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Biomedical and Psychosocial Determinants of Intrusive Recollections in Breast Cancer Survivors

Received Oct. 27, 2003; revision received June 16, 2004; accepted July 22, 2004. From the Psycho-Oncology Division, National Cancer Center Research Institute East; the Division of Adult Mental Health, National Institute of Mental Health National Center of Neurology and Psychiatry; and the Division of Breast Surgery and the Psychiatry Division, National Cancer Center Hospital East, Japan. Address correspondence and reprint requests to Dr. Uchitomi, Psycho-Oncology Division, National Cancer Center Research Institute East, Kashiwanoha 6-5-1, Kashiwa, Chiba 277-8577, Japan; yuchitom{at}east.ncc.go.jp (e-mail).

ABSTRACT

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The authors’ aim was to identify the determinants of intrusive recollections related to receiving a cancer diagnosis in women after cancer treatment. A consecutive series of breast cancer patients at 3–15 months after surgery, consisting of subjects with (N=63) and without (N=92) intrusive recollections was examined. Logistic regression analysis revealed that neuroticism, precancer intrusive recollections, and the number of cancer patients in relatives by marriage were final significant determinants, and receiving radiotherapy was an associated factor. These results suggest that biopsychosocial factors contribute to intrusive recollections and have clinical implications for the use of these characteristics in screening and early intervention.

INTRODUCTION

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A formal diagnosis of posttraumatic stress disorder (PTSD) appears to be limited to a small minority (3%–6%) of adult early-stage breast cancer survivors,^1–3 although subthreshold reports of PTSD are more common. It has been reported that the prevalence of reexperiencing the trauma, such as intrusive recollections, avoidance/numbing in response to trauma reminders, and hyperarousal varies from 11% and 37%, 4% and 11%, and 7% and 28%, respectively.^1–3 It has been indicated that the reexperiencing and intrusion symptoms of PTSD are associated with the presence of persistent depression or anxiety,^4,5 poor psychological adjustment,⁶ and poor quality of life.⁷ Furthermore, in the general population, it was reported that even patients with subthreshold PTSD, in whom the most common symptoms were reexperiencing, suffered from comorbid depression, suicidal ideation, and daily life impairment.⁸ Thus, the early evaluation and intervention of such symptoms among cancer patients may be an important component of public health efforts targeting the disclosure of cancer diagnosis and cancer treatment. Additionally, disclosure of cancer diagnosis to the patients was still taboo in rural areas in Japan; this may be a larger issue in Japan than in the U.S. and other Western countries.

Prior investigations suggest that sociodemographic variables (younger age, lower income, perceived low social support),^7,9 biomedical factors (premorbid health problems, later stage at diagnosis),^9–11 and psychological factors (neuroticism, negative life event, primarily psychiatric diagnosis, precancer trauma, and trait anxiety)^9–12 act as significant predictors in the development and severity of PTSD or PTSD symptoms in early-stage cancer survivors. In women with metastatic breast cancer, a shorter time since recurrence is predictive of intrusion and avoidance symptoms, and the size of the emotional support network is predictive of avoidance symptoms.¹³ However, the relative contribution of each of these factors to subthreshold PTSD development in early-stage cancer survivors has received little empirical attention.¹⁴ To our knowledge, no study has been conducted to examine simultaneously the effects of a broad range of sociodemographic, medical, and psychological factors on intrusive recollections—that is, one of the representative and the most frequent PTSD symptoms—in early-stage cancer survivors.

The objective of this exploratory study was to identify the determinants of intrusive recollections in breast cancer survivors. Furthermore, we expected that our study could be useful both in recommending clinical strategies for more easily evaluating our patients’ expected psychological distress and in developing appropriate supportive communication and/or intervention.

METHOD

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Subjects and Procedure
The subjects were a part of the baseline data set from a longitudinal prospective study investigating cognitive function and brain volume in breast cancer survivors who were seen consecutively in the regular follow-up outpatient clinic of the Division of Breast Surgery, National Cancer Center Hospital East, in Japan from March 1999 to February 2002. The subjects who had survived for 3 to 15 months since their surgery at the time of the investigation were selected from a list of records of breast cancer surgery. Women were included in the study if they met the following criteria: 1) histologically confirmed breast cancer; 2) ages 18 to 58 years, to avoid potential aging effects on cognitive function; 3) no double cancer and no apparent evidence of residual, metastasis, or recurrence of cancer when checked by an attending oncologist; 4) no current active cancer treatment, such as surgery, intravenous chemotherapy, or radiotherapy (except for tamoxifen therapy); 5) no history of substance abuse or dependence; 6) no history of any neurological disorder or traumatic brain injury with loss of consciousness, in order to avoid potential organic mental disorder; 7) not suffering from currently treated psychiatric illness or cognitive impairment (less than 24 on the Mini-Mental State Examination;^15,16 and 8) physical condition was not so severe that they could not participate in an interview and complete a questionnaire. The institutional review board and ethics committee of the National Cancer Center approved the study. After a complete disclosure of the study’s purpose to the subjects, written informed consent was obtained.

