Fatigue and menopausal symptoms in women with breast cancer undergoing hormonal cancer treatment

Fatigue and menopausal symptoms in women with breast cancer undergoing hormonal cancer treatment

original article Annals of Oncology 17: 801–806, 2006 doi:10.1093/annonc/mdl030 Published online 28 February 2006 Fatigue and menopausal symptoms in...

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original article

Annals of Oncology 17: 801–806, 2006 doi:10.1093/annonc/mdl030 Published online 28 February 2006

Fatigue and menopausal symptoms in women with breast cancer undergoing hormonal cancer treatment A. Glaus1*, Ch. Boehme2, B. Thu¨rlimann2,3, T. Ruhstaller2,4, S. F. Hsu Schmitz5, R. Morant1, H. J. Senn1 & R. von Moos2 1

Tumorzentrum ZeTuP, Diagnostik, Behandlung und Pra¨vention, St. Gallen; 2Fachbereich, Onkologie, Department Innere Medizin, Kantonsspital St. Gallen; Senologie Zentrum Ostschweiz, Kantonsspital St. Gallen; 4Fachbereich Onkologie, Innere Medizin, Kantonsspital Mu¨nsterlingen; 5Statistics Unit, Swiss Group for Clinical Cancer Research (SAKK), Bern, Switzerland 3

Received 3 January 2006; revised 22 January 2006; accepted 23 January 2006

introduction Women with breast cancer are not only confronted with organ specific, physical, psychological, sexual and cultural-social issues, but also have to deal with a wide range of therapyinduced problems and side effects. As breast cancer often is a hormone-dependent type of cancer, treatment affects fundamental issues of women’s health which interferes with well-being. From this perspective, it seems very appropriate to speak about breast cancer as a life transition from health to illness, affecting women’s functioning and quality of life [1]. Although surviving remains an important goal for most, quality of survival has been increasingly addressed in this patient population. However, as compared to chemotherapy, side effects and consequences of hormonal treatment in women with breast cancer have been less well reported. The distress that these effects may cause is not always recognised by health care professionals [2]. Hot flashes, night sweats and increased

*Correspondence to: Dr A. Glaus (PhD, MSc, RN), Tumorzentrum ZeTuP, Diagnostik, Behandlung und Pra¨vention, Rorschacherstrasse 150, CH-9006 St. Gallen, Switzerland. Tel: 0041 71 243 00 43; Fax: 0041 71 243 0044; E-mail: [email protected]

ª 2006 European Society for Medical Oncology

vaginal discharge are well known side-effects linked to tamoxifen use but opinion suggests that these are well tolerated and do not unduly impair quality of life [3]. Other researchers found that health care professionals overestimated side effects of tamoxifen compared with patients themselves under tamoxifen treatment [4]. These reports indicate the need for a better understanding of symptoms experienced by patients on endocrine therapy. Clinical experience also suggests that menopausal symptoms still represent a social taboo and therefore may be under-reported by patients and under-treated by care givers. Cancer related fatigue (CRF) may be a relevant issue within this context. CRF is described as the most common side effect of cancer treatment and affects 70–100% of patients receiving chemotherapy or radiation therapy [5]. As linguistic differences do exist in naming this concept, in this paper, fatigue and tiredness are used interchangeably, although tiredness is seen as a phenomenon in healthy individuals and fatigue usually is related to cancer or other illness [6]. Studies indicate that the prevalence in patients with breast cancer is high, with as many as 99% experiencing fatigue during the course of treatment [5]. Whilst it has been proposed that hormonal treatment had

