Effects of Physical Therapy on Pain and Mood in Patients with Terminal Cancer: A Pilot Randomized Clinical Trial

Abstract

Objectives:

The objective of this study was to determine the effects of physical therapy, including massage and exercise, on pain and mood in patients with advanced terminal cancer.

Design:

The design was a randomized controlled pilot study.

Subjects:

Twenty-four (24) patients with terminal cancer were randomly assigned to one of two treatment groups.

Interventions:

Group A received a physiotherapy intervention consisting of several massage techniques, mobilizations, and local and global exercises. Group B received a simple hand contact/touch to areas of pain (cervical area, shoulder, interscapular area, heels, and gastrocnemius), which was maintained for the same period of time as the intervention group. All patients received six sessions of 30–35 minutes in duration over a 2-week period.

Outcomes:

Outcomes were collected at baseline, at 1 week, and at a 2-week follow-up (after treatment completion) by an assessor blinded to the treatment allocation of the participants. Outcomes included the Brief Pain Inventory (BPI, 0–10 scale), Memorial Pain Assessment Card (0–10 scale), and Memorial Symptom Assessment Scale (MSAS Physical, Psychological, 0–4 scale). Baseline between-group differences were assessed with an independent t-test. A two-way repeated-measures analysis of variance was used to examine the effects of the intervention.

Results:

There were no significant between-group baseline differences (p>0.2). A significant group×time interaction with greater improvements in group A was found for BPI worst pain (F=3.5, p=0.036), BPI pain right now (F=3.94, p=0.027), and BPI index (F=13.2, p<0.001), for MSAS Psychological (F=8.480, p=0.001). Conclusions: The combination of massage and exercises can reduce pain and improve mood in patients with terminal cancer. A sustained effect on pain and psychologic distress existed; however, parameters such as physical distress and the least pain were no greater in the intervention group as compared to the sham.

Introduction

T he clinical use and examination of the potential benefits of complementary and alternative medicine in the management of patients with cancer has increased in recent years.^1,2 Despite the historical viewpoint that manual therapy applied to a patient with cancer may generate metastasis,³ one of the most employed therapies in palliative care is massage.⁴ Massage has been shown to be effective for reducing pain, anxiety, distress, and improving quality of life in patients with cancer.^5
–7 Furthermore, massage has also been shown to increase blood and lymphatic circulation, decrease inflammation and edema, relax musculature,⁸ increase dopamine and serotonin levels and also the number of lymphocytes.^9,10

One of the major limitations in examining the effectiveness of manual massage in patients with cancer is the lack of standardization in its application (technique and dosage) and the difficulty in including a control group.¹¹ Despite the lack of scientific evidence in support of massage in cancer, it is often used as the standard care.¹²

Although the beneficial effects of physical therapy in palliative care services has been studied¹³ and shown to exhibit clinical benefits in certain populations,¹⁴ less information exists on the effects of specific physical therapy techniques,¹⁵ such as manual therapy in patients with cancer. Nevertheless, previous studies limited interventions to specific tumors,^16,17 but did not include heterogeneous populations^18,19 with different types of cancer. Furthermore, it has not been determined whether massage is beneficial for patients with terminal cancer. Therefore, the aim of the current study was to determine the effects of physical therapy, including massage therapy and exercise on pain and mood in patients with advanced terminal cancer.

Materials and Methods

Participants

Consecutive patients (n=92) admitted to the Oncology University Hospital Salamanca were examined for potential eligibility to participate. Inclusion criteria were the following: (1) patient in the Oncology Department of University Hospital Salamanca; (2) older than 18 years old; and (3) diagnosed with any type of tumor in stage III-IV. The patient had to report an intensity of pain >4 on a numerical pain rate scale,²⁰ although pain was not necessarily the main symptom.

Patients were excluded if they (1) exhibited fragile tissue (skin, hair, or bone); (2) suffered from any systemic status (e.g., neutropenia, hypercalcemia, hypothyroidism, or anemia);^18,20 (3) were unconscious; (4) were unable to complete the questionnaires used;²¹ (5) were projected to have less than 20 days to live;²⁰ or (6) if they had undergone manual therapy within the past 4 weeks.²⁰ The study protocol was approved by the local Ethics Committee, Universidad de Salamanca, (24/2011) and conducted according to the Helsinki Declaration. All subjects signed informed consent prior to their participation.

