–1280.
10.1002/pon.1481
CAS PubMed Web of Science® Google Scholar
16 Stanton AL, Danoff-Burg S, Huggins ME. The first year after breast cancer diagnosis: hope and coping strategies as predictors of adjustment. Psycho-Oncology 2002; 11: 93–102.
10.1002/pon.574
PubMed Web of Science® Google Scholar
17 Humphris GM, Rogers S, McNally C, Lee-Jones J, Brown D. Fear of recurrence and possible cause of anxiety and depression in orofacial cancer patients. Int J Oral Maxillofac Surg 2003; 32: 486–491.
10.1016/S0901-5027(03)90399-1
CAS PubMed Web of Science® Google Scholar
18 Northouse LL. Mastectomy patients and the fear of cancer recurrence. Cancer Nurs, 1981; 4: 213–220.
10.1097/00002820-198106000-00004
PubMed Google Scholar
19 Mehta SS, Lubeck DP, Pasta DJ, Litwin MS. Fear of cancer recurrence in patients undergoing definitive treatment for prostate cancer: results from CaPSURE. J Urol 2003; 170: 1931–1933.
10.1097/01.ju.0000091993.73842.9b
PubMed Web of Science® Google Scholar
20 Hodges L, Humphris GM. Fear of recurrence and psychological distress in head and neck cancer patients and their carers. Psycho-Oncology 2009; 18: 841–848.
10.1002/pon.1346
PubMed Web of Science® Google Scholar
21 Bellizi KM, Latini DM, Cowan JE, DuChane J, Carroll PR. Fear of recurrence, symptom burden and health related quality of life in men with prostate cancer. Urology 2009; 72: 1269–1273.
10.1016/j.urology.2007.12.084
Web of Science® Google Scholar
22 Curran D, van Dongen JP, Aaronson NK, et al. Quality of life of early stage breast cancer patients treated with radical mastectomy or breast conserving procedures: results of EORTC trial 10801. Eur J Cancer 1998; 24: 307–314.
10.1016/S0959-8049(97)00312-2
Web of Science® Google Scholar
23 De Haes JCJM, Welvaart K. Quality of life after breast cancer surgery. J Surg Oncol 1985; 28: 123–125.
10.1002/jso.2930280211
CAS PubMed Web of Science® Google Scholar
24 Kornblith AB, Powell M, Regen MM, et al. Long-term psychosocial adjustment of older vs younger survivors of breast and endometrial cancer. Psycho-Oncology 2007; 16: 895–903.
10.1002/pon.1146
PubMed Web of Science® Google Scholar
25 Härtl K, Janni W, Kästner R, et al. Impact of medical and demographic factors on long term quality of life and body image of breast cancer patients. Ann Oncol 2003; 14: 1064–1071.
10.1093/annonc/mdg289
CAS PubMed Web of Science® Google Scholar
26 Janz N, Hawley S, Mujahid MS, et al. Correlates of worry about recurrence in a multiethnic population based sample of women with breast cancer. American Cancer Society 2011; 117: 1827–1836.
10.1002/cncr.25740
PubMed Web of Science® Google Scholar
27 McGinty HL, Goldenberg JL, Jacobsen PB. Relationship of threat appraisal with coping appraisal to fear of cancer recurrence in breast cancer survivors. Psycho-Oncology 2012; 21: 203–210.
10.1002/pon.1883
PubMed Web of Science® Google Scholar
28 Leake RL, Gurrin LC, Hammond IG. Quality of life in patients attending a low risk gynaecological oncology follow-up clinic. Psycho-Oncology 2001; 10: 428–435.
10.1002/pon.539
CAS PubMed Web of Science® Google Scholar
29 Skaali T, Fossa SD, Bremnes R, et al. Fear of recurrence in long term testicular cancer survivors. Psycho-Oncology 2009; 18: 580–588.
10.1002/pon.1437
PubMed Web of Science® Google Scholar
30 Mellon S, Kershaw TS, Northouse LL, Freeman-Gibb L. A family-based model to predict fear of recurrence for cancer survivors and their caregivers. Psycho-Oncology 2007; 16: 214–223.
10.1002/pon.1074
PubMed Web of Science® Google Scholar
31 Gill KM, Mishel MH, Belyea M, et al. Triggers of uncertainty about recurrence and long-term treatment effects in older African American and Caucasian breast cancer survivors. Oncol Nurs Forum 2004; 31: 633–639.
PubMed Web of Science® Google Scholar
32 Deimling GT, Bowman K, Sterns S, Wagner LJ, Kahana B. Cancer related health worries and psychological distress among older adult long term cancer survivors. Psycho-Oncology 2006; 15: 306–320.
10.1002/pon.955
PubMed Web of Science® Google Scholar
33 Bergman J, Gore JL, Seigal CS, Kwan L, Litwin MS. Partnership and outcomes in men with prostate cancer. Cancer 2009; 115: 4688–4694.
10.1002/cncr.24544
CAS PubMed Web of Science® Google Scholar
34 Steele N, Haigh R, Knowles G, Mackean M. Carcinoembryonic antigen testing in colorectal cancer follow up: what do patients think? Postgrad Med 2007; 83: 612–614.
