Professional Documents
Culture Documents
The Breast
journal homepage: www.elsevier.com/brst
Original article
a r t i c l e i n f o a b s t r a c t
Article history: The objective of this study was to examine factors impacting long-term functional outcomes and
Received 6 October 2011 psychological sequelae in survivors of breast cancer (BC). A clinical assessment and structured interview
Received in revised form assessed the impact of BC on participants’ (n ¼ 85) current activity and restriction in participation, using
23 January 2012
validated questionnaires: Functional Independence Measure (FIM), Perceived Impact Problem Profile
Accepted 24 January 2012
(PIPP) and Depression Anxiety Stress Scale (DASS). Participants showed good functional recovery
(median motor FIM score ¼ 78). Three-quarters (74%) reported pain, 32% reported upper limb weakness,
Keywords:
31% pain limiting shoulder movement and 29% lymphoedema. One third (32%) reported greatest impact
Breast cancer
Rehabilitation
on psychological wellbeing. A substantial number of participants reported high levels of depression
Disability (22%), anxiety and stress (19% each). Factors associated with poorer current level of functioning and
Participation wellbeing included: younger participants, recent diagnoses, aggressive tumour types, receiving
Functional Independence Measure chemotherapy, shoulder limitation due to pain, and lymphoedema. BC survivors require long-term
Depression Anxiety Stress Scale management of psychological sequelae impacting activity and participation.
Ó 2012 Elsevier Ltd. All rights reserved.
0960-9776/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved.
doi:10.1016/j.breast.2012.01.013
F. Khan et al. / The Breast 21 (2012) 314e320 315
Statistical analysis from <1 year to 24 years (Md ¼ 2.2 years, IQR ¼ 1.4e4.9).
Majority were tertiary educated (n ¼ 43, 51%) and married
A series of analyses were conducted to describe the current level of (n ¼ 53, 62%). Over half of the sample had
function and wellbeing of participants and to identify those factors BloomeRichardsoneElston (BRE) tumour Grade 3 (n ¼ 45, 54%),
associated with scores on the FIM, PIPP and DASS subscales. Given the were estrogen-receptor positive (n ¼ 70, 85%) and with lymph
skewed distributions, continuous predictor variables (age, time since node involvement (n ¼ 56, 66%). More than a third (n ¼ 31, 37%)
diagnosis) were split at the median to form approximately equal had breast conservation surgery (lumpectomy) with axillary
groups for comparison. Non-parametric analyses (ManneWhitney U clearance (Table 1).
tests) were used to compare scores across groups. Although
a substantial number of univariate analyses were conducted,
increasing the likelihood of a Type 1 error, it was decided to report all Current symptoms
p values above .05 as significant. This was consistent with the
descriptive nature of the study to ensure all potentially important Three quarter of the sample reported some degree of breast
predictors of the long-term sequelae of BC were identified. related pain (n ¼ 63, 75%), with 39% (n ¼ 24) rating the pain as 5
on a 10 point scale, and describing it as sharp (n ¼ 12, 19%), aching
Results (n ¼ 12, 19%) or dull (n ¼ 11, 18%).Phantom breast sensation (n ¼ 13,
15%) and phantom breast pain (n ¼ 5, 6%) were noted. Almost one
Sample characteristics third reported limited shoulder movement (n ¼ 28, 33%), with 31%
(n ¼ 26) indicating shoulder limitation due to pain; lymphoedema
The participant’s (n ¼ 85) ages ranged from 33 to 80 yrs (n ¼ 25, 29%), and upper limb weakness of affected side (n ¼ 36,
(median (Md) ¼ 57years, IQR ¼ 47.4e63.9), time since diagnosis 42%) on MRC motor scale (Table 1).
F. Khan et al. / The Breast 21 (2012) 314e320 317
Demographic and disease factors in BC patients (with or without lymphoedema), in reducing side
effects of treatment, fatigue and deconditioning.24,27 Healthy life
Scale scores were compared for two age groups (57 yrs, 57þ style, health promotion and exercise therefore, should be
yrs) using ManneWhitney U tests, and the younger group showed encouraged in this population24,26,28,29 including conservative
significant differences in two of the PIPP subscales (Psychological, therapies for lymphoedema.30
p ¼ .02; Relationship, p ¼ .007). Women in BRE Grade 3 reported Breast pain is a common symptom in women following BC
higher impact on their PIPP Psychological subscale (p ¼ .04). generally, and its prevalence is reported to be as high as 67%.31
Time since diagnosis was divided into three approximately Three-quarters of our sample reported some degree of breast-
equal groups (<¼1.8 yrs, 1.9e4.1 yrs, 4.2þ yrs). Kruskal Wallis tests specific pain (mixed patterns), similar to other reports7; although
showed significantly different scores across these groups on the these have not been well studied in BC. Interestingly, participants
DASS Depression (p ¼ .01), PIPP Participation (p ¼ .01) and PIPP also reported phantom breast pain (6%) and phantom breast
Relationship (p ¼ .02) scales, with higher depression levels and sensation (15%). These however were beyond the scope of this
greater impact for the more recently diagnosed. preliminary study and needs further exploration.
