- Open Access
Physical impairments and physical therapy services for minority and low-income breast cancer survivors
SpringerPlus volume 5, Article number: 1227 (2016)
We describe impairments after breast cancer and its treatment for African American (AA), non-Hispanic white and low-income breast cancer survivors (BCS) and whether physical therapy (PT) was utilized to address these impairments.
BCS from the Southern Community Cohort Study (SCCS) were surveyed about self-reported BC treatment-related impairments (shoulder impairment, muscle weakness, pain, fatigue, skin numbness, abnormal posture) and referral to PT for impairments. We compared impairments by race, income and PT utilization. We used a cross-sectional design.
Among 528 BCS interviewed (266 whites; 262 AA), mean age 64, those with low incomes were more likely to report muscle weakness, pain and postural abnormalities, and a greater total number of impairments than those with higher incomes. Racial differences were few. PT utilization tended to be low, with AAs more likely than whites to utilize PT if they had shoulder impairment or pain, whereas no monotonic trends across income levels were seen in PT utilization.
Low-income level was associated with greater prevalence of BC-related physical impairments, but not higher PT utilization. There appears to be a possible under-utilization of PT, particularly for those with low incomes.
Background and significance
Side effects such as physical impairments (impairments) are persistent reminders of the breast cancer (BC) experience (Hewitt et al. 2006). The most common breast cancer (BC)—related impairments are lymphedema, pain and fatigue. These and less studied impairments such as upper extremity muscle weakness, loss of range of motion, altered skin sensation and integrity, and abnormal posture and shoulder movement (Hewitt et al. 2006; Battaglini et al. 2014; Binkley et al. 2012) fall under the scope of physical therapy (PT) practice (American Physical Therapy Association 2001). Impairment prevalence varies widely. Impaired shoulder range of motion affects up to 67 % of BC survivors (BCS); arm weakness affects 9–28 % (McNeely et al. 2010; Lee et al. 2007); shoulder/arm pain affects 9–68 % (McNeely et al. 2010); and 26 % report having difficulty with activities of daily living (Voogd et al. 2003). Fatigue affects 90 % of all cancer survivors (Cramp and Byron-Daniel 2012). None of these studies, however, consider differences by race.
African American (AA) women have higher BC burden than non-Hispanic whites (“whites”) (Tannenbaum et al. 2013), yet studies on impairments have mostly white middle-income women with health insurance and do not consider combined effects of race and income. Socioeconomic status and race have strong explanatory effects on cancer mortality (Tian et al. 2012), but the relationship of impairment prevalence and PT utilization are less clear.
Rehabilitation such as PT is recommended as part of BC care but it is not part of standard care planning (Alfano et al. 2012). We examine the associations between race and income with BC-related impairments and whether PT is utilized to treat impairments.
Our cross-sectional study includes female BCS enrolled in the Southern Community Cohort Study (SCCS), a long-term, prospective, population-based cohort study that recruited 85,000 adults (age 40–79)—two-thirds AA—from twelve southern states during 2002–2009. Eligibility criteria required participants to speak English and not diagnosed or treated for cancer within the preceding year prior to cohort entry. Most SCCS participants were recruited from community health centers serving low-income individuals in medically underserved areas with face-to-face interviews for survey data collection. SCCS recruitment and survey methods are described online at www.southerncommunitystudy.org (Signorello et al. 2005, 2010).
After institutional review board approval (Vanderbilt University and Northeastern University), we obtained contact information for women in the SCCS who were still alive by September 2010 and a BC history. Contact attempts were made through 2012 with a recruitment packet that included an introduction letter, consent document, and a set of answer choices (similar to hand cards for face-to-face interviews). We made up to 15 follow-up telephone calls to schedule and conduct the study interview. Our professional interviewers obtained verbal consent and used computer assisted telephone interviews (CATI) which took approximately 45 min.
All study materials had a readability level ≤8th grade, and are culturally sensitive and relevant (Bailey et al. 2000).
Participants were asked whether they had BC-related impairments that fall under the scope of PT practice (1 = Yes, 0 = No) to indicate presence of shoulder movement impairment, muscle weakness, pain, fatigue, skin numbness, and abnormal posture.
