Colored body images reveal the perceived intensity and distribution of pain in women with breast cancer treated with adjuvant taxanes: a prospective multi-method study of pain experiences

1 Introduction

Breast cancer is currently the most prevalent adult cancer worldwide [1]. A broader use of screening for earlier detection, multi-disciplinary care, and adjuvant systemic therapy for patients with early breast cancer have resulted in improved survival rates [2]. Taxane-containing chemotherapy is one of the cornerstones of adjuvant breast cancer treatment. However, it may result in acute chemotherapy-induced nociceptive and neuropathic pain, experienced as muscle and joint pain, painful paresthesias, tingling, numbness, dysesthesia and distal muscle weakness [3], [4], [5]. The pathophysiology of chemotherapy-induced pain is not completely understood [6], [7] and no convincing explanations for the pain syndrome arising from joints and muscles are available [8]. Furthermore, to date no validated treatment options have been identified for dealing with taxane-induced pain [9]. Chemotherapy-induced neuropathic pain persisting for several years has been described in 30–43% of patients. Additionally, older patients have been reported to be even more sensitive and thus at higher risk of developing chemotherapy-induced pain [5], [10]. Taxane toxicity such as neuropathy and pain should be valuated all the more since the toxicity are not correlated to the treatment outcome [3]. Nevertheless pain is known to interact with other symptoms and influence the health-related quality of life (HRQoL) [11], both during and after completed treatment. The effects of pain on daily life are considerable, both short and long term [12], [13]. Women with breast cancer treated with adjuvant taxanes could be served well by receiving better information about possible side effects such as polyneuropathy and long-term pain during and after taxane treatment. Improved symptomatic treatment of pain as well as information on and prescription of pre-emptive analgesia treatment, could be highly effective in avoiding unnecessary pain and anxiety.

The visual analog scale (VAS) is a commonly used method for reporting pain and has been found helpful in monitoring chemotherapy-induced pain [14]. The European Organization for Research and Treatment of Cancer Quality of Life Questionnaire (EORTC-QLQ-C30) [15] is a common tool for evaluating HRQoL in patients with cancer, and includes two questions assessing pain. Unfortunately, the reporting of pain in clinical trials is often incomplete, with many studies lacking descriptions of how the assessments were performed [6], [16]. Pain is a symptom that may be difficult to assess reliably in the clinical practice [17]. Even though the VAS is a method that can reasonably communicate the intensity of the subjective pain experience [18], it neither communicates the localization nor the distribution of the perceived pain. One way to overcome these shortages could be to use a supplemental pain chart, such as a colored body image [19]. This is a method for semi-quantitatively assessing the perceived distribution and intensity of the pain. Combining different methods for collecting information about pain may add important information in order to further describe the individual pain experience [20].

The aim of the present study was to document the pain reported by women during and after adjuvant chemotherapy (taxanes/anthracyclins) following breast cancer using three different methods: (1) the VAS, (2) a colored body image and (3) the two pain questions included in the EORTC-QLQ-C30. The following questions were addressed:

1. How do women with breast cancer express pain (as reported on the VAS) (1) at baseline, (2) immediately before each cycle of chemotherapy and (3) on Day 10 after each cycle of the six cycles of chemotherapy?

2. How do the participants experiencing pain >30 on the VAS, report the pain distribution measured on a colored body image, during chemotherapy, and at 12 months after inclusion into the study?

3. How do the participants experiencing pain >30 on the VAS, report the intensity of pain measured semi-quantitatively on a four-level coloring scale of the colored body image, during chemotherapy and 12 months after inclusion into the study?

4. How do the participants estimate pain on the EORTC-QLQ-C30 at baseline, after 3 and 12 months after inclusion into the study?

2 Materials and methods

2.1 Participants

The women were consecutively recruited from “The Breast Cancer and Stress Study”, described elsewhere [21]. The patients were eligible for participation if age 18 years or older and scheduled for adjuvant sequential chemotherapy with doses of ≥75 mg/m² of docetaxel and epirubicin. Fifty-seven women were consecutively asked to participate in the study from August 2010 to September 2012. Four of them did not complete the VAS or EORTC-C30-QLQ assessments and were therefore excluded, resulting in a total of 53 enrolled women. Only the participants with VAS >30, who had been interviewed in an earlier study (n=16), described in detail elsewhere [21], filled out the colored body image; see Fig. 1. Clinical and demographic information was gathered from the women’s health records and inclusion forms.

Fig. 1:

Assessment flow chart.

