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European Journal of Oncology Nursing 17 (2013) 578e587

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European Journal of Oncology Nursing

journal homepage: www.elsevier .com/locate/ejon

A spectrum of hidden morbidities among spousal caregivers forpatients with cancer, and differences between the genders: A reviewof the literature

Qiuping Li a,b, Alice Yuen Loke a,*

a School of Nursing, The Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong, ChinabWuxi Medical School, Jiangnan University, Wuxi, Jiangsu Province, China

Keywords:Hidden morbiditySpousal caregiversGender differencesCancerCaregiving experience

* Corresponding author. Tel.: þ852 2766 6386; faxE-mail address: alice.yuen.loke@polyu.edu.hk (A.Y

1462-3889/$ e see front matter � 2013 Elsevier Ltd.http://dx.doi.org/10.1016/j.ejon.2013.01.007

a b s t r a c t

Objective: To explore the spectrum of hidden morbidities and gender differences in the spousal care-giving experience with regard to cancer patients across the cancer trajectory, and to discuss directions forfuture research and the implications for interventions to improve the caregiving experience.Methods: A systematic search was conducted to identity articles published in English or Chinese fromJanuary 2000 to July 2012. Studies were located using an electronic search, a manual search, and anauthor search.Results: A total of 19 articles were identified and included in this review. This review of the literaturerevealed that female spousal caregivers, in general, experienced more mental morbidity (higher levels ofdistress, depression, and anxiety, lower levels of mental health), physical morbidity (lower physicalhealth scores, poorer physical functioning, and loss of physical strength), and social morbidity (lowermarital satisfaction and less social support) than male spousal caregivers.Conclusions: This review of the literature revealed that spousal caregivers, particularly female spousalcaregivers for cancer patients, are at a high risk of falling victim to a wide spectrum of hidden morbiditiesdue to their caregiving experience. The cultural influences on the couples and their patterns of com-munication that influence the caregiving experience for cancer patients should be further explored.A tailored-made intervention for spousal caregivers, both males and females, in the context of cancercare should be developed to cater to the needs of this population, which suffers from a spectrum ofhidden morbidities.

� 2013 Elsevier Ltd. All rights reserved.

Introduction

Cancer is a leading cause of deathworldwide. In 2008, 7.6millionpeople died from the disease, accounting for 13% of all deaths, and70% of these occurred in low- and middle-income countries (WHO,2012a). Deaths from cancer worldwide are projected to continuerising, reaching a figure of 13.1 million in 2030 (WHO, 2012a). InChina, cancerwas estimated to account for 1.9million deaths (20%ofall deaths) in 2005, or about one fourth of all deaths due to chronicdisease (7.5million). TheWorldHealthOrganization (WHO)has alsoestimated that deaths from chronic disease in Chinawill increase by19% in the ten-year period from 2005 to 2015 (WHO, 2012b).

A diagnosis of cancer and its treatment has an impact not onlyon the patient but also on the family caregivers (Kayser et al.,2007). With new and advanced medical treatment, 68% of adults

: þ852 2364 9663.. Loke).

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diagnosed with cancer today can expect to be alive in five years’time (Jemal et al., 2011). Due to the good five-year survival rate forcancer, shorter hospital stays, limited discharge planning, and theexpansion of home care technology, the burden of caring for cancerpatients has been transferred to the family members of these pa-tients, who are now being asked to shoulder greater burdens forlonger periods of time (Chen et al., 2004; Schulz and Beach, 1999;Zivin and Christakis, 2007).

A review of the costs of family caregiving has shown that thecaregiving role can be highly stressful and can lead to considerablepsychological, social, economic, and health costs for the familycaregiver (Haley, 2003). It has been reported that the spouse is theprimary informal caregiver for cancer patients (Chen et al., 2004;Kurtz et al., 1995; Nijboer et al., 1998) Spouse caregivers of cancerpatients can experience high levels of stress, potential burnout,depressive symptoms, marital distress, poor health, and unmetneeds (Braun et al., 2007; Chen et al., 2004; Hagedoorn et al., 2008;Kurtz et al., 1995; Nijboer et al., 1998). Showing concern and

Q.P. Li, A.Y. Loke / European Journal of Oncology Nursing 17 (2013) 578e587 579

support for spousal caregivers is important since their mental andphysical status affects their capacity to continue to provide care foran ill spouse (Northouse et al., 2001).

Many studies have reported on the negative consequences ofcaregiving, such as fatigue, loss of sleep, loss of appetite, and illness(Blum and Sherman, 2010; Dhruva et al., 2012). There are alsoconsequences that may not be readily recognizable by both care-givers and health professionals until the caregiver falls ill. Care-givers have been reported to suffer from physical, mental, andsocial problems (Braun et al., 2007; Hagedoorn et al., 2008; Kurtzet al., 2004; Matthews et al., 2004; Pitceathly and Maguire,2003). According to the WHO’s health model (Larson, 1999),health is ‘a state of complete physical, mental, and social well-beingand not merely the absence of disease or infirmity’. Where ‘health’is lacking, but before illness has developed, a sub-optimal state ofhealth e ‘hidden morbidity’ e can be considered to exist.

Although the term ‘hidden morbidity’ is not widely used in thecontext of cancer caregiving, the term ‘hidden morbidity’ is used inthis study to refer to a sub-optimal physical, mental and social statein spousal caregivers. In web dictionaries (Proportional Morbidity,2012), the term ‘morbidity’ has been defined as ‘the relative inci-dence of a particular disease’ and ‘an abnormally gloomy or un-healthy state of mind’. Morbidity is also delineated as a ‘departurefrom a state of physical or psychological well-being, resulting fromdisease, illness, injury, or sickness, specially where the affectedindividual is aware of his or her condition (Morbidity, 2012). Theterm ‘hidden morbidity’ used in this review refers to a conditionthat not known to health professionals and even to the personwhois suffering from the sub-optimal condition (Braun et al., 2007).

A few studies have been conducted on the impact on the spouseof providing care to a cancer patient; however, an overall picture ofthe hidden morbidity among spousal caregivers is lacking. Genderhas been recognized as the most predictive factor of negative ex-periences in caregiving (Hagedoorn et al., 2008), and there havebeen isolated studies reporting gender differences in the spousalcaregiving experience for cancer patients. However, no review ofthe literature has been conducted to synthesize the findings relatedto the hidden morbidity and gender differences among spousalcaregivers (Braun et al., 2007).