After a potential subject was identified by research assistants, an investigator reviewed her record to confirm her eligibility. With the permission of each patient’s physician, two psychiatrists contacted and informed the patients about the purpose of the study. The entire primary investigation set, including the Structured Clinical Interview for DSM-IV (SCID),¹⁷ magnetic resonance imaging (MRI), the Wechsler Memory Scale—Revised (WMS-R), and several questionnaires took from 2.5 to 3 hours to complete. The subjects were given a gift voucher (1,000 yen) for their participation.

Of the 642 candidates, 340 subjects met the eligibility criteria. The others were excluded because they were over 59 years old (N=208); had double cancer, metastasis, or recurrence of cancer (N=35); were currently undergoing intensive psychiatric treatment (N=14); had a history of head injury (N=2), brain tumor (N=1), epilepsy (N=2), or poliomyelitis (N=1); or were currently undergoing anticancer treatment during the investigation period (N=39). Of the remaining 340 eligible subjects, 155 (46%) participated, 21 could not be contacted during the investigation period, and 164 refused to complete the primary investigation set, including MRI and the WMS-R. The participation rate of less than 50% was the biggest limitation of the study. Most women had a relatively good performance status, as defined by the criteria of the Eastern Cooperative Oncology Group (performance status=0, 70%; performance status=1, 29%; missing data, 1%). There were no significant differences between the participants (N=155) and the nonparticipants (N=185) in age, clinical stage, and type of surgery, but the nonparticipants may have consisted of more symptomatic women, especially avoiders, who may have had PTSD or another symptom profile.

Psychiatric Assessment
The participants completed the SCID, as administered by trained psychiatrists (Y.M., Y.S.), to assess the current and past PTSD diagnosis and/or each cluster symptom (reexperiencing, avoidance/numbing, hyperarousal) with regard to cancer and noncancer traumatic events. In the cancer-related PTSD module, the designated criterion A stressor event was "the disclosure of your cancer diagnosis." The subjects were required to answer all of the DSM-IV symptoms (17 items) from which we were able to make the PTSD diagnosis and the subthreshold PTSD diagnosis. The subjects were required to have at least one item, such as intrusive recollections in criterion B (5 items) to qualify as having reexperiencing, at least three items in criterion C (7 items) to qualify as having avoidance/numbing, and at least two items in criterion D (5 items) to qualify as having hyperarousal. The definition of cancer-related PTSD was PTSD related to the patient’s experience of the disclosure of cancer diagnosis.

We defined cancer-related intrusive recollections on the basis of a modification of criterion B1 of the PTSD module in DSM-IV as "recurrent and intrusive distressing recollections of the cancer-related event, including images, thoughts, or perceptions." We used sentence F42 from the criteria for PTSD in the administration booklet of the SCID.¹⁷ The subjects were asked, "During your life, from the day when you were diagnosed as having breast cancer to date, did you think about disclosure of your cancer diagnosis when you did not want to, or did thoughts about disclosure of your cancer diagnosis come to you suddenly when you did not want them to?" According to the SCID, each subject’s answer was classified into "absent and subthreshold" or "overthreshold." When the subject said that she did not have a chance to recall the event of receiving the cancer diagnosis at all, we coded it as "absent." When each subject’s recollections of the event met the following entire condition, we judged it "overthreshold"; that is 1) unexpected, 2) recurrent, 3) intrusive, 4) accompanied with unpleasant emotion, 5) lasting at least 1 month and being present in the past 4 weeks. However, we did not particularly evaluate the severity of intrusive recollections. Items 1, 10, and 11 of the Impact of Event Scale¹⁸ were almost equal to the definition of intrusive recollections; therefore, we were compelled to substitute the summing of these 3 items to arrive at the degree of intrusive recollections within the past week. Each item was rated on a scale with ratings of 0, 1, 3, and 5. The scores ranged between 0 and 15, with higher scores indicating frequent experience of cancer-related intrusive recollections.

