NCCN: Continuing Education
Accreditation Statement
This activity has been designated to meet the educational needs of physicians and nurses involved in the management of patients with cancer. There is no fee for this article. No commercial support was received for this article. The National Comprehensive Cancer Network (NCCN) is accredited by the ACCME to provide continuing medical education for physicians.
NCCN designates this journal-based CME activity for a maximum of 1.0 AMA PRA Category 1 Credit(s)™. Physicians should claim only the credit commensurate with the extent of their participation in the activity.
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This activity is accredited for 1.0 contact hour. Accreditation as a provider refers to recognition of educational activities only; accredited status does not imply endorsement by NCCN or ANCC of any commercial products discussed/displayed in conjunction with the educational activity. Kristina M. Gregory, RN, MSN, OCN, is our nurse planner for this educational activity.
All clinicians completing this activity will be issued a certificate of participation. To participate in this journal CE activity: 1) review the learning objectives and author disclosures; 2) study the education content; 3) take the posttest with a 66% minimum passing score and complete the evaluation at http://education.nccn.org/node/71854; and 4) view/print certificate.
Release date: August 18, 2015; Expiration date: August 18, 2016
Learning Objectives
Upon completion of this activity, participants will be able to:
Examine preoperative distress as a predictive factor for development of PPBCT
Identify psychological risk factors for PPBCT that may be targeted in preventive interventions
Background
Persistent pain after breast cancer treatment (PPBCT) affects 25% to 60% of patients treated for breast cancer,1 may persist for several years after treatment,2 and has been reported to negatively affect quality of life3–6 and physical function.7 PPBCT is defined as pain in the breast, side of chest, axilla, or arm more than 3 months after the last surgery, when other causes of pain are ruled out.2 Identifying risk factors for PPBCT is important in order to develop preventive interventions.
Psychological comorbidity, such as anxiety,8 depression,9 fear of pain, and catastrophizing,10,11 are known to influence pain perception. Furthermore, psychological factors as a predictor of persistent pain are suggested to be independent of the surgical procedure.12 Several studies have indicated that psychological comorbidity is a risk factor for PPBCT,1,13 with recent prospective studies indicating a correlation between preoperative psychological symptoms and PPBCT.3,4,14,15 A prevalence of preoperative depression of 37% and anxiety of 70% has been reported among patients with breast cancer,16 whereas the prevalence of severe psychological distress has been reported to be around 40%.17–19 Longitudinal studies suggest a reciprocal relationship between depression and pain,20,21 in that depression may lead to pain and vice versa. Thus, preoperative and postoperative treatment of psychological symptoms may prove to be an interesting strategy for preventing persistent post-operative pain. Evidence is available to support psychological interventions in the treatment and end-of-life phases of cancer, but less research has been performed in the survival phase.22
Distress has been suggested to be the 6th vital sign,23,24 conceptualized as a broader construct than depression, and also including a wide continuum of emotions relating to worry, anxiety, depression, and adjustment disorders.25 This concept may be more useful in clinical settings than psychiatric diagnoses, such as depression or anxiety, because it is not associated with the stigma of a psychiatric diagnosis and is easily understood by patients, thus facilitating quick assessment.25 Distress may be assessed by several tools,25 but the Distress Thermometer (DT) is widely used and has been supported as an appropriate screening tool for distress in a meta-analysis.26
The goal of this prospective study was to examine the construct of distress as a predictor for PPBCT, using a validated Danish version of the DT,27,28 based on the hypothesis that preoperative distress is a significant risk factor for the development of PPBCT.
Methods
Study Design and Participants
We used data from a prospective questionnaire study previously reporting on validation of the Danish version of the DT and distress prevalence.19,28 Between October 28, 2008, and October 28, 2009, patients were consecutively recruited at the Department of Breast Surgery, Rigshospitalet, Copenhagen, Denmark. All women with newly diagnosed primary breast cancer who were older than 18 years old, Danish speaking, and had no cognitive impairments were invited to participate in the study at their last preoperative visit to the outpatient clinic, 1 to 3 days before surgery. Subsequently, patients who underwent bilateral surgery were excluded to avoid bias in pain measurement. Participants filled out a baseline questionnaire at enrollment and follow-up questionnaires at 4 and 8 months after surgery. The study was conducted according to the Act on Research Ethics Review of Health Research Projects in Denmark, and was approved by the Danish Data Protection Authority (2008-41-2605).
