- Email: [email protected]
How do we manage breast cancer in the elderly patients?
Critical Reviews in Oncology/Hematology 52 (2004) 135–141
How do we manage breast cancer in the elderly patients? A survey among members of the British Association of Surgical Oncologists (BASO) Riccardo A. Audisioa,b,∗ , Nadir Osmanb , Matilde M. Audisioc , Fabrizio Montaltod a
Department of General Surgery, Whiston Hospital – Prescot, University of Liverpool, Liverpool College, Merseyside L35 5DR, UK b University of Liverpool, UK c Liverpool College, UK d SSN Distretto 2, Milano, Italy Accepted 6 August 2004
Contents 1.
Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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2.
Materials and methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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3.
Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Surgeons characteristics. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Attitudes toward the elderly . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3. Comprehensive assessment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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4.
Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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Reviewers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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Biography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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Abstract Aims: To frame the attitude and perception of breast surgeons in the UK toward the increasing number of older breast cancer patients. Methods: A 15-item questionnaire was designed to inquire on the definition of elderly, clinical management, age-related differences in surgical treatment, interaction with geriatricians, operative risk assessment, and surveyed identification/descriptive data. The questionnaire was sent to all 350 ABS associates (Association of Breast Surgery) at the British Association of Surgical Oncology (BASO). Results: A 150 questionnaires were returned (compliance 43%) providing the largest sample of breast surgical specialist overview on this topic. The major part of the surveyed (44%) stated age does not stand as the most relevant factor on its own in identifying a patient as “elderly”, nor in offering surgical management (98%) and in dealing with the axilla (75%). The surveyed are aware of the burden of this epidemiological problem and would rather finalise the decision-making process based on multiple factors. This is to tailor the most appropriate treatment aiming to improving quality of life (42%) and quality adjusted survival (40%). Although most breast surgeons are inclined to discuss their onco-geriatric patients with geriatricians on a regular (32%) or occasional (42%) basis, no geriatric assessment is routinely utilised (82%) and the operative risk is predicted with ASA (45%). These figures confirm the surveyed breast surgeons in the UK are not biased by an ageistic approach, and aim to achieve a global well-being to the older patients with breast cancer. ∗
Corresponding author. Tel.: +441514301079; fax: +441514301891. E-mail address: [email protected] (R.A. Audisio).
1040-8428/$ – see front matter © 2004 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.critrevonc.2004.08.002
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Conclusions: This survey confirms our lack of knowledge in the management of elderly patients affected by breast cancer. Taken into account the limitations of a survey, we are pleased to confirm the performance of the largest part of breast surgeons at BASO is not biased by an ageist mentality. © 2004 Elsevier Ireland Ltd. All rights reserved. Keywords: Breast cancer; Elderly; Surgery; Survey; BASO
1. Introduction Breast cancer is highly prevalent among industrialised countries, 45% breast tumours affecting patients >65 years [1]. On the other hand our population is dramatically ageing [2] while the incidence of breast cancer rises with age, peaking at about age 75 and then declining slightly [3]. Despite the epidemiological burden of this condition, literature is conflicting (five references), resulting in a lack of knowledge regarding the management of the older patients, as the surgical attitude is mainly based on personal preferences rather than being evidence based [4–8]. The definition of the “elderly” is obscure at a clinical level, the biology of breast cancer on this group remains unknown, the advantages of aggressive surgical management ± axillary dissection still needs to be defined, pre-operative assessment of the surgical risk is not fully understood, and the quality of life offered to this specific cohort is poorly investigated. With the aim of defining our standards and appraising our perception of the elderly breast cancer patient’s needs, a survey was set up in the UK, where the prevalence of breast cancer is among the highest world wide.
2. Materials and methods The Association of Breast Surgery (ABS) at BASO is the speciality association of surgeons in charge of the management of the largest part of breast cancers in the UK. As a branch of BASO – The Association for Cancer Surgery, the ABS at BASO aims to represent, assist and educate its membership in the constantly changing field of breast surgery. A specifically designed questionnaire was distributed among all 350 members. This is a 15-item questionnaire enquiring on clinical management, definition of the elderly patient, differences in their surgical attitudes when compared to the younger subsetting, interaction with geriatricians, assessment of the operative risk, plus personal data from each single surgeon including special interest, seniority (Table 1). The hospital postcodes were used to group the surveyed surgeons according to the deprivation (i.e. socio-economic status) of the district in which they worked. From the hospital postcode (i.e. zipcode or area code), the national rank (in terms of deprivation) of the district the hospital served was identified [9]. A higher rank meaning the district was more deprived. For the sake of simplicity, the surgeons were then put into three groups: those working in districts ranking in the top third (i.e. most deprived), middle third and bottom third
(i.e. least deprived) nationally. This data was then used to see whether any correlation existed between the deprivation of the district and surgeons attitudes and management of elderly patients.