Therefore, it is the objectives of this review to (i) synthesize theresults of empirical research on the hidden morbidities of spousalcaregivers across the cancer trajectory; (ii) identify differencesbetween the genders; and (iii) illuminate the directions for futureresearch and implications for interventions. By providing a betterunderstanding the caregiving experience and the hidden morbid-ities of caregivers, and providing a basis for designing related in-terventions to support and improve the spousal caregivingexperience according to gender differences, if any, the findings inthis literature review may be helpful to healthcare professionalswho work with couples dealing with cancer.

Methods

A systematic searchwas conducted to identity articles publishedin English or Chinese from January 2000 to July 2012. Studies werelocated using electronic searches, a manual search, and an authorsearch. The following computerized databases were searched:MEDLINE, CINAHL, Science Citation Index Expanded, Scopus, Psy-chINFO, and China Academic Journals Full-text Database. The keysearch terms used were ‘cancer’ or ‘oncology’ or ‘carcinoma’ AND‘caregiver’ or ‘caregiving’ or ‘carer’, AND ‘gender differences’ or‘gender’ AND ‘spouse’ or ‘couple’ or ‘partner’.

Initially, a total of 177 records were identified from the literaturesearch of the six databases using the keywords, a manual search ofreview articles and reference lists, and from the author search.

Given that the six databases were searched, one hundred andtwenty recordswere found to be duplicated; only 57 remained afterremoving the duplicate records. Data and literature were extractedfrom each of the included studies using a standard format: infor-mation on the literature, study method, study aims, samples/settings, and findings. To be included in this review, the studypopulation had to be largely comprised of couples coping withcancer, on the caregiving experiences of spouses caring for patientswith cancer, and to report on findings that included both male andfemale spousal caregivers in the same study. After records werescreened and articles assessed, thirty-eight records were excludedfor not meeting the criteria for inclusion (Fig. 1). In the end, a totalof 19 articles met the criteria and were included in this review.

Results

Quality and characteristics of the selected studies

All of the 19 articles included in this review were published inpeer-review journals. The impact factor of these journals rangesfrom 1.849 to 4.200. With exception of two journals, one is anofficial journal published by the European School of Oncology, andthe other is a journal that “offers reviews of key neuropsychiatrictopics for clinicians, with the aim of tying research findings to theneeds of clinical practice” (JAMA, 2012). In all of these 19 studies,the study design were well defined; time point of data collectionwas specified; characteristics of the targeted couples and samplesize were clearly described; the analysis for confounding variableswere properly adjusted; the outcomes and estimated significanceswere stated without obviously bias. Overall, the 19 articles includedin this review were considered of high quality.

All of the 19 articles included in this review were quantitativestudies (Table 1). There were 9 cross-sectional and 10 longitudinalstudies, with observation times ranging from 2 weeks to 5 yearsfrom baseline. The studies were conducted in the United States (8)(Colgrove et al., 2007; Haley et al., 2003; Kim and Carver, 2007; Kimet al., 2006; Langer, 2003; Langer et al., 2003, 2010; Northouseet al., 2000), the Netherlands (5) (Hagedoorn et al., 2000, 2002;Nijboer et al., 2000, 2001; Tuinstra et al., 2004), Israel (3) (Baideret al., 2003; Barnoy et al., 2006; Goldzweig et al., 2009), Germany(2) (Luszczynska et al., 2007; Pinquart and Duberstein, 2005), andFinland (1) (Gustavsson-Lilius et al., 2007). Of the 19 studies, 16(84.2%) were conducted in Western countries.

The couples in the study were coping with colorectal or coloncancer (5) (Goldzweig et al., 2009; Nijboer et al., 2000, 2001;Northouse et al., 2000; Tuinstra et al., 2004), lung cancer (2) (Haleyet al., 2003; Pinquart and Duberstein, 2005), prostate or breastcancer (1) (Baider et al., 2003), and gastrointestinal cancer (1)(Luszczynska et al., 2007). Over half (10/19, 52.6%) of the studiesinvolved multiple types of cancer: colon, lung, liver, brain, skin, andbone (Barnoy et al., 2006; Colgrove et al., 2007; Gustavsson-Liliuset al., 2007; Hagedoorn et al., 2000, 2002; Kim et al., 2006; Kimand Carver, 2007; Langer, 2003; Langer et al., 2003, 2010).

The sample size in these studies ranged from 40 to 429 couples,and the total number of male and female spousal caregivers was1569 and 1894, respectively. The caregivers were between the agesof 43 and 69.2, and the patients between 43.5 and 70.7. The timethat had elapsed since the diagnosis of cancer varied considerablyfrom newly diagnosed to 5 years or more, with nearly half (10,52.6%) of the studies involving subjects who had been diagnosedfor over 2 years. Stages of cancer also varied across the studies fromStages I/II/III, with one study specifying that no patient was ina terminal condition (Barnoy et al., 2006), while another specifiedthat all of the patients had a life expectancy of less than 6 months(Haley et al., 2003).

Table 1Summary of studies on spousal caregiving for cancer patients.

Authors (country of thestudy)

Aims SD Samples/Gender of SC/Time points Instrument used Significant findings

Baider et al., 2003(Israel)

To identify and compare thepsychological distress of couples withprostate and breast cancer

C 118 prostate cancer couples; 169 breastcancer couples.Time point: 23.3 months afterdiagnosis.

- The Brief Symptom Inventory (BSI, toassess symptoms of psychologicaldistress).

- MCG were significantly more distressed (BSI,m ¼ 65.0) than FCG (BSI, m ¼ 59.2).

Barnoy et al., 2006(Israel)

To examine the influence ofcorrespondence in informationalcoping styles on the psychologicalreactions of cancer patients and theirspouse as the main caregiver

C 98 couplesSCG: males 45, females 53.Time point: in the course of ambulatorychemotherapy, 27.3 months afterdiagnosis.

- The Mental Health Inventory (MHI, Veitand Ware, 1983) to assess psychologicalwell-being and psychological distress.

- FCG experienced more psychological distress thanMCG (MHI, m ¼ 5 vs 6).

