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Prevalence and Treatment Patterns of Physical Impairments in Patients With Metastatic Breast Cancer

Andrea L. Cheville, Andrea B. Troxel, Jeffrey R. Basford, Alice B. Kornblith

From the Department of Physical Medicine and Rehabilitation, Mayo Clinic College of Medicine, Rochester, MN; University of Pennsylvania, PA; and the Dana-Farber Cancer Institute, Boston, MA

Corresponding author: Andrea L. Cheville, MD, MSCE, Department of Physical Medicine and Rehabilitation, Mayo Clinic, 200 First St SW, Rochester, MN 55905; e-mail: cheville.andrea{at}mayo.edu

	ABSTRACT

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Purpose Physical impairments cause profound functional declines in patients with cancer. Although common rehabilitation measures can address many impairments, the extent of their delivery is unknown. We studied these issues by quantifying physical impairments in patients with metastatic breast cancer and by assessing how they are addressed.

Patients and Methods A consecutive sample of 163 community-dwelling patients with metastatic breast cancer was stratified by Karnofsky performance score and administered the Medical Outcomes Study Physical Function Subscale and the Older Americans Resource Study Activities of Daily Living subscales. Cancer-related physical impairments were identified through a physical examination, the 6-Minute Walk Test, and the Functional Independence Measure Mobility Subscale. Patients were questioned regarding the nature, type, and setting of treatments for impairments. Physical rehabilitation needs were determined through a consensus process involving physiatrists and physical/occupational therapists specializing in cancer.

Results Ninety-two percent of patients (150 of 163) had at least one physical impairment. Among 530 identified impairments, 484 (92%) required a physical rehabilitation intervention and 469 (88%) required physical therapy (PT) and/or occupational therapy (OT). Only 30% of impairments requiring rehabilitation services and 21% of those requiring PT/OT received treatment. Impairments detected during hospitalization were overwhelmingly more likely to receive a rehabilitation intervention (odds ratio [OR] = 87.9; 95% CI, 28.5 to 271.4), and PT/OT (OR = 558.8; 95% CI, 187.0 to 1,669.6). Low socioeconomic and minority status were significantly associated with nontreatment.

Conclusion Remediable physical impairments were prevalent and poorly addressed among patients with metastatic breast cancer, drastically so in the outpatient setting. Undertreatment was particularly prominent among minority and socioeconomically disadvantaged groups.

	INTRODUCTION

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Although physical impairments threaten the functioning and quality of life (QOL) of patients with advanced cancer, we have little idea about either their frequency or impact, and no report has focused exclusively on patients with metastatic disease. Data suggest that the needs of this population are poorly recognized and inadequately met by the rehabilitation and oncology communities. In a time that now recognizes the value of QOL, indifference toward patients’ ability to function is a striking inconsistency at odds with the Institute of Medicine's assertion that the purpose of the health care system "is to reduce continually the burden of... disability and to improve the ... function of the people of the United States."^1,2

Previous investigations of cancer-related functional problems have typically been disability-based self-report estimates.^3-7 As such, they reflect patients’ inability to perform activities but do not address the reasons for that failure. This distinction is important. Although the inability to independently eat or climb steps is a disability, the reason for this inability, such as limb weakness or ataxia, occurs at a simpler level and is defined as an impairment. The distinction between impairment and disability is fundamental to current disablement models,^8-11 critical to accurate prognostication, and relevant on a practical basis because impairments lend themselves more directly to treatment than do disabilities.

Cancer-related impairments differ in their nature and causes. Adverse neural, musculoskeletal, and cardiopulmonary effects resulting from metastatic and regional tumor spread are obviously important factors. Cancer treatment also has sequelae. As many as 40% of patients undergoing chemotherapy develop chronic neuropathies.¹² Anatomic disruptions consequent to surgeries contribute to a wide range of impairments. The fact that multiple impairments may coexist only complicates the situation. The prognosis and remediation of disability therefore requires a comprehensive determination of relevant impairments.

