| | Quantitative and Clinical Description of Postural Instability in Women With Breast Cancer Treated With Taxane ChemotherapyPresented, in part, to the American Physical Therapy Association Combined Sections meeting, February 1–5, 2006, San Diego, CA; the Supportive Oncology meeting, October 6–8, 2005, Chicago, IL; and the International Society of Posture and Gait Research XVIIth Conference, May 29–June 2, 2005, Marseille, France. Abstract Wampler MA, Topp KS, Miaskowski C, Byl NN, Rugo HS, Hamel K. Quantitative and clinical description of postural instability in women with breast cancer treated with taxane chemotherapy. ObjectiveTo describe the postural control of women who received taxane chemotherapy for treatment of breast cancer using quantitative and clinically feasible measures. DesignProspective descriptive study. SettingUniversity-based comprehensive cancer center. ParticipantsTwenty women who completed taxane treatment for breast cancer and 20 healthy controls participated in this study. InterventionsNot applicable. Main Outcome MeasuresTwo quantitative measures of postural control were used, Sensory Organization Test (SOT) and center of pressure (COP) velocities. Two clinically feasible measures of postural control were used, the Fullerton Advanced Balance Scale (FABS) and Timed Up & Go (TUG) test. ResultsCompared with healthy controls, women with breast cancer had poorer postural control on all of the outcome measures. FABS and TUG scores correlated moderately with SOT and COP scores. ConclusionsAfter taxane chemotherapy, women with breast cancer show significantly increased postural instability compared with matched controls. Clinically feasible measures of postural control correlated with quantitative tests. These results suggest that these clinical measures may be useful to screen patients to determine who may benefit from rehabilitation. BREAST CANCER IS the most common cancer diagnosis in women in the United States, with 178,480 women expected to be diagnosed with the disease in 2007.1 Chemotherapy is often used to treat this type of cancer. In 1994, the U.S. Food and Drug Administration (FDA) approved paclitaxel (Taxol), a drug derived from the Pacific Yew tree, for the treatment of metastatic breast cancer. In 1999, the FDA expanded the approval to include women with locally advanced disease (eg, positive lymph nodes, but no distant metastases). However, because there are limited natural resources to produce paclitaxel the FDA approved docetaxel (Taxotere), a man-made drug with chemical properties similar to paclitaxel, for the treatment of locally advanced or metastatic breast cancer in 1998. Abraxane (paclitaxel protein-bound particles for injectable suspension) was approved in January 2005. These drugs comprise the taxane class of chemotherapy agents and are often used in combination with anthracyclines and cyclophosphamide (Cytoxan) to treat breast cancer. A growing body of evidence suggests these chemotherapy agents may improve survivorship and decrease the risk of local recurrence of breast cancer.2, 3 Therefore, as taxane use becomes increasingly common, it is important for patients and health care providers to understand the impact that side effects of these drugs may have on physical function in women with breast cancer. The side effects of taxanes include allergic reactions; neutropenia, anemia, and thrombocytopenia; alopecia; joint and/or muscle pain; mucositis; nausea; and peripheral neuropathy.4, 5, 6 Many of these effects are decreased with the use of medications such as erythropoietin, pegfilgastrim, and anti-emetics.7, 8, 9 Although many promising drugs are being tested, no effective peripheral nerve protectants are available at this time. Over half of the patients who receive paclitaxel, docetaxel, or Abraxane develop decreased deep tendon reflexes, increased vibration thresholds, or dysesthesias and paresthesias in a stocking and glove pattern.10, 11, 12, 13, 14 These patients may also show decreased sensory nerve action potential amplitudes on electrodiagnostic testing.10 A subset of these patients develop a painful peripheral neuropathy.15 Peripheral neuropathy can have a significant impact on physical function. Numerous studies have documented that diabetic peripheral neuropathy is associated with postural instability.16, 17, 18, 19, 20 There is also an increased risk of falls in this patient population.21 These patients show greater step width, decreased step length, and decreased gait speed in low light conditions on irregular surfaces.22 Differences in the temporospatial aspects of gait on challenging surfaces were also observed in adults with diabetic peripheral neuropathy who fell compared with those who did not fall.23 Although peripheral neuropathies are reported in women with breast cancer who are treated with taxane chemotherapy,10, 15, 24 to date, no studies have described postural stability. Therefore the