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the palliative setting. Therefore, many women are confronted with early menopause and prolonged oestrogen deprivation and consequently with a variety of quality of life issues, such as menopausal symptoms and fatigue. Patients and methods: It was the aim of this study to explore the occurrence and frequency of menopausal symptoms in women with breast cancer, undergoing hormonal cancer treatment and to investigate their relationship with fatigue. A cross-sectional, quantitative approach was used in this multi-centre study. The Checklist for Patients with Endocrine Therapy (C-PET) and the International Breast Cancer Study Group (IBCSG) Linear Analogue Scales for patients with endocrine treatment were used. Descriptive statistics, as well as cluster analyses were performed. Results: Most frequent menopausal symptoms involved hot flashes/sweats, tiredness, weight gain, vaginal dryness and decreased sexual interest. There were significant differences between the fatigued and the non-fatigued population regarding the intensity of menopausal symptoms, emotional irritability and general coping. Cluster analyses supported a menopausal symptom cluster. Conclusions: Fatigue accompanies menopausal symptoms and an association can be expected. Methods for routine screening for menopausal symptoms, including fatigue, are suggested as a relevant research issue in women with breast cancer undergoing hormonal treatment. Key words: breast cancer, fatigue, hormones, menopausal symptoms

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Background: Hormonal treatment for women with breast cancer is frequently proposed in the adjuvant as well as in

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methods A quantitative research strategy and a prospective, cross-sectional approach were used. The multi-institutional investigation involved oncology outpatient departments of four regional teaching hospitals and four private oncology outpatient centres in Eastern Switzerland. Breast cancer patients undergoing hormone therapy were selected consecutively. Patients confirmed participation by written consent and ethical approval for the study was provided by the local ethical committee.

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instruments Clinical Checklist for Patients with Endocrine Therapy (C-PET). This assessment instrument was developed as an interactive tool to measure the occurrence of side effects associated with hormonal treatment of breast cancer more effectively. It is a dichotomous self-assessment tool with 13 items, representing side effects of hormonal treatment. Patients were asked to fill in the questionnaire before consultation and to indicate their wish to speak about it with the doctor. The C-PET has been developed and tested by a European Task Force [15] and is also available in a validated, German version. The item ‘tiredness’ (Mu¨digkeit) is Part of the C-PET tool. IBCSG/Linear Analogue Scales (LASA) addressing side effects of hormonal treatment and coping with disease and treatment. In addition to the dichotomous C-PET Instrument, LASA Scales, covering seven items related to side effects caused by hormonal anticancer treatment, were used. These scales from the International Breast Cancer Study Group (IBCSG), are also available in German and have been tested widely, with their validity and reliability described elsewhere [16]. The item ‘tiredness’ (Mu¨digkeit) is also integrated as a LASA in this IBCSG tool. Furthermore, two items on global adjustment with disease and treatment, from the Perceived Adjustment to Chronic Illness Scale (PACIS), are integrated in this tool [17].

analyses Symptoms collected by the C-PET instrument were presented by frequency table. The intensity of each symptom, collected by the IBCSG/ LASA, was presented by descriptive statistics. To investigate the relationship between results of LASA and C-PET, the intensity of each LASA symptom was stratified by the occurrence of each relevant C-PET symptom and compared between strata using two-sample t-test (for Tables 3, 4 and 5). Cluster analyses [18] were performed to explore symptoms that tend to occur together respectively for the binary C-PET symptoms and the LASA symptoms. The distance measure was 1 minus the Jaccard coefficient for the C-PET symptoms and 1 minus the squared correlation coefficient for the LASA symptoms. Based on average linkage, clusters were grouped using the agglomerative hierarchical method, starting with each symptom (one per cluster), then the two clusters separated by the shortest average distance are joined. The procedure is repeated until a single large cluster, containing all symptoms is formed. Analyses were performed using SAS version 9.1 (SAS Institute Inc. Cary, NC).

results response rate and patient characteristics Four hundred and five patients were approached and 373 agreed to participate in this study. The response rate was 92%. Patient characteristics are presented in Table 1. Table 1. Patient characteristics (n = 373) Age

No. (%)

£50 y 51–65 y ‡65 y Range 28–88 y, mean 61 y Stage of breast cancer Early Advanced Hormone treatment Antioestrogens, mainly Tamoxifen Aromatase Inhibitors Other anti-hormones

74 (20%) 153 (41%) 146 (39%)

301 (81%) 72 (19%) 268 (72%) 43 (11%) 62 (17%)