We undertook this cross-sectional study of patients with metastatic breast cancer to characterize the prevalence of impairments, to determine whether remediable impairments receive appropriate treatment, and to establish where treatment occurred.

	PATIENTS AND METHODS

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Patients
A consecutive sample of patients receiving outpatient chemotherapy at the Memorial Sloan-Kettering Cancer Center (MSKCC; New York, NY) for metastatic breast cancer was enrolled in July and August 1999. Eligible patients were required to have documented metastatic breast cancer, have Karnofsky performance score (KPS)^13,14 between 40 and 90, be 18 years of age or older, have an intact mental status, and be fluent in English. Disease status was determined by medical record review, physician communication, and imaging studies. Potential participants were approached before receiving parenteral chemotherapy or bisphosphonate treatments.

Stratified sampling was used to ensure adequate representation of participants with lower performance status. Participants were grouped into three KPS strata (80 to 90, 60 to 70, and 40 to 50). Two hundred twelve patients were screened during the study period. Of these, 31 had insufficient English fluency and 18 declined to participate. Patients excluded on the basis of English proficiency were more likely to identify themselves as Asian (73% v 2.5%). Excluded patients did not otherwise differ significantly from the final study sample of 163 participants.

Data Collection
Data were collected from the MSKCC electronic medical record (EMR), clinician-administered testing, the study instruments, and a semistructured interview. On instrument review, obviously incorrect or missing responses were verbally clarified or readministered.

EMR
Relevant treatment histories, diagnostic test results, consultation reports, disease status, and KPS were obtained through review of MSKCC's comprehensive EMR.

Clinician-Administered Testing
Physical examination. The principal investigator performed a standard musculoskeletal and neurologic examination that included goniometric measurements of neck, thoracolumbar spine, shoulder, and hips; limb circumferences; and a detailed neurologic examination involving the cranial nerves, sensation, muscle strength, deep tendon reflexes, gait, and coordination.

Six-minute walk. The 6-Minute Walk Test (6MWT) has well-demonstrated validity and reliability.^15,16 Distances were recorded, and participants rated their dyspnea at its completion on a Likert scale.

Functional Independence Measure Mobility Subscale. The Functional Independence Measure (FIM) Mobility Subscale is a valid clinician-rated scale with adequate discrimination in disabled cancer cohorts.^17-20 The scale is composed of five items. Participant scores range from 5 to 35, with each item having seven levels that increase from 1 (total dependence) to 7 (total independence).

Identification of Impairments
Impairments were identified on the basis of physical examination findings and the 6MWT. Etiologic determination was supplemented with consultation reports, imaging, and other diagnostic studies. Generalized strength deficits in the absence of a confirmed neurologic or myopathic cause were attributed to deconditioning. Similarly, severe dyspnea after the 6MWT in the absence of objective cardiac or pulmonary pathology was attributed to aerobic deconditioning.

Self-Report Study Instrument
Older Americans Resource Study. The Older Americans Resource Study (OARS) Social/Financial Resources, activities of daily living (ADL), and instrumental ADL (IADL) subscales contain 15, seven, and seven items, respectively and have been shown to be responsive and discriminative in cancer cohorts.^21-23

Physical Function-10. The Physical Function-10 (PF-10) is a well-validated subsection of the Medical Outcome Study Short Form-36 that assesses limitations in physical activities.²⁴ The PF-10 and OARS ADL and IADL scales assess overlapping constructs with the PF-10, emphasizing mobility and the OARS self-care.

Distress and interest in rehabilitation. Four nonvalidated questions queried participants about their distress related to problems with mobility and ADL performance (Likert scale) and their willingness to receive help (binary).

Structured Interview
Pre-existing impairments. Patients were asked whether identified impairments were present before their diagnosis with metastatic breast cancer.

