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Page 1: Pre-loss symptoms related to risk of complicated grief in caregivers of terminally ill cancer patients

Brief Report

Pre-loss symptoms related to risk of complicated grief in caregiversof terminally ill cancer patients

Maria Giulia Nanni a,n, Bruno Biancosino a,b, Luigi Grassi a

a Section of Psychiatry, Department of Biomedical and Specialty Surgical Sciences, University of Ferrara, Corso Giovecca 203, 44121 Ferrara, Italyb Integrated Department of Mental Health and Drug Abuse, NHS Local Health Agency, Ferrara, Italy

a r t i c l e i n f o

Article history:Received 23 August 2013Received in revised form12 December 2013Accepted 13 December 2013Available online 30 December 2013

Keywords:BereavementGriefComplicated grief

a b s t r a c t

Purpose: A number of studies have underlined a 10–20% prevalence of complicated grief (CG) amongcaregivers of cancer patients. The study aimed at examining the relationship between pre-loss criteria forCG and post-loss diagnosis of CG and at evaluating the validity and factor structure of a predictive tool,the Inventory of Complicated Grief (ICG), in order to identify the risk of developing CG in a sample ofItalian caregivers.Methods: Sixty family members of terminally ill patients admitted to hospice and receiving a PalliativePrognostic Score (PaP) predictive 30 day survival time o30% completed the Pre-Death ICG (ICG-PL) (T0).Family members were met again 6 months after the death of their loved one (T1) and submitted to theinterview for Complicated Grief (Post-loss interview-PLI).Results: Caseness for CG was shown in 18.3% of caregivers at T1. ICG-PL score (T0) were higher amongthose who developed CG at T1 than non-cases. A cut off score Z49 on the ICG-PL (AUC¼0.98)maximized sensitivity (92%) and specificity (98%) on caseness at T1. Pre-loss criteria related to traumaticdistress, separation distress and emotional symptoms in general were significantly related to a post-lossdiagnosis of CG, while no effect was shown on duration of pre-loss distress.Conclusions: The use of short screening tools, like the ICG-PL, may help health care professionals toidentify subjects at risk for CG.

& 2014 Elsevier B.V. All rights reserved.

1. Introduction

Over last 20 years, several studies have concentrated attentionto complications of grief and bereavement (Zhang et al., 2006;Hudson et al., 2012). A syndrome characterized by emotional,behavioral and cognitive symptoms (e.g. yearning, searching,detachment, numbness, bitterness, emptiness, and lost sense oftrust and control) has been identified and initially named ascomplicated grief (CG), then traumatic grief (TG), and, morerecently, prolonged grief (PG) (Prigerson et al., 2009).1 A bulk ofdata is now available on CG as a distinct entity from otherpsychiatric disorders, such as anxiety, depression, post-traumaticstress disorder and adult separation anxiety (Prigerson et al.,1995a; Boelen and van den Bout, 2005; Bonanno et al., 2007;Golden and Dalgleish, 2010; Boelen et al., 2010; Boelen, 2013). CGhas also been shown to predict long-term functioning impair-ments, reduction of quality of life, risk for mental disorders andsuicidality, and physical health problems (e.g. hypertension, hearth

disorders) (Prigerson et al., 1997; Ott, 2003; Latham and Prigerson,2004; Boelen and Prigerson, 2007).

In order to study the prevalence, possible risk factors, out-comes, and prevention and treatment of CG (Prigerson et al., 1999;Jacobs et al., 2000; Forstmeier and Maercker, 2007), diagnosticcriteria were developed and a diagnosis of PG disorder has beenproposed for the DSM-5 (Prigerson et al., 2008; Kaplow et al.,2012).2 Furthermore, several instruments have been developed toassess CG, including the Inventory of Complicated Grief (ICG). This,as a measure of a single underlying construct, has proved to havehigh internal consistency and test-retest reliability in many studies(Prigerson et al., 1995b, 1996; Chiu et al., 2010; Guildin et al., 2011;Guldin et al., 2012). Prigerson et al. (1999) have suggested that adiagnosis of CG is made if certain criteria are met, specificallycriterion A (i.e. symptoms of “separation distress”), criterion B(“traumatic distress”), criterion C (duration of symptoms) andcriterion D (presence of dysfunctioning).

Less data are available on the relationship between pre-loss CGand post-loss CG. With regard to this, a pre-loss version of theICG, the Pre-Death Inventory of Complicated Grief (ICG-PL), was

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Journal of Affective Disorders

0165-0327/$ - see front matter & 2014 Elsevier B.V. All rights reserved.http://dx.doi.org/10.1016/j.jad.2013.12.023

n Corresponding author. Tel.: þ39 0532 236409; fax: þ30 0532 212240.E-mail address: [email protected] (M.G. Nanni).1 Since in the study we used the Italian version of a tool defined as Inventory

for Complicated Grief we maintained the term “complicated grief” (CG) throughoutthe paper.