3. Results Of the 350 submitted questionnaires, 150 were returned appropriately completed, one of those being invalid (43% response rate). 3.1. Surgeons characteristics The surveyed surgeons were practising in different settings (District General Hospitals 27%; teaching hospitals 32%; comprehensive cancer centres 26%; others 15%); the majority were appointed as consultant breast surgeons (74%), 12% were surgical oncologists, and 14% general surgeons (Table 1). With regards to personal experience in the field, a small number were in place for <5 years (9%), 13% between 6 and 10 years, the largest being in place for over 10 years (78%). The 109 postcodes were made available, with the largest proportion of surgeons working in the top third most deprived districts in the country (48%). This was only for surgeons working in England who had supplied valid postcodes. Surgeons working in other parts of the UK (Wales, Scotland and Ireland) who had supplied valid postcodes were excluded due to deprivation being measured in differing ways in these countries making meaningful comparison difficult. Deprivation ranks have been tested against all variables and there is no statistical evidence of any impact on surgeons’ preferences and management. A very small number (1%) claimed that <20% of their patients were elderly, while 45% considered the proportion of geriatric patients accounted for 20–50% of the overall number of their patients, and 40% claimed that more than half their patients were elderly. 3.2. Attitudes toward the elderly Two surgeons (1%) considered the elderly as a patient beyond the age of 65 years, 12% draw a line beyond the age of 70, 20% beyond the age of 75, and 23% beyond the age of 80 years, while the largest group (44%) stated that age is not the relevant factor on its own.
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Table 1 The 15-item questionnaire Please state your postal code: Deprivation ranks TOP third nationally (most deprived) Middle third nationally Bottom third nationally
52 (48%) 35 (32%) 22 (20%)
How would you define your hospital? Community hospital Teaching hospital Comprehensive cancer centre Other
40 (27%) 48 (32%) 39 (26%) 23 (15%)
What is your role? Breast Surgeon Surgical Oncologist General Surgeon
111 (74%) 18 (12%) 21 (14%)
For how many years have you been dealing with breast cancer? 1–5 Years 6–10 Years >10 Years
13 (9%) 19 (13%) 118 (78%)
How many elderly cancer patients do you see in your routine practice? None <20% of practice 20–50% >50%
2 (1%) 21 (14%) 67 (45%) 60 (40%)
In your clinical practice, what would be your chronological cut-off in defining a patient as “elderly”? ≥65 Years ≥70 Years ≥75 Years ≥80 Years Not relevant
2 (1%) 18 (12%) 30 (20%) 34 (23%) 66 (44%)
What would be your cut-off point for not offering elective breast surgery at all? ≥65 Years ≥70 Years ≥75 Years ≥80 Years Not relevant
– 1 (0.6%) – 1 (0.6%) 148 (98%)
Which of the following criteria would advise in favour of elective breast surgery? Biological characteristics of the tumour Patient’s chronological age Patient’s biological age Social conditions All of the above
5 (3%) 8 (6%) 50 (34%) – 85 (57%)
How do you in principle deal with the axilla in the elderly patients? Dissection Sampling Sentinel node All the above None
50 (33%) 21 (14%) 2 (2%) 32 (21%) 45 (30%)
Is this in any different from the way you would approach the same problem in a younger patient? Yes No
38 (25%) 112 (75%)
What is the age limit you see for breast reconstruction? ≥65 Years ≥70 years ≥75 years ≥80 years Not relevant
28 (19%) 34 (23%) 19 (13%) 1 (1%) 67 (44%)
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Table 1 (Continued ) The most adequate end-point in monitoring surgical outcomes in the elderly patients with breast cancer is: Disease-free survival Overall survival Quality of Life Quality adjusted survival
19 (13%) 6 (4%) 63 (42%) 59 (40%)
Do you co-operate with the geriatricians in managing your elderly patients with breast cancer? Never Rarely Sometimes On a regular basis
7 (5%) 32 (21%) 63 (42%) 48 (32%)
Do you use any of Geriatric Assessment Instrument before planning a surgical procedure? Routinely Sometimes Never
2 (2%) 23 (16%) 122 (82%)
Which Assessment Instrument do you use before planning an elective surgical procedure? ASA Routinely 67 (45%); sometimes 11 (7%) POSSUM Routinely 4 (3%); sometimes 11 (7%) P POSSUM Routinely 3 (2%); sometimes 6 (4%) GA Routinely 2 (1%); sometimes 10 (7%) None 57 (38%) ASA: American Society of Anesthesiologists; POSSUM: physiological and operative severity score for enumeration of mortality and morbidity; P POSSUM: Portsmouth POSSUM modification; GA: geriatric assessment.
When asked what would be a theoretical cut-off point for not offering elective breast surgery at all, almost the entire group stated that age on its own was not a relevant parameter (98%). Surgeons were then asked to specify which criteria would advise in favour of elective breast surgery and only 6% claimed they would adopt the patient’s chronological age as the only parameter; conversely one-third (34%) claimed they would favour the patient’s biological age, 3% would consider the tumour biology, 57% would consider all the above, and 37% would consider all parameters but chronological age. With regards to the surgical management of the axilla, 33% would consider a standard dissection, 14% would favour axillary sampling, 2% would offer sentinel node dissection; 21% would be prepared to offer all the above options and 30% stated they would not consider offering any surgery to the axilla at all. No difference was noticed when the surveyed were distributed according the deprivation ranks. Seventy-five percent stated their surgical management would not differ according to the patients age, while onefourth of the questioned surgeons would provide a different surgical management. The largest number of surgeons (44%) stated they considered age as not relevant in deciding whether to provide breast reconstruction to the elderly breast cancer patient, while the age limit of 65, 70, 75, and 80 years was a relevant cut-off for 19%, 23%, 13%, 1%, respectively. Only six surgeons (4%) consider overall survival as the end-point in monitoring surgical outcomes the elderly patient with breast cancer, 13% would target their treatment on disease free survival, but the majority would privilege the patient’s quality of life (42%) or quality adjusted survival (40%).