Physical therapy utilization
We asked participants whether they utilized PT (1 = Yes; 0 = No) for each impairment reported.
Race was measured with self-report of AA or white using binary responses (1 = Yes; 0 = No). We measured SES with; (1) formal education achieved (<9, 9–11 years, high school/GED, vocational/technical, some college/junior college, and college graduate or higher) (American Community Survey Design and Methodology 2014) and (2) annual household income (<$10 K, $10–20 K, $21–40 K, and >$40 k). We approximate the 2011 US Census Bureau official poverty threshold to represent “low income” ($22,811 for a family of four). Thus, our categories <$10 K and $10–$20 K represented “low-income” (Census Bureau 2011).
Number of years since BC diagnosis was calculated as the year of diagnosis subtracted from the interview date and represents length of survival—a modification of a raw survival calculation with the end-point as the interview date, not death (Cho et al. 2011).
Health insurance, a well-known determinant of health care access, was classified by insurance type (Medicare, Medicaid, private carrier, Champus, other, and no insurance) (Lukavsky and Sariego 2015).
Because the SCCS sample is unique in recruitment method (face-to-face interviews in community health centers and general public recruitment), we include this variable to control for any variation related to recruitment source.
Medical history and comorbid conditions
We control for medical history and comorbid conditions because these contribute to overall health and, in some cases, could explain some variance in our outcome variables (Gallicchio et al. 2014). Using yes/no response choices, participants were asked whether they had high blood pressure, heart attack, diabetes mellitus, stroke, emphysema, depression, osteoarthritis, congestive heart failure, HIV/AIDS, memory problems, paralysis and menopause. These are the same comorbidities asked in the SCCS baseline questionnaire and the sum was used to represent comorbidity (Schou et al. 2012).
Body mass index (BMI) was calculated as self-reported current weight (kg) divided by height2 (m) from the most recent SCCS survey completed.
Barriers to physical therapy utilization
We asked participants about patient, physician, health care system and financial barriers to health care utilization (Fradgley et al. 2015) revised to reflect PT. Patient barriers include: forgot to schedule/attend PT; fear of cancer recurrence/spread; too busy to attend PT; embarrassed; fear of discomfort/pain; lacks social support to attend PT; lacks knowledge of PT clinic location. Physician and health care system barriers include: doctor has not recommended PT; fear of prejudice or racism; inconvenient PT clinic hours; lack of child/elder care services to attend PT; attending PT interferes with spending time with family. Financial barriers include: high cost; lack of insurance coverage for PT; cannot afford to take time off from work to attend. We used yes (1)/no (0) responses and then summed the number of barriers (maximum of 16).
We stratified our sample by race (AA or white) and annual household income to compare impairments and PT utilization. We present frequencies and percentages for categorical variables and means and standard deviations for continuous measures to characterize our participants in terms of sociodemographics, medical history/comorbidity, and prevalence of impairments. Differences by race were assessed with Chi square tests or Fisher’s exact tests for categorical variables and independent samples t-tests for continuous variables. Income differences were assessed with Mantel–Haenszel Chi square tests for ordinal variables, Cochran–Armitage trend tests for categorical variables and ANOVA for continuous variables. We used multiple logistic regression to adjust for potential confounders and present adjusted odds ratios with 95 % confidence intervals. Statistical significance was determined with P values <0.05 and all analyses were performed using SAS version 9.2 (SAS Institute, Cary, NC).
Of 1109 women reported having been diagnosed with BC prior to SCCS enrollment and not previously known to have died, we completed 577 interviews. Of non-participants, 337 could not be reached by telephone, 13 never had cancer, 68 refused, 65 could not be reached, and 49 died per National Death Index verification. Of the responding 577 BCS, those missing race (n = 42) or those not identified as non-Hispanic white or AA (n = 7) were excluded from race-specific analyses yielding a sample of 528 BCS for all analyses comparing racial groups. The sample size was reduced to 524 for income comparisons because 4 additional participants had missing data, refused to answer or did not know.