10.1136/pgmj.2007.059634
PubMed Web of Science® Google Scholar
35 Rogers SN, Scott B, Lowe D, Ozakinci G, Humphris GM. Fear of recurrence following head and neck cancer in the outpatient clinic. Eur Arch Otorhinolaryngol 2010; 267: 1943–1949.
10.1007/s00405-010-1307-y
CAS PubMed Web of Science® Google Scholar
36 Rabin C, Leventhal H, Goodin S. Conceptualisation of disease timeline predicts posttreatment distress in breast cancer patients. Health Psychol 2004; 23: 407–412.
10.1037/0278-6133.23.4.407
PubMed Web of Science® Google Scholar
37 Shim EJ, Shin Y, Oh DY, Hahm B. Increased fear of progression in cancer patients with recurrence. Gen Hosp Psychiatry 2010; 32: 169–175.
10.1016/j.genhosppsych.2009.11.017
PubMed Web of Science® Google Scholar
38 Poulakis V, Witzch U, de Vries R, Moeckel M, Becht E. Quality of life after surgery for localised renal cell carcinoma: comparison between radical nephrectomy and nephron sparing surgery. Urology 2003; 62: 814–820.
10.1016/S0090-4295(03)00687-3
PubMed Web of Science® Google Scholar
39 Lasry JCM, Margolese RG. Fear of recurrence, breast-conserving surgery, and the trade off hypothesis. Cancer 1992; 69: 2111–2115.
10.1002/1097-0142(19920415)69:8<2111::AID-CNCR2820690817>3.0.CO;2-T
CAS PubMed Web of Science® Google Scholar
40 Lasry JCM, Margolese RG, Poisson R, et al. Depression and body image following mastectomy and lumpectomy. J Chron Dis 1987; 40: 529–534.
10.1016/0021-9681(87)90010-5
PubMed Web of Science® Google Scholar
41 De Haes JCJM, van Oostrum MA, Welvaart K. The effect of radical and conserving surgery on the quality of life of early breast cancer patients. Eur J Surgical Oncology 1986; 12: 337–342.
CAS PubMed Web of Science® Google Scholar
42 Noguchi M, Kitagawa H, Kinoshita K, et al. Psychologic and cosmetic self-assessments of breast conserving therapy compared with mastectomy and immediate breast reconstruction. J Surg Oncol 1993; 54: 260–266.
10.1002/jso.2930540416
PubMed Web of Science® Google Scholar
43 De Haes JCJM, Curran D, Aaronson NK, Fentiman IS. Quality of life in breast cancer patients aged over 70 years, participating in the EORTC 10850 randomised clinical trial. Eur J Cancer 2003; 39: 945–951.
10.1016/S0959-8049(03)00149-7
CAS PubMed Web of Science® Google Scholar
44 Bartelink H, van Dam F, van Dongen J. Psychological effects of breast conserving therapy in comparison with radical mastectomy. Int J Radiation Oncology Biol Phys 1985; 11: 381–385.
10.1016/0360-3016(85)90161-0
PubMed Web of Science® Google Scholar
45 Kemeny MM, Wellisch DK, Schain WS. Psychosocial outcome in a randomised surgical trial for treatment of primary breast cancer. Cancer 1998; 62: 1231–1237.
10.1002/1097-0142(19880915)62:6<1231::AID-CNCR2820620631>3.0.CO;2-8
Web of Science® Google Scholar
46 Rosmolen WD, Boer KR, de Leeuw RJR, et al. Quality of life and fear of cancer recurrence after endoscopic and surgical treatment for early neoplasia in Barrett's esophagus. Endoscopy 2010; 42: 525–531.
10.1055/s-0029-1244222
CAS PubMed Web of Science® Google Scholar
47 Wade TD, Nehmy T, Koczwara B. Predicting worries about health after breast cancer surgery. Psychooncology 2005; 14: 503–509.
10.1002/pon.866
PubMed Web of Science® Google Scholar
48 Hipkins J, Whitworth M, Tarrier N, Jayson G. Social support, anxiety and depression after chemotherapy for ovarian cancer: a prospective study. Br J Health Psychol 2004; 9: 569–581.
10.1348/1359107042304542
PubMed Web of Science® Google Scholar
49 Arden-Close E, Gidron Y, Moss-Morris R. Psychological distress and its correlates in ovarian cancer: a systematic review. Psycho-Oncology 2008; 17: 1061–1072.
10.1002/pon.1363
CAS PubMed Web of Science® Google Scholar
50 Visser A, Huizinga GA, Hoekstra HJ, et al. Emotional and behavioral problems in children of parents recently diagnosed with cancer: a longitudinal study. Acta Oncol 2007; 46: 67–76.
10.1080/02841860600949560
PubMed Web of Science® Google Scholar
51 Osborn T. The psychosocial impact of parental cancer on children and adolescents: a systematic review. Psycho-Oncology 2007; 16: 101–126.
10.1002/pon.1113
CAS PubMed Web of Science® Google Scholar