3.3. Comprehensive assessment One-third of the surgeons responding to our questionnaire used to co-operate with geriatricians on a regular basis (32%); conversely, 5% never involved the geriatricians, while 21 and 42% rarely or sometimes discuss their elderly patients with geriatricians, respectively. The largest proportion of breast cancer surgeons (82%) claimed the lack of habit to utilise any Geriatric Assessment Instrument before or after the surgical procedure, 16% occasionally did so, and only 2% utilised such an instrument on a routine basis. When questioned which sort of pre-operative assessment they would provide to appraise the operative risk, 57 (38%) stated they do not use any specific instrument, 78 (52%) rely on the American Society of Anesthesiologists (ASA) score [10] as performed by the anaesthesiologists (67 routinely and 11 on an occasional basis), 15 (10%) use physiological and operative severity score for enumeration of mortality and morbidity (POSSUM) [11,12] (four routinely and 11 occasionally), 9 (6%) use Portsmouth POSSUM modification (P POSSUM) [13], and finally 12 breast surgeons utilise either a standardised Geriatric Assessment tool, or their institutional instrument.
4. Discussion Very little is known about breast cancer in the elderly, apart from the dramatic increase in number [2,3]. Breast cancer is undertreated in the older patient [14], and undertreatment strongly decreases prognosis [15]. The operative risk is increased as a consequence of a higher incidence
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of coexisting diseases, and there is a 20-fold higher rate of non-breast-cancer deaths in patients with ≥3 comorbidities [16]. Our lack of knowledge is due to a lack of definitions: who is elderly? While a vivid debate is undergoing amongst the scientific community, everyday clinical practice is centred on older cancer patients. The authors are not aware of any previous survey on this topic, with the exception of an original article on the attitudes of medical oncologists in the management of elderly breast cancer patients [17]. The present survey was facilitated by the Association of Breast Surgery at BASO, representing the largest majority of surgeons in the UK with an interest in breast cancer. The sample is reliable as it encompasses specialists from teaching hospitals, district general hospitals and comprehensive cancer centres. A 43% compliance confers robustness to this survey, and is in keeping with several other surveys [18–20]. It is interesting to notice how the majority of breast surgeons participating to the survey practice in districts ranking within the top third most deprived in the country (48%), while surgeons from the least deprived areas are obviously reluctant to contribute to surveys. The 74% surveyed clinicians are acting as dedicated breast surgeons and 12% surgical oncologists, while 14% are general surgeons with an interest on breast disease. The most part of the surveyed population (78%) has been in place for over 10 years, and more than 90% over 5 years. The majority of the surgeons seem to be aware of the burden of elderly patients developing breast cancer, since 40% claim their clinical practice is mainly dealing with elderly patients, plus 45% stating they are dealing with elderly patients between 20 and 50% of their workload. A clear age cut-off is not conceivable to define the patient as “elderly” on the sole basis of the chronological age for the largest part of surveyed surgeons (44%), while the rest of the sample considers a possible age cut-off at age 70 (12%), 75 (20%) or 80 (23%). Only two surgeons would consider the elderly as 65 years or older. This differs from the BIG survey [12] where 62% medical oncologists agreed on a 70 year cut-off for the purpose of administering adjuvant palliative therapy, and 65 remains as the starting date for Medicare eligibility in the US. Conversely, there is a trend with the surveyed medical oncologists [12] in that no agreement exists on the age cut-off for denying treatment, with 98% surveyed breast specialists not accepting age as a reason for exclusion to surgical management. The unreliability of crude anagraphical data is reinforced by acknowledging that elective breast cancer surgery should not be denied, no matter the patients age (98%); only two surgeons stating they would not favour breast cancer surgery on election above 70, or 80 years, respectively. Most breast surgeons are inclined to base their treatment planning on a complexity of biological, anagraphical, and
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social issues (57%). Further on, 34% of the surveyed claim they would be inclined to prioritise the patient’s biological age however appraised, while only 6% would rely on chronological age as the main cut-off. We are in need of a standardised pre-operative assessment capable of characterising the patient’s “functional age”, in order to optimise treatment planning and stratify outcomes on the basis of factors other than chronological age. To satisfy this need a prospective clinical research project has been designed and started [21]. The issue of how to treat the axilla is a complex one. It is widely agreed that the axillary lymph nodes should be staged to aid in determining prognosis and therapy [22]. The surprised international reader should appreciate the peculiarity of the UK setting where a level 2 or 3 axillary dissection is rarely performed, as most surgeons still favour the sampling technique. Although most authorities agree that an axillary node dissection in the presence of clinically negative nodes is a necessary staging procedure, controversy exists as to the extent of the procedure because of long-term morbidity (arm discomfort and swelling) associated with it [23]. This is particularly relevant to the older breast cancer patient, where quality of life issues are to be prioritised over a debatable advantage in long-term survival. In the lack of major contraindications, one-third or the surveyed would advise in favour of dissection (33%) and another fraction privileges axillary sampling (14%). An impressive 30% is “in principle” against any surgical dissection: this might be an heritage of a few inappropriately designed and relatively small investigations sadly popularised in the early 1980’s, which set a trend toward conservative (under)treatment [24–27]. In an effort to decrease the morbidity of axillary lymphadenectomy while maintaining accurate staging, several investigators have studied