Improved survival in BC has produced a growing acceptance
Treatment related factors of BC as a long-term illness impacting psychological functioning
and QoL. Psychological morbidity (anxiety, depression, stress,
There were no significant differences in scale scores across altered emotional reactions, sleep disturbance, social isolation)
different surgery types, or for women who received reconstructive are common responses to BC.32e34 These responses may be
surgery, had lymph node involvement, or were estrogen-receptor related to pain,35 treatment side effects, especially chemo-
positive. Chemotherapy was associated with greater impact scores therapy36; and early onset menopause and fertility concerns.37,38
on the PIPP subscales (Psychological, p ¼ .005; Mobility, p < .001; Fann et al. suggest the rate for major depression of 10e25% in
Participation, p ¼ .002; Relationships, p ¼ .02). Women who women with BC.39 Within one year of diagnosis up to 30% of
received radiotherapy recorded slightly higher FIM motor total women with BC may develop a psychological morbidity either
scores (p ¼ .02). anxiety or depressive disorder.40 Participants in our study, with
a median time since diagnosis of 2.2 years, reported elevated
Current symptoms levels of anxiety and depression (22%) (higher than normative
Australian data), in contrast to a previous study of psychological
Lymphodema was associated with higher impact scores on the distress that showed a decrease over a 5-year study period.41
PIPP subscales (Psychological, p ¼ .003; Self-care, p ¼ .001; Another study however showed that anxiety or depression or
Mobility, p ¼ .03; Participation, p ¼ .007), and on DASS Anxiety both reported by women with BC did not change over 5 years of
scale (p ¼ .02). follow-up.42 This range of variation in psychological disorders
Participants with shoulder limitations due to pain recorded may be attributed to methodological differences across studies.43
higher scores on all PIPP subscales (p < .005), and the DASS Stress This has important clinical implications for long-term moni-
(p ¼ .03) and Anxiety (p ¼ .007) subscales. Limited range of toring, education, support and counselling of the BC patients
shoulder movement was also associated with higher scores on the (and their families).
PIPP subscales (Psychological, p ¼ .03; Mobility, p ¼ .02; Relation- Restricted activity alone explains only a minor part in the vari-
ship, p ¼ .03; Self-Care, p ¼ .001). ance of health-related QoL,44 as many factors may influence QoL. In
Participants with upper limb weakness (MRC scores of 0e4 on our study 32% of women after BC reported high impact on PIPP
affected side) had worse scores on the FIM Locomotion scale Psychological wellbeing, and substantial impact (22%) on the
(p ¼ .04); higher impact on PIPP Self-Care (p ¼ .01), Mobility Participation subscales. These are consistent with reports of
(p < .001), Participation (p < .001), and Relationship (p ¼ .04) participatory limitation (work, social and recreational activity,
subscales; and higher DASS Anxiety scores (p ¼ .007). family life, caregiver stress, activities of daily life) in other BC
cohorts.32,34 This study identified factors associated with poorer
Discussion current level of functioning and wellbeing (i.e., high impact on PIPP
and DASS anxiety subscales): younger patients; recent diagnoses,
This is the first report of factors associated with long-term aggressive tumour, those receiving chemotherapy, shoulder limi-
functional and psychological outcomes for women after BC tation due to pain, and lymphoedema; consistent with other
treatment, residing in the Australian community. The BC patients reports.45e48 No significant differences in scale scores were found
in this study are similar to those in other studies in terms of age, across different surgical procedures (including reconstructive
gender, disease severity and treatment.21e23 Most patients are surgery), estrogen-receptor status or lymph node involvement on
expected to make a good recovery following definitive treatment outcomes used.