Sample characteristics by race and income
On average, BCS had survived cancer for 12 years and were approximately 64 years of age at the time of interview. AAs were significantly younger than whites (62 vs. 65 years). Forty-seven percent reported incomes of $20 K or less, with significantly lower incomes among AAs than whites.
Whites were more likely than AAs to report long-term BC medication. Those with low income were more likely to have mastectomy and less likely to have had radiation therapy. More than half reported high blood pressure and 25 % had diabetes, with AAs more likely than whites to have these conditions (Table 1).
We also examined whether participants differed from BCS that did not enroll in our study in terms of these demographic characteristics. Participants tended to be older (mean age at cohort entry of 59.3 vs. 56.7 years and mean age at BC diagnosis as 50.5 vs. 47.4 years) and more often white (52 vs. 42 %). The interviewees also tended to be of higher income at SCCS cohort entry, with 44 vs. 22 % having household incomes over $20,000. On all other variables, participants did not differ from those who did not participate in the study. While these differences require caution in the generalizing the findings, comparisons made among the participants are internally valid because all BCS completed the same questionnaire following identical methods.
Impairments by race and income
Impairment prevalence was highest for skin numbness at 57 % followed by fatigue (55 %), pain (43 %), muscle weakness (38 %), shoulder movement impairment (31 %) and postural abnormality (15 %). There were no significant differences in impairment prevalence by race (Table 2).
The average number of impairments (among 6 queried) was 2.5 (SD = 1.8), but higher for those with lowest-incomes (2.8) versus higher incomes (2.3). Those with household income below $10,000 reported 0.8 more impairments than those with incomes over $40,000 (P = 0.006). Impairment prevalences were higher among those in the lowest income categories—significantly so for pain and muscle weakness (Table 3). Barriers to care were not significantly associated with impairments by race or income.
PT utilization by race and income
Those with shoulder movement impairment were most likely to utilize PT (33 %), followed by muscle weakness (22 %), pain (18 %), postural abnormality (14 %), skin numbness (8 %), and fatigue (5 %) (Table 2). AAs were significantly more likely than whites to utilize PT for shoulder movement impairment and pain. No clear or significant associations between PT utilization and income were apparent.
Low-income was associated with greater impairment prevalence, yet low-income BCS did not report higher PT use. Our study is the first to report on differences of impairments and PT utilization for BCS by race and income. Prior research indicates that AA BCS report higher prevalence of pain, fatigue, and lower overall physical and functional quality of life (Green et al. 2003; Paskett et al. 2008), but among the BCS we interviewed race was inconsistently associated with impairments. Most research on BCS involves white middle-income women with health insurance. Our study has the unique advantage of examining impairments in a large, diverse sample of BCS of all income levels.
Our research supports work that shows those with lower income have significantly lower physical functioning when compared to higher income whites and minorities (Braithwaite et al. 2010). A cross-sectional, observational study of BCS found that 36–59 % had shoulder range of motion restrictions (Cheville et al. 2008). Others found that BCS had significantly more shoulder limitations when compared to controls (Harrington et al. 2011). Our findings highlight the importance of shoulder range of motion limitation and suggest more of a need to address impairments—especially for those with low incomes.
Poorly controlled pain contributes to compensatory patterns of overuse, poor posture, and faulty biomechanics (Norkin and Levangie 1992). Other studies report that AAs may have higher levels of cancer-related pain (Green et al. 2003) yet we found significant differences in pain by income—not race.
Fatigue affects 9–39 % of BC (American Community Survey Design and Methodology 2014; Palmer et al. 2013) and is associated with disability and health care utilization (Servaes et al. 2007). One longitudinal study of 252 BCS reports fatigue affecting 31 % right after treatment declining to 6 % by the end of the first post-treatment year (Green et al. 2003). The majority of our survivors reported fatigue—a substantial finding because our BCS were long-term survivors. Another longitudinal study of 244 long-term BCS found no racial differences in fatigue, pain and other side effects, but they did not make comparisons by income (Gill et al. 2004). Our research shows significant differences by income for pain and utilization of PT to treat pain but not for fatigue.