primary purpose of this prospective study was to describe the postural stability of women who were treated with paclitaxel or docetaxel for breast cancer compared with matched healthy controls. We hypothesized that after the final infusion of taxane therapy, women with breast cancer would present with postural instability compared with matched healthy controls. In addition, the relationships between quantitative and clinically feasible measures of postural control were evaluated. Methods  Participants For the study, we recruited 20 women treated with taxane chemotherapy for breast cancer and 20 healthy women between the ages of 30 to 60. These women were matched on age, height, and weight. All women were screened for pre-existing vestibular, visual, somatosensory, orthopedic, and neurologic disease before entering the study. Women in the breast cancer group were included only if there was no evidence of central nervous system metastases. All women were required to have a corrected low-contrast visual acuity better than 20/60 and a corrected high-contrast visual acuity better than 20/40. These entry criteria were chosen because postural control is related to visual acuity, orthopedic problems, neurologic problems, and vestibular problems.25, 26, 27, 28 Women in the breast cancer group had received 4 cycles of doxorubicin (Adriamycin) and cyclophosphamide (Cytoxan) prior to beginning taxane therapy. All participants signed a written informed consent that was approved by the institutional review board and the protocol review committee at the university-based comprehensive cancer center before participating in the study. We asked women in both the breast cancer and the healthy control groups to complete 1 testing session. Women in the breast cancer group were asked to return and repeat all tests within 1 week of initial testing to establish the intrarater reliability of quantitative and clinically feasible measures of postural control. Women in the breast cancer group were tested within 30 days of their final taxane infusion and healthy controls were tested at the time of enrollment. All measures, except for the Fullerton Advanced Balance Scale (FABS), were performed by 1 physical therapist who was not blinded to participants’ health status. Measurement bias was low for the quantitative measures of postural control and the Timed Up & Go (TUG) test, because none of these tools require a subjective evaluation of performance of a task. However, measurement bias was controlled for the FABS as described below. All participants completed measures of height, weight, and visual acuity; a questionnaire regarding medical history and medication use; and quantitative and clinically feasible measures of postural control, as described below. In addition, all women completed several quantitative measures of peripheral neuropathy, including the total neuropathy score, the modified total neuropathy score, quantitative touch thresholds, quantitative vibration thresholds, and nerve conduction studies. As previously reported, the modified total neuropathy score (TNS) was found to be a clinically feasible measure to evaluate the severity of taxane-induced peripheral neuropathy15 and therefore, only mean modified TNS scores of breast cancer and healthy control groups are reported to indicate the severity of peripheral neuropathy (table 1). Measures of Participant Characteristics Height was measured in centimeters using a stadiometer. Weight was measured in kilograms using a calibrated scale. Medical history and medication use, including chemotherapy, were self-reported by participants using a questionnaire. If women reported they were using a medication with known effects on the central nervous system (ie, gabapentin [Neurontin], zolpidem [Ambien], venlafaxine [Effexor], fluoxetine [Prozac], or lorazepam [Ativan]) this was noted. No women were taking opioid medications. The total number of women using centrally acting medications in each group was recorded for data analysis. Medical history and medication use was confirmed by chart review for women in the breast cancer group. We measured visual acuity using 2 Bailey-Lovie log MAR charts,29,a one with high contrast letters and another with low contrast letters, and is reported as a log MAR score. Log MAR is an acronym for log10 of the minimal angle of resolution and was developed as an improved measure of visual acuity, given the limitations of the Snellen chart. As the letters on the chart become smaller, the angle of resolution also becomes smaller. Therefore the log MAR score represents the minimal angle of resolution which the person can clearly see. Participants stood 6.1m from the chart while keeping both eyes open. If the participant normally wore glasses, they were permitted to wear glasses during the entire testing session. The participant would read each line of progressively smaller letters until they reached a line where