for BC, as the medium to long-term effects of treatment are The ICF11 provides a framework for describing the impact of
considered minimal in the majority of cases. However, long-term disease at the level of impairment, limitation in activity and
physical and psychological morbidity associated with BC treat- participation. This is the first study to assess functional limitation in
ment can be under estimated.24 A recent study showed that 1 year women after BC using the ICF domains. Recently, patient reported
after BC surgery, patients did not recover their pre-operative problems due to BC were linked with categories of ICF49 to high-
physical activity levels, especially in older patients, smokers and light the patient perspective; so that selected disabilities can be
those without a spouse.21 Although participants in our study addressed in multidisciplinary care settings. These in the future
made good functional recovery (a median motor FIM score of 78), may enable more comprehensive measurement of participatory
they reported residual neurological deficits (motor and sensory) issues in this population.
with weakness of the upper limb on the affected side, limited Some caution needs to be exercised in the interpretation of the
shoulder movements (adhesive capsulits), pain limiting shoulder group comparisons conducted in this study due to the substantial
range; and lymphoedema, similar to other reports.24e26 The number of univariate statistical analyses undertaken, with no
incidence of lymphoedema (29%) in this cohort is within the adjustment to the alpha value used to indicate statistical signifi-
reported range of 6e30%.16 A number of reviews support exercise cance. This study was intended as a preliminary descriptive study,
F. Khan et al. / The Breast 21 (2012) 314e320 319
with the aim to identify possible factors that may impact on long- References
term outcomes. Further research using larger studies and sophis-
ticated multivariate analyse need to be undertaken to extend these 1. World Health Organisation. The global burden of disease: 2004 update. Geneva:
WHO; 2008.
finding. This study utilized a relatively small sample in a tertiary 2. Australian Institute of Health and Welfare (AIHW). Breast cancer in Australia: an
regional metropolitan region which may limit the generalizability overview. National Breast and Ovarian Cancer Centre, Cancer Series no 50. Cat
and validity of these findings. The BC survivors in this study no CAN 46. Canberra, Australia: AIHW; 2009.
3. International Agency for Research on Cancer (IARC). World cancer report. Lyon:
however are similar to BC patients in other cohorts in terms of their IARC; 2008.
gender, disease severity and course. This study provides longitu- 4. Lacey Jr JV, Kreimer AR, Buys SS, Marcus PM, Chang S, Leitzmann MF, et al.
dinal information, including information from the BC participants Breast cancer epidemiology according to recognized breast cancer risk factors
in the Prostate, Lung, Colorectal and Ovarian (PLCO) cancer screening trial
in the community. The participants had strict inclusion criteria and cohort. BMC Cancer 2009;9:84.
were listed on a database of people with BC held at the RMH and 5. Danaei G, Vander Hoorn S, Lopez AD, Murray CJ, Ezzati M. Causes of cancer in
who agreed to participate in research projects. In an attempt to the world: comparative risk assessment of nine behavioural and environmental
risk factors. Lancet 2005;366:1784e93.
reduce recall bias, all questions were limited in the main to the
6. Yip C, Smith RA, Anderson BO, Miller AB, Thomas DB, Ang ES, et al. Guideline
current situation. Medical records were used to confirm participant implementation for breast healthcare in low-and middle-income countries:
self-report. This method of information gathering has potential early detection resource allocation. Cancer 2009;113:2244e56.
7. Franklin DJ. Cancer rehabilitation: challenges, approaches and new directions.
information bias. Problems not included within the domains of the
Phys Med Rehabil Clin N Am 2007;18:899e924.
outcome measures used were not able to be identified; the 8. MacDonald L, Bruce J, Scott NW, Smith WC, Chambers W. Long term follow-up
measures used however were broad and expansive. We acknowl- of breast cancer survivors with post mastectomy pain syndrome. Br J Cancer
edge that other factors may have impacted depression and anxiety 2005;92:225e30.
9. Carpenter JS, Andrykowski MA, Sloan P, Cunningham L, Cordova MJ, Studts JL,
in BC participants and were not studied. More research into et al. Post mastectomy/post lumpectomy pain in breast cancer survivors. J Clin
ongoing pain, shoulder limitation and lymphoedema outcomes in Epidemiol 1998;51:1285e92.
these persons is needed. 10. Tager FA, McKinley PS, Schnabel FR, El-Tamer M, Cheung YK, Fang Y, et al. The
cognitive effects of chemotherapy in post-menopausal breast cancer patients:
a controlled longitudinal study. Breast Cancer Res Treat 2010;123:25e34.
11. World Health Organization (WHO). The International Classification of Func-
Conclusions
tioning, Disability and Health (ICF). Geneva: WHO; 2001.
