Introduction

Breast cancer is the leading cause of cancer incidence, disability, and mortality among women [1]. Overall, incidence of breast cancer was stable from 1998 to 2011 while overall mortality and morbidity have been declining, thanks to earlier detection and improvements in treatment modalities [2]. The increase in the number of surviving breast cancer cases might lead to worsening psychological problems, especially depression and anxiety. Initially, diagnosis period and having metastatic disease can cause distress. Subsequently, treatments like surgery, chemotherapy, radiotherapy, and hormone therapy can lead to symptoms of depression and anxiety, resulting in impairment of quality of life, as well as having negative effects on the treatment process and follow-up, thereby potentially generating a negative feedback effect [3,4,5]. Symptoms of depression were found to occur in 3–55% of breast cancer patients, while anxiety was found in 18–33% [6]. These were often encountered in the first 6 months after diagnosis [7]. Of these patients, 20–30% experienced distress even years after following the initial treatment [8,9,10].

Various risk factors and parameters have been identified for post-treatment depression and anxiety in breast cancer survivors. These include a range of patient-related factors such as age, marital status, educational level, menopausal status, comorbidities, social support, and psychiatric history. In addition, disease-related factors including the cancer subtype, treatment modalities (surgery and/or chemotherapy and/or radiotherapy and/or hormone therapy), and possible post-treatment symptoms such as pain and hormonal side effects may be relevant to this issue [11,12,13].

“Illness perception” was proposed to be one of the significant causes of psychological distress in cancer patients in the early follow-up period [14, 15]. Additionally, patients with different cancer types including breast cancer survivors who had completed their therapy within 6 months were evaluated for “illness perception” and this was not found to differ among cancer types [16]. However, it is not known whether this would get better with longer time. In the present cross-sectional study, we aimed to determine the potential impact of “illness perception” on anxiety and depression scores in early-stage breast cancer survivors who were followed for 6 months to12 years after the completion of treatment.

Study design features and methods

Hypothesis

We hypothesized that “illness perception” is an important parameter on anxiety and depression experienced by breast cancer patients and independent to disease-related parameters.

Ethics

This study was conducted at a single center—Gaziantep University, Oncology Hospital in Turkey. The protocol and informed consent documentation were reviewed and approved by the Independent Ethics Committee of the University and agreed with the ethical principles of the Declaration of Helsinki.

Patient selection

Breast cancer patients who were treated in Gaziantep Oncology Hospital between January 2003 and January 2015 were recruited for this cross-sectional study. We assessed the effects of the potential risk factors on depression, anxiety, and illness perception for three periods following the completion of their intravenous (IV) chemotherapy treatment: 6 months to 2 years, 2 to 5 years, and over 5 years. These periods were chosen according to frequency of follow-up at the hospital (every 3 months for 2 years, every 6 months in 2–5 years, and annually after 5 years). The following information were recorded: age, menopausal status, educational level, marital status, disease stage, follow-up period since diagnosis, and rate of “functional social support” (FSS).

The “inclusion criteria” were as follows: (1) 18 years old or older when diagnosed with breast cancer diagnosed histopathologically; (2) received intravenous chemotherapy ± radiotherapy and completed the treatment; (3) having modified radical mastectomy (MRM) or breast-conserving surgery (BCS); and (4) no obvious mental abnormalities, psychological disorder, and cognitive impairment.

The “exclusion criteria” were as follows: (1) recurrence of breast cancer or metastatic disease; (2) suspicious of recurrence; (3) combination with another tumor or major morbidity, such as chronic obstructive pulmonary disease, coronary heart disease, and cerebrovascular disease; and (4) psychotherapy or medical treatment for psychological disorders before the primary diagnosis.

Study measures

Participants completed a standardized questionnaire assessing the demographic factors and medical data, FSS, anxiety, and depression. Thus, the following measures were used:

  1. 1.

    Beck Depression Inventory (BDI). This was used to measure the severity of depression. The scale comprised of 21 items and a range from 0 to 63. The classification of the BDI score of depression was as follows: <10, none or minimal; 10–18, mild to moderate; 19–29, moderate to severe; and 30–63, severe.

  2. 2.