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minimal effect on fatigue and menopausal symptoms, it is still true that adjuvant chemotherapy leads to severe fatigue and menopausal symptoms during treatment, with worse symptoms from chemotherapy-induced than natural menopause [7]. The interference of fatigue with menopausal symptoms, however, may be difficult to disentangle, especially in young breast cancer patients who face premature and sudden menopause and prolonged oestrogen deprivation. Patterns of fatigue-occurrence may differ by type of treatment [8] and stage of cancer [9]. However, knowledge about the influence of hormone deprivation due to breast cancer treatment on CRF is still scarce. A recent study revealed that low energy, apart from sweats, hot flashes and weight gain, was among the most frequent symptoms in 620 breast cancer patients treated either with Megestrol acetate or Anastrazole. By contrast, low energy levels had a tendency to be less prominent for those patients treated with Tamoxifen [10]. The authors concluded, however, that it was difficult to attribute all symptoms to endocrine treatment and that they may also be related to other variables, such as disease-state and age. New endocrine agents now provide novel treatment options and have unique treatment profiles [11], suggesting a different impact on the development of CRF and related symptoms. A symptom cluster has been defined as three or more symptoms that are related and experienced concurrently [12]. A cluster with sleep quality, fatigue and depressive symptoms was compared between breast cancer survivors and healthy individuals experiencing hot flashes. Global sleep quality was significantly correlated with fatigue, depressive symptoms and findings suggest that sleep disturbance is common in menopausal breast cancer patients and in healthy women [13]. This may suggest that fatigue is a symptom of menopause in healthy individuals as well as in breast cancer patients. Ge´linas [14] showed that persistent fatigue in younger breast cancer patients following completion of therapy was also related to menopausal symptoms. It therefore can be hypothesised that endocrine treatment induced menopausal symptoms in patients with breast cancer may interact with fatigue and form a menopausal symptom cluster. It was the aim of this study to look at subjective symptoms of women with breast cancer treated with endocrine therapy and to explore the role of Cancer-Related Fatigue (CRF) within these symptoms. The research questions address (i) the occurrence and frequency of endocrine treatment side effects, menopausal symptoms respectively, and the occurrence of fatigue, (ii) the relationship of fatigue with menopausal symptoms and (iii) possible formation of symptom clusters specific to breast cancer patients with hormonal cancer treatment.

Annals of Oncology

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Annals of Oncology

occurrence and frequency of menopausal symptoms according to the C-PET instrument Symptoms, identified for women with early and advanced beast cancer, are summarised in Table 2. In women with early disease, hot flashes were most frequently endorsed, followed by weight gain, tiredness, vaginal dryness and decreased sexual interest. For women with advanced disease, hot flashes were less prominent, but still most frequently mentioned, followed by tiredness, vaginal dryness, decreased sexual interest and weight gain. The largest differences between the two groups were for hot flashes and weight gain. Tiredness remained one of the three top priorities for both groups.

occurrence of menopausal symptoms in relation to intensity of tiredness/fatigue Table 4 presents the two groups indicating occurrence of C-PET menopausal symptoms (yes or no) and its relation to IBCSG/ LASA tiredness in mm. LASA tiredness/fatigue intensity was statistically different in women who also suffered from irritability (mood) and fluid retention. Otherwise, LASA Table 2. Frequency of symptoms identified by C-PET (yes/no answers) C-PET Symptoms (yes/no)

Early disease Advanced disease All patients (n = 301) (n = 72) (n = 373) Percentage Percentage Percentage

Hot flashes/sweats Weight gain Low energy/tiredness Vaginal dryness Decreased sexual interest Fluid retention Irritability Short of breath Vaginal discharge Skin rash Nausea Vaginal bleeding

73 49 45 35 29 20 18 16 14 11 9 2

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57 28 50 28 28 16 18 19 5 4 10 2

70 45 46 34 29 19 18 17 12 10 10 2

menopausal symptom clusters Using 0.8 as cut-off point for average distance for the C-PET results (Figure 1), the symptoms hot flashes, weight gain, tiredness, decreased sexual interest and vaginal dryness form a cluster. All remaining symptoms did not form obvious clusters.