12. Silver JK. Rehabilitation in women with breast cancer. Phys Med Rehabil Clin N
Many challenges can exist for BC survivors’ years after definitive Am 2007;18:521e37.
treatment, requiring integrated long-term management. The 13. American Joint Committee on Cancer (AJCC). Breast. In: AJCC cancer staging
manual. 6th ed. New York: Springer; 2002.
factors associated with long-term functional and psychological 14. Paternostro-Sluga T, Grim-Stieger M, Posch M, Schuhfried O, Vacariu G,
sequelae in BC participants in this study have important implica- Mittermaier C, et al. Reliability and validity of the Medical Research Council
tions for treating clinicians and need to be explored in larger and (MRC) scale and a modified scale for testing muscle strength in patients with
radial palsy. J Rehabil Med 2008;40:665e71.
different BC cohorts. The ICF may provide clinicians a common 15. Wewers ME, Lowe NK. A critical review of visual analogue scales in the
framework for targeted multidisciplinary care in specific domains, measurement of clinical phenomena. Res Nurs Health 1990;13:227e36.
and focus on participatory issues in these persons. 16. Petrek JA, Pressman PI, Smith RA. Lymphedema: current issues in research and
management. CA Cancer J Clin 2000;50:292e307.
17. Hamilton BB, Granger CV, Sherwin FS, Zielezny M, Tashman JS. A uniform national
data system for medical rehabilitation. In: Fuhrer MJ, editor. Rehabilitation
Ethical approval
outcomes: analysis and measurement. Baltimore, MD: Brookes; 1987. p. 137e47.
18. Heinemann AW, Linacre JM, Wright BD, Hamilton BB, Granger C. Relationships
The study was approved by the Royal Melbourne Hospital between impairment and physical disability as measured by the Functional
Ethical Committee and informed consent was obtained from all the Independence Measure. Arch Phys Med Rehabil 1993;74:566e73.
19. Lovibond SH, Lovibond PF. Manual for the depression, anxiety, stress scales.
subjects. Sydney: The Psychology Foundation of Australia Inc.; 1995.
20. Pallant JF. Development and validation of a scale to measure perceived control
of internal states. J Pers Assess 2000;75:308e37.
Conflict of interest statement 21. Devoogdt N, Van Kampen M, Geraerts I, Coremans T, Fieuws S, Lefevre J, et al.
Physical activity levels after treatment for breast cancer: one-year follow-up.
Breast Cancer Res Treat 2010;123:417e25.
The authors declare that they have no conflict of interest.
22. Han JG, Jiang YD, Zhang CH, Pang D, Zhang M, Wang YB, et al. Clinicopathologic
characteristics and prognosis of young patients with breast cancer. Breast
2011;20:370e2.
Financial disclosure 23. Clayforth C, Fritschi L, McEvoy SP, Byrne MJ, Ingram D, Sterrett G, et al. Five-
year survival from breast cancer in Western Australia over a decade. Breast
None. 2007;16:375e81.
24. Loprinzi PD, Cardinal BJ. Effects of physical activity on common side effects of
breast cancer treatment. Breast Cancer 2011 [Epub ahead of print].
25. Hayes SC, Reul-Hirche H, Turner J. Exercise and secondary lymphedema: safety,
Licence statement
potential benefits, and research issues. Med Sci Sports Exerc 2009;41:483e9.
26. Taira N, Shimozuma K, Shiroiwa T, Ohsumi S, Kuroi K, Saji S, et al. Associations
The Corresponding Author has the right to grant on behalf of all among baseline variables, treatment-related factors and health-related quality of
authors and does grant on behalf of all authors, an exclusive licence life 2 years after breast cancer surgery. Breast Cancer Res Treat 2011;128:735e47.
27. De Backer IC, Schep G, Backx FJ, Vreugdenhil G, Kuipers H. Resistance training
to The Breast. in cancer survivors: a systematic review. Int J Sports Med 2009;30:703e12.
28. Ibrahim EM, Al-Homaidh A. Physical activity and survival after breast cancer
diagnosis: meta-analysis of published studies. Med Oncol 2011;28:753e65.
Acknowledgement 29. Miller WR. Motivational interviewing in the service of health promotion. The
art of health promotion: practical information to make programs more effec-
tive. Am J Health Promot 2004;2:1e10.