Rehabilitation service utilization. Scripted interviews were used to assess rehabilitation service utilization for identified impairments. Separate questions were posed about specific rehabilitation interventions. Photographs of typical orthotics and adaptive equipment were used to improve recall, and participants were asked the setting in which an impairment had been identified.

Determination of Rehabilitation Need
A board-certified physical medicine and rehabilitation (PM&R) physician specializing in cancer rehabilitation (A.L.C.) assessed rehabilitation needs on the basis of impairment-specific treatment standards,²⁵ recommendations in rehabilitation medicine texts,^26,27 and treatment algorithms in physical therapy (PT)/occupational therapy (OT) manuals.^28-30 Five interventions (assistive devices for ADLs, mobility aids, orthotics and compression garments, PT, and OT) were assessed for each impairment as "needs," "doesn't need," "received," or "received and still needs." Table 1 lists evidence-based interventions in the five categories for representative impairments. Determinations were independently reviewed by a second PM&R cancer specialist, with conflicts resolved through a consensus process involving the physicians and PT/OT cancer specialists.

Statistical Analysis
Descriptive statistics were calculated for participant- and impairment-level data. Receipt of treatment at the impairment level was used in logistic regressions because analyses at the participant level would yield spuriously elevated treatment rates. The models were adjusted for clustering of impairments within participants. Independent covariates in the regression models were at both impairment and participant levels.

Univariate logistic regressions were performed with receipt of APRI and PT/OT as outcome variables to assess their association with demographic- and cancer-specific covariates. Standard model-building techniques were applied, including evaluation of interaction effects. Confounding was assessed by evaluating the effect of selectively removing covariates from the model on β coefficients and Wald statistics. The final model was assessed using the Hosmer-Lemeshow goodness-of-fit test.³¹ Predictive accuracy of the final model was assessed with receiver operating characteristic curves.³² Odds ratios (ORs) are presented with their corresponding 95% CI and significance was assessed using Wald tests. All tests were two tailed. P values less than .05 were considered statistically significant. Analysis was performed with STATA for Windows, version 8.0 (StataCorp, College Station, TX).

	RESULTS

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Study Patients
Sociodemographics. The KPS-based stratified sampling failed to yield balanced strata as grant termination forced closure of enrollment. The final study cohort of 163 patients (KPS 80 to 90, n = 72; KPS 60 to 70, n = 51; KPS 40 to 50, n = 40) contained an over-representation of higher-performing participants. Demographic and clinical characteristics are presented in Table 2.

Function characteristics. Physical impairments were identified in 92% of the 163 patients with equal percentages (88%) judged to require either APRI or PT/OT for at least one impairment. Barely half of the participants had normal muscle strength, with the group as a whole demonstrating low levels of physical function (mean PF-10 score, 47.0 ± 31.7) A significant proportion of the cohort reported difficultly with at least one ADL (43%) and IADL (74%). FIM Mobility Subscale score means (30.2 ± 5.8) revealed a generalized compromised mobility. Overall, one third of the participants presented a picture of moderate disability, defined as FIM mobility subscale score less than 30, PF-10 less than 35, and at least 4 problems with IADLs.³³ Fifty-one percent of patients had received APRI, and 39.2% of patients had received PT/OT for at least one impairment. For many patients, receipt of APRI (40.3%) and PT/OT (51.8%) was for arm lymphedema.

Impairments
Table 3 lists impairment prevalences and treatment frequencies. All but 8% of the participants (13/163) had at least one physical impairment with 530 (3.3 ± 2.0/participant) occurring in the remaining 150. Forty six (8.7%) impairments were coded "doesn't need" and required no treatment. APRI was indicated for 484 (91%) of the impairments, with almost as many (469) deemed to require PT/OT. Only 30% of impairments for which APRI was indicated, and only one fifth of those with a PT/OT indication, had received treatment. Less than 10% of patients received treatment for all impairments requiring either APRI or PT/OT.