Pain and Psychological Distress
The primary outcome was the risk of reporting moderate to severe pain after breast cancer treatment at 8 months' follow-up in patients who reported preoperative distress using the DT.27 Pain at 8 months was the primary outcome, because both primary and adjuvant treatment, besides endocrine treatment, were completed at this time, whereas at 4 months, many patients would still be receiving adjuvant treatment. Moderate to severe pain after breast cancer treatment was defined as pain in the breast area, axilla, arm, side of body, and/or shoulder on the operated side, with a pain intensity of 4 or more on a numerical rating scale (NRS) ranging to 10. The NRS is an accepted method of measuring pain.29 The cutoff point used is supported by a study on cutoff points in a postoperative pain setting.30
Preoperative pain in the area of disease was defined as pain in the breast area, axilla, arm, side of body, and/or shoulder on the side where surgery was to occur, dichotomized (yes/no). Distress was measured using the DT, which is a vertical numerical rating scale ranging from 0 (no distress) to 10 (extreme distress).27 The DT has been validated in a Danish population, in which cutoff scores of 7 or more were shown to be optimal for diagnosing distress, whereas cutoff scores of 3 or more were found to be most suitable for screening purposes.28 The questionnaire also included a numerical rating scale from 0 to 10, asking how distress affected the patient's daily life activity, called the impact thermometer.31 With the impact thermometer, a cutoff score of 7 or more was also used, combined with a distress score of 7 or more. Distress was also measured using the Hospital Anxiety and Depression Scale (HADS), a 14-item scale measuring depression and anxiety in 2 subscales, or summarized in a total score measuring emotional distress.32 Cutoffs used were a HADStotal of 15 or more, HADSanxiety of 8 or more, and HADSdepression of 8 or more, as proposed by Zigmond and Snaith.33
Demographic and Disease Characteristics
Demographic data (age at diagnosis) and lifestyle characteristics (alcohol consumption, smoking habits, and physical activity) were obtained from the baseline questionnaire. Treatment details and disease specifications were retrieved from the Danish Breast Cancer Cooperative Group (DBCG) database34 and through medical records. Patients were treated according to the 2007 DBCG protocol,35 receiving surgery with mastectomy or breast-conserving surgery (BCS), and sentinel lymph node biopsy (SLNB) or axillary lymph node dissection (ALND) of levels I through II. Adjuvant treatment was according to risk profile, with chemotherapy consisting of 3 cycles of cyclophosphamide and epirubicin, followed by 3 cycles of docetaxel. Patients receiving BCS were treated with radiotherapy of the residual breast, and patients with axillary metastasis received locoregional radiotherapy. Endocrine treatment consisted of tamoxifen or aromatase inhibitor according to hormonal receptor status and menopausal status.
Statistical Analyses
Statistical analyses were performed with SPSS Statistics for Windows, Version 19.0 (IBM Corp, Armonk, NY). Univariate analyses were calculated using Wald χ2 test. In a multivariate logistic regression analysis, we examined the association between preoperative distress (DT ≥7) and moderate to severe pain after breast cancer treatment at 8 months, adjusting for potential confounders. Adjusted odds ratios and 95% CIs were calculated and the Wald χ2 test was used to test the overall significance of each parameter. Potential confounders associated with both distress and pain were selected before analysis based on what prior studies have shown,1 and included age (dichotomized into ≥60 years and <60 years), preoperative pain, axillary procedure, breast procedure, radiotherapy versus none, and chemotherapy versus none. Tests for interaction between age and distress and between preoperative pain and distress on pain were performed pairwise in separate models applying the Wald χ2 test. Goodness of fit for the main logistic regression analysis was tested with the Hosmer-Lemeshow test and Pearson χ2.
Secondary analyses applying multivariate logistic regression analyses included associations between preoperative distress measured as a HADStotal score of 15 or greater, the impact thermometer and DT scores combined, a DT score of 3 or greater, respectively, and PPBCT at 8 months. A multivariate logistic regression analysis was also performed, examining the association between preoperative distress (DT ≥7) and moderate to severe pain after breast cancer treatment at 4 months. Correlations between moderate to severe pain at 8 months and the reporting of a HADStotal score of 15 or more at 8 months and a DT score of 7 or more at 8 months were calculated using χ2 tests, with P values applied. P values less than .05 were considered statistically significant.
Results
Participants
In all, 426 patients were invited, 357 (84%) participated, and 10 patients were subsequently excluded because they had received bilateral surgery. Of the 357 patients included, 335 (94%) completed the distress thermometer in the first questionnaire, 307 (86%) returned the questionnaire at 4 months' follow-up, and 291 (82%) returned the questionnaires at both 4 and 8 months' follow-up (Figure 1).