they made an error. The log MAR score was calculated by recording the log MAR score of the last complete line read minus .02 multiplied by the number of correct responses on the next smaller line. A log MAR score of 0 corresponds to 20/20 vision on a Snellen chart. A lower log MAR score indicates better visual acuity. Instrumentation and Data Acquisition for Quantitative Measures of Postural Control We collected center of pressure (COP) data by using a Kistler forceplateb to determine the stability of participants in 4 static positions: eyes open with head straight (EOHS), eyes open with head back 40° (EOHB), eyes closed with head straight (ECHS), and eyes closed with head back 40° (ECHB). Sensory feedback parameters for each position are summarized in table 2. This protocol is comparable with a protocol used to test the stability of patients with diabetic peripheral neuropathy.20 Participants were asked to complete three 30-second trials of each condition. A tracing of their self-selected foot position was made to control for variation of foot position between all testing positions and trials. A cervical range of motion devicec was worn by participants to ensure that they maintained 40° of head extension during head back testing positions. | | |  | Testing Position | Visual Feedback | Somatosensory Feedback | Vestibular Feedback | |
|---|
| Kistler forceplate test | | | | | |  Eyes open/head straight | + | + | + | | | Eyes open/head back | + | + | Altered | | | Eyes closed/head straight | − | + | + | | | Eyes closed/head back | − | + | Altered | | | SOT | | | | | | Condition 1 | + | + | + | | | Condition 2 | − | + | + | | | Condition 3 | Altered | + | + | | | Condition 4 | + | Altered | + | | | Condition 5 | − | Altered | + | | | Condition 6 | Altered | Altered | + | | | | |
Eight channels of analog output from the forceplate were sampled at a rate of 100Hz during each 30-second trial. Custom Matlab softwared was used to calculate the ground reaction forces from the digital output. The ground reaction force data was filtered using a fourth-order Butterworth filter with a cutoff frequency of 5Hz. The filtered ground reaction force data was then used to calculate the COP coordinates, displacement, and velocity (total COP excursion [in centimeters] divided by 30s) for each trial. The mean COP velocity of 3 trials was used for statistical analyses. To determine reliability of this measure in women after taxane therapy, all women in the breast cancer group were asked to return for testing within 1 week of initial testing. Seven women agreed to retesting and their data were used to calculate the intraclass correlation coefficients (ICCs) for these tests (EOHS: ICC=.62; ECHS: ICC=.96; EOHB: ICC=.85; ECHB: ICC=.89). We quantified dynamic postural stability by a composite equilibrium score and a mean equilibrium score by condition using the NeuroCom Sensory Organization Test (SOT)e following standard procedures.27, 30, 31 Participants were asked to stand as steady as possible during 3 trials of 6 conditions that challenge the sensory systems important for postural control (see table 2). The conditions become progressively more difficult, beginning with condition 1 in which the participant keeps eyes open on a stable platform and a nonmoving visual surround. The test then progresses by removing visual feedback (by closing eyes), altering visual feedback (by moving the visual surround), or altering somatosensory feedback (by allowing the platform to rotate in the sagittal plane). NeuroCom software was used to calculate an equilibrium score for each condition and a total equilibrium score for all conditions. The equilibrium score, which can range from 0 to 100, represents the amount of sway of the participant during the trial; a lower score indicates more sway and a zero indicates a fall. Reliability in the participants with breast cancer was calculated using the same methods used to calculate forceplate ICCs (total SOT: ICC=.86; condition 1: ICC=.82; condition 2: ICC=.92; condition 3: ICC=.67; condition 4: ICC=.75; condition 5: ICC=.81; condition 6: ICC=.65). Clinically Feasible Measures of Postural Control Many clinics do not have a forceplate or a NeuroCom system. There is literature to support that both of these quantitative measures correlate to clinical tests of balance in other populations.32, 33 Therefore, clinically feasible tests of balance were used to evaluate the relationships between these measures and quantitative measures of postural control. Participants completed the FABS and the TUG test. The FABS is a relatively new task-based measure of balance, that includes standing with feet together and eyes closed, reaching forward to retrieve a pencil held at shoulder height, turning 360° in a right then a left direction, stepping up and over a 15.2cm (6-in) bench, tandem walking, standing on 1 leg, standing on foam with eyes closed, 2-footed jumping for