Introduction

The prevalence of breast cancer-related lymphedema (BCRL) ranges from 8 to 44% [1,2,3], resulting in a high cost to patients due to the frequent number of visits for seeking treatment [4,5,6]. Previous reports have shown that specific symptoms associated with lymphedema, such as pain, may cause greater distress and a lower quality of life in comparison to the size or volume of the affected limb [6,7,8].

Patients with BCRL experience a wide range of psychological distress, physical immobility including impaired limb movement, and pain [9, 10]. In addition, BCRL can cause skin alterations, fibrosis, and heaviness in the arm [8, 11, 12]. Chronic pain in the arm may interfere with patients’ abilities to follow daily routines, thus leading to disability. Recent studies showed that while there was no relationship between size or volume of lymphedema and distress [4, 13], there was a significant association between lymphedema, pain, and the level of distress experienced by patients [6]. Evidently, alleviating pain can improve a patient’s sensation, function, and perceived quality of life.

The combined decongestive therapy (CDT) is the practice of combining treatment techniques together, including manual lymphatic drainage, bandaging, compression garments, exercise, and self-care. This method is considered as the gold standard treatment for lymphedema as it is an intensive therapy program consisting of two phases, phase I as the decongestion phase and phase II as the maintenance phase [14]. Phase I is conducted with professional therapist and that phase II involves self-manual lymphatic drainage and -reduction practices including skin care. It is also worth mentioning that CDT is not a cure for BCRL, but its main purpose is to alleviate swelling, pain, heaviness, and improve quality of life [14, 15]. Although it has been primarily developed for limb volume reduction in lymphedema patients, there are limited data in favor of its effect on pain alleviation [15, 16].

Similar to many other countries, CDT is not covered by insurance companies in Iran. Therefore, due to financial constraints, patients often fail to start or complete their required treatment procedures and had to cut short their treatment. Since pain intensity is reduced significantly during the early treatment sessions, we hypothesize that it would not be necessary for patients to continue further with volume reduction at outpatient clinics when they achieved satisfactory outcomes. As a result, those patients can undergo few number of treatment sessions to reduce pain and/or heaviness intensity and continue with self-treatment procedures for volume reduction at home at an economic cost. Thus, present study aimed to assess the effect of CDT on intensity of pain and heaviness among patients with BCRL and investigate the minimal number of CDT treatment sessions that would be required to significantly reduce the severities of the symptoms in patients with lymphedema in their ipsilateral arm after breast cancer treatment.

Methods

Design and participants

A longitudinal study was conducted at Breast Cancer Research Center (BCRC) in Tehran, Iran. From August 2015 to January 2017, patients with post mastectomy upper limb lymphedema that were referred to the lymphedema clinic for upper arm volume reductions were recruited. We included female breast cancer patients and those who clinically were diagnosed with post mastectomy secondary lymphedema of ipsilateral arm. Also, patients who had a sensation of pain and/or heaviness in the affected side were included.

The following exclusion criteria were used: breast cancer recurrence, other associated malignancies, any previous treatments for lymphedema, affliction with bilateral lymphedema, absolute contraindication for CDT (acute systemic infection, lymphangitis, erysipelas, deep vein thrombosis, congestive heart failure), presence of neuropathy in upper section of body, untreated wounds or skin diseases, as well as any known musculoskeletal disease in the upper limbs. None of the patients who fulfilled inclusion criteria was excluded from the study due to lack of financial resources. The cost of treatment for few patients who were not able to pay was completely waived.

The study flow chart is presented in Fig. 1.

Fig. 1
figure 1

Flowchart for data collection process from 2015 to 2017

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Procedure

All patients were visited by a CDT certified physician. Demographic and clinical data were obtained from patients’ medical records. The first phase of CDT, known as the therapeutic phase, was performed on a daily basis (5 days/week) for 3 to 4 weeks, giving a total of 15 to 20 sessions. However, if during the sessions, patients’ pain or heaviness severity was entirely relived, the sessions were ceased. Each session consisted of 40 min of Dr. Vodder’s method of manual lymph drainage [17] performed by a trained therapist followed by appropriate skin care procedures and moisturization. Multilayer short stretch bandaging was applied using Lohmann and Rauscher’s compression bandaging [Lohmann & Rauscher GmbH & Co. KG, Rengsdorf, Germany and Vienna, Austria]. All patients were instructed to practice remedial exercises of their upper extremities at least two times per day with their bandages on at home. Remedial exercises were given with diaphragmatic breathing exercises in between. The patients sat comfortably, relaxed, place their hands over their abdominal muscles, and took deep breaths through the nose followed by prolonged expiration through the mouth without any strenuous effort. The following order was adopted for remedial exercises: protraction, depression, shoulder extension, elbow flexion and extension, wrist flexion and extension, and ball squeeze.