discussion It has been reported that side effects of hormonal cancer treatment or hormone deprivation may unduly impair quality of life [2–4]. Taking a cut-off point of 15% prevalence, our study shows that menopausal symptoms, such as hot flashes, weight gain, tiredness/fatigue, vaginal dryness, decreased sexual interest, fluid retention and irritability of mood (Table 2), represent a major health issue to women even with early disease of breast cancer and also after the age of 50 years.

occurrence and frequency of menopausal symptoms and fatigue Results show that in patients with early disease, hot flashes are more frequent (73%) than in patients with advanced disease (57%). As the size of the two groups is unbalanced, this has to be interpreted with caution. Eighty-one percent of all patients had early disease and in addition 80% of all patients were older than 50 years, which suggests that the difference between the two groups can only partially be explained by age. It rather may suggest that menopausal symptoms remain are experienced by many women throughout several years after hormone deprivation, due to either the natural course of life or earlier chemotherapy. Weight gain is also distinctly less frequent in this group with advanced disease (28% versus 49%) and this may be explained by the fact that progressing disease is usually accompanied by loss rather than gain of weight. Occurrence of tiredness/fatigue is the third most frequent symptom in patients with early breast disease and the second most frequent symptom in patients with advanced breast disease in this study. These findings support existing evidence that fatigue is a major distressing symptom in patients with cancer [5], although occurrence rates for fatigue generally are expected to be higher in other cancer populations than in breast cancer patients [6], which may be different in breast cancer patients under adjuvant chemotherapy [7]. The frequent endorsement of tiredness in the group with early disease as well as the one with advanced disease (50% vs 45%) support the generally accepted hypothesis that causes of fatigue are of multiple origins in this population. Cancer Related Fatigue (CRF) has been associated with different cytokines, defending tumour growth, impaired energy transformation processes and many other cancer related

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intensity of LASA menopausal symptoms and distress in relation to occurrence of C-PET tiredness/low energy In Table 3, intensity of menopausal symptoms, measured by IBCSG LASA, were presented separately for women who indicated suffering from tiredness in the C-PET instrument and those who indicated not suffering from tiredness. Patients suffering from C-PET tiredness, were significantly more distressed by LASA menopausal symptoms such as hot flashes, tiredness, impaired mood, decreased sexual interest, vaginal dryness and general physical well-being than those who did not indicate C-PET tiredness. For the item tiredness itself, LASA results were congruent with the binary C-PET item tiredness, which supports reliability and validity of the two assessment methods. Table 3 also shows that patients with C-PET tiredness/ fatigue dealt with significantly more coping difficulties with the disease as well as with general treatment distress than those patients who did not suffer from C-PET tiredness/fatigue.

tiredness/fatigue intensity consistently remained about the same problem size within the context of C-PET menopausal symptoms, apart from those where group sizes were small. Again, the item tiredness/low energy from the C-PET instrument was congruent with results from the IBCSG LASA tiredness, showing significant differences between mean tiredness above 50 mm for patients with menopausal symptoms and below 20 mm for patients without menopausal symptom.

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Annals of Oncology

Table 3. Intensity of menopausal symptoms as measured by IBCSG/LASA (mean mm). Stratified by occurrence of tiredness according to C-PET (yes/no) LASA Side effects, symptoms

C-PET Tiredness Yes (n)

LASA Symptoms Mean mm

SD

C-PET Tiredness No (n)

LASA Symptoms Mean mm

SD

P

Hot flashes Weight gain Tiredness, low energy Impaired mood Decreased sex drive Vaginal dryness Reduced physical well-being Coping distress disease General distress from treatment

163 162 160 164 142 151 165 163 163

52.0 28.8 56.9 30.6 40.9 41.8 27.4 33.0 28.7

34.3 28.6 23.7 23.0 32.7 35.6 24.3 25.6 26.8

189 189 188 190 171 181 193 190 184

41.2 35.0 18.9 18.7 30.5 29.5 13.3 22.0 16.6

34.8 33.0 22.3 21.4 30.6 30.7 19.0 22.9 19.2

0.0036 0.0608 <0.0001 <0.0001 0.0041 0.0008 <0.0001 <0.0001 <0.0001

C-PET Menopausal symptoms

C-PET Yes (n)