Randomization

Patients were randomly assigned to receive either physical therapy (intervention) or manual touch (control). A computer-generated randomized table of numbers created prior to the beginning of the study was utilized to determine the randomization scheme. All patients received treatment on the day of the initial examination.

Interventions

The physiotherapy intervention in the experimental group consisted of several different therapeutic massage techniques: effleurage, petrissage, and strain/counterstrain techniques over the tender points.⁶ Hypoallergenic massage cream was used for manual therapies.²² In addition, the patients received passive mobilization, active-assisted or active-resisted exercises, and local- and global-resisted exercises, as well as proprioceptive neuromuscular facilitation (PNF)^23,24 applied over joints and tight/painful muscles. The choice, duration, and strength of each session was determined by the therapist based on the patient response to the intervention.

The control group received a simple hand contact or “simple touch,” which is considered an optimal control-sham condition.¹¹ This simple contact was placed on areas of pain and maintained for the same period as in the intervention group. The treated areas included the lower cervical area, shoulder, interscapular area, heels, dorsal foot, and gastrocnemius.²⁵

In both groups, risk areas (e.g., location of tumors, catheters, surgery) were avoided. All patients received six sessions of 30–35 minutes in duration over a 2-week period.¹¹

Outcome Measures

Primary outcomes: Changes in pain

The Brief Pain Inventory (BPI) was calculated by the average of enjoyment of life, activity, walking, mood, sleep, work, and relation with others that was also scored by 0 (does not interfere) and 10 (interferes completely). A 1.0–1.5-point difference on a 0–10-point scale is considered a clinically important change in pain.^26,27 Additionally, each scale for worst pain, least pain, mean pain, and current pain was scored from 0 (no pain) to 10 (worst pain).^26,28

The effect of treatment was also measured by changes of pain intensity using the Memorial Pain Assessment Card (MPAC; 0–10, 10: worst pain).²⁹ The sustained effects on pain were measured by the BPI.

Secondary outcomes

Secondary outcomes included pre–postintervention differences of the mood, as measured by the mood scale (0–10, 10: best mood) of the MPAC.²⁹ Physical and emotional symptom distress was measured using the Memorial Symptom Assessment Scale (MSAS), which evaluates the presence of and the distress associated with symptoms within the prior week. Degree of physical symptom distress ranges from 0 (not present) to 4 (very much). Frequency of psychologic symptoms is rated from 1 (rarely) to 4 (almost constantly). The MSAS yields a global distress index, physical symptom subscale score (MSAS Phys), and a psychologic symptom subscale score (MSAS Psych). The MSAS Phys was calculated as the average distress for the 12 physical symptoms: lack of energy, lack of appetite, pain, dry mouth, feeling drowsy, weight loss, shortness of breath, nausea, constipation, cough, swelling of arms or legs, and difficulty swallowing. The MSAS Psych was calculated as the average frequency of the five psychologic symptoms: worrying, feeling sad, feeling nervous, feeling irritable, and difficulty concentrating. The Global Distress Index was the average frequency of four psychologic symptoms (worrying, feeling sad, feeling nervous, feeling irritable) and average distress associated with six physical symptoms (lack of energy, lack of appetite, pain, dry mouth, feeling drowsy, constipation).^30
–32 Clinically important changes have not been defined for the MSAS.

Outcomes were collected at baseline, at 1-week follow-up, and at 2-week follow-up (after completion of the treatment). A therapist blind to group assignment collected all outcomes. In addition, changes in mood evaluated with the MPAC were assessed before and after each treatment session (within-sessions changes).

