2013 Depresion y Ansiedad en Sobrevivientes de Cancer de Largo Termino Comparando Con Controles de...

www.thelancet.com/oncology Published online June 5, 2013 http://dx.doi.org/10.1016/S1470-2045(13)70244-4 1

Articles

Depression and anxiety in long-term cancer survivors compared with spouses and healthy controls: a systematic review and meta-analysisAlex J Mitchell, David W Ferguson, John Gill, Jim Paul, Paul Symonds

SummaryBackground Cancer survival has improved in the past 20 years, a ecting the long-term risk of mood disorders. We assessed whether depression and anxiety are more common in long-term survivors of cancer compared with their spouses and with healthy controls.

Methods We systematically searched Medline, PsycINFO, Embase, Science Direct, Ingenta Select, Ovid, and Wiley Interscience for reports about the prevalence of mood disorders in patients diagnosed with cancer at least 2 years previously. We also searched the records of the International Psycho-oncology Society and for reports that cited relevant references. Three investigators independently extracted primary data. We did a random-e ects meta-analysis of the prevalences of depression and anxiety in cancer patients compared with spouses and healthy controls.

Findings Our search returned 144 results, 43 were included in the main analysis: for comparisons with healthy controls, 16 assessed depression and ten assessed anxiety; of the comparisons with spouses, 12 assessed depression and ve assessed anxiety. The prevalence of depression was 116% (95% CI 77162) in the pooled sample of 51 381 cancer survivors and 102% (80126) in 217 630 healthy controls (pooled relative risk [RR] 111, 95% CI 096127; p=017). The prevalence of anxiety was 179% (95% CI 128236) in 48 964 cancer survivors and 139% (98185) in 226 467 healthy controls (RR 127, 95% CI 108150; p=00039). Neither the prevalence of depression (267% vs 263%; RR 101, 95% CI 086120; p=088) nor the prevalence of anxiety (280% vs 401%; RR 071, 95% CI 044114; p=016) di ered signi cantly between cancer patients and their spouses.

Interpretation Our ndings suggest that anxiety, rather than depression, is most likely to be a problem in long-term cancer survivors and spouses compared with healthy controls. E orts should be made to improve recognition and treatment of anxiety in long-term cancer survivors and their spouses.

Funding None.

IntroductionSurvival after cancer has improved over the past 20 years, thanks to advances in diagnosis and targeted treatment. As a result, cancer is increasingly thought of as a chronic diseaseabout 70% of patients live for at least 5 years after diagnosis.1,2 GLOBOCAN estimates3 that by 2030, more than 21 million new cases will be diagnosed yearly worldwide. Prevalence estimates suggest that at least 20 million people in the USA will have cancer by 2030, and perhaps 50 million worldwide.4 Several studies have shown that mood disorders are common in patients with cancer. In a meta-analysis of interview-based studies, Mitchell and colleagues5 reported that the point prevalence of major depression was about 16% and that of anxiety was 10%. In most of the studies, patients were interviewed early in the course of illness, during which time the distress of diagnosis and treatment is probably most intense. The prevalence of mood disorders in long-term cancer survivors has been much less extensively investigated and is widely debated,6 partly because of uncertainty about the de nition of long term. Conventionally, oncologists de ne long-term survivors as those who are alive 5 years after diagnosis.7 However, the

US Centers for Disease Control and National Coalition for Cancer Survivorship both de ne a cancer survivor as any person living with cancer from the time of diagnosis to the time of death.8 We consider 2 years or more to be long term because many cancer relapses occur within 2 years.9 Interpretation of the prevalence of mood disorders is also a ected by methodological di cultieseg, uncertainty about the best diagnostic method, heterogeneity in setting, and cancer type. A key question for clinicians is whether the prevalence of mood disorders is signi cantly di erent in patients compared with spouses. Relatives of patients with cancer can often have mood disorders including anxiety and depression. In some cases, the level of distress in spouses can exceed that of patients.10,11 A meta-analysis12 has reported a positive association between patient and carer psychological distress (r=035; p