    Beck Anxiety Inventory (BAI). This was used to measure the severity of anxiety. The classification of the BAI score was as follows: <8, none; 8–15, mild; 16–25, moderate; and >25, severe.

  3. 3.

    Functional Social Support (FSS). This was determined using the Duke–University of North Carolina Functional Social Support (DUFSS) Questionnaire. The DUFSS questionnaire includes eight items assessing the self-perceived affective support and the support from a confidant. It consists of five-category items to assess social support network. A high average score would reflect the better perceived FSS [17]. The DUFSS questionnaire has been validated in a primary care setting and regarded as a suitable measure for studying social support of patients with cancer.

  4. 4.

    Illness perception. This was assessed using the Brief Illness Perception Questionnaire (B-IPQ). It is an eight-item instrument assessing cognitive and emotional perceptions of the illness [18]. The questions were related to the following: (i) consequences (how much does your illness affect your life?); (ii) timeline (how long do you think your illness will continue?); (iii) personal control (how much control do you feel you have over your illness?); (iv) treatment control (how much do you think your treatment can help your illness?); (v) identity (how much do you experience symptoms from your illness?); (vi) concern (how concerned are you about your illness?); (vii) coherence (how well do you feel you understand your illness?); and (viii) emotions (how much does your illness affect you emotionally?). Each question is rated on linear 0–10 point scale. Higher scores indicate more negative illness representations, except for questions 3, 4, and 7; higher scores indicate more positive illness perception.

Statistics

First, univariate analyses were performed. Two independent groups were compared with Student’s t tests (for normally distributed continuous variables) or Mann–Whitney U test (for non-normally distributed continuous variables). To compare more than two independent groups, ANOVA test was used. To determine any relationship between variables, chi-squared tests (for categorical variables) and Spearman’s rank correlation (for two numerical or ordered variables) were used. Multiple linear regression models were used for making specific predictions. Clinically related variables were included in the model if significance at the 10% level was obtained from the univariate analysis. Multicollinearity was checked by calculating variance inflation factors. All univariate analyses were performed in SPSS for Windows version 22.0. A two-sided P value ≤0.05 was accepted as statistically significant.

Results

A total of 225 female breast cancer patients with stage I–III disease were involved in this study. The demographic and clinical characteristics of the participants are shown in Table 1. The mean age was 49.6 years (range 27 to 85 years). Their educational level was low (83.1% were illiterate or primary school level). All patients were treated with intravenous chemotherapy following surgery and 63.6% of patients also received radiotherapy. The majority (86.1%) of patients went into taking hormone therapy. Table 1 also shows disease- and patient-related factors and mean anxiety and depression scores. It was found that the prevalence of the moderate and severe anxiety and depression rates was 14.6 and 16% after 5 years in all stages. The prevalence of moderate and severe anxiety was 47.9, 42.7, and 45.8% after follow-up durations of 6 months–2 years, 2–5 years, and over 5 years, respectively. For the same periods, the prevalence of moderate and severe depression was 45.1, 46.3, and 50.0%, respectively (P = 0.81 and P = 0.83, respectively). The prevalence of mild, moderate, and severe depression rates according to follow-up period is shown in Fig. 1. The prevalence of mild, moderate, and severe anxiety rates according to follow-up period is shown in Fig. 2.

Table 1 Association of the demographic and clinical characteristics of patients (N = 225) with depression and anxiety
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Fig. 1
figure 1

Depression status according to follow-up period using Beck Depression Inventory (BDI) scoring interpretation

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Fig. 2
figure 2

Anxiety status according to follow-up period using Beck Anxiety Inventory (BAI) scoring interpretation

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The obtained data were also analyzed according to the disease stage. The prevalence of moderate and severe anxiety was 55.2, 43.5, and 44.8% for stages I–III, respectively. For the same groups, the prevalence of moderate and severe depression was 55.2, 46.4, and 44.8%. Again, for both parameters, these scores were not significantly different (P = 0.52 and P = 0.83). The prevalence of mild, moderate, and severe depression rates according to stage is shown in Fig. 3. The prevalence of mild, moderate, and severe anxiety rates according to stage is shown in Fig. 4.