A random sample of 30 cases assessed by two raters (one conducting the interview and one observing) was used to assess interrater reliability. The interrater agreement (kappa) values for the current diagnosis of intrusive recollections and PTSD were all 1.0. Ratings for each of the 17 individual items of PTSD were also reliable, with kappa values ranging from 0.81 to 1.00.

Patient Background
To identify the determinants of intrusive recollections, demographic factors (age at surgery, time elapsed after surgery, education, employment status, marital status, premorbid household size) and social factors (presence of children, having economically dependent children, having unmarried children, having children with health problems, number of confidants, number of cancer patient in relatives by blood and by marriage) were investigated by structured interview. In Japan, married men and women still maintain a close relationship with their parents and continue to adhere to values such as respecting and looking after the husband’s parents.¹⁹ Furthermore, the Japanese traditional family system is based on the assumption that marriages are for the family rather than for individual love.²⁰ Therefore, we assessed the family history of cancer by distinguishing relatives by marriages from relatives by blood. Biomedical factors (menstrual state, Union Internationale Contre le Cancer clinical stage, type of surgery, existence of axially lymph node metastasis, chemotherapy, radiotherapy, and tamoxifen use) were obtained from the patients’ medical records. Anxiety was measured by the trait anxiety subscale scores from the State-Trait Anxiety Inventory.^21,22 Personality traits were measured with two scales from the Eysenck Personality Questionnaire—Revised^23,24: the extroversion and neuroticism scales, each with 12 dichotomous items. The concept of neuroticism refers to a general emotional overresponsiveness and liability to develop neurotic disorders under stress. The concept of extroversion refers to outgoing, sociable, uninhibited, impulsive inclinations.²³ To obtain psychiatric information about precancer (before cancer diagnosis) major depressive disorder, prior trauma (any noncancer traumatic event before cancer diagnosis), precancer intrusive recollections, and precancer onset of PTSD related to prior trauma, the same psychiatrists conducted the SCID. The patients’ characteristics are summarized in Table 1.

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TABLE 1. Demographic and Clinical Characteristics of 155 Breast Cancer Survivors Who Completed the Study

Prevalence of Intrusive Recollections and PTSD Symptoms
The subjects reported an average of 1.9 (SD=2.5) current cancer-related PTSD symptoms (range=0–16) on the SCID and 4.2 (SD=3.6) past cancer-related PTSD symptoms (range=0–16). Among the total participants, 105 subjects (67.7%) met the postcancer (anytime since the cancer diagnosis) criterion for intrusive recollections, and 63 (40.6%) met the criterion for current (still active) intrusive recollections. The most common cluster symptom was reexperiencing (current: N=69, 44.5%; past: N=112, 72.3%), followed by avoidance/numbing (current: N=17, 11.0%; past: N=46, 29.7%) and hyperarousal (current: N=14, 9.0%; past: N=52, 33.5%). Twenty-three subjects (14.8%) met the postcancer criterion for cancer-related PTSD, and 15 subjects (9.7%) met the criterion for a past history of precancer onset of PTSD. Only six subjects (3.9%) met the criterion for current cancer-related PTSD, and three subjects (1.9%) met the criterion for current noncancer PTSD. Additionally, 27 subjects (17.4%) had past major depressive disorder, but no one met the criterion for current major depressive disorder.

Statistical Analysis
To explore the potential determinants of current intrusive recollections (presence or absence), demographic, sociological, biomedical, psychological, and psychiatric variables were included the preliminary bivariate analysis. We tested intergroup differences in categorical, nonparametric, and continuous variables with the chi-square test (or Fisher’s exact test), Wilcoxon’s two-sample test, and Student’s t test for unpaired data, respectively. To identify the final determinants, variables with a p value of less than 0.25 in the bivariate analysis were carefully entered into a multivariate logistic regression model as independent variables. When a variable was significantly correlated (r>0.40) to other similar independent variables, we selected one variable for examining the determinants of intrusive recollections. All p values reported are two-tailed. In all statistical evaluation, p values of 0.05 or less were considered indicative of significant differences. All data analyses were performed with SPSS version 11.01 J for Windows (SPSS Japan Institute Inc., Tokyo).