Flowchart of study process.
Citation: Journal of the National Comprehensive Cancer Network J Natl Compr Canc Netw 13, 8; 10.6004/jnccn.2015.0120
Descriptive Data
The median age among participants was 61 years (interquartile range [IQR], 54–67). The mean follow-up time from surgery to the 2 follow-up questionnaires was 124.5 (SD, 7.4) and 244.5 (SD, 7.0) days, respectively. Details regarding age and some lifestyle characteristics among patients included in the final logistic regression analysis are shown in Table 1, and treatment and disease characteristics are shown in Table 2. Differences regarding treatment, age, preoperative distress, and pain according to attrition are described in Table 3.
Distress
At baseline, 145 patients (43%) reported a DT score of 7 or more and 257 (77%) reported a DT score of 3 or more; 106 patients (32%) reported both an impact thermometer and a DT score of 7 or more. A total of 121 (36%) reported a HADStotal score of 15 or more, 61 (18%) reported a HADSdepression score of 8 or more, and 182 (54%) reported a HADSanxiety score of 8 or more at baseline. At 4 months, 66 patients (22%) among the 307 respondents (with 7 missing) reported a DT score of 7 or more; at 8 months, 42 patients (14%) among 291 respondents (with 8 missing) reported a DT score of 7 or more.
Pain
At baseline, 124 patients (37%) reported pain on the side where surgery was to occur; at 4 months, 73 (24%) reported moderate to severe pain after breast cancer treatment; and at 8 months, 82 (28%) reported moderate to severe pain. Preoperative pain was highly associated with moderate to severe pain at 4 months (adjusted odds ratio [OR], 3.44; 95% CI, 1.89–6.24; P<.01), but not at 8 months (Table 4).
Main Results
Preoperative distress (DT ≥7) was significantly associated with moderate to severe pain 8 months after surgery, with an adjusted OR of 2.05 (95% CI, 1.18–3.56; P=.01; Table 4). The same association was found when combining an impact thermometer score of 7 or more with a DT score of 7 or more (adjusted OR, 2.16; 95% CI, 1.23–3.79; P=.01). When using the DT cutoff score of 3, the association with moderate to severe pain at 8 months was not statistically significant, with an unadjusted OR of 1.87 (95% CI, 0.96–3.66; P=.07) and an adjusted OR of 1.41 (95% CI, 0.69–2.87; P=.34).
Using the HADStotal score of 15 or greater as a measure of distress, the association with moderate to severe pain at 8 months was statistically significant, with an unadjusted OR of 1.77 (95% CI, 1.03–3.03; P=.04); however, when adjusted, the association was
Lifestyle Characteristics and Demographics Among Patients Included in the Final Logistic Regression Analysis According to Preoperative Distress
Concurrent Pain and Distress at 8 Months
Moderate to severe pain at 8 months was highly associated with both a HADStotal score of 15 or greater at 8 months and a DT score of 7 or more at 8 months, with a P value of less than .001 for both the HADS and DT on χ2 tests.
Discussion
Preoperative distress, using the DT with a cutoff point of 7, was a significant risk factor for moderate to severe PPBCT both 4 and 8 months after surgery. A similar association was found when adding the impact thermometer to the DT, although the OR did not increase further. The association between PPBCT and distress was not seen with a DT cutoff point of 3, indicating that the distress needs to be severe to predict PPBCT. Preoperative depression and anxiety using the HADS was not as clearly associated with PPBCT, only being statistically significant in the univariate analysis, and not when adjusting for age, preoperative pain, and treatment characteristics. The HADS was designed to detect patients with states of depression and anxiety in a hospital outpatient clinic,33 whereas the DT was designed to screen patients with cancer for emotional distress.27 However, distress measured using both the DT and HADS at 8-month follow-up were significantly associated with moderate to severe PPBCT, indicating that patients reporting PPBCT do concomitantly score high on both psychometric tests. This finding could emphasize that the construct of distress may be more suitable than anxiety and depression for patients facing a newly diagnosed breast cancer, because both constructs are highly associated with PPBCT when they are reported concomitantly with PPBCT.