distance, walking with head turns, and responding to an unexpected trunk perturbation.34 The FABS was chosen because the tasks challenge the sensory systems (ie, visual, somatosensory, vestibular) used for postural control and therefore may be more sensitive to balance problems in patients with chemotherapy-induced peripheral neuropathy, a primarily sensory neuropathy. The quality of the performance of each task is scored using standardized ordinal scoring criteria, with total scores that can range from 0 to 40 points. Higher scores indicate a better performance. The FABS test was video-taped and scored by 2 reviewers who were blinded to the participants’ health status. The total FABS score had high reliability between session 1 and session 2 in this cohort (ICC=.92). The TUG test is a timed test of a person’s ability to stand from a chair, walk 3m, turn, and return to a seated position. It was chosen because of its moderate correlation with SOT equilibrium scores (Pearson r=−.48).32 It had high reliability in the current cohort (ICC=.88). Data Analysis We calculated ICCs to establish intrarater reliability for all dependent variables and to establish interrater reliability for the FABS. A Kolmogorov-Smirnov test was used to ensure that the data met the criteria of normality to allow the use of parametric statistics. Although participants in the breast cancer and healthy control groups were individually matched by age, height, and weight, a more conservative unpaired t test that assumed unequal variances was used to compare means in the breast cancer and healthy control groups for each measure of postural control and each patient characteristic, except medications that act on the central nervous system. The test of 2 proportions was performed to test for differences in the number of centrally acting medications. Pearson correlations were calculated to test for associations between the quantitative and the clinically feasible measures of postural control. Cohen d statistics were calculated to determine effect sizes between groups, while controlling for differences in standard deviations (SDs). A P value of less than .05 was considered statistically significant. A conservative Bonferroni adjustment was applied for multiple comparisons of postural control measures (family α=.05; 4 comparisons for forceplate analysis, P<.0125 to be considered significant; 7 comparisons for sensory organization analysis, P<.007 to be considered significant). All statistical calculations were performed using Minitab softwaref except ICCs were calculated using the Department of Obstetrics and Gynecology at the Chinese University of Hong Kong webpage (http://department.obg.cuhk.edu.hk/researchsupport/statstesthome.asp). Results All dependent variables and patient characteristics met the criteria of normality (P>.05) using the Kolmogorov-Smirnov test except for 4 of the SOT conditions and 5 of the forceplate conditions. However, those that did not meet the criteria for normality were very close to the cutoff (P within .02). Because parametric statistic tests are considered robust and can withstand minor variations from normality,35 we have reported our data using parametric techniques. Participant Characteristics No significant differences were found between the 2 groups in age, height, weight, number of centrally acting medications, and high contrast acuity (see table 1). However, women in the breast cancer group had significantly poorer low contrast acuity (P=.017) and a mild, yet significant, peripheral neuropathy (P<.001). Quantitative Measures of Postural Control As illustrated in figure 1, COP velocities in all 4 testing positions were significantly higher for women with breast cancer compared with healthy controls (P<.0125). As the conditions increased in difficulty, COP velocities increased for both groups. The highest velocities and largest group mean differences were found in positions in which vision was occluded or there was altered vestibular feedback (eyes open with head straight: Cohen d=1.01; eyes open with head back: Cohen d=1.33; eyes closed with head straight: Cohen d=1.28; eyes closed with head back: Cohen d=1.29). In addition, the equilibrium scores of the SOT were significantly lower in women with breast cancer for all conditions except condition 1 (fig 2). When SDs are accounted for, the largest group mean differences were observed for conditions 2, 3, 5, and 6, where vision is either occluded or altered, thereby increasing the patient’s reliance on somatosensory or vestibular input for postural stability (SOT1: Cohen d=−.74; SOT2: Cohen d=−1.46; SOT3: Cohen d=−1.37; SOT4: Cohen d=−1.05; SOT5: Cohen d=−1.57; SOT6: Cohen d=−1.30). Clinically Feasible Measures of Postural Control Interrater reliability was high for the FABS (ICC=.98). Therefore, rater 1 and rater 2 scores were averaged for further statistical analyses. Women with breast cancer had significantly