RESULTS

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The results of the bivariate analysis are shown in Table 2. Because the trait anxiety score was significantly associated with the neuroticism score (Pearson’s r=0.55, p<0.01), only neuroticism was entered into the multivariate model. Because the incidence of precancer intrusive recollections was associated with a past history of precancer onset of PTSD (²=12.0, df=1, p<0.01), only the incidence of precancer intrusive recollections was entered into the multivariate model. Lymph node metastasis was significantly associated with chemotherapy (²=43.3, df=1, p<0.01) and tamoxifen use (²=19.2, df=1, p<0.01). Chemotherapy was also associated with tamoxifen use (²=6.36, df=1, p=0.01). Therefore, we did not enter either chemotherapy or tamoxifen use, but we did enter lymph node metastasis. Finally, time elapsed after surgery, menopausal state, lymph node metastasis, radiotherapy, neuroticism, the number of prior traumas, precancer intrusive recollections, the number of cancer patients in relatives by blood, and the number of cancer patients in relatives by marriage were entered into the logistic regression analysis. The results of the multivariate analysis are shown in Table 3. Neuroticism, precancer intrusive recollections, the number of cancer patients in relatives by marriage, and radiotherapy were final significant determinants.

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TABLE 2. Bivariate Analyses of Predictive Factors for Intrusive Recollections in Breast Cancer Survivors

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TABLE 3. Multiple Logistic Regression Analysis of Predictive Factors for Intrusive Recollections in 155 Breast Cancer Survivors

Additionally, the same independent variables were also entered into the multiple linear regression analysis to examine the determinants of degree of cancer-related recollections. It was also revealed that neuroticism (standardized coefficient=0.40, t=5.2, df=8, p<0.01), precancer intrusive recollections (standardized coefficient=0.18, t=2.0, df=8, p<0.05), and the number of cancer patients in relatives by marriage (standardized coefficient=0.16, t=2.2, df=8, p=0.03) were significant determinants.

DISCUSSION

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The central findings of this exploratory cross-sectional study were that multidimensional factors, that is, biomedical (receiving radiotherapy), psychological (neuroticism, precancer intrusive recollections), and social (number of cancer patients in relatives by marriage) characteristics, were associated with cancer-related intrusive recollections at the early survival stage. This is partly consistent with previous reports on cancer patients with PTSD, but some new factors have been detected.

Having precancer intrusive recollections about prior trauma was a strong determinant of cancer-related intrusive recollections. It is consistent with previous studies showing a relationship between prior trauma history and current PTSD symptoms in breast cancer survivors at an acute survival stage.^9,11 A psychiatric diagnosis might be less powerful as a predictor when trauma history was controlled, however, suggesting that previous trauma is a risk factor for precancer intrusive recollections, and these, in turn, increase vulnerability for more negative outcomes when later stressors occur. Our finding, which is also compatible with the findings in two meta-analyses of predictors for PTSD in adults,^25,26 suggests the importance of assessing trauma exposure history in studies that attempt to examine how earlier vulnerability, defined by the presence of precancer intrusive recollections, relates to current stressors, such as the disclosure of cancer diagnosis.

Neuroticism was identified as a determinant of the intrusive recollections. Because it was consistent with an earlier study predicting PTSD symptoms in cancer survivors,¹⁰ victims of road traffic accidents,²⁷ and patients with postmyocardial infarction,²⁸ it might not be a new finding in the trauma literature. In an urban population of young adults, it was indicated that neuroticism is one of the significant risk factors for PTSD after exposure to traumatic events²⁹ and that those with high neuroticism are more likely than others to be exposed to traumatic events.³⁰ According to Eysenck et al.,²³ "The typical high neuroticism scorer is an anxious, worrying individual, moody and frequently depressed....He is overly emotional, reacting too strongly to all sorts of stimuli, and finding it difficult to get back to an even keel after each emotionally arousing experience" (e.g., cancer diagnosis). Neuroticism may represent an alternative trajectory to the normal process of adaptation and recovery after traumatic events. Bramsen et al.³¹ revealed that predevelopment personality traits of negativism, that is, a negative, dissatisfied, and hostile attitude toward others and life in general, was the second important predictor of the severity of PTSD symptoms in individuals involved in military peacekeeping activities. Although the use of postcancer personality measures may be problematic as a reliable representation of pretrauma personality, based upon this assumption, intrusive recollections could be expected in these cancer patients.

Another risk factor identified as a determinant of the intrusive recollections was the number of cancer patients in relatives by marriage. It was an intriguing finding because having cancer patients in relatives by blood might seem to have the most psychological impact. Because we only assessed the number of cancer patients in relatives by blood or marriage as the family history of cancer, we could not discuss the qualitative aspect of this finding, such as the nature of the family relationship or function. Of importance, in the generation of this study group (median age: 48 years), there were strong Japanese legacies from the past, including the social expectation that the role of married women was to be good wives and wise mothers and to care for the husband’s parents.²⁰ Therefore, cancer patients in relatives by marriage might be another cause of distress. Further study is needed to clarify this finding.