Sample Size Calculation

All sample size calculations were performed using Spanish ENE 3.0 software (Autonomic University of Barcelona, Spain). The calculations were based on detecting differences of 1.7 units in BPI at postintervention data, assuming a standard deviation of 1.4; an alpha level (α) of 0.05, and a desired power (β) of 80%. These assumptions generated a sample size of 12 subjects per group.²⁰

Statistical Analyses

Statistical analysis was conducted with the SPSS 16.0 package (SPSS, Chicago, IL). Mean, standard deviation, or 95% confidence intervals of the values are presented. The Kolmogorov-Smirnov test was use to assess the distribution of quantitative data. Baseline variables were compared between groups using the independent Student t-tests for quantitative data and χ² analysis for categorical data. Separate 3×2 mixed model analyses of variance (ANOVAs) with group (intervention, control) as between-subjects factor and time (pre-post1-post2) as within-subjects factor were used to examine the main effects of the intervention on BPI and MSAS outcomes. Separate 3×2 mixed model ANOVAs were performed for each outcome measure. The hypothesis of interest was the Group×time interaction. If a significant interaction was identified, the Bonferroni post-hoc analysis was performed to examine differences from baseline to each time point between groups to investigate between-group differences. The statistical analysis was conducted at a 95% confidence level. A p-value<0.05 was considered statistically significant for all analyses. An intention-to-treat analysis was performed using the last-observation-carried-forward approach. Finally, intragroup and intergroup effect sizes were calculated according to the Cohen d statistic. An effect size <0.2 reflects a negligible difference, between ≥0.2 and ≤0.5 a small difference, between ≥0.5 and ≤0.8 a moderate difference, and ≥0.8 the effect size suggests a large difference.

Results

The final sample was composed of 24 subjects with cancer. Figure 1 shows the recruitment and retention of the patients for the study. Twelve (12) patients were randomly assigned to the intervention group, and the remaining 12 patients to the control group. Patients assigned to the control group were offered the same physiotherapy treatment after study completion.²⁵

FIG. 1.

Flow diagram of subject recruitment and retention throughout the course of the study.

The experimental group consisted of 2 women and 10 men, aged 46–68 years, and the control group consisted of 4 women and 8 men, aged 18–78 years. In each group, 50% of the tumors were within the lung, but also included melanomas, sarcomas, prostate, colon, pancreas, and breast. Tumor metastases were mainly located within the skeleton, followed by the hepatobiliary system. The time of diagnosis ranged between 1 and 64 months in the experimental group, and between 2 and 96 months in the control group. No significant differences on baseline characteristics between both groups were found (Table 1).

Table 1.

Baseline Demographics for Both Groups ^a

	Control group	Intervention group	Statistical value (p-value)
Gender (male/female)	8/4	10/2	0.89 (0.35)
Age (years)	54±8	55±21	0.1 (0.92)
Tumor (lung, melanoma, sarcoma, pancreas, breast)	6/2/1/1/1/1/0	6/1/1/2/1/0/1	12.0 (0.60)
Kind of metastases (bone, hepatobiliary, lung, ganglion)	5/3/2/2	8/4/0/0	4.83 (0.18)
Time of diagnosis (months)	17.5±23.4	25.8±34.1	0.7 (0.49)
MPAC
VAS	6.0±2.0	7.5±2.0	1.85 (0.08)
Pain	4.7±1.2	5.3±1.3	1.33 (0.2)
Mood	5.3±1.4	5.8±0.3	0.91 (0.38)

Data are mean±standard deviation except for gender, tumor, and metastasis.

MPAC, Memorial Symptom Assessment Scale; VAS, visual analogue scale.

BPI

The two-way ANOVA revealed a significant group×time for BPI worst pain (F=3.588, p=0.036), BPI pain right now (F=3.940, p=0.027), and BPI index (F=13.267, p<0.001). Post-hoc analysis revealed that improvements in the intervention group were significantly greater than in the control group for the first evaluation (worst pain and current pain) and for the first and second evaluation (total BPI index). By contrast, the comparisons did not reveal significant differences for BPI pain on mean (F=2.160, p=0.127) and least pain (F=0.576, p=0.027) (Table 2). Within-experimental group effect sizes were large for pre–post1 and pre–post2 (d>0.8) for BPI worst pain, BPI current pain, and BPI index (only for pre–post2), although the BPI least pain had a small effect size (pre–post1: d=0.07; pre–post2: d=0.07). Within-group effect sizes for the control group were small or even negative for all variables, with exception of the BPI least, pain which exhibited a moderate effect size (pre–post1: d=0.35; pre–post2: d=0.43).