lymphatic mapping and sentinel lymph node biopsy (SLNB) in women with invasive breast cancer [28]. Although reports demonstrate a 97.5–100% concordance between SLN biopsy and complete axillary lymph node dissection [29–31], SLNB is presently not feasible in the UK outside the ALMANAC trial. The restricted number of breast specialists providing SLNB, no matter the patient’s age, is consequently explained to the surprised international reader. Indeed three out of four surveyed (75%) would not consider a different approach to the axilla solely on the base of the patient’s age. No substantial geographical variation was detected, and the deprivations ranks do not seem to impact on the management. Recent reports have positively commented on the feasibility and outcomes of breast reconstruction in the elderly [32,33], but no clear guideline is available, especially with respect to this patients’ age groups; again, the most part of the surveyed would not base their decision on age (44%), while others would identify a cut-off point at 65 (19%), 70 (23%), 75 (13%), and 80 years (1%), respectively. The amount of time to survive from cancer treatment is identified as the most adequate end-point by a small minority
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(4%), while surviving without cancer is the target for 13%. Conversely, there is consistent agreement on the quality of life the patient is offered as the main target, with 42% aiming for a better quality of life, and 40% for quality adjusted survival. When these findings are compared to the medical oncologists’ survey, we notice a similarity in prioritising quality adjusted survival and neglecting overall survival (45 and 12% in their survey, respectively). Noticeably, a difference is evident in targeting disease-free survival, which was highly rated among medical oncologists (40%) while only 13% surgeons would take it as the endpoint for treatment. This point deserves further medical, ethical, and economical research, in view of the dramatic expansion of life expectancy of senior patients and healthy individuals: a 65, 75, and 85 healthy subject is expected to live 20, 12, and 6 years, respectively; 9.7, 7.3, and 4.5 years, respectively for a sick person [34]. The role and value of a possible co-operation with geriatricians is obviously highly valued among surgeons: only 5% claims never discussing their oncogeriatric patients; conversely, 21% do interact with the geriatricians although rarely, 42% do so only at times, and 32% on a regular basis. While at least 74% surgical patients are likely to be discussed with the care of the elderly team, only 15% were likely to have such a consultation in Biganzoli’s findings [17]. This sharp difference might be explained with a much wider geographical variability of her sample. Finally, a reliable preoperative risk assessment tool is not available as yet and the majority of the surveyed never utilises a Geriatric Assessment Instrument (82%), compared with 16% who use it occasionally; 2% use it on a regular basis. Similar findings are reported for medical oncologists [17]. A simple and reliable pre-surgical assessment tool is being validated within an international prospective study; preliminary results confirm its practical utility in identifying possible associations between its components and postoperative morbidity [21]. The risk assessment is most probably left in the hands of the anaesthetist since 45% surgeons rely on the ASA classification on a routine basis, plus 7% occasionally. A restricted number of breast surgeons attempts stratifying the operative risk with POSSUM (3% routinely, and 7% sometimes), P POSSUM (2% routinely, and 4% sometimes), or a specific Geriatric Assessment Instrument (1%). Still 38% claims not to be utilising a risk assessment tool. Further research is needed to avoid any under-treatment on the basis of an ageistic approach, while protecting the frail older patients from inappropriate over-treatment [35]. Given the limitations of a postal survey and the relatively small sample size, this survey provides an overview of the present approach at a clinical level. The breast surgical community in the UK is not basing their treatment plan on the basis of anagraphycal age, and is committed to providing the best management in order to achieve global well-being to the older patients with breast cancer.
Reviewers Dr. Georges Vlastos, Hˆopitaux Universitaires de Gen`eve, Gyn´ecologie Oncologie et S´enologie, 30, Boulevard de la Cluse CH-1211 Geneva 14, Switzerland. Dr. Arti Hurria, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, NY 10021-6007, USA. Prof. Chris Robertson, Department of Statistics & Modelling Science, Livingstone Tower, Richmond Street, Glasgow, G1 1XT, Scotland, UK. Roberto Gennari, M.D., Vice-Director, Department of surgery, European Institute of Oncology, Via Ripamonti, 435, I-20141 Milan, Italy.
Acknowledgements The authors wish to thank BASO for providing the mailing list and supporting this survey.
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[27] Horobin JM, Preece PE, Dewar JA, Wood RA, Cuschieri A. Longterm follow-up of elderly patients with locoregional breast cancer treated with tamoxifen only. Br J Surg 1991;78(2):213–7. [28] Peintinger F, Reitsamer R, Stranzl H, Ralph G. Comparison of quality of life and arm complaints after axillary lymph node dissection vs. sentinel lymph node biopsy in breast cancer patients. Br J Cancer 2003;89(4):648–52. [29] Veronesi U, Paganelli G, Viale G, et al. Sentinel lymph node biopsy and axillary dissection in breast cancer: results in a large series. J Natl Cancer Inst 1999;91(4):368–73. [30] Veronesi U, Paganelli G, Viale G, et al. A randomized comparison of sentinel-node biopsy with routine axillary dissection in breast cancer. N Engl J Med 2003;349(6):546–53. [31] Rubio IT, Korourian S, Cowan C, et al. Sentinel lymph node biopsy for staging breast cancer. Am J Surg 1998;176(6):532–7. [32] Lipa JE, Youssef AA, Kuerer HM, Robb GL, Chang DW. Breast reconstruction in older women: advantages of autogenous tissue. Plast Reconstr Surg 2003;111(3):1110–21. [33] Girotto JA, Schreiber J, Nahabedian MY. Breast reconstruction in the elderly: preserving excellent quality of life. Ann Plast Surg 2003;50(6):572–8. [34] Extermann M, Balducci L, Lyman GH. What threshold for adjuvant therapy in older breast cancer patients? J Clin Oncol 2000;18:1709–17. [35] Wyld L, Reed MW. The need for targeted research into breast cancer in the elderly. Br J Surg 2003;90(4):388–99.