The finding that radiotherapy in the past acted as a protective factor against the intrusive recollections is intriguing. It is consistent with an earlier study by Tjemsland et al.¹⁰ that examined the frequency and determinants of PTSD symptoms in breast cancer patients at intervals 1 day before surgery, 6 weeks after surgery, and 1 year postoperatively with a self-report questionnaire. They found that patients receiving adjuvant radiotherapy reported decreased intrusion compared to other patients. Patients may be confronted with realistically safe cancer experiences by frequent hospital visits related to radiotherapy, and it may offer patients an enhanced sense of control over an uncontrollable process as well as a perceived prevention of the threat to their lives. It is reported that affiliation among patients of similar emotional status has been found to reduce anxiety,³² and this may play a role in these patients spending time together while receiving their treatment. Further investigations targeting receiving radiotherapy on PTSD symptoms in cancer survivors is needed.

Any interpretation of our results should take into account the following limitations. First, with regard to participation in the population studied, our response rate (46%) was low. Some of the refusals were due to practical reasons, that is, refusal to undergo an MRI or the WMS-R test, but others may have been made by more symptomatic women, especially avoiders, who may have had PTSD or other symptom profiles, since Green et al.² reported that 12% of breast cancer survivors had a current DSM diagnosis. Kessler et al.³³ demonstrated that PTSD was strongly comorbid with other lifetime axis I disorders, especially major depressive disorder (48%) or substance use disorder (27%–52%) in the general population. Marshall et al.⁸ showed that subthreshold PTSD was associated with a significantly higher rate of comorbid major depressive disorder and risk for current suicidal ideation in the general population. Second, the cross-sectional design of the study leaves the findings open to questions concerning the potential effects of retrospective bias. Clearly, a prospective, longitudinal study in which the determinants are measured before the disclosure of cancer diagnosis is more likely to guard against the possibility that psychological characteristics produced by the diagnosis might have influenced the participants’ reports about possible factors, such as personality traits. Because a 2-year follow-up examination of this cohort is already underway in our institute, it may be able to explain some causality. Third, the level of functional disability in cancer patients with intrusive recollections was unclear. Further study is needed to investigate the implication of intrusive recollections on daily life activity. Fourth, data on family history of cancer were gathered in interviews with the participants and were thus subjected to the limitations that characterize all informant-based family history data. Compared with direct interviews with relatives, informants’ data may lead to underestimation of the number of cancer patients in relatives. Although a general qualification on the accuracy of these data are in order, the actual effect on the results might be relatively small. In addition, because we did not assess the nature of the relationship between participants and their relatives with a cancer diagnosis, the implication of the finding is unknown. However, this finding may suggest a clinical implication for the extended family model in Japan, South Korea, and other Asian countries. Further study is needed to clarify this finding to avoid the charge of alpha error. Fifth, there was a sampling bias because the results were obtained from only one institution, which was a teaching hospital cancer center. Despite these limitations, the present study adds interesting information to the growing literature on the psychological impact of cancer and cancer diagnosis.

The implication of this study for clinical practice is that screening for prior trauma history, anxiety traits, and relevant family history would be helpful to address the high risk of developing intrusive recollections posttreatment. Indeed, it has been demonstrated that rapid screening for psychological problems with a self-report measure or checklist was useful to detect psychological distress in cancer patients.^34–36

ACKNOWLEDGMENTS

 
Supported in part by a grant from the Japanese Ministry of Health, Labor, and Welfare (Second-Term Comprehensive 10-Year Strategy for Cancer Control and Research), a grant from the Japan Society for the Promotion of Science (Grant-in-Aid for Scientific Research B KAKENHI 13470100), and a grant from the Japanese Ministry of Education, Culture, Science, and Technology (Target-Oriented Brain Science Program). Drs. Matsuoka, Inagaki, and Sugawara are ex-awardees of a Research Resident Fellowship from the Foundation for Promotion of Cancer Research in Japan.

The authors thank Ms. Nobue Taguchi and Yuko Kojima for research assistance; and Drs. Motoko Matsuoka, Mitsue Nagamine, Yoshiharu Kim, Hiroe Itoh, and Yuko Miyake for their comments on an earlier version of this article.

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