Colgrove et al., 2007(USA)

To examine the moderating effects ofspirituality and gender on the mentaland physical health of spousalcaregivers

C 403 couplesSCG: males 184, females 219.Time point: approximately 2 yearsafter being diagnosed with cancer.

- Functional Assessment of Chronic IllnessTherapy-Spirituality (FACIT-Sp);

- Pearlin Stress Scale (PSS);- Medical Outcomes Study Short Form-36(MOS-SF36).

- Caregiving stress (PSS, m ¼ 6.67) was associated withpoor mental functioning (SF36,m¼ 50.54), which wasless prominent among caregivers with a high level ofspirituality (stress-buffering effect).

- No gender differences were found in stress-bufferingor aggravating effects of spirituality on themental andphysical health of caregivers.

Goldzweig et al., 2009(Israel)

To assess psychological distress andgender differences among middle-agedand older colorectal cancer patients andtheir healthy spouses

C 231 couplesSCG: males 90, females 141.Time point:2e6 years after diagnosis.

- The Brief Symptom Inventory (BSI);- The ENRICH Marital Satisfaction Scale(EMS).

- MCG were more distressed than FCG (BSI, m ¼ 61.48vs 55.70).

- FCG had a higher level of marriage satisfaction thanMCG (EMS, m ¼ 3.72 vs 3.66).

Gustavsson-Lilius et al.,2007 (Finland)

To investigate the sense of coherence(SOC) e distress association amongcancer patients and their partners

L 123 couplesSCG: males 68, females 55.Time points:At the time of diagnosis (T1); 8(T2) and14 (T3) months post-diagnosis.

- Orientation to Life Questionnaire (OLQ, toassess SOC);

- The Beck Depression Inventory (BDI);- Endler Multidimensional Anxiety Scales(EMAS-state).

- FCG had more depression at T1 and T2 than MCG (BDI,m ¼ 6.2 vs 4.0 and 6.0 vs 3.9), and anxiety symptomsat all three time points (EMAS-state, m ¼ 39.5 vs 33.5,35.3 vs 30.1 and 37.3 vs 30.8, respectively).

- No gender differences were found regarding thechange of SOC in caregivers.

Hagedoorn et al., 2000(Netherlands)

To further knowledge on gender androle differences relating to thepsychological distress and quality of lifeof couples dealing with cancer

C Patient Association (PAS, 105 couples,SCG: 34 males, 71 females), Hospital(HS, 68 couples, SC: 36 males, 2females), healthy control (80 couples).Time points: time since diagnosis: 5.02(PAS) and 2.81 (HS) years.

- Epidemiological Studies Depression Scale(CES-D);

- Cantril’s Ladder (for QOL).

- FCG perceived more psychological distress (CES-D,m ¼ 11.83 vs 8.1 in PAS and m ¼ 12.50 vs 7.56 in HS,respectively) and a lower quality of life (QOL,m¼ 7.09vs 7.55 in PAS andm¼ 6.84 vs 7.69 in HS, respectively)than MCG.

Hagedoorn et al., 2002(Netherlands)

To examine identity-relevant stress asa possible explanation for genderdifferences in psychological distress

C 68 couplesSCG: males 36, females 32.Time point: couples were in treatmentor check-up.

- Epidemiological Studies Depression Scale(CES-D, Dutch translation).

- FCG scored higher on distress than MCG (CES-D,m ¼ 12.93 vs 7.50).

Haley et al., 2003 (USA) To examine the risk factors andprotective factors as predictors offamily caregiver well-being

C 40 couples of patients with dementiaand 40 couples of patients with lungcancer.SCG: 16 males, 64 females.Time point: within 14 days after thepatient’s admission to a hospice.

- Epidemiological Studies Depression Scale(CES-D);

- Life Satisfaction Index-Z (LSIZ).

- Caregivers had a high level of depression (CES-D,m ¼ 17.73, scores over 15 have been found to bestrongly associated with clinical depressive disorders)and a low level of life satisfaction (LSIZ, m ¼ 14.64, farbelow published means for older adults).

- FCG had a higher level of depression (r ¼ 0.29,p< 0.01) and lower life satisfaction (r¼ 0.27, p< 0.05)than MCG.

Kim et al., 2006(USA)

To examine how the caregiver’sperception of providing care to a spousewith cancer differs by gender

C 429 couplesSCG: males 190, females 239.Time point:2 years after diagnosis.

- Caregiver Reaction Assessment Scale(CRA), to assess caregiver’s esteem;

- The Pearlin Stress Scale (Pearlin et al.,1990).

- The mean score of caregiver’s esteem and caregivingstress was 30.79 and 6.68, respectively.

- Compared to FCG, MCG were more likely to reporthigher levels of caregiver esteem (b¼ 0.18, p< 0.001),which in turn was related to lower levels of caregivingstress (b ¼ �0.10, p < 0.05).

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Kim et al., 2007 (USA) To explore gender differences in theassociation between attachmentqualities and the level of involvement incaregiving and difficulties in caregiving

C 400 couplesSCG: males 192; females 208.Time point: approximately 2.1 yearsafter being diagnosed with cancer.

- Measure of Attachment Quality (MAQ);- 17-item self-developed care tasks scale:frequencies and difficulties.

- Interaction between attachment security and the frequency of emotional care: greater security of attachment of FCG related to providing more frequentemotional care, whereas among MCG, greater avoidance related to less frequent emotional care.

- Interactions between attachment anxiety and frequencies of tangible andmedical care: more anxiouslyattached FCG provided more frequent tangible care,whereas more anxiously attached MCG provided lessfrequent medical care.

Langer et al., 2003(USA)

To examine the changes and dyadicdifferences in marital satisfaction andnegative affect over time after SCT(Stem Cell Transplantation)

L Pre-transplant (131 couples, 65 males),6 months post-transplant (78 couples),1 year post-transplant (76 couples, 40males).A nonmedical group as a normativesample.

- The Profile of Mood States (POMS);- The Dyadic Adjustment Scale (DAS);- The Short Form 36Health Survey (HSSF36,patients only).

- FCG were more depressed (POMS, m ¼ 0.98 vs 0.57)and anxious (POMS, m ¼ 1.33 vs 0.89) as compared toMCG.

- With respect to marital satisfaction, couples werematched in their perceptions of the relationship priorto transplantation but grew mismatched over time.