Table 2.

Baseline, Middle Treatment Session, Final Treatment Session, and Change Scores for BPI and MSAS

Outcome group	Baseline	Middle of the intervention	End of intervention	Within-group change scores (pre vs. post2)	Between-group difference in change scores (pre vs. post2)
BPI Worst Pain
Experimental	9.5±1.17	8.5±1.31	7.83±1.85	1.67 (0.41, 2.92)^a	−1.5 (−3.08, −0.08)^a
Control	7.67±2.15	7.5±1.57	7.5±1.0	0.16 (−0.94, 1.28)
BPI Least Pain
Experimental	3.33±2.46	3.17±2.44	3.17±2.38	0.15 (−2.41, 2.75)	1.1 (−1.64. 3.64)
Control	4.33±2.93	3.33±2.74	3.2±2.36	1.13 (0.46, 1.87)^a
BPI Pain on the Average
Experimental	6.5±1.68	5.5±1.78	5.33±1.56	1.17 (−0.69, 3.02)	−1.33 (−3.26, 0.6)
Control	5.5±2.32	5.83±1.95	5.67±1.56	−0.17 (−0.87, 0.54)
BPI Pain Right Now
Experimental	7.5±1.98	5.17±3.27	5.33±3.05	2.17 (0.61, 3.72)^a	−2.0 (−3.9, −0.1)^a
Control	5.67±2.15	5.33±2.31	5.5±1.78	0.17 (−1.13, 1.46)
BPI Index
Experimental	8.48±1.19	8.12±1.62	6.78±2.6	1.7 (0.37, 3.04)^a	−2.68 (−4.17, −1.18)^a
Control	5.48±2.13	5.57±1.96	6.45±1.64	−0.98 (−1.79, −0.16)^a
MSAS Phys
Experimental	1.89±0.37	1.6±0.38	1.49±0.39	0.4 (0.17, 0.64)^a	−0.18 (−0.47, 0.11)
Control	1.1±0.6	0.87±0.64	0.88±0.53	0.22 (0.02, 0.42)^a
MSAS Psych
Experimental	2.27±0.89	1.7±0.83	1.77±0.85	0.5 (0.14, 0.86)^a	−0.6 (−1.03, −0.17)^a
Control	1.2±1.11	1.33±1.22	1.3±1.25	−0.1 (−0.38, 0.18)
Global Distress Index
Experimental	4.56±1.21	3.83±1.07	3.83±1.09	0.72 (0.11, 1.34)^a	−0.54 (−1.24, 0.16)
Control	2.79±2.0	2.54±2.02	2.61±1.75	0.18 (−0.21, 0.57)

Values are expressed as mean±standard deviation for Baseline and Final means and as mean (95% confidence interval) for within- and between-group change scores.

Statistically significant (95% confidence interval).

BPI, Brief Pain Inventory; MSAS, Memorial Symptom Assessment Scale.

MSAS

The two-way ANOVA showed a significant group×time interaction for MSAS Psych (F=8.480, p=0.001). Post-hoc analyses revealed differences between groups at the first evaluation. No significant differences for Global Distress Index (F=2.209, p=0.122) and MSAS Phys (F=0.885, p=0.420) were observed (Table 2). Within-experimental group effect sizes were large (pre–post1: d=0.77; pre–post2: d=1.05) for MSAS Phys, and medium (pre–post1: d=0.66; pre–post2: d=0.58) for MSAS Psych. The control group exhibited moderate effects for MSAS Phys (pre–post1: d=0.37; pre–post2: d=0.39), and small effects (d<0.0) for MSAS Psych.

Pre–post intrasession MPAC differences

The two-way ANOVA showed a significant group×time interaction for MPAC pain differences (F=7.416, p=0.04). Post-hoc analyses identified differences between the first assessment, with greater improvement for the experimental group, but not in the other two periods. However, the analyses did not reveal a significant group×time interaction for MPAC mood differences (F=0.174, p=0.841, Table 3).

Table 3.