lower FABS scores compared with healthy controls, indicating a poorer performance (table 3). In addition, a large significant increase in mean TUG scores (Cohen d=.77) was found in women with breast cancer compared with healthy controls (see table 3). The FABS correlated moderately with each quantitative measure of postural control (table 4). The TUG scores correlated with COP velocities in the eyes open with head back, eyes closed with head straight, and eyes closed with head back positions (see table 4). Discussion This study is the first to describe differences in various measures of postural control in women being treated with taxane chemotherapy for breast cancer compared with matched healthy controls. As we hypothesized, women who were treated with taxanes showed poorer static and dynamic postural control and poorer scores on clinically feasible measures of postural control. These findings suggest that in addition to the symptoms of peripheral neuropathy, these patients may experience problems with balance and gait that need further evaluation and treatment by a physical therapist. Problems with postural control may be partially explained by somatosensory changes secondary to taxane chemotherapy. In this sample, although the severity of peripheral neuropathy was relatively mild; the COP velocities from forceplate measures and SOT scores for conditions 1, 2, and 3 were similar to patients with severe peripheral neuropathy secondary to diabetes.20, 36 Moreover, as previously reported, the modified TNS, a measure of the severity of peripheral neuropathy, was moderately correlated with the total SOT score (r=−.66, P=.002),15 explaining 44% of the variance in SOT scores. These findings suggest that other pathologic changes related to chemotherapy may contribute to the postural instability in these women. Instability was not likely secondary to pre-existing disease or injury of the central or peripheral nervous system, musculoskeletal system, visual system, brain metastasis, medications, or physical characteristics of height; weight; or age because these variables were controlled for by rigorous exclusionary criteria or matching. Because a trend was noted in the increased use of centrally acting medications in the breast cancer group, these medications cannot be excluded as possible contributors to postural instability. It is possible that changes in the visual system may occur after chemotherapy. Although visual changes are not documented as a primary side effect of the taxanes, doxorubicin, or cyclophosphamide,4, 5, 6, 37, 38 significant difference in low contrast vision was found in the women with breast cancer compared with the healthy controls. In addition, several reports have documented acute spontaneous visual symptoms, such as scotoma (an area of lost or depressed vision surrounded by an area of more normal vision), photopsia (an appearance of flashes due to retinal irritation), and blurred vision, associated with paclitaxel and cyclophosphamide treatment.39, 40, 41, 42 Late effects, specifically increased incidence of cataract formation, have been associated with cyclophosphamide.43 Given these symptoms have been documented in patients with and without peripheral neuropathy, it is not clear whether these visual symptoms are associated with peripheral neurotoxicity to the optic nerve, vascular changes to the retina, or changes to the cornea.39 Nonetheless, chemotherapy-induced ocular changes may have contributed to the postural instability observed in the women with breast cancer. Although no published reports of taxane induced vestibular toxicity were found, other chemotherapy agents that cause peripheral neuropathy, such as platinum compounds, are associated with vestibular toxicity.44 Our data suggest that the postural instability observed in the women with breast cancer may have a vestibular component. Most notably, 2 of the largest differences in mean equilibrium scores occurred during SOT conditions 5 and 6, which occur on an unstable surface with either absent or conflicting visual feedback, respectively. It has been suggested that these conditions reflect the ability of a patient to appropriately use vestibular information to maintain postural stability.45 In addition, mean scores for the women with breast cancer were 16 points lower on condition 5 and 8 points lower on condition 6 compared with previously reported mean scores for patients with peripheral neuropathy and insulin-dependent diabetes mellitus.36 However, the scores were not as low as those of patients with bilateral vestibular hypofunction (BVH) (n=24) (breast cancer SOT5, 44.90±19.70; BVH SOT5, 9.84±17; breast cancer SOT6, 49.00±20.30; BVH SOT6, 10.52±20.56).27 Interestingly, when the SDs for both cohorts were considered, there appears to be a subset of women with breast cancer with scores that approach those with BVH.27 Scores on the clinically feasible measures of postural