Supervised physical therapy in women treated with radiotherapy for breast cancer

ABSTRACT Objective: to evaluate the effect of physical therapy on the range of motion of the shoulders and perimetry of the upper limbs in women treated with radiotherapy for breast cancer. Methods: a total of 35 participants were randomized into two groups, with 18 in the control group (CG) and 17 in the study group (SG). Both of the groups underwent three evaluations to assess the range of motion of the shoulders and perimetry of the upper limbs, and the study group underwent supervised physical therapy for the upper limbs. Results: the CG had deficits in external rotation in evaluations 1, 2, and 3, whereas the SG had deficits in flexion, abduction, and external rotation in evaluation 1. The deficit in abduction was recovered in evaluation 2, whereas the deficits in all movements were recovered in evaluation 3. No significant differences in perimetry were observed between the groups. Conclusion: the applied supervised physical therapy was effective in recovering the deficit in abduction after radiotherapy, and the deficits in flexion and external rotation were recovered within two months after the end of radiotherapy. Registration number of the clinical trial: NCT02198118.


Sample characteristics
The study population consisted of women treated at the Mastology Clinic and Radiotherapy Service who met the following inclusion criteria: (i) diagnosis of unilateral

Evaluation protocol and physical therapy intervention
The participants were evaluated at three different time points: pre-RT (evaluation 1), post-RT (evaluation 2), and two months after the end of RT (evaluation 3).
The variables evaluated were the ROM of the shoulder joint and perimetry of the upper limbs. Shoulder ROM was evaluated by assessing flexion, extension, abduction, adduction, and internal and external rotation, which were actively performed by the participants.
These measurements were made using a Carci® goniometer, and positioning was performed according to the protocol proposed by Marques (12) . Perimetry involved the performance of measurements at six different points: point A -in the metacarpophalangeal joints of the second, third, fourth, and fifth fingers; point B -an imaginary line pointing in the direction of the metacarpophalangeal joint of the first finger; point C -10 cm below the olecranon; point D -6 cm below the olecranon; point E -6 cm above the olecranon; and point F -10 cm above the olecranon (13) . The subjects remained in a sitting position with the arm resting on the thigh and the forearm supinated. The measurements were bilateral.
The selected participants were randomly divided into two groups: one group was subjected to the evaluations described in the paragraph above and was Leal NFBS, Oliveira HF, Carrara HHA. designated the control group (CG). Another group was subjected to supervised kinesiotherapy of the upper limbs and was designated the study group (SG). The randomization plan was generated using computer software that distributed the participants into the two groups, following the sample size obtained in the sample calculation. The participants were distributed into each group during evaluation 1. The distribution was random but non-blinded.

Statistical analysis
Considering an α of 0.05, a test power of 80%, before and after RT, and a standard deviation of 4.5, a required sample size of 16 was calculated using Power and Sample Size Calculation version software 2.1.31 (15) .
The analysis involved the assessment of the intention to treat (ITT) and included all participants in the study group who were originally allocated by randomization, irrespective of the period of initiation of treatment, discontinuation of therapy, nonadherence to the protocol received, or the use of treatment protocols that differed from the original (16) .
For the intragroup analysis, an unpaired t-test was used to compare the goniometry results between the ipsilateral and contralateral limbs within the same evaluation. One-way analysis of variance (ANOVA) was used to assess differences in perimetry among the three evaluations. For intergroup analysis, unpaired t-tests were used to evaluate the goniometry results in the ipsilateral limb and differences in perimetry. P-values lower than 5% were considered statistically significant. Table 1 shows the characteristics of the participants with respect to age, body weight, type and duration of surgery, and disease staging.   Table 2.

The intragroup point-by-point analysis of perimetry
indicated no significant differences in perimetry.
The deficit in the ROM observed in the CG and SG in evaluation 1 can be attributed to surgery because ROM restrictions and functional problems in the shoulder may still be present at six months or more after surgery (20,23) .
The CG maintained the deficit for external rotation throughout the study period. In the SG, the deficit in the abduction movement was recovered in evaluation 2, and the deficits in flexion and external rotation were recovered in evaluation 3, demonstrating the importance of conducting supervised physical therapy in women undergoing RT for breast cancer.
A study that evaluated the ROM in the shoulder of women before and after RT indicated an increase in the deficit of flexion and abduction in the control group and a decrease in the group subjected to physical therapy (10) .
Moreover, the ROM in women who underwent physical therapy improved during the RT period and worsened in women who did not undergo physical therapy (5) . Physical therapy results in a gain in shoulder ROM when applied during RT; this effect can be observed immediately after the end of RT (5) and persists for up to six months after RT (10) . Our results are consistent with those of previous studies.
Muscles should be at their natural length and have a sufficient ability to glide under adjacent soft tissues (i.e., skin and subcutaneous tissue) to ensure adequate mobility of the joints. Full range of flexion and abduction requires proper functioning of the major and minor pectoral, latissimus dorsi, teres major, subscapularis, and rhomboid muscles. Adequate functioning of the serratus anterior muscle is also required for the upward rotation of the scapula. For external rotation, the pectoralis major, latissimus dorsi, teres major, and subscapularis muscles must be at their natural length and be able to glide (21) .
Because of their origin and insertion, the pectoral and serratus anterior muscles are approached and can be damaged during surgery for breast cancer. Furthermore, these muscles are located in the areas indicated for RT (6) . Therefore, the movements used to recruit these muscles may be adversely affected by the adhesion and fibrosis caused by RT (5,10,19,24) .
The analysis of the mean difference in the upper limb perimetry at each study point indicated no significant differences in the intragroup comparison.
Although intergroup analysis indicated a significant difference in point F in evaluation 3, this result indicates intergroup differences but not the presence of lymphedema, as shown in Table 3. The analysis of mean perimetry values indicated that the participants did not present with lymphedema after surgery and did not develop this complication during RT or two months after its completion. The same result was found in another study, wherein lymphedema was not observed even six months after the completion of RT (10) .
The risk of the onset of lymphedema is associated with several factors, including radical surgery, extent of axillary dissection, and application of RT. However, preexisting lymphatic insufficiency of genetic and traumatic origin may also be responsible for the emergence of lymphedema. After axillary lymphadenectomy , the body adjusts to compensate for the removal of lymph nodes to allow for the transport of lymph, thereby preventing the development of lymphedema (9, [24][25] . The exercises used in this study were free active exercises consisting of a series of 15 repetitions and were performed twice a week during the RT period. These exercises were intended to maintain the movement of joints and soft tissues, minimize the loss of flexibility and the formation of contractures and ensure early rehabilitation (19) . The supervised kinesiotherapy helped recover the deficit in the shoulder ROM between the ipsilateral and contralateral limbs.

Conclusion
Supervised physical therapy that targets the ROM of shoulders of women treated with RT for unilateral breast cancer helps increase the ROM of flexion, abduction, and external rotation. The deficit in the abduction was recovered after RT, and the deficits in flexion and external rotation were recovered two months after the end of RT.
The physical therapy protocol applied did not change the upper limb perimetry, a result that is consistent with the fact that the participants did not have lymphedema and did not develop this condition during the study period.
These results indicate the need to perform this type of physical therapy in patients treated with RT for breast cancer.