Our study suggests that PT may be under-utilized for these impairments despite insurance status. The significantly higher use of PT by AAs was unexpected. Since we studied the presence/absence of impairments, not severity, it is possible that severe impairment might be more likely to trigger a referral to PT. In our sample, AAs were more likely to utilize PT if they had complaints of shoulder impairment, muscle weakness or pain. The total number of barriers to PT was not significantly associated with PT utilization—a surprising finding. While not all BCS need PT, our study suggests that impairments persist and the need for referral to PT may also persist.
Recent rehabilitation services documentation for Medicare patients mandate the use of patient reported outcomes such as those examined in this study. It is possible that some BCS may have issues with recall and attribution of impairments to cancer rather than an alternative medical diagnosis. Since our subjects were drawn from many different states, verification of self-reports was logistically impossible because it would have involved hundreds of hospitals, outpatient clinics and internal review boards.
Although this research included high proportions of low-income BCS (an advantage), the relatively few individuals with higher incomes precluded assessing income effects across upper-middle and higher income ranges. While BC is not rare, we studied a large proportion of minority and poor BCS which is rare and has allowed us to consider three key social determinants—race, income, and insurance.
Our results could also be partially explained by residence differences. For example, rural residents are more likely than urban residents to forgo medical and dental care after cancer (Palmer et al. 2013), travel farther for care and have mastectomy (Meilleur et al. 2013). Areas with higher versus lower health care spending also have higher rates of recommended and preferred health care (Keating et al. 2012). Future research can include these comparisons by taking advantage of hierarchical statistical modeling.
Our results may reflect the effects of reduced physical activity among breast cancer survivors. While exercise has many benefits including cancer control and prevention (Courneya et al. 2014) exercise is not part of survivorship care (Phillips et al. 2014).
Our study suggests that disparities exist among BCS for impairments that fall in the scope of practice for physical therapists. The “surveillance” model (Campbell et al. 2012) tracks signs and symptoms indicative of BC-related impairments, but ownership of surveillance is not clear nor tested with population-based samples. However, rehabilitation models exist in all medical systems that can be leveraged to improve BC-related impairment management. Rehabilitation is standard for those with total joint replacement and significantly improves physical and functional ability (Desmeules et al. 2013) self-efficacy, (Lane-Carlson and Kumar 2012) pain, (Niu et al. 2011) and reduces hospital length of stay, (Mertes et al. 2013) post-operative complications, (Husni et al. 2010) and readmission. (Gooch et al. 2012) The inclusion of PT at the beginning of treatment planning could have a similar effect in the BCS population, especially for those with low-incomes who seem to have the most BC-related impairments. Comparative effectiveness trials could compare referral-based versus rehabilitation models of care delivery.
Impairment burden is high among BCS but especially the poor—precisely those who are least able to afford it. The high prevalence of impairments and low PT utilization suggest that an unmet need for rehabilitation services may exist. Persistent impairments can interfere with the ability to return to work (Clarke et al. 2011) and if untreated may lead to disability. (Goldstein et al. 2012) Our detection of low PT utilization suggests that strategies to enhance opportunities for PT may lighten BC-related impairment burden.