2 In DSM-5 Persistent Complex Bereavement Disorder has been introduced as aCondition for Further Study.

Journal of Affective Disorders 160 (2014) 87–91

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developed as a possible screening tool for those at risk for CG afterloss. Tomarken et al. (2008) administered the ICG-PL to 248caregivers of terminally ill cancer patients, showing that a youngerage, a pessimistic thinking and stressful life events, were riskfactors for pre-loss CG, but without providing data on theprevalence of post-loss CG. A more recent Australian prospectivestudy found that, among 301 caregivers of terminally ill patients,CG symptoms on entry to palliative care were a strong predictor ofboth CG symptoms and CG disorder at 6 and 12 months. Greaterbereavement dependency, a spousal relationship to the patient,greater impact of caring on schedule, poor family functioning, andlow levels of optimism also were risk factors for CG symptoms(Thomas et al., 2013).

A very few data are available in Italy with regard to this area ofresearch and, specifically, on the use of the ICG to predict CG infamily caregivers in palliative care. The ICG was used by Pini et al.(2012) in a general retrospective study of adult psychiatric out-patients with a diagnosis of DSM-IV mood or anxiety disorders.They found that CG (23% rate) was associated with adult separa-tion anxiety disorder (ASAD). In a different retrospective study of116 bereaved patients, Dell0osso et al. (2012), also by using the ICG,showed that adult anxiety separation was higher only in thosewith CG and PTSD, but not in those with CG alone. None of the twostudies were carried out, however, in palliative care settings. In theonly Italian study carried out in this setting, Lai et al. (2013) foundthat female gender and difficulty in describing feelings wereassociated with CG among caregivers of terminally ill patients.

Given the substantial lack of prospective data on pre-lossconditions as possible predictive factors of post-loss CG and therepeatedly underlined need to explore CG and its risk factors(Shear et al., 2013), the aims of the present study were (i) toprospectively evaluate the role of pre-death CG in predicting CGafter loss in caregivers of terminally ill cancer patients, (ii) and toevaluate the applicability and the validity of the Italian version ofthe ICG in a Italian population, in order to confirm its factorstructure.

2. Methods

The study was carried out, during a period of one year, in the onlyhospice available in Ferrara, Northern-East Italy. This is a 12-bed unitlinked to the NHS Local Health Agency that, in agreement with the

palliative care philosophy, provides personalized interventionsaimed at improving the quality of life for the terminally ill patientsand their families. Most patients admitted are affected by cancer andthe mission of the unit is to relieve physical, emotional and spiritualsuffering, and to promote the dignity of the terminally ill persons.The study was introduced as part of the assessment routinely donein the unit and was approved by the Ethics Committee of the localinstitutions.

Prediction of survival time (in weeks) of the patients wasevaluated by using the Palliative Prognostic Score (PaP score)(Pirovano et al., 1999). This is a valid predictive tool (Maltoniet al., 1999; Glare et al., 2004; Tarumi et al., 2011), consisting of analgorithm based on the Karnofsky Performance Scale and fiveother criteria (i.e., dyspnea, anorexia, clinical prediction of survivalin weeks, total white blood cells, lymphocyte percentage) whichcreates three risk groups for survival: group A, with a predictive 30day survival time 470%; group B, with a predictive 30 day survivaltime 30–70%; group C, with a predictive 30 day survival timeo30%. Caregivers of patients included in group C were screenedfor inclusion in the study. Each caregiver was individually met inthe hospice by one of the authors who explained the aims of thestudy and obtained a written informed consent. Sociodemographicdata with information including the degree of relationship withthe patient and if caregiver lives alone or with other memberswere also collected.

2.1. Assessment

2.1.1. Pre-loss assessmentThe ICG-PL (Prigerson, personal communication) was adminis-

tered to each caregiver. The ICG-PL is a 13-item questionnairederived from a longer version of the ICG(Prigerson et al., 1995b),investigating caregivers0 mood and feelings during the terminallyill of their loved one in the last month (e.g., I feel like I havebecome numb since _____ became so seriously ill; I feel that lifewould be empty or meaningless without _____ being healthy).Each item is rated on 1–5 Likert scale, while a further item (item 14)investigates the length of caregiver0s distress. A possible syndromallevel of CG is given if at least 3 of 4 items (items 1, 2, 3, and 11) havea score Z4 (criterion 1; separation distress); at least 4 out of 8 items(items 4, 5, 6, 7, 8, 9, 10, and 12) have a scoreZ4 (criterion 2;traumatic distress); duration of distress is 42 months (criterion 3);and item 13 has a score Z4 (criterion 4; social, occupational or other

Table 1Criteria for Complicated Grief (from Prigerson et al.).