LASA Tiredness Mean mm

SD

C-PET No (n)

LASA Tiredness Mean mm

SD

P

Hot flashes/sweats Weight gain Tiredness, low energy Irritability (mood) Decreased sex drive Vaginal dryness Fluid retention Skin rash Breathlessness Nausea

247 163 160 65 107 120 69 35 58 35

37.9 37.8 56.9 55.4 38.6 37.4 42.7 55.0 50.3 59.2

29.4 29.1 23.7 28.6 28.6 27.8 27.8 28.5 26.4 28.6

101 185 188 283 241 228 279 313 290 313

32.6 35.1 18.9 32.0 35.4 35.8 34.9 34.3 33.6 33.8

30.3 30.3 22.3 28.3 30.2 30.8 30.1 29.2 29.6 28.8

0.1312 0.3856 <0.0001 <0.0001 0.3474 0.6450 0.0494 <0.0001 <0.0001 <0.0001

Figure 1. Menopausal symptom-cluster.

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Table 4. Intensity of tiredness as measured by IBCSG/LASA (mean mm), stratified by occurrence of menopausal symptoms as measured by C-PET (yes/no)

Annals of Oncology

relationship between menopausal symptoms and fatigue When measuring not only occurrence but also intensity of menopausal symptoms and fatigue, using the IBCSG Linear Analog Scales (Table 3), slightly different priorities can be observed. Looking at the 45% of study-participants who indicated tiredness as being a distressing symptom as measured by the C-PET instrument, LASA measurement indicates that mean tiredness is very high with 56.9 mm and ranks first of all symptoms, closely followed by hot flashes, vaginal dryness, decreased sexual interest, impaired mood and reduction of physical well-being. Study participants without indication of tiredness in the C-PET instrument, ranked hot flashes highest, followed by weight gain, decreased sexual interest, vaginal dryness and others. Taking a significance level of 0.05, all C-PET symptoms but weight-gain reached statistical significance between the two groups (Table 3). It can be interpreted that tiredness/fatigue influences the experience of menopausal symptoms. This is supported by the fact that patients suffering from fatigue have indicated significantly more distress related to coping with the disease and the treatment (Table 3). This interpretation finds support in earlier literature, where fatigue has been identified as a global indicator of quality of life—a non-specific symptom in nature but acting at physical, psychological, social levels and other levels [17]. In this context, it needs to be mentioned, that fatigue is also a major symptom of depression and therefore delineation between fatigue and depression in women with menopausal symptoms represents a diagnostic challenge with relevant, therapeutic consequences. When dividing the study participants into one group with and another group without C-PET menopausal symptoms, intensity of tiredness, as measured by IBCSG/LASA, reached statistical significance for tiredness itself and for irritability of mood (Table 4). Patients indicating irritability also showed the highest levels of tiredness and a relationship can be expected with the affective dimension of fatigue [9]. It cannot be answered yet whether fatigue causes more menopausal

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symptom distress or whether menopausal distress causes more fatigue. However, as sleep disturbances are commonly accepted as a menopausal symptom and may be associated with hot flashes and night sweats, the interrelationship of menopausal symptoms with fatigue also can be expected. Carpenter [13] observed, that 73% of breast cancer survivors and 67% of healthy controls indicated severe sleep disturbance. Unfortunately, neither the C-PET instrument nor the IBCSG LASA scales have sleep disturbance integrated as a measurement item and therefore this aspect remains unanswered in this study.