Alfano CM, Ganz PA, Rowland JH et al (2012) Cancer survivorship and cancer rehabilitation: revitalizing the link. J Clin Oncol 30(9):904–906
American Community Survey Design and Methodology (2014) Chapter 6: survey rules, concepts, and definitions. U.S. Census Bureau, Washington, DC
American Physical Therapy Association (2001) Guide to physical therapy practice, 2nd edn. American Physical Therapy Association, Alexandra
Bailey EJ, Erwin DO, Belin P (2000) Using cultural beliefs and patterns to improve mammography utilization among African-American women: the Witness Project. J Natl Med Assoc 92(3):136–142
Battaglini CL, Mills RC, Phillips BL et al (2014) Twenty-five years of research on the effects of exercise training in breast cancer survivors: a systematic review of the literature. World J Clin Oncol. 5(2):177–190
Binkley JM, Harris SR, Levangie PK et al (2012) Patient perspectives on breast cancer treatment side effects and the prospective surveillance model for physical rehabilitation for women with breast cancer. Cancer 118(8 Suppl):2207–2216
Braithwaite D, Satariano WA, Sternfeld B et al (2010) Long-term prognostic role of functional limitations among women with breast cancer. J Natl Cancer Inst 102(19):1468–1477
Campbell KL, Pusic AL, Zucker DS et al (2012) Prospective model of care for breast cancer rehabilitation: function. Cancer 118(8 Suppl):2300–2311
Cheville AL, Troxel AB, Basford JR et al (2008) Prevalence and treatment patterns of physical impairments in patients with metastatic breast cancer. J Clin Oncol 26(16):2621–2629
Cho H, Howlader N, Mariotto AB et al (2011) Estimating relative survival for cancer patients from the SEER Program using expected rates based on Ederer I versus Ederer II method. Surveillance Research Program, NCI, Technical report #2011-01
Clarke TC, Soler-Vila H, Lee DJ et al (2011) Working with cancer: health and disability disparities among employed cancer survivors in the U.S. Prev Med 53(4–5):331–334
Courneya KS, Segal RJ, McKenzie DC et al (2014) Effects of exercise during adjuvant chemotherapy on breast cancer outcomes. Med Sci Sports Exerc 46(9):1744–1751
Cramp F, Byron-Daniel J (2012) Exercise for the management of cancer-related fatigue in adults. Cochrane Database Syst Rev 11:CD006145
Desmeules F, Hall J, Woodhouse LJ (2013) Prehabilitation improves physical function of individuals with severe disability from hip or knee osteoarthritis. Physiother Can 65(2):116–124
Fradgley EA, Paul CL, Bryant J (2015) A systematic review of barriers to optimal outpatient specialist services for individuals with prevalent chronic diseases: what are the unique and common barriers experienced by patients in high income countries? Int J Equity Health 9(14):52
Gallicchio L, Calhoun C, Helzlsouer KJ (2014) Association between race and physical functioning limitations among breast cancer survivors. Support Care Cancer 22(4):1081–1088
Gill KM, Mishel M, Belyea M et al (2004) Triggers of uncertainty about recurrence and long-term treatment side effects in older African American and Caucasian breast cancer survivors. Oncol Nurs Forum 31(3):633–639
Goldstein D, Bennett BK, Webber K et al (2012) Cancer-related fatigue in women with breast cancer: outcomes of a 5-year prospective cohort study. J Clin Oncol 30(15):1805–1812
Gooch K, Marshall DA, Faris PD et al (2012) Comparative effectiveness of alternative clinical pathways for primary hip and knee joint replacement patients: a pragmatic randomized, controlled trial. Osteoarthritis Cartilage 20(10):1086–1094
Green CR, Anderson KO, Baker TA et al (2003a) The unequal burden of pain: confronting racial and ethnic disparities in pain. Pain Med 4(3):277–294
Green CR, Baker TA, Smith EM et al (2003b) The effect of race in older adults presenting for chronic pain management: a comparative study of black and white Americans. J Pain 4(2):82–90
Harrington S, Padua D, Battaglini C et al (2011) Comparison of shoulder flexibility, strength, and function between breast cancer survivors and healthy participants. J Cancer Surviv 5(2):167–174
Hewitt M, Greenfield S, Stovall E (eds) (2006) From cancer patient to cancer survivor: lost in transition. Institute of Medicine, National Academy of Sciences, Washington, DC
Husni ME, Losina E, Fossel AH et al (2010) Decreasing medical complications for total knee arthroplasty: effect of critical pathways on outcomes. BMC Musculoskelet Disord 14(11):160
Keating NL, Landrum MB, Lamont EB et al (2012) Area-level variations in cancer care and outcomes. Med Care 50(5):366–373