Physical Impairments, Disability, and Anticancer Treatments
Figure 1 displays a representative sample of impairments listed in Table 3. The PF-10 and OARS ADL scores for participants with specific impairments are displayed relative to sample means. Impairment groups are defined by the inciting pathology (eg, musculoskeletal). Note that with few exceptions, the degree of disability is significant and relatively uniform across impairments.

View larger version (25K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 1. (A) Physical Function-10 and (B) Older Americans Resource Study activities of daily living (ADL) scores for patients with a representative sample of impairments relative to sample means grouped by the inciting pathology (eg, musculoskeletal). PNS, peripheral nervous system. (*) Mean values for the total study sample. Yellow, lymphedema; blue, neurological impairments; gray, generalized stamina/strength deficits; red, musculoskelatal impairments.

Relationships between cancer, its treatment, and physical impairments were rarely straightforward. Among 46 patients with exertional intolerance attributed to cardio-pulmonary factors, 37 had lung or pericardial metastases, 27 had received a cardiotoxic chemotherapy (18 with multiple gated acquisition scan confirmed cardiomyopathy), 12 had undergone intrathoracic surgery, 25 received radiation encompassing lung fields, and 21 had moderate or worse pleural effusions. More than one factor likely contributed to exertional intolerance in most patients.

Comparable complexity characterized the relationships between impairments and chemotherapy, radiation, and cancer surgeries. Patients had received more than 70 different chemotherapeutic and hormonal regimens. Reducing these to a manageable number yielded no meaningful associations aside from the fact that participants who received second- and third-line regimens or "salvage" chemotherapy had more metastases, impairments, and disability. However, all patients with neuropathies had received at least one taxane-based regimen. Surgical and radiation therapy interventions were equally heterogeneous, and a similar pattern was noted, with patients who received more treatments having more impairments and advanced disease.

Distress and Interest in Receiving Rehabilitation
Table 4 displays the percentages of participants in each KPS substratum and with moderate disability whose mobility and ADL performance distressed them at least moderately, and those interested in receiving treatment. Interest increased with declining KPS scores.

The Wald statistics revealed no significant association between receipt of APRI or PT/OT and disability metrics (PF-10, OARS ADL and IADL subscale, and FIM scores), participants’ desire to receive rehabilitation, and cancer treatment-related covariates.

	DISCUSSION

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This study, to our knowledge, is the first to use clinician-rated, impairment-based assessment to characterize physical rehabilitation needs in patients with any form of cancer. In doing so, it confirmed high prevalence rates and marked undertreatment of physical impairments despite the fact the majority of participants recognized their need for assistance. Particularly striking was the finding that, although more than 90% of the patients appeared to have impairments that would, at least in part, be ameliorated by standard rehabilitation measures, less than a third of these impairments received treatment. Further, participants had metastatic cancer for a mean of 30.3 months (± 27.4 months), suggesting that many may have experienced protracted disability.

Our findings also document an intuitively obvious, but previously unreported, disparity between the delivery of rehabilitation services in the outpatient and inpatient settings. Further, these findings confirm the presence of racial and economic disparities that have been reported for other types of cancer and cancer care.^34-36

The striking association between impairment detection and hospitalization (Table 5) may reflect a combination of increased scrutiny in the inpatient setting, the presence of critical pathways, and the absence of access barriers. The role of formalized discharge planning and the provision of postdischarge services may be important.⁴⁰ The dearth of treatment in the outpatient setting is of particular concern in light of the trend toward greater outpatient cancer management and the fact that impairments are most remediable in their early stages. The fact that arm lymphedema received PT/OT (OR = 69.6) and APRI (OR = 7.2) significantly more other impairments may reflect the convenience afforded by a lymphedema clinic within MSKCC, and suggests that ease of access may be an important determinant in service utilization.