Articles

2 www.thelancet.com/oncology Published online June 5, 2013 http://dx.doi.org/10.1016/S1470-2045(13)70244-4

depression and anxiety after cancer return to baseline? Large, general population surveys13 suggest that the 30-day prevalence of depression is roughly 5% and the 12-month prevalence is about 9% in Europe and the USA. Anxiety disorders are about twice as common as depression, with a 12-month prevalence of about 18%.14 Several well-powered studies have attempted to measure depression prevalence in people with cancer compared with the general population. Rasic and coworkers15 reported that diagnosis of cancer was signi cantly associated with 12-month prevalence of major depression (155% vs 54% in healthy controls) based on Composite International Diagnostic Interviews with 36 984 people aged 1554 years in the Canadian Community Health Survey. Similarly, Dalton and colleagues16 assessed linked data from 608 591 adults with cancer in the Danish Cancer Registry and reported a relative risk (RR) for depression of 116308 in the rst year after diagnosis, which seemed to increase at 10-year follow-up.

Longitudinal studies of depression and anxiety after cancer suggest that the high early prevalence of mood disorders falls slowly with time, suggesting that anxiety or depression in long-term cancer survivors is more common than in healthy controls.17,18 Long-term cancer survivors face prolonged uncertainty about their prognosis,19,20 although manyparticularly those in remissionmake good psychological progress. In one study,21 almost 50% of patients had cancer-related intrusive thoughts, 3 years or more after surgery for breast cancer. However, other studies2225 have documented low rates of depression, good quality of life, and low distress in long-term cancer survivors. Health-related quality of life is often much the same in long-term cancer survivors and age-matched individuals in the general population.2631 Further work is needed to assess the prevalence of speci c mood disorders and to test whether the prevalence of depression or anxiety in long-term cancer survivors is the same as in healthy controls. How rates compare between patients and their spouses is also unclear. We did a systematic review and meta-analysis of depression and anxiety in long-term cancer survivors compared with their spouses and healthy controls.

MethodsStudy selection and proceduresThe protocol for the systematic review was based on the PRISMA statement.32 We did a systematic search of Medline, PsycINFO, and Embase, from inception to March 31, 2013, for publications in English. We also searched four full-text collections (Science Direct, Ingenta Select, Ovid Full text, Wiley Interscience), and theses and meeting abstracts from the International Psycho-oncology Society. When necessary, authors were contacted directly for primary data. We also searched for reports that cited the references identi ed in our systemtic review. The search terms were: Title=((depressi*

or mood or anxious or anxiety)) AND Topic=((long-term or years or months or survivo*) and (control* or healthy or spous* or relative or carer or caregiver or family)) AND Title=((cancer or tumour or tumor or metast* or oncology or palliati* or lymphoma or leukaemia or leukemia or myeloma or bone-marrow transplant)). AJM, DWF, and JG extracted the primary data independently. We rated the articles on quality, giving a total score out of 15 in four domains: study design, sample size, adequacy of comparator matching, and consideration of confounders.5 Study design was scored as: cross-sectional study=1, retrospective cohort study=2, and prospective cohort study=3. Sample size was scored as: 100199 people=1, 200999 people=2, 10009999 people=3, 10 00099 999 people=4, 100 000 people or more=5. Comparator matching was scored as: no e ective matching=1, selected or partial matching=2, near identical matching=3. Adjustment for confounders was scored as: demographics alone=1, demographics and medical or social factors=2, as 2 plus health-care factors=3, as 3 plus additional factors=4. In cases of disagreement the ratings of AJM were used.

We included studies reporting the prevalence of depression or anxiety in adults with cancer assessed at least 2 years after diagnosis. We excluded studies that reported pooled means rather than proportions or raw numbers33 as well as studies that used indirect estimates of population depression or anxiety and studies reporting rates before diagnosis of cancer. We also excluded duplicate publicationsie, two or more studies using the same sample. We did not include studies done within 2 years of cancer diagnosis in the main analysis, but used

144 results from literature search

76 excluded 8 selctive sampling bias 8 non-cancer patients included 49 insucient data for analysis 1 case ascertainment bias 10 duplicate publications

68 analyses

11 short-term comparison with spouses excluded

43 included in main analysis 26 long-term comparison with health controls 16 of depression 10 of anxiety 17 long-term comparison with spouses 12 of depression 5 of anxiety

14 short-term comparisons with healthy controls included in moderator analysis

Figure 1: Study selection HADS=Hospital Anxiety and Depression Scale.

Articles


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Articles


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2 un

ique

peo

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este

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ith tw

o di

ere

nt m

etho

ds.