Biography Riccardo A. Audisio was born and trained in Milan, Italy. He moved to the UK in 1999 as a Consultant Surgical Oncologist and Hon. Senior Lecturer at the University of Liverpool. He has focused his clinical research on Geriatric Oncology, and is presently chair of the surgical task force at SIOG. He is involved with the EORTC Cancer in the Elderly Study Group, and recently chaired an advanced course for ESO on this topic.
How do we manage breast cancer in the elderly patients? A survey among members of the British Association of Surgical Oncologists (BASO) Riccardo A. Audisioa,b,∗ , Nadir Osmanb , Matilde M. Audisioc , Fabrizio Montaltod a
Department of General Surgery, Whiston Hospital – Prescot, University of Liverpool, Liverpool College, Merseyside L35 5DR, UK b University of Liverpool, UK c Liverpool College, UK d SSN Distretto 2, Milano, Italy Accepted 6 August 2004
Contents 1.
Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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2.
Materials and methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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3.
Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Surgeons characteristics. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Attitudes toward the elderly . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3. Comprehensive assessment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
136 136 136 138
4.
Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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Reviewers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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Biography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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Abstract Aims: To frame the attitude and perception of breast surgeons in the UK toward the increasing number of older breast cancer patients. Methods: A 15-item questionnaire was designed to inquire on the definition of elderly, clinical management, age-related differences in surgical treatment, interaction with geriatricians, operative risk assessment, and surveyed identification/descriptive data. The questionnaire was sent to all 350 ABS associates (Association of Breast Surgery) at the British Association of Surgical Oncology (BASO). Results: A 150 questionnaires were returned (compliance 43%) providing the largest sample of breast surgical specialist overview on this topic. The major part of the surveyed (44%) stated age does not stand as the most relevant factor on its own in identifying a patient as “elderly”, nor in offering surgical management (98%) and in dealing with the axilla (75%). The surveyed are aware of the burden of this epidemiological problem and would rather finalise the decision-making process based on multiple factors. This is to tailor the most appropriate treatment aiming to improving quality of life (42%) and quality adjusted survival (40%). Although most breast surgeons are inclined to discuss their onco-geriatric patients with geriatricians on a regular (32%) or occasional (42%) basis, no geriatric assessment is routinely utilised (82%) and the operative risk is predicted with ASA (45%). These figures confirm the surveyed breast surgeons in the UK are not biased by an ageistic approach, and aim to achieve a global well-being to the older patients with breast cancer. ∗
Corresponding author. Tel.: +441514301079; fax: +441514301891. E-mail address: [email protected] (R.A. Audisio).
1040-8428/$ – see front matter © 2004 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.critrevonc.2004.08.002
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Conclusions: This survey confirms our lack of knowledge in the management of elderly patients affected by breast cancer. Taken into account the limitations of a survey, we are pleased to confirm the performance of the largest part of breast surgeons at BASO is not biased by an ageist mentality. © 2004 Elsevier Ireland Ltd. All rights reserved. Keywords: Breast cancer; Elderly; Surgery; Survey; BASO
1. Introduction Breast cancer is highly prevalent among industrialised countries, 45% breast tumours affecting patients >65 years [1]. On the other hand our population is dramatically ageing [2] while the incidence of breast cancer rises with age, peaking at about age 75 and then declining slightly [3]. Despite the epidemiological burden of this condition, literature is conflicting (five references), resulting in a lack of knowledge regarding the management of the older patients, as the surgical attitude is mainly based on personal preferences rather than being evidence based [4–8]. The definition of the “elderly” is obscure at a clinical level, the biology of breast cancer on this group remains unknown, the advantages of aggressive surgical management ± axillary dissection still needs to be defined, pre-operative assessment of the surgical risk is not fully understood, and the quality of life offered to this specific cohort is poorly investigated. With the aim of defining our standards and appraising our perception of the elderly breast cancer patient’s needs, a survey was set up in the UK, where the prevalence of breast cancer is among the highest world wide.
2. Materials and methods The Association of Breast Surgery (ABS) at BASO is the speciality association of surgeons in charge of the management of the largest part of breast cancers in the UK. As a branch of BASO – The Association for Cancer Surgery, the ABS at BASO aims to represent, assist and educate its membership in the constantly changing field of breast surgery. A specifically designed questionnaire was distributed among all 350 members. This is a 15-item questionnaire enquiring on clinical management, definition of the elderly patient, differences in their surgical attitudes when compared to the younger subsetting, interaction with geriatricians, assessment of the operative risk, plus personal data from each single surgeon including special interest, seniority (Table 1). The hospital postcodes were used to group the surveyed surgeons according to the deprivation (i.e. socio-economic status) of the district in which they worked. From the hospital postcode (i.e. zipcode or area code), the national rank (in terms of deprivation) of the district the hospital served was identified [9]. A higher rank meaning the district was more deprived. For the sake of simplicity, the surgeons were then put into three groups: those working in districts ranking in the top third (i.e. most deprived), middle third and bottom third
(i.e. least deprived) nationally. This data was then used to see whether any correlation existed between the deprivation of the district and surgeons attitudes and management of elderly patients.