Criterion A 1: Event CriterionDeath of a significant other, the respondent should be bereaved

Criterion A2: Separation DistressA2.1: Experienced intrusive preoccupations about the deathA2.2: Felt intense longing and yearning for the deceasedA2.3: Felt intensely drawn to places and things associated with the deceasedA2.4: Felt intensely lonely

Criterion B: Traumatic DistressB1. Tried to avoid reminders that the person is gone (e.g., avoid thoughts, feelings, activities, people, places)B2. Felt like the future holds no meaning or purpose without the deceasedB3. Felt numb, detached from others, and an absence of emotional responsivenessB4. Felt stunned, dazed, or shocked over _________0s deathB5. Felt disbelief over ______0s deathB6. Felt that life is empty or meaningless without ______?B7. Felt unable to imagine life being fulfilling without ______?B8. Felt that a part of yourself died along with ______?B9. Felt that the death has changed your view of the world (eg., lost sense of security, trust, or control)?B10. Felt pain in the same area of your body, some of the same symptoms, or assumed any of the behaviors or characteristics of the deceasedB11. Felt excessive anger, irritability or bitterness about ________0s death

Criterion C: ImpairmentDisturbance causes marked and persistent dysfunction in social, occupational, or other important domains

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areas of functioning impairment). The sum of the items yields a totalICG score.

2.1.2. Post-loss assessmentSix months after the death of their loved one, each caregiver

was contacted by the same interviewer and met at his/her home,where the ICG-Structured Clinical Interview (ICG-SCI) was admi-nistered. The ICG-SCI includes the 17 consensus criteria itemsrequired for a diagnosis of CG (Prigerson et al., 1999), namely eventof loss (criterion A1), separation distress (criterion A2¼ foursymptoms; criterion met if 3 of 4 items are present), traumaticdistress (criterion B¼11 symptoms; criterion met if 6 of 11 itemsare present), and impairment (criterion C¼1 item), with a diag-nosis of CG made if all criteria A, B and Care met (Table 1).

2.2. Statistical analysis

Data analysis comprised bivariate statistics (Pearson correlationcoefficients, Student t-test, χ2-test) when appropriate. Cronbach0sα coefficient and factorial analysis were employed to examine thestructure of the ICG. Receiving Operating Characteristics (ROC)analysis was also used to determine sensitivity and specificity ofPre-loss ICG scores in distinguishing CG “cases” and “non-cases”post-loss. The Statistical Package for Social Sciences (SPSS) wasused.

3. Results

During the study period, 167 cancer patients in an advancedstage of illness were admitted to the Hospice. Of these, 76 withcancer at different sites (lung n¼25, 32.9%; gastrointestinal n¼21,27.6%, other n¼30, 39.5%) belonged to the PaP score C-risk groupand had 76 caregivers eligible to be part of the study. Sevencaregivers (9.2%) were not available for the imminent death oftheir loved ones, 9 (11.8%) refused to participate, leaving60 subjects (78.9%) as the study sample. Socio-demographiccharacteristics of the sample are presented in Table 2. There were45 females (75%) and 15 males (25%) (age range: 29–81 years;mean 60.36712.08 years; education 10.3374.18 years). Thirty(50%) caregivers lived alone and 50% lived with other members.Thirty-nine (65%) caregivers were spouses, two (3.3%) were sons/daughters, 2 (3.3%) were brothers/sisters, and 17 (27.3%) wereother parents/family members.

3.1. Pre-loss data

In agreement with the original data (Prigerson et al., 1995b),preliminary factor analysis identified three principal factors (itemloading 40.7), with factor 1 including symptoms related to“traumatic distress” (items 1, 4, 5, 7, 10, 11, 12, and 13) andexplaining 53.83% of the variance; factor 2 including items relatedto “separation distress” (items 3, 6, and 8) and explaining 9.58% ofthe variance; factor 3 including items regarding other emotionalsymptoms (items 2 and 9), explaining a further 7.72% of thevariance. Cronbach0s alpha coefficient of the ICG was 0.92. Spousesreported higher Pre-loss ICG scores than other family caregivers(son/daughter; other members). No difference was found accord-ing to the variable “living alone” (t¼1.36, p¼ns) and age (r¼0.19,p¼ns).