Physical impairments are only a portion of the burden borne by patients with cancer. The ideal scope of cancer rehabilitation encompasses a broad range of vocational, psychological, economic, social, and functional problems. We would have preferred to assess the entire spectrum of needs. However, two factors mitigated against this. First, the task of simultaneously assessing all these factors would be overwhelming. Second, focusing on physical impairments alone reflects conventional PM&R outpatient practice patterns, where cancer specialists address physical impairments and related disabilities. Psychologists and social workers, unaffiliated with rehabilitation medicine, typically address psychosocial issues.

Concerns about the delay between data collection and publication might also be raised. This delay arose from logistic, regulatory, and financial barriers to the interinstitutional transfer of data for analysis. Fortunately, these concerns seem more apparent than real, given that there has been little interval change in the treatment of metastatic breast cancer or in the integration of rehabilitation services. In large rehabilitation departments, the emphasis on cancer has remained stable during the last decade, and reimbursement for rehabilitation services has declined.⁴¹ Moreover, there has been no increase in data-driven publications on this problem. It is telling that the National Comprehensive Cancer Network recent consensus guidelines on supportive care do not mention rehabilitation.⁴²

The consensus process used to classify a patient's rehabilitation needs might also be questioned. However, no reasonable alternative approach seemed possible, and every effort was made to use accepted and objective standards. The high level of functional morbidity in the study cohort argues that rehabilitation was legitimately indicated for the majority of participants. Participant recall bias is a concern, but the use of scripted questions and photographs should have minimized its risk.

This study's focus on patients’ specific impairments rather than their disabilities complements existing data by providing new insights into causes of functional decline and useful information regarding potential screening and treatment strategies. Our data, however, do not shed light on the reason for the discordance between the presence of impairments and their treatment. The lack of outpatient rehabilitation treatment suggests that functional end points are underemphasized in cancer care. This is of particular concern in light of the growing emphasis on quality survivorship, and warrants further investigation. Initial next steps will include characterizing sources of undertreatment. Our results will serve as the basis for focused interventional trials of screening, directed treatment and educational strategies.

In summary, this study indicates that, although 90% of patients being treated for metastatic breast cancer at a tertiary cancer center would benefit from at least one rehabilitation intervention, fewer than 30% actually received appropriate services. This seems particularly unfortunate in view of the efficacy of standard rehabilitation interventions in treating many of these impairments in patients with cancer, as well as other systemic and debilitating diseases.^17,18,43-53

	AUTHORS’ DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

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The author(s) indicated no potential conflicts of interest.

	AUTHOR CONTRIBUTIONS

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Conception and design: Andrea L. Cheville, Andrea B. Troxel, Alice B. Kornblith

Financial support: Andrea L. Cheville

Administrative support: Andrea B. Troxel, Jeffrey R. Basford, Alice B. Kornblith

Provision of study materials or patients: Andrea L. Cheville

Collection and assembly of data: Andrea L. Cheville

Data analysis and interpretation: Andrea L. Cheville, Andrea B. Troxel, Jeffrey R. Basford, Alice B. Kornblith

Manuscript writing: Andrea L. Cheville, Andrea B. Troxel, Jeffrey R. Basford, Alice B. Kornblith

Final approval of manuscript: Andrea L. Cheville, Andrea B. Troxel, Jeffrey R. Basford, Alice B. Kornblith

	ACKNOWLEDGMENTS

 
We thank Richard Payne, MD, who was instrumental in obtaining the Langeloth Foundation grant that supported initial study design and data collection, and Angela DeMichele, MD, MSCE, for her guidance in identifying sources of confounding and bias in this study.

	NOTES

 
Supported by a Langeloth Foundation grant, Department of Defense Grant No. DAMD17-03-1-0622, and National Institutes of Health Grant No. KL2 RR024151-01.

Authors’ disclosures of potential conflicts of interest and author contributions are found at the end of this article.

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Submitted April 23, 2007; accepted January 28, 2008.

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