We thank all the participants with breast cancer who partici-
30. Stamatakos M, Stefanaki C, Kontzoglou K. Lymphedema and breast cancer:
pated in this study. We particularly wish to thank Ms L Oscari for a review of the literature. Breast Cancer 2011;18:174e80.
arranging interviews and Drs N Zhang, M Demetrious and L Ng for 31. Smith RL, Pruthi S, Fitzpatrick LA. Evaluation and management of breast pain.
Mayo Clin Proc 2004;79:353e72.
participant assessments. We also acknowledge support of Prof B
32. Ganz PA, Desmond KA, Leedham B, Rowland JH, Meyerowitz BE, Belin TR.
Mann and Dr A Skandarajah of Cancer Services at the Royal Quality of life in long-term, disease-free survivors of breast cancer: a follow-up
Melbourne Hospital. study. J Natl Cancer Inst 2002;94:39e49.
320 F. Khan et al. / The Breast 21 (2012) 314e320
33. Schnipper HH. Life after breast cancer. J Clin Oncol 2001;19:3581e4. 42. Hopwood P, Sumo G, Mills J, Haviland J, Bliss JM. The course of anxiety and
34. Vos PJ, Visser AP, Garssen B, Duivenvoorden HJ, de Haes HC. Effects of delayed depression over 5 years of follow up and risk factors in women with early
psychosocial interventions versus early psychosocial interventions for women breast cancer: results from the UK Standardisation of Radiotherapy Trials
with early stage breast cancer. Patient Educ Couns 2006;60:212e9. (START). Breast 2010;19:84e91.
35. Reddick BK, Nanda JP, Campbell L, Ryman DG, Gaston-Johansson F. Examining 43. Jassim GA, Whitford DL, Grey IM. Psychological interventions for women with
the influence of coping with pain on depression, anxiety, and fatigue among non-metastatic breast cancer. Cochrane Database Syst Rev 2010 [Art. No.:
women with breast cancer. J Psychosoc Oncol 2005;23:137e57. CD008729].
36. Boehmke MM, Dickerson SS. Symptom, symptom experiences, and symptom 44. Bernsen RA, Jacobs HM, de Jager AE, van der Meche FG. Residual health status
distress encountered by women with breast cancer undergoing current after GuillaineBarre syndrome. J Neurol Neurosurg Psychiatry 1997;62:637e40.
treatment modalities. Cancer Nurs 2005;28:382e9. 45. Arora NK, Gustafson DH, Hawkins RP, McTavish F, Cella DF, Pingree S, et al.
37. Baucom DH, Porter LS, Kirby JS, Gremore TM, Keefe FJ. Psychosocial issues Impact of surgery and chemotherapy on the quality of life of younger women
confronting young women with breast cancer. Breast Dis with breast carcinoma: a prospective study. Cancer 2001;92:1288e98.
2005e2006;23:103e13. 46. Avis NE, Crawford S, Manuel J. Quality of life among younger women with
38. Peate M, Meiser B, Hickey M, Friedlander M. The fertility-related concerns, breast cancer. J Clin Oncol 2005;23:3322e30.
needs, and preferences of younger women with breast cancer: a systematic 47. Janz NK, Mujahid MS, Hawley ST, Griggs JJ, Alderman A, Hamilton AS, et al.
review. Breast Cancer Res Treat 2009;116:215e23. Racial/ethnic differences in quality of life after diagnosis of breast cancer.
39. Fann J. Major depression after breast cancer: a review of epidemiology and J Cancer Surviv 2009;3:212e22.
treatment. Gen Hosp Psychiatry 2008;30:112e26. 48. Kwan ML, Ergas IJ, Somkin CP, Quesenberry Jr CP, Neugut AI, Hershman DL,
40. Bleiker EM, Pouwer F, van der Ploeg HM, Leer JW, Ader HJ. Psychological et al. Quality of life among women recently diagnosed with invasive breast
distress 2 years after diagnosis of breast cancer: frequency and prediction. cancer: the pathways study. Breast Cancer Res Treat 2010;123:507e24.
Patient Educ Couns 2000;40:209e17. 49. Khan F, Amatya B, Ng L, Demetrios M, Pallant JF. Relevance and completeness of
41. Burgess C, Cornelius V, Love S, Graham J, Richards M, Ramirez A. Depression the International Classification of Functioning, Disability and Health (ICF)
and anxiety in women with early breast cancer: five year observational cohort comprehensive breast cancer core set: the patient perspective in an Australian
study. BMJ 2005;330:702e5. community cohort. J Rehabil Med 2011; [accepted for publication, 19 Jan 2012].