- FCG were less satisfied with their marital satisfactionthan male caregivers (DAS, m ¼ 38.45 vs 41.38).

Langer et al., 2003(USA)

To explore the effects of gender and role(patient/spouse) on mood disturbancesin the cancer setting

L 131 hematopoietic stem cell transplant(HSCT) couples.A nonmedical sample for normativecomparison.Time point: before HSCT, 6 months, 1year, and 2 years after HSCT.

- The Profile of Mood States (POMS). - Female caregivers reported greater depression andanxiety than male caregivers.

- Male caregivers showed elevations in negative affectbefore transplant (p < 0.01) but not after (p > 0.05).

- Female caregivers, in contrast, showed elevations atmultiple time points (p < 0.01).

Langer et al., 2010(USA)

To examine the trajectory of maritaladjustment and satisfaction amonghematopoietic stem cell transplant(HSCT) couples e as a function of roleand gender

L 121 Couples pre-HSCT.SCG: males 63, females 58.A nonmedical sample for normativecomparison.Time points: before HSCT, 6 months, 1,2, 3, and 5 years after HSCT.

- The Dyadic Adjustment Scale (DAS, at thefirst five time points, at the 5-year point,only the satisfaction subscale of the DAS).

- FCG reported lower levels of marital satisfaction atmultiple time points: 6 months (DAS, m ¼ 38.42.29 vs40.54), 1 year (DAS, m ¼ 34.44 vs 40.44) and 5 years(DAS, m ¼ 23.34 vs 39.63) post-transplant than MCG.

Luszczynska et al., 2007(Germany)

To examine the function of gender insupport transactions mainly in thecontext of GI cancer surgery

L 173 couplesSCG: males 65, females 108.Time points:During the week before surgery (T1), 1month (T2), and 6 months (T3) aftersurgery.

- The Berlin Social Support Scales (BSSS). - Support provided decreased for male caregivers, butremained high in female caregivers when comparedthe support provided before surgery and at 1 monthafter surgery (BSSS, m ¼ 3.71 vs 3.54 for MCG; 3.77 vs3.74 for FCG).

Nijboer et al., 2000(Netherlands)

To describe patterns of caregivingexperiences in the partners of cancerpatients over a 6-month period

L 148 couplesSCG: males 54, females 94.Time point: the time of the patient’sdiagnosis (T0), 3 months (T1) and 6months (T2) thereafter.

- Caregiver Reaction Assessment Scale(CRA).

- FCG perceived a more negative impact on the loss ofphysical strength as compared to MCG (CRA loss ofphysical strength,m¼ 2.03 vs 1.76,m¼ 1.96 vs 1.75 atT0 and T2, respectively).

Nijboer et al., 2001(Netherlands)

To examine patterns and determinantsof three dimensions of the health ofcaregivers of newly diagnosedcolorectal cancer patients

L 148 couplesSCG: males 54, females 94.Time points: T0 (as soon as possibleafter the patient’s diagnosis), T1 (threemonths after T0), and T2 (three monthsafter T1).

- RAND 36-item Health Survey. - Physical functioning declined within a 6-monthperiod in FCG (RAND, m ¼ 78.8 vs 84.3), while nochange was observed in MCG (RAND, m ¼ 85.2 vs84.5).

Northouse et al., 2000(USA)

To explore couples’ patterns ofadjustment to colon cancer during thefirst year following surgery

L 56 couplesSCG: males 22; females 34.Time points: one week (T0) post-diagnosis, at 60 days (T1) and one year(T2) post-surgery.

- The Smilkstein Stress Scale (SSS);- The Dyadic Adjustment Scale (DAS,assessed at T1 and T2).

- Although no statistically significant gender differenceswere found in the level of concurrent stress reportedby caregivers, female caregivers reported relativelyhigher levels of concurrent stress at all three timepoints than MCG (SSS, m ¼ 16.8 vs 14.6, 17.1 vs 15.2,and 16.6 vs 13.5 at T0, T1, and T2, respectively).

- FCG reported less marital satisfaction (DAS,m ¼ 115.8vs 123.6, 112.4 vs 121.6 at T1 and T2, respectively)than MCG.

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Table

1(con

tinu

ed)

Authors(cou

ntryof

the

study)

Aim

sSD

Samples/Gen

der

ofSC

/Tim

epoints

Instrumen

tused

Sign

ificantfindings

Pinqu

artan

dDube

rstein,2

005

(German

y)

Toassess

how

optimism

andpessimism

relate

todep

ressivesymptomsin

spou

sesof

lungcancerpatients

L13

8an

d60

couplesat

twotimepoints,

resp

ective

lySC

G:males

48,2

1,females

90,3

9at

T1an

dT2

,respective

ly.

Timepoints:duringtrea

tmen

ttime

(T1)

andon

eye

arafter(T2).

-Ham

ilton

Dep

ressionScale(H

DS,forSC

G).

-FC

Ghad

higher

leve

lsof

dep

ressionat

T1(t

(137

)¼4.31

,p<0.00

1,an

dT2

(t(59)

¼4.29

,p<0.01

)than

MCG;

-AtT1

,SCGof

patients

inad

vancedstag

esof

cancer

weremoredep

ressed

than

other

SCG(t

(137

)¼

2.87

,p<

0.05

).Tu

instra

etal.,20

04(N

etherlands)

Toex

aminepattern

sof

psych

olog

ical

distressin

couplesfacingco

lorectal

cancerwithin

6mon

thsaftersu

rgery

L13

7co

uples

SCG:males

48,fem

ales

89.

Timepoints:within

2wee

ksafter

surgery(T1),3

(T2)

and6(T3)

mon

ths

afterT1

.

-Ep

idem

iologicalStudiesDep

ressionScale

(CES

-D).

-Fe

malean

dmalecaregive

rsreportedsimila

rleve

lsof

distressat

T1(CES

-D,m

¼9.3vs

9.2).A

t3an

d6

mon

thsaftersu

rgery,

FCGap

pea

redto

bemoredis

tressedthan

MCG(CES

-D,m

¼11

.3vs

7.8,

and10

.3vs

7.3,

resp

ective

ly).

Abbreviations:

SD,S

tudydesign;C,C

ross-section

alstudy;

L,Lo

ngitudinal

study;

SCG,S

pou

salC

areg

ivers;

MCG,M

aleCareg

ivers;

FCG,F

emaleCareg

ivers;

m,M

ean.