Patients’ education regarding at-home exercise was provided once at first visit and continued if patient experienced any difficulties.

Measures

1. A 100-mm visual analog scale (VAS) [18] was used to determine the severity of pain and heaviness. Patients quantified their pain and heaviness sensations on two separate VAS rating on a scale ranging from 0 to 10, with 0 being none and 10 being most severe. The VAS was completed in the first day prior to commencing the CDT program with similar subsequent forms being completed after the 3rd, 5th, 7th, 10th, and 15th sessions in a 3-week period. The severity of pain and heaviness was categorized into three severity groups based on baseline scores (mild: < 4, moderate: 4–6, and severe: > 6) [18]. Downward transition for at least one category in the severity of each parameter (that are severe to moderate, moderate to mild, and mild to none) was considered as a clinically important improvement [19].

2. Limb volumes for both arms were measured before initiation of CDT and at the end of treatment for each patient. Volume was measured using water displacement method by placing the arm in a column of water to a depth of 15 cm above the elbow and the volume difference between two arms were recorded.

Statistical analysis

Descriptive analyses, including frequencies, means, and standard deviations, were used to explore the data. Repeated measure analysis of variance was conducted to test the effect of time on the severities of pain and heaviness while age, afflicted side with lymphedema, history of chemotherapy, and radiotherapy were considered as covariates. Comparisons between two measurements were performed with Wilcoxon signed ranks. Bonferroni adjusted p value was set to 0.0025. Statistical analyses were conducted using SPSS Version 18.0 (PASW Statistics for Windows, Chicago).

Results

All 169 patients with pain and/or heaviness were studied. Of these, 14 had pain only, 37 had heaviness only, and 118 had both pain and heaviness. Demographic and clinical characteristics of patients are summarized in Table 1. Overall, 133 patients received 15 or more sessions. The remaining patients received less than 15 sessions since in these patients, volume difference between the two arms became very small and the severity of their pain or heaviness reached to zero before completion of sessions.

Table 1 Demographic and clinical characteristics of patients
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Assessment of pain

Varying degrees of pain were reported by 132 (65.3%) patients. Repeated measure analysis revealed a significant effect of time of treatment on pain intensity (p value < 0.001, Table 2). Age, side afflicted with lymphedema, chemotherapy, and radiotherapy all did not interact with the effect of the number of treatments received and the intensity of pain felt. Prior to CDT, 97/132 (73.5%) indicated moderate or severe pain in their affected arm. This value decreased to 58.3%, 40.92%, 25%, 10.6%, and 3% after 3, 5, 7, 10, and 15 treatments, respectively.

Table 2 Result of one-way repeated measure analysis of variance to test the effect of treatment numbers on pain and heaviness intensity
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According to Table 2, the median pain score was reduced from 5 to 4 after three treatments and decreased even further to a value of 1 after seven treatments and zero after ten treatments. Figure 2 depicts the cumulative percentage of patients who reported a reduction in pain intensity of at least one grade during their CDT sessions. The frequency of patients reporting at least a one grade reduction in pain increased continually from the first to the 15th session. As shown in Fig. 2, after five sessions, pain reduction was noticeable in 64.4% of patients, and after seven sessions, this percent was increased to 86.4%. Upon completion of 15 sessions, pain reduction was reported by 97.6% of patients.

Fig. 2
figure 2

Cumulative percentage of patients reporting at least a one grade improvement in pain intensity during CDT sessions

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Assessment of heaviness

From the 169 patients, 155 (92%) reported heaviness in various degrees. Out of 155, a total of 121 (78%) reported moderate or severe heaviness. Through repeated measure analysis, there was a significant reduction in heaviness during treatment course (p value < 0.001), as illustrated in Table 3. Age, side afflicted with lymphedema, past treatments of chemotherapy, or radiotherapy did not influence the effect of treatment numbers on pain reduction. The percentages of patients with moderate or severe heaviness prior to CDT (78%) decreased to 69.7%, 54.8%, 33.6%, 17.4%, and 3.2% after 3, 5, 7, 10, and 15 treatments, respectively.