Fig. 3
figure 3

Depression status according to stage using Beck Depression Inventory (BDI) scoring interpretation

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Fig. 4
figure 4

Anxiety status according to stage using Beck Anxiety Inventory (BAI) scoring interpretation

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A significant negative correlation was observed between the FSS score and both anxiety and depression (r = −0.324 and −0.310, respectively; P < 0.001 for both). From the multiple linear regression analysis, the following conclusions could be drawn: (i) one unit increase in the social support level would result in decreases of 2.7 and 2.9 points in anxiety and depression scores, respectively, and (ii) a 1-year increase in age would result in decreases of 0.18 and 0.21 point in anxiety and depression scores, respectively (Table 2).

Table 2 Multiple linear regression analysis (including functional social support and age) for Beck Anxiety and Beck Depression Scores
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When eight separate parameters in the B-IPQ questionnaire were evaluated, no correlation was found among stage, duration of disease, and positive and negative illness perception except for the low correlation between timeline and disease stage and between personal control and follow-up period (r = −0.137, P = 0.04 and r = 0.155, P = 0.02, respectively). However, illness perception scores were noticeably better with increased social support (Table 3). Positive illness perception parameters such as (i) personal control (question 3—how much control do you feel you have over your illness?) and (ii) treatment control (question 4—how much do you think your treatment can help your illness?) were both negatively correlated with anxiety and depression scores (P < 0.005). Mean score of coherence which is a parameter of positive illness perception was 7.01 (5 to 9). Coherence was not correlated with anxiety and depression scores. In contrast, the following were positively correlated with anxiety and depression scores (P < 0.005 for all): negative illness perception as (i) consequences (question 1—how much does your illness affect your life?), (ii) timeline (question 2—how long do you think your illness will continue?), (iii) identity (question 5—how much do you experience symptoms from your illness?), (iv) concern (question 6—how concerned are you about your illness?), and (v) emotions (question 8—how much does your illness affect you emotionally?) (Table 4).

Table 3 Association of Brief Illness Perception Questionnaire (B-IPQ) with social support, stage, and duration of disease: Spearman’s rho correlation test
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Table 4 Correlation of Brief Illness Perception Questionnaire (B-IPQ) with anxiety and depression score: Spearman’s rho correlation test
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Discussion

Breast cancer survivors experience more distress compared to other cancer types because of the relatively long overall survival [19]. Effects of patient- and disease-related factors on anxiety and depression scores in breast cancer patients were evaluated in earlier studies. Several risk factors were demonstrated, such as metastatic progression, early post-chemotherapy period (first 6 months), and pre-existing depression and anxiety episodes [20]. Additionally, illness perception was found to be an important parameter affecting the fear of recurrence, distress, and quality of life for breast cancer survivors in the early follow-up period [15, 21]. However, it has not been studied comprehensively for the effect of illness perceptions on anxiety and depression scores. In our study, patients receiving chemotherapy at the recruitment time or in the first 6 months of follow-up period were excluded due to high risk of anxiety and depression. Patients with psychological disorders and major comorbidities which are the risk factors for anxiety and depression were also excluded. Follow-up period of patients was stratified based on our routine practice: every 3 months during the first 6 months–2 years, every 6 months after 2–5 years, and annual after 5 years. It was assumed that such frequency of clinical visits and examinations would optimize the distress level of the patients. Patients who were followed for more than 5 years (up to 12 years; mean follow-up period 4.1 years; range 0.6–12 years) were also included in order to obtain a more thorough picture. We found that illness perception had a remarkable effect on anxiety and depression scores regardless of the follow-up duration and the other disease-related factors.

Some studies showed high rates of distress in non-metastatic breast cancer patients. A cohort study assessed the effects of risk factors on anxiety and depression in 170 early-stage breast cancer patients for three periods: around diagnosis (1 month before diagnosis to 4 months after diagnosis), medium term (4 months to 2 years after diagnosis), and longer term (2 to 5 years after diagnosis) [22]. Accordingly, longer-term (patients with 2 to 5 years) depression and anxiety were associated with patient-related factors such as previous psychological treatment, lack of an intimate confiding relationship, younger age, and severely stressful non-cancer life experiences; however, disease-related factors including number of axillary lymph nodes involved, tumor size and histology, and type of adjuvant treatment were not associated with depression and anxiety at any time consistent with our findings. In this study, while a higher anxiety and depression score was shown within the first year including the IV chemotherapy period, a stable anxiety and depression score curve was observed for medium- and longer-term follow-up independent to disease-related factors like stage and histopathological features of the tumor. Also, a large cross-sectional study showed that depression was influenced by educational level (P < 0.001) and menopausal status (P = 0.004) and comorbidity whereas it was not affected by age (<50 versus ≥50, P = 0.329), married status (P = 0.082), and disease-related factors (stage; P = 0.089, time since surgery [<5 versus ≥5]; P = 0.987, adjuvant treatment modalities P = 0.800) [23]. These findings show the possible role of different parameters on anxiety and depression scores of breast cancer patients. In these circumstances, we demonstrated that illness perceptions which is another parameter related to distress were strongly correlated with anxiety and depression scores in patients with median and longer follow-up period.