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Hidden morbidity

A synthesis of the findings of these studies focused on followingthe three main dimensions e mental, physical, and social e of themorbidities of caregivers according to the WHO’s health model(Larson, 1999). The term ‘hidden morbidity’ here refers to thecaregivers’ sub-optimal condition of health, which is not known tohealth professionals and even to the caregivers themselves.

Mental morbidityThemental morbidity of the caregivers refers to the high level of

psychological distress, depression, anxiety, and poor mental well-being suffered by the caregivers.

There were 15 articles related to the mental morbidity of care-givers. Twelve of the fifteen studies reported that female spousalcaregivers had a higher level of distress, depression, and anxiety,and a lower level of mental well-being (Barnoy et al., 2006;Colgrove et al., 2007; Gustavsson-Lilius et al., 2007; Hagedoornet al., 2000, 2002; Haley et al., 2003; Kim et al., 2006; Langer,2003; Langer et al., 2003; Nijboer et al., 2001; Pinquart andDuberstein, 2005; Tuinstra et al., 2004) than male spousal care-givers. One study showed that there were no gender differences inconcurrent stress (Northouse et al., 2000). Two studies showed thatmale spousal caregivers were significantly more distressed thanfemale spousal caregivers (Baider et al., 2003; Goldzweig et al.,2009).

Studies using the Epidemiological Studies Depression Scale(CES-D) scale to measure depression showed that female spousalcaregivers experienced a higher level of psychological distress thanmales, with the mean ¼ 11.83 vs 8.1 in one study (Hagedoorn et al.,2000) and m ¼ 12.93 vs 7.50 in another study (Hagedoorn et al.,2002). One study reported that female spousal caregivers experi-enced depression when caring for patients with cancer (CES-D,m ¼ 17.73) (Haley et al., 2003). In a longitudinal study, increasedlevels of psychological distress prior to a scheduled surgery (CES-D,m ¼ 9.3 and 9.2) were reported for both female and male spousalcaregivers. Three and six months after the surgery, while the dis-tress levels of males returned to normal (m ¼ 7.8 and 7.3), femalescontinued to have a high level of distress (m ¼ 11.3 and 10.3)(Tuinstra et al., 2004).

A study that adopted the Pearlin Stress Scale (PSS), showed thatwhen compared to females, male spousal caregivers reportedexperiencing a lower level of stress (b¼�0.10, p< 0.05) (Kim et al.,2006). A study that explored the influence of correspondence ininformational coping styles on the psychological reactions of mar-ried couples, which used the mental health inventory (MHI),reported that female spousal caregivers experienced slightly morepsychological distress than their male counterparts (Barnoy et al.,2006). Another study on the spousal caregivers of patients withlung cancer, which used the Hamilton Depression Scale (HDS), alsoindicated that higher levels of depression at the time of treatment(t¼ 4.31, p< 0.001) and one year after treatment (t¼ 4.29, p< 0.01)in females was emerged when compared to male spousal care-givers (Pinquart and Duberstein, 2005).

A study using the Profile of Mood States (POMS) that involved of131 couples with a partner whowas suffering from various types ofcancer and who was receiving a hematopoietic stem cell transplant(HSCT), reported that, when compared with male spousal care-givers, females were more depressed (0.98 vs 0.57) and anxious(1.33 vs 0.89) (Langer et al., 2003). The results of another study alsosupported the view that female spousal caregivers were moredepressed and anxious than their male counterparts (Langer, 2003).

The study that explored the relationship between a strong‘sense of coherence’ (SOC) and depression (the Beck DepressionInventory, BDI) and anxiety (the Endler Multidimensional Anxiety

Fig. 1. The flow diagram on identifying the literature.

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Scales, EMAS-state) also reported that female spousal caregiverswere more depressed and had higher levers of anxiety at the timeof the diagnosis of cancer (BDI,m¼ 6.2 vs 4.0; EMAS-state,m¼ 39.5vs 33.5) and at 8 months post-diagnosis (BDI,m¼ 6.0 vs 3.9; EMAS-state, m ¼ 35.3 vs 30.1) than male spousal caregivers (Gustavsson-Lilius et al., 2007).

Therewere two studies that focused on themental well-being ofcaregivers (Colgrove et al., 2007; Nijboer et al., 2001). A study usingthe Medical Outcomes Study Short Form-36 (MOS-SF36) thatexamined the effects of spirituality on the stress and mental healthof spousal caregivers showed that the female gender was asso-ciatedwith poorermental health. However, themental health scoreof the spousal caregivers (m ¼ 50.54) did not significantly differfrom that of the published mean of the general population of theUnited States (m ¼ 50.00) (Colgrove et al., 2007).

Another study using the RAND 36-item Health Survey thatexamined the quality of life of caregivers who have cared for familymembers with colorectal cancer, reported that females experiencedworse mental well-being within a 6-month period than their malecounterparts (m ¼ 70.0 vs 78.0) (Nijboer et al., 2001). In general,female spousal caregivers are more likely to experience poorermental health (Colgrove et al., 2007) or worse mental well-being(Nijboer et al., 2001).

No gender differences in concurrent stress were reported ina study conducted in the USA. The Smilkstein Stress Scale (SSS) was

used to assess the concurrent stress (the mean scores for females vsmales were 16.8 vs 14.6, 17.1 vs 15.2, and 16.6 vs 13.5 at one weekafter the diagnosis, 60 days, and one year post-surgery, respec-tively) (Northouse et al., 2000). Two studies that reported that fe-male spousal caregivers experienced significantly lower levels ofdistress than males were conducted in Israel, and that the sameinstrument (the Brief Symptom Inventory, BSI) was used to mea-sure psychological distress (m¼ 65.0 vs 59.2, and 61.5 vs 55.7 in thetwo studies) (Baider et al., 2003; Goldzweig et al., 2009).

In summary, female spousal caregivers are more likely toexperience more mental morbidity than males, such as a higherlevel of psychological distress, depression, and anxiety and a lowerlevel of mental well-being.