Tabl

e 1: S

tudi

es o

f dep

ress

ion

or a

nxie

ty in

long

-ter

m ca

ncer

surv

ivor

s ver

sus h

ealt

hy co

ntro

ls

Articles


these data for a time series moderator analysis. We excluded studies that recruited patients exclusively from palliative settings.

We strati ed results by study quality, method of diagnosis of depression and anxiety (ie, a structured, semi-structured, or clinical interview given by a trained researcher or health professional; a patient-reported scale; or those relying on medical records), and study setting. We included studies done in children and adolescents but adjusted for their e ect in a sensitivity analysis. For those relying on a patient-reported scale we did not have access to patient-level data; therefore, we used the cuto s proposed by study authors.

Statistical analysisWe tested for heterogeneity (I280%=moderate; 90%=high) and for publication bias (by the Egger method).34 Because heterogeneity was high, we used random-e ects rather than xed-e ect meta-analysis.35 However, the standard error and CIs of the summary e ect are wider with the random-e ects model than with the xed-e ect model. Speci cally, we did a DerSimonian-Laird random e ects meta-analysis with StatsDirect (version 277). We did a moderator analysis by comparing RRs to assess whether e ects were related to any of the following factors: use of the Hospital Anxiety and Depression Scale, quality ratings (a score 8 was de ned as high quality), excellent matching quality (score=3), recruitment setting, and time since diagnosis. We also did a sensitivity analysis to adjust for one possible atypical study (de ned on methodological grounds). To avoid double counting of individuals from one publication containing two analyses, we divided the denominator by two.

Role of the funding sourceThe sponsor of the study had no role in study design, data collection, data analysis, data interpretation, or writing of the report. AJM, JG, DWF, and JP had full access to all the data in the study and the corresponding author had nal responsibility for the decision to submit for publication.

ResultsOur systematic review returned 1886 results, of which 304 publications investigated mood disorders in long-term cancer survivors and 144 mentioned a comparison sample. Of these, most were unsuitable and we identi ed only 68 comparisons that contained primary data. 25 were comparisons in the period soon after cancer diagnosis and were therefore excluded, leaving 43 studies for the main analyses ( gure 1, table 1).50

We identi ed 43 comparative analyses (extracted from 27 publications) comparing mood disorders in long-term cancer survivors with healthy controls or spouses ( gure 1, table 1). Five were excluded because they did not compare patients with cancer with a healthy control

group.5155 One study56 was excluded because the co mparator sample was patients attending for breast-cancer screening. We excluded ve comparative studies27,5761 examining distress alone or quality of life. 24 studies compared depression in long-term cancer survivors with healthy controls but eight recruited individuals within 2 years of diagnosis and so were only included in the moderator analysis (appendix). One study15 did not contain enough data for extraction and none were supplied by the authors. Another study47 used two types of analysis and so could be considered atypical (a methodological outlier); it recruited 820 child and adolescent cancer survivors from the German Childhood Cancer Registry. We identi ed 15 studies comparing anxiety in long-term cancer survivors with healthy controls but six recruited individuals within 2 years of diagnosis and were therefore only included in the analysis of the e ect of time since diagnosis (appendix). One short-term study was excluded from the analysis because it included self-reported cancers.62 In studies comparing patients with healthy controls, the median sample size was 5562 (IQR 132825 245). In studies comparing patients with their spouses, the median sample size was 225 (145270). Studies were done in community populations, but 23 did not initially recruit from the community. 37 of 43 used self reporting to ascertain the extent of depression or anxiety.

14 reports included 16 analyses of the prevalence of depression in long-term cancer survivors versus healthy controls, involving 269 011 people (table 1, gure 2). Mean time since diagnosis was 73 years (SD 45). The prevalence of depression was 116% (95% CI 77162) in the pooled sample of 51 381 cancer survivors and 102% (80126) in 217 630 people without cancer. Heterogeneity

See Online for appendix

Andrykowki et al (2005)36 365 (219625)

Bishop et al (2007)37 283 (150546)

Vistad et al (2007)49 194 (095387)

Seitz et al (2010; HADS)47 178 (114278)

Seitz et al (2010; interview)47 160 (088295)

Ramsey et al (2002)47 142 (099203)

Hung et al (2013)42 114 (0981.34)

Khan et al (2010)44 108 (104113)

Thorsen et al (2005)48 106 (089125)

Foss et al (2003; testicular)40 100 (079125)

Keating et al (2005)43 100 (086116)