Lane-Carlson M, Kumar J (2012) Engaging patients in managing their health care: patient perceptions of the effect of a total joint replacement presurgical class. Perm J 16(3):42–47
Lee TS, Kilbreath SI, Refshauge KM et al (2007) Pectoral stretching program for women undergoing radiotherapy for breast cancer. Breast Cancer Res Treat 102:313–321
Lukavsky R, Sariego J (2015) Insurance status effects on stage of diagnosis and surgical options used in the treatment of breast cancer. South Med J 108(5):258–261
McNeely ML, Campbell K, Ospina M et al (2010) Exercise interventions for upper-limb dysfunction due to breast cancer treatment. Cochrane Database Syst Rev 16(6):CD005211
Meilleur A, Subramanian SV, Plascak JJ et al (2013) Rural residence and cancer outcomes in the United States: issues and challenges. Cancer Epidemiol Biomarkers Prev 22(10):1657–1667
Mertes S, Raut S, Khanduja V (2013) Intergrated care pathways in lower-limb arthroplasty: are they effective in reducing length of hospital stay? Int Orthop 37:1157–1163
Niu NN, Collins JE, Thornhill TS et al (2011) Pre-operative status and quality of life following total joint replacement in a developing country: a prospective pilot study. Open Orthop J 5:307–314
Norkin CC, Levangie PK (1992) Joint structure and function: a comprehensive analysis, 2nd edn. Davis, Philadelphia
Palmer NR, Geiger AM, Lu L et al (2013) Impact of rural residence on forgoing healthcare after cancer because of cost. Cancer Epidemiol Biomarkers Prev 22(10):1668–1676. doi:10.1158/1055-9965.EPI-13-0421
Paskett ED, Alfano CM, Davidson MA et al (2008) Breast cancer survivors’ health-related quality of life: racial differences and comparisons with noncancer controls. Cancer 113(11):3222–3230
Phillips SM, Alfano CM, Perna FM et al (2014) Accelerating translation of physical activity and cancer `survivorship research into practice: recommendations for a more integrated and collaborative approach. Cancer Epidemiol Biomarkers Prev 23(5):687–699
Schou Sarfati D, Bredal I, Smeby NA et al (2012) Review of methods used to measure comorbidity in cancer populations: no gold standard exists. J Clin Epidemiol 65(9):924–933
Servaes P, Gielissen MF, Verhagen S, Bleijenberg G (2007) The course of severe fatigue in disease-free breast cancer patients: a longitudinal study. Psychooncology 16(9):787–795
Signorello LB, Hargreaves MK, Steinwandel MD et al (2005) Southern community cohort study: establishing a cohort to investigate health disparities. J Natl Med Assoc 97(7):972–979
Signorello LB, Hargreaves MK, Blot WJ (2010) The Southern Community Cohort Study: investigating health disparities. J Health Care Poor Underserved 21(1 Suppl):26–37
Tannenbaum SL, Koru-Sengul T, Miao F, Byrne MM (2013) Disparities in survival after female breast cancer diagnosis: a population-based study. Cancer Causes Control 24(9):1705–1715
Tian N, Goovaerts P, Zhan FB et al (2012) Identifying risk factors for disparities in breast cancer mortality among African–American and Hispanic women. Womens Health Issues 22(3):e267–e276
U.S. Census Bureau (2011) Poverty thresholds by size of family and number of children. http://www.census.gov/hhes/www/poverty/data/threshld/index.html. Accessed Sept 2015
Voogd AC, Ververs JM, Vingerhoets AJ et al (2003) Lymphoedema and reduced shoulder function as indicators of quality of life after axillary lymph node dissection for invasive breast cancer. Br J Surg 90(1):76–81
AMF: Conceptualization, methodology, formal analysis, investigation, writing-orginal draft, writing-review and editing, visualization, supervision, funding acquisition. JN: Methodology, formal analysis, writing-original draft, writing-review and editing. LS: Writing-review and editing, project administration. KB: Writing-review and editing, project administration. WJB: Writing-review and editing, supervision. All authors read and approved the final manuscript.
We wish to thank Mark Steinwandel for his assistance with dataset management.
The authors declare that they have no competing interests.
This work was supported by the National Institutes of Health grants R21 CA137483 (Flores) and R01 CA092447 (Blot) and the Vanderbilt Survey and Biospecimen Shared Resource funded by National Institute of Health grant P30 CA68485.
Rights and permissions
Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
About this article
Cite this article
Flores, A.M., Nelson, J., Sowles, L. et al. Physical impairments and physical therapy services for minority and low-income breast cancer survivors. SpringerPlus 5, 1227 (2016). https://doi.org/10.1186/s40064-016-2455-3
- Physical therapy
- Breast cancer