Physical morbidityThe physical morbidity of caregivers refers to their poor physical

health or functioning. There were three articles in this reviewrelating to outcomes on the physical well-being of caregivers(Colgrove et al., 2007; Nijboer et al., 2000, 2001). A study examinedcaregivers’ physical health using theMedical Outcomes Study ShortForm-36 (MOS-SF36). The results revealed that although no genderdifferences were found with regard to the physical health of care-givers, their mean physical health score was significantly lowerthan that of the published mean of the US general population(m ¼ 47.01vs 50.00) (Colgrove et al., 2007).

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Two studies, using the Caregiver Reaction Assessment Scale(CRA) (Nijboer et al., 2000) and the RAND 36-item Scale (Nijboeret al., 2001) respectively, examined the physical health of spouseswho have cared for family members with colorectal cancer. Agreater loss of physical strength in female spousal caregivers, whencompared to their male counterparts, was experienced at the timeof their patient’s diagnosis (CRA, m ¼ 2.03 vs 1.76) and six monthsafter the diagnosis (m ¼ 1.96 vs 1.75) (Nijboer et al., 2000). Whencompared with their male counterparts, poorer physical function-ing within a 6-month period in females was also reported inanother study (RAND 36-items, m ¼ 78.8 vs 85.2) (Nijboer et al.,2001). In conclusion, female spousal caregivers experiencedgreater loss of physical strength (Nijboer et al., 2000) and poorerphysical functioning (Nijboer et al., 2001) than male spousal care-givers. However, no gender differences in physical health werefound in one study (Colgrove et al., 2007).

To summarize, female spousal caregivers were more likely tosuffer physical morbidity, such as a lower physical health score(Colgrove et al., 2007), poorer physical functioning (Nijboer et al.,2001), and a loss of physical strength (Nijboer et al., 2000), whencompared to males.

Social morbidityFour studies on social morbidity included in this review focused

on marital relationships and social support (Goldzweig et al., 2009;Langer et al., 2003, 2010; Northouse et al., 2000). There were threestudies that used the DAS (Dyadic Adjustment Scale) (Langer et al.,2003, 2010; Northouse et al., 2000) to examine marital relation-ships. Two of them reported that marital satisfaction decreasedover time among female spousal caregivers (m ¼ 41.76, 38.42,34.44, 23.34 at pre-HSCT (hematopoietic stem cell transplant), 6months,1 year, and 5 years post-HSCT, respectively), but not amongmale spousal caregivers (DAS,m ¼ 41.06, 40.54, 40.44, and 39.63 atpre-HSCT, 6 months, 1 year, and 5 years post-HSCT, respectively)(Langer et al., 2003, 2010). When compared with males, femalespousal caregivers also had a lower level of marital satisfaction at 1year and 5 years after HSCT (DAS m ¼ 34.44 vs 40.44, and 23.34 vs39.63 respectively) (Langer et al., 2003, 2010). This is in line withanother study in that less marital satisfaction was reported in fe-males at 60 days and 1 year post-surgery when compared to theirmale countparts (DAS, m ¼ 115.8 vs 123.6, 112.4 vs 121.6, respec-tively) (Northouse et al., 2000).

By contrast, a different result was reported in a study thatfocused on the marital satisfaction of 231 colorectal cancer couples,using the ENRICH Marital Satisfaction Scale (EMS). The resultsshowed that male spousal caregivers experienced a lower level ofmarital satisfaction than females (m ¼ 3.66 vs 3.72) (Goldzweiget al., 2009).

Two studies reported that female spousal caregivers experi-enced less social support than their male counterparts (Langeret al., 2003; Northouse et al., 2000). A study on the adjustment ofcouples to colon cancer showed that female spousal caregiversperceived less social support than male ones at one week post-diagnosis, at 60 days post-diagnopsis, and at one year post-surgery, with Social Support Questionnaire scores of m ¼ 92.6 vs99.8; m ¼ 93.8 vs 98.4; and m ¼ 91.2 vs 96.0, respectively(Northouse et al., 2000). Another study also reported that fewerfemale caregivers (51%) received help from family and friends thanmale caregivers (84%) (Langer et al., 2003).

Overall, social morbidity were reported in these studies. As tosocial morbidity in those with lower levels of marital satisfaction,three studies that measured marital satisfaction (DAS) reportedthat female spousal caregivers experienced a higher level of socialmorbidity than males, and that the level became worse over time(Langer et al., 2003, 2010; Northouse et al., 2000). Whereas one

study that used EMS to measure marital satisfaction reported thatmale spousal caregivers had higher social morbidity than their fe-male counterparts (Goldzweig et al., 2009). Regarding social mor-bidity in terms of social support, female spousal caregiversexperienced less social support than males (Langer et al., 2003;Northouse et al., 2000).

Discussion

In this review, a spectrum of hidden morbidities and genderdifferences in the spousal caregiving experience of cancer patientswere explored.

Hidden morbidity

In general, spousal caregivers of patients with cancer sufferedfrom a wide spectrum of hidden morbidities, such as mental mor-bidity (higher levels of distress, depression, and anxiety, and lowerlevels of mental health), physical morbidity (lower level of physicalhealth, poorer physical functioning, and the loss of physicalstrength), and social morbidity (lower marital satisfaction andlower levels of social support). Females of a spouse with cancerperceived the caregiving process more negatively in these di-mensions when compared to their male counterparts. Only two outof the nineteen studies reported that male caregivers had highermental and social morbidities than females. Overall, it can beconcluded that spousal caregivers (particularly females) of cancerpatients are a high-risk or hidden morbidity population in all threedimensions of the WHO’s definition of health (Larson, 1999).

Spousal caregivers for patients with cancer have suffered fromawide spectrum of hiddenmorbidities. This could be due to the factthat informal caregivers of cancer patients need to meet multi-dimensional demands, such as treatment monitoring; treatment-related symptom management; providing emotional, financial,and spiritual support; and assisting with personal and instrumentalcare (Given et al., 2001). Providing care to a loved one with anadvanced or serious disease is one of life’s greatest stressors, andcaregivers are at increased risk of mental and physical morbidityand mortality (Schulz and Beach, 1999). Spousal caregivers may beparticularly vulnerable, since they are more willing to make sacri-fices to care for their partner (Haley, 2003).

The imbalance in the number of studies focusing on differentdimensions of hiddenmorbidity is noteworthy. In this review, therewere 15 studies exploring mental morbidity, and only three andfour studies on physical and social morbidity respectively. Morestudies on physical and social morbidity are needed to providea more comprehensive picture of the hidden physical and socialmorbidities of the spousal caregivers of cancer patients.