control (ie, FABS, TUG) were significantly poorer in women with breast cancer. Given that the FABS test correlated moderately with all quantitative measures of postural control and the TUG correlated moderately with 3 of 4 forceplate measures of postural control, it may be that these measures could serve as useful measures of postural control for clinicians who do not have forceplate or NeuroCom systems in their clinics. Although significant differences in the FABS and TUG tests were found between women with breast cancer and healthy controls, the differences were relatively smaller than those observed for the quantitative tests of postural control. Study Limitations This study has several limitations. First, it was a prospective descriptive study that examined only 1 time point (ie, at the completion of taxane therapy), rather than an evaluation of changes in postural control over time that would indicate whether postural instability improves after cessation of taxane chemotherapy. A longitudinal design would have also allowed the investigators to determine changes in postural control after doxorubicin and cyclophosphamide treatment and further describe the changes after receiving taxane therapy. Perhaps there is an additive affect of chemotherapy agents on somatosensory, visual, vestibular, or other central nervous systems related to postural stability. In addition, pretreatment measures of postural control were not obtained for the women with breast cancer. This limitation was partially overcome by matching the women with breast cancer to healthy controls on potential confounding variables associated with postural control such as age, height, and weight. In addition, participants with known visual, vestibular, orthopedic, or neurologic dysfunction were excluded from this study. Other limitations include the relatively small sample size and multiple measures of postural stability. However, we attempted to control for these limitations by using conservative statistical methods such as unpaired t tests and Bonferroni adjustments. Finally, comprehensive measures of vision and vestibular function were not obtained on the study participants. However, vestibular and visual impairments are not considered primary side effects of doxorubicin, cyclphosphamide, or the taxane class of chemotherapy4, 5, 6, 37, 38 and therefore exhaustive measures of these impairments were not included. In future studies, it will be important to include more specific measures of visual and vestibular function. It will also be important to perform measures before and after each cycle of chemotherapy to determine whether there is an additive effect of chemotherapy agents on postural control versus significant visual and/or vestibular toxicity related to taxane chemotherapy alone. Conclusions This study is the first to identify significant changes in postural stability in women treated with taxane chemotherapy for breast cancer compared with matched healthy controls. Although peripheral neuropathy is monitored as part of standard care in these patients, postural stability is not traditionally measured. The FABS and TUG are sensitive to changes in postural stability and moderately correlate with quantitative measures which may make monitoring for postural instability more feasible in the clinical setting. More information about chemotherapy-induced effects on the sensory, visual, and vestibular systems will facilitate our understanding of the origin, prognosis, and management strategies to restore postural control in this patient population. Suppliers Acknowledgments We thank Pooja Maniar, DPT, and Hope Delevega, MSPT, for their assistance in scoring the FABS. References 1. 1American Cancer Society. Cancer facts and figures. 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a Department of Rehabilitation, Harrison Medical Center, Bremerton, WA b Department of Physical Therapy and Rehabilitation Science, University of California School of Medicine, and Graduate Program in Physical Therapy, San Francisco State University, San Francisco, CA c Department of Physiological Nursing, University of California School of Nursing, San Francisco, CA d School of Medicine, University of California, San Francisco, CA e Department of Kinesiology, San Francisco State University, San Francisco, CA.  Reprint requests to Meredith A. Wampler, PT, DPTSc, Harrison Medical Center, Rehabilitation Services, 2520 Cherry Ave, Bremerton, WA 98310
Supported by the California Breast Cancer Research Program, dissertation award (grant no. 10GB-0001). No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the author(s) or upon any organization with which the author(s) is/are associated. PII: S0003-9993(07)00350-4 doi:10.1016/j.apmr.2007.05.007 © 2007 American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation. Published by Elsevier Inc. All rights reserved. | |
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