Dahl et al (2005)38 096 (082113)

Pirl et al (2009)6 079 (052117)

Kim et al (2010)45 072 (063082)

Ellman et al (1995)39 058 (034098)

Foss et al (2003; Hodgkins)40 013 (005039)

Overall 111 (096127)

001 0201 05 5 101 2Relative risk (95% CI)

F igure 2: Risk of depression in long-term cancer survivors versus healthy controls

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was high (I=849%, 95% CI 768893), but there was no publication bias (Egger bias 020; p=088). The random e ects pooled RR was 111 (95% CI 096127) suggesting no signi cant di erence in depression between long-term cancer survivors and healthy controls ( 19; p=01674). We re-examined the overall e ect after excluding the study by Seitz and colleagues,47 which we deemed a methodological outlier. Heterogeneity was much the same after exclusion, and the RR was 106 (95% CI 092123; 068; p=04317).

We did a moderator analysis of di erences in RR between groups (table 2). The RR of depression (in patients vs controls) was signi cantly higher for studies that used the Center for Epidemiologic Studies Depression Scale (p=0042) but not signi cantly lower for those that used the Hospital Anxiety and Depression Scale (00088) and for studies that included mixed cancer types (p=00219).

We also assessed the e ect of time since diagnosis (including studies that recruited patients less than 2 years since diagnosis). Dividing the studies by length of time after diagnosis showed that the RR was highest in those that included patients less than 2 years since diagnosis, or an absolute di erence of 109% (n=8; RR 219, 95% CI 171279; 389; p

Articles


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in lo

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canc

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rviv

ors v

ersu

s spo

uses

Articles


included patients diagnosed more than 10 years ago (n=6; RR 105, 95% CI 091122; 047; p=049). The RR for depression was signi cantly higher for patients diagnosed within the past 2 years compared with those diagnosed 210 years ago (ratio of risks 174; p=00009) or 10 years ago or more (ratio of risks 209; p

Articles


DiscussionWe did four meta-analyses comparing depression and anxiety in long-term cancer survivors with healthy controls and spouses. After 2 years or more, cancer patients had much the same prevalence of depression as did spouses and healthy controls. The prevalence of anxiety was higher in cancer patients than in healthy controls. Anxiety was also high in spouses, indeed it was signi cantly higher in spouses than in patients if one outlier was removed. To our knowledge, our study is the rst meta-analysis to compare the prevalence of depression and anxiety in long-term cancer survivors and matched healthy controls and spouses. Our estimates di er from those in some previous reports, which included patients early after diagnosis and used robust semistructured interviews. 5,75,76 Our purpose was not to more accurately de ne the prevalence of mood disorders in people with cancer, but rather to compare groups that received the same mood assessment. The prevalence of depression in family members was substantial, even though the mean time since diagnosis was about 7 years; anxiety was even more common. Although depression in spouses is important, we found anxiety to be more common than depression. 40% of relatives of long-term cancer survivors had signi cant anxiety. This nding complements a previous meta-analysis12 that assessed comparative rates of distress.

Our results suggest that after diagnosis of cancer, increased rates of anxiety tend to persist compared with healthy controls, whereas increased rates of depression are less longlasting. In the period immediately after diagnosis, depression is roughly twice as common as in healthy controls, but this increased risk only lasts for roughly 2 years. An increased risk of anxiety disorders seems to persist for up to 10 years or more. However, the RRs for patients with active advanced cancer and patients in palliative settings have not been adequately studied (Meyer F, personal communication). We are surprised that the risk of anxiety was not initially signi cantly increased compared with healthy controls, although the di erence was about 8%, and we cannot exclude the possibility that it was even higher in the rst few months after diagnosis. To examine this possibility further, we re-did the analysis including the study62 initially excluded on methodological grounds, which increased the RR of anxiety for patients diagnosed within the past 2 years, but still not to a signi cant degree. These ndings suggest that anxiety, rather than depression, is likely to be the most common problem in long-term cancer survivors compared with healthy controls. However, screening for anxiety has been overlooked compared with screening for distress and depression.77 The burden of anxiety disorders should not be underestimated.78 Anxiety can hamper quality of life after cancer.7981 Possible predictors of anxiety after cancer include poor social support, impaired quality of life, pain, and burden of disease.8286 Some evidence87 suggests that symptom burden has less of an e ect on prediction of anxiety than on prediction of depression

after cancer, which could explain the relative persistence of anxiety compared with depression in long-term cancer survivors.