3 Results

3.1 Pain measured using the VAS

Forty-seven percent (n=25) of the 53 women assessed VAS pain scores >30 at one or several occasions during the treatment (six cycles). The participants with VAS >30 were slightly older and had a lower annual household income than those reporting VAS values less than >30; see Table 1. The mean VAS scores are presented in Fig. 2. The participants with VAS >30 reached in average the highest VAS value in pain after Cycle 1. The most intense pain for all women was noted after Cycle 3. For Cycle 4, the treatment changed from docetaxel to epirubicin for all women except one. During the epirubicin sequence, the participants with VAS >30 continued reporting some pain on the VAS after each cycle of chemotherapy. Although the VAS estimates dropped towards the end of the chemotherapy treatment, they were still higher than before the start of the first cycle.

Table 1:

Participant characteristics.

Demographics	VAS >30 (n=25)	VAS ≤30 (n=28)a
Age, median, range	57 (37–76)	49 (29–73)
Mean VAS at baseline (SD)	1.16 (2.14)	0.357 (0.55)
Annual household income (EUR), mean	359,000	477,000
Working	17	14
Retired	7	4
On sick leave	15	26
Residential area
Dalarna	5	8
Gävleborg	14	6
Uppsala	6	14
Type of surgery
Breast-conserving surgery	11	12
Mastectomy	14	14
Hormone receptor status
ER+/PR+	14	13
ER+/PR−	6	2
ER−/PR+	–	1
ER−/PR−	4	10
Her2 amplified	7	7
Triple negative	3	6
Not evaluable	1	2
Tumor grade
I	2	2
II	13	9
III	9	13
Not evaluable	1	2
Sequential taxanes/epirubicin	25	28
Radiation	15 (missing 0)b	17 (missing 3)b
Endocrine therapy	20 (missing 3)b	18 (missing 4)b

1. ER=estrogen receptor; PR=progesterone receptor. ^aNo personal bas data ejected (n=2). ^bData missing.

Fig. 2:

Estimated pain before each cycle and Day 10 after cycle.

3.2 Pain described by the participants with VAS >30 by coloring a body image

During chemotherapy, an average of 51% of the area of the body images was colored. Perceived pain intensity colored red (interruptive pain) was the most common, covering 25% of the total body surface area, followed by the perceived pain intensity yellow (acceptable pain) covering 20%, and finally, perceived pain intensity as painted black (excruciating pain), which covered 6% of the total body image area. Pain was most commonly indicated in the lower back, knees, thighs and footpads; see Fig. 3A.

Fig. 3:

(A) A colored body image reveals pain distribution and intensity described during chemotherapy by participants with VAS >30. (B) A colored body image reveals pain distribution and intensity described 12 months after inclusion by participants with VAS >30.

At 12 months after inclusion, the colored pain distribution of the total body area was 18%. At this point the pain intensity colored yellow (acceptable pain) was the most common on over 13% of the total body area, distributed as 5.5% on the trunk, 5% on the legs, 2% on the arms and 0.8% on the head. For the pain intensity colored red (interruptive pain), the total colored area was distributed to 4.5%, with 0.7% on the trunk, 2.4% on the legs, 1.2% on the arms and 0.2% on the head. Traces of black (excruciating pain) (0.2%) were noted on the upper front of the trunk, while the largest part of the body image area, 82%, was colored green and was thus painless (see Fig. 3B). Two of the 15 women colored a completely green body image.

4 Discussion

The current study evaluates the pain experiences of 53 women with breast cancer being treated with sequential adjuvant chemotherapy. The women were assessed regarding the possible development of chemotherapy-induced pain using three different methods: the VAS; a colored body image; and using the two pain items of the European Organization for Research and Treatment of Cancer Quality of Life Questionnaire.

Surprisingly widespread and intense pain was detected using this multi-method approach. Different types of pain were found. Given that pain is augmented by anxiety, good communication about treatment effects and side effects is vital for better symptom control.

Twenty-five women (47%) reported pain scores >30 on the VAS one or more occasions after chemotherapy. Most immediately after Cycle 1, VAS increased the most for the women with VAS >30 and for the whole group it increased the most after Cycle 3 (the last docetaxel treatment); thereafter, there was a decline in pain as reported on the VAS. This might be explained by a systemic accumulation of taxane at Cycle 3, which may increase the risk of pain development [30]. However, the women with VAS >30 seem to have had some pain during the epirubicin sequences as well. Although epirubicin is known to result in fatigue, nausea and alopecia it is rarely associated with development of pain [31].