3. Results Of the 350 submitted questionnaires, 150 were returned appropriately completed, one of those being invalid (43% response rate). 3.1. Surgeons characteristics The surveyed surgeons were practising in different settings (District General Hospitals 27%; teaching hospitals 32%; comprehensive cancer centres 26%; others 15%); the majority were appointed as consultant breast surgeons (74%), 12% were surgical oncologists, and 14% general surgeons (Table 1). With regards to personal experience in the field, a small number were in place for <5 years (9%), 13% between 6 and 10 years, the largest being in place for over 10 years (78%). The 109 postcodes were made available, with the largest proportion of surgeons working in the top third most deprived districts in the country (48%). This was only for surgeons working in England who had supplied valid postcodes. Surgeons working in other parts of the UK (Wales, Scotland and Ireland) who had supplied valid postcodes were excluded due to deprivation being measured in differing ways in these countries making meaningful comparison difficult. Deprivation ranks have been tested against all variables and there is no statistical evidence of any impact on surgeons’ preferences and management. A very small number (1%) claimed that <20% of their patients were elderly, while 45% considered the proportion of geriatric patients accounted for 20–50% of the overall number of their patients, and 40% claimed that more than half their patients were elderly. 3.2. Attitudes toward the elderly Two surgeons (1%) considered the elderly as a patient beyond the age of 65 years, 12% draw a line beyond the age of 70, 20% beyond the age of 75, and 23% beyond the age of 80 years, while the largest group (44%) stated that age is not the relevant factor on its own.
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Table 1 The 15-item questionnaire Please state your postal code: Deprivation ranks TOP third nationally (most deprived) Middle third nationally Bottom third nationally
52 (48%) 35 (32%) 22 (20%)
How would you define your hospital? Community hospital Teaching hospital Comprehensive cancer centre Other
40 (27%) 48 (32%) 39 (26%) 23 (15%)
What is your role? Breast Surgeon Surgical Oncologist General Surgeon
111 (74%) 18 (12%) 21 (14%)
For how many years have you been dealing with breast cancer? 1–5 Years 6–10 Years >10 Years
13 (9%) 19 (13%) 118 (78%)
How many elderly cancer patients do you see in your routine practice? None <20% of practice 20–50% >50%
2 (1%) 21 (14%) 67 (45%) 60 (40%)
In your clinical practice, what would be your chronological cut-off in defining a patient as “elderly”? ≥65 Years ≥70 Years ≥75 Years ≥80 Years Not relevant
2 (1%) 18 (12%) 30 (20%) 34 (23%) 66 (44%)
What would be your cut-off point for not offering elective breast surgery at all? ≥65 Years ≥70 Years ≥75 Years ≥80 Years Not relevant
– 1 (0.6%) – 1 (0.6%) 148 (98%)
Which of the following criteria would advise in favour of elective breast surgery? Biological characteristics of the tumour Patient’s chronological age Patient’s biological age Social conditions All of the above
5 (3%) 8 (6%) 50 (34%) – 85 (57%)
How do you in principle deal with the axilla in the elderly patients? Dissection Sampling Sentinel node All the above None
50 (33%) 21 (14%) 2 (2%) 32 (21%) 45 (30%)
Is this in any different from the way you would approach the same problem in a younger patient? Yes No
38 (25%) 112 (75%)
What is the age limit you see for breast reconstruction? ≥65 Years ≥70 years ≥75 years ≥80 years Not relevant
28 (19%) 34 (23%) 19 (13%) 1 (1%) 67 (44%)
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Table 1 (Continued ) The most adequate end-point in monitoring surgical outcomes in the elderly patients with breast cancer is: Disease-free survival Overall survival Quality of Life Quality adjusted survival
19 (13%) 6 (4%) 63 (42%) 59 (40%)
Do you co-operate with the geriatricians in managing your elderly patients with breast cancer? Never Rarely Sometimes On a regular basis
7 (5%) 32 (21%) 63 (42%) 48 (32%)
Do you use any of Geriatric Assessment Instrument before planning a surgical procedure? Routinely Sometimes Never
2 (2%) 23 (16%) 122 (82%)
Which Assessment Instrument do you use before planning an elective surgical procedure? ASA Routinely 67 (45%); sometimes 11 (7%) POSSUM Routinely 4 (3%); sometimes 11 (7%) P POSSUM Routinely 3 (2%); sometimes 6 (4%) GA Routinely 2 (1%); sometimes 10 (7%) None 57 (38%) ASA: American Society of Anesthesiologists; POSSUM: physiological and operative severity score for enumeration of mortality and morbidity; P POSSUM: Portsmouth POSSUM modification; GA: geriatric assessment.