Previous comparison work has focused on distress and quality of life rather than mood disorders but even among such studies, few had a large sample size.12,88,89 Two studies43,90 reported lower mental health-related quality-of-life domains in long-term cancer survivors compared with population controls. At least one91 has reported improved health-related quality of life in some long-term cancer survivors whereas others noted no di erences in psychological wellbeing.27,58,60,92 Thus, how health-related quality-of-life changes with time in relation to anxiety and depression is unclear. Investigators should assess speci c emotion domainseg, anxiety, depressionnot just general distress or quality of life.

Our results suggest that emotional wellbeing is mixed in long-term cancer survivors, which might be a ected by cancer type and concomitant physical complications. Notably, not all patients will improve at the same rate and psychological risk factors di er.93 However, in patients without complications, the evidence suggests that most patients adjust well, psychologically.20

Our analysis has some limitations. There was substantial heterogeneity in the studies. For example, the quality of the reviewed studies varied and only 12 included in the dataset had excellent quality ratings. The quality of matching with healthy controls varied and only ten studies had high quality matching scores. The quality of matching did not seem to signi cantly a ect RRs; however, statistical power was low when limited to analyses with excellent matching. Studies with low methodological ratings tended to nd larger di erences in prevalence of depression (but not anxiety) between patients and controls, suggesting that study design might be an important factor. Method of case ascertainment was also variable, with the most common method being the Hospital Anxiety and Depression Scale followed by the Center for Epidemiologic Studies Depression Scale. The psychometric properties of the Hospital Anxiety and Depression Scale are disputed.9496 Mitchell and colleagues95 noted that the Hospital Anxiety and Depression Scale had an overall sensitivity of 820% and speci city of 770% for diagnosis of depression in patients with cancer. The method of ascertainment might have a ected our results because the moderator analysis showed a high RR of anxiety but low RR of depression in studies that used the Hospital Anxiety and Depression Scale, and a high RR of depression in studies that used the Center for Epidemiologic Studies Depression Scale. Taken together these e ects might suggest di erences in symptoms of depression or anxiety but not necessarily di erences by clinical case. The Hospital Anxiety and Depression Scale is not a diagnostic method but a symptom screening questionnaire. Only four studies used a structured or semistructured psychiatric interview (none were included in the spousal dataset). The paucity of interview-based data is understandable, given the large

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populations studied. We identi ed two possible outliers, one of which did a ect the ndings.

Another important limitation is that few studies provided adequate clinical descriptions of functional performance, social support, past history, or stage of disease. Thus, we were unable to adequately examine predictors of anxiety and depression. These factors could account for important individual variability predicting depression or anxiety in long-term cancer survivors. We also noted that the prevalence of depression and anxiety was higher in studies involving spouses than those involving healthy controls. Several uncontrolled factors could have a ected this nding, particularly time since cancer diagnosis, which was much lower in the healthy control comparisons. Finally, heterogeneity in healthy controls might have had a role. Little information was presented about recruitment of healthy controls. We restricted our analysis to studies in which some attempt at matching occurred. Several excluded studies recruited patients with other illnesses. In two such studies,97,98 the RR of depression in cancer exceeded depression in stroke, diabetes, and heart disease. Yet in four studies that compared patients with cancer versus patients with other diseases, patients with cancer had similar or lower rates of depression.51,52,55,99 Our ndings underline the importance of detection and treatment of anxiety disorders, not only depression. Future studies should clarify RRs of depression and anxiety in palliative settings or in patients with advanced cancer as well as obtaining more reliable RRs by use of interview methods of diagnosis of mental disorders.Con icts of interestWe declare that we have no con icts of interest.

AcknowledgmentsWe thank the authors who responded to requests for primary data. We also thank Dr Chun-Yu Liu (Taipei Veterans General Hospital, Taiwan).

ContributorsAJM had the idea for the study, extracted data, supervised data extraction, analysed data, and wrote and revised the report. DWF and JG had the idea for the study and extracted data. JP analysed data, PS had the idea for the study and revised the report.

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Depression and anxiety in long-term cancer survivors compared with spouses and healthy controls: a systematic review and meta-analysisIntroductionMethodsStudy selection and proceduresStatistical analysisRole of the funding source

ResultsDiscussionAcknowledgmentsReferences

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