We found that the prevalence of moderate–severe anxiety and depression was ∼15% even after 5 years (up to 12 years) for all stages of breast cancer. This agrees with earlier results. Younger ages were associated with more anxiety and depression consistent with other studies [22,23,24]. Unlike the literature, although pre-menopausal patients had similar depression rates with post-menopausal patients, there was a significant difference for anxiety [23]. While increased depression and anxiety scores were observed in patients with higher levels of education, consistent with previous studies [23, 25], there was no statistically significant difference for anxiety scores. It can be explained by the fact that patients with higher education levels may have greater awareness of the disease and this may lead to stressful condition or worse illness perception; on the other hand, patients with lower education levels can be more easily convinced by their physicians in our society. Observed different results compared to the other studies might be associated with the great number of parameters acting on distress and ethnicity.

One of the important parameters on anxiety and depression scores was also social environment. The social environment may provide a protective layer from the harmful effects of depression and anxiety associated with cancer [26, 27]. Bardwell et al. studied the importance of social support with other parameters on depression score in early-stage breast cancer patients. It was found that depressive symptoms are not associated with disease-related factors including stage, time since diagnosis, and treatment modalities (only surgery ± chemotherapy ± radiotherapy), whereas they are most strongly linked to many subjective psychosocial variables: younger age, being unmarried, poorer physical functioning, and social support, consistent with our study [24]. We showed the remarkable effect and importance of social support on anxiety and depression scores and illness perception parameters in patients with all follow-up period and stages. We found that negative illness perception parameters (including concern, emotional representation, consequences, and timeline) and positive illness perception parameters (including personal control and treatment control) were not correlated with follow-up period and disease stage except for the low correlation between timeline and disease stage and between personal control and follow-up period. However, increments in social support were associated with higher scores of positive illness perception parameters and lower scores of negative illness perception parameters.

Distress affecting breast cancer survivors was correlated with various psychosocial variables including quality of life, illness perception, fear of recurrence, anxiety, and depression [21, 28]. Distress during the initial treatment period could be explained by patient’s perceived illness [29, 30]. In our study, we found a strong correlation between illness perception score and anxiety/depression score regardless of disease stage and follow-up period after the treatment period. Patients who had lower positive illness perception exhibited more anxiety and depression and vice versa. Coherence, one of the positive illness perception items, was generally high score in our patient group. When the patients felt that they understood their illness sufficiently, they gave a high score, which means the sense of positive disease as in items 3 and 4. Understanding the disease is important for struggling to cope with the disease. There was no significant correlation between coherence and anxiety and depression in our study. This may be related to our clinic’s precision to give information and education that leads patients to understand their illnesses at high level. On the other hand, patients with higher negative illness perception scores showed higher anxiety and depression scores. In this connection, illness perception is an important determinant of anxiety and depression not only for early period of the disease but also for later follow-up period and “illness perception questions” is a preliminary test predicting anxiety and depression, guiding the oncologist in regard to consulting a psychiatrist.

The limitation of this study is that the majority of patients are of low educational level and therefore the generalizability of the study is questionable. Additionally, cohort studies should be designed to assess the long-term changes in illness perceptions. However, even with cross-sectional analysis, this study showed that illness perception is an important determinant of anxiety and depression for both early and long-term follow-up period.

Conclusion

Illness perception, level of social support, and age were associated strongly with anxiety and depression scores in breast cancer survivors. We recommend that all patients should be evaluated for the illness perception not only at the diagnosis but also periodically during follow-up.