Interpreting the two pain questions on the EORTC-QLQ-C30 at baseline, possibly indicates that there is higher initial pain on EORTC for the group of women with VAS >30. Elevated pain scores at baseline is a warning sign for perceiving more acute clinical pain [32]. However, the VAS measurements before the first cycle of chemotherapy, in which the whole group recorded approximately the same levels of pain, contradict such a conclusion. However, The EORTC-QLQ-C30 questions report perceived pain the past week whereas the VAS reports present pain.

In order to more appropriately detect pain during and after treatment with taxane, the timing of the assessment is important [14]. Cavaletti et al. discussed and evaluated different assessment tools for peripheral neuropathy. They found in their tailored study high levels of pain not previously described in clinical study’s of chemotherapy induced neuropatic pain [33]. One potential explanation for this could be the systematic collection of pain data during the evaluation period, the assessment tools used, the timing of the assessments and, whereby a systematic underreporting of pain is omitted. This also calls attention to the fact that different pain assessment tools capture pain differently. In several previous studies of acute taxane-induced pain, it is not possible to identify either the pain assessment tools nor the time point(s) at which the pain was assessed [34].

The colored body image showed a perceived pain distribution of 51% of the total body surface area during treatment. During chemotherapy, the hands and footpads were colored, which may indicate what is described in the literature as neuropathic pain [35]. Other colored areas possibly indicate myofascial and nociceptive pain in the major muscle groups; the lower back, thighs and calves, and joints. The pain intensity in these areas of the colored body image was mainly ranked as interruptive high pain. This is an alarmingly high percentage of women experiencing a widespread intense pain during chemotherapy. A colored body image can reveal blind spots that are undetectable in conventional pain assessments, and thereby provide important information on pain. Twelve months after inclusion 18% of the body area was involved in pain following the same patterns as during chemotherapy; but its distribution and intensity were lower. These aspects of pain are very important, but are not apparent when conventional pain assessment tools are used. A strength of the colored body image is its communicability, being easily shared and discussed between patients and health professionals. High pain intensities and/or pain perceived over large proportions of the body may also be better indicators that a health professional should offer assistance to the patient.

All measurement tools have limitations, and Dworkin et al. claim that there is a risk of false negative results if one only uses simple estimates of pain in clinical research [17]. This is especially important as cancer patients have been shown to underreport symptoms because they fear this will lead to a change in treatment and a subsequent loss of effectiveness [36]. What patients consider important may depend on a number of individual factors such as symptom burden as well as social and physical conditions [37], and we must communicate these factors and bring them to light during the patient’s care as they are important for the treatment outcome for this individual. The literature highlights certain groups of patients with a higher risk of developing more complex symptoms and receiving less satisfactory relief from these symptoms, such as those in active cancer treatment, and cancer survivors [38]. These two groups are likely undertreated for pain and other symptoms [39].

The merits of a proposed treatment must be considered in relation to its toxicity. What we know today about the likelihood of clinical benefits versus toxicities allows clinicians to adjust the dose of chemotherapy for breast cancer treatment without risking treatment results [7], [8]. Attention must be paid to benefit versus harm, keeping one eye on the dose and the other on the toxicity and the reactions of the nervous system. Preventive pain relief possibly needs to be included in the chemotherapy treatment, with individual escalation of the pain treatment in a way parallel to that in cases of chemotherapy-triggered nausea. This is also indicated by a newly conducted study by Fries et al. in which pain was the most frequently reported symptom [40].

We know that the risk of pain development is at its highest 24–48 h after receiving taxane chemotherapy [14], [34]. Attention should be given to pain evaluation and treatment during this time window. Outpatient chemotherapy treatment may be a further clinical challenge that requires a sensitive, person-centered communication between the patient and the health care personnel. Evaluating important side effects like pain should not be left to the women themselves. Such evaluations should also be done routinely by the health care personnel.

5 Conclusion

This study provides information on how different pain assessment tools offer different information. The VAS provides a clear picture of the development of pain during chemotherapy whereas the two pain questions of the EORTC QLQ-C30 give a rough estimate of the pain, most suitable for comparisons between groups. Additionally, the colored body image brings another dimension to the pain assessment, offering additional information on body areas where the pain is perceived, and on pain intensities as experienced by the patient. The colored body image offers unique information on pain that is not available with the two other assessment tools. A multi-method approach to pain assessment, offers many advantages. Prophylactic analgesia during taxane chemotherapy could reduce pain during taxane chemotherapy. Nevertheless, if pain occurs, it is important to quickly identify and treat it. The colored body image is a simple tool for visualizing and sharing the patient’s pain experience. It may be a useful tool for helping the patient and the health care personnel to understand, interpret and treat pain during and after chemotherapy.