When asked what would be a theoretical cut-off point for not offering elective breast surgery at all, almost the entire group stated that age on its own was not a relevant parameter (98%). Surgeons were then asked to specify which criteria would advise in favour of elective breast surgery and only 6% claimed they would adopt the patient’s chronological age as the only parameter; conversely one-third (34%) claimed they would favour the patient’s biological age, 3% would consider the tumour biology, 57% would consider all the above, and 37% would consider all parameters but chronological age. With regards to the surgical management of the axilla, 33% would consider a standard dissection, 14% would favour axillary sampling, 2% would offer sentinel node dissection; 21% would be prepared to offer all the above options and 30% stated they would not consider offering any surgery to the axilla at all. No difference was noticed when the surveyed were distributed according the deprivation ranks. Seventy-five percent stated their surgical management would not differ according to the patients age, while onefourth of the questioned surgeons would provide a different surgical management. The largest number of surgeons (44%) stated they considered age as not relevant in deciding whether to provide breast reconstruction to the elderly breast cancer patient, while the age limit of 65, 70, 75, and 80 years was a relevant cut-off for 19%, 23%, 13%, 1%, respectively. Only six surgeons (4%) consider overall survival as the end-point in monitoring surgical outcomes the elderly patient with breast cancer, 13% would target their treatment on disease free survival, but the majority would privilege the patient’s quality of life (42%) or quality adjusted survival (40%).
3.3. Comprehensive assessment One-third of the surgeons responding to our questionnaire used to co-operate with geriatricians on a regular basis (32%); conversely, 5% never involved the geriatricians, while 21 and 42% rarely or sometimes discuss their elderly patients with geriatricians, respectively. The largest proportion of breast cancer surgeons (82%) claimed the lack of habit to utilise any Geriatric Assessment Instrument before or after the surgical procedure, 16% occasionally did so, and only 2% utilised such an instrument on a routine basis. When questioned which sort of pre-operative assessment they would provide to appraise the operative risk, 57 (38%) stated they do not use any specific instrument, 78 (52%) rely on the American Society of Anesthesiologists (ASA) score [10] as performed by the anaesthesiologists (67 routinely and 11 on an occasional basis), 15 (10%) use physiological and operative severity score for enumeration of mortality and morbidity (POSSUM) [11,12] (four routinely and 11 occasionally), 9 (6%) use Portsmouth POSSUM modification (P POSSUM) [13], and finally 12 breast surgeons utilise either a standardised Geriatric Assessment tool, or their institutional instrument.
4. Discussion Very little is known about breast cancer in the elderly, apart from the dramatic increase in number [2,3]. Breast cancer is undertreated in the older patient [14], and undertreatment strongly decreases prognosis [15]. The operative risk is increased as a consequence of a higher incidence
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of coexisting diseases, and there is a 20-fold higher rate of non-breast-cancer deaths in patients with ≥3 comorbidities [16]. Our lack of knowledge is due to a lack of definitions: who is elderly? While a vivid debate is undergoing amongst the scientific community, everyday clinical practice is centred on older cancer patients. The authors are not aware of any previous survey on this topic, with the exception of an original article on the attitudes of medical oncologists in the management of elderly breast cancer patients [17]. The present survey was facilitated by the Association of Breast Surgery at BASO, representing the largest majority of surgeons in the UK with an interest in breast cancer. The sample is reliable as it encompasses specialists from teaching hospitals, district general hospitals and comprehensive cancer centres. A 43% compliance confers robustness to this survey, and is in keeping with several other surveys [18–20]. It is interesting to notice how the majority of breast surgeons participating to the survey practice in districts ranking within the top third most deprived in the country (48%), while surgeons from the least deprived areas are obviously reluctant to contribute to surveys. The 74% surveyed clinicians are acting as dedicated breast surgeons and 12% surgical oncologists, while 14% are general surgeons with an interest on breast disease. The most part of the surveyed population (78%) has been in place for over 10 years, and more than 90% over 5 years. The majority of the surgeons seem to be aware of the burden of elderly patients developing breast cancer, since 40% claim their clinical practice is mainly dealing with elderly patients, plus 45% stating they are dealing with elderly patients between 20 and 50% of their workload. A clear age cut-off is not conceivable to define the patient as “elderly” on the sole basis of the chronological age for the largest part of surveyed surgeons (44%), while the rest of the sample considers a possible age cut-off at age 70 (12%), 75 (20%) or 80 (23%). Only two surgeons would consider the elderly as 65 years or older. This differs from the BIG survey [12] where 62% medical oncologists agreed on a 70 year cut-off for the purpose of administering adjuvant palliative therapy, and 65 remains as the starting date for Medicare eligibility in the US. Conversely, there is a trend with the surveyed medical oncologists [12] in that no agreement exists on the age cut-off for denying treatment, with 98% surveyed breast specialists not accepting age as a reason for exclusion to surgical management. The unreliability of crude anagraphical data is reinforced by acknowledging that elective breast cancer surgery should not be denied, no matter the patients age (98%); only two surgeons stating they would not favour breast cancer surgery on election above 70, or 80 years, respectively. Most breast surgeons are inclined to base their treatment planning on a complexity of biological, anagraphical, and