52 Thastum M, Watson M, Kienbacher C, et al. Prevalence and predictors of emotional and behavioural functioning of children where a parent has cancer: a multinational study. Cancer 2009; 115: 4030–4039.
10.1002/cncr.24449
CAS PubMed Web of Science® Google Scholar
53 Easterling D, Leventhal H. Contribution of concrete cognition to emotion: neutral symptoms as elicitors of worry about cancer. J Appl Psychol 1989; 74: 787–796.
10.1037/0021-9010.74.5.787
CAS PubMed Web of Science® Google Scholar
54 Fallowfield LJ, Baum M, Maguire GP. Effects of breast conservation on psychological morbidity associated with diagnosis and treatment of early breast cancer. Br Med J 1986; 293: 1331–1334.
10.1136/bmj.293.6558.1331
PubMed Web of Science® Google Scholar
55 Humprhis GM, Roger SN. The association of cigarette smoking and anxiety, depression and fears of recurrence in patients following treatment of oral and oropharyngeal malignancy. Eur J Cancer Care 2004; 13: 328–335.
10.1111/j.1365-2354.2004.00479.x
Web of Science® Google Scholar
56 Simard S, Savard J. Fear of cancer recurrence inventory: development and initial validation of a multidimensional measure of fear of cancer recurrence. Support Care Cancer 2009; 17: 241–251.
10.1007/s00520-008-0444-y
PubMed Web of Science® Google Scholar
57 Burnstein HJ, Glebbr S, Guadagoli E, Weeks J. Use of alternative medicine by women with early-stage breast cancer. N Engl J Med 1999; 340: 1733–1739.
10.1056/NEJM199906033402206
PubMed Web of Science® Google Scholar
58 Meyerowitz BE. Psychological correlations of breast cancer and its treatments. Psychol Bull 1980; 87: 108–131.
CAS PubMed Web of Science® Google Scholar
59 Wellisch DK, Schain WS, Noone BR, Little JW. Psychosocial correlates of immediate versus delayed reconstruction of the breast. Plast Reconstr Surg 1985; 76: 713–718.
10.1097/00006534-198511000-00010
CAS PubMed Web of Science® Google Scholar
60 Avery AD, Lelak T, Solomon NE, et al. Quality of Medical Care Assessment Using Outcome Measures. Eight Disease Specific Applications. Rand: Santa Monica, 1986.
Google Scholar
61 Schipper H, Clinch J, McMurray A, Levitt M. Measuring the quality of life of cancer patients: the Functional Living Index—cancer. J Clin Oncol 1984; 2: 472–483.
10.1200/JCO.1984.2.5.472
CAS PubMed Web of Science® Google Scholar
62 Greenberg DB, Kornblith AB, Herndon JE, et al. Quality of life of adult leukemia survivors treated on clinical trials of the Cancer and Leukemia Group. Cancer 1997; 80: 1936–1944.
10.1002/(SICI)1097-0142(19971115)80:10<1936::AID-CNCR10>3.0.CO;2-Z
CAS PubMed Web of Science® Google Scholar
63 Bowman KF, Smerglia VL, Deimling GT. A stress model of cancer survivorship in older long-term survivors. J Ment Health Aging 2004; 10: 163–182.
Google Scholar
64 Roth AJ, Rosenfeld B, Kornblith AB, et al. The Memorial Anxiety Scale for prostate cancer. Cancer 2003; 97: 2910–2918.
10.1002/cncr.11386
PubMed Web of Science® Google Scholar
65 Mehnert A, Herschbach P, Petra B, et al. Fear of progression in breast cancer patients—validation of the short form of the Fear of Progression Questionnaire. Zeitschrift für Psychoso Med Psycho 2006; 52: 274–288.
10.13109/zptm.2006.52.3.274
PubMed Web of Science® Google Scholar
66 Abu-Nab Z, Grunfeld EA. Satisfaction with outcome and attitudes towards scarring among women undergoing breast reconstructive surgery. Patient Educ Couns 2007; 66(2): 243–249.
10.1016/j.pec.2006.12.008
CAS PubMed Web of Science® Google Scholar
67 Begum S, Grunfeld EA, Ho-Asjoe M, Farhadi J. An exploration of patient decision-making for autologous breast reconstructive surgery following a mastectomy. Patient Educ Couns 2011; 84(1): 105–110.
10.1016/j.pec.2010.07.004
PubMed Web of Science® Google Scholar
68 Humphris G, Ozakinci G. The AFTER intervention: a structured psychological approach to reduce fears of recurrence in patients with head and neck cancer. Br J Health Psychol 2008; 13: 223–230.
10.1348/135910708X283751
PubMed Web of Science® Google Scholar
69 Fukui S, Kugaya A, Okamura H, et al. A psychosocial group intervention for Japanese women with primary breast carcinoma. Cancer 2000; 89: 1026–1036.
10.1002/1097-0142(20000901)89:5<1026::AID-CNCR12>3.0.CO;2-5
CAS PubMed Web of Science® Google Scholar

Citing Literature

Volume22, Issue5

May 2013

Pages 978-986

Factors reported to influence fear of recurrence in cancer patients: a systematic review