Gender differences in caregiving

It is concluded in this review that there are gender differences inthe spousal caregiving experience. The gender differences in rolecommitment may account for the differences between female andmale caregivers (Kramer and Kipnis, 1995). Female carers of cancerpatients have been found to position themselves as all-encompassing expert carers, leading to the taking on of too manyresponsibilities, self-sacrifice, and distress, in contrast to malecarers who see caring as a task of competency (not their traditionalrole), leading to feelings of self-mastery or satisfaction (Kim et al.,2007; Ussher and Sandoval, 2008). Also, female caregivers tradi-tionally are likely to perform more personal care and householdchores, which may be more time-consuming, demanding, andongoing than traditional male tasks (Kim et al., 2007; Rose-Regoet al., 1998).

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Moreover, differences in emotional attentiveness and copingstyles may explain the general differences that have been observedbetween the genders (Rose-Rego et al., 1998). As female caregiverswere found to be more attentive than male caregivers to theiremotions, they were more likely to report negative effects fromcaregiving. Also, females have been found to use more emotion-focused coping strategies, which are associated with higherreported levels of negative health outcomes (Miller and Cafasso,1992). For male spousal caregivers, the most difficult aspect ofcaregiving is that of expressing themselves (Lopez et al., 2012).Their own emotional reactions can potentially be positioned asshameful or as a sign of being ‘crazy’, leading to avoidance asa coping strategy (Ussher and Sandoval, 2008).

There are also gender differences in social networks. Femaleidentities have been described as possibly being more strongly tiedto social networks, whereas male identities may be more stronglybound up with their partners and work (Pinquart and Sorensen,2001). As a consequence, the connection between perceived sup-port and relationship satisfaction may not be as strong for males asfor females. Social norms and the subjective perception of thequality of their relationship may determine who provides care tothe spouse with cancer or how the caregiving experience is per-ceived by each spouse (Yarry et al., 2007).

Study design, samples, instruments and cultural differences

The studies included in this review were cross-sectional andlongitudinal in design. Given that a cross-sectional design cannotexplore dynamic patterns and the direction of changes over time inthe experience of spousal caregivers (Baider et al., 2003), a needexists for longitudinal studies to explore the whole trajectory of theexperience of spousal caregivers from the time of the diagnosis ofcancer to the bereavement phase. Although ten of the studiesincluded in this review were longitudinal studies with observationtimes ranging from the time of diagnosis to 5 years (Gustavsson-Lilius et al., 2007; Langer, 2003; Langer et al., 2003, 2010;Luszczynska et al., 2007; Nijboer et al., 2000, 2001; Northouse et al.,2000; Pinquart and Duberstein, 2005; Tuinstra et al., 2004), none ofthe studies explored the whole trajectory of the effort by the cou-ples to cope with cancer.

Although ‘hidden’ morbidity’ may not be readily or objectivelyexplored in qualitative studies, qualitative research is essential togain in-depth insights into the experiences of spousal caregiversand to identify phenomena that may not be revealed in a quanti-tative study (Hagedoorn et al., 2008). No qualitative study relatingto ‘hidden morbidities’ in the experience of the spousal caregiversof cancer patients was identified in this literature search.

The studies included in this review covered different points ofassessment in the cancer trajectory, from shortly after diagnosis tocancer survivorship, but not the whole trajectory. The longitudinalstudies included in this review reported that as the disease pro-gressed, the coping style of couples changed over time, and theexperiences of spousal caregivers, such as marital satisfaction,distress, and physical functioning also changed over time(Gustavsson-Lilius et al., 2007; Langer, 2003; Langer et al., 2003,2010; Luszczynska et al., 2007; Nijboer et al., 2000, 2001;Northouse et al., 2000; Pinquart and Duberstein, 2005; Tuinstraet al., 2004). The different assessment points may affect compari-sons of the results from different studies.

These studies covered couples dealing with different stages,sites, and types of cancer. Samples included patients in Stages I/II/III of cancer, with one study specifying that no patient was ina terminal condition (Barnoy et al., 2006), while another studystated that all patients had a life expectancy of less than 6 months(Haley et al., 2003). Obviously, it would be valuable to explore

more studies focusing on couples coping with advanced-stagecancer, and following the spousal caregivers during the bereave-ment phase, as it would be of benefit to investigate the ‘hiddenmorbidities’ of spousal caregivers’ at these stages of the caregivingexperience. Therefore, studies focusing on the whole cancertrajectory will be crucial for gaining a better understanding of‘hidden morbidities’ in the experience of spouses caring for cancerpatients.

Different measurements were used in these studies to measurethe same concept or type of morbidity. For example, a variety ofmeasurements of psychological distress were used to measurestress: the Smilkstein Stress Scale (Northouse et al., 2000), BSI(Baider et al., 2003; Goldzweig et al., 2009), CES-D (Hagedoornet al., 2000, 2002; Haley et al., 2003; Tuinstra et al., 2004), PSS(Colgrove et al., 2007; Kim et al., 2006), and the Mental HealthInventory (Barnoy et al., 2006). This not only affected the researchoutcomes, but also made it difficult to compare the findings ofthese studies.

It was noteworthy that the two studies that reported that malespousal caregivers had higher levels of distress than females, andthe one study that showed that male spousal caregivers experi-enced a lower level of marital satisfaction than their female coun-terparts were conducted in a non-Western country e Israel. Thedifferences were thought to be related to cultural differences inIsrael (Baider et al., 2003; Goldzweig et al., 2009). Although it ispremature to conclude that culture is a determining factor in thedifferences in hidden morbidities and gender differences in theexperience of spousal caregivers, it is an area worthy of furtherexploration.

Consequently, it can be drawn from the above discussion thatthe inconsistent findings in this review may lie in the variations instudy design, assessment points, study sample, measurements, andculture.

Study gap identified

Of the 19 articles included in this review, three were conductedin Israel, while the other 16 were conducted in Western countries.The use of search engines turned up no study conducted in Chinafocusing on gender differences among spousal caregivers of cancerpatients.