3.2. Post-loss data

At post-loss interview (PLI), 11 caregivers (18.3%) met thecriteria for CG. The pre-loss ICG-total score was higher amongCG (54.2774.22) in comparison with non-CG caregivers(32.61710.33) (t¼6.78; po0.001). By using ROC analysis, pre-loss ICG scores showed an Area Under the Curve (AUC) of 0.98,with a score of Z49 on ICG maximizing sensitivity (92%) andspecificity (98%) on post-loss diagnosis of CG, as measured by theICG-SCI (Fig. 1). Pre-loss criterion 1 (χ2¼22.98, df 1, p¼0.001),2 (χ2¼22.87, df 1, p¼0.001), 4 (χ2¼35.09, df 1, p¼0.001), and5 (χ2¼50.28, df 1, p¼0.001) were significantly related to a post-loss diagnosis of CG, while no effect was shown on criterion 3(χ2¼2.7, df l, p¼ns).

4. Discussion

To our knowledge, this is the first Italian study prospectivelyexamining the application of the short version of the ICG, amongstcaregivers of terminally ill cancer patients in order to predict post-loss CG.

A first result was that almost one out of five caregivers showedsymptoms meeting the criteria for a diagnosis of CG. This is in linewith other studies (Hudson et al., 2012; Brintzenhofe-Szoc et al.,1999; Prigerson et al., 2003) suggesting that monitoring the

Table 2Socio-demographic characteristics.

Complicated Grief Non-cases χ² P

Freq. % Freq. %

SexMale 1 9.10 14 28.60 1.81 0.16Female 10 90.90 35 71.40Living aloneYes 5 45.50 25 51.00 0.11 0.50No 6 54.50 24 49.00RelationshipHusb./Wife 8 13.3 31 51.7 11.32 0.05Parent 1 1.7 13 21.7

Mean DS Mean DS t P

EducationStudy years 9 3.40 10.63 4.31 �1.17 0.22AgeYears 63 12.68 49 12.00 0.79 0.73

Fig. 1. Area Under the Curve at ROC analysis.

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process of grief is extremely important in order to refer thoseshowing CG to proper services.

A second result was that the ICG, in its short and pre-loss form,when applied in the Italian cultural context, was a valid instru-ment. Factorial analysis confirmed that CG is characterized by thedimensions of “traumatic distress” (e.g., numbness, disbelief,anger, insecurity), “separation distress” (e.g., longing and search-ing for the deceased) and emotional symptoms, (e.g., yearning,being bitter over the relative0s illness). This is in agreement withPrigerson et al. (1999) who indicated that “separation distress” and“traumatic distress” are two of the four main criteria of CG.

A further finding regards the usefulness of the pre-loss ICG inidentifying caregivers who developed CG after the loss of theirloved ones. Higher ICG pre-loss scores differentiated subjects inthe CG group with respect to “non-cases” after loss. A positiveresponse (score Z4) on most pre-loss ICG items, includingemotional distress, traumatic distress, other emotional symptoms,was also associated to a higher risk of post-loss CG. With respect tothis, a cut-off score of 49 on the pre-loss ICG maximized sensitivityand specificity in predicting individuals who, 6 months after theloss of their loved ones, met the criteria for CG.

Major limitations should be mentioned. The small number ofsubjects cannot allow us to generalize the results. Multicentrestudies, involving larger samples are necessary to confirm the datapresented here. Second, attention was concentrated on pre-lossclinical symptoms of CG, without taking into consideration themany other possible variables (e.g. family functioning, familysupport, level of general distress, and history of mood co-morbid-ity) that have been found to be risk factor for CG in other studies(Chiu et al., 2010; Thomas et al., 2013; Fujisawa et al., 2010). Third,we applied only the ICG and the ICG structured interview, whilethe conceptualization and the criteria for what is now calledProlonged Grief disorder (Prigerson et al., 2009) are not comple-tely overlapping with those of CG (Prigerson et al., 2008;Wakefield, 2012; Maercker and Lalor, 2012). Further research usingmore recent and specific criteria can add information about thisissue. Lastly, the study concentrated attention to the specificsetting of palliative care (hospice) for cancer patients and theoutcome of bereavement in their caregivers, reducing the possi-bility to generalize our results. More studies should be carried outin other settings, including hospital settings and the community.

In spite of these limitations, a short instrument such as the ICGshowed to be useful in predicting subjects who developed post-loss CG, confirming the need for a regular assessment of symptomsantedating the loss of one0s loved one. Since caring for terminallyill people is a source of emotional burden for the family that canmake grief extremely difficult (Grassi, 2007; Chentsova-Duttonet al., 2000; Holtslander, 2008; Stajduhar et al., 2010), applicationof screening instruments is recommended.

Role of funding sourceAuthors have not developed an open access policy for the research, not

applicable.

Conflict of interestAll authors declare that they have no conflicts of interest.

AcknowledgmentsThe authors wish to express their gratitude to Holly Prigerson, Ph.D. for her

help and support in conceiving the study and providing the instruments. TheUniversity of Ferrara and the staff are also gratefully acknowledged.

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