The relationship between distress and persistent pain is unresolved, but it is plausible that the reaction to a crisis may imply pain catastrophizing and fear of pain, which both have been shown to predict persistent postsurgical pain.36 Interestingly, preoperative pain in the area where surgery was to take place was highly associated with PPBCT at 4
Treatment Characteristics and Disease Specifics Among Patients Included in the Final Logistic Regression Analysis According to Preoperative Distress
The results of the present study are supported by other recent prospective studies in similar constructs. Miaskowski et al3,4 showed that moderate to severe persistent pain in the breast and axilla/arm was associated with the reporting of higher preoperative levels of depressive symptoms, trait anxiety, sleep disturbance, and fatigue and lower levels of attentional function. Another recent prospective study showed that preoperative decreased psychological robustness, constructed from a range of validated psychological questionnaires, was associated with moderate to severe pain at 9 months after surgery.14 Preoperative depression, measured with the Beck Depression Inventory, has also been found to be significantly associated with pain at 12 months after surgery for breast cancer,15 and a small cross-sectional study showed that preoperative levels of anxiety and depression were higher among patients who subsequently reported chronic postoperative pain.39 On the contrary, Poleshuck et al40 did not find a significant association between preoperative emotional functioning and the presence of chronic pain 3 months after breast cancer surgery when using the Beck Depression Inventory, the Spielberger State-Trait Anxiety Inventory, or the Hamilton Depression and Anxiety Rating Scales. However, this study only included 95 patients, among which 29% were treated for a benign tumor, leaving only 67 patients treated for breast cancer.40 A recent systematic review on the association between preoperative anxiety and catastrophizing and chronic postsurgical pain found that in 55% of 29 studies, preoperative
Treatment Characteristics, Preoperative Pain, and Preoperative Distress According to Attrition Due to Loss to Follow-Up, Missing Data, and Exclusions
Multivariate Logistic Regression Analysis of Treatment Modalities, Age, Preoperative Distress, and Preoperative Pain on 8-Month Postoperative Pain of 4 or Greater (n=286)
The limitation of the present study is primarily that only approximately 80% of invited patients were included in preoperative analyses, and a further 10% were lost to 8 months' follow-up, potentially introducing selection bias. It is likely that this bias, if anything, underestimates the prevalence of preoperative distress, because patients declining to participate are often the most emotionally traumatized and lacking sufficient resources to participate. However, we found no difference in preoperative distress reporting between patients included in the final analysis and those lost to follow-up, but the patients lost to follow-up did receive more extensive surgical treatment. Excluded patients differed slightly more from participants, in that they were older and receiving more extensive surgery, and fewer were receiving chemotherapy. Furthermore, potential confounders such as comorbidity and some lifestyle characteristics were not taken into account in the present study. Strengths of the study are the longitudinal, prospective design with 8 months' follow-up, and that all participants were enrolled at the same point in the disease trajectory. Furthermore, the study used a very easy, useable numerical rating scale for distress.
With the present prospective study, along with some other recent prospective studies, highlighting preoperative emotional distress as an important risk factor for PPBCT, future studies focusing on early treatment of patients with a high level of preoperative distress as a potential way of reducing PPBCT are clearly needed.4 A meta-analysis on the effect of psychosocial interventions on persistent pain among patients with breast cancer showed a small to medium overall effect of interventions on pain.42 However, many studies included in the review used different intervention types, resulting in considerable heterogeneity.42
Conclusions
The present study showed that preoperative distress measured with a DT score of 7 or more was associated with PPBCT. Measuring preoperative emotional distress with the DT may identify patients at risk of developing PPBCT. Preoperative identification of patients at risk allows for further research in psychological and pharmacologic treatment for prevention of PPBCT.
Acknowledgments
The authors would like to thank Rune Gärtner, Henrik Kehlet, and Niels Kroman for their contributions to this study.
The authors have disclosed that they have no financial interests, arrangements, affiliations, or commercial interests with the manufacturers of any products discussed in this article or their competitors.
This study was supported by the Aase and Ejnar Danielsens Fond and by a grant from the Danish Cancer Society. The study is part of the Europain Collaboration, which has received support from the Innovative Medicines Initiative Joint Undertaking, under grant agreement no 115007, resources of which are composed of financial contribution from the European Union's Seventh Framework Program (FP7/2007-2013) and EFPIA companies' in kind contribution.
CE AUTHORS
Deborah J. Moonan, RN, BSN, Director, Continuing Education, has disclosed that she has no relevant financial relationships.
Ann Gianola, MA, Manager, Continuing Education Accreditation & Program Operations, has disclosed that she has no relevant financial relationships.
Kristina M. Gregory, RN, MSN, OCN, Vice President, Clinical Information Operations, has disclosed that she has no relevant financial relationships.
Rashmi Kumar, PhD, Senior Manager, Clinical Content, has disclosed that she has no relevant financial relationships.
Susan Darlow, PhD, Oncology Scientist/Medical Writer, has disclosed that she has no relevant financial relationships.
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