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social issues (57%). Further on, 34% of the surveyed claim they would be inclined to prioritise the patient’s biological age however appraised, while only 6% would rely on chronological age as the main cut-off. We are in need of a standardised pre-operative assessment capable of characterising the patient’s “functional age”, in order to optimise treatment planning and stratify outcomes on the basis of factors other than chronological age. To satisfy this need a prospective clinical research project has been designed and started [21]. The issue of how to treat the axilla is a complex one. It is widely agreed that the axillary lymph nodes should be staged to aid in determining prognosis and therapy [22]. The surprised international reader should appreciate the peculiarity of the UK setting where a level 2 or 3 axillary dissection is rarely performed, as most surgeons still favour the sampling technique. Although most authorities agree that an axillary node dissection in the presence of clinically negative nodes is a necessary staging procedure, controversy exists as to the extent of the procedure because of long-term morbidity (arm discomfort and swelling) associated with it [23]. This is particularly relevant to the older breast cancer patient, where quality of life issues are to be prioritised over a debatable advantage in long-term survival. In the lack of major contraindications, one-third or the surveyed would advise in favour of dissection (33%) and another fraction privileges axillary sampling (14%). An impressive 30% is “in principle” against any surgical dissection: this might be an heritage of a few inappropriately designed and relatively small investigations sadly popularised in the early 1980’s, which set a trend toward conservative (under)treatment [24–27]. In an effort to decrease the morbidity of axillary lymphadenectomy while maintaining accurate staging, several investigators have studied lymphatic mapping and sentinel lymph node biopsy (SLNB) in women with invasive breast cancer [28]. Although reports demonstrate a 97.5–100% concordance between SLN biopsy and complete axillary lymph node dissection [29–31], SLNB is presently not feasible in the UK outside the ALMANAC trial. The restricted number of breast specialists providing SLNB, no matter the patient’s age, is consequently explained to the surprised international reader. Indeed three out of four surveyed (75%) would not consider a different approach to the axilla solely on the base of the patient’s age. No substantial geographical variation was detected, and the deprivations ranks do not seem to impact on the management. Recent reports have positively commented on the feasibility and outcomes of breast reconstruction in the elderly [32,33], but no clear guideline is available, especially with respect to this patients’ age groups; again, the most part of the surveyed would not base their decision on age (44%), while others would identify a cut-off point at 65 (19%), 70 (23%), 75 (13%), and 80 years (1%), respectively. The amount of time to survive from cancer treatment is identified as the most adequate end-point by a small minority
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(4%), while surviving without cancer is the target for 13%. Conversely, there is consistent agreement on the quality of life the patient is offered as the main target, with 42% aiming for a better quality of life, and 40% for quality adjusted survival. When these findings are compared to the medical oncologists’ survey, we notice a similarity in prioritising quality adjusted survival and neglecting overall survival (45 and 12% in their survey, respectively). Noticeably, a difference is evident in targeting disease-free survival, which was highly rated among medical oncologists (40%) while only 13% surgeons would take it as the endpoint for treatment. This point deserves further medical, ethical, and economical research, in view of the dramatic expansion of life expectancy of senior patients and healthy individuals: a 65, 75, and 85 healthy subject is expected to live 20, 12, and 6 years, respectively; 9.7, 7.3, and 4.5 years, respectively for a sick person [34]. The role and value of a possible co-operation with geriatricians is obviously highly valued among surgeons: only 5% claims never discussing their oncogeriatric patients; conversely, 21% do interact with the geriatricians although rarely, 42% do so only at times, and 32% on a regular basis. While at least 74% surgical patients are likely to be discussed with the care of the elderly team, only 15% were likely to have such a consultation in Biganzoli’s findings [17]. This sharp difference might be explained with a much wider geographical variability of her sample. Finally, a reliable preoperative risk assessment tool is not available as yet and the majority of the surveyed never utilises a Geriatric Assessment Instrument (82%), compared with 16% who use it occasionally; 2% use it on a regular basis. Similar findings are reported for medical oncologists [17]. A simple and reliable pre-surgical assessment tool is being validated within an international prospective study; preliminary results confirm its practical utility in identifying possible associations between its components and postoperative morbidity [21]. The risk assessment is most probably left in the hands of the anaesthetist since 45% surgeons rely on the ASA classification on a routine basis, plus 7% occasionally. A restricted number of breast surgeons attempts stratifying the operative risk with POSSUM (3% routinely, and 7% sometimes), P POSSUM (2% routinely, and 4% sometimes), or a specific Geriatric Assessment Instrument (1%). Still 38% claims not to be utilising a risk assessment tool. Further research is needed to avoid any under-treatment on the basis of an ageistic approach, while protecting the frail older patients from inappropriate over-treatment [35]. Given the limitations of a postal survey and the relatively small sample size, this survey provides an overview of the present approach at a clinical level. The breast surgical community in the UK is not basing their treatment plan on the basis of anagraphycal age, and is committed to providing the best management in order to achieve global well-being to the older patients with breast cancer.
Reviewers Dr. Georges Vlastos, Hˆopitaux Universitaires de Gen`eve, Gyn´ecologie Oncologie et S´enologie, 30, Boulevard de la Cluse CH-1211 Geneva 14, Switzerland. Dr. Arti Hurria, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, NY 10021-6007, USA. Prof. Chris Robertson, Department of Statistics & Modelling Science, Livingstone Tower, Richmond Street, Glasgow, G1 1XT, Scotland, UK. Roberto Gennari, M.D., Vice-Director, Department of surgery, European Institute of Oncology, Via Ripamonti, 435, I-20141 Milan, Italy.
Acknowledgements The authors wish to thank BASO for providing the mailing list and supporting this survey.
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Biography Riccardo A. Audisio was born and trained in Milan, Italy. He moved to the UK in 1999 as a Consultant Surgical Oncologist and Hon. Senior Lecturer at the University of Liverpool. He has focused his clinical research on Geriatric Oncology, and is presently chair of the surgical task force at SIOG. He is involved with the EORTC Cancer in the Elderly Study Group, and recently chaired an advanced course for ESO on this topic.