Comparisons of the Increment Pre–Postintervention for the MPAC Outcomes

Outcome group	1st session	3rd session	6th session	Group×time p-value	Group factor p-value
MPAC pain differences
Experimental	1.83 (1.189, 2.48)^a	1.01 (0.489, 1.51)	1.5 (0.76, 2.24)	0.04^a	0.07
Control	0.0 (−0.65, 0.65)	1.0 (0.7, 1.31)	1.3 (0.59, 2.07)
Mood MPAC differences
Experimental	2.33 (1.92, 2.75)	2.17 (1.72, 2.62)	2.0 (1.39, 2.6)	0.84	<0.01^b
Control	1.0 (0.58, 1.42)	0.67 (0.22, 1.16)	0.3 (−0.27, 0.94)

Statistically significant (95% confidence interval) between first pre–postintervention differences between groups.

Statistically significant (95% confidence interval) between both groups.

MPAC, Memorial Symptom Assessment Scale.

Discussion

To the authors' knowledge, this is the first randomized controlled study that examined the effects of massage and exercises in patients with terminal cancer. The current study demonstrated that the combination of massage and exercises can reduce pain and can improve mood in patients with terminal cancer. It was also shown that a sustained effect on pain and psychologic distress existed; however, parameters such as physical distress and the least pain did not increase more in the experimental group.

Despite the lack of studies examining the impact of physiotherapy for patients with terminal cancer,⁴ the current results are promising in palliative care.²² Patients with cancer often exhibit myofascial pain,³³ which has resulted in the implementation of physiotherapy techniques in patients after breast cancer surgery,^34,35 and head and neck surgery.³⁶

The analgesia produced by the intervention in this study is consistent with that obtained in other studies.²⁵ However, in the current case, a significant sustained effect was demonstrated, at least in the current level of pain and in the worst pain, as well as tendency to reduce the pain on the average. Therapist contact has been recognized to have positive effects in patients who have terminal illness.¹⁴ Similar to the current results, massage has been shown to be effective in reducing immediate stress in palliative care in patients with cancer, including terminal patients.²¹

The protocol in this study included manual techniques and exercises, such as PNF. Fatigue was not evaluated, although data on the physical MSAS showed no differences between groups. Previous studies had shown that physical activity improves standardized fatigue and quality of life of patients with terminal cancer¹⁸ as well as humor and general welfare in mastectomy.³⁷ However, in these studies the intervention protocols were different and in some cases, the life expectancy of patients was higher.¹⁹

In the current study, the results were positive; however, the Global Index of Distress and physical distress only showed changes in intragroup analysis within the intervention group. In patients with nonterminal specific cancers (e.g., breast cancer) passive exercises did not induce positive results on pain,¹⁶ although active and passive exercises have had a positive impact on quality of life in the long term.³⁸ On sternocleidomastoid tumors,³⁹ kinesiotherapy failed to increase the amount of movement and reduce postural defects, although pain was reduced after lung surgery.¹⁷ However, this study is the first to assess pain and distress related to symptoms after application of exercise therapy in patients with terminal cancer.

Although this study revealed promising results, potential limitations should be considered. First, it is difficult to obtain improvements in individuals with terminal cancer,¹⁸ which can explain the lack improvement for some outcomes. In the current study, the control group (simple touch) improved in the least pain (BPI), the BPI index, and the MSAS Phys, which was unexpected. However, placebo has been shown to be effective in other studies.²⁵ Furthermore, patients with different types of terminal cancer were included. Second, the high dropout rates should also be considered, which could have biased the results;⁴⁰ but this limitation is inherent when patients with a terminal cancer were included. Third, the therapy group received different manual interventions based on the patients' response, which reflects clinical daily practice but makes it difficult for others to reproduce the exact protocol. Finally, the sample size in this study may be considered small; however, adequate power calculations to obtain between-group differences were previously conducted. In addition, previous studies included similar²¹ or smaller sample sizes.¹⁷ Nevertheless, to further confirm current results, a randomized clinical trial with a greater sample size is currently planned.

Conclusions

The current study revealed that physical therapy including massage and exercise seem to be effective in producing immediate reductions of pain and distress and aspects related to symptoms and mood in patients with terminal cancer. Future studies including greater sample sizes with different types of cancer are planned to further elucidate the role of physical therapy in patients with terminal cancer.

Footnotes

Disclosure Statement

No financial conflicts exist.

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