symptom clusters One of the research questions was whether a typical pattern of symptom complex can be observed in women with menopausal symptoms. Analyses of data provided by the dichotomous CPET instrument showed a cluster with hot flashes, weight-gain, tiredness, reduced sexual interest and vaginal dryness (Figure 1). Bender et al. [18] also found a cluster with fatigue, perceived cognitive impairment and mood problems in patients with breast cancer. Supported by clinical experience, the one cluster model with five symptoms is proposed (Figure 1) although a further three cluster model was produced when testing results collected with the LASA instruments. Cluster analyses are exploratory and therefore it is difficult to prove reliability. Relevance of such clusters needs to be further substantiated. Still, the five-symptom cluster could serve as a guide for the development of simple, targeted screening in routine practice and easy identification of specific needs of breast cancer patients in the clinical setting. symptom screening in routine practice and cut-off points for significant fatigue This study revealed an interesting methodological aspect of fatigue measurement in relation to cut-off points. Patients indicating suffering from tiredness in the dichotomous C-PET instrument, showed a mean tiredness of 56.9 mm (as measured with LASA) (Table 3). A cut-off point of 50 mm has been identified as significant in symptom measurement (Holmes 1991). Those patients who did not indicate tiredness in the dichotomous C-PET, showed mean tiredness of 18.9 mm only, which may be similar in a healthy population [21]. This supports the use of simple yes/no questions for screening purposes in a busy clinical setting. However, when it comes to the question of significance or relevance of a symptom to identify interventional needs, a more detailed LASA method seems appropriate. Results from this study propose that levels of fatigue up to 20 mm may be considered as normal and levels above 50 mm as significant fatigue. Screening for symptoms can help identifying neglected issues or taboos. Only few patients indicated that they wanted to speak about menopausal symptoms with their physician. They may feel ashamed, especially in the light of life-threatening cancer, and may feel that it is of little or no interest to physicians and nurses. Patients may also feel that busy physicians are not the right persons to talk about sexual issues and that mentioning such symptoms could lead the physician to induce changes of treatment. These interpretations are supported by

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pathologies [5, 6], rather than by hormonal cancer treatment or hormone deprivation alone. Tannok observed fatigue, menopausal symptoms and cognitive functions in women with breast cancer under adjuvant chemotherapy and compared these aspects in controls with natural menopause [7]. He concluded that patients had worse symptoms from chemotherapy-induced menopause than from natural menopause and that hormonal treatment had minimal effect on fatigue and menopausal symptoms. This may suggest that fatigue is less associated with hormonal treatment of breast cancer than with chemotherapy or the disease itself. In this study, 72% of patients were treated with antioestrogens, mainly Tamoxifen. Malinovsky et al. [10] suggested different levels of fatigue associated with different groups of anti-hormones and concluded in their study that Tamoxifen was less associated with low levels of of energy than other anti-hormones. In our study, 72% of patients were treated with anti-oestrogens, mainly with tamoxifen and therefore comparison between the groups is not possible.

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original article other research, where patients kept fatigue unmentioned because they felt that physicians and nurses had no interest in their fatigue [22].

limitations The consecutive selection of patients led to uneven distributions of disease status, with 81% of patients having early disease. Hormonal treatment mainly included Tamoxifen. Only 20% of patients were under the age of 50 years. Results of this study reflect a majority of women being peri- and post-menopausal. However, this limitation also provides interesting information, showing that hot flashes remain a severe problem for patients with hormonal cancer treatment, even long after menopause. As the study did not include a control group, differences with other populations are to be established.

The relevance of menopausal symptoms and fatigue in patients with breast cancer requires specific routine assessment and support. In order to bridge communication gaps, a screening approach for menopausal symptoms and fatigue is proposed, probably outside of the regular, busy physician consultation. Results may be used for further research in the field of routine screening for specific symptoms in women with breast cancer and anti-hormonal treatment. This appears especially relevant in the light of therapeutic advances, as practical guidelines to the evidence based management of menopausal symptoms in breast cancer patients have recently been published [23] and awareness and easy symptom measurement are prerequisites for successful treatment.

acknowledgements We thank Dr Pierluigi Ballabeni and Dr Kaspar Rufibach at the Statistics Unit of the Swiss Group for Clinical Cancer Research (SAKK), Bern, for their statistical support. We also thankfully acknowledge Dr B. Spa¨ti, St. Gallen, Dr U. Mu¨ller, Sargans and Dr M. Ho¨fliger, Alsta¨tten, all oncologists in private practice, for their contribution in recruiting patients for the study.

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conclusions

Annals of Oncology