Table 3 Changes in severities of pain and heaviness from one to ten sessions of CDT
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Figure 3 presents the cumulative percentage of patients who reported at least a reduction of a grade of 1 in their intensity of heaviness felt. Majority of patients reported a noticeable reduction in heaviness as the number of CDT sessions progressed from one to 15 treatments. After 5 sessions, 53.5% of patients had a reduction of one grade in heaviness, while after 7 and 15 treatments, 83% and 97.9% of subjects reported such reductions, respectively.

Fig. 3
figure 3

Cumulative percentage of patients reporting at least a one grade improvement in heaviness intensity during CDT sessions

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Discussion

The findings indicated that a considerable number of breast cancer patients with lymphedema suffer from pain and heaviness. Treatment of BCRL using CDT not only significantly reduced limb volume, but also the intensity of pain and heaviness experienced from early on during treatment. Based on our data, a large percentage of patients experienced at least a single-grade reduction of pain and heaviness after seven sessions of treatment of CDT.

To the best of our knowledge, the current research is the first longitudinal study that investigates the effect of CDT on intensity of pain and heaviness during the early periods of therapy. The intensity of pain and heaviness progressively improved after CDT sessions in 98% of BCRL patients. Similar findings were reported by other investigators [9, 15, 16, 20] where for instance, a study by Hamner et al. [15] reported that after treatments, pain intensity was reduced from 6.9 to 1.1 on the VAS. However, our study not only confirms their findings in illustrating the effect of CDT in controlling pain, but also addresses the minimal number of treatments required to sufficiently reduce the severity of the pain.

Since CDT tends to be time-consuming and requires the patient’s cooperation throughout treatment phases, it is important for both the therapist and the patient to be assured that the pain will reduce soon after starting treatment. Although CDT can result in a marked decrease in volume and percentage of lymphedema, it takes at least 3 weeks for any noticeable results to occur. Meanwhile, pain intensity reduction during the early sessions can diminish patients’ distress and improve their compliance. The results depict that after five treatment sessions, pain intensity and heaviness was decreased by at least one category (severe to moderate or moderate to mild) in 64.4% and 53.5% of patients, respectively. These figures were elevated after the 7th session to 86.4% of subjects for pain and 83% for heaviness. This suggests that if the therapy continues for at least seven treatments, the majority of patients would feel a significant decline in the two symptoms, which can improve associated depressive symptoms and encourage patients to successfully complete their CDT course.

Certain patients in our clinic were unable to pay the fee for CDT and have to cut short their treatment despite the fact that in BCRC lymphedema clinic, patients are charged at a very low cost compared to the other centers. Patients with BCRL suffering from pain and who could not afford to pay for the full treatment course were still able to benefit from the minimal number of sessions and observe improvement in pain and heaviness sensed after just seven treatments at the outpatient clinic. After significant reduction of pain, patients were enabled to continue self-treatment procedures and follow in-home programs [16] more effectively while gaining maximum volume reduction of the arm. This strategy not only can reduce the cost of treatment, but also may possibly persuade insurance companies to at least cover a small portion of the CDT sessions for patients with pain.

Strengths and limitations

The main strength of the current study was its longitudinal design and its discrete measurements of pain and heaviness throughout the CDT course. Moreover, assessing the impact of the number of treatments on patients’ experience of pain and heaviness was an additional strength to the study. In the BCRC lymphedma clinic, CDT was performed by two well-trained therapists under the supervision of a lymphologist. However, similar to many studies, our study also suffers from certain limitations. One caveat is that we did not consider how long patients had lymphedema and the duration of the pain felt. In addition, the possible effect of lymphedema stage (I, II, and III) on the pain severity was not assessed. These would have shed light upon the possible interaction of chronic pain and any changes in its intensity while undergoing CDT. Moreover, we did not include the use of painkillers by patients. However, most patients with pain had already tested multiple painkillers but with little success, and so were referred to our clinic not only for volume reduction, but for pain alleviation as well.

Conclusions

The findings indicated that CDT could reduce the intensity of pain and heaviness in breast cancer patients who suffer from lymphedema. According to our results, it seems that with seven sessions of treatments, a vast majority of patients might benefit from a clinically important improvement. This would allow patients to still reap the health benefits of CDT at a lower cost and allow for better adherence to self-treatment strategies.