Although many studies discussed the issue of effective com-munication between spouses resulting in an improved ability toadjust to the illness (Baider et al., 2003; Barnoy et al., 2006;Colgrove et al., 2007; Goldzweig et al., 2009; Gustavsson-Liliuset al., 2007; Hagedoorn et al., 2002; Kim et al., 2006; Kim andCarver, 2007; Langer et al., 2003, 2010; Luszczynska et al., 2007;Northouse et al., 2000), only one article specifically identified theinfluence of a correspondence in informational coping styles on thepsychological reactions of couples dealing with cancer (Barnoyet al., 2006). No systematic study on communication was foundin the context of couples coping with cancer.

Most studies included in this review focused on negative ex-periences in caregiving. There is a dearth of literature focusing onthe positive experiences of spouses caring for cancer patients. Itwould be valuable to explore such positive experiences and theircontributing factors. It has been claimed that a lack of attention tothe positive aspects of caregiving seriously skews perceptions ofcaregiving and limits the ability to fully understand caregivers(Kramer, 1997). Thus, many investigators have argued that a moreholistic view be taken by considering positive aspects of caregiving(Hudson et al., 2005; Louderback, 2000; Semiatin and O’Connor,2012).

Although the samples in different studies included patients invarious stages of cancer, no one study was found that explored the

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whole trajectory of the caregiving experience from the diagnosis ofthe cancer to the provision of bereavement care.

Limitations of this review

Literature was searched from six electronic databases that pro-vided comprehensive coverage of key nursing, medical and health-affiliated journals published in English and Chinese. However,publication bias cannot be avoided in the literature search andreview process. In addition, commentaries, editorials, literaturereviews, and conference proceedings were not included in thisreview.

Implications for interventions and recommendations for futureresearch

Highlighted here are recommendations for healthcare pro-fessionals working with cancer couples and researchers to considerin future research on hidden morbidities in the spousal caregivingof cancer patients, with special reference to gender differences.

The importance of identifying hidden morbidities in caregivingis to provide insights into areas where interventions can bedesigned to alleviate them to achieve better caregiving outcomes(Fletcher et al., 2012). Eight out of the 19 studies included in thisreview highlighted the importance and benefits of interventions forcouples coping with cancer (Baider et al., 2003; Goldzweig et al.,2009; Kim et al., 2006; Kim and Carver, 2007; Langer et al., 2003,2010; Luszczynska et al., 2007; Northouse et al., 2000). Thesestudies suggested that such interventions should start early forcouples dealing with different stages of the cancer trajectory(Northouse et al., 2000). They should involve improving empathiclistening and effective communication (Kim et al., 2006; Kim andCarver, 2007), person-specific and relationship-protective in-terventions (Langer et al., 2003, 2010), psychological interventions(Baider et al., 2003), cognitive and behavioral interventions(Goldzweig et al., 2009), and helping partners learn about eachother’s needs (Luszczynska et al., 2007). A systematic review ofinterventions focused on improving the spousal caregiving expe-rience for cancer patients is needed if evidence-based interventionsare to be developed.

There is a need to develop conceptual frameworks or models forworking with cancer couples. Having a conceptual framework willhelp to establish a systematic means to guide and promote sup-portive relationships in which both the patient and the caregiverwill benefit (Blum and Sherman, 2010). Several models wereadopted in the articles included in this review, such as a cognitive-appraisal model of stress (Northouse et al., 2000), a stress-copymodel (Colgrove et al., 2007), a stress process model (Haley et al.,2003), an adult attachment theory (Kim and Carver, 2007),a model on identity-relevant stress (Hagedoorn et al., 2002),a cognitive stress model (Nijboer et al., 2001), and the meditationalmodel of predictors of distress in cancer patients and their partners(Gustavsson-Lilius et al., 2007). However, none of the studies pro-vided a comprehensive model that covers the whole cancer tra-jectory involving both partners of a cancer couple. A modelspecifically for cancer couples will be valuable in developingstrategies to halt the development of hidden morbidities amongspousal caregivers of patients with cancer.

A mixed quantitative and qualitative study design will be val-uable if researchers are keen to attain a better understanding of thelong-term impact of caregiving on the spouses of cancer patients,including the issue of hidden morbidities, and an in-depth under-standing of the experiences of such couples. A comprehensive long-term study remains to be conducted to explore the experiences ofspousal caregivers throughout the process of dealing with cancer.

It is recommended that research be undertaken in two areas:communication and culture. With regard to communication, it iswell recognized by some of the authors of articles included in thisreview that the more effectively spouses communicated, the betterthey adjusted to the situation of cancer (Baider et al., 2003; Barnoyet al., 2006; Colgrove et al., 2007; Goldzweig et al., 2009;Gustavsson-Lilius et al., 2007; Hagedoorn et al., 2002; Kim et al.,2006; Kim and Carver, 2007; Langer et al., 2003, 2010;Luszczynska et al., 2007; Northouse et al., 2000). However, thisreview found that only one study focusing on couples’ communi-cation (Barnoy et al., 2006).

Cultural differences relating to the hidden morbidities ofspousal caregivers are another issue of concern. It was noted thatwhile most of the studies reported that female spousal caregivershad a higher level of morbidity, the two studies that reported malespousal caregivers had higher levels of distress than females anda third showing that male spousal caregivers perceived lowermarital satisfaction than their female counterparts came froma non-Western countrye Israel (Baider et al., 2003; Goldzweig et al.,2009). Although cultural differences were considered to be a factorthat may impact the caregiving experience both with regard tohidden morbidities and gender differences, no study was found inthis review that explored the impact of culture on hidden morbid-ities in caregiving. The issue of culture and communication meritsa systematic exploration in order obtain a better understanding ofhidden morbidities and the whole caregiving process, as this isa subject that is relatively under-studied (Fletcher et al., 2012).

Conclusion

This literature review revealed that spousal caregivers of cancerpatients are at a high risk of developing sub-optimal mental,physical, and social statese i.e., hiddenmorbidities. Although therewere inconsistencies of findings on gender differences related tocaregivers’ mental, and social morbidities, in general, female care-givers suffered more than male spousal caregivers of cancer pa-tients in all dimensions of sub-optimal health. Interventionprogrammes need to be developed to prevent spousal caregiversfrom suffering from hidden morbidities. Further research is neededto systematically explore hidden morbidities and gender differ-ences in the spousal caregiving experience for cancer patients,particularly, the aspects of culture and communication.

Conflict of interest

The authors have no funding or conflicts of interest to disclose.

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